Timing of breeding in variable environments: tropical birds as model systems

Animals need to adjust reproductive decisions to environmental seasonality. In contrast to species from the well-studied temperate zones, little is known for tropical birds about the environmental cues that stimulate reproductive activity and the physiological mechanisms that regulate reproduction. I am investigating the environmental and endocrine mechanisms that underlie the timing of reproduction in spotted antbirds from the near-equatorial Panamanian rainforest and in small ground finches from the equatorial arid Galápagos islands. Spotted antbirds live in a fairly predictable seasonal environment and show regular changes in gonad sizes and some reproductive hormones. Despite the small annual variation in photoperiod close to the equator, these birds can measure slight photoperiodic increases and use it to initiate reproductive activity. Spotted antbirds also respond to seasonal changes in food availability, which allows them to flexibly adjust gonad growth to environmental conditions. Testosterone is involved in regulating song and aggressive behavior in these year-round territorial birds, although it can remain at low plasma levels throughout the year. In contrast, small ground finches exposed to a rather unpredictable climate on Galápagos appear to grow their gonads whenever heavy rains fall and have regressed gonads during other times of the year. The lack of a physiological preparation for the breeding season and their response to short-term cues related to rainfall indicate a striking flexibility in the regulation of breeding in small ground finches. I suggest that tropical birds can serve as model systems to study the physiological adaptations to different environments. Unraveling the neuroendocrine mechanisms behind the flexibility in reproductive timing will clarify whether differences found between temperate and tropical birds represent variations of the same basic mechanism or instead reflect a fundamental divergence in physiological control systems.     

Carotenoids modulate the trade-off between egg production and resistance to oxidative stress in zebra finches

The allocation of resources to reproduction and survival is a central question of studies of life history evolution. Usually, increased allocation to current reproduction is paid in terms of reduced future reproduction and/or decreased survival. However, the proximal mechanisms underlying the cost of reproduction are poorly understood. Recently, it has been shown that increased susceptibility to oxidative stress might be one of such proximate links between reproduction and self-maintenance. Organisms possess a range of antioxidant defenses, including endogenously produced molecules (e.g., enzymes) and compounds ingested with food (e.g., carotenoids). If reproductive effort increases the production of reactive oxygen species, the availability of antioxidant defenses may partly or fully counteract the free-radical damages. One could, therefore, expect that the trade-off between reproduction and oxidative stress is modulated by the availability of antioxidant defenses. We tested this hypothesis in zebra finches. We manipulated reproductive effort by either allowing or preventing pairs to breed. Within each breeding or non-breeding group, the availability of antioxidant compounds was manipulated by supplementing or not supplementing the drinking water with carotenoids. We found that although birds in the breeding and non-breeding groups did not differ in their resistance to oxidative stress (the breakdown of red blood cells submitted to a controlled free-radical attack), one aspect of breeding effort (i.e., the number of eggs laid by birds in both breeding and non-breeding groups) was negatively correlated with resistance to oxidative stress only in birds that did not benefit from a carotenoid-supplemented diet. This result therefore suggests that carotenoid availability can modulate the trade-off between reproduction and resistance to oxidative stress.     

Visual and nutritional food cues fine-tune timing of reproduction in a neotropical rainforest bird

Food may act as a proximate factor in the regulation of avian seasonal breeding. Food cues could provide particularly important seasonal information to birds living in variable tropical environments, but this has not yet been tested. Spotted antbirds (Hylophylax n. naevioides) inhabiting a humid forest in central Panama (9 degrees N) likely use changes in the tropical photoperiod to time reproduction on a long-term, seasonal basis. We predicted that these insectivorous birds also adjust reproduction to short-term cues such as food availability because the onset of the rainy season and the resulting increase in insect abundance varies considerably between years. To test this prediction, prior to their breeding season (when they had half-maximal gonads), we either exposed captive male spotted antbirds to an ad libitum standard diet only or added live crickets to this diet. Males that received live crickets significantly increased gonad sizes within 3 weeks over controls on the standard diet. Moreover, in six additional experiments cricket availability always increased song rate, usually within a few days. The stimulatory effect of live crickets on song activity may function independent of nutritional aspects: Freshly killed crickets, providing similar nutritional content as live crickets, did not stimulate the birds' song activity. However, song activity increased to intermediate levels when live crickets were shown under a clear plastic wrap, i.e., when birds could see but not eat crickets. We hypothesize that the opportunity to see and handle live insects stimulates song and reproductive activity in these birds. Our data indicate for the first time that a tropical rainforest bird can use food cues to evaluate the suitability of local environmental conditions for breeding. J. Exp. Zool. 286:494-504, 2000.     

Empirical evidence of a trade-off between reproductive effort and expectation of future reproduction in female three-spined sticklebacks

Optimal life-history models generally predict that the reproductive effort of iteroparous organisms may increase with age, as their expectation of future reproduction decreases. The population of three-spined sticklebacks (Gasterosteus aculeatus) in the Camargue (Rhone River Delta, France) is annual, all adults dying after their first breeding season. As the three-spined stickleback is a multiple spawner, we tested the hypothesis that reproductive effort may increase during the breeding season on field data. From 1987 to 1998, 653 female sticklebacks were collected in the field during the breeding seasons. The body size, body weight and weights of the liver, gonads and carcass were measured for these individuals. Only gravid females with mature eggs (176 fish) were included in the analysis. Considering the female three-spined stickleback as a capital breeder, the energetic resources available for allocation between soma and gonads were estimated by its body weight. Somatic condition decreased during the breeding season and reproductive effort (gonad weight relative to body weight) increased. These patterns did not vary significantly between years. These observed variations in reproductive effort during the breeding season can be interpreted as empirical evidence of a trade-off between reproductive effort and expectation of future reproduction.     

Population dynamics in a long-lived seabird: I. Impact of breeding activity on survival and breeding probability in unbanded king penguins

Understanding the trade-off between current reproductive effort, future survival and future breeding attempts is crucial for demographic analyses and life history studies. We investigated this trade-off in a population of king penguins (Aptenodytes patagonicus) marked individually with transponders using multistate capture-recapture models. This colonial seabird species has a low annual proportion of non-breeders (13%), despite a breeding cycle which lasts over 1 year. To draw inferences about the consequences of non-breeding, we tested for an effect of reproductive activity on survival and on the probability of subsequent breeding. We found that birds non-breeding in year t show the same survival rate as breeders (two-states analysis: breeding and non-breeding). However, breeders had a lower probability of breeding again the following year. This negative phenotypic correlation suggests the existence of reproductive costs affecting future breeding probability, but it might also be strengthened by late arrival for courtship in year t. A three-state analysis including breeding success revealed that failed breeders in year t have a lower probability to reproduce successfully in year t + 1 than non-breeders in year t, providing some evidence for the existence of reproductive costs. Moreover, successful breeders showed higher survival probability. This positive phenotypic correlation between current reproduction and subsequent survival supports the hypothesis of an heterogeneity in individual quality. Males breeding in year t had a lower probability to breed again in year t + 1 than females, suggesting higher reproductive costs for this sex. Such additional costs might be due to higher male parental investment in the final phase of chick-rearing, which also delays the arrival of males in year t + 1, and decreases their breeding probability. Our study is the first to explore the breeding biology and the demography of penguins without the disturbance of flipper-bands.     

Seasonal changes in testosterone and corticosterone levels in four social classes of a desert dwelling sociable rodent

Animals have to adjust their physiology to seasonal changes, in response to variation in food availability, social tactics and reproduction. I compared basal corticosterone and testosterone levels in free ranging striped mouse from a desert habitat, comparing between the sexes, breeding and philopatric non-breeding individuals, and between the breeding and the non-breeding season. I expected differences between breeders and non-breeders and between seasons with high and low food availability. Basal serum corticosterone was measured from 132 different individuals and serum testosterone from 176 different individuals of free living striped mice. Corticosterone and testosterone levels were independent of age, body weight and not influenced by carrying a transmitter. The levels of corticosterone and testosterone declined by approximately 50% from the breeding to the non-breeding season in breeding females as well as non-breeding males and females. In contrast, breeding males showed much lower corticosterone levels during the breeding season than all other classes, and were the only class that showed an increase of corticosterone from the breeding to the non-breeding season. As a result, breeding males had similar corticosterone levels as other social classes during the non-breeding season. During the breeding season, breeding males had much higher testosterone levels than other classes, which decreased significantly from the breeding to the non-breeding season. My results support the prediction that corticosterone decreases during periods of low food abundance. Variation in the pattern of hormonal secretion in striped mice might assist them to cope with seasonal changes in energy demand in a desert habitat.     

Spatial distribution and time budget of radio-tagged grey herons, Ardea cinerea, during the breeding season

Spatial distribution of foraging grey herons during the breeding season seemed to be determined by a trade-off between costs and benefits of area sampling versus site fidelity. Breeding birds with little experience of the area spent more time exploring than birds with more experience in the early stages of reproduction. Non-breeding herons and first-year breeders showed little site fidelity. Time budgets appeared to be affected mainly by daily changes in food availability and, for breeding birds, by demands of the brood.     

Malaria-Infected Female Collared Flycatchers (Ficedula albicollis) Do Not Pay the Cost of Late Breeding

Life-history theory predicts that the trade-off between parasite defense and other costly traits such as reproduction may be most evident when resources are scarce. The strength of selection that parasites inflict on their host may therefore vary across environmental conditions. Collared flycatchers (Ficedula albicollis) breeding on the Swedish island Öland experience a seasonal decline in their preferred food resource, which opens the possibility to test the strength of life-history trade-offs across environmental conditions. We used nested-PCR and quantitative-PCR protocols to investigate the association of Haemosporidia infection with reproductive performance of collared flycatcher females in relation to a seasonal change in the external environment. We show that despite no difference in mean onset of breeding, infected females produced relatively more of their fledglings late in the season. This pattern was also upheld when considering only the most common malaria lineage (hPHSIB1), however there was no apparent link between the reproductive output and the intensity of infection. Infected females produced heavier-than-average fledglings with higher-than-expected recruitment success late in the season. This reversal of the typical seasonal trend in reproductive output compensated them for lower fledging and recruitment rates compared to uninfected birds earlier in the season. Thus, despite different seasonal patterns of reproductive performance the overall number of recruits was the same for infected versus uninfected birds. A possible explanation for our results is that infected females breed in a different microhabitat where food availability is higher late in the season but also is the risk of infection. Thus, our results suggest that another trade-off than the one we aimed to test is more important for explaining variation in reproductive performance in this natural population: female flycatchers appear to face a trade-off between the risk of infection and reproductive success late in the season.     

Thermal parameters changes in males of Rhinella arenarum (Anura:Bufonidae) related to reproductive periods

The regulation of body temperature in ectotherms has a major impact in their physiological and behavioral processes. Observing changes in thermal parameters related with reproduction allows us to better understand how Rhinella arenarum optimizes a thermal resource. The aim of this study was to compare the thermal parameters of this species between breeding and non-breeding periods. In the field, we recorded the body temperature from captured animals, the air temperature, and the temperature of the substrate. In the laboratory, we measured the temperature R. arenarum selected on a thermal gradient and the critical extreme temperatures. The results of our study show variations in thermal parameters between the two situations studied. This species makes efficient use of thermal resources during the breeding period by basking to significantly increase body temperature. Because calling is energetically costly for males, this behavior results in increased efficiency to callers during the breeding period.     

Home-ranges of tropical Red-capped Larks are influenced by breeding rather than vegetation,rainfall or invertebrate availability

Home-range studies have received considerable attention from ecologists but are greatly skewed towards the north temperate areas. Tropical areas offer an ideal setting to tease apart hypotheses about weather, food availability and social interactions as important factors influencing home-range. In this study, we investigated home-range and movement patterns of the tropical Red-capped Lark Callandrella cineria, a year-round breeding bird with a dynamic social structure. We tracked 56 individuals using radiotransmitters and colour-ring readings over a 23-month period. Our objective was to understand year-round variation in home-range size in the context of the highly aseasonal and unpredictable variation in weather and resources typical of many equatorial habitats, in addition to the birds’ changing social structure and year-round breeding. The mean composite monthly home-range of Red-capped Larks was 58.0 ha, and the mean individual home-range size was 19.9 ha, but this varied considerably between individuals. The total number of nests found per month (breeding intensity) best predicted home-range size of non-breeding birds, and of breeding and non-breeding birds combined. We show for the first time that breeding intensity decreases the home-range size of non-breeding individuals. Our study also underlines the relevance of conducting more studies in aseasonal tropical areas in order to disentangle effects of weather, food availability and breeding that vary in parallel, peaking simultaneously in most seasonal areas.     

At the crossroads of physiology and ecology: Food supply and the timing of avian reproduction

The decision of when to breed is crucial to the reproductive success and fitness of seasonally breeding birds. The availability of food for adults prior to breeding has long been thought to play a critical role in timing the initiation of seasonal reproductive events, in particular laying. However, unequivocal evidence for such a role remains limited and the physiological mechanisms by which an increase in food availability results in seasonal activation of the reproductive system are largely speculative. This lack of mechanistic information partly reflects a lack of integration of ecological and physiological approaches to study seasonal reproduction. Indeed, most work pertaining to the role of food availability for adults on the timing of avian reproduction has been ecological and has focused almost exclusively on female traits associated with reproductive timing (e.g., lay date and clutch size). By contrast, most work on the physiological bases of the relationship between food availability and the timing of reproduction has investigated male traits associated with reproductive development (e.g., reproductive hormones and gonadal development). To advance our understanding of these topics, we review the role of proximate factors including food availability, social factors, and ambient temperature in the control of breeding decisions, and discuss the role of three potential candidates (leptin, glucocorticoids, and GnIH–neuropeptide Y) that may mediate the effects of food availability on these decisions. We emphasize that future progress in this area is heavily contingent upon the use of physiology-based approaches and their integration into current ecological frameworks.     

Vasotocin treatment inhibits courtship in male zebra finches; concomitant androgen treatment inhibits this effect

Zebra finches evolved in arid areas of Australia. Their reproduction is stimulated by water availability, which is unpredictable. Cheng (Poult. Sci. Rev. 5 (1993) 37) hypothesized that the primary mechanism controlling reproduction in species relying on unpredictable cues should be inhibitory. The onset of stimulatory environmental conditions terminates the inhibition, allowing rapid initiation of reproduction. As the primary hormone regulating water balance in birds, arginine vasotocin (AVT) appears a likely candidate to modulate reproduction in finches. Drought conditions cause sustained AVT release, which in other species inhibits androgen production. To determine whether increased AVT inhibits reproductive behavior, intact males were tested with females and divided into three groups matched for courtship behavior. Osmotic minipumps containing (a) saline, (b) 264 ng AVT, or (c) 1320 ng AVT in saline were implanted subcutaneously and males tested 48 h later. AVT-treated males socialized with females, but the high dose significantly reduced singing and courtship displays. To determine whether AVT acted by depressing androgen secretion, additional males were given subcutaneous androgen implants and divided into two groups matched for courtship behavior. Males were then implanted with minipumps containing (a) saline or (b) the high AVT dose. Males treated with AVT plus androgen showed no deficits in courtship behavior. These data suggest that AVT secretion during periods of drought may inhibit reproduction by inhibiting androgen production. Inhibition of reproductive behavior by AVT may be a more general phenomenon. Large quantities of AVT or, in mammals the closely-related peptide vasopressin (VP), are released when animals are stressed, and high levels of AVT/VP may inhibit reproductive behavior. The extremely short half-life of these peptides means that once proximal factors become more favorable, the gonads should rapidly be released from the peptides' inhibitory actions.     

Sex and migratory strategy influence corticosterone levels in winter-grown feathers,with positive breeding effects in a migratory pelagic seabird

To overcome unpredictable stressful transitory events, animals trigger an allostatic response involving the hypothalamic–pituitary–adrenal cortex. This hormonal response, which involves the release of glucocorticoids which in turn mediate between the main physiological mechanisms that regulate the energetic demands and resource allocation trade-off with behavioural responses to environmental perturbations and may ultimately lead to variation in fitness. We have used the Cory’s shearwater Calonectris borealis, a sexually dimorphic pelagic seabird with a partial migratory strategy, as a model bird species to analyse a number of traits related to the stress response. We investigated whether the activation of a stressful response, mediated by corticosterone, during the wintering period (1) correlated with the previous breeding success, (2) was affected by the migratory behaviour of male birds and (3) had consequences in the fitness of the birds. Corticosterone levels in feathers grown overwinter were analysed in 61 adult birds during three consecutive migratory periods (2009–2012) and in 14 immature birds in the wintering period 2010–2011. Moreover, the levels of corticosterone were analysed in experimental birds which were freed from their reproductive duties and compared with control birds which raised fledglings to the end of the breeding period. The results show that the levels of corticosterone were sex dependent, differed between years and were affected by the migratory strategy performed by the birds. The activation of the stressful response over the wintering period generated residual carry-over effects that positively affected the reproductive output in the subsequent breeding stage, a phenomenon previously undescribed in a long-lived pelagic seabird. Our study provides evidence that the analysis of corticosterone from feathers is a useful tool to evaluate carry-over effects in birds far away from breeding sites, opening new possibilities for future studies in this field.     

睾酮对鸟类繁殖影响研究进展

类固醇激素睾酮是影响鸟类繁殖最重要的性激素之一,与鸟类的繁殖行为的各个方面息息相关。睾酮通过影响鸟类的羽色、鸣声等来影响鸟类的配偶选择,同时睾酮可以调节配偶选择和繁殖投入之间的平衡。睾酮水平影响出雏数、出飞数、孵化率成功率等繁殖成效。睾酮还对个体的免疫活性和个体的存活率等产生影响。目前关于睾酮对鸟类繁殖影响的研究大多是通过外源性植入睾酮的方式来改变个体睾酮的浓度,其研究结果也常出现相互矛盾之处,对于自然状态下影响睾酮水平变化的因素尚缺乏了解,睾酮对雌雄鸟在繁殖过程中的影响也不尽相同,有必要继续深入研究。     

Parental investment and its sensitivity to corticosterone is linked to melanin-based coloration in barn owls

Behavioral and physiological responses to unpredictable changes in environmental conditions are, in part, mediated by glucocorticoids (corticosterone in birds). In polymorphic species, individuals of the same sex and age display different heritable melanin-based color morphs, associated with physiological and reproductive parameters and possibly alternative strategies to cope with variation in environmental conditions. We examined whether the role of corticosterone in resolving the trade-off between self-maintenance and reproductive activities covaries with the size of melanin-based spots displayed on the ventral body side of male barn owls. Administration of corticosterone to simulate physiological stress in males revealed pronounced changes in their food-provisioning rates to nestlings compared to control males. Corticosterone-treated males with small eumelanic spots reduced nestling provisioning rates as compared to controls, and also to a greater degree than did corticosterone-treated males with large spots. Large-spotted males generally exhibited lower parental provisioning and appear insensitive to exogenous corticosterone suggesting that the size of the black spots on the breast feathers predicts the ability to cope with stressful situations. The reduced provisioning rate of corticosterone-treated males caused a temporary reduction in nestling growth rates but, did not affect fledgling success. This suggests that moderately elevated corticosterone levels are not inhibitory to current reproduction but rather trigger behavioral responses to maximize lifetime reproductive success.     

Reproduction in shark-attacked sea turtles is supported by stress-reduction mechanisms

Vertebrates exhibit varied behavioural and physiological tactics to promote reproductive success. We examined mechanisms that could enable female loggerhead turtles to undertake nesting activities and maintain seasonal reproduction despite recent shark injuries of varying severity. We proposed that endocrinal mechanisms that regulate both a turtle's stress response and reproductive ability are modified to promote successful and continued reproduction. Irrespective of the degree of injury, females did not exhibit increased levels of the stress hormone corticosterone, nor decreased levels of the reproductive steroid testosterone; hormone responses consistent with stress. When exposed to a capture stressor, females with shark injury did not exhibit any greater corticosterone response than controls. In addition, breeding females showed a reduced corticosterone stress response compared to non-breeding females. Reduced endocrinal responses following shark injury, and during breeding in general may, in part, enable females to maintain behavioural and physiological commitment to reproduction.     

Influence of breeding on foraging behaviour and diet of Crowned Cranes

Gichuki, N. 2000. Influence of breeding on foraging behaviour and diet of crowned cranes. Ostrich 71 (1 & 2): 74–79.

This study investigated the effects of breeding on the foraging behaviour and diet of Grey Crowned Cranes Balearica regulorum in the Kitale area, western Kenya. During the study period (July 1994 to June 1996), 86 pairs successfully bred in 290 ha of wetlands. Egg-laying extended from July to November, indicating that the timing of nesting was flexible. Breeding and non-breeding adult cranes as well as immature birds foraged in grasslands, crop stubble, sown fields and wetlands. These habitats were not used according to the available proportions. Breeding commitments restricted parental adults to habitats within their territories while non-parental adults and sub-adults exploited a wider range of habitats. Further, breeding adults and juveniles had smaller foraging range sizes than those of non- breeding adults and sub-adults. Reduced foraging ranges by breeding birds appear to be a trade-off between energy expenditure in self-maintenance and reproduction. The diet of breeding and non-breeding adults was generally similar consisting of graminoid seeds and arthropods. Breeding birds, however, increased consumption of protein rich animal food and non-seed plant material. Selectivity of food items was greatest among breeding adults. Overall, breeding commitments resulted in reduced foraging range and variety of food items available but the major components of the diet remained the same for all adults and immature birds.     

Circannual variation in habitat use of the White-winged Snowfinch Montifringilla nivalis nivalis

High mountain areas are subject to strong seasonal fluctuations, and species inhabiting these particular environments show a high degree of habitat specialization to cope with extreme abiotic conditions. Estimates of habitat use are influenced by the spatial and seasonal scales at which they are evaluated, so studies at multiple scales are important in order to explore adaptive responses to seasonal environments. In the present study, we assessed habitat use of the White-winged Snowfinch Montifringilla nivalis subsp. nivalis (henceforth Snowfinch) during breeding and non-breeding seasons at three different spatial scales (diameters of 100, 250 and 500 m). Although Snowfinches clearly used high-elevation habitats in both seasons, there was evidence that they are less specific during the non-breeding period: the variance explained by habitat and topographical factors was lower in winter than in the breeding season. Moreover, our results suggest that the use of habitat is scale-dependent. This pattern was especially relevant in the breeding season, perhaps because habitat use might be more related to nest-site selection and specific foraging sites to provide food for nestlings. Snowfinches use high mountain habitats throughout the year, probably as a consequence of physiological and morphological specializations typical of high-elevation species, but in winter they show a certain flexibility in habitat use. Snowfinches might thus adopt a flexible specialist strategy. This could represent a trade-off to overcome possible effects on survival, condition and fitness, which can be particularly strong in harsh, unpredictable environments.     

哺乳动物季节性繁殖的神经内分泌调节机制

动物的季节性繁殖,是指其繁殖活动从静止到复苏的一个年周期性循环。研究显示,kisspeptin和RFRP对繁殖的季节性变化具有重要作用。非繁殖期最显著的特点是雌激素对GnRH分泌的负反馈效应的增加,而雌激素的这种效应是由kisspeptin神经元传导的。因此,kisspeptin是影响繁殖活动的一个重要因子。RFRP的表达依赖于褪黑激素的分泌并呈现出季节性变化,在非繁殖期对繁殖活动的抑制作用非常明显。此外,甲状腺激素在繁殖期的终止上发挥着至关重要的作用,而多巴胺能神经元A14/A15也促进了雌激素负反馈效应的季节性变化。这些神经元系统通过协同作用一起调节了生殖功能随光周期的季节性转变。文章对繁殖的季节性和这4个神经内分泌系统之间的关系进行了系统的阐述。     

哺乳动物季节性繁殖的神经内分泌调节机制

动物的季节性繁殖, 是指其繁殖活动从静止到复苏的一个年周期性循环。研究显示, kisspeptin和RFRP对繁殖的季节性变化具有重要作用。非繁殖期最显著的特点是雌激素对GnRH分泌的负反馈效应的增加, 而雌激素的这种效应是由kisspeptin神经元传导的。因此, kisspeptin是影响繁殖活动的一个重要因子。RFRP的表达依赖于褪黑激素的分泌并呈现出季节性变化, 在非繁殖期对繁殖活动的抑制作用非常明显。此外, 甲状腺激素在繁殖期的终止上发挥着至关重要的作用, 而多巴胺能神经元A14/A15也促进了雌激素负反馈效应的季节性变化。这些神经元系统通过协同作用一起调节了生殖功能随光周期的季节性转变。文章对繁殖的季节性和这4个神经内分泌系统之间的关系进行了系统的阐述。