Female house martins (Delichon urbica) reduce egg androgen deposition in response to a challenge of their immune system

Female birds deposit in the yolks of eggs substantial amounts of androgens, such as testosterone and androstenedione. These androgens have been shown to speed up nestling development, induce a fast development of ornaments and increase dominance in adults. Experiments in several species have reported that females invest greater amounts of androgens in the eggs fathered by attractive males, suggesting that yolk androgen is a costly investment for either the offspring or the mother. There is some evidence that nestling immunocompetence may be partially suppressed by high levels of yolk androgens, but it is not known whether this is also the case for females. We tested this hypothesis in the house martin by inducing an immune challenge through an injection of sheep red blood cells, a standard challenge of the humoral immune system. Experimental birds laid eggs with lower amounts of yolk androstenedione than controls, and there was a similar non-significant trend for testosterone. Furthermore, the probability of laying a replacement clutch was higher for birds that had laid a first clutch with relatively high levels of yolk testosterone. These results suggest that yolk androgen deposition is limited by immune costs in the female, and that only females in good condition may afford to invest high levels of androgen in eggs in this species.     

The effects of testosterone on antibody production and plumage coloration in male house sparrows (Passer domesticus)

Many bird species have patches of colour in their plumage, contrasting with their basic coloration, which are used to display and signal status to conspecifics. These are called ’badges of status’, because they are believed to be low-cost signals of social status. For a signalling system to be evolutionarily stable, cheating must be controlled. The conventional view is that there is frequent testing, which uncovers cheats. Recently, the immunocompetence handicap hypothesis (ICHH) suggested that signals may be dependent on testosterone for their development, with a cost being imposed through immune suppression. We report experiments on house sparrows (Passer domesticus) which show that testosterone significantly influences the size of the bib (a ’badge of status’). The ultimate effect of the testosterone manipulation was to impair antibody production, as predicted by the ICHH. However, testosterone manipulations also changed the levels of the ’stress hormone’ corticosterone. The level of corticosterone was also related to the degree of immunosuppression. After controlling for the effect of corticosterone, testosterone enhanced the birds’ ability to produce antibodies, counter to the ICHH. The hypothesis therefore must be modified. We suggest that testosterone has a dual effect: it leads to immunosuppression through a mechanism involving corticosterone but, conversely, leads to increased immunocompetence probably via dominance influencing access to resources. Received: 5 March 1999 / Received in revised form: 1 October 1999 / Accepted: 16 October 1999     

Is avian humoral immunocompetence suppressed by testosterone?

A key issue in sexual selection theory is how a correlation between male secondary sexual characters and male genetic quality can be maintained. The immunocompetence-handicap hypothesis proposes that testosterone-dependent male characters remain honest signals because of the immunosuppressive effect of elevated steroid hormone levels. The hypothesis requires that physiological levels of testosterone depress immune system function. We quantified testosterone titers and humoral immunocompetence of captive male and female red-winged blackbirds (Agelaius phoeniceus) at three points in the annual cycle (autumn, prebreeding, and breeding). We also conducted an implant experiment on the males to assess the effects of prolonged, above-normal testosterone titers on humoral immune responses. Humoral immunocompetence was measured as secondary antibody production to a non-pathogenic protein antigen, keyhole limpet hemocyanin, using an enzyme-linked immunosorbent assay we developed for A. phoeniceus. Secondary antibody responses of individuals were highly repeatable between sampling periods. Neither physiological nor above-normal levels of plasma testosterone suppressed secondary antibody production. In paired tests of the same individuals between prebreeding and breeding, and between breeding and implant, plasma testosterone increased significantly but secondary antibody responses were unaffected. We are confident in these results because with 80% power, an 11–14% difference in antibody titers would have been detected. There was no relationship between plasma testosterone levels and humoral immunocompetence in free-ranging males tested at the peak of breeding. These results cast doubt on a key assumption of the immunocompetence-handicap hypothesis. Received: 13 April 1998 / Accepted after revision: 7 October 1998     

Parasite faunas,testosterone and secondary sexual traits in male red-winged blackbirds

Summary We examined associations among parasite infections, secondary sexual traits and testosterone in male red-winged blackbirds sampled at the start of the breeding season. Parasites quantified included ectoparasitic lice and mites and endoparasitic blood protozoans, nematodes, trematodes and cestodes. Secondary sexual traits that we quantified included body size, epaulet size and color, song repertoire size and song switching rate, and behavioral responses to male and female models. Overall we found few significant associations between parasites and secondary sexual traits, between secondary sexual traits and testosterone, or between parasites and testosterone. In addition, most parasite taxa appeared to infect birds independently, although the low prevalence (<50%) of many of the parasites meant that our sample sizes were too small to detect weak associations. Our most promising results were obtained for ectoparasitic mites, which tended to occur on birds uninfected with other parasites, on birds with longer epaulets, and on birds with higher levels of testosterone. Epaulet length and testosterone are both probable correlates of dominance in this species. Further research will be required to determine whether there is a causal link between the immunosuppressive effects of testosterone and the mite infections, and between testosterone, epaulet length and male mating success. Correspondence to: P. Weatherhead     

Social stimulation,nuptial colouration,androgens and immunocompetence in a sexual dimorphic cichlid fish

The nature of the costs maintaining honesty of sexual signalling in inter- and intrasexual interactions remains a contentious issue. For carotenoid-based colour ornaments, it has been hypothesized that the honesty of the signal is enforced when carotenoid allocation to colour expression is traded off against carotenoid availability for immunocompetence. In addition, honesty is enforced if androgens required for colour expression are immunosuppressive. We tested whether there is a trade-off between colour expression and immunocompetence in a lek-breeding haplochromine cichlid fish, Pundamilia nyererei, from Lake Victoria with a carotenoid-based nuptial dress. First, we showed that expression of red nuptial colouration and social rank in a group were positively correlated. We then successfully manipulated the level of colour advertisement by socially stimulating individually housed males with a rival male: Stimulated males developed larger areas of red nuptial colouration and had higher levels of circulating 11-ketotestosterone (11-KT) than non-stimulated males. We subsequently tested the humoral immune response to a novel antigen (sheep red blood cells). There was no overall significant effect of social stimulation on antibody production, but in the stimulated males, the degree of red colouration and the antibody response were negatively correlated. This significant interaction between colour and treatment thus shows that the negative correlation between colouration and antibody production is dependent on the (manipulated) social environment. This study provides correlational and experimental evidence for a trade-off between expression of a sexual trait and one component of immune function in fish. We found no evidence for a direct effect of 11-KT on antibody production, and we discuss alternative mechanisms that could mediate the trade-off.     

Tests of association between the humoral immune response of red-winged blackbirds (<Emphasis Type="Italic">Agelaius phoeniceus</Emphasis>) and male plumage,testosterone, or reproductive success

We explored the potential relationships between male traits, reproductive success, testosterone levels in the breeding season, and humoral immunocompetence in male red-winged blackbirds (Agelaius phoeniceus). Males responded to a single injection of diphtheria-tetanus vaccine by producing antibodies to both antigens. The primary responses to each antigen were positively correlated with each other, but the relationship was clearly non-linear. No male responded strongly to diphtheria without also responding strongly to tetanus, but many males had strong responses to tetanus and weak responses to diphtheria. Response to tetanus was positively associated with hormone levels, whereas the relationship between testosterone and the response to diphtheria was weakly and nonsignificantly negative. We found no convincing relationships between immune responses and male morphological traits (epaulet size, body blackness, and body size), male success in male-male competition (territory size and tenure), or male reproductive success (number of mates, average clutch size, proportion of offspring sired, or proportion of young fledged). These results do not support testosterone acting as a constraint on immunity. Testosterone could be mediating a condition-dependent trade-off between sexual ornaments and the immune system, but the evidence for this was weak, as neither any male sexual trait nor any measure of performance was associated with immune responses. We could not eliminate the possibility that male sexual traits advertise other aspects of immunity that are not dependent upon condition or hormones.     

The annual testosterone profile in cooperatively breeding superb fairy-wrens, Malurus cyaneus, reflects their extreme infidelity

Superb fairy-wrens are cooperatively breeding birds that combine stable, socially monogamous pair bonds and high levels of paternal care, with extreme levels of extra-pair mating and high levels of sexual competition. Our aim was to determine which testosterone correlates would prevail in such a life history that combines features that are conventionally associated with divergent hormone profiles. Unlike the situation in other species with monogamous pair bonds and high levels of paternal care, testosterone was elevated for a very long period of several months. During breeding there was a broad peak in testosterone followed by a gradual decline: this resembles the profile found in polygynous and promiscuous species. We found that three factors correlated with testosterone: development of the sexually selected nuptial plumage, social status and extra-group mating opportunities. Testosterone started increasing months prior to breeding, when the males that are later preferred as extra-group sires develop their nuptial plumage. Although these males did not have higher testosterone levels during breeding, they sustained high testosterone for much longer, and this might lend reliability to this sexual signal. Dominant males in groups had higher testosterone than pair-dwelling males and subordinate helpers. This was not due to differences in age, reproductive capability or mating opportunities, but was presumably associated with the assertion of dominance. In contrast to findings in other species, male testosterone level was not correlated with whether the resident female was fertile or had dependent nestlings. However, testosterone was strongly correlated with the total number of fertile females in the population, and hence with the opportunities for extra-group mating.     

Seasonal variation in the relationship between cellular immune response and badge size in male house sparrows (Passer domesticus)

The immunocompetence handicap hypothesis postulates that secondary sexual traits are honest signals of male quality because steroid hormones (such as corticosteroids and sex steroids), which are supposed to favor the development of secondary sexual traits, may also have immunosuppressive effects. Certain secondary sexual traits are not only used as mate choice signals but also play a role as badges of status. In the house sparrow (Passer domesticus), males have a bib of black feathers which is used both as a signal of social status in male-male interactions and by females when choosing a mate. We investigated the relationships between bib size and cellular immune response in male house sparrows during and outside the reproductive season. Males with large badges were found to have lower levels of immunocompetence, as assessed using a T-cell-mediated immunity assay, during the reproductive season, as predicted by the immunocompetence handicap hypothesis. Conversely, in November, the correlation between badge size and cellular immune response was positive, possibly reflecting the better access to trophic resources of large-badged dominant males in winter flocks. Received: 24 September 1998 / Received in revised form: 2 February 1999 / Accepted: 14 February 1999     

Effects of testosterone on male-male competition and male-female interactions in blue tits

In temperate-zone birds, testosterone (T) influences male behavior during the breeding season. The elevation of plasma levels of T to a breeding baseline is necessary for basic reproductive behaviors, but it is still unclear whether variation in T levels above this critical threshold influences the intensity of these behaviors. Such a relationship between T and sexually selected traits is a critical assumption of the immunocompetence handicap hypothesis. We here experimentally elevated T levels in blue-tit males above the natural mean (T-males) during the period of nest building and egg laying, without manipulating hormone levels during chick feeding. T-males neither interacted more often with other males, nor did they respond more aggressively to a dummy intruder, compared to males with control implants. T-males did not guard their social mates more closely, but they were more likely to interact with potential extra-pair mates. Females mated to T-males did not change their behavior during egg laying and the treatment did not significantly affect male and female feeding rates. Despite this, nests of T-males produced larger and heavier fledglings in one study year. Our observations suggest that T levels above the natural mean during the mating period do not increase aggressive or territorial behavior in male blue tits. However, if females perceived T-males as high-quality mating partners, superior offspring development in nests of T-males might be caused by higher maternal investment. Hence, male behaviors involved in mate attraction may have been influenced by T levels above the natural mean.Communicated by R. Gibson     

Bill color, not badge size, indicates testosterone-related information in house sparrows

The honesty of ornamental signals of quality is often argued to be enforced via costs associated with testosterone. It is still poorly understood, however, how seasonal variation of testosterone within individuals is related to the timing and extent of ornament development. Here, we studied inter- and intra-individual variability of plasma testosterone levels in a population of 150 captive male house sparrows (Passer domesticus) through the course of a full year. We further analyzed the relationship between plasma testosterone levels and two sexually dimorphic ornaments: badge size and bill coloration. Also, because of a known negative relation between molt and circulating testosterone levels, we analyzed the relationship between ornamentation and molt status during the fall. We found that testosterone levels increased towards the breeding season and decreased before the onset of annual molt. However, within individuals, relative testosterone titers demonstrated low repeatability between seasons. Plasma testosterone levels were not correlated with badge size in any season but were correlated strongly with bill coloration during all periods, except the breeding season when variation in bill color was low. Finally, we found that bill coloration strongly correlated with molt status during fall. Our results indicate that bill coloration, not badge size, is the best ornamental indicator of a “running average” of male testosterone in house sparrows and therefore the best potential indicator of qualities and/or behavioral strategies associated with testosterone.     

Impact of miniature geolocation loggers on a small petrel, the thin-billed prion Pachyptila belcheri

Effects of deployment of miniaturised transmitters and loggers have been studied mainly in diving seabirds such as penguins, and less so in flying seabirds. However, some studies of albatrosses and petrels recorded extended trip durations and elevated rates of nest desertion following device attachment, especially if transmitter loads exceeded 3 % of adult mass. Studies have usually compared performance parameters such as trip duration, meal mass, breeding success or rate of return in the next season between birds with devices and controls. We here examined the effects of geolocator loggers (Global Location Sensing, (GLS)) on thin-billed prions Pachyptila belcheri (130 g), by comparing performance parameters and additionally eco-physiological parameters. GLS weighed ca. 1 % of the body mass, and were fixed on leg rings, which may influence the flight efficiency by creating an asymmetric load. We found no differences in the performance parameters, either in the season of attachment or the season following recovery. Similar stable isotope ratios in adult blood and feather samples further indicated that the foraging ecology was not influenced. However, after 1 year of logger deployment, adults differed in their hormonal response to stress: while baseline corticosterone levels were not influenced, corticosterone levels in response to handling were elevated. Moreover, increased heterophil/lymphocyte ratios and a decreased tail growth in winter suggest that carrying the GLS was energetically costly, and adults adapted physiologically to the higher work load, while keeping up a normal breeding performance.     

Are white-crowned sparrow badges reliable signals?

Status badges, such as crown plumage, mediate intraspecific interactions. The reliability of crown morphology as a status badge in male mountain white-crowned sparrows (Zonotrichia leucophrys oriantha) is uncertain. We examined morphological and physiological correlates of the proportion of crown that was white (“crown-white”) in 178 male mountain white-crowned sparrows during the 2008–2009 breeding seasons. Using a paired experimental design, we presented territory-holding males with white-enhanced and white-reduced decoys and recorded aggressive behaviors. To assess physiological constraints on signal bluffing, a subsample of birds was captured and released after manipulating natural crowns to simulate bluffed white-enhanced or white-reduced crowns; corticosterone concentrations were assayed from blood drawn upon recapture and after a restraint-induced stressor. We found a significant positive association between crown-white and a measure of body size—tarsus length—which is an established indicator of resource-holding potential. In the decoy challenge, males responded more aggressively toward white-enhanced than white-reduced decoys. In the hormone experiment, white-enhanced birds had higher baseline corticosterone levels, whereas white-reduced birds had similar concentrations to controls. Furthermore, white-enhanced birds had an attenuated restraint-induced corticosterone response, while white-reduced birds mounted a significantly larger increase in corticosterone than controls. Taken together, these findings indicate that crown-white is a reliable status badge of resource-holding potential in male mountain white-crowned sparrows during the breeding season.     

Fitness costs of an immune response in the house martin (<Emphasis Type="Italic">Delichon urbica</Emphasis>)

Immune responses constitute a major way for hosts to defend themselves against parasites. Because hosts do not habitually produce strong responses all the time, immune responses might be costly to produce or maintain. We tested experimentally if the production of a response to a challenge with a novel antigen resulted in a cost in terms of fitness using the highly colonial house martin Delichon urbica as a model system. We injected adult breeding birds during laying of the first clutch with either Newcastle disease virus (NDV) or a control injection, and the clutch was subsequently removed to induce relaying. NDV stimulates the non-specific immune system, causing production of antibodies during a period of more than 2 weeks. Accordingly, we found an increase in leukocyte counts in experimental birds compared to controls. Experimental treatment reduced the frequency of re-laying, caused a delay in timing of relaying and a reduction in brood size. Quality of nestlings in terms of body size, body mass and T-cell-mediated immune response did not differ significantly between treatments. Overall, seasonal reproductive success differed significantly between treatments, showing that the production of an immune response by adult birds is costly in terms of future fecundity.     

Dominance behaviour,body weight and fat variations,and partial migration in European blackbirds Turdus merula

Summary A partially migratory population of European blackbirds Turdus merula was studied in central Europe during the non-breeding season. Body weight and the amount of subcutaneous fat deposits showed seasonal variations typical for each age and sex category. Juveniles were fattest in autumn and spring and both juveniles and females lost fat and body weight in mid-winter. Adults and males reached their maximum body weight in mid-winter. These findings together with data from Schwabl (1983) suggest that juveniles and females constitute the main fraction of those birds migrating from the area in autumn. In winter mainly adults and males have access to food resources. These patterns may be regulated by dominance behaviour, since adults and males are usually dominant over juveniles and females throughout the non-breeding season. Subordinate birds that stay in the area probably suffer from a higher winter mortality but have the advantage of early breeding.     

Diving costs and benefits during post-breeding movements of the Mediterranean shag in the North Adriatic Sea

From the 1980s, Mediterranean shags Phalacrocorax aristotelis desmarestii have become regular summer visitors in the Gulf of Trieste (N-E Italy), as post-breeding movements from Croatian breeding colonies. To characterize such a recent habit and to explore diving optimality models, we investigate foraging strategies and diving patterns at different depths, during breeding and post-breeding seasons. Behavioural data were cross-checked with the species’ diet. Shags foraged on and close to the sea bed, with a prevalent anticipatory breathing strategy. In the Gulf of Trieste, the shallow depths and low mobility of prey allowed shags to use just the oxygen of the respiratory tract, reducing the physiological stress for diving. In Croatia, dive costs increased with depth and prey mobility, resulting in a higher oxygen expenditure that involved also respiratory stores. Such ecological and physiological aspects characterize the Gulf of Trieste as an optimal area for feeding and restoring from the costs of breeding season incurred in Croatia and could be the basis of these post-breeding movements.     

Effect of photoperiod on the adrenal activities of male rose ringed parakeet, Psittacala krameri

Adult male rose ringed parakeets were exposed to very long photoperiod (22 hr L: 2 hr D) and very short photoperiod (2 hr L: 22 hr D) daily for 60 days during different phases of the annual testicular cycle. Adrenal activities of the experimental birds were compared with that of parallel held natural photoperiodic birds. Marked atrophy of adrenocortical cells was noted in the glands of long photoperiod (22 hr L:2 hr D) during different phases, i.e., post-breeding, quiescent and pre-breeding phases of annual gonadal cycle. The atrophied cells were not uniformly distributed in different groups of long photoperiod responsive birds. During pre-breeding, post-breeding and quiescent phases marked atrophy of the adrenocortical cells were restricted to the sub capsular zone of the gland. The cytometric and karyometric studies also revealed significant decrease in the cortical cord width and diameter of nuclei in the cortical cells in either subcapsular zone in the gland of long photoperiodic birds considered for treatment during pre-breeding, post-breeding and quiescent phase or in both the sub capsular zone and the inner zone. The cytometric and karyometric values did not show any change from control birds.     

Transatlantic migration by post-breeding puffins: a strategy to exploit a temporarily abundant food resource?

The distribution of Atlantic puffins (Fratercula arctica) from Skellig Michael, south-west Ireland, was investigated using geolocation loggers between the 2010 and 2011 breeding seasons. All tracked birds travelled rapidly west into the North Atlantic at the end of the breeding season in August, with the majority undertaking transatlantic trips from Ireland to the Newfoundland-Labrador shelf. The furthest distance from the colony reached by each bird was not influenced by body mass or sex and was achieved in approximately 20 days. By October, all birds had moved back to the mid Atlantic where they remained resident until returning to the breeding colony. The most parsimonious explanation for the rapid, directed long-distance migration is that birds exploit the seasonally high abundance of prey [e.g., fish species such as capelin (Mallotus villosus) and sandlance (Ammodytes spp.)] off the Canadian coast, which is also utilised by large populations of North American seabirds at this time. Once the availability of this short-term prey resource has diminished, the tracked puffins moved back towards the north-east Atlantic. A relationship between relative abundance of puffins and zooplankton was found in all winter months, but after correcting for spatial autocorrelation, was only significant in November and January. Nevertheless, these results suggest a potential switch in diet from mainly fish during the breeding and early post-breeding periods to zooplankton over the remaining winter period. This study suggests that puffins from south-west Ireland have a long-distance migration strategy that is rare in breeding puffins from the UK and identifies a key non-breeding destination for puffins from Ireland. This has implications for the susceptibility of different breeding populations to the effects of possible climatic or oceanographic change.     

The endocrinology of male rhesus macaque social and reproductive status: a test of the challenge and social stress hypotheses

Social status primarily determines male mammalian reproductive success, and hypotheses on the endocrinology of dominance have stimulated unprecedented investigation of its costs and benefits. Under the challenge hypothesis, male testosterone levels rise according to competitive need, while the social stress hypothesis predicts glucocorticoid (GC) rises in high-ranking individuals during social unrest. Periods of social instability in group-living primates, primarily in baboons, provide evidence for both hypotheses, but data on social instability in seasonally breeding species with marked social despotism but lower reproductive skew are lacking. We tested these hypotheses in seasonally breeding rhesus macaques on Cayo Santiago, Puerto Rico. We documented male fecal GC and androgen levels over a 10-month period in relation to rank, age, natal status, and group tenure length, including during a socially unstable period in which coalitions of lower ranked males attacked higher ranked males. Androgen, but not GC, levels rose during the mating season; older males had lower birth season levels but underwent a greater inter-season rise than younger males. Neither endocrine measure was related to rank except during social instability, when higher ranked individuals had higher and more variable levels of both. High-ranking male targets had the highest GC levels of all males when targeted and also had high and variable GC and androgen levels across the instability period. Our results provide evidence for both the challenge and social stress hypotheses.     

Interactions among endocrinology,seasonal reproductive cycles and the nesting biology of the female green sea turtle

We collected data on plasma levels of testosterone+5a-dihydrotestosterone (T+DHT) and corticosterone (CORT) from adult female green sea turtles (Chelonia mydas) from southern Queensland during distinct stages of their reproductive cycle. Those females capable of breeding in a given year had elevated plasma steroid levels (T+DHT 0.91ǂ.08; CORT 1.05ǂ.29 ng/ml), associated with follicular development, until courtship began in October. At the beginning of the nesting season in November plasma levels of CORT were related to when the female first nested (r²=0.06; F=10.45; P=0.01). However, they were not correlated with the number of clutches a female laid in that season (F=3.65; P=0.08). We repeatedly sampled 23 turtles over the nesting season and profiled changes in steroids immediately following oviposition of each clutch. Levels of T+DHT (range 0.41-0.58 ng/ml) and CORT (range 2.13-2.81 ng/ml) were similar through the early stages of the nesting season and inter-nesting period, and declined to near basal levels (T+DHT 0.37ǂ.03 and CORT 1.85-ng/ml) following the last clutch for the season. Steroid hormone levels were also low (T+DHT 0.38ǂ.16; CORT 0.46ǂ.21 ng/ml) in four independent post-breeding (atretic) females; samples for these females were taken at a time when body condition was presumably at the lowest for the season. Subtle changes in the nesting environment, such as variation in nesting habitat or the time of night that nesting occurred, were associated with a small and slow CORT increase. We suggest CORT is increased in nesting females to assist in lipid transfer to prepare the ovarian follicles and/or the reproductive organs for ovulation.