[Show abstract][Hide abstract] ABSTRACT: Female birds may adjust their offspring phenotype to the specific requirements of the environment by differential allocation of physiologically active substances into yolks, such as androgens. Yolk androgens have been shown to boost embryonic development, growth rate and competitive ability of nestlings, but they can also entail immunological costs. The balance between costs and benefits of androgen allocation is expected to depend on nestling environment. We tested this hypothesis in a multi-brooded passerine, the spotless starling, Sturnus unicolor. We experimentally manipulated yolk androgen levels using a between-brood design, and evaluated its effects on nestling development, survival and immune function. Both in first and replacement broods, the embryonic development period was shorter for androgen-treated chicks than controls, but there were no differences in second broods. In replacement broods, androgen-treated chicks were heavier and larger than those hatched from control eggs, but this effect was not observed in the other breeding attempts. Androgen exposure reduced survival with respect to controls only in second broods. Regarding immune function, we detected non-significant trends for androgen treatment to activate two important components of innate and adaptive immunity (IL-6 and Ig-A levels, respectively). Similarly, androgen-treated chicks showed greater lymphocyte proliferation than controls in the first brood and an opposite trend in the second brood. Our results indicate that yolk androgen effects on nestling development and immunity depend on the environmental conditions of each breeding attempt. Variation in maternal androgen allocation to eggs could be explained as the result of context-dependent optimal strategies to maximize offspring fitness. This article is protected by copyright. All rights reserved.
This article is protected by copyright. All rights reserved.
Journal of Evolutionary Biology 06/2015; DOI:10.1111/jeb.12668 · 3.48 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Lipid peroxidation products are widely used as markers of oxidative damage in the organism. To properly interpret the information provided by these markers, it is necessary to know potential sources of bias and control confounding factors. Here, we investigated the relationship between two indicators of lipid mobilization (circulating levels of triglycerides and cholesterol) and two common markers of oxidative damage (plasma levels of malondialdehyde and hydroperoxides; the latter estimated from the d-ROMs assay kit). The following five avian species were studied: red-legged partridge (Alectoris rufa), zebra finch (Taeniopygia guttata), spotless starling (Sturnus unicolor), marsh harrier (Circus aeroginosus), and Montagu’s harrier (Circus pygargus). In all cases, plasma triglyceride levels positively and significantly correlated with lipid peroxidation markers, explaining between 8% and 34% of their variability. Plasma cholesterol, in contrast, showed a significant positive relationship only among spotless starling nestlings and a marginally significant association in zebra finches. These results indicate that lipid peroxidation marker levels covary with circulating lipid levels. We discuss the potential causes and implications of this covariation and recommend that future studies that measure oxidative damage using lipid peroxidation markers report both raw and relative levels (i.e., corrected for circulating triglycerides). Whether the observed pattern also holds for other tissues and in other taxa would deserve further research.
[Show abstract][Hide abstract] ABSTRACT: Anthropogenic noise is a major pollutant for organisms that live in urban areas. City birds modify their songs in ways that can increase their communication potential in spite of noise. However, these changes cannot prevent song masking by the extremely loud noises to which some urban bird populations are exposed. Here, we show that birds near a major airport advance their dawn singing time, thus reducing overlap with periods of intense aircraft noise. This modification was stronger in species whose normal singing time was relatively late, those which overlapped the most with aircraft noise. Although suggestive of a causal relationship, this pattern does not allow us to tell apart the effect of aircraft noise from that of other variables that may correlate with dawn singing time. In order to control for such potentially confounding variables, we replicated the study in several airports at different latitudes in Spain and Germany. The results show that indeed the overlap of song chorus with aircraft noise was the key factor that influenced time advancement. Aircraft traffic time was the main predictor of song advancement: across Europe, those bird populations whose singing time overlapped the most with aircraft traffic were those that advanced their song timing to a higher extent. Our results exemplify how behavioral plasticity may allow the survival of avian populations in areas of high noise pollution. However, such an adaptation likely involves departing from optimal singing times, leading to higher energetic costs and amplifying between-species differences in competitive ability and resilience.
[Show abstract][Hide abstract] ABSTRACT: Several techniques in ecological immunology have been used to assess bird immunocompetence thus providing useful information to understand the contribution of the immunological system in life-history decisions. The phytohaemagglutinin (PHA)-skin test has been the most widely employed technique being interpreted as the sole result of T lymphocytes proliferation and hence used to evaluate acquired immunological capacity. However, the presence of high numbers of phagocytic cells in the swelling point has cast some doubt about such an assumption. To address this issue, we collected blood from 14 days-old nestlings of spotless starling (Sturnus unicolor), administered subcutaneous PHA immediately after and then measured the swelling response 24 hours later. Differential counts of white blood cells suggested that an intense development of acquired immunological defences was taking place. The phagocytic activity of both heterophiles and monocytes was also very intense as it was the swelling response. Moreover, our results show, for the first time in birds, a positive relationship between the phagocytic activity of both kinds of cells and the swelling response. This broadens the significance of the PHA test from reflecting T lymphocytes proliferation -as previously proposed but still undetermined in vivo- to evaluate phagocytosis as well. In other words, our data suggest that the PHA swelling response may not be considered as the only consequence of processes of specific and induced immunity -T lymphocytes proliferation- but also of constitutive and nonspecific immunity -heterophiles and monocytes phagocytosis. We propose the extensive use of PHA-skin test as an optimal technique to assess immunocompetence.
PLoS ONE 12/2013; 8(12):e84108. DOI:10.1371/journal.pone.0084108 · 3.23 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Variable environments impose constraints on adaptation by modifying selection gradients unpredictably. Optimal bird development requires an adequate thermal range, outside which temperatures can alter nestling physiology, condition and survival. We studied the effect of temperature and nest heat exposure on the reproductive success of a population of double-brooded Spotless Starlings Sturnus unicolor breeding in a nestbox colony in central Spain with a marked intra-seasonal variation in temperature. We assessed whether the effect of temperature differed between first and second broods, thus constraining optimal nest-site choice. Ambient temperature changed greatly during the chick-rearing period and had a strong influence on nestling mass and all body size measures we recorded, although patterns of clutch size or nestling mortality were not influenced. This effect differed between first and second broods: nestlings were found to have longer wings and bills with increasing temperature in first broods, whereas the effect was the opposite in second broods. Ambient temperature was not related to nestling body mass or tarsus-length in first broods, but in second broods, nestlings were lighter and had smaller tarsi with higher ambient temperatures. The exposure of nestboxes to heat influenced nestling morphology: heat exposure index was negatively related to nestling body mass and wing-length in second broods, but not in first broods. Furthermore, there was a positive relationship between nest heat exposure and nestling dehydration. Our results suggest that optimal nest choice is constrained by varying environmental conditions in birds breeding over prolonged periods, and that there should be selection for parents to switch from sun-exposed to sun-protected nest-sites as the season progresses. However, nest-site availability and competition for sites are likely to impose constraints on this choice.
[Show abstract][Hide abstract] ABSTRACT: Begging in birds is a complex behaviour used by nestlings to solicit feeds from caregivers. Besides calling when parents are present, nestlings of some species also perform less conspicuous repeat calls when parents are absent. The fact that these calls are produced when parents are not at the nest does not mean that parents cannot hear them when they approach the nest or forage in its vicinity. In this study, we experimentally investigated the relationship between parent-absent repeat calls (ARC) and frequency of parental visits, considering parent/offspring communication as a possible implication of these acoustic signals. A playback experiment was conducted to detect changes in parental investment in response to increases in parent-ARC, expecting a differential sexual response. Results showed that females clearly responded to repeat calls, increasing their visit rate significantly with respect to females that received the control treatment. Males, on the contrary, did not change their visit rate in response to the treatment. This result provides evidence for a role of parent/offspring communication in parent-absent repeat calling, an additional function to sibling negotiation processes. The sex-specific response that we found is in agreement with previous studies that have found that females are more responsive than males to variation in solicitation and hunger signals performed by nestlings.
[Show abstract][Hide abstract] ABSTRACT: Yolk androgens in avian eggs play a significant role in embryo and nestling development. However, few studies have examined the differential effect of two of the main yolk androgens, testosterone (T) and androstenedione (A4). Here, we injected eggs of spotless starlings with physiological levels of either T, A4, the combination T+A4 or vehicle substance (control), to examine the differential ability of these steroids to influence nestling development. We found that the duration of the embryonic period was increased by T, and less so by A4, but not by the combination T+A4. Body condition was reduced in all experimental treatments where A4 was present, particularly so in the combination T+A4. Tarsus length was increased in males by A4, and in a lower degree by T, whereas the combination T+A4 inhibited growth. However, these differences in tarsus length between groups disappeared at the end of the nestling period. Cell-mediated immune responsiveness was marginally affected by the interaction between treatment and sex. These patterns suggest that in this species, T has a stronger influence during embryo development than A4, whereas during nestling development the capacities of both androgens to influence growth are similar. The combination T+A4 showed non-additive effects, suggesting either some kind of inhibition between the two androgens, or else an excessive effect due to a bell-shaped pattern of response. Our results suggest a complex picture of sex and age-dependent effects of T and A4, and underline the necessity of further research in the metabolism and action of egg androgens.
General and Comparative Endocrinology 09/2013; 194. DOI:10.1016/j.ygcen.2013.09.013 · 2.67 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: In noisy conditions, several avian species modulate their songs in amplitude and in the temporal or frequency domains, presumably to improve communication. Most studies on how passerine birds perform such adjustments have been carried out in oscines, a group well known for the importance of learning in the development of their songs. On the other hand, suboscines, in which learning appears to have little influence on the development of their songs, have been largely neglected. We evaluated song adjustment to noise in the vermilion flycatcher (Pyrocephalus rubinus), a suboscine bird. We conducted song recordings and noise measurements at several territories within Mexico City during the length of the dawn chorus. Males living in noisier places sang long songs, while those males inhabiting quieter places sang both short and long songs. We also found evidence of individual song plasticity, as males sang less versatile songs (i.e., songs with more introductory elements) later in the morning when noise levels were higher. This individual shift in song seems to be more associated to time of the day rather than to the observed rise in noise. However, we cannot discard an effect of noise, which should be evaluated with an experiment. We discuss our results in the context of other studies with oscine passerines and other taxa and consider implications for signaling in intra- and intersexual contexts.
[Show abstract][Hide abstract] ABSTRACT: Song learning has evolved within several avian groups. Although its evolutionary advantage is not clear, it has been proposed that song learning may be advantageous in allowing birds to adapt their songs to the local acoustic environment. To test this hypothesis, we analysed patterns of song adjustment to noisy environments and explored their possible link to song learning. Bird vocalizations can be masked by low-frequency noise, and birds respond to this by singing higher-pitched songs. Most reports of this strategy involve oscines, a group of birds with learning-based song variability, and it is doubtful whether species that lack song learning (e.g. suboscines) can adjust their songs to noisy environments. We address this question by comparing the degree of song adjustment to noise in a large sample of oscines (17 populations, 14 species) and suboscines (11 populations, 7 species), recorded in Brazil (Manaus, Brasilia and Curitiba) and Mexico City. We found a significantly stronger association between minimum song frequency and noise levels (effect size) in oscines than in suboscines, suggesting a tighter match in oscines between song transmission capacity and ambient acoustics. Suboscines may be more vulnerable to acoustic pollution than oscines and thus less capable of colonizing cities or acoustically novel habitats. Additionally, we found that species whose song frequency was more divergent between populations showed tighter noise-song frequency associations. Our results suggest that song learning and/or song plasticity allows adaptation to new habitats and that this selective advantage may be linked to the evolution of song learning and plasticity.
[Show abstract][Hide abstract] ABSTRACT: Recent changes in migration distances and propensity for migration associated with climate change have suggested that these traits can evolve rapidly. Part of this rapid response to selection may be due to maternal effects that facilitate changes in the underlying physiology of migration. We hypothesize that exposure to large amounts of antioxidants in the egg will facilitate assimilation and metabolism of dietary antioxidants later in life, thereby allowing offspring to better cope with extreme strenuous exercise such as the bursts of rapid migration shown during spring migration. We tested the relationship between temporal change in mean arrival date of migratory birds since 1960 and concentrations of 2 antioxidants in the eggs of 14 species of birds. Only egg concentration of vitamin E was a significant predictor of advancement in spring arrival date. Furthermore, we experimentally manipulated egg content of vitamin E in barn swallows Hirundo rustica and subsequently recorded arrival date of yearling male recruits. Arrival date advanced significantly by > 1 standard deviation due to treatment, providing experimental evidence for a relationship between egg concentration of vitamin E and subsequent migration behavior. These results are consistent with the hypothesis that maternal effects have played an important role in the evolution of bird migration.
Climate Research 11/2011; 49(3-3):201-210. DOI:10.3354/cr01030 · 2.71 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Research has shown that bird songs are modified in different ways to deal with urban noise and promote signal transmission through noisy environments. Urban noise is composed of low frequencies, thus the observation that songs have a higher minimum frequency in noisy places suggests this is a way of avoiding noise masking. Most studies are correlative and there is as yet little experimental evidence that this is a short-term mechanism owing to individual plasticity. Here we experimentally test if house finches (Carpodacus mexicanus) can modulate the minimum frequency of their songs in response to different noise levels. We exposed singing males to three continuous treatments: low-high-low noise levels. We found a significant increase in minimum frequency from low to high and a decrement from high to low treatments. We also found that this was mostly achieved by modifying the frequency of the same low-frequency syllable types used in the different treatments. When different low-frequency syllables were used, those sung during the noisy condition were longer than the ones sang during the quiet condition. We conclude that house finches modify their songs in several ways in response to urban noise, thus providing evidence of a short-term acoustic adaptation.
[Show abstract][Hide abstract] ABSTRACT: Recent changes in migration distances and propensity for migration associated with climate change have suggested that these traits can evolve rapidly. Part of this rapid response to selection may be due to maternal effects that facilitate changes in the underlying physiology of migration. We hypothesize that exposure to large amounts of antioxidants in the egg will facilitate assimilation and metabolism of dietary antioxidants later in life, thereby allowing offspring to better cope with extreme strenuous exercise such as the bursts of rapid migration shown during spring migration. We tested the relationship between temporal change in mean arrival date of migratory birds since 1960 and concentrations of 2 antioxidants in the eggs of 14 species of birds. Only egg concentration of vitamin E was a significant predictor of advancement in spring arrival date. Furthermore, we experimentally manipulated egg content of vitamin E in barn swallows Hirundo rustica and subsequently recorded arrival date of yearling male recruits. Arrival date advanced significantly by >1 standard deviation due to treatment, providing experimental evidence for a relationship between egg concentration of vitamin E and subsequent migration behavior. These results are consistent with the hypothesis that maternal effects have played an important role in the evolution of bird migration.
Climate Research 01/2011; 49(3):201-210. · 2.71 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: 1. Social and ecological conditions experienced by individuals during early life can strongly influence their development and survival. Nestlings of many species present important variations in plasma androgens that can be associated with begging and sibling competition and may translate into fitness effects, since broods with higher testosterone (T) production may have better body condition and higher fledging success. However, the positive effects of androgens may be counterbalanced by a reduction of immune defences and a greater susceptibility to diseases.
2. In this study we examined the potential relationships between natural variation in plasma T, immunity and post-fledging survival rate in nestlings of the spotless starling (Sturnus unicolor).
3. We found that nestlings with higher cellular-mediated immune responses (CMI; measured as a swelling response to phytohaemagglutinin injection) were more likely to be recruited in the population than nestlings with lower CMI responses. Males presented higher CMI response than females, possibly due to differences in competitive advantage over food. We also found that CMI response was negatively related to T levels, as predicted by the immunocompetence handicap hypothesis. However, despite this reduction in CMI response, we failed to find an association between nestling T levels and survival prospects. Our results add to the evidence of the role played by immune defences in determining survival prospects in natural populations.
4. In conclusion, our study reveals that CMI response can be considered as a good predictor of post-fledging recruitment. As far as we know, this is the first study attempting to evaluate the relationship between nestling T and post-fledging survival. Our results suggest that the potential benefits accrued by high levels of T in sibling competition during the nestling stage do not translate into increased survival.
[Show abstract][Hide abstract] ABSTRACT: Multiple male traits and displays may act in signalling sexually selected processes during courtship. Spotless starling males (Sturnus unicolor) carry green plants into their nests before egg laying, and recent studies have shown that this behaviour is related to female breeding decisions and the production of male-biased broods. Although the functional implications of this effect on females are not yet clear, data suggest that it could be mediated by female circulating hormones. Additionally, females may show higher androgen levels as a consequence of the increased female–female competition generated by the increase in male attractiveness. We tested this hypothesis using the same manipulation of green nesting material that has been previously shown to result in an increase of male attractiveness in male spotless starlings. We found that females in experimental nests increased their circulating testosterone levels during the laying period. In addition, there was an increase of social interferences in the experimental nests because of the addition of green plants. We hypothesise that testosterone may allow females to maintain their mating status when competing with other females for the preferred males. Addition of green plants also increased the variance in the levels of circulating testosterone, suggesting plasticity between females in their response to the manipulation. We propose that there is a functional link between high testosterone levels, male-biased sex ratios and female resource-holding potential in intra-sexual competition in this species.
[Show abstract][Hide abstract] ABSTRACT: In songbirds, sensory and social learning processes in juveniles contribute to variation in male song and female preferences. The developmental stress hypothesis proposes that suboptimal early development affects the costly brain structures involved in male song learning and, as a consequence, song quality. As an extension of this hypothesis we tested in this study whether developmental conditions also modulate female song preference acquisition. We tested song preferences in adult female zebra finches, Taeniopygia guttata, originating from a brood size manipulation experiment that had induced differences in mass, condition, immune response and levels of plasma testosterone at the early nestling stage. During the song-learning phase, juvenile birds were housed in small mixed-treatment groups with unrelated adult male song tutors. Adult females' song preferences were tested in an operant set-up where females could trigger different song playbacks by pecking different response keys. When females could choose between their own and an unfamiliar tutor's song they preferred their tutors' songs independent of experimental brood size. However, when females chose between two unfamiliar songs there was a significant effect of experimental brood size on preference strength: females from small broods showed significantly stronger preferences than those from medium and large broods. Hence, both females' rearing environment and sensory learning processes appear to contribute to variation in the direction and strength of female preference for male mating signals.
[Show abstract][Hide abstract] ABSTRACT: Bright yellow to red signals used in mate choice or intrasexual competition are based on carotenoid pigments that are hypothesized to be traded between physiological functions and coloration. These signals have recently been shown to be influenced by maternal effects. Indeed, yolk-derived carotenoids are essential for embryos to develop efficient carotenoid metabolism in posthatching life. Maternal effects facilitate adaptation to environmental variability and influence the evolution of phenotypic traits such as secondary sexual signals. Here we propose that maternal investment in yolk carotenoids promotes the evolution of carotenoid-based ornaments. We conducted a comparative analysis of lipid-soluble antioxidants (carotenoids and vitamins A and E) in the eggs of 112 species of bird. Species with large clutch sizes deposited higher yolk concentrations of the three antioxidants. There was a significant positive relationship between yolk carotenoids and the expression of male carotenoid-based signals, but not between yolk carotenoids and sexual dichromatism in these signals. These relationships were specific to carotenoids, as they were not found for vitamins A and E. This provides evidence consistent with the hypothesis that maternal effects mediated by yolk carotenoids play a role in the evolution of carotenoid-based signals as a response to sexual selection, likely based on organizational effects of carotenoids during embryo development.
The American Naturalist 09/2009; 174(5):696-708. DOI:10.1086/606021 · 4.45 Impact Factor
[Show abstract][Hide abstract] ABSTRACT: Although it is well documented that testosterone (T) is an important mediator in the regulation of behaviour in male vertebrates, its functional significance in females is less understood. Experimentally increased T in adult female birds has been found to have both advantageous and detrimental effects on behaviour and fitness. In addition, T may also mediate maternal effects when it is deposited into the egg yolk, and variations in androgen concentration between eggs contribute to differences in offspring phenotype and fitness. In this study we examined the effects of experimentally elevated female T on reproductive success and yolk androgen deposition in the spotless starling. The administration of exogenous T in female spotless starlings before egg laying caused negative effects on reproductive performance: when compared to control females T-females laid fewer eggs and raised fewer chicks. We also found an effect of elevated female T on yolk androgen deposition: T-females laid eggs with greater amounts of yolk T than control females, whereas yolk androstenedione levels were not affected. Although some of these effects likely involved a direct interference of female T with female reproductive function, some of them could be due to effects operating in eggs through maladaptive high T levels.
[Show abstract][Hide abstract] ABSTRACT: The influence of ambient noise in shaping birdsong attributes has received much attention lately. Recent work shows that some birds sing higher-pitched songs in noisy areas, which may allow them to avoid acoustic interference; yet it is not clear how this is achieved. Higher-pitched songs may be produced either by using the same syllable types in quiet and noisy areas, but singing them at a higher frequency in the latter (syllable pitch plasticity), or by using different syllable types in silent and in noisy circumstances (differential syllable use). Here we explored both strategies in the Mexico City population of house finch (Carpodacus mexicanus), a species known to possess a repertoire of several hundreds of syllable types. Birds produced songs with higher minimum frequencies in noisy than in quiet areas. This was mostly due to the minimum frequency of some syllable types being higher in noisy areas than in quiet locations. Also, males modulated the minimum frequency of the same syllable type during momentary increases of noise. Our results can help explain the high success of house finches at colonizing urban areas, while providing evidence of syllable pitch plasticity.