34. 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
33. 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
32. 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
31. 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
30. 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
29. 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
28. 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
27. 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
26. 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
25. 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
24. 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
23. 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
22. 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
21. 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
20. 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
19. 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
18. 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
17. 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
16. 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
15. 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
14. 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
13. 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
12. 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
11. 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
10. 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
9.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
8. 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
7. 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
6. 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
5. 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
4. 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
3.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
2. 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
