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1.  Rich Pickings Near Large Communal Roosts Favor ‘Gang’ Foraging by Juvenile Common Ravens, Corvus corax 
PLoS ONE  2009;4(2):e4530.
Ravens (Corvus corax) feed primarily on rich but ephemeral carcasses of large animals, which are usually defended by territorial pairs of adults. Non-breeding juveniles forage socially and aggregate in communal winter roosts, and these appear to function as ‘information centers’ regarding the location of the rare food bonanzas: individuals search independently of one another and pool their effort by recruiting each other at roosts. However, at a large raven roost in Newborough on Anglesey, North Wales, some juveniles have been observed recently to forage in ‘gangs’ and to roost separately from other birds. Here we adapt a general model of juvenile common raven foraging behavior where, in addition to the typical co-operative foraging strategy, such gang foraging behavior could be evolutionarily stable near winter raven roosts. We refocus the model on the conditions under which this newly documented, yet theoretically anticipated, gang-based foraging has been observed. In the process, we show formally how the trade off between search efficiency and social opportunity can account for the existence of the alternative social foraging tactics that have been observed in this species. This work serves to highlight a number of fruitful avenues for future research, both from a theoretical and empirical perspective.
PMCID: PMC2646834  PMID: 19240813
2.  Social bonds and rank acquisition in raven nonbreeder aggregations 
Animal Behaviour  2012;84(6):1507-1515.
Complex social life has been characterized as cognitively challenging and recently, social relationships such as long-term social bonds and alliances have been identified as key elements for brain evolution. Whereas good evidence is available to support the link between social relations and cognition in mammals, it remains unsatisfying for birds. Here we investigated the role of avian social bonds in a nonbreeder aggregation of ravens, Corvus corax, in the Austrian Alps. We individually marked 138 wild ravens, representing approximately half of a population that uses the area of a local zoo for foraging. For 2 years, we observed the dynamics of group composition and the birds' agonistic and affiliative interactions. We identified two levels of organization: the formation of an unrelated local group and the individuals' engagement in social bonds of different length and reciprocity pattern. Whereas belonging to the local group had no significant effect on conflicts won during foraging, the individual bonding type did. Birds that engaged in affiliative relationships were more successful when competing for food than those without such bonds. Bonded birds did suffer from aggression by other bonded birds and, probably as a consequence, most of the ravens' social relations were not stable over time. These results support the idea that social bonding and selective cooperation and competition are prominent features in nonbreeding ravens. Proximately, bonding may qualify as a social manoeuvre that facilitates access to resources; ultimately it might function to assess the quality of a partner in these long-term monogamous birds.
► Big brains correlate with the formation of strong nonsexual bonds in mammals. ► We examine formation and use of bonds in birds, namely wild nonbreeder ravens. ► Individuals engage in different social bonds and benefit from them in conflicts. ► Active investment in nonsexual strong bonds for rank acquisition in a big-brained bird.
PMCID: PMC3518779  PMID: 23264693
Corvus corax; dominance; nonbreeder aggregation; raven; social bond; social structure
3.  Haemosporidian infection in captive masked bobwhite quail (Colinus virginianus ridgwayi), an endangered subspecies of the northern bobwhite quail 
Veterinary parasitology  2011;182(0):113-120.
The avian haemosporidian parasites (phylum Apicomplexa) are taxonomically diverse and cosmopolitan in distribution; infecting most bird families. Sources of concern are reports of clinical haemosporidian infections in birds kept as part of zoo and aviary collections. Recently, severe and acute mortality episodes have been reported in masked bobwhite quail (Colinus virginianus ridgwayi), an endangered subspecies from the American Southwest. Two hundred and five eggs of the captive flock held in Arivaca, Arizona, were hatched at a zoo in the American Southwest. Thirty four sub-adult or adult animals had lesions associated with tissue phases of hemoparasites, especially vasculitis, ventricular leiomyositis and ulcerative pododermatitis. Molecular techniques applied to blood collected from the zoo’s last twelve remaining animals resulted in the detection of a Plasmodium juxtanucleare-like and Haemoproteus sp. parasites. A Raven (Corvus corax), in a contiguous exhibit, was positive for the same Plasmodium juxtanucleare-like parasite, but remained asymptomatic for three years following detection. These findings indicate that other birds in the exhibit within the zoo premises could act as reservoirs. We conclude that haemosporidian infections could be a factor in the demise of the captive masked bobwhite quails housed at the zoo. We suggest that active surveillance for haemoporidian parasites should be incorporated as a precaution to ex-situ conservation efforts of susceptible endangered species.
PMCID: PMC3742108  PMID: 21726940
Masked Bobwhite Quail; Haemosporidia; Plasmodium; Haemoproteus; Cytochrome b gene; vasculitis; ventricular leiomyositis; ulcerative pododermatitis
4.  Corticosterone, testosterone and life-history strategies of birds 
Steroid hormones have similar functions across vertebrates, but circulating concentrations can vary dramatically among species. We examined the hypothesis that variation in titres of corticosterone (Cort) and testosterone (T) is related to life-history traits of avian species. We predicted that Cort would reach higher levels under stress in species with higher annual adult survival rates since Cort is thought to promote physiological and behavioural responses that reduce risk to the individual. Conversely, we predicted that peak T during the breeding season would be higher in short-lived species with high mating effort as this hormone is known to promote male fecundity traits. We quantified circulating hormone concentrations and key life-history traits (annual adult survival rate, breeding season length, body mass) in males of free-living bird species during the breeding season at a temperate site (northern USA) and a tropical site (central Panama). We analysed our original data by themselves, and also combined with published data on passerine birds to enhance sample size. In both approaches, variation in baseline Cort (Cort0) among species was inversely related to breeding season length and body mass. Stress-induced corticosterone (MaxCort) also varied inversely with body mass and, as predicted, also varied positively with annual adult survival rates. Furthermore, species from drier and colder environments exhibited lower MaxCort than mesic and tropical species; T was lowest in species from tropical environments. These findings suggest that Cort0, MaxCort and T modulate key vertebrate life-history responses to the environment, with Cort0 supporting energetically demanding processes, MaxCort promoting survival and T being related to mating success.
PMCID: PMC2982062  PMID: 20554550
life-history trade-offs; steroid hormone; latitude; bird; reproduction; survival
5.  Reciprocity of agonistic support in ravens 
Animal Behaviour  2012;83(1):171-177.
Cooperative behaviour through reciprocation or interchange of valuable services in primates has received considerable attention, especially regarding the timeframe of reciprocation and its ensuing cognitive implications. Much less, however, is known about reciprocity in other animals, particularly birds. We investigated patterns of agonistic support (defined as a third party intervening in an ongoing conflict to attack one of the conflict participants, thus supporting the other) in a group of 13 captive ravens, Corvus corax. We found support for long-term, but not short-term, reciprocation of agonistic support. Ravens were more likely to support individuals who preened them, kin and dominant group members. These results suggest that ravens do not reciprocate on a calculated tit-for-tat basis, but aid individuals from whom reciprocated support would be most useful and those with whom they share a good relationship. Additionally, dyadic levels of agonistic support and consolation (postconflict affiliation from a bystander to the victim) correlated strongly with each other, but we found no evidence to suggest that receiving agonistic support influences the victim’s likelihood of receiving support (consolation) after the conflict ends. Our findings are consistent with an emotionally mediated form of reciprocity in ravens and provide additional support for convergent cognitive evolution in birds and mammals.
► We examine patterns of agonistic support in captive ravens. ► We find support for long-term but not short-term reciprocation of support. ► Ravens supported individuals who preened them, kin and dominant individuals. ► Strong correlation between dyadic levels of agonistic support and consolation. ► Ravens may use emotions to mediate reciprocation of support.
PMCID: PMC3255075  PMID: 22298910
agonistic support; coalition; corvid; Corvus corax; interchange; raven; reciprocity
6.  Non-breeding feather concentrations of testosterone, corticosterone and cortisol are associated with subsequent survival in wild house sparrows 
Potential mechanistic mediators of Darwinian fitness, such as stress hormones or sex hormones, have been the focus of many studies. An inverse relationship between fitness and stress or sex hormone concentrations has been widely assumed, although empirical evidence is scarce. Feathers gradually accumulate hormones during their growth and provide a novel way to measure hormone concentrations integrated over time. Using liquid chromatography–tandem mass spectrometry, we measured testosterone, corticosterone and cortisol in the feathers of house sparrows (Passer domesticus) in a wild population which is the subject of a long-term study. Although corticosterone is considered the dominant avian glucocorticoid, we unambiguously identified cortisol in feathers. In addition, we found that feathers grown during the post-nuptial moult in autumn contained testosterone, corticosterone and cortisol levels that were significantly higher in birds that subsequently died over the following winter than in birds that survived. Thus, feather steroids are candidate prospective biomarkers to predict the future survival of individuals in the wild.
PMCID: PMC3282351  PMID: 22090380
corticosteroid; glucocorticoid; mass spectrometry; mortality; Passer domesticus; LC–MS/MS; stress
7.  Cryptic genetic variation and paraphyly in ravens. 
Widespread species that are morphologically uniform may be likely to harbour cryptic genetic variation. Common ravens (Corvus corax) have an extensive range covering nearly the entire Northern Hemisphere, but show little discrete phenotypic variation. We obtained tissue samples from throughout much of this range and collected mitochondrial sequence and nuclear microsatellite data. Our study revealed a deep genetic break between ravens from the western United States and ravens from throughout the rest of the world. These two groups, the 'California clade' and the 'Holarctic clade' are well supported and over 4% divergent in mitochondrial coding sequence. Microsatellites also reveal significant differentiation between these two groups. Ravens from Minnesota, Maine and Alaska are more similar to ravens from Asia and Europe than they are to ravens from California. The two clades come in contact over a huge area of the western United States, with mixtures of the two mitochondrial groups present in Washington, Idaho and California. In addition, the restricted range Chihuahuan raven (Corvus cryptoleucus) of the south-west United States and Mexico is genetically nested within the paraphyletic common raven. Our findings suggest that the common raven may have formerly consisted of two allopatric groups that may be in the process of remerging.
PMCID: PMC1690844  PMID: 11197122
8.  Ravens Reconcile after Aggressive Conflicts with Valuable Partners 
PLoS ONE  2011;6(3):e18118.
Reconciliation, a post-conflict affiliative interaction between former opponents, is an important mechanism for reducing the costs of aggressive conflict in primates and some other mammals as it may repair the opponents' relationship and reduce post-conflict distress. Opponents who share a valuable relationship are expected to be more likely to reconcile as for such partners the benefits of relationship repair should outweigh the risk of renewed aggression. In birds, however, post-conflict behavior has thus far been marked by an apparent absence of reconciliation, suggested to result either from differing avian and mammalian strategies or because birds may not share valuable relationships with partners with whom they engage in aggressive conflict. Here, we demonstrate the occurrence of reconciliation in a group of captive subadult ravens (Corvus corax) and show that it is more likely to occur after conflicts between partners who share a valuable relationship. Furthermore, former opponents were less likely to engage in renewed aggression following reconciliation, suggesting that reconciliation repairs damage caused to their relationship by the preceding conflict. Our findings suggest not only that primate-like valuable relationships exist outside the pair bond in birds, but that such partners may employ the same mechanisms in birds as in primates to ensure that the benefits afforded by their relationships are maintained even when conflicts of interest escalate into aggression. These results provide further support for a convergent evolution of social strategies in avian and mammalian species.
PMCID: PMC3064662  PMID: 21464962
9.  Comparison of Stress-Induced Changes in Adults and Pups: Is Aldosterone the Main Adrenocortical Stress Hormone during the Perinatal Period in Rats? 
PLoS ONE  2013;8(9):e72313.
Positive developmental impact of low stress-induced glucocorticoid levels in early development has been recognized for a long time, while possible involvement of mineralocorticoids in the stress response during the perinatal period has been neglected. The present study aimed at verifying the hypothesis that balance between stress-induced glucocorticoid and mineralocorticoid levels is changing during postnatal development. Hormone responses to two different stressors (insulin-induced hypoglycaemia and immune challenge induced by bacterial lipopolysaccharid) measured in 10-day-old rats were compared to those in adults. In pups corticosterone responses to both stressors were significantly lower than in adults, which corresponded well with the stress hyporesponsive period. Importantly, stress-induced elevations in aldosterone concentration were significantly higher in pups compared both to corticosterone elevations and to those in adulthood with comparable adrenocorticotropin concentrations in the two age groups. Greater importance of mineralocorticoids compared to glucocorticoids in postnatal period is further supported by changes in gene expression and protein levels of gluco- (GR) and mineralocorticoid receptors (MR) and selected enzymes measured by quantitative PCR and immunohystochemistry in the hypothalamus, hippocampus, prefrontal cortex, liver and kidney. Gene expression of 11beta-hydroxysteroid dehydrogenase 2 (11β-HSD2), an enzyme enabling preferential effects of aldosterone on mineralocorticoid receptors, was higher in 10-day-old pups compared to adult animals. On the contrary, the expression and protein levels of GR, MR and 11β-HSD1 were decreased. Presented results clearly show higher stress-induced release of aldosterone in pups compared to adults and strongly suggest greater importance of mineralocorticoids compared to glucocorticoids in stress during the postnatal period.
PMCID: PMC3763995  PMID: 24039750
10.  Social, state-dependent and environmental modulation of faecal corticosteroid levels in free-ranging female spotted hyenas. 
Little is known about to what extent the sensitivity of the hypothalamic-pituitary-adrenal (HPA) axis may be state dependent and vary in the same species between environments. Here we tested whether the faecal corticosteroid concentrations of matrilineal adult female spotted hyenas are influenced by social and reproductive status in adjacent ecosystems and whether they vary between periods with and without social stress. Females in the Serengeti National Park frequently become socially subordinate intruders in other hyena territories by undertaking long-distance foraging trips to migratory herds, whereas in the Ngorongoro Crater they usually forage inside their own small territories on resident prey. The faecal corticosteroid concentrations in Serengeti females were significantly higher than in Ngorongoro females. Energy expenditure by lactation is exceptionally high in spotted hyenas and this may be reflected in their corticosteroid levels. The faecal corticosteroid levels in both populations were higher in lactating than in non-lactating females. During periods of social stability, faecal corticosteroid concentrations increased in non-lactating females but not in lactating females as social status declined. Lactating Serengeti females had significantly higher faecal corticosteroid concentrations during periods with acute severe social stress than during periods without, indicating that the HPA axis is sensitive to social stimuli even in lactating females. So far few studies have used non-invasive monitoring methods for assessing social stress in freeranging animals. This study demonstrates for the first time, to the authors' knowledge, that corticosteroid concentrations may differ between periods with and without social stress for a free-ranging female mammal and that the modulating effect of social status may depend on reproductive status.
PMCID: PMC1088899  PMID: 11747563
11.  Modulation of the hypothalamic-pituitary-adrenal axis of an Arctic-breeding polygynandrous songbird, the Smith's longspur, Calcarius pictus. 
To successfully reproduce in the Arctic, birds must modulate their neuroendocrine and behavioural systems. These adjustments include an attenuation of the stress responsiveness of the hypothalamic-pituitary-adrenal (HPA) axis to external stimuli and a behavioural insensitivity to high corticosterone (B) levels. The HPA axis was examined in free-living territorial polygynandrous Smith's longspurs (Calcarius pictus) that migrate to breed on the Arctic tundra. Basal and stress-induced B levels were measured through the breeding season and were found to be significantly lower in females compared with males. This was not a consequence of adrenal insensitivity, because intrajugular injections of adrenocorticotrophin hormone (ACTH) enhanced B release in incubating females. In males the adrenocortical response to stress was significantly attenuated during the parental phase compared with arrival at the breeding ground. In contrast to temperate passerines, there was no significant decrease in male territorial aggressive behaviour when B was experimentally elevated, suggesting a behavioural insensitivity to glucocorticoids. This mechanism is hypothesized to increase reproductive success by preventing interruptions to parental care during transient deleterious environmental perturbations, which are often experienced in the short Arctic breeding season. Modulation of the HPA axis in this species in relation to life-history stage, lifetime reproductive success and the polygynandrous mating system is discussed.
PMCID: PMC1691444  PMID: 12964988
12.  Deprivation of maternal care has long-lasting consequences for the hypothalamic–pituitary–adrenal axis of zebra finches 
Early-life stress caused by the deprivation of maternal care has been shown to have long-lasting effects on the hypothalamic–pituitary–adrenal (HPA) axis in offspring of uniparental mammalian species. We asked if deprivation of maternal care in biparental species alters stress responsiveness of offspring, using a biparental avian species—the zebra finch, Taeniopygia guttata. In our experiment, one group of birds was raised by both male and female parents (control), and another was raised by males alone (maternally deprived). During adulthood, offspring of both groups were subjected to two stressors (restraint and isolation), and corticosterone concentrations were measured. Additionally, we measured baseline levels of the two corticosteroid receptors—glucocorticoid receptor (GR) and mineralocorticoid receptor (MR)—in the hippocampus, hypothalamus and cerebellum. Our results suggest that maternally deprived offspring are hyper-responsive to isolation in comparison with controls. Furthermore, mRNA levels of both GR and MR receptors are altered in maternally deprived offspring in comparison with controls. Thus, absence of maternal care has lasting consequences for HPA function in a biparental species where paternal care is available.
PMCID: PMC3248735  PMID: 21775332
zebra finch; stress; corticosterone; mineralocorticoid receptor; glucocorticoid receptor; maternal deprivation
13.  Experimentally increased food resources in the natal territory promote offspring philopatry and helping in cooperatively breeding carrion crows 
Kin-based societies, where families represent the basic social unit, occur in a relatively small number of vertebrate species. In the majority of avian kin societies, families form when offspring prolong their association with the parents on the natal territory. Therefore, the key to understanding the evolution of families in birds is to understand natal philopatry (i.e. the tendency to remain on the natal territory). It has been shown that, within populations, the strength of the association between parents and offspring (i.e. family stability) increases when offspring dispersal is constrained by external environmental factors, but it is unclear whether and how family wealth influences juvenile dispersal decisions. Here, we show that young carrion crows (Corvus corone corone) from territories that were food-supplemented year-round were more philopatric and more likely to help at their family's nest than the unfed ones. The results suggest that offspring philopatry and helping behaviour are influenced by the quality of ‘home’ and that the availability of food resources positively affects the cohesion of the family.
PMCID: PMC1560324  PMID: 16777748
philopatry; wealth; cooperative breeding; territory quality; carrion crow
14.  Long-Term Memory for Affiliates in Ravens 
Current Biology  2012;22(9):801-806.
Complex social life requires individuals to recognize and remember group members [1] and, within those, to distinguish affiliates from nonaffiliates. Whereas long-term individual recognition has been demonstrated in some nonhuman animals [2–5], memory for the relationship valence to former group members has received little attention. Here we show that adult, pair-housed ravens not only respond differently to the playback of calls from previous group members and unfamiliar conspecifics but also discriminate between familiar birds according to the relationship valence they had to those subjects up to three years ago as subadult nonbreeders. The birds' distinction between familiar and unfamiliar individuals is reflected mainly in the number of calls, whereas their differentiation according to relationship valence is reflected in call modulation only. As compared to their response to affiliates, ravens responded to nonaffiliates by increasing chaotic parts of the vocalization and lowering formant spacing, potentially exaggerating the perceived impression of body size. Our findings indicate that ravens remember relationship qualities to former group members even after long periods of separation, confirming that their sophisticated social knowledge as nonbreeders is maintained into the territorial breeding stage.
► Ravens remember former group members for extended time periods ► Ravens memorize relationship valence (affiliation) in addition to group membership ► Familiarity is coded in the number of calls given in response to playback ► Relationship valence is coded in the modulation of response calls
PMCID: PMC3348500  PMID: 22521788
15.  Stress hormone dynamics: an adaptation to migration? 
Biology Letters  2009;5(4):480-483.
The hormone corticosterone (CORT) is an important component of a bird’s response to environmental stress, but it can also have negative effects. Therefore, birds on migration are hypothesized to have repressed stress responses (migration-modulation hypothesis). In contrast to earlier studies on long-distance migrants, we evaluate this hypothesis in a population containing both migratory and resident individuals. We use a population of partially migratory blue tits (Cyanistes caeruleus) in southern Sweden as a model species. Migrants had higher CORT levels at the time of capture than residents, indicating migratory preparations, adaptation to stressors, higher allostatic load or possibly low social status. Migrants and residents had the same stress response, thus contradicting the migration-modulation hypothesis. We suggest that migrants travelling short distances are more benefited than harmed by retaining the ability to respond to stress.
PMCID: PMC2781924  PMID: 19429650
stress; corticosterone; partial migration
16.  Physiological Stress Mediates the Honesty of Social Signals 
PLoS ONE  2009;4(3):e4983.
Extravagant ornaments used as social signals evolved to advertise their bearers' quality. The Immunocompetence Handicap Hypothesis proposes that testosterone-dependent ornaments reliably signal health and parasite resistance; however, empirical studies have shown mixed support. Alternatively, immune function and parasite resistance may be indirectly or directly related to glucocorticoid stress hormones. We propose that an understanding of the interplay between the individual and its environment, particularly how they cope with stressors, is crucial for understanding the honesty of social signals.
Methodology/Principal Findings
We analyzed corticosterone deposited in growing feathers as an integrated measure of hypothalamic-pituitary-adrenal activity in a wild territorial bird, the red grouse Lagopus lagopus scoticus. We manipulated two key, interrelated components, parasites and testosterone, which influence both ornamentation and fitness. Birds were initially purged of parasites, and later challenged with parasites or not, while at the same time being given testosterone or control implants, using a factorial experimental design. At the treatment level, testosterone enhanced ornamentation, while parasites reduced it, but only in males not implanted with testosterone. Among individuals, the degree to which both parasites and testosterone had an effect was strongly dependent on the amount of corticosterone in the feather grown during the experiment. The more stressors birds had experienced (i.e., higher corticosterone), the more parasites developed, and the less testosterone enhanced ornamentation.
With this unique focus on the individual, and a novel, integrative, measure of response to stressors, we show that ornamentation is ultimately a product of the cumulative physiological response to environmental challenges. These findings lead toward a more realistic concept of honesty in signaling as well as a broader discussion of the concept of stress.
PMCID: PMC2656621  PMID: 19319197
17.  Carrion Crows Cannot Overcome Impulsive Choice in a Quantitative Exchange Task 
The ability to control an immediate impulse in return for a more desirable – though delayed – outcome has long been thought to be a uniquely human feature. However, studies on non-human primates revealed that some species are capable of enduring delays in order to get food of higher quality or quantity. Recently two corvid species, common raven (Corvus corax) and carrion crow (Corvus corone corone), exchanged food for a higher quality reward though seemed less capable of enduring delays when exchanging for the same food type in a higher quantity. In the present study, we specifically investigated the ability of carrion crows to overcome an impulsive choice in a quantitative exchange task. After a short delay, individuals were asked to give back an initial reward (cheese) to the human experimenter in order to receive a higher amount of the same reward (two, four, or eight pieces). We tested six captive crows – three individuals never exchanged the initial reward for a higher quantity; the other three birds did exchange though at very low rates. We performed a preference test between one or more pieces of cheese in order to address whether crow poor performance could be due to an inability to discriminate between different quantities or not attributing a higher value to the higher quantities. All birds chose the higher quantities significantly more often, indicating that they can discriminate between quantities and that higher quantities are more desirable. Taken together, these results suggest that, although crows may possess the cognitive abilities to judge quantities and to overcome an impulsive choice, they do so only in order to optimize the qualitative but not quantitative output in the exchange paradigm.
PMCID: PMC3328082  PMID: 22529833
impulse control; quantity; exchange task; carrion crows; Corvus corone corone
18.  The Behavioral Implications of a Multi-Individual Bonebed of a Small Theropod Dinosaur 
PLoS ONE  2013;8(5):e64253.
Central Patagonia, Argentina, preserves an abundant and rich fossil record. Among vertebrate fossils from the Upper Cretaceous Bajo Barreal Formation of Patagonia, five individuals of the small, non-avian theropod dinosaur Aniksosaurus darwini were recovered. Group behavior is an important aspect of dinosaur paleoecology, but it is not well-documented and is poorly understood among non-avian Theropoda.
Methods/Principal Findings
The taphonomic association of individuals from the Bajo Barreal Formation and aspects of their bone histology suggest gregarious behavior for Aniksosaurus, during at least a portion of the life history of this species. Histology indicates that the specimens were juvenile to sub-adult individuals. In addition, morphological differences between individuals, particularly proportions of the appendicular bones, are probably related to body-size dimorphism rather than ontogenetic stage.
Gregarious behaviour may have conferred a selective advantage on Aniksosaurus individuals, contributing to their successful exploitation of the Cretaceous paleoenvironment preserved in the Bajo Barreal Formation. The monospecific assemblage of Aniksosaurus specimens constitutes only the second body fossil association of small, coelurosaurian theropods in South America and adds valuable information about the paleoecologies of non-avian theropod dinosaurs, particularly in the early Late Cretaceous of Patagonia.
PMCID: PMC3655058  PMID: 23691183
19.  Experimental evidence that corticosterone affects offspring sex ratios in quail 
Recent studies have shown that some species of birds have a remarkable degree of control over the sex ratio of offspring they produce. However, the mechanism by which they achieve this feat is unknown. Hormones circulating in the breeding female are particularly sensitive to environmental perturbations, and so could provide a mechanism for her to bias the sex ratio of her offspring in favour of the sex that would derive greatest benefit from the prevailing environmental conditions. Here, we present details of an experiment in which we manipulated levels of testosterone, 17β-oestradiol and corticosterone in breeding female Japanese quail (Coturnix coturnix japonica) using Silastic implants and looked for effects on the sex ratio of offspring produced. Offspring sex ratio in this species was significantly correlated with faecal concentrations of the principal avian stress hormone, corticosterone, and artificially elevated levels of corticosterone resulted in significantly female-biased sex ratios at laying. Varying testosterone and 17β-oestradiol had no effect on sex ratio alone, and faecal levels of these hormones did not vary in response to corticosterone. Our results suggest that corticosterone may be part of the sex-biasing process in birds.
PMCID: PMC1560264  PMID: 16600886
maternal effects; hormones; primary sex ratio manipulation; mechanism; Coturnix coturnix japonica
20.  Predators as stressors? Physiological and reproductive consequences of predation risk in tropical stonechats (Saxicola torquata axillaris). 
Tropical birds usually lay smaller clutches and are less likely to initiate a second brood than their temperate-zone relatives. This reduction in annual fecundity is generally explained as an adaptation either to higher rates of nest predation or to a more limited food supply concurrent with higher adult survival in the tropics. However, the physiological parameters associated with lower annual fecundity in tropical birds have not been well investigated. We compared the annual fecundity, behaviour and a number of physiological parameters of stonechat parents feeding fledged juveniles in territories with and without fiscal shrikes, a predator on adult and fledged birds. Stonechat pairs in territories with shrikes were less likely to initiate a second brood and delayed successive broods compared to pairs in territories without shrikes. After fledging of their young, males showed a greater propensity than females to initiate distraction calls after a human intrusion into their territory and, therefore, invested more in the defence of their young. In territories with shrikes stonechat males had higher initial plasma corticosterone levels and lower body conditions than males in territories without shrikes, suggesting that they were chronically stressed. In contrast, the females from both types of territory had low initial plasma corticosterone levels. We conclude that shrike presence might account for the delay in initiation of a second brood and the reduction in the tendency to initiate a second brood. Whether these effects are mediated by the elevated levels of corticosterone remains to be demonstrated.
PMCID: PMC1088780  PMID: 11487404
21.  A Non-Invasive Stress Assay Shows That Tadpole Populations Infected with Batrachochytrium dendrobatidis Have Elevated Corticosterone Levels 
PLoS ONE  2013;8(2):e56054.
Batrachochytrium dendrobatidis (Bd) is a fungus that causes the disease chytridiomycosis and is associated with widespread amphibian declines. Populations vary in their susceptibility to Bd infections, and the virulence of the infecting lineage can also vary. Both of these factors may manifest as a differential physiological stress response. In addition, variation in disease susceptibility across amphibian populations may be influenced by immunosuppression caused by chronic stress imposed by environmental factors. Here, we use a non-invasive water-borne hormone technique to assess stress levels (corticosterone) of free-living tadpole populations that are infected by Bd. We found that corticosterone release rates were higher in infected populations of two species of tadpoles (Alytes obstetricans and A. muletensis) than in an uninfected population for both species. The relationship between corticosterone and the intensity of infection differed between species, with only the infected A. obstetricans population showing a significant positive correlation. The higher corticosterone release rates found in A. obstetricans may be an outcome of infection by a highly virulent lineage of Bd (BdGPL), whereas A. muletensis is infected with a less virulent lineage (BdCAPE). These results suggest that different lineages of Bd impose different levels of stress on the infected animals, and that this may influence survival. The next step is to determine whether higher corticosterone levels make individuals more susceptible to Bd or if Bd infections drive the higher corticosterone levels.
PMCID: PMC3572145  PMID: 23418508
22.  Robust behavioral effects of song playback in the absence of testosterone or corticosterone release 
Hormones and behavior  2012;62(4):418-425.
Some species of songbirds elevate testosterone in response to territorial intrusions while others do not. The search for a general explanation for this interspecific variation in hormonal response to social challenges has been impeded by methodological differences among studies. We asked whether song playback alone is sufficient to bring about elevation in testosterone or corticosterone in the dark-eyed junco (Junco hyemalis), a species that has previously demonstrated significant testosterone elevation in response to a simulated territorial intrusion when song was accompanied by a live decoy. We studied two populations of juncos that differ in length of breeding season (6–8 v. 14–16 weeks), and conducted playbacks of high amplitude, long-range song. In one population, we also played low amplitude, short-range song, a highly potent elicitor of aggression in juncos and many songbirds. We observed strong aggressive responses to both types of song, but no detectable elevation of plasma testosterone or corticosterone in either population. We also measured rise in corticosterone in response to handling post-playback, and found full capacity to elevate corticosterone but no effect of song class (long-range or short-range) on elevation. Collectively, our data suggest that males can mount an aggressive response to playback without a change in testosterone or corticosterone, despite the ability to alter these hormones during other types of social interactions. We discuss the observed decoupling of circulating hormones and aggression in relation to mechanisms of behavior and the cues that may activate the HPA and HPG axes.
PMCID: PMC3477244  PMID: 22850247
23.  Feather corticosterone of a nestling seabird reveals consequences of sex-specific parental investment 
Offspring of long-lived species should face costs of parental trade-offs that vary with overall energetic demands encountered by parents during breeding. If sex differences exist in how parents make the trade-off, sex-specific differences may exist in the contribution of each parent to those costs. Adaptations of offspring facing such costs are not well understood, but the hormone corticosterone probably plays a role. We manipulated breeding effort in Cory's shearwaters (Calonectris diomedea) to increase costs to offspring and used an integrated measure of corticosterone from chick feathers to investigate how experimental variation in parental investment influences offspring physiology. Average foraging trip duration and foraging efficiency (FE) of breeding pairs were not related to chick corticosterone, but sex biases in FE were. Adult male investment was more strongly related to chick corticosterone than was female investment. Importantly, we show for the first time suppression of adrenocortical activity in nestling Procellariiform seabirds, and explain how our results indicate an adaptive mechanism invoked by chicks facing increased costs of parental trade-offs.
PMCID: PMC3223659  PMID: 21632628
Cory's shearwater; feather corticosterone; life history; parental investment; stress physiology; trade-offs
24.  Progesterone modulates aggression in sex-role reversed female African black coucals 
Testosterone is assumed to be the key hormone related to resource-defence aggression. While this role has been confirmed mostly in the context of reproduction in male vertebrates, the effect of testosterone on the expression of resource-defence aggression in female vertebrates is not so well established. Furthermore, laboratory work suggests that progesterone inhibits aggressive behaviour in females. In this study, we investigated the hormonal changes underlying territorial aggression in free-living female African black coucals, Centropus grillii (Aves; Cuculidae). Females of this sex-role reversed polyandrous bird species should be particularly prone to be affected by testosterone because they aggressively defend territories similar to males of other species. We show, however, that territorial aggression in female black coucals is modulated by progesterone. After aggressive territorial challenges female black coucals expressed lower levels of progesterone than unchallenged territorial females and females without territories, suggesting that progesterone may suppress territorial aggression and is downregulated during aggressive encounters. Indeed, females treated with physiological concentrations of progesterone were less aggressive than females with placebo implants. This is one of the first demonstrations of a corresponding hormone–behaviour interaction under challenged and experimental conditions in free-living females. We anticipate that our observation in a sex-role reversed species may provide a more general mechanism, by which progesterone—in interaction with testosterone—may regulate resource-defence aggression in female vertebrates.
PMCID: PMC2600909  PMID: 18252672
territorial aggression; females; testosterone; progesterone; sex-role reversal; classical polyandry
25.  Do adult eastern bluebird Sialia sialis males recognize juvenile-specific traits? 
Animal behaviour  2009;77(5):1267-1272.
Juveniles of many avian species possess spotted or mottled plumage that is distinct from the plumage of adults. Such plumage has typically been assumed to aid in camouflaging vulnerable immature birds. Here, we propose that spotty plumage signals juvenile status, thereby decreasing aggression from territorial adults. We tested this hypothesis by measuring the aggressive responses of adult eastern bluebird males to different combinations of simultaneously presented taxidermic mounts. We found that territorial males attacked adult models significantly more than juvenile models, and that they attacked adult models with orange breasts (typical of adults) more frequently than they attacked adult models with spotty breasts (typical of juveniles). We found no difference in attack rates when models with white breasts (a novel trait) were presented with models possessing spotty breasts. These observations indicate that breast colour is a cue used by territorial adults when identifying conspecific intruders, but that adults do not recognize juvenile-specific plumage as such. Adults respond aggressively only to orange-breasted intruders.
PMCID: PMC2703501  PMID: 20161226
Aggression; Eastern Bluebird; Juvenal Plumage; Honest Signals; Sialia sialis; Territoriality; Juveniles

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