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Publications of Tony Williams
218 Publications
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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
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