218. Gorman, KB; Ruck, KE; Williams, TD; Fraser, WR. (2021) Advancing the Sea Ice Hypothesis: Trophic Interactions Among Breeding Pygoscelis Penguins With Divergent Population Trends Throughout the Western Antarctic Peninsula.Front. Mar. Sci. 8 Advancing the Sea Ice Hypothesis: Trophic Interactions Among Breeding Pygoscelis Penguins With Divergent Population Trends Throughout the Western Antarctic Peninsula
delta C-13 and delta N-15 stable isotopes; food web; Pygoscelis penguin; reproduction; sea ice; western Antarctic Peninsula
We evaluated annual and regional variation in the dietary niche of Pygoscelis penguins including the sea ice-obligate Adelie penguin (Pygoscelis adeliae), and sea ice-intolerant chinstrap (Pygoscelis antarcticus) and gentoo (Pygoscelis papua) penguins, three species that nest throughout the western Antarctic Peninsula (AP) to test the sea ice trophic interaction hypothesis, which posits that penguin breeding populations with divergent trends, i.e., declining or increasing, are reliant on differing food webs. Our study relies on values of naturally occurring carbon (C-13/C-12, delta C-13) and nitrogen (N-15/N-14, delta N-15) stable isotopes as integrated proxies of penguin food webs measured over three years at three different breeding colonies. At Anvers Island in the north, where reductions in sea ice and changes in breeding population trends among sympatric sea ice-obligate (Adelie) and sea ice-intolerant (chinstrap and gentoo) penguins have been most notable, our analyses show that all three species of Pygoscelis penguins became more similar isotopically over the reproductive period. By late chick-rearing at Anvers Island, creched chicks at 5-weeks-old for all species occupied similar trophic positions. Isotopic mixing models indicated that the proportions of prey provisioned by adult penguins to 5-week-old chicks at Anvers Island were generally similar across species within years, consisting primarily of Antarctic krill (Euphausia superba). Creched Adelie chicks had higher delta C-13 and delta N-15 values at Avian and Charcot Islands, southern breeding colonies where sea ice is more prominent and populations of Adelie penguins have increased or remain stable. Trophic position increased with latitude, while the proportions of prey provisioned by Adelie penguin adults to chicks at southern breeding colonies included species typical of high Antarctic marine food webs, especially crystal krill (Euphausia crystallorophias). A Bayesian metric for dietary niche width, standard ellipse area (SEA-B), indicated that Pygoscelis penguins with greater population changes in the north had more variability in dietary niche width than stable populations further south. Our results lend insight on marine food web drivers of Pygoscelis penguin reproduction at the regional scale and question the long-standing paradigm that Antarctic krill are the only food web component critical to penguin reproductive survival in this region of the Southern Ocean. DOI
217. Husak, JF; Fuxjager, MJ; Johnson, MA; Vitousek, MN; Donald, JW; Francis, CD; Goymann, W; Hau, M; Kircher, BK; Knapp, R; Martin, LB; Miller, ET; Schoenle, LA; Williams, TD. (2021) Life history and environment predict variation in testosterone across vertebrates.Evolution 75: 1003-1010 Life history and environment predict variation in testosterone across vertebrates
Endocrine systems act as key intermediaries between organisms and their environments. This interaction leads to high variability in hormone levels, but we know little about the ecological factors that influence this variation within and across major vertebrate groups. We study this topic by assessing how various social and environmental dynamics influence testosterone levels across the entire vertebrate tree of life. Our analyses show that breeding season length and mating system are the strongest predictors of average testosterone concentrations, whereas breeding season length, environmental temperature, and variability in precipitation are the strongest predictors of within-population variation in testosterone. Principles from small-scale comparative studies that stress the importance of mating opportunity and competition on the evolution of species differences in testosterone levels, therefore, likely apply to the entire vertebrate lineage. Meanwhile, climatic factors associated with rainfall and ambient temperature appear to influence variability in plasma testosterone, within a given species. These results, therefore, reveal how unique suites of ecological factors differentially explain scales of variation in circulating testosterone across mammals, birds, reptiles, amphibians, and fishes. DOI PubMed
216. King, MD; Elliott, JE; Williams, TD. (2021) Effects of petroleum exposure on birds: A review.Sci. Total Environ. 755 Effects of petroleum exposure on birds: A review
Oil; Spill; Feathers; Toxicity; Avian; Unconventional oil
Birds are vulnerable to petroleum pollution, and exposure has a range of negative effects resulting from plumage fouling, systemic toxicity, and embryotoxicity. Recent research has not been synthesized since Leighton's 1993 review despite the continued discharge of conventional petroleum, including high-volume oil spills and chronic oil pollution, as well as the emergence of understudied unconventional crude oil types. To address this, we reviewed the individual-level effects of crude oil and refined fuel exposure in avifauna with peer-reviewed articles published 1993-2020 to provide a critical synthesis of the state of the science. We also sought to answer how unconventional crude petroleum effects compare with conventional crude oil. Relevant knowledge gaps and research challenges were identified. The resulting review examines avian exposure to petroleum and synthesizes advances regarding the physical effects of oil hydrocarbons on feather structure and function, as well the toxic effects of inhaled or ingested oil, embryotoxicity, and how exposure affects broader scale endpoints related to behavior, reproduction, and survival. Another outcome of the review was the knowledge gaps and challenges identified. The first finding was a paucity of oil ingestion rate estimates in birds. Characterizing environmentally realistic exposure and ingestion rates is a higher research priority than additional conventional oral dosing experiments. Second, there is an absence of toxicity data for unconventional crude petroleum. Although the effects of air and water contamination in the Canadian oil sands region have received attention, toxicity data for direct exposure to unrefined bitumen produced there in high volumes and other such unconventional oil types are needed. Third, we encountered barriers to the interpretation, replication, broad relevance, and comparability of studies. We therefore propose best practices and promising technological advancements for researchers. This review consolidates our understanding of petroleum's effects on birds and points a way forward for researchers and resource managers. Crown Copyright (C) 2020 Published by Elsevier B.V. DOI PubMed
215. Pavlik, M; Williams, TD; Green, DJ. (2021) Female Songbirds Can Initiate the Transition from a Migratory to a Reproductive Physiology during Spring Migration.Physiol. Biochem. Zool. 94: 188-198 Female Songbirds Can Initiate the Transition from a Migratory to a Reproductive Physiology during Spring Migration
breeding phenology; carryover effects; Neotropical migrant; plasma triglyceride; very low-density lipoprotein (VLDL)
The high energetic costs of both migration and reproduction and the physiological changes to support these costs suggest that these life-history stages should be compartmentalized with little overlap between stages. In contrast, previous studies have shown that male birds can initiate reproductive development during migration before arrival on the breeding grounds with increases in plasma testosterone levels and testis size. However, sex differences in seasonal gonadal function are now recognized as profound, and few studies to date have shown that females can initiate the costly, but critical, estrogen-dependent final stages of gonadal maturation and changes in liver function (yolk precursor synthesis, vitellogenesis) while on migration. Here, we show that female yellow warblers (Setophaga petechia) arrive on the breeding grounds with elevated plasma triglyceride levels compared with males. Some females had plasma triglyceride levels of 5-7 mmol L-1, suggesting that they arrived in a relatively advanced stage of yolk precursor production. Furthermore, we show that females that arrived with higher plasma triglyceride levels took less time to initiate their first clutch. Adaptive plasticity in the timing of the transition from a migratory to a reproductive physiology might help migrant birds buffer against a mismatch between timing of arrival and conditions on the breeding grounds and allow them to advance timing of breeding to maximize breeding productivity. DOI PubMed
214. Ruberg, EJ; Elliott, JE; Williams, TD. (2021) Review of petroleum toxicity and identifying common endpoints for future research on diluted bitumen toxicity in marine mammals.Ecotoxicology 30: 537-551 Review of petroleum toxicity and identifying common endpoints for future research on diluted bitumen toxicity in marine mammals
Petroleum toxicity; Marine mammals; Mini-review; Polycyclic aromatic hydrocarbons; Diluted bitumen; Oil spill
Large volumes of conventional crude oil continue to be shipped by sea from production to consumption areas across the globe. In addition, unconventional petroleum products also transverse pelagic habitats; for example, diluted bitumen from Canada's oils ands which is shipped along the Pacific coast to the United States and Asia. Therefore, there is a continuing need to assess the toxicological consequences of chronic and catastrophic petroleum spillage on marine wildlife. Peer-reviewed literature on the toxicity of unconventional petroleum such as diluted bitumen exists for teleost fish, but not for fauna such as marine mammals In order to inform research needs for unconventional petroleum toxicity we conducted a comprehensive literature review of conventional petroleum toxicity on marine mammals The common endpoints observed in conventional crude oil exposures and oil spills include hematological injury, modulation of immune function and organ weight, genotoxicity, eye irritation, neurotoxicity, lung disease, adrenal dysfunction, metabolic and clinical abnormalities related to oiling of the pelage, behavioural impacts, decreased reproductive success, mortality, and population-level declines. Based on our findings and the body of literature we accessed, our recommendations for future research include: 1) improved baseline data on PAH and metals exposure in marine mammals, 2) improved pre- and post-spill data on marine mammal populations, 3) the use of surrogate mammalian models for petroleum toxicity testing, and 4) the need for empirical data on the toxicity of unconventional petroleum to marine mammals. [GRAPHICS] . DOI PubMed
213. Ruberg, EJ; Williams, TD; Elliott, JE. (2021) Review of petroleum toxicity in marine reptiles.Ecotoxicology 30: 525-536 Review of petroleum toxicity in marine reptiles
Petroleum toxicity; Marine reptiles; Physiology; Fitness; Mini-review; Sea turtles
Worldwide petroleum exploration and transportation continue to impact the health of the marine environment through both catastrophic and chronic spillage. Of the impacted fauna, marine reptiles are often overlooked. While marine reptiles are sensitive to xenobiotics, there is a paucity of petroleum toxicity data for these specialized fauna in peer reviewed literature. Here we review the known impacts of petroleum spillage to marine reptiles, specifically to marine turtles and iguanas with an emphasis on physiology and fitness related toxicological effects. Secondly, we recommend standardized toxicity testing on surrogate species to elucidate the mechanisms by which petroleum related mortalities occur in the field following catastrophic spillage and to better link physiological and fitness related endpoints. Finally, we propose that marine reptiles could serve as sentinel species for marine ecosystem monitoring in the case of petroleum spillage. Comprehensive petroleum toxicity data on marine reptiles is needed in order to serve as a foundation for future research with newer, unconventional crude oils of unknown toxicity such as diluted bitumen. [GRAPHICS] . DOI PubMed
212. Yap, KN; Powers, DR; Vermette, ML; Tsai, OHI; Williams, TD. (2021) Physiological adjustments to high foraging effort negatively affect fecundity but not final reproductive output in captive zebra finches.J. Exp. Biol. 224 Physiological adjustments to high foraging effort negatively affect fecundity but not final reproductive output in captive zebra finches
Exercise physiology; Workload; Oxidative stress; Reproduction; Taeniopygia guttata
Foraging at elevated rates to provision offspring is thought to be an energetically costly activity and it has been suggested that there are physiological costs associated with the high workload involved. However, for the most part, evidence for costs of increased foraging and/or reproductive effort is weak. Furthermore, despite some experimental evidence demonstrating negative effects of increased foraging and parental effort, the physiological mechanisms underlying costs associated with high workload remain poorly understood. To examine how high workload affects haematology, oxidative stress and reproductive output, we experimentally manipulated foraging effort in captive zebra finches, Taeniopygia guttata, using a previously described technique, and allowed individuals to breed first in low foraging effort conditions and then in high foraging effort conditions. We found that birds upregulated haematocrit and haemoglobin concentration in response to training. Birds subjected to increased workload during reproduction had lower fecundity, although final reproductive output was not significantly different than that of controls. Offspring of parents subjected to high workload during reproduction also had higher oxidative stress when they were 90 days of age. Total antioxidant capacity and reactive oxygen metabolites of birds responded differently in the two breeding attempts, but we did detect an overall increase in oxidative stress in response to training in either attempt, which could explain the lower fecundity observed in birds subjected to increased workload during reproduction. DOI
211. Yap, KN; Powers, DR; Vermette, ML; Tsai, OHI; Williams, TD. (2021) Sex-specific energy management strategies in response to training for increased foraging effort prior to reproduction in captive zebra finches.J. Exp. Biol. 224 Sex-specific energy management strategies in response to training for increased foraging effort prior to reproduction in captive zebra finches
Exercise; Workload; Parental care; Energetics; Reproduction; Taeniopygia guttata
Free-living animals often engage in behaviour that involves high rates of workload and results in high daily energy expenditure (DEE), such as reproduction. However, the evidence for elevated DEE accompanying reproduction remains equivocal. In fact, many studies have found no difference in DEE between reproducing and non-reproducing females. One of the hypotheses explaining the lack of difference is the concept of an 'energetic ceiling'. However, it is unclear whether the lack of increase in energy expenditure is due to the existence of an energetic ceiling and/or compensation by males during parental care. To investigate whether an energetic ceiling exists, we experimentally manipulated foraging effort in captive zebra finches, Taeniopygia guttata, creating two groups with high and low foraging efforts followed by both groups breeding in the low foraging effort common garden condition. DEE was measured in both sexes throughout the experiment. We show sex-specific energy management strategies in response to training for increased foraging effort prior to reproduction. Specifically, males and females responded differently to the high foraging effort treatment and subsequently to chick rearing in terms of energy expenditure. Our results also suggest that there is an energetic ceiling in females and that energetic costs incurred prior to reproduction can be carried over into subsequent stages of reproduction in a sex-specific manner. DOI PubMed
210. Boynton, CK; Mahony, NA; Williams, TD. (2020) Barn Swallow (Hirundo rustica) fledglings use crop habitat more frequently in relation to its availability than pasture and other habitat types.Condor 122 Barn Swallow (Hirundo rustica) fledglings use crop habitat more frequently in relation to its availability than pasture and other habitat types
Barn Swallow; habitat use; Hirundo rustica; post-fledging; radio-telemetry; survival
Populations of birds that forage on aerial insects have been declining across North America for several decades, but the main causes of and reasons for geographical variation in these declines remains unclear. We examined the habitat use and survival of post-fledging Barn Swallows (Hirundo rustled) near Vancouver, British Columbia, Canada, using VHF radio telemetry. We predicted that fledgling Barn Swallows hatched in higher-quality natal habitat (pasture) would fledge at higher quality, stay closest to the nest, disproportionately use higher-quality habitat during the post-fledge stage, and have higher survival rates in the region. Contrary to our predictions, we found that natal habitat (crop, pasture, or non-agriculture) had no effect on fledgling quality or movement distance. Barn Swallow fledglings used crop habitat more frequently in relation to its availability than other habitat types, including pasture. Barn Swallows had low post-fledging survival rates (0.44; 95% CI: 0.35-0.57), which could negatively influence the population trend of the species in this region. While natal habitat had only minor effects, crop habitat appears to be important for fledgling Barn Swallows and, therefore, a decline in this habitat type could have further negative implications for an already declining species. DOI
209. Criscuolo, F; Torres, R; Zahn, S; Williams, TD. (2020) Telomere dynamics from hatching to sexual maturity and maternal effects in the 'multivariate egg'.J. Exp. Biol. 223 Telomere dynamics from hatching to sexual maturity and maternal effects in the 'multivariate egg'
Maternal effects; Egg; Growth; Maternal antibodies; Testosterone; Telomere; Bird
Avian eggs contain a large number of molecules deposited by the mother that provide the embryo with energy but also potentially influence its development via the effects of maternally derived hormones and antibodies: the avian egg is thus 'multivariate'. Multivariate effects on offspring phenotype were evaluated in a study on captive zebra finches, by simultaneously manipulating maternally derived antibodies (MAb) by lipopolysaccharide (LPS) treatment of mothers and injection of testosterone into the egg yolk. LPS treatment had a positive effect on body mass growth at 30 days after hatching and immune response at sexual maturity, while egg testosterone treatment positively influenced immune response at fledging and courtship behaviour in sexually mature male offspring. Maternal effects are known to modulate offspring telomere length (TL). However, the multivariate effects of egg-derived maternal components on offspring telomere dynamics from hatching to sexual maturity are undefined. Here, we tested: (1) the effects of LPS and testosterone treatments on TL from hatching to sexual maturity (day 82); (2) how LPS treatment modulated TL over reproduction in adult females; and (3) the relationship between maternal and offspring TL. We predicted that TL would be shorter in LPS fledglings (as a cost of faster growth) and that TL would be longer in sexually mature adults after yolk testosterone treatment (as a proxy of individual quality). In adult females, there was an overall negative relationship between laying and rearing investments and TL, this relationship was weaker in LPS-treated females. In chicks, there was an overall negative effect of LPS treatment on TL measured at fledging and sexual maturity (day 25-82). In addition, at fledging, there was a SexxLPSxTestosterone interaction, suggesting the existence of antagonistic effects of our treatments. Our data partially support the hypothesis that telomeres are proxies of individual quality and that individual differences in TL are established very early in life. DOI
208. Currier, HA; Fremlin, KM; Elliott, JE; Drouillard, KG; Williams, TD. (2020) Bioaccumulation and biomagnification of PBDEs in a terrestrial food chain at an urban landfill.Chemosphere 238 Bioaccumulation and biomagnification of PBDEs in a terrestrial food chain at an urban landfill
PBDEs; Terrestrial food-chain; Bioaccumulation; Biomagnification; Stable isotopes; European starling
Biota samples from the Vancouver municipal landfill located in Delta, BC, Canada, have some of the highest polybrominated diphenyl ether (PBDE) levels reported from North America. We followed a population of European starlings (Sturnus vulgaris) breeding in a remediated area in the landfill to identify exposure routes and bioaccumulation of PBDE5 in a simple terrestrial food chain. This population was compared to a reference farm site located 40 km east in Glen Valley. We analyzed samples of European starling eggs and nestling livers as well as invertebrate prey species consumed by starlings for PBDE concentrations. We also collected soil samples from starling foraging areas. All samples from the Delta landfill had higher PBDE congener concentrations compared to the Glen Valley reference site and were dominated by BDE-99 and BDE-47. Stable nitrogen (delta N-15 ) and carbon (delta C-13) isotope analysis of starling blood samples and provisioned invertebrates revealed that stable delta(13)(C) signatures differed between the sites indicating that the diet of starlings in the Delta landfill included a component of human refuse. Biota-soil accumulation factors (BSAFs) > 1 demonstrated that PBDEs were bioaccumulating in soil invertebrates, particularly earthworms, which were readily accessible to foraging starlings in the landfill. Biomagnification factors (BMFs) calculated from foraged food items and starling egg and liver samples were >1, indicating that a diet of soil invertebrates and refuse contributed substantially to the PBDE exposure of local starlings. Crown Copyright (C) 2019 Published by Elsevier Ltd. All rights reserved. DOI PubMed
207. Heddle, C; Elliott, JE; Brown, TM; Eng, ML; Perkins, M; Basu, N; Williams, TD. (2020) Continuous exposure to mercury during embryogenesis and chick development affects later survival and reproduction of zebra finch (Taeniopygia guttata).Ecotoxicology 29: 1117-1127 Continuous exposure to mercury during embryogenesis and chick development affects later survival and reproduction of zebra finch (Taeniopygia guttata)
Methylmercury; Passerine; Hatching success; Survival; Reproduction; Courtship behaviour
Methylmercury (MeHg) is a global environmental contaminant that bioaccumulates and has multiple toxic modes of action. Aquatic species have traditionally been the focus of wildlife toxicological research on mercury, but terrestrial organisms, including passerine birds, can be exposed to similarly elevated levels of MeHg. In this study we exposed a model passerine, the zebra finch (Taeniopygia guttata), to MeHg in ovo, as chicks only, or with a combined 'in ovo + chick' treatment. We isolated exposure to specific developmental stages through the use of egg injections (3.2 mu g Hg/g egg) and controlled oral dosing of chicks (0.24 mu g Hg/g bw/day from day 1 to day 30). In ovo exposure to MeHg reduced hatching success, but there was no effect of MeHg on chick growth. We found that in ovo only or chick only exposure did not have long-term effects, but there was some evidence for longer-term effects of combined 'in ovo + chick' exposure on post-fledging survival and potentially sex-biased survival which resulted in very few 'in ovo + chick' exposed females surviving to breed. These females also had lower overall breeding productivity that was mainly due to lower hatching success of their offspring, not lower chick-rearing success. We found no effect of treatment on clutch size or latency to laying among females that did lay eggs. Our study suggests that combined embryonic and nestling MeHg exposure has compounding latent effects on productivity, likely through a mechanism that influences the ability of females to lay fertile eggs that hatch. DOI PubMed
206. Injaian, AS; Francis, CD; Ouyang, JQ; Dominoni, DM; Donald, JW; Fuxjager, MJ; Goymann, W; Hau, M; Husak, JF; Johnson, MA; Kircher, BK; Knapp, R; Martin, LB; Miller, ET; Schoenle, L; Williams, T; Vitousek, AN. (2020) Baseline and stress-induced corticosterone levels across birds and reptiles do not reflect urbanization levels.Conserv. Physiol. 8 Baseline and stress-induced corticosterone levels across birds and reptiles do not reflect urbanization levels
anthropogenic noise; artificial light at night; glucocorticoid; human footprint; population density; stress
Rates of human-induced environmental change continue increasing with human population size, potentially altering animal physiology and negatively affecting wildlife. Researchers often use glucocorticoid concentrations (hormones that can be associated with stressors) to gauge the impact of anthropogenic factors (e.g. urbanization, noise and light pollution). Yet, no general relationships between human-induced environmental change and glucocorticoids have emerged. Given the number of recent studies reporting baseline and stress-induced corticosterone (the primary glucocorticoid in birds and reptiles) concentrations worldwide, it is now possible to conduct large-scale comparative analyses to test for general associations between disturbance and baseline and stress-induced corticosterone across species. Additionally, we can control for factors that may influence context, such as life history stage, environmental conditions and urban adaptability of a species. Here, we take a phylogenetically informed approach and use data from HormoneBase to test if baseline and stress-induced corticosterone are valid indicators of exposure to human footprint index, human population density, anthropogenic noise and artificial light at night in birds and reptiles. Our results showa negative relationship between anthropogenic noise and baseline corticosterone for birds characterized as urban avoiders. While our results potentially indicate that urban avoiders are more sensitive to noise than other species, overall our study suggests that the relationship between human-induced environmental change and corticosterone varies across species and contexts; we found no general relationship between human impacts and baseline and stress-induced corticosterone in birds, nor baseline corticosterone in reptiles. Therefore, it should not be assumed that high or low levels of exposure to human-induced environmental change are associated with high or low corticosterone levels, respectively, or that closely related species, or even individuals, will respond similarly. Moving forward, measuring alternative physiological traits alongside reproductive success, health and survival may provide context to better understand the potential negative effects of human-induced environmental change. DOI PubMed
205. Jubinville, I; Williams, TD; Trathan, PN; Crossin, GT. (2020) Trade-off between aerobic performance and egg production in migratory macaroni penguins.Comp. Biochem. Physiol. A-Mol. Integr. Physiol. 247 Trade-off between aerobic performance and egg production in migratory macaroni penguins
Migration; Hematocrit; Reticulocyte index; Vitellogenesis
When successive stages of an organism's life-history overlap, conflicts and trade-offs can emerge due to competition among physiological pathways. For example, long periods of sustained locomotion in migrating birds are supported by the androgenic up-regulation of aerobic factors, such as new red blood cell production and hematocrit. However, towards the end of migration, many female birds begin up-regulating 17 beta-estradiol (E-2) to support vitellogenesis and egg production, but E-2 secretion is known to have suppressive effects on red blood cell production (anti-erythropoiesis). We explored potential trade-offs between factors related to aerobic performance (hematocrit, reticulocyte index) and the expression of factors related to E-2-mediated vitellogenesis (i.e. yolk precursor production) in female macaroni penguins (Eudyptes chrysolophus), a species in which the physiologies controlling egg production and migratory activity run simultaneously (e.g. females experience a migratory conflict). We collected blood samples from penguins immediately upon their return to the colony, prior to egg laying. Hematocrit was elevated when the penguins returned to the colony (50.05% +/- 3.40 SD), which is similar to pre-laying values observed in other migratory bird species. Furthermore, mean reticulocyte levels were elevated (34.87% +/- 2.34), which is the highest level yet recorded in birds. Similarly, both plasma vitellogenin and yolk-targeted very low density lipoprotein levels were upregulated (2.30 +/- 0.06 mu g Zn ml(-1), and 9.70 +/- 0.19 mmol l(-1), respectively), indicating that penguins were reproductively active and producing eggs during migration and upon arrival on land. As predicted, a negative relationship between hematocrit and plasma vitellogenin was found, but we found no evidence to suggest that birds were experiencing reproductive anemia. Alternatively, we attribute the negative relationship to a hemodilution effect of yolk precursor secretion into circulation. It appears that female macaroni penguins are able to preserve hematocrit levels and new red blood cell production when migratory activity overlaps with reproductive processes. DOI PubMed
204. Maury, C; Serota, MW; Williams, TD. (2020) Plasticity in diurnal activity and temporal phenotype during parental care in European starlings, Sturnus vulgaris.Anim. Behav. 159: 37-45 Plasticity in diurnal activity and temporal phenotype during parental care in European starlings, Sturnus vulgaris
chronotype; daily activity; life history; parental care; plasticity; telemetry
We used an automated radiotelemetry system to determine diurnal patterns of activity and temporal phenotype (onset and cessation of activity) in female European starlings during breeding. Parental care is thought to be the most 'costly' part of reproduction, with high rates of intense activity due to foraging and provisioning for chicks, so we predicted that variation in timing of activity should be closely related to breeding success. Diurnal variation in activity varied systematically with breeding stage in a way consistent with specific demands of each phase of parental care: incubating females were more active late in the day (1600-1800 hours), while chick-rearing females were more active early in the morning (0700-1100 hours). There was marked individual variation in timing of onset, and to a lesser extent cessation, of activity, e.g. chick-rearing females first became active 7-127 min after morning civil twilight, with low to moderate repeatability within and among breeding stages (individual explained 2-62% of total variation). On average, females were active later, and ceased being active earlier, during chick rearing compared with incubation. Chick-rearing birds had a longer active day, but only by 2.3% (36% of the seasonal increase in total available daylength). Thus, chick-rearing females were relatively less active ('lazier'), which is consistent with the idea that parents work more efficiently rather than simply working harder. We found little evidence that chick-rearing activity was associated with variation in measures of current reproduction (provisioning rate, number and quality of chicks), future fecundity (initiating a second brood, cumulative 2-year productivity) or survival (local return rate). Our study demonstrates that time-keeping mechanisms show plasticity in response to reproductive state and can be modulated by 'biotic' (e.g. prey availability) or 'social' time (demands of parental care). (C) 2019 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. DOI
203. Criscuolo, F; Cornell, A; Zahn, S; Williams, TD. (2019) Oxidative status and telomere length are related to somatic and physiological maturation in chicks of European starlings (Stumus vulgaris).J. Exp. Biol. 222 Oxidative status and telomere length are related to somatic and physiological maturation in chicks of European starlings (Stumus vulgaris)
Growth; Body mass; Physiological traits; Telomere; Bird
Telomere length can be considered as an indicator of an organism's somatic state, long telomeres reflecting higher energy investment in self-maintenance. Early-life is a period of intense investment in somatic growth and in physiological maturation but how this is reflected in telomere length remains unclear. Using European starling chicks we tested: (i) how telomere length measured at asymptotic mass is related to proxies of somatic growth and physiological maturity in 17-day-old nestlings; (ii) how telomere length measured at 17 days then predicts the changes in somatic and physiological maturity occurring in fledglings (between 17 and 21 days); (iii) how growth and telomere length co-vary when chicks are under experimentally good (fed) growth conditions. Depending on environmental conditions, our data suggest links between somatic growth, physiological maturation and body maintenance parameters (positive with oxidative stress and negative with telomere length) in nestlings. Telomere length measured at day 17 predicted a subsequent change in physiological maturation variables observed in fledglings, but only in second-brood chicks: chicks with shorter telomeres had a higher pre-fledging rate of increase in haematocrit and haemoglobin content and a greater decrease in reticulocyte count. Finally, food supplementation of chicks did not change telomere length compared with that in control siblings. Our results suggest that physiological maturation prior to fledging may occur at the expense of telomere length but only when environmental conditions are sub-optimal. DOI PubMed
202. Eng, ML; Karouna-Renier, NK; Henry, PFP; Letcher, RJ; Schultz, SL; Bean, TG; Peters, LE; Palace, VP; Williams, TD; Elliott, JE; Fernie, KJ. (2019) In ovo exposure to brominated flame retardants Part II: Assessment of effects of TBBPA-BDBPE and BTBPE on hatching success, morphometric and physiological endpoints in American kestrels.Ecotox. Environ. Safe. 179: 151-159 In ovo exposure to brominated flame retardants Part II: Assessment of effects of TBBPA-BDBPE and BTBPE on hatching success, morphometric and physiological endpoints in American kestrels
Brominated flame retardants; Emerging flame retardants; American kestrels Falco sparverius; Avian toxicity; Developmental toxicity; Deiodinase enzymes
Tetrabromobisphenol A bis(2,3-dibromopropyl ether) (TBBPA-BDBPE) and 1,2-bis(2,4,6-tribromophenoxy) ethane (BTPBE) are both brominated flame retardants (BFRs) that have been detected in birds; however, their potential biological effects are largely unknown. We assessed the effects of embryonic exposure to TBBPA-BDBPE and BTBPE in a model avian predator, the American kestrel (Falco sparverius). Fertile eggs from a captive population of kestrels were injected on embryonic day 5 (ED5) with a vehicle control or one of three doses within the range of concentrations that have been detected in biota (nominal concentrations of 0, 10, 50 or 100 ng/g egg; measured concentrations 0, 3.0, 13.7 or 33.5 ng TBBPA-BDBPE/g egg and 0, 5.3, 26.8 or 58.1 ng BTBPE/g egg). Eggs were artificially incubated until hatching (ED28), at which point blood and tissues were collected to measure morphological and physiological endpoints, including organ somatic indices, circulating and glandular thyroid hormone concentrations, thyroid gland histology, hepatic deiodinase activity, and markers of oxidative stress. Neither compound had any effects on embryo survival through 90% of the incubation period or on hatching success, body mass, organ size, or oxidative stress of hatchlings. There was evidence of sex-specific effects in the thyroid system responses to the BTBPE exposures, with type 2 deiodinase (D2) activity decreasing at higher doses in female, but not in male hatchlings, suggesting that females may be more sensitive to BTBPE. However, there were no effects of TBBPA-BDBPE on the thyroid system in kestrels. For the BTPBE study, a subset of high-dose eggs was collected throughout the incubation period to measure changes in BTBPE concentrations. There was no decrease in BTBPE over the incubation period, suggesting that BTBPE is slowly metabolized by kestrel embryos throughout their similar to 28-d development. These two compounds, therefore, do not appear to be particularly toxic to embryos of the American kestrel. DOI PubMed
201. Eng, ML; Williams, TD; Fernie, KJ; Renier, NKK; Henry, PFP; Letcher, RJ; Elliott, JE. (2019) In ovo exposure to brominated flame retardants Part I: Assessment of effects of TBBPA-BDBPE on survival, morphometric and physiological endpoints in zebra finches.Ecotox. Environ. Safe. 179: 104-110 In ovo exposure to brominated flame retardants Part I: Assessment of effects of TBBPA-BDBPE on survival, morphometric and physiological endpoints in zebra finches
Brominated flame retardants; Emerging flame retardants; Avian; Zebra finch; Developmental toxicity; Tetrabromobisphenol A derivative
Tetrabromobisphenol A bis(2,3-dibromopropyl) ether (TBBPA-BDBPE) is an additive flame retardant used in polyolefins and polymers. It has been detected in biota, including in avian eggs, yet little is known of its effects. We assessed the pattern of TBBPA-BDBPE concentrations in songbird eggs over the incubation period, and the effects of embryonic exposure to TBBPA-BDBPE in a model songbird species, the zebra finch (Taeniopygia guttata). To assess concentrations during embryo development, eggs were injected on the day they were laid with the vehicle control (safflower oil) or 100 ng TBBPA-BDBPE/g egg, and whole egg contents were collected throughout embryonic development on day 0 (unincubated), 5, 10 and 13. To evaluate effects of embryonic exposure to TBBPA-BDBPE, eggs were injected at Hamburger-Hamilton stage 18 (similar to 80 h after initiation of incubation) with safflower oil only, 10, 50 or 100 ng TBBPA-BDBPE/g egg (albumin injection volume 1 mu l/g). Eggs were monitored for hatching success, and nestlings were monitored for growth and survival. At 15 days post-hatch, tissues were collected to assess physiological effects. TBBPA-BDBPE was incorporated into the egg as the embryo developed, and concentrations started declining in late incubation, suggesting biotransformation by the embryo. There were no effects on hatching success, nestling survival, growth, organ somatic indices, or thyroid hormone homeostasis; however, there was evidence that body condition declined in a dose-dependent manner towards the end of the rapid nestling growth phase. This decreased body condition could be a delayed effect of early developmental exposure, or it may be the result of increased exposure to biotransformation products of TBBPA-BDBPE produced over the nestling period, which are predicted to be more bioaccumulative and toxic than the parent compound. DOI PubMed
200. Laine, VN; Verhagen, I; Mateman, AC; Pijl, A; Williams, TD; Gienapp, P; van Oers, K; Visser, ME. (2019) Exploration of tissue-specific gene expression patterns underlying timing of breeding in contrasting temperature environments in a song bird.BMC Genomics 20 Exploration of tissue-specific gene expression patterns underlying timing of breeding in contrasting temperature environments in a song bird
Transcriptomics; Seasonal timing; Aves; Selection line
Background Seasonal timing of breeding is a life history trait with major fitness consequences but the genetic basis of the physiological mechanism underlying it, and how gene expression is affected by date and temperature, is not well known. In order to study this, we measured patterns of gene expression over different time points in three different tissues of the hypothalamic-pituitary-gonadal-liver axis, and investigated specifically how temperature affects this axis during breeding. We studied female great tits (Parus major) from lines artificially selected for early and late timing of breeding that were housed in two contrasting temperature environments in climate-controlled aviaries. We collected hypothalamus, liver and ovary samples at three different time points (before and after onset of egg-laying). For each tissue, we sequenced whole transcriptomes of 12 pools (n = 3 females) to analyse gene expression. Results Birds from the selection lines differed in expression especially for one gene with clear reproductive functions, zona pellucida glycoprotein 4 (ZP4), which has also been shown to be under selection in these lines. Genes were differentially expressed at different time points in all tissues and most of the differentially expressed genes between the two temperature treatments were found in the liver. We identified a set of hub genes from all the tissues which showed high association to hormonal functions, suggesting that they have a core function in timing of breeding. We also found ample differentially expressed genes with largely unknown functions in birds. Conclusions We found differentially expressed genes associated with selection line and temperature treatment. Interestingly, the latter mainly in the liver suggesting that temperature effects on egg-laying date may happen down-stream in the physiological pathway. These findings, as well as our datasets, will further the knowledge of the mechanisms of tissue-specific avian seasonality in the future. DOI PubMed
199. Serota, MW; Williams, TD. (2019) Adjustment of total activity as a response to handicapping European starlings during parental care.Anim. Behav. 148 Adjustment of total activity as a response to handicapping European starlings during parental care
activity; automated telemetry; costs of reproduction; handicapping; parental care
Parental care is widely assumed to be costly, and life-history theory predicts that individuals that invest more in parental care should benefit in terms of number of offspring produced but that increased parental care might come at a cost in terms of decreased future fecundity and/or survival. However, the notion that parents that work 'harder', commonly measured by the rate at which parents visit the nestbox to provision their chicks, produce more, fitter chicks is surprisingly poorly supported. One potential reason for this apparent lack of relationship between measured workload during parental care and breeding productivity is that nest visit rate does not provide a good measure of foraging effort. Here, we used an automated radiotelemetry system to measure activity of individual female European starlings, Sturnus vulgaris, during breeding, combined with a handicapping experiment (combination of radiotransmitters and wing clipping) and measures of foraging metrics, current breeding productivity, future fecundity and return rate. Handicapping decreased current breeding success due to higher abandonment and nest failure, but among successful birds (fledging >= 1 chick) there was no effect of handicapping on brood size at fledging for the current breeding attempt. Handicapping decreased future fecundity, the probability of initiating a second brood, and return rate, but there was no evidence for additive costs of reproduction in wing-clipped females. Handicapping had no effect on provisioning rate but automated tracking data showed that, during chick rearing, wing-clipped females had 22% lower activity compared to females with radios only. Our data provide an explanation for the often contradictory effects of handicapping reported on reproductive effort and costs of reproduction: individuals can use behavioural flexibility - decreasing overall activity while maintaining provisioning rate - along with changes in mass and nestling diet to mitigate putative effects of increased workload imposed by handicapping. (C) 2018 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. DOI
198. Torres, R; Chin, E; Rampton, R; Williams, TD. (2019) Are there synergistic or antagonistic effects of multiple maternally derived egg components on offspring phenotype?J. Exp. Biol. 222 Are there synergistic or antagonistic effects of multiple maternally derived egg components on offspring phenotype?
Multivariate egg; Maternal effects; Maternal antibodies; Yolk testosterone; Taeniopygia guttata
Eggs are 'multivariate' in that they contain multiple maternally derived egg components (e.g. hormones, antibodies, mRNA, antioxidants) which are thought to influence offspring phenotype. However, most studies have focused on single egg components and on short-term effects. Here, we simultaneously manipulated two egg components, maternally derived antibodies (MAb) and yolk testosterone, to assess potential synergistic or antagonistic effects on zebra finch offspring phenotype from hatching to sexual maturity. We found no evidence for short- or long-term effects of either MAb or yolk testosterone alone, or their interaction, on hatching mass, size at fledging (tarsus length), body mass at sexual maturity (day 82), chick survival, humoral immune function or any measured female reproductive trait at sexual maturity. There was a positive effect of yolk testosterone, but not MAb, on offspring phytohaemagglutinin (PHA) response at 26 days of age but at 82 days of age. MAb, but not yolk testosterone, had a positive effect on PHA response. There was also a MAbxsex interaction on 30 day chick mass, and a positive effect of yolk testosterone on male courtship behaviour at sexual maturity. However, we found no evidence for synergy, i.e. where offspring treated with both MAb and yolk testosterone had higher trait values than offspring treated with either MAb or yolk testosterone alone for any measured trait. Similarly, evidence for antagonistic (compensatory) effects, where offspring treated with both MAb and yolk testosterone had intermediate trait values compared with offspring treated with either MAID or yolk testosterone alone, was equivocal. DOI PubMed
197. Verhagen, I; Laine, VN; Mateman, AC; Pijl, A; de Wit, R; van Lith, B; Kamphuis, W; Viitaniemi, HM; Williams, TD; Caro, SP; Meddle, SL; Gienapp, P; van Oers, K; Visser, ME. (2019) Fine-tuning of seasonal timing of breeding is regulated downstream in the underlying neuro-endocrine system in a small songbird.J. Exp. Biol. 222 Fine-tuning of seasonal timing of breeding is regulated downstream in the underlying neuro-endocrine system in a small songbird
Reproductive timing; Individual variation; Gene expression; qPCR; Parus major
The timing of breeding is under selection in wild populations as a result of climate change, and understanding the underlying physiological processes mediating this timing provides insight into the potential rate of adaptation. Current knowledge on this variation in physiology is, however, mostly limited to males. We assessed whether individual differences in the timing of breeding in females are reflected in differences in candidate gene expression and, if so, whether these differences occur in the upstream (hypothalamus) or downstream (ovary and liver) parts of the neuroendocrine system. We used 72 female great tits from two generations of lines artificially selected for early and late egg laying, which were housed in climate-controlled aviaries and went through two breeding cycles within 1 year. In the first breeding season we obtained individual egg-laying dates, while in the second breeding season, using the same individuals, we sampled several tissues at three time points based on the timing of the first breeding attempt. For each tissue, mRNA expression levels were measured using qPCR for a set of candidate genes associated with the timing of reproduction and subsequently analysed for differences between generations, time points and individual timing of breeding. We found differences in gene expression between generations in all tissues, with the most pronounced differences in the hypothalamus. Differences between time points, and early- and late-laying females, were found exclusively in the ovary and liver. Altogether, we show that fine-tuning of the seasonal timing of breeding, and thereby the opportunity for adaptation in the neuroendocrine system, is regulated mostly downstream in the neuro-endocrine system. DOI PubMed
196. Vitousek, MN; Johnson, MA; Downs, CJ; Miller, ET; Martin, LB; Francis, CD; Donald, JW; Fuxjager, MJ; Goymann, W; Hau, M; Husak, JF; Kircher, BK; Knapp, R; Schoenle, LA; Williams, TD. (2019) Macroevolutionary Patterning in Glucocorticoids Suggests Different Selective Pressures Shape Baseline and Stress-Induced Levels.Am. Nat. 193: 866-880 Macroevolutionary Patterning in Glucocorticoids Suggests Different Selective Pressures Shape Baseline and Stress-Induced Levels
stress; comparative physiology; cortisol; corticosterone; steroid; evolutionary endocrinology
Glucocorticoid (GC) hormones are important phenotypic mediators across vertebrates, but their circulating concentrations can vary markedly. Here we investigate macroevolutionary patterning in GC levels across tetrapods by testing seven specific hypotheses about GC variation and evaluating whether the supported hypotheses reveal consistent patterns in GC evolution. If selection generally favors the "supportive" role of GCs in responding effectively to challenges, then baseline and/or stress-induced GCs may be higher in challenging contexts. Alternatively, if selection generally favors "protection" from GC-induced costs, GCs may be lower in environments where challenges are more common or severe. The predictors of baseline GCs were all consistent with supportive effects: levels were higher in smaller organisms and in those inhabiting more energetically demanding environments. During breeding, baseline GCs were also higher in populations and species with fewer lifetime opportunities to reproduce. The predictors of stress-induced GCs were instead more consistent with the protection hypothesis: during breeding, levels were lower in organisms with fewer lifetime reproductive opportunities. Overall, these patterns indicate a surprising degree of consistency in how some selective pressures shape GCs across broad taxonomic scales; at the same time, in challenging environments selection appears to operate on baseline and stress-induced GCs in distinct ways. DOI PubMed
195.Williams, TD; Cornell, A; Gillespie, C; Hura, A; Serota, M. (2019) Effects of an introduced, novel prey on diet and reproduction in the diet-specialist European Starling (Sturnus vulgaris).Can. J. Zool. 97 Effects of an introduced, novel prey on diet and reproduction in the diet-specialist European Starling (Sturnus vulgaris)
insect farming; European Starlings; diet specialization; tipulid; Hermetia illucens; breeding productivity; specialist-generalist
Diet specialization has important consequences for how individuals or species deal with environmental change that causes changes in availability of prey species. We took advantage of a "natural experiment" - establishment of a commercial insect farm - that introduced a novel prey item, black soldier flies (Hermetia illucens (Linnaeus, 1758)), to the diet-specialist European Starling (Sturnus vulgaris Linnaeus, 1758). We investigated evidence for individual diet specialization (IDS) and the consequences of diet specialization and exploitation of novel prey on breeding productivity. In all 4 years of our study, tipulid larvae were the most common prey item. Soldier flies were not recorded in diets in 2013-2014; however, coincident with the establishment of the commercial insect farming operation, they comprised 22% and 30% of all prey items in the diets of European Starling females and males, respectively, in 2015. There was marked individual variation in use of soldier flies (4%-48% and 2%-70% in females and males, respectively), but we found little evidence of dichotomous IDS, i.e., where only some individuals have a specialized diet. We found no evidence for negative effects of use of soldier flies on breeding productivity: brood size at fledging and chick quality (mass, tarsus length) were independent of the number and proportion (%) of soldier flies returned to the nest. DOI
194. Yap, KN; Tsai, OHI; Williams, TD. (2019) Haematological traits co-vary with migratory status, altitude and energy expenditure: a phylogenetic, comparative analysis.Sci Rep 9 Haematological traits co-vary with migratory status, altitude and energy expenditure: a phylogenetic, comparative analysis
Aerobic capacity is assumed to be a main predictor of workload ability and haematocrit (Hct) and haemoglobin (Hb) have been suggested as key determinants of aerobic performance. Intraspecific studies have reported increases in Hct and Hb in response to increased workload. Furthermore, Hct and Hb vary markedly among individuals and throughout the annual cycle in free-living birds and it has been suggested that this variation reflects adaptive modulation of these traits to meet seasonal changes in energy demands. We used a comparative dataset of haematological traits, measures of metabolic rate (57 species), and life-history traits (160 species) to test several hypotheses for adaptive variation in haematology in relation to migration and altitude. We then extended these general ideas to test relationships between Hct and basal metabolic rate, daily energy expenditure and activity energy expenditure, using the 57 species that we have metabolic rate information for. We found that at the interspecific level, full migrants have higher Hct and Hb than partial migrants and non-migrants, and that altitude is positively correlated with Hb but not Hct. Hct is positively associated with activity energy expenditure (energy spent specifically on costly activities), suggesting that haematological traits could be adaptively modulated based on life-history traits and that Hct is a potential physiological mediator of energetic constraint. DOI PubMed
193. Casagrande, S; Garamszegi, LZ; Goymann, W; Donald, J; Francis, CD; Fuxjager, MJ; Husak, JF; Johnson, MA; Kircher, B; Knapp, R; Martin, LB; Miller, ET; Schoenle, LA; Vitousek, MN; Williams, TD; Hau, M. (2018) Do Seasonal Glucocorticoid Changes Depend on Reproductive Investment? A Comparative Approach in Birds.Integr. Comp. Biol. 58 Do Seasonal Glucocorticoid Changes Depend on Reproductive Investment? A Comparative Approach in Birds
Animals go through different life history stages such as reproduction, moult, or migration, of which some are more energy-demanding than others. Baseline concentrations of glucocorticoid hormones increase during moderate, predictable challenges and thus are expected to be higher when seasonal energy demands increase, such as during reproduction. By contrast, stress-induced glucocorticoids prioritize a survival mode that includes reproductive inhibition. Thus, many species down-regulate stress-induced glucocorticoid concentrations during the breeding season. Interspecific variation in glucocorticoid levels during reproduction has been successfully mapped onto reproductive investment, with species investing strongly in current reproduction (fast pace of life) showing higher baseline and lower stress-induced glucocorticoid concentrations than species that prioritize future reproduction over current attempts (slow pace of life). Here we test the "glucocorticoid seasonal plasticity hypothesis", in which we propose that interspecific variation in seasonal changes in glucocorticoid concentrations from the non-breeding to the breeding season will be related to the degree of reproductive investment (and thus pace of life). We extracted population means for baseline (for 54 species) and stress-induced glucocorticoids (for 32 species) for the breeding and the non-breeding seasons from the database "HormoneBase", also calculating seasonal glucocorticoid changes. We focused on birds because this group offered the largest sample size. Using phylogenetic comparative methods, we first showed that species differed consistently in both average glucocorticoid concentrations and their changes between the two seasons, while controlling for sex, latitude, and hemisphere. Second, as predicted seasonal changes in baseline glucocorticoids were explained by clutch size (our proxy for reproductive investment), with species laying larger clutches showing a greater increase during the breeding season-especially in passerine species. In contrast, changes in seasonal stress-induced levels were not explained by clutch size, but sample sizes were more limited. Our findings highlight that seasonal changes in baseline glucocorticoids are associated with a species' reproductive investment, representing an overlooked physiological trait that may underlie the pace of life. DOI
192. Eng, ML; Winter, V; Elliott, JE; MacDougall-Shackleton, SA; Williams, TD. (2018) Embryonic Exposure to Environmentally Relevant Concentrations of a Brominated Flame Retardant Reduces the Size of Song-Control Nuclei in a Songbird.Dev. Neurobiol. 78 Embryonic Exposure to Environmentally Relevant Concentrations of a Brominated Flame Retardant Reduces the Size of Song-Control Nuclei in a Songbird
PBDEs; avian; song system; neurotoxicology; developmental stress
Environmental contaminants have the potential to act as developmental stressors and impair development of song and the brain of songbirds, but they have been largely unstudied in this context. 2,2',4,4,5-Pentabromodiphenyl ether (BDE-99) is a brominated flame retardant congener that has demonstrated endocrine disrupting effects, and has pervaded the global environment. We assessed the effects of in ovo exposure to environmentally relevant levels of BDE-99 on the neuroanatomy of the song-control system in a model songbird species, the zebra finch (Taeniopygia guttata). Embryos were exposed via egg injection to a vehicle control (DMSO), 10, 100, or 1000 ng BDE-99/g egg on the day the egg was laid. Chicks were raised to sexual maturity to investigate long-term effects of BDE-99 on the adult male brain. Three key song-control nuclei (Area X, HVC, RA) all showed a dose-dependent trend toward decreasing volume as BDE-99 concentration increased, and birds exposed to 1000 ng/g in ovo BDE-99 had significantly smaller song-control nuclei volume compared to control birds. High environmental concentrations of BDE-99 in avian tissues can be within that range and thus could affect development of the song-control system in birds, and potentially other processes. We previously found that BDE-99 exposure during the nestling period had no effect of on the song-control system, although it did have significant effects on some behaviural endpoints. Taken together, these results suggest that exposure to polybrominated diphenyl ether (PBDEs) during critical developmental windows can significantly alter neurological development. (c) 2018 Wiley Periodicals, Inc. DOI PubMed
191. Fowler, MA; Paquet, M; Legault, V; Cohen, AA; Williams, TD. (2018) Physiological predictors of reproductive performance in the European Starling (Sturnus vulgaris).Front. Zool. 15 Physiological predictors of reproductive performance in the European Starling (Sturnus vulgaris)
Dysregulation; European starling; Physiological complexity; Physiological state; Principal components analysis; Reproductive fitness; Statistical distance; Sturnus vulgaris
Background: It is widely assumed that variation in fitness components has a physiological basis that might underlie selection on trade-offs, but the mechanisms driving decreased survival and future fecundity remain elusive. Here, we assessed whether physiological variables are related to workload ability or immediate fitness consequences and if they mediate future survival or reproductive success. We used data on 13 physiological variables measured in 93 female European starlings (Sturnus vulgaris) at two breeding stages (incubation, chick-rearing), for first-and second-broods over two years (152 observations). Results: There was little co-variation among the physiological variables, either in incubating or chick-rearing birds, but some systematic physiological differences between the two stages. Chick-rearing birds had lower hematocrit and plasma creatine kinase but higher hemoglobin, triglyceride and uric acid levels. Only plasma corticosterone was repeatable between incubation and chick-rearing. We assessed relationships between incubation or chick-rearing physiology and measures of workload, current productivity, future fecundity or survival in a univariate manner, and found very few significant relationships. Thus, we next explored the utility of multivariate analysis (principal components analysis, Mahalanobis distance) to account for potentially complex physiological integration, but still found no clear associations. Conclusions: This implies either that a) birds maintained physiological variables within a homeostatic range that did not affect their performance, b) there are relatively few links between physiology and performance, or, more likely, c) that the complexity of these relationships exceeds our ability to measure it. Variability in ecological context may complicate the relationship between physiology and behavior. We thus urge caution regarding the over-interpretation of isolated significant findings, based on single traits in single years, in the literature. DOI PubMed
190. Francis, CD; Donald, JW; Fuxjager, MJ; Goymann, W; Hau, M; Husak, JF; Johnson, MA; Kircher, BK; Knapp, R; Martin, LB; Miller, ET; Schoenle, LA; Vitousek, MN; Williams, TD; Downs, CJ. (2018) Metabolic Scaling of Stress Hormones in Vertebrates.Integr. Comp. Biol. 58 Metabolic Scaling of Stress Hormones in Vertebrates
Glucocorticoids (GCs) are stress hormones that can strongly influence physiology, behavior, and an organism's ability to cope with environmental change. Despite their importance, and the wealth of studies that have sought to understand how and why GC concentrations vary within species, we do not have a clear understanding of how circulating GC levels vary within and across the major vertebrate clades. New research has proposed that much interspecific variation in GC concentrations can be explained by variation in metabolism and body mass. Specifically, GC concentrations should vary proportionally with mass-specific metabolic rates and, given known scaling relationships between body mass and metabolic rate, GC concentrations should scale to the -1/4 power of body mass and to the power of 1 with mass-specific metabolic rate. Here, we use HormoneBase, the newly compiled database that includes plasma GC concentrations from free-living and unmanipulated vertebrates, to evaluate this hypothesis. Specifically, we explored the relationships between body mass or mass-specific metabolic rate and either baseline or stress-induced GC (cortisol or corticosterone) concentrations in tetrapods. Our phylogenetically-informed models suggest that, whereas the relationship between GC concentrations and body mass across tetrapods and among mammals is close to -1/4 power, this relationship does not exist in amphibians, reptiles, and birds. Moreover, with the exception of a positive association between stress-induced GC concentrations and mass-specific metabolic rate in birds, we found little evidence that GC concentrations are linked to metabolic rate, although the number of species sampled was quite limited for amphibians and somewhat so for reptiles and mammals. Nevertheless, these results stand in contrast to the generally accepted association between the two and suggest that our observed positive association between body mass and GC concentrations may not be due to the well-established link between mass and metabolism. Large-scale comparative approaches can come with drawbacks, such as pooling and pairing observations from separate sources. However, these broad analyses provide an important counterbalance to the majority of studies examining variation in GC concentrations at the population or species level, and can be a powerful approach to testing both long-standing and new questions in biology. DOI PubMed
189. Garamszegi, LZ; Donald, J; Francis, CD; Fuxjager, MJ; Goymann, W; Hau, M; Husak, JF; Johnson, MA; Kircher, B; Knapp, R; Martin, LB; Miller, ET; Schoenle, LA; Vitousek, MN; Williams, TD. (2018) Species-Specific Means and Within-Species Variance in Glucocorticoid Hormones and Speciation Rates in Birds.Integr. Comp. Biol. 58 Species-Specific Means and Within-Species Variance in Glucocorticoid Hormones and Speciation Rates in Birds
At macroevolutionary scales, stress physiology may have consequences for species diversification and subspecies richness. Populations that exploit new resources or undergo range expansion should cope with new environmental challenges, which could favor higher mean stress responses. Within-species variation in the stress response may also play a role in mediating the speciation process: in species with broad variation, there will always be some individuals that can tolerate an unpredictable environment, whereas in species with narrow variation there will be fewer individuals that are able to thrive in a new ecological niche. We tested for the evolutionary relationship between stress response, speciation rate, and subspecies richness in birds by relying on the HormoneBase repository, from which we calculated within-and among-species variation in baseline (BL) and stress-induced (SI) corticosterone levels. To estimate speciation rates, we applied Bayesian analysis of macroevolutionary mixtures that can account for variation in diversification rate among clades and through time. Contrary to our predictions, lineages with higher diversification rates were not characterized by higher BL or SI levels of corticosterone either at the tips or at the deeper nodes of the phylogeny. We also found no association between mean hormone levels and subspecies richness. Within-species variance in corticosterone levels showed close to zero repeatability, thus it is highly unlikely that this is a species-specific trait that influences diversification rates. These results imply that stress physiology may play a minor, if any, role in determining speciation rates in birds. DOI PubMed
188. Hennin, HL; Dey, CJ; Bety, J; Gilchrist, HG; Legagneux, P; Williams, TD; Love, OP. (2018) Higher rates of prebreeding condition gain positively impacts clutch size: A mechanistic test of the condition-dependent individual optimization model.Funct. Ecol. 32 Higher rates of prebreeding condition gain positively impacts clutch size: A mechanistic test of the condition-dependent individual optimization model
clutch size; common eider; condition gain; fattening rate; individual optimization; laying date; path analysis; triglyceride
1. A combination of timing of and body condition (i.e., mass) at arrival on the breeding grounds interact to influence the optimal combination of the timing of reproduction and clutch size in migratory species. This relationship has been formalized by Rowe et al. in a condition-dependent individual optimization model (American Naturalist, 1994, 143, 689-722), which has been empirically tested and validated in avian species with a capital-based breeding strategy. 2. This model makes a key, but currently untested prediction; that variation in the rate of body condition gain will shift the optimal combination of laying date and clutch size. This prediction is essential because it implies that individuals can compensate for the challenges associated with late timing of arrival or poor body condition at arrival on the breeding grounds through adjustment of their life history investment decisions, in an attempt to maximize fitness. 3. Using an 11-year data set in arctic-nesting common eiders (Somateria mollissima), quantification of fattening rates using plasma triglycerides (an energetic metabolite), and a path analysis approach, we test this prediction of this optimization model; controlling for arrival date and body condition, females that fatten more quickly will adjust the optimal combination of lay date and clutch size, in favour of a larger clutch size. 4. As predicted, females fattening at higher rates initiated clutches earlier and produced larger clutch sizes, indicating that fattening rate is an important factor in addition to arrival date and body condition in predicting individual variation in reproductive investment. However, there was no direct effect of fattening rate on clutch size (i.e., birds laying on the same date had similar clutch sizes, independent of their fattening rate). Instead, fattening rate indirectly affected clutch size via earlier lay dates, thus not supporting the original predictions of the optimization model. 5. Our results demonstrate that variation in the rate of condition gain allows individuals to shift flexibly along the seasonal decline in clutch size to presumably optimize the combination of laying date and clutch size. DOI
187. Martin, LB; Vitousek, M; Donald, JW; Flock, T; Fuxjager, MJ; Goymann, W; Hau, M; Husak, J; Johnson, MA; Kircher, B; Knapp, R; Miller, ET; Schoenle, LA; Williams, T; Francis, CD. (2018) IUCN Conservation Status Does Not Predict Glucocorticoid Concentrations in Reptiles and Birds.Integr. Comp. Biol. 58 IUCN Conservation Status Does Not Predict Glucocorticoid Concentrations in Reptiles and Birds
Circulating glucocorticoids (GCs) are the most commonly used biomarkers of stress in wildlife. However, their utility as a tool for identifying and/or managing at-risk species has varied. Here, we took a very broad approach to conservation physiology, asking whether International Union for the Conservation of Nature (IUCN) listing status (concern versus no obvious concern) and/or location within a geographic range (edge versus non-edge) predicted baseline and post-restraint concentrations of corticosterone (CORT) among many species of birds and reptiles. Even though such an approach can be viewed as coarse, we asked in this analysis whether CORT concentrations might be useful to implicate species at risk. Indeed, our effort, relying on HormoneBase, a repository of data on wildlife steroids, complements several other large-scale efforts in this issue to describe and understand GC variation. Using a phylogenetically informed Bayesian approach, we found little evidence that either IUCN status or edge/non-edge location in a geographic distribution were related to GC levels. However, we did confirm patterns described in previous studies, namely that breeding condition and evolutionary relatedness among species predicted some GC variation. Given the broad scope of our work, we are reluctant to conclude that IUCN status and location within a range are unrelated to GC regulation. We encourage future more targeted efforts on GCs in at-risk populations to reveal how factors leading to IUCN listing or the environmental conditions at range edges impact individual performance and fitness, particularly in the mammals, amphibians, and fish species we could not study here because data are currently unavailable. DOI PubMed
186. Morran, SAM; Elliott, JE; Young, JML; Eng, ML; Basu, N; Williams, TD. (2018) Ecologically-relevant exposure to methylmercury during early development does not affect adult phenotype in zebra finches (Taeniopygia guttata).Ecotoxicology 27 Ecologically-relevant exposure to methylmercury during early development does not affect adult phenotype in zebra finches (Taeniopygia guttata)
Methylmercury; Avian; Growth; Behaviour; Reproduction; Zebra Finch
Methylmercury causes behavioural and reproductive effects in adult mammals via early developmental exposure. Similar studies in birds are limited and mostly focussed on aquatic systems, but recent work has reported high blood mercury concentrations in terrestrial, passerine songbirds. We used the zebra finch (Taeniopygia guttata) as a model to explore the long-term effects of early developmental exposure to methylmercury exposure. Chicks were dosed orally with either the vehicle control, 0.0315 A mu g Hg/g bw/day, or 0.075 A mu g Hg/g bw/day throughout the nestling period (days 1-21 post-hatching). We then measured (a) short-term effects on growth, development, and behaviour (time to self-feeding, neophobia) until 30 days of age (independence), and (b) long-term effects on courtship behaviour and song (males) and reproduction (females) once methylmercury-exposed birds reached sexual maturity (90 days post-hatching). High methylmercury treated birds had mean blood mercury of 0.734 +/- 0.163 A mu g/g at 30 days post-hatching, within the range of values reported for field-sampled songbirds at mercury contaminated sites. However, there were no short-term effects of treatment on growth, development, and behaviour of chicks, and no long-term effects on courtship behaviour and song in males or reproductive performance in females. These results suggest that the nestling period is not a critical window for sensitivity to mercury exposure in zebra finches. Growing nestlings can reduce blood mercury levels through somatic growth and depuration into newly growing feathers, and as a result they might actually be less susceptible compared to adult birds receiving the same level of exposure. DOI PubMed
185. Vitousek, MN; Johnson, MA; Donald, JW; Francis, CD; Fuxjager, MJ; Goymann, W; Hau, M; Husak, JF; Kircher, BK; Knapp, R; Martin, LB; Miller, ET; Schoenle, LA; Uehling, JJ; Williams, TD. (2018) Data Descriptor: HormoneBase, a population-level database of steroid hormone levels across vertebrates.Sci. Data 5 Data Descriptor: HormoneBase, a population-level database of steroid hormone levels across vertebrates
Hormones are central regulators of organismal function and flexibility that mediate a diversity of phenotypic traits from early development through senescence. Yet despite these important roles, basic questions about how and why hormone systems vary within and across species remain unanswered. Here we describe HormoneBase, a database of circulating steroid hormone levels and their variation across vertebrates. This database aims to provide all available data on the mean, variation, and range of plasma glucocorticoids (both baseline and stress-induced) and androgens in free-living and un-manipulated adult vertebrates. HormoneBase (www.HormoneBase.org) currently includes >6,580 entries from 476 species, reported in 648 publications from 1967 to 2015, and unpublished datasets. Entries are associated with data on the species and population, sex, year and month of study, geographic coordinates, life history stage, method and latency of hormone sampling, and analysis technique. This novel resource could be used for analyses of the function and evolution of hormone systems, and the relationships between hormonal variation and a variety of processes including phenotypic variation, fitness, and species distributions. DOI PubMed
184.Williams, TD. (2018) Physiology, activity and costs of parental care in birds.J. Exp. Biol. 221 Physiology, activity and costs of parental care in birds
Parental care; Costs of reproduction; Activity; Foraging; Physiological costs; Flight
Parental care is assumed to be costly in that it requires sustained, high-intensity activity sufficient to cause costs of reproduction (decreased survival and future fecundity of parents). Costs of reproduction are, in turn, thought to have a physiological basis where intense activity causes a decrease in parental condition. However, attempts to identify the physiological basis of costs of reproduction have produced mixed results. Here, I argue that in birds, the central idea that parental care represents sustained, high-intensity work might be incorrect. Specifically: (a) the duration of intense activity associated with chick-rearing might be quite limited; (b) flight, the most obvious sustained, high-intensity activity, might only represent a small component of an individual's overall activity budget; (c) some (high-quality) individuals might be able to tolerate costs of intense activity, either owing to their physiological state or because they have access to more resources, without perturbation of physiological homeostasis; and (d) individuals might utilise other mechanisms to modulate costs of activity, for example, mass loss, again avoiding more substantial physiological costs. Furthermore, I highlight the important fact that life-history theory predicts that reproductive trade-offs should only be expected under food stress. Most birds breed in spring and early summer precisely because of seasonal increases in food abundance, and so it is unclear how often parents are food stressed. Consequently, I argue that there are many reasons why costs of reproduction, and any physiological signature of these costs, might be quite rare, both temporally (in different years) and among individuals. DOI PubMed
183. Yap, KN; Dick, MF; Guglielmo, CG; Williams, TD. (2018) Effects of experimental manipulation of hematocrit on avian flight performance in high- and low-altitude conditions.J. Exp. Biol. 221 Effects of experimental manipulation of hematocrit on avian flight performance in high- and low-altitude conditions
Hemoglobin; Aerobic capacity; Hemodilution; Wind tunnel; Exercise; Birds
Despite widely held assumptions that hematocrit (Hct) is a key determinant of aerobic capacity and exercise performance, this relationship has not often been tested rigorously in birds and results to date are mixed. Migration in birds involves high-intensity exercise for long durations at various altitudes. Therefore, it provides a good model system to examine the effect of Hct on flight performance and physiological responses of exercise at high altitude. We treated yellow-rumped warblers (Setophaga coronata) with avian erythropoietin (EPO) and anti-EPO to experimentally manipulate Hct and assessed flight performance at low and high altitudes using a hypobaric wind tunnel. We showed that anti-EPO-treated birds had lower Hct than vehicle- and EPO-treated birds post-treatment. Anti-EPO-treated birds also had marginally lower exercise performance at low altitude, committing a higher number of strikes (mistakes) in the first 30 min of flight. However, anti-EPO-treated birds performed significantly better at high altitude, attaining a higher altitude in a ramped altitude challenge to 3000 m equivalent altitude, and with a longer duration of flight at high altitude. Birds exercising at high altitude showed decreased Hct, increased glucose mobilization and decreased antioxidant capacity, regardless of treatment. In summary, we provide experimental evidence that the relationship between Hct and exercise performance is dependent on altitude. Future studies should investigate whether free-living birds adaptively modulate their Hct, potentially through a combination of erythropoiesis and plasma volume regulation (i.e. hemodilution), based on the altitude they fly at during migratory flight. DOI PubMed
182. Cornell, A; Gibson, KF; Williams, TD. (2017) Physiological maturity at a critical life-history transition and flight ability at fledging.Functional Ecology 31: 662-670 Physiological maturity at a critical life-history transition and flight ability at fledging
developmental maturity; fledging; flight ability; haemoglobin; life-history transition; physiology
<ol start="1" class="">
<li>Developmental maturity (e.g. body condition, body mass) at major life-history transitions is known to affect fitness across a wide range of taxa.</li>
<li>Fledging (leaving the nest), a major life-history transition in birds, is associated with high post-fledging mortality and is widely assumed to be related to poor initial flight ability of fledglings, which, in turn, might be related to developmental maturity at fledging.</li>
<li>We investigated individual variation in developmental maturity of both somatic and physiological traits at this critical life-history transition in different ecological contexts (year, first or second broods) to determine the importance of physiological traits related to oxygen-carrying capacity (haematocrit, haemoglobin) for individual variation in initial flight ability at fledging.</li>
<li>Haemoglobin concentration and haematocrit at fledging had much higher variance than somatic traits and were more variable across ecological contexts. Furthermore, fledgling haemoglobin concentration was the least developmentally mature of all traits (on average, only 78% of adult concentration).</li>
<li>Fledglings from second broods, which are known to have lower post-fledging survival, were less developmentally mature than fledglings from first broods for all traits (except tarsus), with haematocrit and haemoglobin concentration being the most developmentally immature traits (in first vs. second broods, haematocrit: 47·1% vs. 40·9%; haemoglobin: 13·3 vs. 11·6 g dL<sup>−1</sup>).</li>
<li>Models predicting individual variation in two aspects of initial flight ability (total energy gain, take-off angle) were significantly improved when physiological traits (in particular haemoglobin) were incorporated into models based on somatic traits.</li>
</ol> DOI
181. Cornell, A; Hou, JJ; Williams, TD. (2017) Experimentally increased prebreeding male social behaviour has no effect on female breeding phenology and performance.Animal Behaviour 126: 243-251 Experimentally increased prebreeding male social behaviour has no effect on female breeding phenology and performance
bird; egg laying; phenology; social cue; song
In the context of breeding phenology, social behaviour (especially song) has long been considered an important 'supplemental cue' that females integrate with other environmental information to determine timing of egg laying. However, to our knowledge, no studies have experimentally manipulated song in the wild in the context of female breeding phenology and performance. We studied natural variation in, and response to experimental manipulation of, prebreeding song and social behaviour in European starlings, Sturnus vulgaris, to determine whether male behaviour acts as a phenological cue determining female timing of egg laying and subsequent, postlaying breeding performance. In our highly synchronous system, natural variation in prebreeding male song quality and singing effort was surprisingly high, and singing increased slightly closer to egg-laying date. There was a strong prebreeding response of both males and females to the playback treatment, but no effect on female breeding phenology (egg-laying date) or performance (nestbox occupancy, egg size, clutch size, total chicks hatched, total chicks fledged or double-brooding behaviour). Our 3-year study finds no evidence that male prebreeding song is a cue determining female breeding phenology or performance in starlings. (C) 2017 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. DOI
180. Cornell, A; Williams, TD. (2017) Variation in developmental trajectories of physiological and somatic traits in a common songbird approaching fledging.Journal of Experimental Biology 220: 4060-4067 Variation in developmental trajectories of physiological and somatic traits in a common songbird approaching fledging
Development; Chick; Ecophysiology; Food supplementation; Haemoglobin; Haematocrit
In avian species, little is known about the development of physiological traits in the days preceding fledging, a critical life history transition marked by a high mortality rate. Developmental trajectory during this period may be flexible based on ecological context or hardwired, with potential costs for variation in growth in the form of oxidative stress. Patterns in development are likely to relate to variation in life history, for which seabirds and aerial insectivores have been well studied, while our focal species is a grassland ground forager, the European starling (Sturnus vulgaris). We show that changes in haematocrit, body mass and wing length are independent of year and brood quality, while changes in haemoglobin concentration are higher in low-quality broods. Moreover, we also identify higher oxidative stress in low-quality year and second broods, a potential cost for maintaining a hardwired developmental trajectory in a lower quality environment. Finally, we experimentally test the effects of food supplementation on development and maturity of chicks at fledging to show that although food increases body mass early in development, it does not change the trajectory or final maturity of chicks at fledging. Collectively this study demonstrates that some developmental changes prior to fledging may be hardwired, but may have long-term oxidative costs in low-quality environments. DOI
179. Crossin, GT; Phillips, RA; Lattin, CR; Romero, LM; Bordeleau, X; Harris, CM; Love, OP; Williams, TD. (2017) Costs of reproduction and carry-over effects in breeding albatrosses.Antarctic Science 29: 155-164 Costs of reproduction and carry-over effects in breeding albatrosses
feather corticosterone; glucocorticoids; haematocrit; migration; testosterone; triglycerides
We investigated the physiology of two closely related albatross species relative to their breeding strategy: black-browed albatrosses (Thalassarche melanophris) breed annually, while grey-headed albatrosses (T. chrysostoma) breed biennially. From observations of breeding fate and blood samples collected at the end of breeding in one season and feather corticosterone levels (fCort) sampled at the beginning of the next breeding season, we found that in both species some post-breeding physiological parameters differed according to breeding outcome (successful, failed, deferred). Correlations between post-breeding physiology and fCort, and links to future breeding decisions, were examined. In black-browed albatrosses, post-breeding physiology and fCort were not significantly correlated, but fCort independently predicted breeding decision the next year, which we interpret as a possible migratory carry-over effect. In grey-headed albatrosses, post-breeding triglyceride levels were negatively correlated with fCort, but only in females, which we interpret as a potential cost of reproduction. However, this potential cost did not carry-over to future breeding in the grey-headed albatrosses. None of the variables predicted future breeding decisions. We suggest that biennial breeding in the grey-headed albatrosses may have evolved as a strategy to buffer against the apparent susceptibility of females to negative physiological costs of reproduction. Future studies are needed to confirm this. DOI
178. Davis, ML; Elliott, JE; Williams, TD. (2017) The Glaucous-Winged Gull (Larus glaucescens) as an Indicator of Chemical Contaminants in the Canadian Pacific Marine Environment: Evidence from Stable Isotopes.Arch. Environ. Contam. Toxicol. 73: 247-255 The Glaucous-Winged Gull (Larus glaucescens) as an Indicator of Chemical Contaminants in the Canadian Pacific Marine Environment: Evidence from Stable Isotopes
The Glaucous-winged gull (Larus glaucescens) has been selected by Environment Canada as a marine indicator species for long-term monitoring of persistent contaminants in the Canadian Pacific. However, the indicator value of this species depends on its trophic level and proportion of marine prey in its diet. Eggs, used as the monitoring medium, are produced entirely from maternal resources and knowledge of adult diet before and during egg production is critical to interpreting contaminant levels. Due to a lack of recent and reliable dietary ecology work, we examined the diet of breeding Glaucous-winged gulls through carbon (delta C-13) and nitrogen (delta N-15) stable isotope analysis at three colonies on the Pacific coast. Near-shore marine prey, occupying a high trophic level (delta N-15), composed a predominant component of all Glaucous-winged gull diet. Adult diet composition from colonies in the Salish Sea was more varied than the west coast of Vancouver Island, reflecting the opportunistic foraging nature of this species in areas where the abundance of marine prey is known to fluctuate. Compared with incubating adults, pre-laying adults had a significantly lower trophic level that may reflect the need to consume marine invertebrates to acquire specific nutrients necessary for egg production. Interannual variation in both trophic level and prey source (delta C-13) in egg and chick tissues indicates the need to pair ongoing contaminant monitoring with stable isotope analysis. The predominantly marine diet and relatively high trophic level of this gull supports its use as an indicator of marine pollution on the Pacific coast. DOI
177. Eng, ML; Bishop, CA; Crump, D; Jones, SP; Williams, TD; Drouillard, KG; Elliott, JE. (2017) Catbirds are the New Chickens: High Sensitivity to a Dioxin-like Compound in a Wildlife Species.Environ. Sci. Technol. 51: 5252-5258 Catbirds are the New Chickens: High Sensitivity to a Dioxin-like Compound in a Wildlife Species
Dioxins and dioxin-like compounds (DLCs) are highly toxic and persistent global pollutants with extremely large differences in sensitivity across taxonomic groups. The chicken has long been considered uniquely sensitive to DLCs among avian species; but DLC toxicity in nondomesticated birds is largely untested, and the relevance of the chicken as an ecological model is uncertain. New approaches that use genotyping of the AHR1 ligand binding domain to screen for DLC sensitivity among avian species predicted that the gray catbird, a relevant wildlife species, is also highly sensitive. We tested this prediction using egg injections of a dioxin-like PCB (PCB-126) and found that the catbird is at least as sensitive as the chicken to DLCs, based on both embryotoxicity and mRNA induction of phase I metabolizing enzymes (CYP1A4/5). This study is the first to confirm that there are wildlife species as sensitive as the chicken and demonstrates how using predictive genotyping methods and targeted bioassays can focus toxicity assessments on ecologically relevant species. DOI
176. Eng, ML; Letcher, RJ; Williams, TD; Elliott, JE. (2017) In ovo tris(2-butoxyethyl) phosphate concentrations significantly decrease in late incubation after a single exposure via injection, with no evidence of effects on hatching success or latent effects on growth or reproduction in zebra finches.Environmental Toxicology and Chemistry 36: 83-88 In ovo tris(2-butoxyethyl) phosphate concentrations significantly decrease in late incubation after a single exposure via injection, with no evidence of effects on hatching success or latent effects on growth or reproduction in zebra finches
Organophosphate flame retardant; Avian toxicity; Developmental toxicity; Organophosphate; Flame retardant; Metabolism; Passerine
Zebra finch (Taeniopygia guttata) eggs were injected with the organophosphate triester flame retardant tris(2-butoxyethyl) phosphate (TBOEP) at 0g/g, 0.01g/g, 1g/g, 10g/g, or 50g/g egg. Subsets of high-dose eggs were collected throughout incubation to measure TBOEP, which started declining in late incubation and then decreased rapidly to 28% of injected concentration by hatching. The authors found no effects of TBOEP on survival, growth, or reproduction even at very high doses. Environ Toxicol Chem 2017;36:83-88. (c) 2016 SETAC DOI
175. Fowler, MA; Williams, TD. (2017) A Physiological Signature of the Cost of Reproduction Associated with Parental Care.Am. Nat. 190: 762-773 A Physiological Signature of the Cost of Reproduction Associated with Parental Care
physiological cost of reproduction; workload; parental care; oxygen-carrying capacity; oxidative stress; energy
Costs of reproduction are an integral and long-standing component of life-history theory, but we still know relatively little about the specific physiological mechanisms underlying these trade-offs. We experimentally manipulated workload during parental care in female European starlings (Sturnus vulgaris) using attachment of radios and/or wing clipping and assessed measures of workload, current breeding productivity, future fecundity, and survival (local return rate) in relation to treatment. Females with wing clipping and radio attachment paid a clear cost of reproduction compared with all other treatment groups: they had lower future fecundity and lower return rates despite having lower current breeding productivity. We then measured 13 physiological traits, including measures of aerobic/metabolic capacity, oxidative stress and muscle damage, intermediary metabolism and energy supply, and immune function. Our results show that the cost of reproduction in females with wing clipping and radio attachment was associated with lower oxygen-carrying capacity (lower hematocrit and hemoglobin levels), lower energy reserves (plasma nonesterified fatty acid and triglyceride levels), decreased immune function (lower haptoglobin levels), and elevated levels of oxidative stress (higher levels of dROMs [reactive oxygen metabolites] and lower levels of the endogenous antioxidant uric acid). Our study provides evidence that costs of reproduction involve a widespread decline in physiological function across multiple physiological systems consistent with long-standing ideas of cumulative wear and tear and allostatic load. DOI
174. Gibson, KF; Williams, TD. (2017) Intraclutch egg size variation is independent of ecological context among years in the European Starling Sturnus vulgaris.J. Ornithol. 158: 1099-1110 Intraclutch egg size variation is independent of ecological context among years in the European Starling Sturnus vulgaris
Individual variation; Early brood loss; Hatching asynchrony; Offspring quality; Adaptive strategy
Female birds can potentially utilise various mechanisms, such as intraclutch egg size variation (ICESV), to modulate offspring quality. If this represents an 'adaptive' strategy allowing females to adjust reproductive effort after laying of the first egg, as information on resources becomes more predictable later in the laying sequence, then we would predict that ICESV would vary with ecological context, e.g. in 'good' versus 'bad' years. Here, in European Starlings (Sturnus vulgaris), we tested specific predictions that (1) females would lay relatively small last laid eggs in 'poor' years (with early laying and below-average breeding productivity); and (2) that ICESV would be lower in good years (late laying, above-average productivity) so that late-hatched chicks would not be disadvantaged. At the individual level we predicted (3) that repeatability of ICESV would be low if females adjusted this in relation to the environment in different years; and (4) that within-individual variation in ICESV should correlate with the number, and timing, of loss of chicks. Mean ICESV averaged -1.9% (measured as last egg mass relative to mean egg mass), typical of other hole-nesting passerines. However, our results did not support any of our hypotheses: (1) although there was annual variation in ICESV, in all years egg mass decreased through the laying sequence; (2) annual variation in ICESV was not consistent with variation in phenology or breeding productivity among years; (3) marked individual variation in ICESV (last laid egg varied from -20 to +10% relative to mean egg mass within clutches) was repeatable, i.e. individual females did not adjust ICESV in subsequent breeding attempts; and (4) variation in the magnitude of ICESV, alone and combined with hatching asynchrony, did not predict early brood loss. Our study suggests that ICESV is a relatively inflexible component of an individual female's phenotype that might contribute to variation in individual quality. DOI
173. Gorman, KB; Talbot, SL; Sonsthagen, SA; Sage, GK; Gravely, MC; Fraser, WR; Williams, TD. (2017) Population genetic structure and gene flow of Adelie penguins (Pygoscelis adeliae) breeding throughout the western Antarctic Peninsula.Antarctic Science 29: 499-510 Population genetic structure and gene flow of Adelie penguins (Pygoscelis adeliae) breeding throughout the western Antarctic Peninsula
climate warming; microsatellite; mitochondrial DNA; population delineation; sea ice
Adelie penguins (Pygoscelis adeliae) are responding to ocean-climate variability throughout the marine ecosystem of the western Antarctic Peninsula (WAP) where some breeding colonies have declined by 80%. Nuclear and mitochondrial DNA (mtDNA) markers were used to understand historical population genetic structure and gene flow given relatively recent and continuing reductions in sea ice habitats and changes in numbers of breeding adults at colonies throughout the WAP. Genetic diversity, spatial genetic structure, genetic signatures of fluctuations in population demography and gene flow were assessed in four regional Adelie penguin colonies. The analyses indicated little genetic structure overall based on bi-parentally inherited microsatellite markers (F-ST = -0.006-0.004). No significant variance was observed in overall haplotype frequency (mtDNA Phi(ST) = 0.017 ;P = 0.112). Some comparisons with Charcot Island were significant, suggestive of female-biased philopatry. Estimates of gene flow based on a two-population coalescent model were asymmetrical from the species' regional core to its northern range. Breeding Adelie penguins of the WAP are a panmictic population and hold adequate genetic diversity and dispersal capacity to be resilient to environmental change. DOI
172. Griffith, SC; Crino, OL; Andrew, SC; Nomano, FY; Adkins-Regan, E; Alonso-Alvarez, C; Bailey, IE; Bittner, SS; Bolton, PE; Boner, W; Boogert, N; Boucaud, ICA; Briga, M; Buchanan, KL; Caspers, BA; Cichon, M; Clayton, DF; Deregnaucourt, S; Forstmeier, W; Guillette, LM; Hartley, IR; Healy, SD; Hill, DL; Holveck, MJ; Hurley, LL; Ihle, M; Krause, ET; Mainwaring, MC; Marasco, V; Mariette, MM; Martin-Wintle, MS; McCowan, LSC; McMahon, M; Monaghan, P; Nager, RG; Naguib, M; Nord, A; Potvin, DA; Prior, NH; Riebel, K; Romero-Haro, AA; Royle, NJ; Rutkowska, J; Schuett, W; Swaddle, JP; Tobler, M; Trompf, L; Varian-Ramos, CW; Vignal, C; Villain, AS; Williams, TD. (2017) Variation in Reproductive Success Across Captive Populations: Methodological Differences, Potential Biases and Opportunities.Ethology 123: 1-29 Variation in Reproductive Success Across Captive Populations: Methodological Differences, Potential Biases and Opportunities
Taeniopygia guttata; zebra finch; reproductive failure; captivity; domestication; husbandry; model species; captive breeding
Our understanding of fundamental organismal biology has been disproportionately influenced by studies of a relatively small number of model' species extensively studied in captivity. Laboratory populations of model species are commonly subject to a number of forms of past and current selection that may affect experimental outcomes. Here, we examine these processes and their outcomes in one of the most widely used vertebrate species in the laboratory - the zebra finch (Taeniopygia guttata). This important model species is used for research across a broad range of fields, partly due to the ease with which it can be bred in captivity. However despite this perceived amenability, we demonstrate extensive variation in the success with which different laboratories and studies bred their subjects, and overall only 64% of all females that were given the opportunity, bred successfully in the laboratory. We identify and review several environmental, husbandry, life-history and behavioural factors that potentially contribute to this variation. The variation in reproductive success across individuals could lead to biases in experimental outcomes and drive some of the heterogeneity in research outcomes across studies. The zebra finch remains an excellent captive animal system and our aim is to sharpen the insight that future studies of this species can provide, both to our understanding of this species and also with respect to the reproduction of captive animals more widely. We hope to improve systematic reporting methods and that further investigation of the issues we raise will lead both to advances in our fundamental understanding of avian reproduction as well as to improvements in future welfare and experimental efficiency. DOI
171. Killen, SS; Calsbeek, R; Williams, TD. (2017) The Ecology of Exercise: Mechanisms Underlying Individual Variation in Behavior, Activity, and Performance: An Introduction to Symposium.Integr. Comp. Biol. 57: 185-194 The Ecology of Exercise: Mechanisms Underlying Individual Variation in Behavior, Activity, and Performance: An Introduction to Symposium
Wild animals often engage in intense physical activity while performing tasks vital for their survival and reproduction associated with foraging, avoiding predators, fighting, providing parental care, and migrating. In this theme issue we consider how viewing these tasks as "exercise"-analogous to that performed by human athletes-may help provide insight into the mechanisms underlying individual variation in these types of behaviors and the importance of physical activity in an ecological context. In this article and throughout this issue, we focus on four key questions relevant to the study of behavioral ecology that may be addressed by studying wild animal behavior from the perspective of exercise physiology: (1) How hard do individual animals work in response to ecological (or evolutionary) demands?; (2) Do lab-based studies of activity provide good models for understanding activity in free-living animals and individual variation in traits?; (3) Can animals work too hard during "routine" activities?; and (4) Can paradigms of "exercise" and "training" be applied to free-living animals? Attempts to address these issues are currently being facilitated by rapid technological developments associated with physiological measurements and the remote tracking of wild animals, to provide mechanistic insights into the behavior of free-ranging animals at spatial and temporal scales that were previously impossible. We further suggest that viewing the behaviors of non-human animals in terms of the physical exercise performed will allow us to fully take advantage of these technological advances, draw from knowledge and conceptual frameworks already in use by human exercise physiologists, and identify key traits that constrain performance and generate variation in performance among individuals. It is our hope that, by highlighting mechanisms of behavior and performance, the articles in this issue will spur on further synergies between physiologists and ecologists, to take advantage of emerging cross-disciplinary perspectives and technologies. DOI
170. Yap, KN; Kim, OR; Harris, KC; Williams, TD. (2017) Physiological effects of increased foraging effort in a small passerine.Journal of Experimental Biology 220: 4282-4291 Physiological effects of increased foraging effort in a small passerine
Exercise physiology; Workload; Oxidative stress; Energetics; Body composition; Taeniopygia guttata
Foraging to obtain food, either for self-maintenance or at presumably elevated rates to provide for offspring, is thought to be an energetically demanding activity but one that is essential for fitness (higher reproductive success and survival). Nevertheless, the physiological mechanisms that allow some individuals to support higher foraging performance, and the mechanisms underlying costs of high workload, remain poorly understood. We experimentally manipulated foraging behaviour in zebra finches (Taeniopygia guttata) using the technique described by Koetsier and Verhulst (2011). Birds in the 'high foraging effort' (HF) group had to obtain food either while flying/hovering or by making repeated hops or jumps from the ground up to the feeder, behaviour typical of the extremely energetically expensive foraging mode observed in many free-living small passerines. HF birds made significantly more trips to the feeder per 10 min, whereas control birds spent more time (perched) at the feeder. Despite this marked change in foraging behaviour, we documented few short- or long-term effects of 'training' (3 days and 90 days of 'training', respectively) and some of these effects were sex specific. There were no effects of treatment on basal metabolic rate, haematocrit, haemoglobin or plasma glycerol, triglyceride and glucose levels, and masses of kidney, crop, large intestine, small intestine, gizzard and liver. HF females had higher masses of flight muscle, leg muscle, heart and lung compared with controls. In contrast, HF males had lower heart mass than controls and there were no differences for other organs. When both sexes were pooled, there were no effects of treatment on body composition. Finally, birds in the HF treatment group had higher levels of reactive oxygen metabolites (dROMs) and, consequently, although treatment did not affect total anti-oxidant capacity, birds in the HF treatment group had higher oxidative stress. DOI
169. Yap, KN; Serota, MW; Williams, TD. (2017) The Physiology of Exercise in Free-Living Vertebrates: What Can We Learn from Current Model Systems?Integr. Comp. Biol. 57: 195-206 The Physiology of Exercise in Free-Living Vertebrates: What Can We Learn from Current Model Systems?
Many behaviors crucial for survival and reproductive success in free-living animals, including migration, foraging, and escaping from predators, involve elevated levels of physical activity. However, although there has been considerable interest in the physiological and biomechanical mechanisms that underpin individual variation in exercise performance, to date, much work on the physiology of exercise has been conducted in laboratory settings that are often quite removed from the animal's ecology. Here we review current, laboratory-based model systems for exercise (wind or swim tunnels for migration studies in birds and fishes, manipulation of exercise associated with non-migratory activity in birds, locomotion in lizards, and wheel running in rodents) to identify common physiological markers of individual variation in exercise capacity and/or costs of increased activity. Secondly, we consider how physiological responses to exercise might be influenced by (1) the nature of the activity (i.e., voluntary or involuntary, intensity, and duration), and (2) resource acquisition and food availability, in the context of routine activities in free-living animals. Finally, we consider evidence that the physiological effects of experimentally-elevated activity directly affect components of fitness such as reproduction and survival. We suggest that developing more ecologically realistic laboratory systems, incorporating resource-acquisition, functional studies across multiple physiological systems, and a life-history framework, with reproduction and survival end-points, will help reveal the mechanisms underlying the consequences of exercise, and will complement studies in free-living animals taking advantage of new developments in wildlife-tracking. DOI
168. Yu, MS; Eng, ML; Williams, TD; Guigueno, MF; Elliott, JE. (2017) Assessment of neuroanatomical and behavioural effects of in ovo methylmercury exposure in zebra finches (Taeniopygia guttata).Neurotoxicology 59: 33-39 Assessment of neuroanatomical and behavioural effects of in ovo methylmercury exposure in zebra finches (Taeniopygia guttata)
Methylmercury; Passerines; In ovo exposure; Developmental neurotoxicity; Courtship behavior
Methylmercury (MeHg) readily crosses the blood brain barrier and is a known neuro-toxicant. MeHg accumulation in the brain causes histopathological alterations, neurobehavioral changes, and impairments to cognitive motor functions in mammalian models. However, in birds the neurotoxic effects of MeHg on the developing pre-hatching brain and consequent behavioral alterations in adult birds have not received much attention. Moreover, passerine birds are poorly represented in MeHg neurotoxicology studies in comparison to other avian orders. Hence in this study, we used the egg injection method to investigate the long term effects of in ovo MeHg exposure on brain histopathology and courtship behavior in a model songbird species, the zebra finch (Taeniopygia guttata). Egg treatment groups included: a low MeHg dose of 0.2 mu g Hg g(-1) egg, a high MeHg dose of 3.2 mu g Hg g(-1), egg, and a vehicle control (water). No adverse effects of in ovo MeHg treatment were detected on courtship song quality or on mating behavior in experimental males at sexually maturity which would suggest that observable neurobehavioral effects of MeHg exposure may depend on the timing of exposure during offspring development. However, neuroanatomical analysis indicated an increase in telericephalon volume with increased MeHg concentrations which may suggest a prolonged inflammatory response in this region of the brain. (C) 2017 Elsevier B.V. All rights reserved. DOI
167. Cornell, A; Williams, TD. (2016) Individual quality and double-brooding in a highly synchronous songbird population.Auk 133: 251-260 Individual quality and double-brooding in a highly synchronous songbird population
multiple brooding; breeding phenology; individual quality; laying date
Multiple brooding, the production of more than one set of offspring per breeding season, is a life-history trait that potentially doubles or triples fecundity, but the factors responsible for variation in the occurrence of multiple brooding within species remain poorly understood. We investigated the potential causes and consequences of double-brooding in the highly synchronously breeding European Starling (Sturnus vulgaris), for which we predicted that clutch initiation date would have little effect on double-brooding propensity compared with individual quality. Double-brooding effectively doubled annual fecundity in European Starlings (based on the annual number of chicks fledged), but on average only 38% of individual females had a second brood. Furthermore, 39% of females that initiated a second clutch experienced total failure of their second brood, and thus accrued no advantage in fecundity from their decision to double-brood. As we predicted, variation in the propensity for, and success of, double-brooding was independent of laying date, but also of other putative measures of individual quality (clutch size, egg mass, relative female age, and nestling provisioning rate). However, we found no evidence of a cost of double-brooding; females that double-brooded had significantly higher return rates and similar breeding productivity in the year after double-brooding compared with single-brooding females. Thus, a small proportion (similar to 20%) of 'high-quality' female European Starlings effectively double their potential breeding productivity through double-brooding without apparently paying a cost or experiencing any simple tradeoffs. DOI
166. Crossin, GT; Love, OP; Cooke, SJ; Williams, TD. (2016) Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context and reproductive state.Functional Ecology 30: 116-125 Glucocorticoid manipulations in free-living animals: considerations of dose delivery, life-history context and reproductive state
baseline levels; corticosterone; cortisol; fitness; glucocorticoids; implants
1. Experimental glucocorticoid (GC) manipulations can be useful for identifying the mechanisms that drive life-history and fitness variation in free-living animals, but predicting the effects of GC treatment can be complicated. Much of the uncertainty stems from the multifaceted role of GCs in organismal metabolism, and their variable influence with respect to life-history stage, ecological context, age, sex and individual variation. 2. Glucocorticoid hormones have been implicated in the regulation of parental care in many vertebrate taxa but in two seemingly contradictory ways, which sets up a potential GC-induced 'reproductive conflict'. Circulating GCs mediate adaptive physiological and behavioural responses to stressful events, and elevated levels can lead to trade offs between reproductive effort and survival (e.g. the current reproduction vs. survival hypothesis). The majority of studies examining the fitness effects of GC manipulations extend from this hypothesis. However, when animals are not stressed (likely most of the time) baseline GCs act as key metabolic regulators of daily energy balance, homoeostasis, osmoregulation and food acquisition, with pleiotropic effects on locomotor activity or foraging behaviour. Slight increases in circulating baseline levels can then have positive effects on reproductive effort (e.g. the 'cort' fitness/adaptation hypotheses), but comparatively few GC manipulation studies have targeted these small, non-stress induced increases. 3. We review studies of GC manipulations and examine the specific hypotheses used to predict the effects of manipulations in wild, breeding vertebrates. We argue that given the dichotomous function of GCs the current 'reproduction vs. survival' paradigm is unnecessarily restrictive and predicts only deleterious GC effects on fitness. Therefore, a broader set of hypotheses should be considered when testing the fitness effects of GC manipulations. 4. When framing experimental manipulation studies, we urge researchers to consider three key points: life-history context (e.g. long vs. short lived, semelparous vs. iteroparous, etc.), ecological context and dose delivery. DOI
165. Fronstin, RB; Christians, JK; Williams, TD. (2016) Experimental reduction of haematocrit affects reproductive performance in European starlings.Functional Ecology 30: 398-409 Experimental reduction of haematocrit affects reproductive performance in European starlings
cost of reproduction; haemoglobin; interindividual variation; reproductive anaemia; reproductive success
1. Given the function of haemoglobin and observed increases in haematocrit during periods of increased energetic demands, haematocrit and haemoglobin are assumed to be related to aerobic capacity. Reductions in haematocrit and haemoglobin during reproduction are similar in magnitude to increases associated with aerobically demanding activities, and therefore, we sought to investigate whether these reductions in haematology have consequences for reproductive performance. 2. We analysed associations between natural variation in haematology in free-living European starlings (Sturnus vulgaris) and reproductive performance. To test whether transient reductions in haematology during different stages of reproduction (egg production and late incubation/early chick rearing) affected measures of reproductive performance, we also manipulated haematology using phenylhydrazine (PHZ), which lyses red blood cells. 3. To investigate effects of reductions of haematology during egg-laying, we treated females with PHZ or saline (control) upon completion of their unmanipulated first clutch and removed eggs to induce the production and rearing of a replacement clutch. To investigate effects of reductions of haematology during chick rearing, we treated females during incubation of the unmanipulated first clutch and then monitored the subsequent hatching and rearing of the clutch. 4. Individuals with higher haematocrit and haemoglobin initiated nesting earlier. Furthermore, higher haemoglobin levels during incubation were associated with a greater number of chicks fledged. 5. PHZ treatment prior to egg production resulted in a significant delay in the laying of replacement clutches, but had no effect on provisioning rate or the size or number of chicks fledged. PHZ treatment during incubation and early chick rearing resulted in decreased hatchling mass in all years and a decrease in the size and number of fledglings in one of 2years. The year that the effect of PHZ was observed appeared to be a particularly difficult year, as hatchling mass, brood size at hatching and at fledging were low among control females compared to other years. 6. Our results suggest that a reduction in haematology during reproduction can be functionally significant, but that these costs are context-dependent. DOI
164. Hennin, HL; Bety, J; Legagneux, P; Gilchrist, HG; Williams, TD; Love, OP. (2016) Energetic Physiology Mediates Individual Optimization of Breeding Phenology in a Migratory Arctic Seabird.American Naturalist 188: 434-445 Energetic Physiology Mediates Individual Optimization of Breeding Phenology in a Migratory Arctic Seabird
individual optimization; breeding phenology; fattening rate; energetic management; triglycerides; glucocorticoids
The influence of variation in individual state on key reproductive decisions impacting fitness is well appreciated in evolutionary ecology. Rowe et al. (1994) developed a condition-dependent individual optimization model predicting that three key factors impact the ability of migratory female birds to individually optimize breeding phenology to maximize fitness in seasonal environments: arrival condition, arrival date, and ability to gain in condition on the breeding grounds. While empirical studies have confirmed that greater arrival body mass and earlier arrival dates result in earlier laying, no study has assessed whether individual variation in energetic management of condition gain effects this key fitness-related decision. Using an 8-year data set from over 350 prebreeding female Arctic common eiders (Somateria mollissima), we tested this component of the model by examining whether individual variation in two physiological traits influencing energetic management (plasma triglycerides: physiological fattening rate; baseline corticosterone: energetic demand) predicted individual variation in breeding phenology after controlling for arrival date and body mass. As predicted by the optimization model, individuals with higher fattening rates and lower energetic demand had the earliest breeding phenology (shortest delays between arrival and laying; earliest laying dates). Our results are the first to empirically determine that individual flexibility in prebreeding energetic management influences key fitness-related reproductive decisions, suggesting that individuals have the capacity to optimally manage reproductive investment. DOI
163. Legagneux, P; Hennin, HL; Gilchrist, HG; Williams, TD; Love, OP; Bety, J. (2016) Unpredictable perturbation reduces breeding propensity regardless of pre-laying reproductive readiness in a partial capital breeder.Journal of Avian Biology 47: 880-886 Unpredictable perturbation reduces breeding propensity regardless of pre-laying reproductive readiness in a partial capital breeder
Theoretically, individuals of migratory species should optimize reproductive investment based on a combination of timing of and body condition at arrival on the breeding grounds. A minimum threshold body mass is required to initiate reproduction, and the timing of reaching this threshold is critical because of the trade-off between delaying breeding to gain in condition against the declining value of offspring with later reproductive timing. Long-lived species have the flexibility within their life history to skip reproduction in a given year if they are unable to achieve this theoretical mass threshold. Although the decision to breed or not is an important parameter influencing population dynamics, the mechanisms underlying this decision are poorly understood. Here, we mimicked an unpredictable environmental perturbation that induced a reduction in body mass of Arctic pre-breeding (before the laying period) female common eiders Somateria mollissima; a long-lived migratory seaduck, while controlling for individual variation in the pre-laying physiological reproductive readiness via vitellogenin (VTG) - a yolk-targeted lipoprotein. Our aim was to causally determine the interaction between body condition and pre-laying reproductive readiness (VTG) on breeding propensity by experimentally reducing body mass in treatment females. We first demonstrated that arrival body condition was a key driver of breeding propensity. Secondly, we found that treatment and VTG levels interacted to influence breeding propensity, indicating that our experimental manipulation, mimicking an unpredictable food shortage, reduced breeding propensity, regardless of the degree of pre-laying physiological reproductive readiness (i.e. timing of ovarian follicles recruitment). Our experiment demonstrates that momentary environmental perturbations during the pre-breeding period can strongly affect the decision to breed, a key parameter driving population dynamics. DOI
162. Reers, AR; Eng, ML; Williams, TD; Elliott, JE; Cox, ME; Beischlag, TV. (2016) The Flame-Retardant Tris(1,3-dichloro-2-propyl) Phosphate Represses Androgen Signaling in Human Prostate Cancer Cell Lines.Journal of Biochemical and Molecular Toxicology 30: 249-257 The Flame-Retardant Tris(1,3-dichloro-2-propyl) Phosphate Represses Androgen Signaling in Human Prostate Cancer Cell Lines
Organophosphate Flame Retardants; Endocrine Disruptor; Androgen Receptor; Estrogen Receptor; Aryl Hydrocarbon Receptor; LNCaP
The effects of six organophosphate flame retardants (OPFRs) tris(2-butoxyethyl) phosphate, tris(2-chloroethyl) phosphate, tris(1-chloro-2-propyl) phosphate, tris(methylphenyl) phosphate, tris(1,3-dichloro-2-propyl) phosphate (TDCIPP), and triethyl phosphate on the activities of androgen receptor (AR), estrogen receptor (ER), and aryl hydrocarbon receptor (AhR) were assessed in human prostate and endometrial cancer cells. OPFRs had no effect on ER or AhR target gene activation in ECC-1 cells. The effect of TDCIPP on mRNA and protein accumulation of AR target genes was examined further. AR-inducible gene and protein expression were significantly altered by TDCIPP exposure and repressed PSA levels in conditioned media of prostate cancer cells. We demonstrated that TDCIPP has no affinity for the AR ligand binding domain (AR-LBD) and exerts its antiandrogenic effects in a noncompetitive fashion. Thus, the clinical relevance of TDCIPP exposure on prostate cancer detection and progression to a therapeutically refractile state ought to be investigated further. (C) 2015 Wiley Periodicals, Inc. DOI
161. Wong, LIL; Reers, AR; Currier, HA; Williams, TD; Cox, ME; Elliott, JE; Beischlag, TV. (2016) The Effects of the Organic Flame-Retardant 1,2-Dibromo-4-(1,2-dibromoethyl) Cyclohexane (TBECH) on Androgen Signaling in Human Prostate Cancer Cell Lines.Journal of Biochemical and Molecular Toxicology 30: 239-242 The Effects of the Organic Flame-Retardant 1,2-Dibromo-4-(1,2-dibromoethyl) Cyclohexane (TBECH) on Androgen Signaling in Human Prostate Cancer Cell Lines
Organic Flame Retardant; Endocrine Disruptor; Androgen Receptor; LNCaP
The effects of the organic flame retardant 1,2-Dibromo-4-(1,2-dibromoethyl) cyclohexane (TBECH) on androgen receptor target gene expression were examined in the human LNCaP prostate cancer cell line. While gamma-/delta-TBECH alone led to a significant increase in prostate-specific antigen (PSA) mRNA accumulation, both the alpha-/-TBECH and gamma-/delta-TBECH mixtures repressed androgen-inducible PSA mRNA and protein accumulation in human LNCaP cells. Thus, we hypothesize that isomeric mixtures of TBECH may act as partial agonists of the androgen receptor. (C) 2015 Wiley Periodicals, Inc. DOI
160. Yu, MS; Eng, ML; Williams, TD; Basu, N; Elliottz, JE. (2016) ACUTE EMBRYOTOXIC EFFECTS BUT NO LONG-TERM REPRODUCTIVE EFFECTS OF IN OVO METHYLMERCURY EXPOSURE IN ZEBRA FINCHES (TAENIOPYGIA GUTTATA).Environmental Toxicology and Chemistry 35: 1534-1540 ACUTE EMBRYOTOXIC EFFECTS BUT NO LONG-TERM REPRODUCTIVE EFFECTS OF IN OVO METHYLMERCURY EXPOSURE IN ZEBRA FINCHES (TAENIOPYGIA GUTTATA)
Methylmercury; Passerine; In ovo exposure; Hatching success; Reproduction
Mercury bioaccumulates in terrestrial ecosystems as methylmercury (MeHg), yet little is known about its effects on terrestrial organisms, including songbirds. The authors used a model songbird species, the zebra finch (Taeniopygia guttata), to assess short-term embryotoxic effects of in ovo MeHg exposure on hatching success and posthatching growth and nestling survival, as well as longer-term effects on mating behavior and reproduction. Egg treatment groups included a low-MeHg dose of 0.2 mg Hg g(-1) egg (n = 36), a high-MeHg dose of 3.2 mg Hg g(-1) egg (n = 49), and a control (n = 34). Doses were dissolved in nanopure filtered water and injected into the albumen on the day eggs showed signs of viability (3 d incubation). In ovo exposure to MeHg significantly reduced hatching success (53% in the high-MeHg dose group vs 94% in vehicle controls). Among hatched chicks, however, no effects of MeHg on growth, hematological variables, or nestling survival were detected. While the in ovo injection method resulted in a dose-dependent pattern of MeHg concentrations in blood of surviving chicks at 15 d and 30 d posthatching, there was evidence of rapid excretion of MeHg with nestling age during that growth period. At reproductive maturity (90 d of age), no long-term effects of in ovo exposure to MeHg on female mating behavior, reproductive effort (egg or clutch size), or growth and survivorship of offspring were observed. (C) 2015 SETAC DOI
159. Crossin, GT; Takahashi, A; Sakamoto, KQ; Trathan, PN; Williams, TD. (2015) Habitat selection by foraging macaroni penguins correlates with hematocrit, an index of aerobic condition.Marine Ecology Progress Series 530: 163-176 Habitat selection by foraging macaroni penguins correlates with hematocrit, an index of aerobic condition
Biologging; Time-depth recorders; GPS; Telemetry; Parental care; Eudyptes; Ocean temperature
Reproductive investment during the chick-rearing period is an important contributor to lifetime fitness. Key to chick-rearing is the success of parental foraging, as food deliveries affect chick growth and survival up until fledging. For seabirds, oceanographic conditions including factors such as sea surface temperature are known to influence foraging decisions, but few studies have examined the physiological variables that might affect those decisions. We used global positioning systems (GPS), time-depth recorders (TDR), and physiological sampling techniques to explore links between ocean temperature, diving behavior, and foraging success in chick-rearing female macaroni penguins Eudyptes chrysolophus. We then explored correlations between these foraging variables and measures of individual physiological condition, specifically aerobic capacity (hematocrit) and metabolic state (corticosterone). In GPS-tracked penguins, 2 principal for aging tactics were observed: penguins made deep dives in cool, near-shore areas surrounding the breeding colony at Bird Island, South Georgia, or they traveled farther to dive shallower in warmer shelf-break areas. TDR-equipped penguins showed similar patterns. Blood sampling of TDR penguins at the onset of trips revealed strong positive correlations between hematocrit and the mean duration of foraging trips, the ocean temperature experienced during these trips, and the relative efficiency of foraging activity in terms of the number of foraging behaviors recorded per dive. These results suggest that aerobic capacity might be an important determinant of for aging trip range, as well as workload. Corticosterone was unrelated to diving behavior, which counters previous studies examining the effects of experimental increases of this hormone on foraging behavior, and we discuss reasons for this disparity. DOI
158. Currier, HA; Letcher, RJ; Williams, TD; Elliott, JE. (2015) Effects of the Bioaccumulative Polybrominated Diphenyl Ether Flame Retardant Congener BDE-47 on Growth, Development, and Reproductive Success in Zebra Finches.Bulletin of Environmental Contamination and Toxicology 94: 140-145 Effects of the Bioaccumulative Polybrominated Diphenyl Ether Flame Retardant Congener BDE-47 on Growth, Development, and Reproductive Success in Zebra Finches
Zebra finches; Oral dosing; Intergenerational; Breeding success; Polybrominated diphenyl ethers; BDE-47
This study investigated the effects of the polybrominated diphenyl ether congener, 2,2',4,4'-tetrabromodiphenyl ether (BDE-47) on the growth and development, and subsequent breeding success of exposed zebra finches (Taeniopygia guttata). Using oral dosing procedures and treatments adjusted by weight, we treated newly hatched chicks daily for the first 20-days-post-hatch (dph) with varying treatments of BDE-47 (0, 5, 50, and 500 ng/g bw/day). Weight and tarsal measurements were monitored from hatch to 90 dph, but no differences were observed between treatment groups at any age. Treated females that reached sexual maturity were mated with untreated males; however, again no treatment effects were observed on breeding success. Analysis of tissue samples at 21 dph did indicate that debromination of BDE-47 had occurred resulting in BDE-28 and BDE-17 metabolites. DOI PubMed
157. Fowler, MA; Williams, TD. (2015) Individual variation in parental workload and breeding productivity in female European starlings: is the effort worth it?Ecology and Evolution 5: 3585-3599 Individual variation in parental workload and breeding productivity in female European starlings: is the effort worth it?
Female parental care; individual variation; provisioning; reproductive success; workload
We analyzed individual variation in work load (nest visit rate) during chick-rearing, and the consequences of this variation in terms of breeding productivity, in a highly synchronous breeder, the European starling (Sturnus vulgaris) focusing on female birds. There was marked (10- to 16-fold) variation in total, female and male nest visit rates, among individuals, but individual variation in female nest visit rate was independent of environment (rainfall, temperature) and metrics of individual quality (laying date, clutch size, amount of male provisioning help), and was only weakly associated with chick demand (i.e., day 6 brood size). Female nest visit rate was independent of date and experimentally delayed birds provisioned at the same rate as peak-nesting birds; supporting a lack of effect of date per se. Brood size at fledging was positively but weakly related to total nest visit rate (male+female), with >fivefold variation in nest visit rate for any given brood size, and in females brood size at fledging and chick mass at fledging were independent of female nest visit rate, that is, individual variation in workload was not associated with higher productivity. Nevertheless, nest visit rate in females was repeatable among consecutive days (6-8 posthatching), and between peak (first) and second broods, but not among years. Our data suggest that individual females behave as if committed to a certain level of parental care at the outset of their annual breeding attempt, but this varies among years, that is, behavior is not fixed throughout an individual's life but represents an annually variable decision. We suggest females are making predictable decisions about their workload during provisioning that maximizes their overall fitness based on an integration of information on their current environment (although these cues currently remain unidentified). DOI
156. Perfito, N; Guardado, D; Williams, TD; Bentley, GE. (2015) Social Cues Regulate Reciprocal Switching of Hypothalamic Dio2/Dio3 and the Transition Into Final Follicle Maturation in European Starlings (Sturnus vulgaris).Endocrinology 156: 694-706 Social Cues Regulate Reciprocal Switching of Hypothalamic Dio2/Dio3 and the Transition Into Final Follicle Maturation in European Starlings (Sturnus vulgaris)
With final maturation of ovarian follicles, birds are committed to a major energetic investment: egg laying. Follicles develop in a 2-step process: 1) initial development of regressed follicles stimulated by long days and 2) yolk incorporation into hierarchical follicles, ovulation, and oviposition. We know little about how females transduce environmental cues into neuroendocrine signals regulating the second step. The present study measures gene expression in tissues within the hypothalamo- pituitary-gonadal axis. Females were housed in seminatural enclosures experiencing natural changes in photoperiod and environmental cues (eg, temperature, rainfall, etc), without males or with constant access to males (January to April). By April, females with males had begun to lay eggs, whereas those without males had not. In a second study, females without males for 3.5 months were then given access to males for 7 days. Restricting male access completely inhibited final follicle maturation, whereas 7-day male access stimulated full vitellogenesis and follicle maturation. Few gene expression changes were attributable to constant male access (January to March), but naive females given 7-day male access had increased type 2 deiodinase (DIO2) and decreased DIO3 synthesis in the hypothalamus, potentially influencing local thyroid hormone metabolism, increased expression of LH receptor and aromatase in follicles and vitellogenin in liver. Our data suggest that initial follicle development may be more heavily influenced by photoperiod, but the second step (final maturation) is sensitive to other cues such as social interactions. This is the first demonstration of a social effect on the Dio2/Dio3 system, previously thought only responsive to photoperiod cues. DOI PubMed
155. Ryan, CP; Dawson, A; Sharp, PJ; Williams, TD. (2015) Uncoupling clutch size, prolactin, and luteinizing hormone using experimental egg removal.General and Comparative Endocrinology 213: 1-8 Uncoupling clutch size, prolactin, and luteinizing hormone using experimental egg removal
Clutch size; Prolactin; Luteinizing hormone; Avian reproduction; Egg removal
Clutch size is a key avian fitness and life history trait. A physiological model for clutch size determination (CSD), involving an anti-gonadal effect of prolactin (PRL) via suppression of luteinizing hormone (LH), was proposed over 20 years ago, but has received scant experimental attention since. The few studies looking at a PRL-based mechanistic hypothesis for CSD have been equivocal, but recent experiments utilizing a pharmacological agent to manipulate PRL in the zebra finch (Taeniopygia guttata) found no support for a role of this hormone in clutch size determination. Here, we take a complementary approach by manipulating clutch size through egg removal, examining co-variation in PRL and LH between two breeding attempts, as well as through experimentally-extended laying. Clutch size increased for egg removal females, but not controls, but this was not correlated with changes in PRL. or LH. There were also no differences in PRL between egg removal females and controls, nor did PRL levels during early, mid- or late-laying of supra-normal clutches predict clutch size. By uncoupling PRL, LH and clutch size in our study, several key predictions of the PRL-based mechanistic model for CSD were not supported. However, a positive correlation between PRL levels late in laying and days relative to the last egg (clutch completion) provides an alternative explanation for the equivocal results surrounding the conventional PRL-based physiological model for CSD. We suggest that females coordinate PRL-mediated incubation onset with clutch completion to minimize hatching asynchrony and sibling hierarchy, a behavior that is amplified in females laying larger clutches. (C) 2015 Elsevier Inc. All rights reserved. DOI PubMed
154. Steenweg, RJ; Hennin, HL; Bety, J; Gilchrist, HG; Williams, TD; Crossin, GT; Love, OP. (2015) Sources of diel variation in energetic physiology in an Arctic-breeding, diving seaduck.General and Comparative Endocrinology 216: 39-45 Sources of diel variation in energetic physiology in an Arctic-breeding, diving seaduck
Corticosterone; Triglyceride; Energetic physiology; Diel rhythm; Arctic; Sea duck
Diel variation in baseline glucocorticoid (GC) secretion influences energetics and foraging behaviors. In temperate breeding, diurnal vertebrates, studies have shown that daily patterns of baseline GC secretion are influenced by environmental photoperiod, with baseline GCs peaking prior to sunrise to stimulate waking and foraging behaviors. Measures of physiological energy acquisition are also expected to peak in response to foraging activity, but their relationship to GC levels have not been well studied. In contrast to temperate breeding species, virtually nothing is known about diel GC and energetic metabolite secretion in Arctic breeding species, which experience almost constant photoperiods in spring and summer. Using a ten-year dataset, we examined the daily, 24-h pattern of baseline corticosterone (CORT) and triglyceride (TRIG) secretion in approximately 800 female pre-breeding Arctic-nesting common eiders (Somateria mollissima). We related these traits to environmental photoperiod and to tidal cycle. In contrast to temperate breeding species, we found that that neither time of day nor tidal trend predicted diel variation in CORT or TRIG secretion in Arctic-breeding eiders. Given the narrow window of opportunity for breeding in polar regions, we suggest that eiders must decouple their daily foraging activity from light and tidal cycles if they are to accrue sufficient energy for successful breeding. As CORT is known to influence foraging behavior, the absence of a distinct diel pattern of CORT secretion may therefore be an adaptation to optimize reproductive investment and likelihood for success in some polar-breeding species. (C) 2015 Elsevier Inc. All rights reserved. DOI
153. Webster, KH; Harr, KE; Bennett, DC; Williams, TD; Cheng, KM; Maisonneuve, F; Elliott, JE. (2015) Assessment of toxicity and coagulopathy of brodifacoum in Japanese quail and testing in wild owls.Ecotoxicology 24: 1087-1101 Assessment of toxicity and coagulopathy of brodifacoum in Japanese quail and testing in wild owls
Brodifacoum; Rodenticide; Prothrombin time; Japanese quail; Biomarker; Barn owl
Based on detection of hepatic residues, scavenging and predatory non-target raptors are widely exposed to second generation anticoagulant rodenticides (SGARs). A small proportion, generally < 10 %, of tested birds are diagnosed as acutely poisoned. Little is known, however, of sub-lethal effects of SGARs, such as interaction of clotting capacity with traumatic injury. Assessment of coagulation function of birds submitted live to wildlife rehabilitators or veterinarians may provide a means of establishing the proportion of animals suffering sub-lethal coagulopathies, as well as identifying individuals requiring treatment. As a first step in exploring the potential of this approach, we dosed Japanese quail (Coturnix japonica) with the SGAR, brodifacoum, at 0, 0.8, 1.4, 1.9, and 2.5 mg/kg and sampled birds at 1, 3, 5 and 7 days post-dosing. Prothrombin time (PT), which measures the extrinsic coagulation pathway, was significantly prolonged in 98 % of brodifacoum-exposed quail in a dose- and time-dependent manner. 50-fold prolongation of PT occurred at higher brodifacoum dosages and correlated to hemorrhage found at necropsy. Activated clotting time (ACT), a measure of the intrinsic pathway also increased with dose and time. Hemoglobin (Hb) and hematocrit (Hct) decreased dose- and time-dependently at doses a parts per thousand yen1.4 mg/kg with no significant change at 0.8 mg/kg. Reference intervals for PT (10.0-16.2 s), ACT (30-180 s), Hb (9.6-18.4 g/dl), and Hct (34-55 %) were established in Japanese quail. Species-specific reference intervals are required as barn owl PT (17-29 s) and quail PT were different. The proportion of brodifacoum-exposed quail with hemorrhage was not correlated with liver residues, but was correlated with PT, suggesting that this assay is a useful indicator of avian anticoagulant rodenticide exposure. PTs measured in free-living barn owls sampled between April 2009 and August 2010 in the lower Fraser Valley of BC do not suggest significant exposure to SGARs. DOI
152.Williams, TD; Bourgeon, S; Cornell, A; Ferguson, L; Fowler, M; Fronstin, RB; Love, OP. (2015) Mid-winter temperatures, not spring temperatures, predict breeding phenology in the European starling Sturnus vulgaris.Royal Society Open Science 2 Mid-winter temperatures, not spring temperatures, predict breeding phenology in the European starling Sturnus vulgaris
temperature; breeding phenology; egg-laying date; clutch size; tipulids
In many species, empirical data suggest that temperatures less than 1 month before breeding strongly influence laying date, consistent with predictions that short lag times between cue and response are more reliable, decreasing the chance of mismatch with prey. Here we show in European starlings (Sturnus vulgaris) that mid-winter temperature ca 50-90 days before laying (8 January-22 February) strongly (r(2) = 0.89) predicts annual variation in laying date. Mid-winter temperature also correlated highly with relative clutch size: birds laid later, but laid larger clutches, in years when mid-winter temperatures were lower. Despite a high degree of breeding synchrony (mean laying date 5-13 April = +/- 4 days; 80% of nests laid within 4.8 days within year), European starlings show strong date-dependent variation in clutch size and productivity, but this appears to be mediated by a different temporal mechanism for integration of supplemental cue (temperature) information. We suggest the relationship between mid-winter temperature and breeding phenology might be indirect with both components correlating with a third factor: temperature-dependent development of the starling's insect (tipulid) prey. Mid-winter temperatures might set the trajectory of growth and final biomass of tipulid larvae, with this temperature cue providing starlings with information on breeding season prey availability (though exactly how remains unknown). DOI
151.Williams, TD; Fowler, MA. (2015) Individual variation in workload during parental care: can we detect a physiological signature of quality or cost of reproduction?Journal of Ornithology 156: S441-S451 Individual variation in workload during parental care: can we detect a physiological signature of quality or cost of reproduction?
Parental care; Exercise physiology; Workload; Sturnus vulgaris; Cost of reproduction; Physiological costs
How hard do birds work during parental care, chick rearing, or provisioning of their nestlings? And if birds do work hard, can we detect a physiological signature of individual variation in workload ability (perhaps related to 'quality') or costs associated with high workload? Here, we provide a broad conceptual perspective on these questions. Life-history theory predicts (or requires) that (1) parental care is hard work, (2) individuals that invest more in parental care benefit in terms of rearing more, larger, fitter offspring, but that (3) increased investment in parental care comes at a cost: decreased future fecundity and/or survival. However, we start by highlighting studies that are inconsistent with this conventional view, e.g., (1) females often do not pay a survival cost of increased workload (though males do), (2) some (high quality?) individuals appear to maximise numerous life-history traits, and (3) workload during parental care often does not predict productivity. We suggest that an "exercise physiology" perspective on parental care might be informative, but highlight the fact that existing models of exercise often involve conditions very different from that free-living animals experience while foraging (e.g., using forced exercise) and are often divorced from the critical relationship in free-living animals between exercise and acquisition of resources. We briefly review studies looking at physiological effects of workload during parental care in freeliving birds, but again highlight our surprising lack of knowledge in this area especially where experimental manipulation of workload is coupled with comprehensive, physiological analysis. Finally, we make three recommendations for how can we advance the study of physiology of parental care in chick-rearing birds: (1) experimental manipulation of workload, (2) obtaining better measures of workload, for large numbers of known-individuals, and (3) better assessment of physiology of individual quality, and identification of specific metrics of workload-induced 'wear and tear'. DOI
150. Eng, ML; Elliott, JE; Jones, SP; Williams, TD; Drouillard, KG; Kennedy, SW. (2014) AMINO ACID SEQUENCE OF THE AHR1 LIGAND-BINDING DOMAIN PREDICTS AVIAN SENSITIVITY TO DIOXIN LIKE COMPOUNDS: IN VIVO VERIFICATION IN EUROPEAN STARLINGS.Environmental Toxicology and Chemistry 33: 2753-2758 AMINO ACID SEQUENCE OF THE AHR1 LIGAND-BINDING DOMAIN PREDICTS AVIAN SENSITIVITY TO DIOXIN LIKE COMPOUNDS: IN VIVO VERIFICATION IN EUROPEAN STARLINGS
Dioxin-like compounds; Polychlorinated biphenyl; Aryl hydrocarbon receptor; Embryotoxicity; Birds
Research has demonstrated that the sensitivity of avian species to the embyrotoxic effects of dioxin-like compounds can be predicted by the amino acid identities at two key sites within the ligand-binding domain of the aryl hydrocarbon receptor 1 (AhR1). The domestic chicken (Gallus gallus domesticus) has been established as a highly sensitive species to the toxic effects of dioxin-like compounds. Results from genotyping and in vitro assays predict that the European starling (Sturnus vulgaris) is also highly sensitive to dioxin-like compound toxicity. The objective of the present study was to test that prediction in vivo. To do this, we used egg injections in field nesting starlings with 3,3,4,4,5-pentachlorobiphenyl (PCB-126), a dioxin-like polychlorinated biphenyl. Eggs were dosed with either the vehicle control or 1 of 5 doses (1.4, 7.1, 15.9, 32.1, and 52.9ng PCB-126/g egg). A dose-dependent increase in embryo mortality occurred, and the median lethal dose (LD50; 95% confidence interval [CI]) was 5.61 (2.33-9.08) ng/g. Hepatic CYP1A4/5 messenger RNA (mRNA) expression in hatchlings also increased in a dose-dependent manner, with CYP1A4 being more induced than CYP1A5. No effect of dose on morphological measures was seen, and we did not observe any overt malformations. These results indicate that, other than the chicken, the European starling is the most sensitive species to the effects of PCB-126 on avian embryo mortality reported to date, which supports the prediction of relative sensitivity to dioxin-like compounds based on amino acid sequence of the AhR1. Environ Toxicol Chem 2014;33:2753-2758. (c) 2014 SETAC DOI PubMed
149. Eng, ML; Elliott, JE; Williams, TD. (2014) An assessment of the developmental toxicity of BDE-99 in the European starling using an integrated laboratory and field approach.Ecotoxicology 23: 1505-1516 An assessment of the developmental toxicity of BDE-99 in the European starling using an integrated laboratory and field approach
PBDEs; Photoperiod manipulations; Thyroid hormones; Avian toxicology; Songbird; European starling
Developmental exposure of wildlife to anthropogenic contaminants can have long-term effects that are difficult to assess in field monitoring studies, and may not be evident in laboratory studies that lack ecological components. The objective of this study was to assess the long-term effects of early exposure to contaminants under ecological conditions in a model passerine species, the European starling (Sturnus vulgaris). We selected 2,2',4,4',5-pentabromodiphenyl ether (BDE-99) as a representative contaminant, as it is one of the major constituents of the commercial penta-BDE flame retardant mixture, and has been reported in avian egg and tissue samples worldwide. We developed a novel approach to assess the developmental toxicity of BDE-99 in starlings by combining aspects of laboratory and field studies. We dosed free-living nestlings living in natural broods in the field with environmentally relevant concentrations of BDE-99 (0-173.8 ng/g bw/day) for the duration of the nesting cycle. To simulate monitoring of long-term effects we brought birds into captivity just prior to fledging and used photoperiod manipulations to induce reproductive development. We assessed a range of physiological and development measures such as hematocrit, oxidative stress, thyroid hormones, neuroanatomy, growth, molt rate, bill color, and testes development. We found some evidence of thyroid hormone disruption, but there were no effects on any other measures of physiology or development. The European starling could serve as a valuable model species for assessing early exposure and long-term effects of anthropogenic contaminants in terrestrial wildlife using this combined field/laboratory approach. DOI PubMed
148. Eng, ML; Williams, TD; Letcher, RJ; Elliott, JE. (2014) Assessment of concentrations and effects of organohalogen contaminants in a terrestrial passerine, the European starling.Science of the Total Environment 473: 589-596 Assessment of concentrations and effects of organohalogen contaminants in a terrestrial passerine, the European starling
Polybrominated diphenyl ethers; Polychlorinated biphenyls; Organochlorine pesticides; Passerine eggs; Reproductive success; Physiology
European starlings (Sturnus vulgar(s) are a valuable model species for the assessment of concentrations and effects of environmental contaminants in terrestrial birds. Polybrominated diphenyl ethers (PBDEs) are found in birds throughout the world, but relatively little is known of their concentrations or effects in free-living terrestrial passerines. We used a nest box population of European starlings to 1) measure the variation in egg concentrations of persistent organohalogen contaminants at an agricultural site, and 2) assess whether individual variation in PBDE concentrations in eggs was related to reproductive parameters, as well as maternal or nestling characteristics including body condition, thyroid hormones, oxidative stress, and hematocrit. As PBDEs were the main contaminant class of interest, we only assessed a subset of eggs for other organohalogen contaminants to establish background concentrations. Exposure to organohalogen contaminants was extremely variable over this relatively small study area. Geometric mean wet weight concentrations (range in brackets) of the major contaminants were 36.5 (12-174) ng/g Sigma DDT (n = 6 eggs) and 10.9 (2-307) ng/g Sigma PBDEs (n = 14). Sigma PCBs at 3.58 (1.5-6.4) ng/g (n = 6) were lower and less variable. There were low levels of other organochlorine (0C) pesticides such as dieldrin (2.02 ng/g), chlordanes (1.11 ng/g) and chlorobenzenes (0.23 ng/g). The only form of DDT detected was p,p'-DDE. The congener profiles of PBDEs and PCBs reflect those of industrial mixtures (i.e. DE-71, Aroclors 1254, 1260 and 1262). For all of the contaminant classes, concentrations detected in eggs at our study site were below levels previously reported to cause effects. Due to small sample sizes, we did not assess the relationship between Sigma PCBs or Sigma OCs and adult or chick condition. We observed no correlative relationships between individual variation in PBDE concentrations in starling eggs and reproductive success, maternal condition, or nestling condition in the corresponding nests. (C) 2014 Elsevier B.V. All rights reserved. DOI
147. Gorman, KB; Williams, TD; Fraser, WR. (2014) Ecological Sexual Dimorphism and Environmental Variability within a Community of Antarctic Penguins (Genus Pygoscelis).PLOS One 9 Ecological Sexual Dimorphism and Environmental Variability within a Community of Antarctic Penguins (Genus Pygoscelis)
Background: Sexual segregation in vertebrate foraging niche is often associated with sexual size dimorphism (SSD), i.e., ecological sexual dimorphism. Although foraging behavior of male and female seabirds can vary markedly, differences in isotopic (carbon, delta C-13 and nitrogen, delta N-15) foraging niche are generally more pronounced within sexually dimorphic species and during phases when competition for food is greater. We examined ecological sexual dimorphism among sympatric nesting Pygoscelis penguins asking whether environmental variability is associated with differences in male and female pre-breeding foraging niche. We predicted that all Pygoscelis species would forage sex-specifically, and that higher quality winter habitat, i.e., higher or lower sea ice coverage for a given species, would be associated with a more similar foraging niche among the sexes. Results: P2/P8 primers reliably amplified DNA of all species. On average, male Pygoscelis penguins are structurally larger than female conspecifics. However, chinstrap penguins were more sexually dimorphic in culmen and flipper features than Adelie and gentoo penguins. Adelies and gentoos were more sexually dimorphic in body mass than chinstraps. Only male and female chinstraps and gentoos occupied separate delta N-15 foraging niches. Strong year effects in delta N-15 signatures were documented for all three species, however, only for Adelies, did yearly variation in delta N-15 signatures tightly correlate with winter sea ice conditions. There was no evidence that variation in sex-specific foraging niche interacted with yearly winter habitat quality. Conclusion: Chinstraps were most sexually size dimorphic followed by gentoos and Adelies. Pre-breeding sex-specific foraging niche was associated with overall SSD indices across species; male chinstrap and gentoo penguins were enriched in delta N-15 relative to females. Our results highlight previously unknown trophic pathways that link Pygoscelis penguins with variation in Southern Ocean sea ice suggesting that each sex within a species should respond similarly in pre-breeding trophic foraging to changes in future winter habitat. DOI
146. Love, OP; Madliger, CL; Bourgeon, S; Semeniuk, CAD; Williams, TD. (2014) Evidence for baseline glucocorticoids as mediators of reproductive investment in a wild bird.General and Comparative Endocrinology 199: 65-69 Evidence for baseline glucocorticoids as mediators of reproductive investment in a wild bird
Corticosterone; Reproductive investment; Phenotypic flexibility; Reaction norm; Fitness; European starling (Sturnus vulgaris)
Determining the mechanisms that mediate investment decisions between current and future reproductive attempts is still a key goal of life-history studies. Since baseline levels of stress hormones (glucocorticoids - GCs) act as predictive and labile regulators of daily energetic balance in vertebrates they remain excellent candidates for mediating investment decisions both within and across reproductive attempts. Using free-living female European starlings (Sturnus vulgaris) we experimentally reduced investment in current reproduction (number of offspring raised in the first brood) to examine whether baseline corticosterone (CORT) acted as a hormonal mediator preparing individuals for a predictable increase in future investment (number of offspring raised in the second brood). Although treatment and control birds raised the same total amount of offspring across two broods, the experimental birds increased reproductive investment in second broods to compensate for the reduced investment in the first brood. Data on both mean and intra-individual changes in baseline CORT support the idea that an increase in baseline CORT between the incubation stages in treatment birds strongly predicted this increase in investment. Importantly, we measured the increase in baseline CORT during late incubation prior to the increase in energetic demand associated with increased reproductive investment in offspring, indicating that flexible within-individual changes in baseline GCs can act as a labile mechanism preparing individuals for predictable increases in reproductive investment. As such, our experimental results indicate that elevated baseline GCs can prepare individuals for investment in energetically expensive life-history stages, rather than simply being elevated as a consequence of increased effort or demand. This suggests that short-term preparative increases in baseline GCs benefit individuals by successfully allowing them to maximize fitness under varying environmental conditions. (C) 2014 Elsevier Inc. All rights reserved. DOI
145. Ryan, CP; Dawson, A; Sharp, PJ; Meddle, SL; Williams, TD. (2014) Circulating breeding and pre-breeding prolactin and LH are not associated with clutch size in the zebra finch (Taeniopygia guttata).General and Comparative Endocrinology 202: 26-34 Circulating breeding and pre-breeding prolactin and LH are not associated with clutch size in the zebra finch (Taeniopygia guttata)
Prolactin; Clutch size; Luteinizing hormone; Life history; Avian reproduction; Plasticity
Clutch size is a fundamental predictor of avian fitness, widely-studied from evolutionary and ecological perspectives, but surprisingly little is known about the physiological mechanisms regulating clutch size variation. The only formal mechanistic hypothesis for avian clutch-size determination predicts an anti-gonadal effect of circulating prolactin (PRL) via the inhibition of luteinizing hormone (LH), and has become widely-accepted despite little experimental support. Here we investigated the relationship between pre-breeding and breeding plasma PRL and LH and clutch-size in captive-breeding female zebra finches (Taeniopygia guttata). Using a repeated-measures design, we followed individual females from pre-breeding, through multiple breeding attempts, and attempted to decrease PRL using the D-2-receptor agonist, bromocriptine. Clutch size was independent of variation in pre-breeding PRL or LH, although pre-breeding LH was negatively correlated with the time between pairing and the onset of laying. Clutch size was independent of variation in plasma PRL on all days of egg-laying. Bromocriptine treatment had no effect on plasma PRL, but in this breeding attempt clutch size was also independent of plasma PRL. Finally, we found no evidence for an inverse relationship between plasma PRL and LH levels, as predicted if PRL had inhibitory effects via LH. Thus, our data fail to provide any support for the involvement of circulating PRL in clutch size determination. These findings suggest that alternative models for hormonal control of avian clutch size need to be considered, perhaps involving downstream regulation of plasma PRL at the level of the ovary, or other hormones that have not been considered to date. (C) 2014 Elsevier Inc. All rights reserved. DOI
144. Tissier, ML; Williams, TD; Criscuolo, F. (2014) Maternal Effects Underlie Ageing Costs of Growth in the Zebra Finch (Taeniopygia guttata).PLOS One 9 Maternal Effects Underlie Ageing Costs of Growth in the Zebra Finch (Taeniopygia guttata)
Maternal effects provide a mechanism to adapt offspring phenotype and optimize the mother's fitness to current environmental conditions. Transferring steroids to the yolk is one way mothers can translate environmental information into potential adaptive signals for offspring. However, maternally-derived hormones might also have adverse effects for offspring. For example, recent data in zebra finch chicks suggested that ageing related-processes (i.e. oxidative stress and telomere loss) were increased after egg-injection of corticosterone (CORT). Still, we have few experimental data describing the effect of maternal effects on the growth-ageing trade-off in offspring. Here, we chronically treated pre-laying zebra finch females (Taeniopygia guttata) with 17-beta-estradiol (E-2) or CORT, and followed offspring growth and cellular ageing rates (oxidative stress and telomere loss). CORT treatment decreased growth rate in male chicks and increased rate of telomere loss in mothers and female offspring. E-2 increased body mass gain in male offspring, while reducing oxidative stress in both sexes but without affecting telomere loss. Since shorter telomeres were previously found to be a proxy of individual lifespan in zebra finches, maternal effects may, through pleiotropic effects, be important determinants of offspring life-expectancy by modulating ageing rate during embryo and post-natal growth. DOI
143. Wagner, DN; Green, DJ; Cooper, JM; Love, OP; Williams, TD. (2014) Variation in Plasma Corticosterone in Migratory Songbirds: A Test of the Migration-Modulation Hypothesis.Physiological and Biochemical Zoology 87: 695-703 Variation in Plasma Corticosterone in Migratory Songbirds: A Test of the Migration-Modulation Hypothesis
Physiological mechanisms underlying migration remain poorly understood, but recent attention has focused on the role of the glucocorticoid hormone corticosterone (CORT) as a key endocrine regulator of migration. The migration-modulation hypothesis (MMH) proposes that baseline plasma CORT levels are elevated in migratory birds to facilitate hyperphagia and lipogenesis and that further elevation of CORT in response to acute stress is suppressed. Consequently, CORT may be a poor indicator of individual condition or environmental variation in migratory birds. We tested the MMH by measuring baseline and stress-induced CORT in common yellowthroats (Geothlypis trichas) during fall migration over 2 consecutive years in the Revelstoke Reach drawdown zone, a migratory stopover site affected by local hydroelectric operations. Birds had low baseline CORT at initial capture (<5 ng/mL) and then showed a robust stress response, with CORT increasing to ca. 50 ng/mL within 10-20 min. Our data therefore do not support the MMH. Baseline CORT did not vary with body mass, time of capture, Julian day, or year, suggesting that variable flooding regimes did not affect baseline CORT. Individual variation in the rate of increase in CORT was correlated with Julian day, being higher later in the migration period. Our data suggest that plasma CORT can be a useful metric in migration studies. DOI PubMed
142. Crespi, EJ; Williams, TD; Jessop, TS; Delehanty, B. (2013) Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals?Functional Ecology 27: 93-106 Life history and the ecology of stress: how do glucocorticoid hormones influence life-history variation in animals?
PREDICT SURVIVAL PROBABILITIES; MARSUPIAL ANTECHINUS-STUARTII; PHASCOGALE-CALURA MARSUPIALIA; TROUT ONCORHYNCHUS-MYKISS; GALAPAGOS MARINE IGUANAS; RED-TAILED PHASCOGALE; LONG-LIVED SEABIRD; CORTICOSTERONE LEVELS; STEROID-HORMONES; PHYSIOLOGICAL STRESS
Glucocorticoids hormones (GCs) are intuitively important for mediation of age-dependent vertebrate life-history transitions through their effects on ontogeny alongside underpinning variation in life-history traits and trade-offs in vertebrates. These concepts largely derive from the ability of GCs to alter energy allocation, physiology and behaviour that influences key life-history traits involving age-specific life-history transitions, reproduction and survival. Studies across vertebrates have shown that the neuroendocrine stress axis plays a role in the developmental processes that lead up to age-specific early life-history transitions. While environmental sensitivity of the stress axis allows for it to modulate the timing of these transitions within species, little is known as to how variation in stress axis function has been adapted to produce interspecific variation in the timing of life-history transitions. Our assessment of the literature confirms that of previous reviews that there is only equivocal evidence for correlative or direct functional relationships between GCs and variation in reproduction and survival. We conclude that the relationships between GCs and life-history traits are complex and general patterns cannot be easily discerned with current research approaches and experimental designs. We identify several future research directions including: (i) integration of proximate and ultimate measures, including longitudinal studies that measure effects of GCs on more than one life-history trait or in multiple environmental contexts, to test explicit hypotheses about how GCs and life-history variation are related and (ii) the measurement of additional factors that modulate the effects of GCs on life-history traits (e.g. GC receptors and binding protein levels) to better infer neurendocrine stress axis actions. Conceptual models of HPA/I axis actions, such as allostatic load and reactive scope, to some extent explicitly predict the role of GCs in a life-history context, but are descriptive in nature. We propose that GC effects on life-history transitions, survival probabilities and fecundity can be modelled in existing quantitative demographic frameworks to improve our understanding of how GC variation influences life-history evolution and GC-mediated effects on population dynamics DOI
141. Crossin, GT; Phillips, RA; Lattin, CR; Romero, LM; Williams, TD. (2013) Corticosterone mediated costs of reproduction link current to future breeding.General and Comparative Endocrinology 193: 112-120 Corticosterone mediated costs of reproduction link current to future breeding
GIANT PETRELS MACRONECTES; PIED FLYCATCHERS; ADRENOCORTICAL-RESPONSE; FORAGING BEHAVIOR; SEXUAL CONFLICT; FEATHER QUALITY; SOUTH GEORGIA; KING PENGUINS; PARENTAL CARE; LONG-TERM
Life-history theory predicts that costs are associated with reproduction. One possible mediator of costs involves the secretion of glucocorticoid hormones, which in birds can be measured in feathers grown during the breeding period. Glucocorticoids mediate physiological responses to unpredictable environmental or other stressors, but they can also function as metabolic regulators during more predictable events such as reproduction. Here we show that corticosterone ("Cort") in feathers grown during the breeding season reflects reproductive effort in two Antarctic seabird species (giant petrels, Macronectes spp.). In females of both species, but not males, feather Cort ("fCort") was nearly 1.5-fold higher in successful than failed breeders (those that lost their eggs/chicks), suggesting a cost of successful reproduction, i.e., high fCort levels in females reflect the elevated plasma Cort levels required to support high metabolic demands of chick-rearing. Successful breeding also led to delayed moult prior to winter migration. The fCort levels and pre-migration moult score that we measured at the end of current breeding were predictive of subsequent reproductive effort in the following year. Birds with high fCort and a delayed initiation of moult were much more likely to defer breeding in the following year. Cort levels and the timing of moult thus provide a potential mechanism for the tradeoff between current and future reproduction. Crown Copyright (C) 2013 Published by Elsevier Inc. All rights reserved. DOI
140. Currier, HA; Letcher, RJ; Williams, TD; Elliott, JE. (2013) An Assessment of In Ovo Toxicity of the Flame Retardant 1,2-Dibromo-4-(1,2-Dibromoethyl) Cyclohexane (TBECH) in the Zebra Finch.Bulletin of Environmental Contamination and Toxicology 91: 455-459 An Assessment of In Ovo Toxicity of the Flame Retardant 1,2-Dibromo-4-(1,2-Dibromoethyl) Cyclohexane (TBECH) in the Zebra Finch
TETRABROMOETHYLCYCLOHEXANE TBECH; BEHAVIOR; EXPOSURE; HORMONES; EGGS
Embryonic toxicity of a brominated flame retardant, TBECH (1,2-dibromo-4-(1, 2-dibromoethyl) cyclohexane) was investigated using the zebra finch (Taeniopygia guttata) as our model. Using in ovo dosing procedures, we injected the technical TBECH compound, consisting of 50:50 alpha-/beta-isomers, directly into the yolk of freshly laid eggs at concentrations of 2.3-94 ng/g egg. No significant effects were observed in terms of growth or survival for either pre-hatch embryos or post-hatch chicks. Analysis of tissue samples at various developmental stages suggests that alpha-/beta-TBECH was metabolized rapidly, and thus is unlikely to cause any direct, long-term effects on the development of zebra finch embryos or offspring. DOI
139. Eens, M; Jaspers, VLB; Van den Steen, E; Bateson, M; Carere, C; Clergeau, P; Costantini, D; Dolenec, Z; Elliott, JE; Flux, J; Gwinner, H; Halbrook, RS; Heeb, P; Mazgajski, TD; Moksnes, A; Polo, V; Soler, JJ; Sinclair, R; Veiga, JP; Williams, TD; Covaci, A; Pinxten, R. (2013) Can starling eggs be useful as a biomonitoring tool to study organohalogenated contaminants on a worldwide scale?Environment International 51: 141-149 Can starling eggs be useful as a biomonitoring tool to study organohalogenated contaminants on a worldwide scale?
BROMINATED FLAME RETARDANTS; POLYBROMINATED DIPHENYL ETHERS; PERSISTENT ORGANIC POLLUTANTS; ENDOCRINE-DISRUPTING CHEMICALS; STURNUS-VULGARIS; EUROPEAN STARLINGS; GREAT-LAKES; PARUS-MAJOR; ORGANOCHLORINE PESTICIDES; GLOBAL DISTRIBUTION
Large-scale international monitoring studies are important to assess emission patterns and environmental distributions of organohalogenated contaminants (OHCs) on a worldwide scale. In this study, the presence of OHCs was investigated on three continents (Europe, North America and Australasia), using eggs of starlings (Sturnus vulgaris and Sturnus unicolor) to assess their suitability for large-scale monitoring studies. To the best of our knowledge, this is the first study using bird eggs of the same species as a biomonitor for OHCs on an intercontinental scale. We found significant differences in OHC concentrations of the eggs among sampling locations, except for hexachlorocyclohexanes (HCHs). Mean concentrations of sum polychlorinated biphenyls (PCBs) in eggs ranged from 78 26 ng/g lipid weight (lw) in Australia to 2900 +/- 1300 ng/g lw in the United States. The PCB profile was dominated by CB 153 and CB 138 in all locations, except for New Zealand, where the contribution of CB 95, CB 101 and CB 149 was also high. The highest mean sum polybrominated diphenyl ether (PBDE) concentrations were found in Canada (4400 +/- 830 ng/g lw), while the lowest mean PBDE concentrations were measured in Spain (3.7 +/- 0.1 ng/g lw). The PBDE profile in starling eggs was dominated by BDE 47 and BDE 99 in all countries, but in Belgium, the higher brominated PBDEs had a higher contribution compared to other countries. For the organochlorine pesticides (OCPs), dichlorodiphenyltrichloroethanes (DDTs) ranged from 110 +/- 16 ng/g lw in France to 17,000 +/- 3400 ng/g lw in New Zealand, while HCHs and hexachlorobenzene were generally in low concentrations in all sampling locations. Chlordanes were remarkably high in eggs from the United States (2500 +/- 1300 ng/g lw). The OCP profile in all countries was largely dominated by p,p'-DDE. In general, the worldwide trends we observed in starling eggs were in accordance with the literature on human and environmental OHC data, which suggests that there is potential for using starling eggs as a biomonitoring tool on a large geographical scale. (C) 2012 Elsevier Ltd. All rights reserved. DOI
138. Eng, ML; Elliott, JE; Letcher, RJ; Williams, TD. (2013) Individual variation in body burden, lipid status, and reproductive investment is related to maternal transfer of a brominated diphenyl ether (BDE-99) to eggs in the zebra finch.Environmental Toxicology and Chemistry 32: 345-352 Individual variation in body burden, lipid status, and reproductive investment is related to maternal transfer of a brominated diphenyl ether (BDE-99) to eggs in the zebra finch
YOLK PRECURSOR DYNAMICS; HERRING GULL EGGS; ORGANOCHLORINE COMPOUNDS; POLYCHLORINATED-BIPHENYLS; TAENIOPYGIA-GUTTATA; FLAME RETARDANTS; TEMPORAL TRENDS; DOMESTIC-FOWL; GREAT-LAKES; BIRDS
Avian eggs are exposed to hydrophobic contaminants through maternal transfer. How maternal transfer of contaminants within a species is influenced by individual variation in characteristics such as body burden, yolk precursor levels, or reproductive investment is not understood. The authors investigated sources of variation in the maternal transfer of 2,2',4,4',5-pentabromodiphenyl ether (BDE-99) in zebra finches (Taeniopygia guttata). The authors dosed adult female zebra finches with levels of BDE-99 relevant to exposure in wild birds (0, 33.7 or 173.8?ng/g body wt/d) for three weeks prior to pairing. Maternal BDE-99 and very-low-density lipoprotein (VLDL) in plasma were measured during egg formation and at clutch completion, and BDE-99 was measured in the corresponding egg. The lipid-normalized egg-to-maternal tissue BDE-99 relationship decreased with increasing maternal burden. Individual variation in maternal VLDL was related to BDE-99 transfer to the eggs when BDE-99 was at background levels in control birds, but not when BDE-99 was elevated in dosed birds. The decrease in maternal plasma BDE-99 over the laying period was only significant (p?<?0.05) in the high-dose birds. Finally, the decrease in BDE-99 in maternal plasma during egg-laying was significantly positively correlated with clutch mass in the high-dose group. These results suggest that the relationship between maternal and egg contaminant levels can be highly variable. This has significant implications for using eggs as indicators of adult or environmental concentrations. Environ. Toxicol. Chem. 2013;32:345352. (C) 2012 SETAC DOI
137. Eng, ML; Williams, TD; Elliott, JE. (2013) Developmental exposure to a brominated flame retardant: An assessment of effects on physiology, growth, and reproduction in a songbird, the zebra finch.Environmental Pollution 178: 343-349 Developmental exposure to a brominated flame retardant: An assessment of effects on physiology, growth, and reproduction in a songbird, the zebra finch
POLYBROMINATED DIPHENYL ETHERS; KESTRELS FALCO-SPARVERIUS; AMERICAN KESTRELS; TAENIOPYGIA-GUTTATA; HALIAEETUS-LEUCOCEPHALUS; ANAS-PLATYRHYNCHOS; EMBRYONIC EXPOSURE; THYROID-HORMONES; OXIDATIVE STRESS; STURNUS-VULGARIS
Mixtures of polybrominated diphenyl ethers (PBDEs) have been widely used as additive flame retardants, and BDE-99 is one of the most predominant congeners found in the environment. BDE-99 has been reported in avian samples worldwide, yet knowledge of its toxicity to birds is minimal. We assessed the short- and long-term effects of nestling exposure to environmentally relevant levels of BDE-99 in a model passerine, the zebra finch. Early exposure to BDE-99 did not affect hematocrit, oxidative stress, or thyroid hormones in either the juvenile or adult stages, and there were no effects on chick growth or survival. BDE-99 exposure caused a dose-dependent delay in timing of reproduction, but there were no other effects on reproductive success. In zebra finches, endpoints related to reproductive behavior appear to be the most sensitive to BDE-99. However, passerines overall appear to be less sensitive than birds of prey or mammals to PBDE exposure. (c) 2013 Elsevier Ltd. All rights reserved. DOI
136. Ogden, LJE; Martin, K; Williams, TD. (2013) ELEVATIONAL DIFFERENCES IN ESTIMATED FATTENING RATES SUGGEST THAT HIGH-ELEVATION SITES ARE HIGH-QUALITY HABITATS FOR FALL MIGRANTS.Auk 130: 98-106 ELEVATIONAL DIFFERENCES IN ESTIMATED FATTENING RATES SUGGEST THAT HIGH-ELEVATION SITES ARE HIGH-QUALITY HABITATS FOR FALL MIGRANTS
SANDPIPERS CALIDRIS-MAURI; PLASMA-LIPID METABOLITES; WESTERN SANDPIPERS; POSTFLEDGING DISPERSAL; AUTUMN MIGRATION; REFUELING RATES; MASS CHANGES; LAND BIRDS; NEW-WORLD; STOPOVER
Many migrant songbird species use high-elevation habitats for stopovers in fall throughout North America, but whether these are good migration habitats as indicated by high fueling rates or other measures has not been previously quantified. At high-quality stopover sites, birds can refuel while maintaining their optimal or preferred migration schedules. We used plasma metabolite analysis to estimate fueling rates of four songbird species during the fall migration period over 3 years at two high-elevation (1,200 m above sea level) and two low-elevation (<25 m above sea level) sites in southwestern British Columbia. For three species with more frugivorous diets during fall the Fox Sparrow (Passerella iliaca), Golden-crowned Sparrow (Zonotrichia atricapilla), and Hermit Thrush (Catharus guttatus)-estimated fattening rates (defined as residual plasma triglyceride levels) were 37-65% higher at high-elevation sites than at low-elevation sites. By contrast, the largely insectivorous and smaller-bodied Orange-crowned Warbler (Oreothlypis celata) had higher estimated fattening rates at low-elevation sites. We found no elevational differences in plasma beta-hydroxybutyrate or glycerol levels except in Hermit Thrushes, which had lower glycerol levels at high elevation. Estimated fattening rates did not differ among the two sparrows and the Hermit Thrush at high-elevation sites, and all three had higher fattening rates than Orange-crowned Warblers. Our data showing strong elevational differences in residual plasma triglyceride levels support the hypothesis that high elevations can be high-quality stopover habitats and, thus, should be considered for protection in songbird management and conservation plans. Received 7 October 2011, accepted 30 August 2012. DOI
135. Palm, EC; Esler, D; Anderson, EM; Williams, TD; Love, OP; Wilson, MT. (2013) Baseline Corticosterone in Wintering Marine Birds: Methodological Considerations and Ecological Patterns.Physiological and Biochemical Zoology 86: 346-353 Baseline Corticosterone in Wintering Marine Birds: Methodological Considerations and Ecological Patterns
WHITE-WINGED SCOTERS; PLASMA-CORTICOSTERONE; PHYSIOLOGICAL STRESS; ADRENOCORTICAL-RESPONSE; FOOD AVAILABILITY; SURF SCOTERS; GLUCOCORTICOID CONCENTRATIONS; FEEDING OPPORTUNITIES; FORAGING BEHAVIOR; CROWNED SPARROW
Previous studies have related levels of plasma corticosterone (CORT) of seabirds to variation in foraging conditions during the breeding period, but it is unclear whether similar relationships between foraging conditions and baseline CORT exist during other life stages. We validated methods for identifying baseline CORT of lethally sampled birds and assessed variation in baseline CORT relative to winter habitat conditions. We collected free-living white-winged scoters (Melanitta fusca) at four wintering sites during December and February. We found increasing CORT values beyond 3 min after time since flush (the duration between initial flush and death), presumably reflecting acute stress responses. Our results demonstrate that it is possible to obtain baseline CORT from lethally sampled birds if the time from initial flush until death is measured. Our study sites varied appreciably in exposure to wind and waves, predation danger, diving depths, and the fraction of preferred foods in scoter diets. Despite these habitat differences, baseline CORT did not vary across sites or winter periods. We interpret this lack of variation as evidence that birds select wintering areas where they can successfully manage site-specific costs and maintain physiological homeostasis. DOI
134. Stein, RW; Williams, TD. (2013) Extreme Intraclutch Egg-Size Dimorphism in Eudyptes Penguins, an Evolutionary Response to Clutch-Size Maladaptation.American Naturalist 182: 260-270 Extreme Intraclutch Egg-Size Dimorphism in Eudyptes Penguins, an Evolutionary Response to Clutch-Size Maladaptation
BREEDING BIOLOGY; ROCKHOPPER PENGUINS; MACARONI PENGUINS; PYGOSCELIS-PAPUA; SPHENISCUS-HUMBOLDTI; MAGELLANIC PENGUINS; CRESTED PENGUINS; SOUTH GEORGIA; BIRD ISLAND; SUCCESS
Eudyptes penguins (six species) are uniquely characterized by a two-egg clutch with extreme intraclutch egg-size dimorphism (ESD): the first-laid A-egg is 17.5%-56.9% smaller than the B-egg. Although A-eggs are viable, they almost never produce fledged chicks (genus average <1%). Using classical life-history theory and phylogenetic comparative methods, we demonstrate a marked slow-down in the life history of Eudyptes: age of first reproduction is 52% later and annual fecundity 48% lower compared with other two-egg clutch penguin species. All six Eudyptes species have retained a two-egg clutch, despite this pronounced life-history slow-down; this suggests evolutionary mismatch between clutch size and chicks fledged per clutch. Consistent with this, we show that Eudyptes fledge 43% fewer chicks per clutch than other two-egg clutch penguin species. Extreme intraclutch ESD in Eudyptes is associated primarily with a uniform (5%) increase in relative B-egg size, and B-egg size has evolved in accord with life history. We further show that intraclutch ESD is positively correlated with age of first reproduction in Eudyptes but not in other two-egg clutch penguin species. We argue that Eudyptes' persistent failure to evolve a one-egg clutch constitutes a unique genus-wide evolutionary maladaptation and that extreme intraclutch ESD evolved as a correlated response to selection favoring a slower life history imposed by their extreme pelagic overwintering and migration ecology. DOI
133. Winter, V; Elliott, JE; Letcher, RJ; Williams, TD. (2013) Validation of an egg-injection method for embryotoxicity studies in a small, model songbird, the zebra finch (Taeniopygia guttata).Chemosphere 90: 125-131 Validation of an egg-injection method for embryotoxicity studies in a small, model songbird, the zebra finch (Taeniopygia guttata)
In ova exposure; Embryotoxicity; Developmental effects; Zebra finch; Flame retardant; PBDE-99
Female birds deposit or 'excrete' lipophilic contaminants to their eggs during egg formation. Concentrations of xenobiotics in bird eggs can therefore accurately indicate levels of contamination in the environment and sampling of bird eggs is commonly used as a bio-monitoring tool. It is widely assumed that maternally transferred contaminants cause adverse effects on embryos but there has been relatively little experimental work confirming direct developmental effects (cf. behaviorally-mediated effects). We validated the use of egg injection for studies of in ovo exposure to xenobiotics for a small songbird model species, the zebra finch (Taeniopygia guttata), where egg weight averages only 1 g. We investigated a) the effect of puncturing eggs with or without vehicle (DMSO) injection on egg fate (embryo development), chick hatching success and subsequent growth to 90 days (sexual maturity), and b) effects of two vehicle solutions (DMSO and safflower oil) on embryo and chick growth. PBDE-99 and -47 were measured in in ovo PBDE-treated eggs, chicks and adults to investigate relationships between putative injection amounts and the time course of metabolism (debromination) of PBDE-99 during early development. We successfully injected a small volume (5 mu L) of vehicle into eggs, at incubation day 0, with no effects on egg or embryo fate and with hatchability similar to that for non-manipulated eggs in our captive-breeding colony (43% vs. 48%). We did find some evidence for an inhibitory effect of DMSO vehicle on post-hatching chick growth, in male chicks only. This method can be used to treat eggs in a dose-dependent, and ecologically-relevant, manner with PBDE-99, based on chemical analysis of eggs, hatchling and adults. (C) 2012 Elsevier Ltd. All rights reserved. DOI
132. Winter, V; Williams, TD; Elliott, JE. (2013) A three-generational study of In ovo exposure to PBDE-99 in the zebra finch.Environmental Toxicology and Chemistry 32: 562-568 A three-generational study of In ovo exposure to PBDE-99 in the zebra finch
POLYBROMINATED DIPHENYL ETHERS; BROMINATED FLAME RETARDANTS; KESTRELS FALCO-SPARVERIUS; CHICKEN GALLUS-GALLUS; HERRING GULL EGGS; AMERICAN KESTRELS; 2,2',4,4',5-PENTABROMODIPHENYL ETHER; TAENIOPYGIA-GUTTATA; REPRODUCTIVE EFFORT; NEONATAL EXPOSURE
Based on a literature review of avian data for polybrominated diphenyl ethers (PBDEs), ecologically relevant doses, low (10ng/egg), medium (100ng/egg), and high (1,000ng/egg) of the 2,2,4,4,5-pentabromodiphenyl ether (BDE-99) congener along with dimethylsulfoxide (DMSO) control were injected into the yolk sac of un-incubated eggs of zebra finch, Taeniopygia guttata. Offspring development and adult phenotype were followed over three generations. No effects of in ovo PBDE exposure on hatching success, chick growth, thyroid hormone levels, or hematological traits were measured at sexual maturity (90d posthatching). However, the authors did detect significant effects of BDE-99 treatment on adult phenotype of in ovoexposed birds by breeding observations, in which clutch size was significantly smaller in all PBDE-dosed birds (low, medium, and high) compared with controls. A trend was also seen for longer laying intervals in PBDE-dosed birds (1314d) compared with control birds (8d). In addition, a significant effect of PBDE was found on growth of the second-generation offspring of in ovotreated females; body mass was significantly lower in the high-PBDE dosed birds compared with controls from hatch through to fledging (day 30). The authors found no evidence of effects over the longer term and in successive generations, whether in adult, reproductive phenotype of the second-generation offspring of in ovotreated birds, or in the growth of their (third-generation) offspring. Their results suggest that egg levels as low as 10ng/g BDE-99 may affect reproduction in small passerines by reducing clutch size. Environ. Toxicol. Chem. 2013;32:562568. (c) 2012 SETAC DOI
131. Zanette, LY; Hobson, KA; Clinchy, M; Travers, M; Williams, TD. (2013) Food use is affected by the experience of nest predation: implications for indirect predator effects on clutch size.Oecologia 172: 1031-1039 Food use is affected by the experience of nest predation: implications for indirect predator effects on clutch size
SNOWSHOE HARE CYCLE; EGG-PRODUCTION; PREY INTERACTIONS; SONG SPARROWS; RISK; STRESS; REPRODUCTION; COST; ELK; CONSEQUENCES
Indirect predator effects on prey demography include any effect not attributable to direct killing and can be mediated by perceived predation risk. Though perceived predation risk clearly affects foraging, few studies have yet demonstrated that it can chronically alter food intake to an extent that affects demography. Recent studies have used stable isotopes to gauge such chronic effects. We previously reported an indirect predator effect on the size of subsequent clutches laid by song sparrows (Melospiza melodia). Females that experienced frequent experimental nest predation laid smaller clutches and were in poorer physiological condition compared to females not subject to nest predation. Every female was provided with unlimited supplemental food that had a distinctive C-13 signature. Here, we report that frequent nest predation females had lower blood delta C-13 values, suggesting that the experience of nest predation caused them to eat less supplemental food. Females that ate less food gained less fat and were in poorer physiological condition, consistent with the effect on food use contributing to the indirect predator effect on clutch size. Tissue delta N-15 values corroborated that clutch size was not likely constrained by endogenous resources. Finally, we report that the process of egg production evidently affects egg delta C-13 values, and this may mask the source of nutrients to eggs. Our results indicate that perceived predation risk may impose food limitation on prey even where food is unlimited and such predator-induced food limitation ought to be added to direct killing when considering the total effect of predators on prey numbers. DOI
130. Crossin GT, Poisbleau M, Demongin L, Chastel O, Williams TD, Eens M, Quillfeldt P. (2012) Migratory constraints on yolk precursors limit yolk androgen deposition and underlie a brood reduction strategy in rockhopper penguins.Biol Lett. 2012 Dec 23;8(6):1055-8. Epub 2012 Jul 18. 8: 1055-1058 Migratory constraints on yolk precursors limit yolk androgen deposition and underlie a brood reduction strategy in rockhopper penguins.
androstenedione; testosterone; physiological epiphenomenon hypothesis; vitellogenin; maternal effects; carryover effects
Hormonally mediated maternal effects link maternal phenotype and environmental conditions to offspring phenotype. The production of lipid-rich maternal yolk precursors may provide a mechanism by which lipophilic steroid hormones can be transported to developing yolks, thus predicting a positive correlation between yolk precursors in mothers and androgen levels in eggs. Using rockhopper penguins (Eudyptes chrysocome), which produce a two-egg clutch characterized by extreme egg-size dimorphism, reversed hatching asynchrony and brood-reduction, we examined correlations between circulating concentrations of the primary yolk-precursor vitellogenin (VTG) and levels of yolk androgens. Previous work in Eudyptes penguins has shown that egg-size dimorphism is the product of migratory constraints on yolk precursor production. We predicted that if yolk precursors are constrained, androgen transport to developing yolks would be similarly constrained. We reveal positive linear relationships between maternal VTG and androgens in small A-eggs but not larger B-eggs, which is consistent with a migratory constraint operating on the A-egg. Results suggest that intra-clutch variation in total yolk androgen levels depends on the production and uptake of yolk precursors. The brood reduction strategy common to Eudyptes might thus be best described as the result of a migratory constraint.
DOI
129. Crossin, GT; Dawson, A; Phillips, RA; Trathan, PN; Gorman, KB; Adlard, S; Williams, TD. (2012) Seasonal patterns of prolactin and corticosterone secretion in an Antarctic seabird that moults during reproduction.General and Comparative Endocrinology 175: 74-81 Seasonal patterns of prolactin and corticosterone secretion in an Antarctic seabird that moults during reproduction
Prolactin; Corticosterone; Physiological conflict; Incubation; Chick rearing; Giant petrel; Macronectes; Life-history; Foraging behaviour; Parental care
In avian species that have evolved life-history strategies wherein molt and breeding overlap, there are potential conflicts between the regulatory roles of baseline prolactin and corticosterone in parental care (positive) and moult (negative). We describe seasonal patterns of hormonal secretion, moult, and parental behaviour in sibling species of giant petrels (Macronectes spp.) which begin moult during the incubation/early chick-rearing stage of reproduction. With the exception of male Southern giant petrels (Macronectes giganteus), prolactin secretion and moult in Northern (Macronectes halli) and female Southern giant petrels conformed to those observed in all other avian species, with the initiation of moult coincident with decreases from peak prolactin levels. However, male Southern giant petrels began moulting early in incubation when prolactin was increasing and had not yet peaked, which suggests a requirement of prolactin for incubation behaviour and a dissociation of prolactin from moult. Corticosterone showed little seasonal variation and no relationship with moult. When comparing prolactin, corticosterone, and moult in failed vs. active breeders, we found that failed breeding enabled a more rapid down-regulation of prolactin, thus facilitating a more rapid moult. We present specific examples of the behavioural ecology of giant petrels which we conclude help mediate any potential hormonal conflicts between parental care and moult. Crown Copyright (C) 2011 Published by Elsevier Inc. All rights reserved. DOI
128. Crossin, GT; Phillips, RA; Trathan, PN; Fox, DS; Dawson, A; Wynne-Edwards, KE; Williams, TD. (2012) Migratory carryover effects and endocrinological correlates of reproductive decisions and reproductive success in female albatrosses.General and Comparative Endocrinology 176: 151-157 Migratory carryover effects and endocrinological correlates of reproductive decisions and reproductive success in female albatrosses
Trade-offs; Vitellogenin; Physiological conflict; Yolk precursors; Reproductive hormones; Seabirds
Physiological mechanisms mediating carryover effects, wherein events or activities occurring in one season, habitat, or life-history stage affect important processes in subsequent life-history stages, are largely unknown. The mechanism most commonly invoked to explain carryover effects from migration centres on the acquisition and utilization of resources (e.g. body mass, or individual 'condition'). However, other mechanisms are plausible, e.g. trade-offs reflecting conflict or incompatibility between physiological regulatory systems required for different activities or life-history stages (migration vs. reproduction). Here we show that in female black-browed albatrosses (Thalassarche melanophris) the decision to reproduce or to defer reproduction, made prior to their arrival at breeding colonies after long-distance migration, is associated with condition-related (body mass, hematocrit, hemoglobin concentrations) and hormonal (progesterone, testosterone, estrogen-dependent yolk precursors) traits. In contrast, reproductive success showed little association with condition but showed significant associations with the steroidogenic processes underlying follicle development. Specifically, success was determined by reproductive readiness via differences in steroid hormones and hormone-dependent traits. Successful albatrosses were characterized by high progesterone and high estradiol-dependent yolk precursor levels, whereas failed albatrosses had high testosterone and low yolk precursor levels. Results are discussed with reference to migratory carryover effects and how these can differentially affect the physiologies influencing reproductive decisions and reproductive success. (C) 2012 Elsevier Inc. All rights reserved. DOI
127. Crossin, GT; Trathan, PN; Phillips, RA; Gorman, KB; Dawson, A; Sakamoto, KQ; Williams, TD. (2012) Corticosterone Predicts Foraging Behavior and Parental Care in Macaroni Penguins.American Naturalist 180: E31-E41 Corticosterone Predicts Foraging Behavior and Parental Care in Macaroni Penguins
allostasis; time-depth recorders; telemetry; parental care; reproductive investment; stress hormones
Corticosterone has received considerable attention as the principal hormonal mediator of allostasis or physiological stress in wild animals. More recently, it has also been implicated in the regulation of parental care in breeding birds, particularly with respect to individual variation in foraging behavior and provisioning effort. There is also evidence that prolactin can work either inversely or additively with corticosterone to achieve this. Here we test the hypothesis that endogenous corticosterone plays a key physiological role in the control of foraging behavior and parental care, using a combination of exogenous corticosterone treatment, time-depth telemetry, and physiological sampling of female macaroni penguins (Eudyptes chrysolophus) during the brood-guard period of chick rearing, while simultaneously monitoring patterns of prolactin secretion. Plasma corticosterone levels were significantly higher in females given exogenous implants relative to those receiving sham implants. Increased corticosterone levels were associated with significantly higher levels of foraging and diving activity and greater mass gain in implanted females. Elevated plasma corticosterone was also associated with an apparent fitness benefit in the form of increased chick mass. Plasma prolactin levels did not correlate with corticosterone levels at any time, nor was prolactin correlated with any measure of foraging behavior or parental care. Our results provide support for the corticosterone-adaptation hypothesis, which predicts that higher corticosterone levels support increased foraging activity and parental effort. DOI
126. Crossin, GT; Trathan, PN; Williams, TD. (2012) Potential mode of clutch size determination and follicle development in Eudyptes penguins.Polar Biology 35: 313-317 Potential mode of clutch size determination and follicle development in Eudyptes penguins
Egg follicle; Follicle recruitment; Macaroni penguin; Yolk
It has long been held that Eudyptes penguins will only ever develop a maximum of two mature yolky follicles to match their invariant two-egg clutch, an idea inferred largely from egg removal studies. Combining our own data with those from a previous but rarely cited study and by applying these to a simple developmental model, we show that macaroni penguins (Eudyptes chrysolophus) develop up to four large, yolky vitellogenic follicles, and they do so despite the fact that they will never lay more than two eggs or rear more than one chick, a tactic that seems maladaptive given their realized reproductive success. We discuss these results within the context of the usual pattern of reproductive investment in Eudyptes penguins and suggest a broader significance to modes of clutch size determination among all penguins (order Sphenisciformes). DOI
125. Eng, ML; Elliott, JE; MacDougall-Shackleton, SA; Letcher, RJ; Williams, TD. (2012) Early Exposure to 2,2 ',4,4 ',5-Pentabromodiphenyl Ether (BDE-99) Affects Mating Behavior of Zebra Finches.Toxicological Sciences 127: 269-276 Early Exposure to 2,2 ',4,4 ',5-Pentabromodiphenyl Ether (BDE-99) Affects Mating Behavior of Zebra Finches
BDE-99; PBDEs; brain; song-control system; mating behavior; birds
2,2',4,4',5-Pentabromodiphenyl ether (BDE-99) is a brominated flame retardant congener that has pervaded global food chains, being reported in avian egg and tissue samples throughout the world. Its effects on birds are not well known, but there is evidence in exposed mammals that it directly mediates and causes neurotoxicity, alters thyroid hormone homeostasis, and lowers sex steroid hormone concentrations. In birds, those processes could disrupt the song-control system and male mating behavior. In this study, the effects of nestling exposure to environmentally relevant levels of BDE-99 were assessed in a model songbird species, the zebra finch (Taeniopygia guttata). A tissue residue study in which zebra finch nestlings were orally exposed to 0, 2.5, 15.8, or 50.7 ng BDE-99/g body weight (bw) per day over the 21-day nesting period validated dosing methods and confirmed dose levels were environmentally relevant (332.7 +/- 141.0 to 4450.2 +/- 1396.2 ng/g plasma lipid). A full-scale study exposing nestlings to 0, 2.5, 15.8, 50.7, or 173.8 ng BDE-99/g bw/day was carried out to investigate long-term effects of BDE-99 on the adult song-control nuclei volumes, song quality, and male mating behavior. Early exposure to BDE-99 had significant effects on male mating behavior and the response of clean experienced females to exposed males. There was no effect on male song-control nuclei or song quality, and there were nondose-dependent effects on female song-control nuclei. The results demonstrate that early exposure to environmentally relevant levels of BDE-99 affects the behavior of zebra finches. DOI
124. Vezina, F; Williams, TD; Piersma, T; Morrison, RIG. (2012) Phenotypic compromises in a long-distance migrant during the transition from migration to reproduction in the High Arctic.Functional Ecology 26: 500-512 Phenotypic compromises in a long-distance migrant during the transition from migration to reproduction in the High Arctic
arrival biology; basal metabolic rate; breeding; energetics; life-history stages; phenotypic flexibility; physiological conflicts; polar environment; reproduction; thermoregulation
1. Seasonal carry-over effects may be important structuring components of avian life-history cycles. However, little is known on physiological transitions between stages and on phenotypic compromises that may be made at such time to improve fitness. 2. We studied postmigratory body remodelling in red knots (Calidris canutus islandica) arriving on the Arctic breeding grounds. Our objectives were to determine the effects of body reconstruction and preparation for breeding on maintenance energy costs and to determine whether weather conditions can force compromises between functions required for postmigration recovery of body composition, thermoregulation and breeding. 3. During two consecutive springs at the northernmost land on Earth (Alert, Ellesmere Island, Canada, 82 degrees 30' N), we monitored changes in knots post- arrival body stores. Using ultrasonography, we also tracked changes in gizzard size, an indicator of gut size, and pectoral muscle thickness, not only an endogenous protein source but also a thermogenic organ. We measured basal metabolic rate (BMR) throughout reconstruction and compared it with BMR of nonbreeding red knots wintering in the Dutch Wadden Sea. 4. Arriving knots faced temperatures up to 13 degrees C lower than during midwinter. Birds arrived with large body stores and pectoral muscles, which declined in size while they grew their gizzard and prepared for breeding. BMR at arrival was indistinguishable from winter BMR and increased linearly throughout reconstruction. BMR increased up to 69% faster in females than males, likely due to the development of their reproductive organs. 5. Birds had lower body stores but larger muscles in the colder year, and muscle loss was correlated with the warming of spring temperatures. Therefore, muscles would not only serve as a nutrient source, but their thermogenic function could also provide the flexibility to cope with high thermostatic costs in the spring. However, retaining muscles for shivering may limit protein recirculation and delay the onset of breeding. 6. Postmigratory recovery therefore involves significant energy costs and arriving birds likely have to make physiological compromises, depending on spring conditions, which may impact on fitness. Although this period is clearly critical in the life cycle of red knots, it is one of the least understood life- history stages in Arctic- breeding shorebirds. DOI
123.Williams, TD. (2012) Hormones, life-history, and phenotypic variation: Opportunities in evolutionary avian endocrinology.General and Comparative Endocrinology 176: 286-295 Hormones, life-history, and phenotypic variation: Opportunities in evolutionary avian endocrinology
Phenotypic variation; Breeding; Clutch size; Hormonal pleiotropy; Hormonal conflict
Life-histories provide a powerful, conceptual framework for integration of endocrinology, evolutionary biology and ecology. This has been a commonly articulated statement but here I show, in the context of avian reproduction, that true integration of ultimate and proximate approaches has been slow. We have only a rudimentary understanding of the physiological and hormonal basis of phenotypic variation in (a) reproductive traits that contribute most to individual variation in lifetime fitness in birds (e.g. laying date, clutch size, parental effort) and (b) trade-offs that link these traits or that link reproduction to other life stages (e.g. migration, molt). I suggest that some reasons for this relative lack of progress include (a) an increasingly reductionist and centralist (upstream) focus which is more and more removed from ecological/evolutionary context, and from peripheral (downstream) mechanisms that actually determine how phenotypes work (b) a long-standing male-bias in experimental studies, even though the key reproductive traits which contribute most to variation in fitness are female-specific traits (e.g. onset of vitellogenesis, egg size or number). Endocrine systems provide strong candidate mechanisms for regulation of phenotypic variation in single traits, and two endocrine concepts capture the essence of life-history trade-offs: (a) hormonal 'pleiotropy', when single hormones have both positive and negative effects on multiple physiological systems and (b) hormonal conflict between regulatory systems required for different but over-lapping or linked life-history stages. I illustrate these ideas with examples of reproductive anemia, migration-reproduction overlap, and molt-breeding overlap, to highlight some of the tremendous opportunities that exist for comparative endocrinologists to contribute to mechanistic studies of avian reproduction in an evolutionary context. (C) 2011 Elsevier Inc. All rights reserved. DOI
122.Williams, TD; Fronstin, RB; Otomo, A; Wagner, E. (2012) Validation of the use of phenylhydrazine hydrochloride (PHZ) for experimental manipulation of haematocrit and plasma haemoglobin in birds.Ibis 154: 21-29 Validation of the use of phenylhydrazine hydrochloride (PHZ) for experimental manipulation of haematocrit and plasma haemoglobin in birds
European Starlings; experimental manipulation; haemolytic anaemia; individual variation; Zebra Finches
The levels of haematocrit (Hct) and plasma haemoglobin (Hb) vary markedly through the annual cycle of birds, as well as among individuals at all life-stages (embryos, chicks, adults). It is thus surprising that the functional, fitness-related consequences of this variation are poorly understood. Putative adaptive variation in these haematological traits has been associated with varying demands for aerobic capacity and oxygen transport, for example during migration, winter acclimatization, with increasing altitude, or during parental care. It has also been proposed that changes in Hct might reflect costs of parental investment, for example during reproductive anaemia. However, almost all studies to date have been correlative. Here we describe a series of experiments that validate the use of phenylhydrazine hydrochloride (PHZ) for the transient, reversible experimental manipulation of Hct and Hb in birds. A single bolus injection (12.5 mu g PHZ/g body weight delivered via intra-muscular injection) caused a rapid decrease in Hct and plasma Hb within 24 h, from pretreatment values of 5054% to 4044% in non-breeding Zebra Finches Taenipoygia guttata and European Starlings Sturnus vulgaris, and to 35% in breeding female Zebra Finches, changes within the normal physiological range. Hct and Hb returned to pre-injection levels within 510 days of treatment. Changes in plasma Hb paralleled those for Hct. We suggest that PHZ treatment provides a widely applicable technique for use in experimental work to establish relationships between haematological status, aerobic capacity, workload (e.g. migration, parental care, thermoregulation), individual quality (of both adults and chicks) and trade-offs such as costs of reproduction. DOI
121. Bourgeon, S; Guindre-Parker, S; Williams, TD. (2011) Effects of Sibling Competition on Growth, Oxidative Stress, and Humoral Immunity: A Two-Year Brood-Size Manipulation.Physiological and Biochemical Zoology 84: 429-437 Effects of Sibling Competition on Growth, Oxidative Stress, and Humoral Immunity: A Two-Year Brood-Size Manipulation
We investigated the effects of ecological context (by comparing data from two consecutive years) and experimentally manipulated nestling developmental conditions (large vs. small brood size) on immune function (immunoglobulin Y [IgY]) and oxidative stress in nestling European starlings Sturnus vulgaris. On the basis of annual differences in chicks' morphological traits and body masses close to fledging, we established that 2007 was a relative low-quality year and 2008 was a relatively high-quality year. Total antioxidant capacity (TAC) was significantly lower in experimentally enlarged broods, but only in the low-quality year (2007). Total oxidant status (TOS) was independent of brood size in both years but was 45% higher in the low-quality year. Consequently, plasma oxidative status (the ratio between TOS and TAC) was higher in 2007. In contrast, plasma IgY levels were higher in the experimentally enlarged broods and in the high-quality year (2008). Thus, immune function and oxidative stress showed inverse relationships with developmental conditions and annual variation in year quality. Finally, TOS and TAC were positively correlated, but only in the low-quality year (2007), and there was no relationship observed between IgY and markers of oxidative stress. Our results demonstrate the importance of taking into account year effects or ecological context when assessing environmental effects on physiological mechanisms underlying the life-history traits of chicks, such as oxidative stress. DOI
120. Love, OP; Williams, TD. (2011) Manipulating developmental stress reveals sex-specific effects of egg size on offspring phenotype.Journal of Evolutionary Biology 24: 1497-1504 Manipulating developmental stress reveals sex-specific effects of egg size on offspring phenotype
STARLING STURNUS-VULGARIS; FLUCTUATING ASYMMETRY; FLIGHT PERFORMANCE; REARING CONDITIONS; REPRODUCTIVE INVESTMENT; HAEMATOPUS-OSTRALEGUS; COMPENSATORY GROWTH; IMMUNE-RESPONSE; TIT NESTLINGS; SURVIVAL
The general lack of experimental evidence for strong, positive effects of egg size on offspring phenotype has led to suggestions that avian egg size is a neutral trait. To better understand the functional significance of intra-specific variation in egg size as a determinant of offspring fitness within a life-history (sex-specific life-history strategies) and an environmental (poor rearing conditions) context, we experimentally increased developmental stress (via maternal feather-clipping) in the sexually size-dimorphic European starling (Sturnus vulgaris) and measured phenotypic traits in offspring across multiple biological scales. As predicted by life-history theory, sons and daughters had different responses when faced with developmental stress and variation in egg size. In response to developmental stress, small egg size in normally faster-growing sons was associated with catch-up growth prior to attaining larger adult size, resulting in a reduction in developmental stability. Daughters apparently avoided this developmental instability by reducing growth rate and eventual adult body mass and size. Interestingly, large egg size provided offspring with greater developmental flexibility under poor growth conditions. Large-egg sons and daughters avoided the reduction in developmental stability, and daughters also showed enhanced escape performance during flight trials. Furthermore, large egg size resulted in elevated immune responses for both sexes under developmental stress. These findings show that there can be significant, but complex, context-specific effects of egg size on offspring phenotype at least up to fledging, but these can only be demonstrated by appreciating variation in the quality of the offspring environment and life histories. Results are therefore consistent with egg size playing a significant role in shaping the phenotypic outcome of offspring in species that show even greater intra-specific variation in egg size than starlings. DOI
119. BLIGHT, L.K., BERTRAM, D.F., WILLIAMS, T.D. & COWEN, L. (2010) Interannual variation in egg neglect and incubation routine of Rhinoceros Auklets Cerorhinca monocerata during the 1998-1999 El Niño / La Niña events.Marine Ornithology 38: 11-15 Interannual variation in egg neglect and incubation routine of Rhinoceros Auklets Cerorhinca monocerata during the 1998-1999 El Niño / La Niña events.
We used artificial eggs containing miniature temperature loggers to quantify nest attendance patterns by breeding Rhinoceros Auklets Cerorhinca monocerata over two seasons. The first year coincided with a strong El Niño event and low breeding success, while the second was one of La Niña conditions and high colony-wide productivity. Logger data revealed highly variable patterns of parental nest attendance between the two years. In 1998, we recorded 0-17 periods of neglect per breeding pair (n = 7), as well as nest abandonment part way through the incubation period. In 1999, the number of periods of egg neglect ranged from 0-3 (n = 13), and no monitored nests were abandoned. As in other seabird species, more pairs (62%) exhibited neglect during the first third of incubation than during the subsequent two-thirds. The longest period an egg was left unattended was nearly 3 d (69 h); the shortest was 9 h. We conclude that incubating Rhinoceros Auklets were able to modulate nest attendance behaviour in response to changing oceanographic conditions and prey availability, likely mediated via their own body condition. We recommend use of similar egg models for future studies on avian nest attendance.PDF
118. Cesh, LS; Elliott, KH; Quade, S; McKinney, MA; Maisoneuve, F; Garcelon, DK; Sandau, CD; Letcher, RJ; Williams, TD; Elliott, JE. (2010) POLYHALOGENATED AROMATIC HYDROCARBONS AND METABOLITES: RELATION TO CIRCULATING THYROID HORMONE AND RETINOL IN NESTLING BALD EAGLES (HALIAEETUS LEUCOCEPHALUS).Environmental Toxicology and Chemistry 29: 1301-1310 POLYHALOGENATED AROMATIC HYDROCARBONS AND METABOLITES: RELATION TO CIRCULATING THYROID HORMONE AND RETINOL IN NESTLING BALD EAGLES (HALIAEETUS LEUCOCEPHALUS)
Contaminants; Thyroid hormone; Retinol; Bald eagle; PCBs
Polyhalogenated aromatic hydrocarbons are global contaminants that are often considered to be endocrine disruptors and include 1,1-dichloro-2,2-bis(4-chlorophenyl)ethylene (p,p'-DDE), polychlorinated biphenyls (PCBs), and polybrominated diphenyl ethers (PBDEs). The present study examined these compounds and their hydroxylated metabolites or analogues and relationships with circulating thyroid hormones and retinols in plasma from nestling and adult bald eagles in British Columbia, Canada. and California, USA. We also compared our results with published data. Thyroxine (T4) decreased with Sigma PCB and CB153 in nestling bald eagles. which was congruent with results from nine of 14 other published avian laboratory and field studies. Free thyroid hormone levels also decreased with CB-153 and hydroxylated PCBs (OH-PCBs). Retinol increased with CBI 18 and CB180 in nestling eagles, decreased with OH-PCBs in a subset of nestlings, and decreased in 7 of 12 PCB published studies. Thyroxine decreased with p,p'-DDE for nestlings and with data reported in one of five other published studies. In our samples, plasma retinol, triiodothyronine (T3), and T4 were independent of Sigma PBDEs, whereas Sigma OH-PBDEs were weakly but significantly correlated with increases in T3 and retinol. Adult bald eagles showed no relationship between contaminants and thyroid hormones, which is consistent with other studies of long-lived birds, perhaps because adult birds have time to adjust to contaminant levels. Measurement of circulating thyroid hormones appears to be a more useful biomarker than retinols, given the more consistent response of T4 to PCBs here and reported in the literature. We conclude that current environmental exposures to PCBs in British Columbia and in southern California are associated with significant decreases in T4, suggesting a potential negative effect on the endocrine system of nestling bald eagles. Environ. Toxicol. Chem. 2010;29:1301 1310. (C) 2010 SETAC DOI
117. Crossin, GT; Trathan, PN; Phillips, RA; Dawson, A; Le Bouard, F; Williams, TD. (2010) A Carryover Effect of Migration Underlies Individual Variation in Reproductive Readiness and Extreme Egg Size Dimorphism in Macaroni Penguins.American Naturalist 176: 357-366 A Carryover Effect of Migration Underlies Individual Variation in Reproductive Readiness and Extreme Egg Size Dimorphism in Macaroni Penguins
carryover effect; Eudyptes; physiological conflict; egg development; reproductive trade-off; vitellogenin
Where life-history stages overlap, there is the potential for physiological conflicts that might be important in mediating carryover effects. However, our knowledge of the specific physiological mechanisms underlying carryover effects remains rudimentary, and specific examples remain rare. Here we show that female macaroni penguins (Eudyptes chrysolophus) initiate vitellogenesis and yolk formation while at sea during return migrations to breeding colonies; yolk formation takes approximately 16 days, but females lay only 7-14 days after their return. Once on land, Eudyptes penguins show a unique reproductive pattern of extreme egg size dimorphism in which the smaller, first-laid A-egg is 55%-75% of the size of the larger B-egg. We show that the degree of egg size dimorphism is inversely correlated with time between arrival and laying; that is, females that begin reproductive development well in advance of their return produce more dimorphic eggs. Furthermore, late-arriving females that produce the most dimorphic eggs have lower plasma levels of the yolk precursor vitellogenin on arrival; that is, they show lower reproductive readiness. These data support the hypothesis that extreme egg size dimorphism in Eudyptes penguins is due to a physiological constraint imposed by a migratory carryover effect and argue against small A-eggs having a specific, adaptive function. DOI
114. Kordonowy, LL; McMurtry, JP; Williams, TD. (2010) Variation in plasma leptin-like immunoreactivity in free-living European starlings (Sturnus vulgaris).General and Comparative Endocrinology 166: 47-53 Variation in plasma leptin-like immunoreactivity in free-living European starlings (Sturnus vulgaris)
Leptin-like immunoreactivity; European starling; Sturnus vulgaris; Reproduction; Seasonal variation
Leptin, a protein hormone secreted by fat cells, is best known for its role as an adiposity signal; however, leptin has diverse physiological roles ranging from regulation of feeding behavior and body weight, to effects on reproduction and immune function. Although leptin has been extensively studied in mammals, the identification and function of leptin in birds remains controversial, and studies have focused on captive or domesticated species. Here, we describe changes in plasma leptin-like immunoreactivity during the reproductive and non-reproductive seasons in free-living female European starlings (Sturnus vulgaris). Plasma leptin-like immunoreactivity was high during egg-laying (27.8 +/- 2.4 ng/mL) and clutch completion (23.8 +/- 1.6ng/mL), decreased during incubation (13.0 +/- 1.6ng/mL) and chick-rearing (12.0 +/- 1.3 ng/mL), but was elevated again in non-breeders in November (23.7 +/- 1.1 ng/mL). Although there was marked and consistent variation in total body mass and body composition with breeding stage and season in this population, plasma leptin-like immunoreactivity did not parallel changes in body mass or body composition. These data suggest that the strong positive relationship between plasma leptin-like immunoreactivity and body mass reported for captive birds and mammals does not hold for free-living birds. Rather, among free-living female European starlings, variation in plasma leptin-like immunoreactivity is associated with breeding stage or seasonal variation per se, and we discuss possible mechanisms underlying this variation, focusing on ovarian function and egg production. (C) 2009 Elsevier Inc. All rights reserved. DOI
113. Salvante, KG; Vezina, F; Williams, TD. (2010) Evidence for within-individual energy reallocation in cold-challenged, egg-producing birds.Journal of Experimental Biology 213: 1991-2000 Evidence for within-individual energy reallocation in cold-challenged, egg-producing birds
egg production; cold acclimation; metabolic rate; thermoregulation; energy reallocation; Taeniopygia guttata
Recent studies have shown that the metabolic cost of avian egg production involves a 16-27% increase in metabolic rate (MR) above non-reproductive basal or resting values (BMR and RMR, respectively). To determine how the metabolic cost of egg production interacted with the costs of other essential processes (such as cold acclimation and active heat production), we measured the MR of non-breeding and egg-producing zebra finches (Taeniopygia guttata) while (a) warm-acclimated (to 19-21 degrees C) and measured within their thermoneutral zone (at 35 degrees C), (b) cold-acclimated (to 7 degrees C) and measured at thermoneutrality (at 35 degrees C, i.e. not actively producing heat), and (c) cold-acclimated and measured below thermoneutrality (at 7 degrees C) (i.e. during active heat production). The metabolic cost of egg production was small (24% above BMR) compared with the additive costs of cold acclimation and active heat production (224% above BMR). Exposure to low ambient temperatures was accompanied by an increase in seed consumption (by 72%) and a decrease in locomotor activity (by 72%) compared with warm-acclimated, non-breeding values. By contrast, egg production in heat-producing females was associated with an 11% decrease in MR and a 22% decrease in seed consumption compared with non-breeding thermoregulating values. Our data suggest that while the increase in MR associated with egg production is small in relation to the birds' capacity to increase MR in response to other energetically demanding processes, the addition of egg production to these metabolically costly activities may be enough to necessitate the use of energy-saving strategies, such as internal energy reallocation, to cope with the additional energetic demands. DOI
112. Travers, M; Clinchy, M; Zanette, L; Boonstra, R; Williams, TD. (2010) Indirect predator effects on clutch size and the cost of egg production.Ecology Letters 13: 980-988 Indirect predator effects on clutch size and the cost of egg production
Clutch size; cost of reproduction; egg production; nest predation; non-consumptive effects; oxidative stress; predator-prey ecology
Predator-induced changes in physiology and behaviour may negatively affect a prey's birth rate. Evidence of such indirect predator effects on prey demography remains scarce in birds and mammals despite invertebrate and aquatic studies that suggest ignoring such effects risks profoundly underestimating the total impact of predators. We report the first experimental demonstration of indirect predator effects on the annual 'birth' rate resulting from negative effects on the size of subsequent clutches laid by birds. We manipulated the probability of nest predation and measured the size of subsequent clutches and multiple indices of the mother's physiological condition, while controlling for food availability, date and stage of breeding. Females subject to frequent experimental nest predation laid smaller subsequent clutches and were in poorer physiological condition, particularly regarding non-resource-based indices (e.g. oxidative stress and glucocorticoid mobilization) consistent with both a response to the threat of predation and an increased cost of egg production. DOI
110. Willie, J; Travers, M; Williams, TD. (2010) Female Zebra Finches (Taeniopygia guttata) Are Chronically but Not Cumulatively "Anemic" during Repeated Egg Laying in Response to Experimental Nest Predation.Physiological and Biochemical Zoology 83: 119-126 Female Zebra Finches (Taeniopygia guttata) Are Chronically but Not Cumulatively "Anemic" during Repeated Egg Laying in Response to Experimental Nest Predation
STARLING STURNUS-VULGARIS; HEMATOCRIT VALUES; BODY CONDITION; CLUTCH SIZE; DYNAMICS; SPARROWS; COSTS; MANIPULATIONS; REPEATABILITY; REPRODUCTION
Recently it has been recognized that reproduction itself, or the regulatory processes controlling reproduction, might contribute to physiological costs of reproduction. Reproductive anemia, a decrease in hematocrit and hemoglobin concentration, might provide one such mechanism underlying the costs of egg production in birds. In this study, we investigated the effect of repeated cycles of egg production in response to experimental nest predation (egg removal) on hematological traits in female zebra finches (Taeniopygia guttata). We predicted that if the negative effect of egg production on hematocrit and hemoglobin concentration was cumulative, with anemia being proportional to reproductive effort, then females laying more clutches, or laying successive clutches without recovery during incubation, would show greater reproductive anemia. In contrast, if females maintain hematocrit and hemoglobin concentration at some minimum functional level independent of reproductive effort, then there should be no difference in hematological traits among females laying two or more successive clutches. Our results supported the second of these hypotheses: egg-laying females had reduced hematocrit (-7.5%) and hemoglobin concentrations (-10%), but the extent of reproductive anemia did not differ among females laying either two or three successive clutches, with or without recovery during incubation, or in females laying 7-21 eggs. Females maintained low hematocrit and hemoglobin for 20-35 d, and we suggest that prolonged periods of anemia might be common and functionally important in free-living birds, for example, where females produce multiple successive clutches in response to high levels of nest predation or where they initiate a second clutch while still rearing first brood chicks. DOI
109. Caro, SP; Charmantier, A; Lambrechts, MM; Blondel, J; Balthazart, J; Williams, TD. (2009) Local adaptation of timing of reproduction: females are in the driver's seat.Functional Ecology 23: 172-179 Local adaptation of timing of reproduction: females are in the driver's seat
TITS PARUS-CAERULEUS; MEDITERRANEAN BLUE TITS; NON-PHOTOPERIODIC FACTORS; WHITE-CROWNED SPARROWS; 2 CORSICAN POPULATIONS; SONG CONTROL NUCLEI; EGG-PRODUCTION; PHENOTYPIC PLASTICITY; CLUTCH SIZE; GREAT TIT
Breeding at the right time of the year is crucial for many temperate zone organisms, as any mismatch with their optimal breeding period leads to a reduction in fitness. The roles of the breeding partners in these adaptive decisions have, however, only rarely been studied. In blue tits (Cyanistes caeruleus) that breed in heterogenous Mediterranean habitats, nearby populations show up to 1-month differences in breeding time. This difference is adaptive as the optimal time for breeding varies by the same amount due to habitat characteristics. But which sex is determining this large difference in timing? We show here that the seasonal development of female reproductive activity (yolk precursor production) closely matches the local optimal breeding time in these two highly contrasted landscapes, while previous studies have demonstrated that male gonadal development does not. In accordance with this, quantitative genetic analyses reveal that timing for breeding is determined by the female only, with no evidence for an additive genetic male effect on laying date. Our results strongly suggest that the adaptive inter-population difference in the laying periods has been driven by females. The central role of females in the determination of breeding period needs to be included when studying how micro-evolutionary processes are affected by global climate change. DOI
108. Chin, EH; Love, OP; Verspoor, JJ; Williams, TD; Rowley, K; Burness, G. (2009) Juveniles exposed to embryonic corticosterone have enhanced flight performance.Proceedings of the Royal Society B-Biological Sciences 276: 499-505 Juveniles exposed to embryonic corticosterone have enhanced flight performance
STURNUS-VULGARIS; ENZYME-ACTIVITIES; THYROID-HORMONES; MATERNAL STRESS; PREDATION RISK; BODY-MASS; TAKE-OFF; BIRDS; BEHAVIOR; ABILITY
Exposure to maternally derived glucocorticoids during embryonic development impacts offspring phenotype. Although many of these effects appear to be transiently 'negative', embryonic exposure to maternally derived stress hormones is hypothesized to induce preparative responses that increase survival prospects for offspring in low-quality environments; however, little is known about how maternal stress influences longer-term survival-related performance traits in free-living individuals. Using an experimental elevation of yolk corticosterone (embryonic signal of low maternal quality), we examined potential impacts of embryonic exposure to maternally derived stress on flight performance, wing loading, muscle morphology and muscle physiology in juvenile European starlings (Sturnus vulgaris). Here we report that fledglings exposed to experimentally increased corticosterone in ovo performed better during flight performance trials than control fledglings. Consistent with differences in performance, individuals exposed to elevated embryonic corticosterone fledged with lower wing loading and had heavier and more functionally mature flight muscles compared with control fledglings. Our results indicate that the positive effects on a survival-related trait in response to embryonic exposure to maternally derived stress hormones may balance some of the associated negative developmental costs that have recently been reported. Moreover, if embryonic experience is a good predictor of the quality or risk of future environments, a preparative phenotype associated with exposure to apparently negative stimuli during development may be adaptive. DOI
107. Gorman, KB; Esler, D; Walzem, RL; Williams, TD. (2009) Plasma Yolk Precursor Dynamics during Egg Production by Female Greater Scaup (Aythya marila): Characterization and Indices of Reproductive State.Physiological and Biochemical Zoology 82: 372-381 Plasma Yolk Precursor Dynamics during Egg Production by Female Greater Scaup (Aythya marila): Characterization and Indices of Reproductive State
LOW-DENSITY LIPOPROTEINS; GALLUS-DOMESTICUS; MARBLED MURRELET; OVARIAN-FOLLICLE; CLUTCH SIZE; LAYING HEN; VITELLOGENIN; HYPERLIPIDEMIA; MANIPULATION; LONGEVITY
We characterized dynamics of the plasma yolk precursors vitellogenin (VTG), very-low-density lipoprotein ( total VLDLTG), and VLDL particle size distribution during egg production by female greater scaup (order: Anseriformes, Aythya marila). We also evaluated VTG and total VLDL-TG as physiological indices of reproductive state. Mean (+/- 1 SE) plasma concentrations of VTG and total VLDL-TG for females with nondeveloped ovaries were 0.58 +/- 0.05 mu g Zn mL(-1) and 3.75 +/- 0.29 mmol TG L-1, respectively. Yolk precursor concentrations increased rapidly to maximum levels in association with small increases in ovary mass during rapid follicle growth. Mean concentrations of VTG and total VLDL- TG for females with a full ovarian follicle hierarchy were 3.38 +/- 0.40 mu g Zn m(-1) and mmol TG L-1, respectively. Concentrations of VTG 7.31 +/- 2.56 and total VLDL remained elevated throughout the laying cycle and decreased markedly by 3 d into incubation. Individual reproductive state (non-egg producing vs. egg producing) was more accurately identified by plasma profiles of VTG (90%) than by those of total VLDL-TG (74%). Greater scaup VLDL particle sizes during egg production were within the range for predicted yolk-targeted VLDL size (25-44 nm). We conclude that plasma profiles of VTG and total VLDL-TG can be used as nonlethal, physiological indices of reproductive state in greater scaup and should be of great utility to a variety of evolutionary, ecological, and applied conservation studies of reproduction in waterfowl. DOI
106. Han, D; Haunerland, NH; Williams, TD. (2009) Variation in yolk precursor receptor mRNA expression is a key determinant of reproductive phenotype in the zebra finch (Taeniopygia guttata).Journal of Experimental Biology 212: 1277-1283 Variation in yolk precursor receptor mRNA expression is a key determinant of reproductive phenotype in the zebra finch (Taeniopygia guttata)
LOW-DENSITY-LIPOPROTEIN; CHICKEN OOCYTE GROWTH; TISSUE-SPECIFIC EXPRESSION; STARLING STURNUS-VULGARIS; GENE FAMILY-MEMBER; VITELLOGENIN RECEPTOR; INDIVIDUAL VARIATION; INTERINDIVIDUAL VARIATION; ONCORHYNCHUS-MYKISS; OVARIAN-FOLLICLES
The vitellogenin/very low density lipoprotein receptor (VTG/VLDL-R), a 95 kDa protein that belongs to the low density lipoprotein receptor gene family, mediates the uptake of yolk precursors by developing follicles during oocyte growth. However, the extent to which variation in VTG/VLDL-R expression plays a role in determining inter-individual variation in reproductive phenotype ( e. g. follicle or egg size) is not known. Here we show that the mRNA sequence of the zebra finch (Taeniopygia guttata) VTG/VLDL-R shows a high degree of sequence identity (92%) with chicken VTG/VLDL-R mRNA. Using quantitative real-time PCR we measured transcriptional expression of VTG/VLDL-R mRNA in various tissues, and for different stages of oocyte growth, in individual female zebra finches. VTG/VLDL-R mRNA was expressed at high levels in vitellogenic oocytes and in skeletal muscle, and was also detectable in liver, but these tissues expressed different splice variants: the short-form LR8-in oocytes and liver, and the LR8+ form in skeletal muscle. There was significant temporal variation in VTG/VLDL-R expression during follicle growth, with highest levels in ovary and a gradual decrease from pre-F3 to F1 vitellogenic follicles. Variation in ovary mRNA expression was correlated with inter-individual variation in clutch size and laying interval. Furthermore, variation in F3 follicle VTG/VLDL-R mRNA expression was correlated with inter-individual variation in egg mass and F1 follicle mass, suggesting that VTG/VLDL receptor mRNA expression is a key determinant of inter-individual variation in reproductive phenotype. DOI
105. JANSSEN, M.H., ARCESE, P., KYSER, T.K., BERTRAM, D.F., MCFARLANE TRANQUILLA, L., WILLIAMS, T.D. & NORRIS, R.D. (2009) Pre-breeding diet, condition, and timing of breeding in a threatened seabird, the Marbled Murrelet Brachyramphus marmoratus.Marine Ornithology 37: 33-40.Pre-breeding diet, condition, and timing of breeding in a threatened seabird, the Marbled Murrelet Brachyramphus marmoratus.
Murrelets; Marbled Murrelets;
Marbled Murrelets Brachyramphus marmoratus are small, threatened seabirds that nest in old growth coniferous forests along the west coast of North America and spend most of their lives in nearshore waters. Recent evidence suggests that long term declines in pre-breeding trophic feeding level may be associated with reduced reproductive success. To test the hypothesis that pre-breeding trophic feeding level positively influences breeding success, we investigated relationships between timing of breeding, female body condition, and pre-breeding trophic feeding level. We predicted that females feeding on higher trophic level prey prior to breeding would be in better condition, and initiate egg production earlier, than females feeding on lower trophic level prey. Egg producing females were identified based on elevated yolk precursor (vitellogenin) levels, and diet composition was inferred using stable-carbon (δ13C) and -nitrogen (δ15N) analysis of murrelet and prey tissues during the pre-breeding seasons of 1999, 2000, 2006, and 2007 in Desolation Sound, British Columbia. Contrary to our predictions, females feeding on a higher proportion of low trophic level prey in 2007 were in better condition and more likely to produce an egg early in the breeding season. However, differences in pre-breeding diet between egg-producing females and non-egg producers were not consistent among years. Although our results suggest that low trophic level prey in pre-breeding diet promoted egg production and breeding success in 2007, this was likely not the case in others years studied. To reconcile results presented here and previous work on diet composition and breeding success in the Marbled Murrelet, we propose an alternative hypothesis of diet quality incorporating optimal foraging theory, whereby the net energy gain from feeding on a prey type is a function of its relative availability. PDF
104. Love, OP; Gilchrist, HG; Bety, J; Wynne-Edwards, KE; Berzins, L; Williams, TD. (2009) Using life-histories to predict and interpret variability in yolk hormones.General and Comparative Endocrinology 163: 169-174 Using life-histories to predict and interpret variability in yolk hormones
CORTICOSTERONE LEVELS; MATERNAL ANDROGENS; STRESS HORMONES; PASSERINE BIRDS; EVOLUTION; BENEFITS; EGGS; TESTOSTERONE; REPRODUCTION; INVESTMENT
Variation in yolk hormones is assumed to provide the plasticity necessary for mothers to individually optimize reproductive decisions via changes in offspring phenotype, the benefit being to maximise fitness. However, rather than routinely expecting adaptive variation within all species, the pattern and magnitude of yolk hormone deposition should theoretically relate to variation in life-histories. Here we present data on intra-clutch variation in yolk corticosterone in three species along a developmental continuum (European starling (Sturnus vulgaris): fully altricial; black guillemot (Cepphus grylle): semi-precocial; common eider (Somateria mollissima): fully precocial) to examine how and why variation in life-histories might relate to the evolution of variation in yolk steroids. Starlings and guillemots showed a significant increase in yolk corticosterone across the laying sequence; however, we found no pattern within eider clutches. Moreover, starlings showed the largest difference (94.6%) in yolk corticosterone between first- and last-laid eggs, whereas guillemots showed a moderate difference (58.9%). Despite these general species-specific patterns, individuals showed marked variation in the intra-clutch patterns of yolk corticosterone within each species indicating potential differences in intra-clutch flexibility among females. It is well documented that exposure to elevated yolk glucocorticoids reduces offspring quality at birth/hatching in many taxa and it has therefore been proposed that elevated yolk levels may modulate offspring competition and/or facilitate brood reduction under harsh conditions in birds. Our data suggests that intra-clutch variation in yolk corticosterone has the potential to act as an adaptive maternal effect in species where modulation of competition between nest-bound offspring would benefit mothers (starlings and guillemots). However, in precocial species where mothers would not benefit from a modulation of offspring quality, intra-clutch variation in yolk hormones may play little or no adaptive role. While future phylogenetically-controlled studies will be helpful in examining questions of adaptive mechanisms once more data on yolk corticosterone becomes available, our results nonetheless suggest that research on the evolutionary role of yolk hormones can benefit by a prior! incorporating species-specific life-history-driven hypotheses. (C) 2008 Elsevier Inc. All rights reserved. DOI
103. Vezina, F; Love, OP; Lessard, M; Williams, TD. (2009) Shifts in Metabolic Demands in Growing Altricial Nestlings Illustrate Context-Specific Relationships between Basal Metabolic Rate and Body Composition.Physiological and Biochemical Zoology 82: 248-257 Shifts in Metabolic Demands in Growing Altricial Nestlings Illustrate Context-Specific Relationships between Basal Metabolic Rate and Body Composition
AEROBIC PERFORMANCE VARIATION; ENERGY-EXPENDITURE; ORGAN MASSES; MUS MUSCULUS; PHALACROCORAX-ARISTOTELIS; PHENOTYPIC FLEXIBILITY; OXYGEN-CONSUMPTION; RESTING METABOLISM; POSTNATAL-GROWTH; CALIDRIS-CANUTUS
Basal metabolic rate (BMR) in animals is interpreted as reflecting the size and metabolic intensity of energy-consuming tissues. However, studies investigating relationships between the mass of specific organs and interindividual variation in BMR have produced inconsistent patterns with regard to which organs have the largest impact on BMR variation. Because of the known flexibility in organ mass and metabolic intensity within individual organs, relationships between BMR and body-composition variables are bound to be context specific. Altricial nestlings are excellent models to illustrate this phenomenon because of the extreme variation in body composition occurring during growth. Using European starlings at three age classes, we studied changes in body composition together with its effect on variation in resting metabolic rate (RMR) in order to highlight the context-specific nature of these relationships. Our data suggest a transition in metabolic costs during growth in starling nestlings. During the linear phase of growth, energy is mainly consumed by tissue-synthesis processes, with fast-growing organs having a large influence on RMR. In the plateau phase of growth, the energy expenditure is transferred to functional costs, with high-intensity organs having a predominant effect on RMR variation. Our data illustrates the context-specific nature of organ mass-metabolic rate correlations, which complicates inter- and intraspecific comparisons of BMR. In the future, such comparisons must be done while taking the physiological state of the study animal into account. DOI
102. Wada, H; Salvante, KG; Wagner, E; Williams, TD; Breuner, CW. (2009) Ontogeny and Individual Variation in the Adrenocortical Response of Zebra Finch (Taeniopygia guttata) Nestlings.Physiological and Biochemical Zoology 82: 325-331 Ontogeny and Individual Variation in the Adrenocortical Response of Zebra Finch (Taeniopygia guttata) Nestlings
CORTICOSTEROID-BINDING GLOBULIN; CROWNED SPARROW NESTLINGS; STRESS-RESPONSE; MATERNAL CORTICOSTERONE; PLASMA-CORTICOSTERONE; POSTNATAL-DEVELOPMENT; AMERICAN KESTRELS; BODY CONDITION; CHICKS; AGE
Numerous studies indicate interspecies variation in the ontogeny of the adrenocortical response in birds; however, little is known about the extent of interindividual variation in avian young. Toward this end, we examined the ontogeny and interindividual variation in the adrenocortical response in zebra finch (Taeniopygia guttata) nestlings. We measured baseline and stress-induced total (bound and free) corticosterone, corticosteroid binding globulin capacity, and resulting estimated free corticosterone levels in nestlings of four different ages ( days 5, 10, 16, and 21). In addition, we investigated the potential correlates of interindividual variation (brood size and mass). Nestlings at days 5 and 10 post-hatching showed no significant increase in total or free corticosterone levels in response to a standardized handling stress, whereas an adult-like stress response was seen by day 16 post-hatching. There was large interindividual (fivefold) variation in both baseline and stress-induced corticosterone among individual nestlings at any age. We estimate that half of this individual variation in the adrenocortical response could be explained by between-clutch variation (e.g., genetics), while the other half could be explained by other factors such as rearing environment (based on estimated intraclass correlation coefficients). Total baseline corticosterone, but not stress-induced corticosterone, was negatively correlated with fledging mass in this species. DOI
101.Williams, TD; Vezina, F; Speakman, JR. (2009) Individually variable energy management during egg production is repeatable across breeding attempts.Journal of Experimental Biology 212: 1101-1105 Individually variable energy management during egg production is repeatable across breeding attempts
DOUBLY-LABELED WATER; BASAL METABOLIC-RATE; KITTIWAKES RISSA-TRIDACTYLA; TIT PARUS-MAJOR; REPRODUCTIVE-PERFORMANCE; ZEBRA FINCHES; SMALL MAMMALS; MUS MUSCULUS; BODY-WATER; EXPENDITURE
It is axiomatic that whole-animal metabolism, measured for example as daily energy expenditure (DEE), plays a central role in determining reproductive success and survival (fitness) in all organisms. Nevertheless, strong evidence for consistent systematic relationships between DEE and either individual traits (age, sex, body size), environmental factors (e. g. food availability, temperature) or 'fitness' traits (e. g. number of offspring, survival) remains far from compelling in birds and mammals. Recently, we suggested that female birds might utilise complex, individually variable energy management strategies to meet the metabolic demands of reproduction, generating a wide spectrum of effects on reproductive DEE, from overcompensation (net decrease in DEE) to additive effects (net increase in DEE). Here we show that this individually variable adjustment or 'plasticity' in energy expenditure associated with egg production is repeatable among individuals between successive breeding attempts in female zebra finches (Taeniopygia guttata). Our study highlights the importance (a) of measuring 'plasticity' or change associated with transitions of physiological state (e. g. non-breeding to breeding) based on multiple measurements of the same individual, and (b) of extending consideration of how selection might drive the evolution of phenotypic plasticity per se to include physiological and metabolic traits. DOI
100. Albert, C; Williams, TD; Morrissey, CA; Lai, VWM; Cullen, WR; Elliott, JE. (2008) Tissue uptake, mortality, and sublethal effects of monomethylarsonic acid (MMA(V)) in nestling zebra finches (Taeniopygia guttata).Journal of Toxicology and Environmental Health-Part A-Current Issues 71: 353-360 Tissue uptake, mortality, and sublethal effects of monomethylarsonic acid (MMA(V)) in nestling zebra finches (Taeniopygia guttata)
Monosodium methanearsonate (MSMA), an arsenic-based pesticide, has been used since the mid 1980s in attempts to suppress mountain pine beetle (Dendroctonus ponderosae) outbreaks in British Columbia, Canada. It was previously shown that cavity nesting forest birds forage and breed in MSMA-treated pine stands. The present study was designed to investigate the effects of ecologically relevant oral exposure to MSMA, including tissue distribution, growth parameters, and general health, including survival and immune function, of a model passerine, the zebra finch (Taeniopygia guttata). Nestling finches were orally dosed for 20 d from hatching to fledging with 4, 8, 12, 24, 36, or 72 mu g/g bw/d of monomethylarsonic acid (MMA(V), which corresponds to MSMA at physiological pH). Preliminary trials showed complete mortality at 36 and 72 mu g/g bw/d, and repeat trials also resulted in high mortality at 24 mu g/g bw/d. Surviving nestlings showed dose-dependent trends in accumulation of arsenic in blood and specific tissues, and decreased tarsi and wing cord length upon fledging. There were no observed effects of dosing on measured immune function (phytohemagglutinin [PHA], hematocrit, and leukocrit). The data obtained suggest that passerine nestlings may be at risk of mortality and reduced growth due to exposure to MSMA under current environmental conditions. DOI
98. Bentzen, RL; Powell, AN; Williams, TD; Kitaysky, AS. (2008) Characterizing the nutritional strategy of incubating king eiders Somateria spectabilis in northern Alaska.Journal of Avian Biology 39: 683-690 Characterizing the nutritional strategy of incubating king eiders Somateria spectabilis in northern Alaska
We measured plasma concentrations of variables associated with lipid metabolism (free fatty acids, glycerol, triglyceride, and beta-hydroxybutyrate), protein metabolism (uric acid), and baseline corticosterone to characterize the nutritional state of incubating king eiders Somateria spectabilis and relate this to incubation constancy at two sites, Kuparuk and Teshekpuk, in northern Alaska. King eiders at both sites appeared to employ a partial-income incubation strategy, relying on both endogenous and exogenous energy resources. Females maintained high invariant levels of free fatty acids, beta-hydroxybutyrate, and glycerol throughout incubation, indicating that fat reserves were a major energy source, and not completely depleted during incubation. Similarly, uric acid did not increase, suggesting effective protein sparing or protein ingestion and adequate lipid reserves throughout incubation. Baseline corticosterone and triglyceride levels increased during incubation, indicative of an increase in foraging during late stages of incubation. Incubating females at Kuparuk had higher triglyceride concentrations but also had higher beta-hydroxybutyrate concentrations than females at Teshekpuk. This dichotomy may reflect a short-term signal of feeding overlaying the longer-term signal of reliance on endogenous lipid reserves due to higher food intake yet higher metabolic costs at Kuparuk because of its colder environment. Incubation constancy was not correlated with plasma concentrations of lipid or protein metabolites. DOI
97. Bond, JC; Esler, D; Williams, TD. (2008) Breeding propensity of female harlequin ducks.Journal of Wildlife Management 72: 1388-1393 Breeding propensity of female harlequin ducks
breeding propensity; Histrionicus histrionicus; nonbreeders; radiotelemetry; vitellogenin; yolk precursors
Breeding propensity, the proportion of sexually mature females that initiate egg production, can be an important demographic trait when considering reproductive performance and, subsequently, population dynamics in birds. We measured egg production using yolk precursor (vitellogenin andvery-low-density lipoprotein) analyses and we measured nesting using radiotelemetry to quantify breeding propensity of adult female harlequin ducks (Histrionicus histrionicus) in British Columbia, Canada, in 2003 and 2004. Using both methods combined, and accounting for error rates of each, we estimated that breeding propensity of adult females that migrated to breeding streams was 92%. These data suggest that, despite speculation that harlequin ducks have low breeding propensity, almost all adult females on our study site were not constrained in their ability to produce eggs and that influences on reproductive performance at later stages likely have much stronger effects on population dynamics. DOI
96. Cesh, LS; Williams, TD; Garcelon, DK; Elliott, JE. (2008) Patterns and trends of chlorinated hydrocarbons in nestling bald eagle (Haliaeetus leucocephalus) plasma in British Columbia and southern California.Archives of Environmental Contamination and Toxicology 55: 496-502 Patterns and trends of chlorinated hydrocarbons in nestling bald eagle (Haliaeetus leucocephalus) plasma in British Columbia and southern California
Patterns and trends of chlorinated hydrocarbons were assessed in bald eagle nestling plasma from sites along the west coast of North America. Eagle plasma was sampled from four areas in southwestern British Columbia (BC), a reference site in northern BC, and from Santa Catalina Island, off the coast of California. Sites were chosen to reflect variation in contaminant exposure due to differing recent and/or historic anthropogenic activities. Santa Catalina Island had significantly greater mean concentrations of p,p'-DDE, 41.3 mu g/kg wet weight (ww), than other sites, and Nanaimo/Crofton, BC had the greatest mean concentration of total PCBs, 28.9 mu g/kg ww. Contaminant levels measured in 2003 in BC were compared to levels measured in 1993; over that ten year span, concentrations and patterns of chlorinated hydrocarbons have not significantly changed. There were no significant differences in levels of p,p'-DDE or hexachlorobenzene between 1993 and 2003, but significant decreases were found for trans-nonachlor and PCBs at BC sites. Levels of total PCBs and trans-nonachlor in the central Fraser Valley and Nanaimo/Crofton area have significantly decreased. Mean concentrations of p,p'-DDE measured in bald eagle nestling plasma samples in 2003 exceeded published criteria for effects on bald eagle reproduction at Santa Catalina Island and Barkley Sound, more than 30 years since heavy usage restrictions were imposed. DOI
95. Gorman, K.B., D. Esler, P.L. Flint and T.D. Williams. (2008) Nutrient-reserve dynamics during egg production by female Greater Scaup (Aythya marila): relationships with timing of reproduction.Auk 125: 384-394. Nutrient-reserve dynamics during egg production by female Greater Scaup (Aythya marila): relationships with timing of reproduction.
We studied nutrient-reserve dynamics of female Greater Scaup (Aythya marila) to quantify intraspecific strategies of
nutrient acquisition for egg production, particularly in relation to the seasonal timing of reproduction (i.e., date of initiation of rapid follicle
growth [RFG]). We collected female Greater Scaup on the Yukon-Kuskokwim Delta, Alaska, from arrival through clutch formation during
the 2002 and 2003 breeding seasons, and we subsequently conducted standard proximate body-composition analysis. Endogenous lipid,
protein, and mineral reserve levels did not decline during egg production. This result differs from most other nutrient-reserve studies of
waterfowl, suggesting that female Greater Scaup rely on exogenous food resources, rather than endogenous nutrient reserves, to meet
the energy and nutrient costs of clutch formation. Furthermore, endogenous nutrient-reserve levels did not decline with date of RFG
initiation, which indicates that body condition at initiation of egg production was similar across the nesting season. We found evidence
of nutrient-reserve thresholds for initiation of RFG, in that lipid, protein, and mineral reserves were smaller in nonreproductive than
in reproductive females. In light of recent conservation concerns over declining North American scaup populations, our data contrast
with nutrient-reserve dynamics described for Lesser Scaup (A. affinis).PDF
94. Love, OP; Salvante, KG; Dale, J; Williams, TD. (2008) Specific variability in the immune system across life-history stages.American Naturalist 172: E99-E112 Specific variability in the immune system across life-history stages
cell-mediated immunity; life-history theory; sex-specific differences; individual variation; repeatability; zebra finch (Taeniopygia guttata)
Organisms theoretically manage their immune systems optimally across their life spans to maximize fitness. However, we lack information on ( 1) how the immune system is managed across life-history stages, ( 2) whether the sexes manage immunity differentially, and ( 3) whether immunity is repeatable within an individual. We present a within-individual, repeated-measures experiment examining life-history stage variation in the inflammatory immune response in the zebra finch (Taeniopygia guttata). In juveniles, age-dependent variation in immune response differed in a sex-and context-specific manner, resulting in no repeatability across stages. In adults, females displayed little stage-dependent variation in immune response when laying while receiving a high-quality ( HQ) diet; however, laying while receiving a low-quality (LQ) diet significantly reduced both immune responses and reproductive outputs in amanner consistent with a facultative (resource-driven) effect of reproduction on immunity. Moreover, a reduced immune response in females who were raising offspring while receiving an HQ diet suggests a residual effect of the energetic costs of reproduction. Conversely, adult males displayed no variation in immune responses across stages, with high repeatability from the nonbreeding stage to the egg-laying stage, regardless of diet quality ( HQ diet,; LQ diet,). r = 0.51 r = 0.42 Females displayed high repeatability when laying while receiving the HQ diet (r = 0.53); however, repeatability disappeared when individuals received the LQ diet. High-response females receiving the HQ diet had greater immune flexibility than did low-response females who were laying while receiving the LQ diet. Data are consistent with immunity being a highly plastic trait that is sex-specifically modulated in a context-dependent manner and suggest that immunity at one stage may provide limited information about immunity at future stages. DOI
93. Love, OP; Williams, TD. (2008) The adaptive value of stress-induced phenotypes: Effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness.American Naturalist 172: E135-E149 The adaptive value of stress-induced phenotypes: Effects of maternally derived corticosterone on sex-biased investment, cost of reproduction, and maternal fitness
yolk corticosterone; maternal effects; sex allocation; cost of reproduction; plasticity; maternal fitness
The question of why maternal stress influences offspring phenotype is of significant interest to evolutionary physiologists. Although embryonic exposure to maternally derived glucocorticoids (i.e., corticosterone) generally reduces offspring quality, effects may adaptively match maternal quality with offspring demand. We present results from an interannual field experiment in European starlings (Sturnus vulgaris) designed explicitly to examine the fitness consequences of exposing offspring to maternally derived stress hormones. We combined a manipulation of yolk corticosterone (yolk injections) with a manipulation of maternal chick-rearing ability (feather clipping of mothers) to quantify the adaptive value of corticosterone-induced offspring phenotypes in relation to maternal quality. We then examined how corticosterone-induced "matching" within this current reproductive attempt affected future fecundity and maternal survival. First, our results provide support that low-quality mothers transferring elevated corticosterone to eggs invest in daughters as predicted by sex allocation theory. Second, corticosterone-mediated sex-biased investment resulted in rapid male-biased mortality resulting in brood reduction, which provided a better match between maternal quality and brood demand. Third, corticosterone-mediated matching reduced investment in current reproduction for low-quality mothers, resulting in fitness gains through increased survival and future fecundity. Results indicate that the transfer of stress hormones to eggs by low-quality mothers can be adaptive since corticosterone-mediated sex-biased investment matches the quality of a mother to offspring demand, ultimately increasing maternal fitness. Our results also indicate that the branding of the proximate effects of maternal glucocorticoids on offspring as negative ignores the possibility that short-term phenotypic changes may actually increase maternal fitness. DOI
92. Love, OP; Williams, TD. (2008) Plasticity in the adrenocortical response of a free-living vertebrate: The role of pre- and post-natal developmental stress.Hormones and Behavior 54: 496-505 Plasticity in the adrenocortical response of a free-living vertebrate: The role of pre- and post-natal developmental stress
corticosterone; stress response; maternal effects; yolk hormones; body condition; predictive adaptive responses; developmental plasticity
Optimal functioning of the hypothalamo-pituitary-adrenal (HPA) axis is paramount to maximizing fitness in vertebrates. Research in laboratory mammals has suggested that maternally-induced stress can cause significant variation in the responsiveness of an offspring's HPA axis involving both pre- and post-natal developmental mechanisms. However, very little is known regarding effects of maternal stress on the variability of offspring adrenocortical functioning in free-living vertebrates. Here we use an experimental approach that independently lowers the quality of both the pre- and post-natal developmental environment to examine programming and plasticity in the responsiveness of the HPA axis in fledglings of a free-living passerine, the European starling (Sturnus vulgaris). We found that mimicking a hormonal signal of poor maternal condition via an experimental prenatal increase in yolk corticosterone decreased the subsequent responsiveness of the HPA axis in fledglings. Conversely, decreasing the quality of the post-natal developmental environment (by decreasing maternal provisioning capability via a maternal feather-clipping manipulation) increased subsequent responsiveness of the HPA axis in fledglings, apparently through direct effects on nestling body condition. The plasticity of these responses was sex-specific with smaller female offspring showing the largest increase in HPA reactivity. We suggest that pre-natal, corticosterone-induced, plasticity in the HPA axis may be a 'predictive adaptive response' (PAR): a form of adaptive developmental plasticity where the advantage of the induced phenotype is manifested in a future life-history stage. Further, we introduce a new term to define the condition-driven post-natal plasticity of the HPA axis to an unpredictable post-natal environment, namely a 'reactive adaptive response' (RAR). This study confirms that the quality of both the pre- and post-natal developmental environment can be a significant source of variation in the responsiveness of the HPA axis, and provides a frame-work for examining ecologically-relevant sources of stress-induced programming and plasticity in this endocrine system in a free-living vertebrate, respectively. (C) 2008 Elsevier Inc. All rights reserved. DOI
91. Love, OP; Wynne-Edwards, KE; Bond, L; Williams, TD. (2008) Determinants of within- and among-clutch variation in yolk corticosterone in the European starling.Hormones and Behavior 53: 104-111 Determinants of within- and among-clutch variation in yolk corticosterone in the European starling
corticosterone; yolk hormones; maternal effects; nesting density; maternal condition; laying order; European starling (Sturnus vulgaris)
Maternal glucocorticoids are known to affect offspring phenotype in numerous vertebrate taxa. In birds, the maternal transfer of corticosterone to eggs was recently proposed as a hormonal mechanism by which offspring phenotype is matched to the relative quality of the maternal environment. However, current hypotheses lack supporting information on both intra- and inter-clutch variation in yolk corticosterone for wild birds. As such, we examined variation in yolk corticosterone levels in a wild population of European starlings (Sturnus vulgaris). Maternal condition, clutch size and nesting density were all negatively related to yolk conicosterone deposition, females with high condition indices, those laying larger clutches and those nesting in high-density associations deposited lower amounts of the lion-none into eggs than those with low condition indices, laying small clutches and nesting in isolation. Alternatively, we found no effects of maternal age or human disturbance on yolk corticosterone deposition. Intra-clutch variation of yolk corticosterone was significant, with levels increasing across the laying sequence in all clutch sizes examined, with the difference between first and last-laid eggs being greater in large versus small clutches. Given the reported effects of yolk corticosterone on offspring size and growth, intra-clutch variation in yolk corticosterone has the potential to alter the competitive environment within a brood. Furthermore, our results indicate that variation in yolk corticosterone can originate from variation in both the mother's quality as well as the quality of her breeding environment. The presence of inter-female variation in particular is an important pre-requisite in testing whether the exposure of offspring to maternally-derived corticosterone is a mechanistic link between offspring phenotypic plasticity and maternal quality. (c) 2007 Elsevier Inc. All rights reserved. DOI
90. Pomeroy, A.C., D.A. Acevedo Seaman, R.W. Butler, R.W. Elner, T.D. Williams and R.C. Ydenberg. (2008) Feeding-danger tradeoffs underlie stopover site selection by migrants.Avian Conservation and Ecology - Écologie et Conservation des Oiseaux 3(1): 7 Feeding-danger tradeoffs underlie stopover site selection by migrants.
To migrate successfully, birds need to store adequate fat reserves to fuel each leg of the journey. Migrants acquire their fuel reserves at stopover sites; this often entails exposure to predators. Therefore, the safety attributes of sites may be as important as the feeding opportunities. Furthermore, site choice might depend on fuel load, with lean birds more willing to accept danger to obtain good feeding. Here, we evaluate the factors underlying stopover-site usage by migrant Western Sandpipers (Calidris mauri) on a landscape scale. We measured the food and danger attributes of 17 potential stopover sites in the Strait of Georgia and Puget Sound region. We used logistic regression models to test whether food, safety, or both were best able to predict usage of these sites by Western Sandpipers. Eight of the 17 sites were used by sandpipers on migration. Generally, sites that were high in food and safety were used, whereas sites that were low in food and safety were not. However, dangerous sites were used if there was ample food abundance, and sites with low food abundance were used if they were safe. The model including both food and safety best-predicted site usage by sandpipers. Furthermore, lean sandpipers used the most dangerous sites, whereas heavier birds (which do not need to risk feeding in dangerous locations) used safer sites. This study demonstrates that both food and danger attributes are considered by migrant birds when selecting stopover sites, thus both these attributes should be considered to prioritize and manage stopover sites for conservation.Website
89. Pomeroy, AC; Seaman, DAA; Butler, RW; Elner, RW; Williams, TD; Ydenberg, RC. (2008) Feeding-Danger Trade-Offs Underlie Stopover Site Selection by Migrants.Avian Conserv. Ecol. 3 Feeding-Danger Trade-Offs Underlie Stopover Site Selection by Migrants
Calidris mauri; food abundance; migration; predation danger; stopover site conservation; trade-off hypothesis; Western Sandpiper
To migrate successfully, birds need to store adequate fat reserves to fuel each leg of the journey. Migrants acquire their fuel reserves at stopover sites; this often entails exposure to predators. Therefore, the safety attributes of sites may be as important as the feeding opportunities. Furthermore, site choice might depend on fuel load, with lean birds more willing to accept danger to obtain good feeding. Here, we evaluate the factors underlying stopover-site usage by migrant Western Sandpipers (Calidris mauri) on a landscape scale. We measured the food and danger attributes of 17 potential stopover sites in the Strait of Georgia and Puget Sound region. We used logistic regression models to test whether food, safety, or both were best able to predict usage of these sites by Western Sandpipers. Eight of the 17 sites were used by sandpipers on migration. Generally, sites that were high in food and safety were used, whereas sites that were low in food and safety were not. However, dangerous sites were used if there was ample food abundance, and sites with low food abundance were used if they were safe. The model including both food and safety best-predicted site usage by sandpipers. Furthermore, lean sandpipers used the most dangerous sites, whereas heavier birds (which do not need to risk feeding in dangerous locations) used safer sites. This study demonstrates that both food and danger attributes are considered by migrant birds when selecting stopover sites, thus both these attributes should be considered to prioritize and manage stopover sites for conservation.
88. Wada, H; Salvante, KG; Stables, C; Wagner, E; Williams, TD; Breuner, CW. (2008) Adrenocortical responses in zebra finches (Taeniopygia guttata): Individual variation, repeatability, and relationship to phenotypic quality.Hormones and Behavior 53: 472-480 Adrenocortical responses in zebra finches (Taeniopygia guttata): Individual variation, repeatability, and relationship to phenotypic quality
adrenocortical response; individual variation; phenotypic quality; Theniopygia guttata
Although individual variation is a key requirement for natural selection, little is known about the magnitude and patterns of individual variation in endocrine systems or the functional significance of that variation. Here we describe (1) the extent and repeatability of inter-individual variation in adrenocortical responses and (2) its relationship to sex-specific phenotypic quality, such as song duration and frequency and timing of egg laying. We measured adrenocortical responses to a standardized stressor in zebra finches (Taeniopygia guttata) at two life history stages: similar to day 16 (nestlings) and 3 months of age (sexually mature adults). Subsequently, we assessed phenotypic (reproductive) quality of all individuals as adults. Marked inter-individual variation in the adrenocortical response was seen in both sexes and ages, e.g., stress-induced corticosterone ranged from 2.2 to 62.5 ng/mL in nestlings and 5.0-64.0 ng/mL in adults. We found sex differences in (a) inter-individual variation in the adrenocortical response, (b) repeatability, and (c) relationships between corticosterone levels and phenotypic quality. In males, variation in nestling corticosterone was weakly but positively correlated with brood size and negatively correlated with nestling mass (though this relationship was dependent on one individual). There was no significant correlation of adrenocortical responses between two stages in males and adult phenotypic quality was significantly correlated only with adult corticosterone levels. In contrast, in females there was no relationship between nestling corticosterone and brood size or mass but adrenocortical response was repeatable between two stages (r(2) =0.413). Phenotypic quality of adult females was correlated with nestling baseline and adrenocortical response. (c) 2008 Elsevier Inc. All rights reserved. DOI
87. Wagner, EC; Prevolsek, JS; Wynne-Edwards, KE; Williams, TD. (2008) Hematological changes associated with egg production: estrogen dependence and repeatability.Journal of Experimental Biology 211: 400-408 Hematological changes associated with egg production: estrogen dependence and repeatability
hematocrit; cost of reproduction; egg production; erythropoiesis; estrogen; zebra finch
The. cost of reproduction' (i.e. the trade-off between current reproduction and future fecundity and/or survival) is a central concept in life history theory, yet we still know very little about the physiological mechanisms underlying such costs. Recently it has been recognized that reproduction itself or the regulatory ( hormonal) mechanisms underlying reproduction might result in. costs' (cf. resource-allocation based mechanisms). As one example, it has been suggested that the decrease in hematocrit observed during egg production in birds might be due to antagonistic pleiotropic effects of estrogens. This could generate costs of reproduction by reducing oxygen-carrying capacity during subsequent aerobically demanding stages such as chick-provisioning. Here we show that the reduction in hematocrit during egg-laying is dependent on receptor-mediated actions of endogenous estrogens: blocking estrogen receptors using the anti-estrogen tamoxifen reduces the decrease in hematocrit during egg production in female zebra finches (Taeniopygia guttata) such that hematocrit at the 1-egg stage is not significantly different than pre-breeding, baseline values. We also show that both pre-breeding hematocrit and the decrease in hematocrit associated with egg production are repeatable, and that females with the highest pre- breeding hematocrit values tend to show the largest decreases in hematocrit during egg production. We suggest that hematological changes during egg production are a good candidate mechanism for a regulatory-network based trade-off involving antagonistic pleiotropic effects of estrogens, which otherwise have essential reproductive functions. DOI
86. Wagner, EC; Stables, CA; Williams, TD. (2008) Hematological changes associated with egg production: direct evidence for changes in erythropoiesis but a lack of resource dependence?Journal of Experimental Biology 211: 2960-2968 Hematological changes associated with egg production: direct evidence for changes in erythropoiesis but a lack of resource dependence?
anemia; cost of reproduction; egg production; erythropoiesis; estrogen; zebra finch
Reductions in hematological parameters among laying birds are well reported, but the cause of this anemia is not known. We tested specific predictions generated from several, non-mutually exclusive hypotheses for mechanisms underlying reproductive anemia associated with egg production (hemodilution, transient suppression of erythropoiesis, resource dependence) in relation to (1) the time-course of development and recovery from anemia, (2) changes in specific hematological traits, and (3) the effect of diet quality, in female zebra finches (Taeniopygia guttata). Female zebra finches showed marked decreases in hematocrit (similar to 6%), red blood cell counts (similar to 8%), and plasma hemoglobin concentration (similar to 9%) during egg production, even on a high-quality ad libitum diet, consistent with an effect of hemodilution associated with yolk precursor production. However, our results provide strong support for the hypothesis that erythropoiesis is transiently suppressed during egg-laying and that the recovery from anemia is relatively long-lasting, extending through incubation and hatching periods. Decreased hematocrit, red blood cell counts, and hemoglobin concentration did not recover at clutch completion, but showed evidence of recovery to baseline pre-breeding levels at hatching. More importantly, there was significant time-dependent variation in the proportion of reticulocytes, which increased at clutch completion but peaked at hatching 10-12 days after clutch completion, and in mean red blood cell volume, which showed a significant increase at clutch completion; consistent with enhanced production and release of larger immature cells into the circulation following suppression of erythropoiesis. Finally, we found no evidence for resource dependence of anemia associated with egg production in relation to diet quality, i.e. exogenous lipid and protein resources available to the laying female. This study demonstrates that transient suppression of erythropoiesis and, subsequently, increased reticulocytosis, are key components of reproductive anemia in egg-laying females. DOI
85.Williams, TD. (2008) Individual variation in endocrine systems: moving beyond the 'tyranny of the Golden Mean'.Philosophical Transactions of the Royal Society B-Biological Sciences 363: 1687-1698 Individual variation in endocrine systems: moving beyond the 'tyranny of the Golden Mean'
endocrine systems; inter-individual variation; reaction norms; heritability; plasticity
Twenty years ago, Albert Bennett published a paper in the influential book New directions in ecological physiology arguing that individual variation was an 'underutilized resource'. In this paper, I review our state of knowledge of the magnitude, mechanisms and functional significance of phenotypic variation, plasticity and flexibility in endocrine systems, and argue for a renewed focus on inter-individual variability. This will provide challenges to conventional wisdom in endocrinology itself, e. g. re-evaluation of relatively simple, but unresolved questions such as structure-function relationships among hormones, binding globulins and receptors, and the functional significance of absolute versus relative hormone titres. However, there are also abundant opportunities for endocrinologists to contribute solid mechanistic understanding to key questions in evolutionary biology, e. g. how endocrine regulation is involved in evolution of complex suites of traits, or how hormone pleiotropy regulates trade-offs among life-history traits. This will require endocrinologists to embrace the raw material of adaptation (heritable, individual variation and phenotypic plasticity) and to take advantage of conceptual approaches widely used in evolutionary biology (selection studies, reaction norms, concepts of evolutionary design) as well as a more explicit focus on the endocrine basis of life-history traits that are of primary interest to evolutionary biologists (cf. behavioural endocrinology). DOI
84. Wingfield, JC; Visser, ME; Williams, TD. (2008) Introduction. Integration of ecology and endocrinology in avian reproduction: a new synthesis.Philosophical Transactions of the Royal Society B-Biological Sciences 363: 1581-1588 Introduction. Integration of ecology and endocrinology in avian reproduction: a new synthesis
ecology; endocrinology; evolution; global warming; climate change; maternal effects
Birds are some of the most familiar organisms of global ecosystems. Changes in the visibility and abundance of birds are therefore excellent indicators of population and physiological responses to habitat changes and are a major focus for public concern about detrimental environmental changes. In order to understand how birds respond to these challenges, it is essential to determine how the environment affects reproduction under natural conditions. The continuum from environmental variables (cues) to reproductive life-history traits depends upon a cascade of neural and physiological processes that determine the extent and rate at which birds will be able to adapt to changes in their environment. For a full understanding of this ability to adapt, ecologists and endocrinologists need to collaborate and build a common framework. The objective of this theme issue is to bring together a series of papers addressing how evolutionary ecologists and endocrinologists can collaborate directly using avian reproduction as a model system. First, we address the need to integrate ecology and endocrinology and what benefits to biological knowledge will be gained. The papers collected in this issue represent a new synthesis of ecology and endocrinology as discussed in three E-BIRD workshops. The three main foci are trade-offs and constraints, maternal effects and individual variation. Authors within each group present ecological and endocrinological aspects of their topics and many go on to outline testable hypotheses. Finally, we discuss where the major problems remain and how this issue points out where these need collaborative efforts of ecologists and endocrinologists. Specific challenges are raised to future researchers to break through intellectual barriers and explore new frontiers. This framework of topics will ultimately apply to all taxa because the principles involved are universal and hopefully will have direct application to programmes integrating organisms and genes throughout biological sciences. DOI
83. Gorman, KB; Flint, PL; Esler, D; Williams, TD. (2007) Ovarian follicle dynamics of female Greater Scaup during egg production.Journal of Field Ornithology 78: 64-73 Ovarian follicle dynamics of female Greater Scaup during egg production
Studies of female waterfowl nutrient reserve use during egg production require a precise understanding of ovarian follicle dynamics to correctly interpret breeding status, and, therefore, derive proper inference. Concerns over numerical declines of North American scaup have increased the need to better understand the role of female condition in reproductive performance. We quantified ovarian follicle dynamics of female Greater Scaup (Aythya marila) breeding on the Yukon-Kuskokwim Delta, Alaska, using a method that accounts for within day variation in follicle size. We considered several models for describing changes in follicle growth with the best supported model estimating the duration of rapid follicle growth (RFG) to be 5.20 +/- 0.52 days (+/- 95% confidence intervals) for each developing follicle. Average diameter and dry mass of preovulatory follicles were estimated to be 9.36 mm and 0.26 g, respectively, at the onset of RFG, and these follicle characteristics were 41.47 mm and 15.57 g, respectively, at ovulation. The average diameter of postovulatory follicles immediately following ovulation was estimated to be 17.35 mm, regressing quickly over several days. In addition, we derived predictive equations using diameter and dry mass to estimate the number of days before, and after, ovulation for pre- and postovulatory follicles, as well as an equation to estimate dry mass of damaged follicles. Our results allow precise definition of RFG and nest initiation dates, clutch size, and the daily energetic and nutritional demands of egg production at the individual level. This study provides the necessary foundation for additional work on Greater Scaup reproductive energetics and physiology, and offers an approach for quantifying ovarian follicle dynamics in other species.
81. Rowland, E; Love, OP; Verspoor, JJ; Sheldon, L; Williams, TD. (2007) Manipulating rearing conditions reveals developmental sensitivity in the smaller sex of a passerine bird, the European starling Sturnus vulgaris.Journal of Avian Biology 38: 612-618 Manipulating rearing conditions reveals developmental sensitivity in the smaller sex of a passerine bird, the European starling Sturnus vulgaris
Traditionally, studies of sexually size-dimorphic birds and mammals report that the larger sex is more sensitive to adverse environmental conditions during ontogeny. However, recent studies in avian species that exhibit moderate size-dimorphism indicate that the smaller sex may be more sensitive to poor rearing conditions. To better understand sex-specific sensitivity in a passerine exhibiting moderate size-dimorphism, we examined growth, cell-mediated immunity (CMI) and survival of European starling Sturnus vulgaris nestlings following an experimental reduction of maternal rearing ability (via a feather-clipping manipulation). Contrary to conventional theory, daughters showed reduced growth in both body mass and measures of structural size in response to the maternal treatment. In contrast, sons showed no reductions in any of these traits in relation to the treatment. No sex-specific differences in nestling CMI were found for either group, although CMI of nestlings raised by manipulated mothers were higher than those of control nestlings. Finally, fledging sex ratios did not change from those at hatching indicating that neither sex appeared differentially sensitive to the maternal treatment in terms of mortality. These results reveal that variation in the quality of the rearing environment can have significant effects on the smaller sex of a passerine exhibiting moderate dimorphism and as such support recent studies of species with small-moderate sexual size-dimorphism. Combined results suggest that sex-specific effects of environmental variation on nestling development may be both context- (i.e., brood size, resource level, hatching order) and temporally- (when during development they occur) specific. Furthermore, more studies are needed that examine multiple traits at several developmental stages and then follow the sexes over the longer-term to examine potential effects on fitness. DOI
80. Salvante, KG; Lin, G; Walzem, RL; Williams, TD. (2007) Characterization of very-low density lipoprotein particle diameter dynamics in relation to egg production in a passerine bird.Journal of Experimental Biology 210: 1064-1074 Characterization of very-low density lipoprotein particle diameter dynamics in relation to egg production in a passerine bird
VLDL; yolk-targeted VLDL; reproduction; VLDL particle diameter; zebra finch
During avian egg production, oestrogen mediates marked increases in hepatic lipid production and changes in the diameter of assembled very-low density lipoprotein (VLDL). A nearly complete shift from generic VLDL (similar to 70 nm in diameter), which transports lipids to peripheral tissues, to yolk-targeted VLDL (VLDLy) (similar to 30 nm), which supplies the yolk with energy-rich lipid, has been observed in the plasma of laying domestic fowl. We validated an established dynamic laser scattering technique for a passerine songbird Taeniopygia guttata, the zebra finch, to characterize the dynamics of VLDL particle diameter distribution in relation to egg production. We predicted that non-gallinaceous avian species that have not been selected for maximum egg production would exhibit less dramatic shifts in lipid metabolism during egg production. As predicted, there was considerable overlap between the VLDL particle diameter distributions of laying and nonlaying zebra finches. But unexpectedly, non-laying zebra finches had VLDL diameter distributions that peaked at small particles and had relatively few large VLDL particles. As a result, laying zebra finches, in comparison, had diameter distributions that were shifted towards larger VLDL particles. Nevertheless, laying zebra finches, like laying chickens, had larger proportions of particles within proposed VLDLy particle diameter ranges than non-laying zebra finches (e.g. sVLDLy: 50% vs 37%). Furthermore, zebra finches and chickens had similar modal (29.7 nm in both species) and median (32.7 nm vs 29.6 nm) VLDL particle diameters during egg production. Therefore, although zebra finches and chickens exhibited opposing directional shifts in VLDL particle diameter distribution during egg production, the modifications to VLDL particle structure in both species resulted in the realization of a common goal, i.e. to produce and maintain a large proportion of small VLDL particles of specific diameters that are capable of being incorporated into newly forming egg yolks. DOI
79. Salvante, KG; Walzem, RL; Williams, TD. (2007) What comes first, the zebra finch or the egg: temperature-dependent reproductive, physiological and behavioural plasticity in egg-laying zebra finches.Journal of Experimental Biology 210: 1325-1334 What comes first, the zebra finch or the egg: temperature-dependent reproductive, physiological and behavioural plasticity in egg-laying zebra finches
temperature; egg production; lipid allocation; very low density lipoprotein (VLDL); food intake; zebrafinch; chicken
Avian reproduction is generally timed to synchronize chick-rearing with periods of increased food abundance. Consequently, the energetically demanding period of egg production may coincide with periods of lower food availability, fluctuating temperature and more unstable weather. Little is known about the physiological mechanisms underlying temperature-induced variation in egg production. We therefore examined the influence of low ambient temperature (7 degrees C vs 21 degrees C) on reproductive output (e.g. egg mass, clutch size, laying interval, laying rate), daily food consumption and lipid variables in zebra finches Taeniopygia guttata. When faced with egg production at 7 degrees C, laying zebra finches increased energy intake by 12.67 kJ day(-1), and were thus able to maintain body condition (e.g. body mass, fat and muscle score) and circulating triacylglyceride at levels comparable to those at 21 degrees C. However, when producing eggs at 7 degrees C, females took longer to initiate egg laying (6.5 vs 6.1 days at 21 degrees C), and ultimately laid fewer eggs (5.5 vs 6.0 eggs) at a slower rate (0.90 eggs day(-1) vs 0.95 eggs day(-1)). These temperature-related declines in reproductive output were accompanied by decreases in modal (from 36.6 at 21 degrees C to 24.3 nm at 7 degrees C) and median very low density lipoprotein (VLDL) particle diameter (from 29.6 to 26.4 nm) and in the proportion of VLDL particles that were capable of passing through the pores in the ovary to access the developing ovarian follicles (i.e. particles with diameters between 25 and 44 nm; from 45.90% to 32.55%). However, variation in reproductive output was not related to any static concentration or structural measure of VLDL. Therefore, other temperature-dependent mechanisms must be involved in the physiological processes that regulate reproductive output of passerine birds at low ambient temperatures. DOI
78. Verspoor, JJ; Love, OP; Rowland, E; Chin, EH; Williams, TD. (2007) Sex-specific development of avian flight performance under experimentally altered rearing conditions.Behavioral Ecology 18: 967-973 Sex-specific development of avian flight performance under experimentally altered rearing conditions
development; escape performance; european starling; flight ability; predation risk; sexual size dimorphism
Numerous studies have examined predation risk resulting from the costs of impaired flight performance associated with many key life-history stages such as reproduction and migration. Interestingly, although avian nestlings experience multiple resource-based physiological trade-offs and undergo considerable morphological and physiological changes during postnatal development, there is no data available on how nestlings manage the competing demands of growth and the development of flight ability at this critical life-history stage. We examined numerous morphological traits to determine which are responsible for variation in flight performance in juvenile European starlings (Sturnus vulgaris), a sexually size-dimorphic passerine. We then manipulated maternal quality during chick rearing (via feather clipping) to examine sex-specific sensitivity of fledgling flight performance to the quality of the rearing environment. Results suggest that the mechanics underlying variation in juvenile flight performance are relatively simple, being principally determined by the ratio of pectoral muscle mass to body mass (BM) and the surface area of the wings. Interestingly, although the maternal quality manipulation decreased BM and structural size in daughters, only the flight performance of sons was negatively affected. Our results suggest that a survival-related trait can be significantly affected in the larger sex when raised under stressful conditions. Furthermore, measuring only BM and structural size may not be sufficient in understanding how the sexes are affected by stressful rearing conditions in sexually size-dimorphic species. DOI
77. Wagner, EC; Williams, TD. (2007) Experimental (antiestrogen-mediated) reduction in egg size negatively affects offspring growth and survival.Physiological and Biochemical Zoology 80: 293-305 Experimental (antiestrogen-mediated) reduction in egg size negatively affects offspring growth and survival
The relationship between egg size and offspring phenotype is critical to our understanding of the selective pressures acting on the key reproductive life-history traits of egg size and number. Yet there is surprisingly little empirical evidence to support a strong, positive relationship between egg size and offspring quality (i.e., offspring growth, condition, and survival) in birds, in part because of confounding effects of parental quality and the lack of experimental techniques for directly manipulating avian egg size independently of maternal condition. Previously, we showed that treatment of laying female zebra finches (Taeniopygia guttata) with the antiestrogen tamoxifen can decrease egg size by ca. 8% but that this reduction in egg size had few effects on offspring mass and size at fledging. Here, we extend the use of this technique to induce larger decreases in egg size (up to 50% in individual females) and show that a reduction in egg size of ca. 18% is associated with decreased embryo viability, increased hatchling mortality, and lower posthatching offspring survival. Furthermore, we show that although hatchlings from eggs reduced in size by ca. 9% can survive to fledging, these chicks show slower initial growth during the linear growth phase (5 - 10 d of age), fledge at lower masses than chicks from control eggs, and show postfledging compensatory growth. Our results provide empirical support for significant effects of egg size on offspring quality and further suggest that among individual females there is a minimum egg size required to maintain embryo viability and offspring quality.
76.Williams, TD; Warnock, N; Takekawa, JY; Bishop, MA. (2007) Flyway-scale variation in plasma triglyceride levels as an index of refueling rate in spring-migrating Western Sandpipers (Calidris mauri).Auk 124: 886-897 Flyway-scale variation in plasma triglyceride levels as an index of refueling rate in spring-migrating Western Sandpipers (Calidris mauri)
Calidris mauri; migration; plasma triglycerides; radiotelemetry; stopover; Western Sandpiper
We combined radiotelemetry, plasma metabolite analyses, and macro-invertebrate prey sampling to investigate variation in putative fattening rates (estimated as plasma triglyceride levels) at the flyway scale in Western Sandpipers (Calidris mauri) migrating between Punta Banda, Mexico (31 degrees N), and Hartney Bay, Alaska (60 degrees N), a distance of 4,240 km. Birds were caught at a wintering site (San Francisco Bay) and eight stopover sites along this Pacific Flyway. Body mass was higher in females than in males at six sites, but variation was not correlated with latitude for either sex, and the relationship of change in mass by date within sites was uninformative with regard to possible latitudinal variation in fattening rates. At San Francisco Bay, triglyceride levels were higher in the spring than in the winter. Mean plasma triglyceride varied among stopover sites, and there was a significant linear trend of increasing triglyceride levels with latitude as birds migrated north. At San Francisco Bay, length of stay was negatively related to triglyceride levels. However, plasma triglyceride levels at wintering or initial stopover sites (San Francisco and Punta Banda) did not predict individual variation in subsequent rates of travel during migration. We found no significant relationship between triglyceride levels and prey biomass at different stopover sites, which suggests that the latitudinal pattern is not explained by latitudinal changes in food availability. Rather, we suggest that differences in physiology of migratory birds at southern versus northern stopover sites or behavioral differences may allow birds to sustain higher fattening rates closer to the breeding grounds.
74. McKinney, MA; Cesh, LS; Elliott, JE; Williams, TD; Garcelon, DK; Letcher, RJ. (2006) Brominated flame retardants and halogenated phenolic compounds in North American west coast bald eaglet (Haliaeetus leucocephalus) plasma.Environ Sci Technol 40: 6275-6281 Brominated flame retardants and halogenated phenolic compounds in North American west coast bald eaglet (Haliaeetus leucocephalus) plasma
We report on the identity, characterization, and spatial trends of several brominated flame retardants and hydroxylated (OH-) and methoxylated (MeO-) organohalogen contaminants in bald eagle (Haliaeetus leucocephalus) nestling plasma collected from sites along the west coast of North America. Samples were from four southwestern British Columbia (BC) locations, a reference site in northern BC (Fort St. James; FSJ), and from Santa Catalina Island, CA (SCI), an area of high DDT and PCB contamination. Mean concentrations of Sigma polybrominated diphenyl ether (Sigma PBDE (8 congeners monitored); 1.78-8.49 ng/g), Sigma OH-polychlorinated biphenyl (Sigma OH-PCB (30 congeners monitored); 0.44-0.87 ng/g), and Sigma OH- PBDE (14 congeners monitored; 0.31-0.92 ng/g) were similar in eaglets from southwestern BC yet lower than for SCI and significantly higher than for FSJ. Dominant PBDE congeners were BDE47, BDE99, and BDE100, but SCI eaglets also contained low levels of higher brominated congeners. 4-OH-CB187 and 4'-OH- CB202 accounted for 65-100% of Sigma OH-PCB in all BC eaglets, with 4'-OH-CB202 as well as 3'-OH-CB138 and 4-OH-CB146 dominating in SCI eaglets. Ostensibly of biogenic origin, 6'-OH-BDE49 and 6-OH-BDE47 were found in BC nestlings. Only 4'-OH-BDE49 (2.10 ng/g) was found in SCI eaglets. MeO-PBDEs and total hexabromocyclododecane (HBCD) were not found in any birds, but the polybrominated biphenyl BB101 was detected in southwestern BC samples. This study demonstrates that west coast North American bald eagles contain previously unreported organohalogens, which have the potential to impact the health and survival of these raptors.
73. Seaman, DAA; Guglielmo, CG; Elner, RW; Williams, TD. (2006) Landscape-scale physiology: Site differences in refueling rates indicated by plasma metabolite analysis in free-living migratory sandpipers.Auk 123: 563-574 Landscape-scale physiology: Site differences in refueling rates indicated by plasma metabolite analysis in free-living migratory sandpipers
Calidris mauri; fattening rate; geographic variation; plasma metabolites; Western Sandpipers
Variation in plasma metabolite profiles can provide information on physiological state and relative rates of mass change in free-living birds caught only once, and this technique could be used to compare rates of mass change (fattening) among populations or sites in relation to habitat quality. We compared plasma metabolite levels, as an index of relative refueling rates, in migratory Arctic-nesting Western Sandpipers (Calidris mauri), on a landscape scale at as many as nine sites over two years and during three different migratory stages within the Georgia Basin-Puget Sound region of British Columbia and Washington. There was significant intersite variation in plasma triglyceride levels in both years, but only for the northward migration. By contrast, there was little evidence of intrasite variability (i.e. metabolite profiles of birds using the same site were consistent between years and migratory stages), though we documented intrasite variation resulting from birds' use of different microllabitats at the same site. Plasma glycerol levels did not vary systematically among sites, though they varied among years; on average, birds had higher glycerol levels during northward migration than during Southward migration. For the northward migration only, there was a positive relationship between plasma triglyceride levels and total macrofaunal prey abundance among sites. Birds using smaller sites with a lower index of mudflat exposure (mean number of kilometer-hours of mudflat exposed in a 24-h period, reflecting the opportunity to forage at each site) tended to have lower triglyceride levels.
72. Stein, RW; Williams, TD. (2006) Causes and consequences of post-growth age-dependent differences in small intestine size in a migratory sandpiper (Calidris mauri, Western Sandpiper).Funct Ecol 20: 142-150 Causes and consequences of post-growth age-dependent differences in small intestine size in a migratory sandpiper (Calidris mauri, Western Sandpiper)
cestode; Charadriiformes; digestive system; gut size; refuelling
1. Calidris mauri Cabanis (Western Sandpiper) exhibits a pronounced post-growth age-dependent difference in small intestine size during southward migration, such that the later-migrating juveniles have larger small intestines than do the adults. Potential causes and consequences of this age-dependent difference are examined. 2. Premigrant juveniles of full structural size had small intestines that were 10% longer than those of the premigrant adults, even though the juveniles had not attained asymptotic body mass. The elongated small intestines of premigrant juveniles appear to be growth-related. 3. Adults and juveniles exhibited parallel increases in intestinal length (7.0%) and circumference (9.5%) in association with the initiation of migration; these effects are consistent with migratory hyperphagia. 4. Refuelling juveniles had small intestines that were 8.5% longer than those of the refuelling adults. Retaining an enlarged small intestine during migration confers increased digestive capacity to the juveniles, which may be under selection to minimize stopover duration. 5. Refuelling juveniles had a higher prevalence of cestode infection than refuelling adults in one of two years, and the length-corrected mass of the small intestine was 9.7% heavier in infected individuals. Cestode infection may be an important determinant of migration-related mortality for juveniles, by compromising their health and increasing stopover duration.
71. Vezina, F; Speakman, JR; Williams, TD. (2006) Individually variable energy management strategies in relation to energetic costs of egg production.Ecology 87: 2447-2458 Individually variable energy management strategies in relation to energetic costs of egg production
basal metabolic rate (BMR); daily energy expenditure (DEE); egg production costs; energy reallocation; reproduction; resting metabolic rate (RMR); Taeniopygia guttata; Zebra Finch
Marked interindividual variation in metabolic rate suggests considerable complexity in energy management strategies, but attempts to further our understanding of the relationship between resting metabolic rate (RMR), daily energy expenditure (DEE), and reproductive effort have been hampered by the complexity of studying this system in the field. Here, we describe energy management strategies in a captive-breeding system, using Zebra Finches (Taeniopygia guttata), to demonstrate the high-level of complexity and interindividual variability in energy expenditure, food intake, locomotor activity, and reproductive effort. In particular, we investigated whether the increase in RMR associated with egg production is additive, resulting in higher DEE and a need for elevated food intake, or whether this cost is compensated by reduced expenditure in nonreproductive components of the energy budget. We found high levels of intra-individual variation in energy expenditure associated with egg production in female Zebra Finches, e.g., comparing nonbreeding stage with the one-egg stage, change in RMR varied from 4.0% and 41.3%, and change in DEE varied from -33.3% to +46.4%. This variation was systematically related to aspects of locomotor activity and reproductive effort. Females with the largest increase in RMR during egg production decreased locomotor activity the most but still had increased DEE at the one-egg stage, and females with high DEE at the one-egg stage produced larger clutches. Our study suggests that females minimize increases in DEE during egg production through behavioral energy reallocation (reduced locomotor activity) but that individuals differ in their use of this strategy, which, in turn, is related to the absolute level of reproductive investment. This suggests a very complex, individually variable system of energy management to meet the demands of egg production.
69. Chin, EH; Love, OP; Clark, AM; Williams, TD. (2005) Brood size and environmental conditions sex-specifically affect nestling immune response in the European starling Sturnus vulgaris.J Avian Biol 36: 549-554 Brood size and environmental conditions sex-specifically affect nestling immune response in the European starling Sturnus vulgaris
In sexually size-dimorphic species, the larger sex can be more sensitive to stressful environmental conditions, often resulting in reduced growth and elevated mortality rates. Development of the immune system is regarded as highly resource dependent, and recent data suggest that nestling passerines experience a possible resource-based trade-off between growth and immunity. Given the hypothesized importance of maximizing growth for the larger sex, the corresponding immune system may also exhibit similar sensitivity to limited resources. To better understand how natural variation in brood size and resources might differentially affect growth and immune function in nestlings of a sexually size-dimorphic species, we examined the relationship between brood size and inter-sexual differences in cell-mediated immunity (CMI) and survival in European starling Sturnus vulgaris nestlings where males are larger in both mass and structural size. We hypothesized that male CMI response should be negatively impacted by increasing sibling competition (brood size), especially during periods of low resource availability. In a year of reduced parental provisioning rates and reduced chick growth rates, male offspring exhibited the predicted negative relationship, whereas female CMI response was unaffected. However, in a year of improved provisioning rates and chick growth, neither sex exhibited a negative relationship between immune response and brood size. Thus, natural variation in brood size can affect sex-specific immunity differently in offspring of a sexually size-dimorphic passerine. However, this relationship appears resource-dependent, suggesting that the hypothesized resource-based trade-off may be compensated for in years of adequate resource abundance.
68. Dods, PL; Birmingham, EM; Williams, TD; Ikonomou, MG; Bennie, DT; Elliott, JE. (2005) Reproductive success and contaminants in tree swallows (Tachycineta bicolor) breeding at a wastewater treatment plant.Environmental Toxicology and Chemistry 24: 3106-3112 Reproductive success and contaminants in tree swallows (Tachycineta bicolor) breeding at a wastewater treatment plant
tree swallow; nonylphenol; wastewater
The uptake and effects of contaminants were measured in the insectivorous tree swallow (Tachycineta bicolor) at a wastewater treatment site. The study examined reproductive, immunological, and growth endpoints in tree swallows exposed to chlorinated hydrocarbon contaminants and to 4-nonylphenol in wastewater lagoons at the Iona Wastewater Treatment Plant, Vancouver (BC, Canada). Clutch size was significantly lower in tree swallows breeding at Iona Island in 2000 and 2001 compared to the reference site. In 2000, fledging success was significantly lower and mean mass of nestling livers was significantly higher in the tree swallows breeding at the Iona Island Wastewater Treatment Plant. Additional factors that may influence reproductive success, such as parental provisioning and diet composition, did not differ significantly between sites. Levels of 4-nonylphenol detected in sediment and insects were elevated at the Iona Island Wastewater Treatment Plant (2000: lagoon sediment 82,000 ng/g dry wt, insects 310 ng/g wet wt; 2001: lagoon sediment 383,900 ng/g dry wt, insects 156 ng/g wet wt) compared to the reference site (2000: pond sediment 1,100 ng/g dry wt, insects not sampled; 2001: pond sediment 642 ng/g dry wt, insects 98 ng/g wet wt). These results indicate that tree swallows might be a useful indicator species for exposure to 4-nonylphenol at wastewater treatment sites; however, further work is necessary to determine the extent of uptake and effects of 4-nonylphenol in riparian insectivorous birds.
67. Gill, H; Williams, TD; Bishop, CA; Cheng, KM; Elliott, JE. (2005) Effects of azinphos-methyl on cholinergic responses and general health in zebra finches (Taeniopygia guttata) after previous treatment with p,p '-DDE.Archives of Environmental Contamination and Toxicology 48: 118-126 Effects of azinphos-methyl on cholinergic responses and general health in zebra finches (Taeniopygia guttata) after previous treatment with p,p '-DDE
Although organochlorine (OC) pesticides were replaced with organophosphates (OPs) in the early 1970s, they continue to persist in orchard environments today. Extensive research has been conducted to determine the effects of currently used OPs on cholinesterase (ChE) activity; however, although OCs continue to be prevalent in areas of previous use, few studies have looked at the toxicity of a combination of residual OC compounds with currently used OP pesticides. The focus of our study was to determine the effects of azinphos-methyl (a common OP used in apple orchards today) on ChE activity and general health in zebra finches (Taeniopygia guttata) previously exposed to p,p'-DDE (a commonly detected metabolite of DDT). The main results of our study were as follows: (1) azinphos-methyl alone caused a dose-dependent inhibition of plasma and brain ChE activity; (2) p,p'-DDE in combination with azinphos-methyl did not change azinphosmethyl inhibition of ChE activity; and (3) there were suggestions of immunostimulation in birds dosed 1 year previously to p,p'-DDE and of anemia when p,p'-DDE was combined with azinphos-methyl; however, there was no dose-response for these parameters in birds subsequently dosed with p,p'-DDE.
66. Gorman, KB; Williams, TD. (2005) Correlated evolution of maternally derived yolk testosterone and early developmental traits in passerine birds.Biology Letters 1: 461-464 Correlated evolution of maternally derived yolk testosterone and early developmental traits in passerine birds
maternal effects; yolk hormones; testosterone; early development; independent contrasts
Recent studies on hormone-mediated maternal effects in birds have highlighted the influence of variable maternal yolk androgen concentration on offspring phenotype, particularly in terms of early development. If genetic differences between laying females regulate variation in yolk hormone concentration, then this physiological maternal effect is an indirect genetic effect which can provide a basis for the co-evolution of maternal and offspring phenotypes. Thus, we investigated the evolutionary associations between maternally derived yolk testosterone (T) and early developmental traits in passerine birds via a comparative, phylogenetic analysis. Our results from species-correlation and independent contrasts analyses provide convergent evidence for the correlated evolution of maternal yolk T concentration and length of the prenatal developmental period in passerines. Here, we show these traits are significantly negatively associated (species-correlation: p<0.001, r(2) = 0.85; independent contrasts: p=0.005). Our results highlight the need for more studies investigating the role of yolk hormones in evolutionary processes concerning maternal effects.
65. Gurney, KE; Williams, TD; Smits, JE; Wayland, M; Trudeau, S; Bendell-Young, LI. (2005) Impact of oil-sands based wetlands on the growth of mallard (Anas platyrhynchos) ducklings.Environmental Toxicology and Chemistry 24: 457-463 Impact of oil-sands based wetlands on the growth of mallard (Anas platyrhynchos) ducklings
Anas platyrhynchos; duckling; wetlands; ecotoxicology
Identifying the potential effects of industrially formed wetlands on waterfowl populations is important for assessing the suitability of such wetlands in industrial reclamation strategies. Mallard ducklings were held in situ on two industrially formed wetlands and one reference wetland in northern Alberta, Canada. Duckling mass and skeletal size were measured at regular intervals over 33 d, and blood was collected to investigate the analysis of plasma metabolites (triglyceride and glycerol) as an indicator of physiological condition. In repeated-measures analysis of variance (ANOVA), multivariate ANOVA, and subsequent multiple-comparisons tests, body mass and skeletal size were significantly lower in ducklings maintained on the industrial wetland after 2, 5, 9, and 13 d of exposure. In this situation, plasma metabolite analysis did not provide additional information on mass-independent condition. We conclude that if the observed differences in growth and size translate into a decreased survival of juvenile waterfowl inhabiting these wetlands, then populations of these birds in the area could be negatively affected. We emphasize the importance of field-based ecological research in toxicological studies of wildlife.
64. Love, OP; Chin, EH; Wynne-Edwards, KE; Williams, TD. (2005) Stress hormones: A link between maternal condition and sex-biased reproductive investment.American Naturalist 166: 751-766 Stress hormones: A link between maternal condition and sex-biased reproductive investment
corticosterone; sex ratio theory; sex allocation theory; maternal condition; maternal effects; yolk hormones
In species where offspring fitness is sex-specifically influenced by maternal reproductive condition, sex allocation theory predicts that poor-quality mothers should invest in the evolutionarily less expensive sex. Despite an accumulation of evidence that mothers can sex-specifically modulate investment in offspring in relation to maternal quality, few mechanisms have been proposed as to how this is achieved. We explored a hormonal mechanism for sex-biased maternal investment by measuring and experimentally manipulating baseline levels of the stress hormone corticosterone in laying wild female European starlings (Sturnus vulgaris) and examining effects on sex ratio and sex-specific offspring phenotype adjustment. Here we show that baseline plasma corticosterone is negatively correlated with energetic body condition in laying starlings, and subsequent experimental elevation of maternal baseline plasma corticosterone increased yolk corticosterone without altering maternal condition or egg quality per se. Hormonal elevation resulted in the following: female-biased hatching sex ratios (caused by elevated male embryonic mortality), lighter male offspring at hatching (which subsequently grew more slowly during postnatal development), and lower cell-mediated immune (phytohemagglutinin) responses in males compared with control-born males; female offspring were unaffected by the manipulation in both years of the study. Elevated maternal corticosterone therefore resulted in a sex-biased adjustment of offspring quality favorable to female offspring via both a sex ratio bias and a modulation of male phenotype at hatching. In birds, deposition of yolk corticosterone may benefit mothers by acting as a bet-hedging strategy in stochastic environments where the correlation between environmental cues at laying (and therefore potentially maternal condition) and conditions during chick-rearing might be low and unpredictable. Together with recent studies in other vertebrate taxa, these results suggest that maternal stress hormones provide a mechanistic link between maternal quality and sex-biased maternal investment in offspring.
63. Seaman, DA; Guglielm, CG; Williams, TD. (2005) Effects of physiological state, mass change and diet on plasma metabolite profiles in the western sandpiper Calidris mauri.Journal of Experimental Biology 208: 761-769 Effects of physiological state, mass change and diet on plasma metabolite profiles in the western sandpiper Calidris mauri
metabolites; mass change; migration physiology; fattening; captive shorebirds
We used a food restriction/refeeding protocol to put birds through a controlled cycle of mass loss and mass gain to investigate the effects of rate and phase of mass change on plasma metabolite levels in relation to diet. Despite marked differences in fat content of the two diets (18% vs 4%) mean rate of mass loss or mass gain was independent of diet. There was also no effect of diet on plasma levels of any of the four measured metabolite (triglyceride, glycerol, uric acid and beta-0H-butyrate) during mass loss. However, during mass gain birds on the low fat diet had higher plasma levels of triglyceride and uric acid and lower P-OH-butyrate than birds gaining mass on the high-fat diet. Thus, diet composition can affect plasma metabolite profiles independently of differences in rates of mass change. Nevertheless, certain plasma metabolites were related to variation in rates of mass change across physiological states. Glycerol levels were negatively related to the rate of mass change (independent of diet), and butyrate was negatively related to the rate of mass change on both diets (though the slope of this relationship was diet dependent). Uric acid was positively related to the rate of mass change but only for birds on the low-fat diet. Our study therefore confirms that measurement of plasma metabolites can provide robust information on physiological state (gain, loss) and the rate of mass change (e.g. in free-living birds caught only once) although researchers should be cogniscent of potential confounding effects of diet composition for certain metabolites, both for field studies and for future experimental validations of this technique.
62. Stein, RW; Place, AR; Lacourse, T; Guglielmo, CG; Williams, TD. (2005) Digestive organ sizes and enzyme activities of refueling western sandpipers (Calidris mauri): Contrasting effects of season and age.Physiological and Biochemical Zoology 78: 434-446 Digestive organ sizes and enzyme activities of refueling western sandpipers (Calidris mauri): Contrasting effects of season and age
We examined seasonal and age-related variation in digestive organ sizes and enzyme activities in female western sandpipers (Calidris mauri) refueling at a coastal stopover site in southern British Columbia. Adult sandpipers exhibited seasonal variation in pancreatic and intestinal enzyme activities but not in digestive system or organ sizes. Spring migrants had 22% higher total and 67% higher standardized pancreatic lipase activities but 37% lower total pancreatic amylase activity than fall migrants, which suggests that the spring diet was enriched with lipids but low in glycogen. Spring migrants also had 47% higher total intestinal maltase activity as well as 56% higher standardized maltase and 13% higher standardized aminopeptidase-N activities. Spring migrants had higher total enzymic capacity than fall migrants, due primarily to higher total lipase and maltase activities. During fall migration, the juvenile's digestive system was 10% larger than the adult's, and it was composed differently: juveniles had a 16% larger small intestine but a 27% smaller proventriculus. The juvenile's larger digestive system was associated with lower total enzymic capacity than the adult's due to 20% lower total chitinase and 23% lower total lipase activities. These results suggest that juvenile western sandpipers may process food differently from adults and/or have a lower-quality diet.
61. Vezina, F; Williams, TD. (2005) The metabolic cost of egg production is repeatable.Journal of Experimental Biology 208: 2533-2538 The metabolic cost of egg production is repeatable
basal metabolic rate; resting metabolic rate; repeatability; egg production; reproduction; zebra finch; Taeniopygia guttata
The metabolic cost of egg production in birds (passerines) has been measured as a 16-27% increase in basal or resting metabolic rate (BMR and RMR, respectively) when comparing non-breeding values with those in egg-producing individuals. However, available data to date have been obtained in free-living birds and may thus be confounded by the effect of variable ecological conditions on non-reproductive physiological machinery (organ mass or metabolic activity) which might contribute to measured variation in RMR. Here, we show that in captive, controlled conditions, the process of egg formation induces a 22% increase in RMR in female zebra finches Taeniopygia guttata. Among individuals, variation in laying RMR is independent of egg mass, clutch size or total clutch mass. Importantly, we show that individual variation in both non-breeding and laying RMR is repeatable over periods of at least 8-10 months, i.e. individual variation in RMR remained constant over time for any given physiological state. This suggests that the metabolic cost of egg formation should respond to selection. However, we also show that in males, but not females, repeatability of RMR declines over time even when birds are kept in constant controlled conditions.
60. Vezina, F; Williams, TD. (2005) Interaction between organ mass and citrate synthase activity as an indicator of tissue maximal oxidative capacity in breeding European Starlings: implications for metabolic rate and organ mass relationships.Functional Ecology 19: 119-128 Interaction between organ mass and citrate synthase activity as an indicator of tissue maximal oxidative capacity in breeding European Starlings: implications for metabolic rate and organ mass relationships
body composition; BMR; egg production; phenotypic flexibility
1. Numerous studies have suggested that basal metabolic rate (BMR) is related to variation in mass of specific 'energy-expensive' organs such as heart and kidney. 2. However, there are inconsistencies among studies with regard to those organs that show positive relationships with BMR, potentially because such studies assume constant organ metabolic intensity or capacity (e.g. oxidative activity). 3. This paper investigates metabolic adjustments (citrate synthase activity) in four key organs (pectoral muscle, heart, kidney and liver) in free-living reproductive female European Starlings (Sturnus vulgaris) throughout the breeding season to determine if the cost of egg production results in readjustments in organ mass-specific enzyme activity. 4. Citrate synthase (CS) activity varied in relation to breeding stage and/or year, but this variation was not consistent among different organs. For some organs, total enzymatic activity was directly related to changes in organ mass in relation to breeding stage. For others, increased organ mass was associated with a decrease in mass-specific CS activity, resulting in no net change in total organ oxidative capacity among breeding stages. 5. Even though the liver is actively involved in yolk precursor production during egg formation, no evidence was found for up-regulation of mass-specific oxidative enzyme activity in this organ. 6. Metabolic adjustments at the organ level may occur independently from organ mass changes and this confounding effect may be responsible for part of the inconsistencies found between previous studies in terms of organs mass-RMR relationships.
59.Williams, TD. (2005) Mechanisms underlying the costs of egg production.Bioscience 55: 39-48 Mechanisms underlying the costs of egg production
egg production; costs of reproduction; hormones; individual variation; pleiotropy
Female birds incur costs associated with increased egg production, including reductions in chick provisioning ability, vival, and in egg and chick viability. It should be possible to identify the components of the physiological system underlying reproduction, or the specific reproductive traits themselves, that explain these costs, but this has proved to be difficult, in part because of marked, but unexplained, individual variation in these traits. Resolving the physiological and evolutionary consequences of this individual variation represents an exciting challenge for the future. Several mechanisms have been proposed for the cost of egg production (e.g., protein depletion and impaired flight muscle function; immunosuppression), which assume relatively simple resource-allocation trade-offs. I argue that such mechanisms provide an unsatisfactory explanation for costs that can occur over months or even years. A more productive approach for future research will be to focus on hormonally mediated, non-resource-based costs of egg production caused by pleiotropic effects of reproductive hormones that can operate, over the longer time scales at which costs of reproduction are expressed.
58.Williams, TD; Ames, CE; Kiparissis, Y; Wynne-Edwards, KE. (2005) Laying-sequence-specific variation in yolk oestrogen levels, and relationship to plasma oestrogen in female zebra finches (Taeniopygia guttata).Proceedings of the Royal Society B-Biological Sciences 272: 173-177 Laying-sequence-specific variation in yolk oestrogen levels, and relationship to plasma oestrogen in female zebra finches (Taeniopygia guttata)
maternal effects; plasma oestradiol-17 beta; Taeniopygia guttata; yolk hormones
We investigated the relationship between plasma and yolk oestrogens in laying female zebra finches (Taeniopygia guttata) by manipulating plasma oestradiol (E2) levels, via injection of oestradiol-17beta, in a sequence-specific manner to maintain chronically high plasma levels for later-developing eggs (contrasting with the endogenous pattern of decreasing plasma E2 concentrations during laying). We report systematic variation in yolk oestrogen concentrations, in relation to laying sequence, similar to that widely reported for androgenic steroids. In sham-manipulated females, yolk E2 concentrations decreased with laying sequence. However, in E2-treated females plasma E2 levels were higher during the period of rapid yolk development of later-laid eggs, compared with control females. As a consequence, we reversed the laying-sequence-specific pattern of yolk E2: in E2-treated females, yolk E2 concentrations increased with laying-sequence. In general therefore, yolk E2 levels were a direct reflection of plasma E2 levels. However, in control females there was some inter-individual variability in the endogenous pattern of plasma E2 levels through the laying cycle which could generate variation in sequence-specific patterns of yolk hormone levels even if these primarily reflect circulating steroid levels.
57. Love, OP; Breuner, CW; Vezina, F; Williams, TD. (2004) Mediation of a corticosterone-induced reproductive conflict.Hormones and Behavior 46: 59-65 Mediation of a corticosterone-induced reproductive conflict
corticosterone; corticosteroid-binding globulin; reproduction; nest desertion; European starling (Sturnus vulgaris)
Current research in birds suggests that a conflict should exist during reproduction for the role of the glucocorticoid corticosterone (CORT). While elevated levels have been correlated with the increased energetic demand of raising offspring, elevated CORT levels have traditionally been implicated in reproductive abandonment. We examined the relationship between CORT and nest desertion in breeding wild female European starlings (Sturnus vulgaris) incorporating analyses of both total circulating levels and 'free', unbound CORT through analysis of corticosteroid-binding globulin (CBG). Free baseline CORT levels of nest-abandoning birds were significantly higher than nonabandoning birds within each stage, with chick-rearing birds exhibiting the highest free baseline CORT levels, while concurrently remaining the most resistant stage to nest desertion. Elevated free baseline CORT levels in chick-rearing birds were not due to increased total CORT secretion, but rather to a decrease in CBG levels. Overall, our results suggest that CORT and CBG interact to play a role in mediating the increased energetic demand of offspring, while minimizing the chances of nest desertion, thereby alleviating any potential behavioral conflict for CORT during reproduction. Furthermore, these results demonstrate that the traditional view of the role of CORT during reproduction is much more complex than previously appreciated. Together with mounting evidence, we suggest that elevated corticosteroid levels are an inherent and necessary part of reproduction in nonmammalian tetrapods. (C) 2004 Elsevier Inc. All rights reserved.
56. Peery, AZ; Beissinger, SR; Newman, SH; Becker, BH; Burkett, E; Williams, TD. (2004) Individual and temporal variation in inland flight behavior of Marbled Murrelets: Implications for population monitoring.Condor 106: 344-353 Individual and temporal variation in inland flight behavior of Marbled Murrelets: Implications for population monitoring
Brachyramphus marmoratus; breeding; inland flights; Marbled Murrelet; population monitoring; radar; radio-telemetry; Marbled Murrelets;
We studied the inland flight behavior of 46 radio-marked Marbled Murrelets (Brachyramphus marmoratus) in 2000 and 2001 in central California to determine how the frequency of inland flights varied among individuals and over time. All breeding murrelets regularly flew inland (mean 82% of daily surveys), but we observed considerable variation in the inland flight behavior of non-nesters. Non-nesters that were physiologically in breeding condition (potential breeders) regularly flew inland (90% of individuals; mean 41% of daily surveys), but non-nesters that were not in breeding condition (nonbreeders) rarely flew inland (20% of individuals; mean 1% of daily surveys). The mean percentage of surveys on which individual murrelets flew inland increased from 20% in 2000 to 61% in 2001, which was partly due to an increase in the percentage of breeders from 11% in 2000 to 50% in 2001. The frequency of inland flights was greatest during the incubation and chick-provisioning stages (100% in both stages), and lowest during the pre- and postbreeding stages (70% and 78%, respectively). Although the mean percentage of flights increased dramatically between years, the regional population estimate from at-sea surveys increased only 28% from 496 to 637 individuals during the same period, indicating that monitoring techniques such as radar that count inland flights are more likely to reflect annual variation in breeding effort than changes in regional population size. Moreover, the inland flight behavior of potential breeders indicates that radar surveys will overestimate breeding population size, even though the lack of inland flights by nonbreeders indicates that radar surveys will underestimate regional population size.
55. Peery, MZ; Beissinger, SR; Newman, SH; Burkett, EB; Williams, TD. (2004) Applying the declining population paradigm: Diagnosing causes of poor reproduction in the marbled murrelet.Conservation Biology 18: 1088-1098 Applying the declining population paradigm: Diagnosing causes of poor reproduction in the marbled murrelet
conservation; demography; declining population paradigm; Marbled Murrelet; population declines; reproductive success; Marbled Murrelets;
We identified six approaches to diagnosing causes of population declines and illustrate the use of the most general one ("multiple competing hypotheses") to determine which of three candidate limiting factors-food availability, nesting site availability, and nest predation-were responsible for the exceptionally poor reproduction of Marbled Murrelets (Brachyramphus marmoratus) in central California. We predicted how six attributes of murrelet demography, behavior, and physiology should be affected by the candidate limiting factors and tested predictions with field data collected over 2 years. The average proportion of breeders, as estimated with radiotelemetry, was low (0.31) and varied significantly between years: 0.11 in 2000 and 0.50 in 2001. Murrelets spent significantly more time foraging in 2000 than in 200 1, suggesting that low food availability limited breeding in 2000. In 2001, 50% of radio-marked murrelets nested and 67% of females were in breeding condition, suggesting that enough nest sites existed for much of the population to breed. However, rates of nest failure and nest predation were high (0.84 and 0.67-0.81, respectively) and few young were produced, even when a relatively high proportion of murrelets bred. Thus, we suggest that reproduction of Marbled Murrelets in central California is limited by food availability in some years and by nest predation in others, but apparently is not limited by availability of nesting sites. The multiple-competing-hypotheses approach provides a rigorous framework for identifying causes of population declines because it integrates multiple types of data sets and can incorporate elements of other commonly used approaches.
54. Sockman, KW; Williams, TD; Dawson, A; Ball, GF. (2004) Prior experience with photostimulation enhances photo-induced reproductive development in female European starlings: A possible basis for the age-related increase in avian reproductive performance.Biology of Reproduction 71: 979-986 Prior experience with photostimulation enhances photo-induced reproductive development in female European starlings: A possible basis for the age-related increase in avian reproductive performance
aging; behavior; environment; neuroendocrinology; seasonal reproduction
Reproductive performance in female birds improves with age, and this is generally attributed to experiences obtained during breeding. In temperate-zone species, experience with photostimulation during the first breeding year may prime the hypothalamo-pituitary-gonadal axis to respond to photic cues more rapidly or robustly in subsequent years. To test this idea, we captured 32 photorefractory juvenile (hence naive to photostimulation) female European starlings (Sturnus vulgaris) and held half of them (naive group) on a photoperiod of 8L:16D for 32 wk and the other half (experienced group) on 81.16D for 12 wk, 16L:8D for 12 wk, and then 8L:16D for 8 wk. When we subsequently transferred all birds to 16L:8D, the increase in body mass, which may presage egg laying in the wild, was more robust in experienced than in naive females. Experienced females also showed a more robust elevation in plasma concentrations of the yolk-precursor protein vitellogenin, although naive females showed an initial rapid but transient rise in vitellogenin that we attribute to their extended exposure to short-day photoperiods prior to photostimulation. Finally, the photo-induced increase in diameter of the largest ovarian follicle, in plasma concentrations of luteinizing hormone, and in the number of septo-preoptic fibers relative to the number of cell bodies immunoreactive to GnRH was greater in experienced than in naive females. Thus, prior experience with photostimulation enhances some initial phases of photo-induced reproductive development and may explain, in part, why reproductive performance improves with age in temperate-zone birds.
53.Williams, TD; Ames, CE. (2004) Top-down regression of the avian oviduct during late oviposition in a small passerine bird.Journal of Experimental Biology 207: 263-268 Top-down regression of the avian oviduct during late oviposition in a small passerine bird
cost of egg production; oviduct; organ size-function relationship; maternal effect; Taeniopygia guttata
Egg production in oviparous vertebrates is assumed to be costly but the physiological basis of any costs remains unknown. The avian oviduct is a highly differentiated linear organ, with five functionally specific regions. Here we show that the oviduct regresses rapidly 'from the top down' as soon as the more proximal regions have completed their function but while the distal regions still retain an oviductal egg. In zebra finches Taeniopygia guttata, oviduct mass did not differ between early laying birds at the 1-egg stage compared with late-laying birds (with one remaining yolky follicle; dry mass, 151-167 mg). However, in birds with no remaining yolky follicles but with an oviductal egg, oviduct mass decreased to 94 mg (44%). Regression occurred unequally among different regions of the oviduct, with significant decreases in the proximal infundibulum/magnum. and isthmus regions (59% and 40%, respectively), but no change in distal shell gland/vagina mass. The shell gland did not regress until after the last oviposition. Thus, the avian oviduct has a highly regulated size-function relationship consistent with a high maintenance energy cost for this organ. We suggest that oviduct function is a significant contributor to the physiological costs of egg production and might mediate individual variation in maternal effects associated with non-yolk components of egg quality (e.g. immunoglobulins, lysozyme).
52.Williams, TD; Challenger, WO; Christians, JK; Evanson, M; Love, O; Vezina, F. (2004) What causes the decrease in haematocrit during egg production?Functional Ecology 18: 330-336 What causes the decrease in haematocrit during egg production?
Aerobic performance; cost of reproduction; egg-laying; hematocrit
1. Anaemia has been reported in wild animals, typically associated with traumatic events or ill health. However, female birds routinely become 'anaemic' during egg-laying; we sought to determine the causes of this reduction in haematocrit. 2. Haematocrit in female European Starlings (Sturnus vulgaris Linnaeus) decreased between pre-breeding and egg-laying in 3 out of 4 years (the decrease was marginally non-significant in the fourth year). This was independent of changes in ambient temperature altering the metabolic requirements for thermoregulation. 3. There was a positive relationship between haematocrit and plasma levels of the yolk precursor vitellogenin among egg-laying birds, supporting the hypothesis that the initial reduction in haematocrit is caused by increased blood volume associated with osmoregulatory adjustments to elevated levels of yolk precursors. 4. However, haematocrit did not always recover upon cessation of egg production, remaining low at clutch completion (2 of 4 years), incubation (1 of 2 years) and chick rearing (1 of 4 years), suggesting an additional cause of the prolonged reduction in haematocrit. 5. Given the magnitude and prolonged nature of the changes in haematocrit we report, and the interannual variation in haematocrit even during chick-rearing (47-54%), we suggest that 'anaemia' associated with egg production might have implications for aerobic performance during later stages of breeding.
51.Williams, TD; Kitaysky, AS; Vezina, F. (2004) Individual variation in plasma estradiol-17 beta and androgen levels during egg formation in the European starling Sturnus vulgaris: implications for regulation of yolk steroids.General and Comparative Endocrinology 136: 346-352 Individual variation in plasma estradiol-17 beta and androgen levels during egg formation in the European starling Sturnus vulgaris: implications for regulation of yolk steroids
Sturnus vulgaris; estradiol-17 beta; androgens; egg formation; maternal effects
While it is clear that maternal transfer of steroids to egg yolk can have significant effects on offspring phenotype, an unresolved question is whether females can facultatively adjust yolk hormone levels independently of their own plasma levels or whether yolk steroid levels are simply a direct consequence of temporal variation in the female's hormonal status. In part, this is because we lack detailed information about the day-to-day pattern of changes in plasma hormone levels during the laying cycle for non-domesticated birds. Here, we describe changes in plasma estradiol-17beta (E2) and androgens, throughout laying in relation to specific stages of ovarian follicular development in the European starling (Sturnus vulgaris). Plasma E2 levels increased rapidly from the onset of rapid yolk development (RYD) to reach maximum levels in birds with a complete follicle hierarchy ( greater than or equal to 4 yolky follicles). However, levels decreased linearly throughout the later stages of follicle development returning to pre-breeding values before the final yolky follicle was ovulated. In females with greater than or equal to 4 yolky follicles there was 10-fold variation in plasma E2 levels among individual females, but this was not related to plasma levels of the main yolk precursor vitellogenin or to the total mass of yolky follicles developing at the time of blood sampling. In contrast to E2, plasma androgen levels showed only a very gradual linear decline throughout the laying cycle from pre-RYD to clutch completion. Furthermore, androgen levels showed less individual variability: 4-fold variation among females with greater than or equal to 4 yolky follicles, although this was also independent of our measures of reproductive function. Data on inter- and intra-individual variation in female hormone levels are important to set-up a priori predictions for, and interpretation of, studies of yolk hormone levels. (C) 2004 Elsevier Inc. All rights reserved.
50. Egeler, O; Seaman, D; Williams, TD. (2003) Influence of diet on fatty-acid composition of depot fat in Western sandpipers (Calidris mauri).Auk 120: 337-345 Influence of diet on fatty-acid composition of depot fat in Western sandpipers (Calidris mauri)
Western Sandpipers (Calidris mauri) have been previously shown to undergo seasonal changes in the fatty acid composition of their fat stores, even though they do not show the marked seasonal variation in diet common to many migratory passerines. We investigated the effect of dietary fatty acid composition on the fatty acid composition of adipose tissue in captive Western Sandpipers by feeding birds experimental diets with different fatty acid composition. In addition, we determined the effect of total percentage of fat content of the diet (5 vs. 10%) on fatty acid composition of depot fat. Birds maintained normal body mass (24-27 g) throughout all experimental treatments. Most adipose fatty acids were sensitive to dietary manipulation to some extent. Changes in fatty acid composition of the diet had the largest effect on adipose tissue composition for the essential polyunsaturated fatty acid linoleate (18:2), whereas it bad the least effect for the monounsaturated fatty acid oleate (18:1). The saturated fatty acid palmitate (16:0) demonstrated an intermediate capacity to alter fatty acid composition of adipose tissue. Total amount of fat in the diet did not influence the effect of diet on fatty acid deposition. Results of dietary manipulations in this study suggest that diet does explain some of the variation in fatty acid composition observed during migration in Western Sandpipers, but that certain fatty acids can be modulated independently of diet (probably through de novo synthesis, postabsorption modification, or both).
49. Guglielmo, CG; Williams, TD. (2003) Phenotypic flexibility of body composition in relation to migratory state, age, and sex in the western sandpiper (Calidris mauri).Physiological and Biochemical Zoology 76: 84-98 Phenotypic flexibility of body composition in relation to migratory state, age, and sex in the western sandpiper (Calidris mauri)
We investigated the flexibility of body composition in relation to seasonally variable demands for endurance flight capacity and hyperphagia in a migratory shorebird. Migrating western sandpipers were sampled in spring and fall while refueling at a north temperate stopover and were compared with nonmigrating birds captured at a tropical wintering area in Panama. Sandpipers weighed 25% more at stopover, and nearly 40% of migratory mass increase consisted of lean body components. Most organs and flight muscles were 10%-100% larger during migration, and the greatest relative size increases occurred in the digestive system (including liver). Birds preparing to initiate spring migration from Panama deposited only fat, suggesting that changes in lean body components take place after migration has begun, possibly through training effects. Sex did not influence body composition. Juveniles making their first southward migration were similar to adults in structural size and body mass but had substantially enlarged alimentary tracts. Sandpipers appeared to deposit lean mass during stopover in fall but not in spring. The dramatic enlargement of the digestive system in this small species that makes short flights and fuels frequently contrasts with the reduction of digestive components in larger species that fuel only once or twice by making one or two very long flights to their destination.
48. Salvante, KG; Williams, TD. (2003) Effects of corticosterone on the proportion of breeding females, reproductive output and yolk precursor levels.General and Comparative Endocrinology 130: 205-214 Effects of corticosterone on the proportion of breeding females, reproductive output and yolk precursor levels
In this study we investigated the role of corticosterone (B) in regulating the proportion of laying females, timing of breeding, reproductive output (egg size and number), and yolk precursor levels in chronically B-treated female zebra finches (Taeniopygia guttata). Corticosterone treatment via silastic implant elevated plasma B to high physiological (stress-induced) levels (24.1 +/- 5.3 ng/ ml at 7-days post-implantation). B-treated females had high plasma levels of very-low density lipoprotein (VLDL) but low levels of plasma vitellogenin 7-days post-implantation, suggesting that corticosterone inhibited yolk precusor production and perhaps shifted lipid metabolism away from production of yolk VLDL and towards production of generic (non-yolk) VLDL. Only 56% of B-treated females (n = 32) initiated laying, compared with 100% of sham-implanted females (n = 18). In females that did breed, corticosterone administration delayed the onset of egg laying: B-treated females initiated laying on average 14.5 +/- 0.5 days after pairing compared to 6.4 +/- 0.5 days in sham-implanted females. B-treated females that laid eggs had significantly higher plasma B levels at the 1st-egg stage (45.9 +/- 9.0 ng/ml) than did sham-implanted females (7.9 +/- 6.8 ng/ml). Despite this there was no difference in mean egg mass, clutch size, or egg composition in B-treated and sham-implanted females. These results are consistent with the idea that elevated corticosterone levels inhibit reproduction, but contrast with studies of other oviparous vertebrates (e.g., lizards) in relation to the role of corticosterone in regulating egg and clutch size. (C) 2003 Elsevier Science (USA). All rights reserved.
46. Tranquilla, LAM; Bradley, RW; Lank, DB; Williams, TD; Lougheed, LW; Cooke, F. (2003) The reliability of brood patches in assessing reproductive status in the Marbled Murrelet: Words of caution.Waterbirds 26: 108-118 The reliability of brood patches in assessing reproductive status in the Marbled Murrelet: Words of caution
brood patch; reproductive status; incubation; Marbled Murrelet; Brachyramplens marmoratus; radio telemetry; vitellogenin; Marbled Murrelet; Marbled Murrelets;
The assumption that brood patches identify incubating birds is a pervasive one in avian literature, and its a result, brood patches are often used to infer breeding status. Although the developmental stages of the brood patch with specific: reproductive stages in passerines have been described, this information for seabirds is not often reported. Thus, for birds whose breeding activities are not easily observed, it is difficult to confirm (1) that it is valid to assume that a bird which has some stage of brood patch is a nester or putative nester, and (2) whether specific stages of brood patch development reflect specific stages of the breeding cycle. We tested the utility oh brood patch scores to infer breeding status in a non-colonial seabird, the Marbled Murrelet (Brachyramphus marmoratus), a species always captured away from the nest site. We confirmed the breeding status of murrelets with brood patches, and assessed the specific stages of brood patch development to the timing of egg-production (using a physiological analysis) and the onset of incubation (rising radio telemetry). Murrelets with brood patches were not always nesters or putative nesters (58% of birds with brood patches were producing eggs, and 56% of radio-tagged birds with brood patches began incubation), and brood patch score did not predict which birds were more likely to become egg-producers or incubators. Specific brood patch stages did not always correlate with specific breeding stages (e.g., the brood patch of egg-producers ranged from absent to fully-developed). Birds with fully developed brood patches took from 3-30 days to start incubation. Brood patch development accurately depicted the average population incubation time, but we caution against rising brood patches to predict the timing of an individual breeding attempt, and suggest that when possible, researchers should try to confirm breeding activities using other methods.
45. Tranquilla, LAM; Yen, PPW; Bradley, RW; Vanderkist, BA; Lank, DB; Parker, NR; Drever, M; Lougheed, LW; Kaiser, GW; Williams, TD. (2003) Do two murrelets make a pair? Breeding status and behavior of marbled murrelet pairs captured at sea.Wilson Bulletin 115: 374-381 Do two murrelets make a pair? Breeding status and behavior of marbled murrelet pairs captured at sea
Murrelets, sea birds; Marbled Murrelet; ; Marbled Murrelets;
Marbled Murrelets (Brachyramphus marmoratus) observed at sea usually are in pairs throughout the year. Although it has been assumed that these pairs are mates, this assumption has not been formally examined. Using data from three study sites during the breeding seasons of 1997-2001, we found that 92% of the birds that were paired at capture were of male-female pairs, and that paired females were more likely (73%) to be producing eggs than were single females (8%). Fourteen of fifteen pairs were tracked to a single nest location per pair. No pair members caught at sea were found breeding at separate nest sites. One pair was caught in two successive seasons, suggesting that at least some pairs are long lasting. Notably, pair members breeding together and radio tracked throughout the summer were detected without their breeding partners for 77% of the time. Thus, while pairs of Marbled Murrelets observed at sea most likely are members of a breeding pair, single murrelets observed at sea should not be assumed to be unpaired or nonbreeders.
44. Tranquilla, LM; Williams, T; Cooke, F. (2003) Using vitellogenin to identify interannual variation in breeding chronology of marbled murrelets (Brachyramphus marmoratus).Auk 120: 512-521 Using vitellogenin to identify interannual variation in breeding chronology of marbled murrelets (Brachyramphus marmoratus)
Marbled Murrelet; ; Marbled Murrelet;
Vitellogenin is a lipophosphoprotein found in plasma of egg-producing birds prior to laying that may be used to identify fecund females whose reproductive status is otherwise unknown. We captured Marbled Murrelets (Brachyramphus marmoratus) at sea in Desolation Sound, British Columbia, and used vitellogenin to (1) identify variation in egg production between 1999 and 2000, (2) predict timing of subsequent breeding stages on the basis of egg production, and (3) describe proportion of captured females producing eggs. We also used vitellogenin to investigate a capture bias previously detected in mist-netted birds in the study area and found a corresponding bias in number of egg producers caught. Dates that egg producers were present (27 April to 6 July 1999, 20 April to 6 July 2000) indicate that breeding is highly asynchronous in that species but was similar in both years. Predicted chick-fledging based on vitellogenin analyses was within one day of first sightings of fledglings at sea in both years, confirming that the vitellogenin technique provides accurate information on breeding chronology. Percentage of egg producers (54% in 1999, 56% in 2000) were similar in both years. Vitellogenin analyses provided a chronology very similar to that previously estimated using multiple techniques in the same study area (1996-1998), confirming that vitellogenin analyses alone may be used to describe chronology when sampling encompasses the entire laying period. We recommend that technique, for use in other studies of secretive species where egg production cannot normally be monitored by direct observation.
43. Vezina, F; Salvante, KG; Williams, TD. (2003) The metabolic cost of avian egg formation: possible impact of yolk precursor production?Journal of Experimental Biology 206: 4443-4451 The metabolic cost of avian egg formation: possible impact of yolk precursor production?
egg production; energy cost; resting metabolic rate; RMR; vitellogenin; very-low-density lipoprotein; zebra finch; Taeniopygia guttata; yolk precursor production
Little is known about the energy costs of egg production in birds. We showed in previous papers that, during egg production, European starlings (Sturnus vulgaris) undergo a 22% increase in resting metabolic rate (RMR) and that the maintenance and activity costs of the oviduct are responsible for 18% of the variation in elevated laying RMR. Therefore, other energy-consuming physiological mechanisms must be responsible for the remaining unexplained variation in elevated laying RMR. Yolk precursor [vitellogenin (VTG) and very-low-density lipoprotein (VILDL)] production is likely to be costly because it signifies a marked increase in the biosynthetic activity of the liver. We documented the pattern of yolk precursor production in response to daily injections of 17beta-estradiol (E-2) in zebra finches (Taeniopygia guttata). Based on this pattern we carried out an experiment in order. to evaluate the metabolic costs of producing VTG and VLDL. Our E-2 treatment resulted in a significant increase in plasma VTG and VLDL levels within the natural breeding range for the species. Although RMR was measured during the period of active hepatic yolk precursor production, it did not differ significantly within individuals in response to the treatment or when comparing E-2-treated birds with sham-injected birds. This could mean that yolk precursor production represents low energy investment. However, we discuss these results in light of possible adjustments between organs that could result in energy compensation.
42. Vezina, F; Williams, TD. (2003) Plasticity in body composition in breeding birds: What drives the metabolic costs of egg production?Physiological and Biochemical Zoology 76: 716-730 Plasticity in body composition in breeding birds: What drives the metabolic costs of egg production?
Body composition in vertebrates is known to show phenotypic plasticity, and changes in organ masses are usually rapid and reversible. One of the most rapid and reversible changes is the transformation of the female avian reproductive organs before breeding. This provides an excellent system to investigate the effects of plasticity in organ size on basal metabolic rate (BMR) through relationships between organ masses and BMR. We compared body composition of female European starlings (Sturnus vulgaris) during various reproductive stages over 3 yr and investigated the pattern of changes in reproductive and nonreproductive organ mass during follicular development and ovulation. Furthermore, we analyzed the relationship between organ mass and resting metabolic rate (RMR) in nonbreeding, laying, and chick-rearing females. Our analysis revealed marked variation in organ masses between breeding stages but no consistent pattern among years except for kidney and pectoralis muscle. Furthermore, changes in nonreproductive organs did not parallel the cycle of growth and regression of the reproductive organs. The oviduct gained 62% of its 22-fold increase in mass in only 3 d, and oviduct regression was just as rapid and began even before the final egg of the clutch was laid, with 42% of the oviduct mass lost before laying of the final egg. In laying females, 18% of variation in mass-corrected RMR was explained by the mass of the oviduct (r(2) = 0.18, n = 80, P < 0.0005), while pectoralis muscle mass in nonbreeding individuals and liver and gizzard mass in chick-rearing females were the only organs significantly related to RMR (r(2) = 0.31-0.44). We suggest that the nonreproductive organs are affected more by changes in local ecological conditions than the reproductive state itself and that the activity and maintenance cost of the oviduct is high enough that selection has led to a very tight size-function relationship for this organ.
41.Williams, TD; Christians, JK. (2003) Experimental dissociation of the effects of diet, age and breeding experience on primary reproductive effort in zebra finches Taeniopygia guttata.Journal of Avian Biology 34: 379-386 Experimental dissociation of the effects of diet, age and breeding experience on primary reproductive effort in zebra finches Taeniopygia guttata
Reproductive performance varies with age in a wide range of organisms, and increasingly such patterns are interpreted in terms of state-dependent models. We sought to characterise 'state' with regards to age-related variation in clutch size, egg mass and timing of breeding in captive zebra finches Taeniopygia guttata, focusing on the roles of diet quality, age and breeding experience. Females on a high-quality diet laid larger clutches of larger eggs than did females on a low-quality diet. The effect of age on reproductive performance was examined by comparing females breeding (i.e. paired) for the first time at either 3- and/or 6-months of age. Clutch size increased with age but on the low-quality diet only, not on the high-quality diet. Furthermore, clutch size decreased between 3- and 6-months of age in birds bred first on the high-quality diet and then on the low-quality diet. Age did not affect egg mass but older birds had shorter laying intervals. Reproductive performance did not differ between females breeding at 6-months of age for the first or second time: the effects of age were not due to 'training' effects or experience specific to breeding (e.g. undergoing the physiological process of egg formation). In conclusion, nutritional condition (diet) emerged as a central component of state that could strongly influence, and even reverse, any age-dependent increase in primary reproductive performance.
40.Williams, TD; Miller, M. (2003) Individual and resource-dependent variation in ability to lay supranormal clutches in response to egg removal.Auk 120: 481-489 Individual and resource-dependent variation in ability to lay supranormal clutches in response to egg removal
We investigated individual and resource-dependent variation in ability of female Zebra Finches (Taeniopygia guttata) to lay supranormal clutches in response to egg removal, and effect of continuous laying on (1) egg composition and (2) plasma yolk precursor levels. Egg removal significantly increased the number of eggs that individual females laid, but that response was diet-dependent: on a high-quality (egg-supplemented) diet, females laid 12.4 +/- 1.0 more eggs compared with their pretreatment clutch size; whereas on the low-quality (seed-only) diet, females laid only 4.9 +/- 1.2 more eggs. Removal clutch size (i.e. total number of eggs laid in response to egg removal) was positively correlated with pretreatment mean egg mass and clutch size on the low-quality diet, but not on the high-quality diet. That suggests that there is interindividual variation in egg-laying ability ("large-egg" females had a greater capacity to respond to egg removal than "small-egg" females), but that higher resource levels can overcome individual differences. Egg mass did not vary with laying sequence in supranormal clutches (up to 22 eggs); however, there was a significant decrease (6%) in yolk protein content of additional eggs that was apparent by the tenth egg laid (i.e. only 4-5 more than the normal clutch size). Plasma levels of the two yolk precursors, vitellogenin and very-low-density lipoprotein (VLDL), were independent of diet and did not differ in individual birds at the 1 egg stage versus the 14 egg stage. However, there was a systematic change in relationship between yolk lipid content and plasma VLDL levels, from nonsignificant for third-laid eggs to significant and positive for sixteenth-laid eggs. We propose a possible mechanism linking female condition and egg-laying ability: good quality females, capable of laying extended clutches, are able to maintain production of generic VLDL for their own metabolic needs, as well as producing yolk-targeted VLDL, whereas poor quality females are not.
39. Christians, JK; Williams, TD. (2002) Effects of porcine follicle-stimulating hormone on the reproductive performance of female zebra finches (Taeniopygia guttata).General and Comparative Endocrinology 125: 121-131 Effects of porcine follicle-stimulating hormone on the reproductive performance of female zebra finches (Taeniopygia guttata)
FSH; egg production; egg size; clutch size; trade-off; phenotypic engineering
It has been suggested that follicle-stimulating hormone (FSH) may play a role in egg size/number trade-offs in oviparous vertebrates. We tested this hypothesis in an avian species by administering porcine FSH (pFSH) to intact, captive female zebra finches (Taeniopygia guttata) during egg formation. We predicted that (1) pFSH would increase the number of ovarian follicles recruited into rapid yolk development and so increase clutch size, (2) an increase in clutch size would lead to a reduction in egg size, and (3) doses of pFSH that were not sufficient to increase clutch size would increase yolk deposition and so increase egg mass. Although a range of pFSH doses decreased egg mass by ca. 10% in three separate experiments, the reduction in egg mass occurred in the absence of an increase in the number of eggs laid. Porcine FSH decreased mean clutch size significantly in one experiment and reduced median clutch size significantly in the other two experiments. The results of this study did not support the hypothesis that FSH mediates a trade-off between egg size and clutch size in birds. (C) 2002 Elsevier Science (USA).
38. Guglielmo, CG; Haunerland, NH; Hochachka, PW; Williams, TD. (2002) Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird.American Journal of Physiology-Regulatory Integrative and Comparative Physiology 282: R1405-R1413 Seasonal dynamics of flight muscle fatty acid binding protein and catabolic enzymes in a migratory shorebird
endurance exercise; fuel selection; lipid transport; metabolism
We developed an ELISA to measure heart-type fatty acid binding protein (H-FABP) in muscles of the western sandpiper (Calidris mauri), a long-distance migrant shorebird. H-FABP accounted for almost 11% of cytosolic protein in the heart. Pectoralis H-FABP levels were highest during migration (10%) and declined to 6% in tropically wintering female sandpipers. Premigratory birds increased body fat, but not pectoralis H-FABP, indicating that endurance flight training may be required to stimulate H-FABP expression. Juveniles making their first migration had lower pectoralis H-FABP than adults, further supporting a role for flight training. Aerobic capacity, measured by citrate synthase activity, and fatty acid oxidation capacity, measured by 3-hydroxyacyl-CoA- dehydrogenase and carnitine palmitoyl transferase activities, did not change during premigration but increased during migration by 6, 12, and 13%, respectively. The greater relative induction of H-FABP (+70%) with migration than of catabolic enzymes suggests that elevated H-FABP is related to the enhancement of uptake of fatty acids from the circulation. Citrate synthase, 3-hydroxyacyl-CoA-dehydrogenase, and carnitine palmitoyl transferase were positively correlated within individuals, suggesting coexpression, but enzyme activities were unrelated to H-FABP levels.
37. Guglielmo, CG; O'Hara, PD; Williams, TD. (2002) Extrinsic and intrinsic sources of variation in plasma lipid metabolites of free-living western sandpipers (Calidris mauri).Auk 119: 437-445 Extrinsic and intrinsic sources of variation in plasma lipid metabolites of free-living western sandpipers (Calidris mauri)
Plasma lipid metabolites may be useful indicators of mass changes in migratory birds. To test utility of plasma metabolites in field studies, we examined effects of several extrinsic (bleed time, time of day, location) and intrinsic (body mass, sex, age, migratory state) factors on plasma concentrations of triglycerides (TRIG), glycerol (GLYC), and B-OH-butyrate (BUTY) in free-living Western Sandpipers (Calidris mauri). TRIG and GLYC decreased rapidly following capture (2-20 min), whereas BUTY did not change. GLYC and BUTY were negatively correlated to body mass. TRIG was positively correlated to body mass in migrant females, but not consistently in migrant males, or in females captured on the wintering grounds. Taking into account other sources of variation, the two measures of lipid utilization (GLYC and BUTY) varied little through the year. TRIG showed the greatest potential for use in field studies. TRIG was lowest during winter, when birds were leanest, and highest during spring and fall migration, when sandpipers were gaining mass rapidly at stopovers. TRIG differed between sandpipers refuelling a two stopover sites separated by 35 km, demonstrating that populations of birds can have characteristic lipid metabolite profiles that may reflect local differences in fattening rate. Received 12 February 2001, accepted 12 December 2001.
36. Guglielmo, CG; Williams, TD; Zwingelstein, G; Brichon, G; Weber, JM. (2002) Plasma and muscle phospholipids are involved in the metabolic response to long-distance migration in a shorebird.Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 172: 409-417 Plasma and muscle phospholipids are involved in the metabolic response to long-distance migration in a shorebird
bird; exercise; lipid; nutrition; substrate metabolism
We studied: (1) concentrations and fatty acid compositions of plasma non-esterified fatty acids, neutral lipids, and phospholipids, and (2) fatty acid composition of flight muscle phospholipids in wintering, premigratory, and spring and fall migrating western sandpipers (Calidris mauri). Plasma neutral lipid and phospholipid levels were elevated in migrants, reflecting high rates of fat deposition. An important role of phospholipids in fattening is suggested by the fact that the amount of fatty acids in plasma phospholipids was similar to, or in spring as much as twice, that of neutral lipids. Changes in the ratio of plasma neutral lipids to phospholipids may indicate seasonal changes in triacylglycerol stores of invertebrate prey. Monounsaturation and total unsaturation of plasma neutral lipids and phospholipids increased during migration. Muscle phospholipids were more monounsaturated in spring and fall, but total unsaturation was reduced in fall. Arachidonic acid [20:4(n-6)] was especially abundant in muscle phospholipids In winter (29%) and declined during migration (19-22%), contributing to a decline in the ratio of n-6 to n-3 fatty acids. The abundance of plasma phospholipids and variability of neutral lipid to phospholipid ratio indicates that measurement of plasma phospholipids will improve methods for assessment of fattening rates of birds. The functional significance of changes in muscle phospholipids is unclear, but may relate to depletion of essential n-6 fatty acids during exercise.
35. McFarland, CN; Bendell-Young, LI; Guglielmo, C; Williams, TD. (2002) Kidney, liver and bone cadmium content in the western sandpiper in relation to migration.Journal of Environmental Monitoring 4: 791-795 Kidney, liver and bone cadmium content in the western sandpiper in relation to migration
Cadmium content was measured in kidney, liver and tarsus bones of western sandpipers (Calidris mauri) at a temperate migratory stopover site ( Fraser Delta, British Columbia, Canada) and a wintering site ( Playa el Agallito, Chitre, Panama) over a two year period. Cadmium content in liver and kidney was age and sex dependent. Adult females generally had lower kidney and liver cadmium than adult males (P < 0.05), but a sex difference was not detected in juveniles. Cadmium increased with age in kidney, liver and to a lesser extent in bone (P < 0.001) with average "steady-state" kidney and liver content being reached within the sandpipers first year. In general, tissue cadmium residues in adult males and females were independent of sampling location although for bone, site-specific differences did occur (P < 0.001). Bone cadmium was lower in females sampled from their wintering grounds as compared to temperate stopover sites suggesting that bone cadmium may be mobilized during periods of feather molt. Comparison of cadmium residues among sandpipers of increasing age suggest that exposure is occurring along the Pacific Coast, at stopover sites as the birds migrate north to Alaska and south to Panama. This study points to the importance of considering the ecology of the species (e.g., in this case migratory behavior) in interpreting trace metal residues.
34. Salvante, KG; Williams, TD. (2002) Vitellogenin dynamics during egg-laying: daily variation, repeatability and relationship with egg size.Journal of Avian Biology 33: 391-398 Vitellogenin dynamics during egg-laying: daily variation, repeatability and relationship with egg size
Daily variation in circulating levels of the avian yolk precursor, vitellogenin (VTG), throughout the laying cycle was investigated in female zebra finches Taeniopygia guttata and compared with predicted ovarian follicle demand (based on a model of follicular development for this species). In general, the pattern of variation in plasma VTG matched the predicted demand from the developing ovarian follicle hierarchy. Plasma VTG was non-detectable in non-breeders, but increased rapidly with onset of yolk development, remaining high (1.43-1.82 mug/ml, zinc) through to the 3-egg stage. Plasma levels then declined at the 5-egg stage (to 0.78 +/- 0.32 mug/ml) and were undetectable at clutch completion. This result is consistent with the hypothesis that yolk precursor production is costly and that selection has matched supply and demand. While inter-individual variation in plasma VTG was marked (e.g. 0.47-4.26 mug/ml at the I-egg stage), it also exhibited high intra-individual repeatability (r = 0.87-0.93). Finally, we examined the relationship between plasma VTG and primary reproductive effort. While individual variation in plasma VTG was independent of clutch size, laying interval and laying rate, there was a complex, diet-dependent relationship between VTG and egg size, with low plasma VTG levels being associated with both very small (< 0.90 g) and very large (> 1.15 g) egg sizes.
33. Vezina, F; Williams, TD. (2002) Metabolic costs of egg production in the European starling (Sturnus vulgaris).Physiological and Biochemical Zoology 75: 377-385 Metabolic costs of egg production in the European starling (Sturnus vulgaris)
The energy cost of egg production in passerine birds has typically been estimated to be 45%-60% of basal metabolic rate (BMR), but this is based on theoretical models using data on energy content of eggs and reproductive tissue; there are still very few empirical data on egg production costs. In this study, we directly measured resting metabolic rate (RMR) in egg-laying female European starlings (Sturnus vulgaris) over 3 yr. We compared these data with RMR of nonbreeding and chick-rearing birds and with estimated energy expenditure generated from a typical energy content model by using empirically derived data from body composition analysis for this species. We found marked variation in RMR between years and between reproductive stages, which complicates comparisons among breeding stages for the assessment of relative egg production costs. On the basis of this method, RMR during egg laying varied from +74% to -13% of nonbreeding RMR and from +20% to -7% of chick-rearing RMR. We therefore used an alternate approach: measuring changes in RMR through the complete cycle of follicle development and ovulation. The increase in RMR from the beginning of prelaying to the six-follicle stage ( before first ovulation) when birds have a complete developing follicle hierarchy was 22.4%. This value is still much lower than that estimated from our energy content model. We discuss conceptual problems associated with the theoretical energy content approach but also suggest, on the basis of earlier work done in our lab, that the measured increase in RMR might still underestimate the actual cost of egg production if birds reallocate energy between different physiological systems.
32. Challenger, WO; Williams, TD; Christians, JK; Vezina, F. (2001) Follicular development and plasma yolk precursor dynamics through the laying cycle in the European starling (Sturnus vulgaris).Physiological and Biochemical Zoology 74: 356-365 Follicular development and plasma yolk precursor dynamics through the laying cycle in the European starling (Sturnus vulgaris)
We investigated the quantitative matching of plasma yolk precursor supply (the plasma pool) to follicle demand during yolk formation in European starlings (Sturnus vulgaris). Plasma concentrations of the two yolk precursors, vitellogenin (VTG) and very low density lipoprotein (VLDL), were only elevated coincident with rapid yolk development (RYD) and matched variation in total yolky follicle mass. VTG and VLDL were low (<0.4 <mu>g/mL and <4.2 mg/mL, respectively) in nonbreeders and prebreeders with no yolky follicles, and at clutch completion. They increased to 4.02 <mu>g/mL and 19.4 mg/mL in birds with a full follicle hierarchy (F-1-F-4), and concentrations then remained high and actually increased up to the point where only a single, yolky (F-1) follicle remained. However, there was some evidence for mismatching of supply and demand: (a) precursor concentrations increased throughout the laying cycle even though the number of developing follicles decreased. We suggest that this is because of a requirement to maintain a large precursor pool to maintain high uptake rates; and (b) in birds with a full follicle hierarchy, precursor concentrations were negatively correlated with total follicle mass. This suggests that high uptake rates in large follicles can actually deplete circulating precursor concentrations. Plasma concentrations of both yolk precursors increased rapidly in the early morning with (predicted) time after ovulation, consistent with a lack of fine control of precursor concentrations. However, mean plasma VTG concentrations did not differ between morning or evening samples. In contrast, plasma VLDL concentrations were lower in the morning (16.8 mg/mL) than in the evening (22.9 mg/mL). Although there is marked individual variation in plasma VTG and VLDL (four- to eightfold), both precursors were repeatable in the short term (24 h), and plasma VTG was repeatable over a 14-d interval between successive breeding attempts.
31. Christians, JK; Williams, TD. (2001) Interindividual variation in yolk mass and the rate of growth of ovarian follicles in the zebra finch (Taeniopygia guttata).Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 171: 255-261 Interindividual variation in yolk mass and the rate of growth of ovarian follicles in the zebra finch (Taeniopygia guttata)
intraspecific variation; egg size; rapid yolk development; repeatability; vitellogenin
The amount of resources invested in an individual egg yolk must be determined by its rate of growth and/or the duration of growth. We examined interindividual variation in the growth rate of yolks by injecting radiolabeled amino acid into breeding female zebra finches and measuring the activity associated with protein in the yolks of eggs laid subsequently. We predicted that (1) there would be a positive correlation between yolk mass and the rate of uptake of activity into the yolk; and (2) there would be a negative correlation between clutch size and the amount of activity taken up by each of the follicles due to competition between follicles for circulating yolk precursors. The rate of uptake of activity by the yolks was positively related to yolk mass (r(2)=0.24, 0.35 and 0.50 for the yolks of the third-, fourth- and fifth-laid eggs, respectively), suggesting that interindividual variation in yolk mass is due, at least in part, to variation in the rate of follicle growth. However, we found no evidence of a trade-off between yolk size and number. The uptake of activity was generally repeatable between breeding attempts (repeatability = 0.23-0.44), as was mean yolk mass (repeatability = 0.35), suggesting that these traits are characteristics of individual females.
30. Christians, JK; Williams, TD. (2001) Intraspecific variation in reproductive physiology and egg quality in the European Starling Sturnus vulgaris.Journal of Avian Biology 32: 31-37 Intraspecific variation in reproductive physiology and egg quality in the European Starling Sturnus vulgaris
Egg mass shows large intraspecific variation in birds and is repeatable within individuals. The mechanisms underlying this variation are unknown. We hypothesized that measures of egg quality (the mass of yolk protein, yolk lipid, and albumen protein) would be positively correlated with the plasma pools of the yolk precursor vitellogenin, and the masses of the oviduct, metabolic machinery (liver, heart, lungs, kidneys, gizzard, small intestine and pancreas), and endogenous stores of protein and lipid. We tested these predictions in European Starlings Sturnus vulgaris is collected at the peak of egg production effort. In contrast to our predictions, both yolk protein and yolk lipid were negatively correlated with plasma vitellogenin levels. Albumen protein was positively related to oviduct mass, but other aspects of body composition failed to explain variation in egg quality. Hence, while we observed correlations between egg composition and peripheral systems (circulating precursor pools and the oviduct), we found no evidence that egg quality is determined by more general processes, i.e., the supply and processing of nutrients.
29. Clair, CCS; Clair, RCS; Williams, TD. (2001) Does kleptoparasitism by glaucous-winged gulls limit the reproductive success of Tufted Puffins?Auk 118: 934-943 Does kleptoparasitism by glaucous-winged gulls limit the reproductive success of Tufted Puffins?
Interspecific kleptoparasitism (food stealing) occurs in many seabird species and can sometimes significantly affect host individuals and populations. We investigated effects of kleptoparasitism by Glaucous-winged Gulls (Larus glaucescens) on a population of Tufted Puffins (Fratercula cirrhata) in which almost all chicks die before fledging in some years, Rates of kleptoparasitism were estimated during two seasons and compared with several spatial and temporal factors that have been predicted to influence kleptoparasitism rates both within and among seasons. Kleptoparasitism rates increased from 2% in the first year to 19% in the second, whereas puffin fledging success declined precipitously from 81% in the first year to 11% in the second. Within years, kleptoparasitism rates increased with number of puffins returning with fish, decreased during fair weather, and were unaffected by tidal height. Spatially, those rates increased with puffin burrow,, density and declined with angle of the nesting slope. Gull kleptoparasitism success increased during foul weather and at higher puffin nesting elevations. Despite those associations, survival of puffin chicks was not influenced by kleptoparasitism activity near their nests although it increased with a combination of low elevation and high slope at the nesting burrow. Neither kleptoparasitism nor predation by gulls were exceptional relative to other seabird colonies and they were unlikely to cause reproductive failures that characterize puffins at that site. Other factors, particularly food shortages at sea, merit further attention in explaining those failures.
28. Guglielmo, C; Piersma, T; Williams, TD. (2001) A sport-physiological perspective on bird migration: Evidence for flight-induced muscle damage.Journal of Experimental Biology 204: 2683-2690 A sport-physiological perspective on bird migration: Evidence for flight-induced muscle damage
bird; capture stress; creatine kinase; exercise; flight; migration; muscle damage; settling time; Calidris mauri; Limosa lapponica
Exercise-induced muscle damage is a well-described consequence of strenuous exercise, but its potential importance in the evolution of animal activity patterns is unknown. We used plasma creatine kinase (CK) activity as an indicator of muscle damage to investigate whether the high intensity, long-duration flights of two migratory shorebird species cause muscle damage that must be repaired during stopover. In two years of study, plasma CK activity was significantly higher in migrating western sandpipers (a non-synchronous, short-hop migrant), than in non-migrants. Similarly, in the bar-tailed godwit (a synchronous, long-jump migrant), plasma CK activity was highest immediately after arrival from a 4000-5000 km flight from West Africa to The Netherlands, and declined before departure for the arctic breeding areas. Late-arriving godwits had higher plasma CK activity than birds that had been at the stopover site longer. Juvenile western sandpipers making their first southward migration had higher plasma CK activity than adults. These results indicate that muscle damage occurs during migration, and that it is exacerbated in young, relatively untrained birds. However, the magnitude of the increases in plasma CK activity associated with migratory flight were relatively small, suggesting that the level of muscle damage is moderate. Migrants may avoid damage behaviourally, or have efficient biochemical and physiological defences against muscle injury.
27. Shepherd, PCF; Lank, DB; Smith, BD; Warnock, N; Kaiser, GW; Williams, TD. (2001) Sex ratios of Dunlin wintering at two latitudes on the Pacific coast.Condor 103: 352-360 Sex ratios of Dunlin wintering at two latitudes on the Pacific coast
Calidris alpina; Dunlin; latitudinal cline; maximum likelihood model; morphometric measurement error; sex ratio; shorebirds
Latitudinal dines in sex ratio during the nonbreeding season occur in some shorebirds of the Scolopacidae. We compared populations of nonbreeding Dunlin (Calidris alpina pacifica) from two latitudes along the Pacific flyway: the Fraser River Delta, British Columbia, and Bolinas Lagoon, California, to determine whether, and to what degree, they exhibited sex ratios consistent with a latitudinal cline. Dunlin are plumage monomorphic, so we used a maximum likelihood model to estimate overall and monthly sex ratios for each population based on culmen length distributions. Sex ratios in the Fraser River Delta were corrected for sex differences in habitat use. Monthly sex ratios were similar at the two sites but varied throughout the winter, likely reflecting differences in seasonal movement patterns between the sexes. Both populations showed an overall bias toward males (Fraser = 61% males, Bolinas = 65% males). Since there is no evidence to support the possibility of a skew toward males in C. a. pacifica as a whole, our data are consistent with some form of latitudinal dine in the sex ratio of C. a. pacifica. However, additional data from the Oregon coast, southern California, and Mexico are required to resolve this question. We also tested the hypothesis that mean body size within each sex is larger at the higher-latitude site (Fraser River Delta), but this did nor appear to be the case.
26.Williams, TD. (2001) Experimental manipulation of female reproduction reveals an intraspecific egg size-clutch size trade-off.Proceedings of the Royal Society of London Series B-Biological Sciences 268: 423-428 Experimental manipulation of female reproduction reveals an intraspecific egg size-clutch size trade-off
egg size; clutch size; trade-off; physiological manipulation
A negative relationship, or trade-off, between egg size and clutch size is a central and long-standing component of life-history theory, yet there is little empirical evidence for such a trade-off, especially at the intraspecific level. Here, I show that female zebra finches (Taeniopygia guttata) treated chronically during egg formation with the anti-oestrogen tamoxifen lay smaller eggs (by 8%) but produce larger clutches (on average two eggs more) than controls. Decreased egg mass in tamoxifen-treated females was associated with a 50% decrease in plasma levels of the two yolk precursors, vitellogenin and very-low-density lipoprotein. Although tamoxifen-treated females laid more; smaller eggs (and had a higher total expenditure in their clutch), they did not differ from controls in the number of chicks fledged: the mass or size of these chicks at fledging, or the chicks' egg-production performance at three months of age. However, tamoxifen-treated females had lower relative hatching success: they laid more eggs but hatched the same number of chicks. Among individual tamoxifen-treated females, birds that laid the smallest eggs early in their laying sequence laid the largest number of additional eggs, that is, there was a negative correlation, or trade-off between egg size and clutch size.
25. Egeler, O; Williams, TD. (2000) Seasonal, age, and sex-related variation in fatty-acid composition of depot fat in relation to migration in Western Sandpipers.Auk 117: 110-119 Seasonal, age, and sex-related variation in fatty-acid composition of depot fat in relation to migration in Western Sandpipers
The composition of depot fat in Western Sandpipers (Calidris mauri) was dominated by C-16 and C-18 fatty acids (palmitate, 16:0; palmitoleate, 16:1; stearate, 18:0; oleate, 18:1), which together comprised 80 to 90% of all fatty acids analyzed. Significant seasonal variation occurred in the relative proportion of specific fatty acids and the ratio of saturated to unsaturated fatty acids in relation to the migratory cycle of the sandpipers. In adults of both sexes, the proportion of 16:0 and 18:0 fatty acids decreased from winter (December) to premigration (March) to spring migration (May), whereas the proportion of 16:1 and 18:1 fatty acids increased over these same periods. Consequently, total unsaturated fatty acids increased by 34% between the winter and premigratory phase, and by a further 22% between premigration and spring migration. Therefore, biochemical modification of adipose tissue in Western Sandpipers begins during the premigratory period in preparation for long-distance flight but continues as migration progresses, perhaps reflecting a training component of physiological modulation for migration. Juveniles showed similar changes to adults in the composition of their depot fat during the "premigratory" period, even though most juveniles do not undergo hyperphagia or rapid fattening at this wintering site. Potential prey species collected from a wintering site in Panama had a higher proportion of saturated fatty acids, less 16:1 and 18:1, and more 18:0 fatty acid compared with those from a migratory stopover site in British Columbia, paralleling the seasonal changes in depot fatty-acid composition observed in Western Sandpipers. However, the fact that Western Sandpipers show an increase in level of unsaturation and in the amounts of 16:1 and 18:1 fatty acids in their fat stores on the wintering ground prior to migration suggests that seasonal variation in fatty-acid composition is not entirely diet dependent.
24. Egeler, O; Williams, TD; Guglielmo, CG. (2000) Modulation of lipogenic enzymes, fatty acid synthase and Delta(9)-desaturase, in relation to migration in the western sandpiper (Calidris mauri).Journal of Comparative Physiology B-Biochemical Systemic and Environmental Physiology 170: 169-174 Modulation of lipogenic enzymes, fatty acid synthase and Delta(9)-desaturase, in relation to migration in the western sandpiper (Calidris mauri)
migration; lipogenesis; lipogenic enzymes; intraspecific variation
Long-distance migration in birds is characterized physiologically by periods of rapid fattening and lipogenesis, and increased desaturation of fatty acids stored in adipose tissue. We investigated seasonal, age- and sex-related differences in activities of two lipogenic enzymes, fatty acid synthase and Delta(9)-desaturase, in relation to migration in the small, Arctic-nesting western sandpiper (Calidris mauri). Migration, and associated lipogenesis and fattening, involved marked upregulation of these enzymes in this species. However, this increase in enzyme activity was only seen in actively migrating birds during spring migration, when fatty acid synthase and Delta(9)-desaturase levels increased by 53% and 113%, respectively, compared to Iron-migrating birds. There was no change in fatty acid synthase enzyme activity during the premigration period, even though body mass of adult birds increased significantly during this period. Similarly, there was no increase in Delta(9)-desaturase activity during premigration, despite the fact that birds increase the proportion of monounsaturated fatty acids in their fat stores at this time. We suggest that upregulation of lipogenic enzymes is required to support high rates of mass gain (0.4 g day(-1)) during short (1-4 day) periods at stop-over sites. However, slower rates of mass gain (0.09 g day(-1)) over several weeks prior to migration can be achieved without any increase in tissue-specific enzyme activity.
23. Moore, DJ; Williams, TD; Morris, RD. (2000) Mate provisioning, nutritional requirements for egg production, and primary reproductive effort of female Common Terns Sterna hirundo.Journal of Avian Biology 31: 183-196 Mate provisioning, nutritional requirements for egg production, and primary reproductive effort of female Common Terns Sterna hirundo
We assessed the nutritional importance of male provisioning to females during egg production and its effects on clutch parameters (egg size, length of the laying period) in Common Terns Sterna hirundo: (1) we estimated the costs of egg production by modeling the daily protein, lipid, and energy requirements of laying females, and (2) compared these costs to both the amount, and the timing, of the male's contribution via mate provisioning. Net lipid, net protein, and gross energy requirements for a three-egg clutch were estimated to be 5.4 g, 8.6 g, and 569 kJ respectively. Peak protein and lipid requirements occurred one (day - 1) and two (day - 2) days before laying, respectively. peal; energy requirement occurred on day - 1; a cost of 127% to 157% above maintenance. Variation in male provisioning effort (in terms of energy and nutrients delivered) paralleled variation in predicted female requirements For egg production at the level of individual pairs. Males delivered protein in excess of the female's requirements on all days investigated. Male lipid delivery accounted for 45% of female net requirement on the day when demand was greatest (day - 2), but exceeded requirements on all other days. However, the proportion of the female's total energy budget (egg production, maintenance, and activity costs) that was supplied by her mate rose from an average of 29% on day - 2 to 76% during the interval between second and third eggs. Paradoxically, females that were fed at higher rates during the interval between first and second eggs produced clutches with lower total volumes, smaller last-laid eggs, and clutches with a greater egg-size hierarchy than conspecifics receiving less food from their mates. Also, females fed at higher rates during the interval between second and third eggs took longer to produce their clutch. These negative relationships between mate provisioning and clutch parameters contrast with previous studies in this and other species.
22. Vanderkist, BA; Williams, TD; Bertram, DF; Lougheed, LW; Ryder, JL. (2000) Indirect, physiological assessment of reproductive state and breeding chronology in free-living birds: an example in the Marbled Murrelet (Brachyramphus marmoratus).Functional Ecology 14: 758-765 Indirect, physiological assessment of reproductive state and breeding chronology in free-living birds: an example in the Marbled Murrelet (Brachyramphus marmoratus)
physiological methods; Ptychoramphus; vitellogenin Murrelets; Marbled Murrelets;
1. An indirect, physiological method to assess reproductive state in individuals of unknown status is described. The plasma levels of two main yolk precursors, vitellogenin (VTG) and very-low density lipoproteins (VLDL), are focused on as indices of egg production, for the characterization of fecund females. 2. Data for a species where breeding chronology could be directly assessed, at the population level (Cassin's Auklet. Ptychoramphus aleuticus), confirmed the validity of this approach: plasma VTG levels were highest during the defined egg-laying period, and the highest proportion of females were defined as 'egg-producing' in this period. 3. Analysis of samples for Marbled Murrelets (Brachyramphus marmoratus) caught off-nest (i.e. where all individuals were of unknown status), clearly identified a putative egg-laying phase, with a single, protracted laying period (cf multiple-broodiness). 4. Analysis of body mass confirmed our characterization of 'egg-producing' females: birds with elevated plasma VTG were on average 40 g heavier than other females, equivalent to the mass of the single egg (36-41 g). 5. Indirect, physiological assessment of reproductive state provided valuable information on the breeding biology of Marbled Murrelets which would have been difficult to obtain in any other way (e.g. proportion of fecund females, breeding phenology, single vs multiple-clutch breeding pattern). Despite some limitations, this technique should be applicable to any oviparous vertebrate population where essential information on breeding biology cannot be obtained by more traditional methods.
21. Vanderkist, BA; Williams, TD; Bertram, DF; Lougheed, LW; Ryder, JL. (2000) Indirect, physiological assessment of reproductive state and breeding chronology in free-living birds: an example in the Marbled Murrelet (Brachyramphus marmoratus).Funct. Ecol. 14: 758-765 Indirect, physiological assessment of reproductive state and breeding chronology in free-living birds: an example in the Marbled Murrelet (Brachyramphus marmoratus)
physiological methods; Ptychoramphus; vitellogenin
1. An indirect, physiological method to assess reproductive state in individuals of unknown status is described. The plasma levels of two main yolk precursors, vitellogenin (VTG) and very-low density lipoproteins (VLDL), are focused on as indices of egg production, for the characterization of fecund females. 2. Data for a species where breeding chronology could be directly assessed, at the population level (Cassin's Auklet. Ptychoramphus aleuticus), confirmed the validity of this approach: plasma VTG levels were highest during the defined egg-laying period, and the highest proportion of females were defined as 'egg-producing' in this period. 3. Analysis of samples for Marbled Murrelets (Brachyramphus marmoratus) caught off-nest (i.e. where all individuals were of unknown status), clearly identified a putative egg-laying phase, with a single, protracted laying period (cf multiple-broodiness). 4. Analysis of body mass confirmed our characterization of 'egg-producing' females: birds with elevated plasma VTG were on average 40 g heavier than other females, equivalent to the mass of the single egg (36-41 g). 5. Indirect, physiological assessment of reproductive state provided valuable information on the breeding biology of Marbled Murrelets which would have been difficult to obtain in any other way (e.g. proportion of fecund females, breeding phenology, single vs multiple-clutch breeding pattern). Despite some limitations, this technique should be applicable to any oviparous vertebrate population where essential information on breeding biology cannot be obtained by more traditional methods. DOI
20.Williams, TD. (2000) Experimental (Tamoxifen-Induced) manipulation of female reproduction in zebra finches (Taeniopygia guttata).Physiological and Biochemical Zoology 73: 566-573 Experimental (Tamoxifen-Induced) manipulation of female reproduction in zebra finches (Taeniopygia guttata)
Experimental manipulation of reproductive phenotype is a potentially powerful approach for understanding the fitness relationships of traits such as egg size, egg composition, and egg number. In this study, I investigated the effect of the antiestrogen tamoxifen on multiple, estrogen-dependent reproductive traits in female zebra finches (Taeniopygia guttata). Short-term tamoxifen treatment of egg-laying females (two daily injections before laying) had no effect on the timing or the pattern of egg laying compared to sham controls. However, tamoxifen treatment caused (1) a marked, but transient, decrease in egg size; (2) increased within-clutch egg-size variation; (3) a reduction in plasma vitellogenin (VTG) levels; and (4) lower dry yolk and yolk protein content of tamoxifen-treated females. Plasma levels of the second yolk precursor, very low density lipoprotein (VLDL), were not affected by tamoxifen, and tamoxifen appeared to have no effect on oviduct function in egg-laying females. These results are consistent with tamoxifen blocking estrogen receptors in the liver, suppressing VTG production, and decreasing the plasma pool of yolk precursors below a level required to maintain yolk formation at the normal rate. Tamoxifen treatment can therefore be used successfully to manipulate several components of the female reproductive phenotype (egg composition, intraclutch egg-size variation) to further explore the fitness consequences of these traits.
19.Williams, TD; Martyniuk, CJ. (2000) Tissue mass dynamics during egg-production in female Zebra Finches Taeniopygia guttata: dietary and hormonal manipulations.Journal of Avian Biology 31: 87-95 Tissue mass dynamics during egg-production in female Zebra Finches Taeniopygia guttata: dietary and hormonal manipulations
Changes in tissue masses associated with egg production were investigated in female Zebra Finches Taeniopygia gutatta using dietary and hormonal manipulations. We tested three hypotheses: that changes in organ masses, (a) reflect utilisation of endogenous nutrient stores due to inadequate daily dietary intake. (b) involve changes in organ structure or 'functional capacity', and (c) are initiated by onset of reproductive development (e.g. elevated plasma estrogen or yolk precursor levels, oviduct growth). Pectoral muscle lean dry mass was 18-22% lower in breeding females at the 1-egg stage compared to non-breeders, and this was independent of nutritional plane, i.e. similar changes occurred in birds provided with supplemental protein or egg food. Heart lean dry mass was also lower (16%) in breeding females, but only in birds on a low-quality seed diet, not in birds on supplemented diets. Decreases in total liver mass (14%) were due to changes in lipid content not lean dry mass, and were diet-dependent. These results demonstrate that changes in organ masses associated with egg production are complex, and do not simply reflect a general mobilisation of stored protein. We discuss why there is no hypertrophy of biosynthetic or metabolic 'machinery' associated with egg production in birds (cf. reproducing mammals). Exogenous 17 beta-estradiol induced plasma levels of yolk precursors typical of breeding birds, and initiated oviduct growth (to 31% of mature size). However, estradiol treatment caused no change in mass of pectoral muscle. heart or liver. demonstrating that there is no simple relationship between onset of reproductive development and associated tissue mass changes.
18. Butler, RW; Williams, TD; Bishop, MA; Warncock, N. (1999) Gone with the wind? Reply.Auk 116: 563-564 Gone with the wind? Reply
17. Christians, JK; Williams, TD. (1999) Organ mass dynamics in relation to yolk precursor production and egg formation in European starlings Sturnus vulgaris.Physiological and Biochemical Zoology 72: 455-461 Organ mass dynamics in relation to yolk precursor production and egg formation in European starlings Sturnus vulgaris
Egg production in passerines and other birds requires rapid synthesis of proteins and lipids. We hypothesized that these biosynthetic demands would necessitate hypertrophy of the liver, which produces the yolk precursors vitellogenin and very low-density Lipoprotein (VLDL), and of the metabolic machinery that supports the liver's biosynthetic activity (e.g., heart, kidneys, lungs, and digestive organs). To test this hypothesis, free-living female European starlings (Sturnus vulgaris) were collected through two breeding seasons. Change in liver mass in relation to breeding stage differed between years, as did the relationship between liver mass and plasma vitellogenin levels. In the first year, dry lean glycogen-free liver mass showed little seasonal variation and was not correlated with vitellogenin levels among egg-laying females. In the second year, liver mass was 4%-44% greater during egg laying than at other stages of breeding and was positively related to vitellogenin levels. In both years, the mass of the liver was not related to plasma VLDL levels. Thus, we did not find consistent relationships between liver mass and its biosynthetic output. In contrast to our hypotheses, the masses of the heart and digestive organs were lower during egg laying than they were before breeding. Meeting the biosynthetic demands of egg production does not appear to require hypertrophy of the liver or supporting metabolic machinery.
16. Christians, JK; Williams, TD. (1999) Effects of exogenous 17 beta-estradiol on tee reproductive physiology and reproductive performance of European starlings (Sturnus vulgaris).Journal of Experimental Biology 202: 2679-2685 Effects of exogenous 17 beta-estradiol on tee reproductive physiology and reproductive performance of European starlings (Sturnus vulgaris)
egg production; yolk; oocyte growth; vitellogenin; intraspecific variation; starling; Sturnus vulgaris
Egg mass shows large intraspecific variation in birds and yet the mechanisms underlying this variation remain unknown. We hypothesized that estradiol would play a central role in determining egg mass, since this hormone stimulates the production of yolk precursors (vitellogenin and very-low density lipoprotein, VLDL) by the liver, and of albumen by the oviduct. We gave European starlings (Sturnus vulgaris) silastic implants containing estradiol prior to egg formation, which we predicted would increase egg mass. As expected, exogenous estradiol stimulated a marked (49 %) increase in plasma vitellogenin levels at the beginning of laying. At clutch completion, plasma VLDL levels and oviduct mass were also elevated in estradiol-treated females compared with controls. However, estradiol had no effect on fresh egg mass or clutch size. Estradiol treatment actually decreased the mass of yolk protein and lipid, perhaps by decreasing the rate of uptake of yolk precursors at the ovary. The failure of estradiol to increase egg mass indicates that this phenotype may be regulated at higher levels of organization (e.g. negative feedback, uptake of yolk precursors) than those studied in this experiment. Despite elevating yolk precursor levels, treatment with estradiol had no effect on the mass of the liver or endogenous stores of protein and lipid at clutch completion.
15. Smits, JE; Williams, TD. (1999) Validation of immunotoxicology techniques in passerine chicks exposed to oil sands tailings water.Ecotoxicology and Environmental Safety 44: 105-112 Validation of immunotoxicology techniques in passerine chicks exposed to oil sands tailings water
avian immunocompetence; immunotoxicity; phytohemagglutinin skin test; antibody response; zebra finch; bioindicators
Avian species, through their trophic relationships, may represent ideal indicators for assessing environmental health. In this study several assays of immune function in young passerines are validated and compared. From 6 to 10 days of age, zebra finch nestlings (Taeniopygia guttata) were given daily oral doses of Oil Sands tailings water (CT), an immunosuppressant dexamethasone, or phosphate-buffered saline. At 9-10 days of age, a phytohemagglutinin (PHA) skin test of immune function was conducted; at 11 days of age, five chicks from each group were euthanized for gross and histopathologic examination of immune system organs. The remaining birds mere vaccinated with sheep red blood cells (srbc) to evaluate antibody-mediated immunity. The main findings were that in 10-day-old nestlings, T lymphocytes were sensitive to PHA stimulation, while B lymphocytes were unable to respond to srbc; that hematocrit was approximately 30% lower than in mature birds; that precision of leucocrit determination was heavily technique-dependent; that endogenous steroids increased the total leucocrit, while exogenous steroids increased heterophil and decreased lymphocyte counts, thus increasing H:L; that dexamethasone exposure temporarily reduced growth rate; that CT exposure stimulated germinal cell development in the bursa of Fabricius; and that dexamethazone and CT exposure were associated with decreased splenic white pulp formation. (C) 1999 Academic Press.
14. Vanderkist, BA; Xue, XH; Griffiths, R; Martin, K; Beauchamp, W; Williams, TD. (1999) Evidence of in male-bias in capture samples of Marbled Murrelets from genetic studies in British Columbia.Condor 101: 398-402 Evidence of in male-bias in capture samples of Marbled Murrelets from genetic studies in British Columbia
Brachyramphus marmoratus; male-bias; Marbled Murrelet; Marbled Murrelets;
We report a significant male-bias ( 1.8:1) in Marbled Murrelets (Brachyramphus marmoratus) captured with floating mist nets during the breeding season over four years (1994-1997) at Theodosia Inlet, Desolation Sound, British Columbia. There was little evidence for marked annual or diurnal variation in male-bias, or for variation due to flight direction of birds when the contacted the net (inland vs, out to sea). In contrast, samples of adult and juvenile Marbled Murrelets captured using a night-lighting technique at Desolation Sound in 1997 were not male-biased. We believe that the most likely explanation for our results is that there are sex-specific differences in behavior of Marbled Murrelets during the breeding period. such that more males than females are flying between marine foraging and inland nesting areas.
13. Vanderkist, BA; Xue, XH; Griffiths, R; Martin, K; Beauchamp, W; Williams, TD. (1999) Evidence of in male-bias in capture samples of Marbled Murrelets from genetic studies in British Columbia.Condor 101: 398-402 Evidence of in male-bias in capture samples of Marbled Murrelets from genetic studies in British Columbia
Brachyramphus marmoratus; male-bias; Marbled Murrelet
We report a significant male-bias ( 1.8:1) in Marbled Murrelets (Brachyramphus marmoratus) captured with floating mist nets during the breeding season over four years (1994-1997) at Theodosia Inlet, Desolation Sound, British Columbia. There was little evidence for marked annual or diurnal variation in male-bias, or for variation due to flight direction of birds when the contacted the net (inland vs, out to sea). In contrast, samples of adult and juvenile Marbled Murrelets captured using a night-lighting technique at Desolation Sound in 1997 were not male-biased. We believe that the most likely explanation for our results is that there are sex-specific differences in behavior of Marbled Murrelets during the breeding period. such that more males than females are flying between marine foraging and inland nesting areas. DOI
12.Williams, TD. (1999) Parental and first generation effects of exogenous 17 beta-estradiol on reproductive performance of female zebra finches (Taeniopygia guttata).Hormones and Behavior 35: 135-143 Parental and first generation effects of exogenous 17 beta-estradiol on reproductive performance of female zebra finches (Taeniopygia guttata)
17 beta-estradiol; female reproductive effort; intergenerational effects
Steroids hormones have numerous "activational" effects in adult birds, regulating sexual behavior, and more recently maternal androgens have been shown to have potentially important "organizational" effects in ovo, influencing offspring growth, development, and behavior. In this study I investigated parental and first-generation effects of exogenous estrogens on female reproduction in zebra finches (Taeniopygia guttata). 17 beta-Estradiol (E-2; 1.2 mu g/g, 4 daily injections i.m.) elevated plasma levels of the yolk precursors, vitellogenin (VTG) and very low-density lipoprotein (VLDL), in nonbreeding females to levels similar to those of breeding females. However, E-2-treatment of breeding females caused no significant change in plasma VTG or VLDL levels compared to control birds (measured at the 1-egg stage), and there was no difference in reproductive performance between groups (egg size, clutch size, timing of laying). E-2-treated females produced significantly more daughters than sons (21F:8M) at fledging, compared to control females (18F:19M). Nestling mortality was significantly higher in broods of E-2-treated females, suggesting that the skewed sex ratio may have resulted from differential mortality of male chicks. The pattern of chick mortality in E-2-broods was not consistent with this being caused by estrogen-mediated changes in parental behavior (e.g., provisoning). Mean egg mass of daughters of E-2-treated females was typical of experienced, adult breeders, and larger than normal, first-time breeders or control offspring (0.947 vs 0.850 g). There was no treatment effect on offspring clutch size or laying interval. These results suggest that early exposure to maternal estrogens in ovo might be involved in establishing intraindividual variation in female-specific phenotypic traits, as has previously been demonstrated for androgens and mate behavioral traits (e.g., aggression). (C) 1999 Academic Press.
11.Williams, TD; Christians, JK; Aiken, JJ; Evanson, M. (1999) Enhanced immune function does not depress reproductive output.Proceedings of the Royal Society of London Series B-Biological Sciences 266: 753-757 Enhanced immune function does not depress reproductive output
immune function; reproductive effort; trade-offs
Costs of reproduction might be mediated by a physiological (resource allocation) trade-off between immune function and reproductive effort, and several recent studies have shown that an experimental increase in reproductive effort is associated with decreased immune function. Here we test the complementary prediction of this hypothesis: that increased immune function (specific antibody production) depresses reproductive output. Female European starlings (Sturnus vulgaris) were injected with a nonpathogenic antigen (sheep red blood cells) following completion of laying of their first clutch, to stimulate an in vivo humoral immune response (primary antibody production). We induced laying of a second clutch by removing the first clutch, and assessed changes in reproductive performance in individual females pre- and post-treatment. Injection of sheep red blood cells produced a significant antibody response in 96% (n=29) of treated females, with titres comparable to previous studies (range 1-7). However, increased antibody production did not decrease primary or secondary female reproductive effort (re-laying interval, egg size, clutch size, chick growth or fledging success), compared with control, saline-injected birds (n = 22). These data do not support a simple resource allocation model for the cost of reproduction, based on a reciprocal, negative relationship between resources allocated to immune function and reproduction.
10.Williams, TD; Guglielmo, CG; Egeler, O; Martyniuk, CJ. (1999) Plasma lipid metabolites provide information on mass change over several days in captive western sandpipers.Auk 116: 994-1000 Plasma lipid metabolites provide information on mass change over several days in captive western sandpipers
Individual quality is often assessed using a static measure of body condition, such as size-corrected body mass. Plasma metabolites have the potential to provide information on the dynamics of physiological state and thus may be better measures of individual performance capacity land fitness). We studied relationships between rate of mass change and circulating levels of triglycerides, glycerol, and beta-hydroxybutyrate in captive Western Sandpipers (Calidris mauri). The rate of mass change over one and two days prior to blood sampling was positively related to residual triglyceride (controlling for body mass at sampling) and negatively related to residual glycerol and residual beta-hydroxybutyrate. The relationship between metabolite level and mass change was still apparent over a seven-day interval for glycerol, but not for the other two metabolites. In a stepwise multiple regression of mass change over two days (controlling for body mass), only beta-hydroxybutyrate and glycerol were entered in the model at P < 0.15. Analysis of group means for seven sampling events showed that body-mass change in a group of individuals was related to mean circulating levels of each metabolite, i.e. to a characteristic metabolite profile. Thus, it may be feasible to employ these metabolites to assess habitat quality based on animal performance (e.g. at migratory stopover sites), or to understand the effects of climatic or anthropogenic factors on the health and survival of animals.
9.Williams, TD; Ternan, SP. (1999) Food intake, locomotor activity, and egg laying in zebra finches: Contributions to reproductive energy demand?Physiological and Biochemical Zoology 72: 19-27 Food intake, locomotor activity, and egg laying in zebra finches: Contributions to reproductive energy demand?
We tested two alternative hypotheses: (1) that energy costs of egg production in a small, short-lived passerine, the zebra finch (Taeniopygia guttata), are additive to the animal's total energy budget and are met by an increase in food intake or (2) that birds compensate for the energy costs of egg production by reducing energy expended on locomotor activity, thus, reallocating, but not increasing, their total energy budget. Breeding pairs of zebra finches had 8% lower daily food intake than nonbreeding pairs. Among breeding pairs, food intake varied with stage of egg formation but was lowest during egg laying, when egg formation costs were predicted to be highest. Female feeding behaviour (number of feeding bouts, peck rate) did not vary significantly during the laying cycle. Clutch size, but not egg size, was negatively correlated with food intake; that is, daily food intake was lowest for pairs in which females laid the largest clutches. Breeding pairs had much lower locomotor activity levels (114 hops h(-1)) than nonbreeding pairs (214 hops h(-1)), and activity declined sharply from 177 hops h(-1) during the prelaying period to 106 hops h(-1) at the start of the yolk-formation period. Clutch size was negatively correlated with locomotor activity on the day of peak energy demand for laying; that is, daily locomotor activity level was lowest for pairs in which females laid the largest clutches. Therefore, females reduced activity but did not increase food intake during the laying cycle, despite the additional energy requirements of egg production. These data suggest that the prevailing view of small passerines as "classic" income breeders needs to be reevaluated.
8. Balzer, AL; Williams, TD. (1998) Do female zebra finches vary primary reproductive effort in relation to mate attractiveness?Behaviour 135: 297-309 Do female zebra finches vary primary reproductive effort in relation to mate attractiveness?
Female choice and mate preference have been shown to affect female reproductive effort both prior to copulation (e.g. females seeking extra-pair copulation) and during parental care ('secondary' reproductive effort) in relation to mate quality. Here we show that female zebra finches, Taeniopygia guttata, vary their 'primary' reproductive effort in egg production in relation to the attractiveness of their male partner, for some components of reproduction but not others. Females were allowed to choose 'preferred' and 'non-preferred' males in standard mate choice trials, and were then paired sequentially with each male. Preferred males had significantly higher song duration and song frequency than non-preferred males confirming that females preferred attractive, higher quality males. Male attractiveness had a positive, but weak, effect on clutch size: in breeding experiments individual females laid on average 0.5 eggs more when paired with their preferred male compared to the non-preferred male. However, there was no significant difference in breeding propensity (whether females laid eggs or not), number of days between pairing and laying, mean egg size or egg quality (protein and lipid composition) in relation to male type. These results suggest that components of primary reproductive effort in individual female zebra finches are relatively non-plastic traits.
7. Guglielmo, CG; Haunerland, NH; Williams, TD. (1998) Fatty acid binding protein, a major protein in the flight muscle of migrating Western Sandpipers.Comparative Biochemistry and Physiology B-Biochemistry & Molecular Biology 119: 549-555 Fatty acid binding protein, a major protein in the flight muscle of migrating Western Sandpipers
bird; endurance exercise; FABP; flight; heart; lipid transport; migration; muscle
Migratory flight in birds is fueled primarily by fatty acid oxidation imposing a requirement for high rates of fatty acid: (a) transport; (b) uptake; and (c) delivery to intracellular sites of beta-oxidation. Muscle fatty acid binding protein (M-FABP) is a cytosolic protein involved in the intracellular transport of fatty acids. Its expression appears to be correlated with muscle fatty acid oxidation capacity. The M-FABP was isolated for the first time from a long distance migrant bird using: (i) size exclusion; (ii) anion exchange; and (iii) hydroxyapatite chromatography. M-FABP has a molecular weight of approximately 14000 Da and an isoelectric point of pH 4.8. A partial amino acid sequence of the protein demonstrated homology to M-FABPs from other species (80% identical to human heart FABP). It was estimated that M-FABP comprises approximately 14 and 21% of total cytosolic protein of the pectoralis and heart, respectively; the highest values yet reported from any vertebrate muscle. The abundance of M-FABP in these tissues suggests that the protein may play a key role in fatty acid supply during endurance flight. Thus, it is proposed that a seasonal increase in M-FABP expression could be a component of physiological preparation for migration. (C) 1998 Elsevier Science Inc. All rights reserved.
6. Butler, RW; Williams, TD; Warnock, N; Bishop, MA. (1997) Wind assistance: A requirement for migration of shorebirds?Auk 114: 456-466 Wind assistance: A requirement for migration of shorebirds?
We investigated the importance of wind-assisted night for northward (spring) migration by Western Sandpipers (Calidris mauri) along the Pacific Coast of North America. Using current models of energy costs of flight and recent data on the phenology of migration, we estimated the energy (fat) requirements for migration in calm winds and with wind-assisted flight for different rates of fat deposition: (1) a variable rate, assuming that birds deposit the minimum amount of fat required to reach the next stopover site; (2) a constant maximum rate of 1.0 g/day; and (3) a lower constant rate of 0.4 g/day. We tested these models by comparing conservative estimates of predicted body mass along the migration route with empirical data on body mass of Western Sandpipers at different stopover sites and upon arrival at the breeding grounds. In calm conditions, birds would have to deposit unrealistically high amounts of fat (up to 330% of observed values) to maintain body mass above absolute lean mass values. Fat-deposition rates of 1.0 g/day and 0.4 g/day, in calm conditions, resulted in a steady decline in body mass along the migration route with predicted body masses on arrival in Alaska of only 60% (13.6 g) and 26% (5.9 g) of average lean mass (22.7 g). Conversely, birds migrating with wind assistance would be able to complete migration with fat-deposition rates as low as 0.4 g/day, similar to values reported for this size bird from field studies. Our results extend the conclusion of the importance of winds for large, long-distance migrants to a small, short-distance migrant. We suggest that the migratory decisions of birds are more strongly influenced by the frequency and duration of winds aloft, i.e. by events during the flight phase, than by events during the stopover phase of migration, such as fat-deposition rate, that have been the focus of much recent migration theory. Received 3 September 1996, accepted 14 February 1997.
5.Williams, TD; Monaghan, P; Mitchell, PI; Scott, I; Houston, DG; Ramsey, S; Ensor, K. (1997) Evaluation of a non-destructive method for determining egg composition using total body electrical conductivity (TOBEC) measurements.Journal of Zoology 243: 611-622 Evaluation of a non-destructive method for determining egg composition using total body electrical conductivity (TOBEC) measurements
It is widely assumed that there is a positive relationship between egg quality (or egg size) and offspring fitness. However, obtaining unequivocal data in support of this hypothesis has been hampered by the lack of any method for non-destructive determination of egg composition, preventing a direct analysis of egg quality and subsequent chick growth and survival in the same egg(s). In this paper, we describe the application of a rapid, non-destructive technique using measurement of total body electrical conductivity (TOBEC) for determination of egg composition in intact eggs. The TOBEC index was positively and highly correlated with egg lean mass and with the mass of some egg components (albumen and water content). Values for predicted lean mass, based on the regression equation for lean mass against TOBEC index, were within +/-6% of actual lean mass. Egg lipid mass was most accurately predicted (+/-15%) using a multiple regression model, with fresh egg mass and TOBEC index included as independent variables. Egg temperature, and the position of the egg in the sampling chamber, markedly affected the TOBEC index obtained.
4.Williams, TD. (1996) Variation in reproductive effort in female zebra finches (Taeniopygia guttata) in relation to nutrient-specific dietary supplements during egg laying.Physiological Zoology 69: 1255-1275 Variation in reproductive effort in female zebra finches (Taeniopygia guttata) in relation to nutrient-specific dietary supplements during egg laying
Although dietary intake is thought to be more important than endogenous reserves for egg production in small, altricial birds (such as passerines), few experimental data are available to address this question. I investigated the reproductive responses of female zebra finches, Taeniopygia guttata, to enhanced dietary intake of macronutrients during the Period of egg formation. Lipid supplementation had no effect on egg or clutch size. In contrast, protein-supplemented females laid larger eggs (10%-12%) than controls, both immediately (i.e., first clutch) and in the longer term (second and third clutches up to 21 d after cessation of protein feeding). Interindividual egg size variation was maintained on the enhanced protein diet. The effect of protein on clutch size was equivocal with some evidence for a longer-term increase in size of second (replacement) clutches 10-14 d after protein feeding. Increased egg size involved an increase in both yolk protein and albumen content but not yolk lipid content These data suggest that zebra finches are protein limited during egg production. By mass decreased 2.4 g (15% of initial mass) during the laying cycle in control and lipid-fed females but did not change significantly in protein-fed birds. These mass changes are consistent with the idea that females use stored endogenous protein for egg production. However, mass loss was reduced or nonsignificant during laying of second (replacement) clutches with the same number and size of eggs. Mass loss during egg laying mag, thus have an alternate, more complex, and individually variable physiological basis rather than simply reflect a negative energy or nutrient balance.
3.Williams, TD. (1996) Intra- and inter-individual variation in reproductive effort in captive breeding zebra finches (Taeniopygia guttata).Canadian Journal of Zoology-Revue Canadienne de Zoologie 74: 85-91 Intra- and inter-individual variation in reproductive effort in captive breeding zebra finches (Taeniopygia guttata)
Intraspecific variation in egg size, clutch size, and timing of laying was studied in captive-breeding zebra finches (Taeniopygia guttata) maintained under conditions of constant temperature, humidity, photoperiod (14 h light : 10 h dark), and ad libitum food supply. Individual variation was marked in the experimental population: egg size 0.915-1.342 g, clutch size 2-7 eggs, and laying interval 4-13 days; however, within individual females egg size (r = 0.742) and clutch size (r = 0.588) were highly repeatable between first and second clutches. Body condition explained only 8% of egg size variation, and clutch size and laying interval were independent of body condition. Clutch size was negatively related to laying interval: females laying later relative to pairing laid smaller clutches (b = -0.175 eggs/day). Body mass of breeding females decreased by 1.57 g (9% of initial mass) during laying of first clutches; mass loss was positively related to initial body condition (R(2) = 27.8%) and total clutch mass (R(2) = 7.6%). Mass loss was lower (0.47 g) during laying of second or replacement clutches than during laying of first clutches. Individual variation in reproductive effort in captive-breeding zebra finches is very similar to that in free-living avian populations. Laboratory studies on captive-breeding species can provide a valuable approach for the study of proximate physiological mechanisms underlying intraspecific variation in reproduction.
2.Williams, TD; Cooch, EG. (1996) Egg size, temperature and laying sequence: Why do Snow Geese lay big eggs when it's cold?Functional Ecology 10: 112-118 Egg size, temperature and laying sequence: Why do Snow Geese lay big eggs when it's cold?
physiological trade-offs; rapid yolk development; reproduction; thermoregulation
1. Several studies of altricial passerines ('income breeders') have shown that females lay smaller eggs when they experience low temperatures during egg formation, This is usually explained in terms of a 'physiological trade-off': birds having to divert more of their finite resources to maintenance and away from reproduction in cold weather, although little is known about the proximate mechanism(s) underlying this phenomenon. 2. We investigated the relationship between egg size and ambient temperature during egg formation period in the Lesser Snow Goose (Anser caerulescens caerulescens), a precocial, 'capital-breeding' species, using 10 years of data derived from a long-term. population study of this species at La Perouse Bay, Man., Canada. 3. Egg size was negatively correlated with ambient temperature in the Snow Goose, i.e. females laid larger eggs when temperatures were lower during egg formation, contrasting markedly with the positive correlation reported in altricial, income-breeders. 4. The effect of temperature on egg size was most marked for last-laid eggs within a clutch (b = 0.675 g degrees C-1), and for temperatures during the last half of the rapid yolk development (RYD) period (rather than for the whole or the middle of the RYD period), as predicted by an exponential growth curve for yolk development. 5. The relationship between egg mass and temperature was time- and laying-sequence specific: for first and middle eggs the correlation was positive early in the period of RYD and negative closer to ovulation. For last-laid eggs the correlation between egg mass and temperature was negative throughout the 10 day RYD period. 6. We suggest that the different relationship between egg size and temperature in the Snow Goose, compared to passerine species, may reflect different contributions of exogenous vs endogenous reserves, and different opportunities to increase energy availability through dietary intake. 7. Although statistically significant, temperature has only a small effect on egg size in the Lesser Snow Goose: the average range of temperatures encountered would only lead to a 3-5% difference in mean egg mass, This is consistent with high heritability of egg size.
1.Williams, TD; Jeffs, C; Murray, KA; Choudhury, S. (1996) Intraclutch egg-size variation in the barnacle goose Branta leucopsis: An egg-removal experiment.Ibis 138: 499-505 Intraclutch egg-size variation in the barnacle goose Branta leucopsis: An egg-removal experiment
We carried out an egg-removal experiment on Barnacle Geese Branta leucopsis to test the hypothesis that tactile contact between the brood patch and eggs accumulating in the nest during laying was causally related to intraclutch egg-size variation, acting through the development of incubation behaviour. Egg removal had no effect on mean egg mass, relaying interval or clutch size: mean (+/- s.e.) clutch sizes for first clutches were 4.9 +/- 0.9 and 4.7 +/- 0.9 eggs for control and experimental females, respectively, We therefore conclude that Barnacle Geese have a determinate pattern of egg laying, Daily removal of all eggs from the first-laid egg did not affect the within-clutch pattern of egg-size variation: in both control and experimental clutches the first egg was relatively small, the second or third egg was largest and there was a linear decline in egg size to the smallest, last-laid egg, There was no significant difference in either the absolute or relative size of the last-laid eggs in control and experimental clutches, Tactile contact with eggs in the nest, therefore, is not required for the expression of intraclutch egg-size variation in Barnacle Geese, In this respect, determinate-laying Barnacle Geese differ from species with indeterminate laying patterns (e.g. gulls) where egg removal does affect the normal pattern of within-clutch egg-size variation. If hormonal changes (e.g. prolactin) associated with onset of incubation are causally related to the intraclutch decrease in egg size, then the stimuli involved appear to differ between determinate and indeterminate layers.
