Michaela Hau

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.

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.

A neotropical forest bird can measure the slight changes in tropical photoperiod

Many tropical birds breed seasonally, but it is largely unknown which environmental cues they use to time reproduction. Changes in tropical photoperiod have been regarded as too small to be used as a proximate environmental cue. This hypothesis, however, has never been rigorously tested. Here, we report on experimental evidence that photoperiodic changes characteristic of tropical latitudes stimulate reproductive activity in a neotropical bird from the forest understory. In the central Republic of Panam (9 degrees N), photoperiod varies annually between 12 hours (December) and 13 hours (June). Free–living spotted antbirds (Hylophylax n. naevioides) had regressed gonads in December, but increased gonads ahead of the rainy (the breeding) season in May. Captive spotted antbirds exposed to a ‘long’ photoperiod of 13 hours increased gonadal size eight–fold and song activity six–fold over that of control birds remaining on a simulated ‘short’ photoperiod of 12 hours of daylight. Moreover, even a photoperiod of 12 hours 17 minutes was sufficient to stimulate gonadal growth in photostimulated birds over that of controls. The dramatic changes in gonadal development were not accompanied by similar changes in hormone titres such as luteinizing hormone and testosterone as expected from temperate zone birds. We propose a more general role of the tropical photoperiod in the regulation of seasonal events in tropical organisms, or in temperate zone species migrating to the tropics.

Social instability increases plasma testosterone in a year–round territorial neotropical bird

In many vertebrates, elevated levels of plasma testosterone (T) are important for reproduction and territorial aggression. However, many tropical birds reproduce and defend territories while plasma T–levels are basal. We studied how aggression and T–levels are regulated in male neotropical spotted antbirds, which defend territories year–round in the Panamanian rainforest. Although spotted antbirds reproduce seasonally, T–levels of individual males often remained at baseline (0.2 ng ml−1) throughout the year, even in courting males. On the other hand, T–levels were elevated (maximally to 1.57 ng ml−1) during periods of social instability at any time of the year, even when males had entirely regressed gonads. Experimental territorial intrusions (broadcast of conspecific song) confirmed these observations by showing that T–levels increased after about two hours of playback time. Our data suggest that spotted antbirds avoided the potential costs associated with constantly high plasma T–levels (e.g. increased mortality rates). Contrary to temperate zone birds, spotted antbirds had the potential to react to social challenges with an increase of plasma T year–round. These results are, to our knowledge, presently unique, but may apply to many vertebrate species that inhabit the tropics.

Territorial aggression and hormones during the non-breeding season in a tropical bird

The hormonal control of territorial aggression in male and female vertebrates outside the breeding season is still unresolved. Most vertebrates have regressed gonads when not breeding and do not secrete high levels of sex steroids. However, recent studies implicate estrogens in the regulation of non-breeding territoriality in some bird species. One possible source of steroids during the non-breeding season could be the adrenal glands that are known to produce sex steroid precursors such as dehydroepiandrosterone (DHEA). We studied tropical, year-round territorial spotted antbirds (Hylophylax n. naevioides) and asked (1). whether both males and females are aggressive in the non-breeding season and (2). whether DHEA is detectable in the plasma at that time. We conducted simulated territorial intrusions (STIs) with live decoys to male and female free-living spotted antbirds in central Panama. Non-breeding males and females displayed robust aggressive responses to STIs, and responded more intensely to decoys of their own sex. In both sexes, plasma DHEA concentrations were detectable and higher than levels of testosterone (T) and 17beta-estradiol (E(2)). In males, plasma DHEA concentrations were positively correlated with STI duration. Next, we conducted STIs in captive non-breeding birds. Captive males and females displayed robust aggressive behavior. Plasma DHEA concentrations were detectable in both sexes, whereas T was non-detectable (E(2) was not measured). Plasma DHEA concentrations of males were positively correlated with aggressive vocalizations and appeared to increase with longer STI durations. We conclude that male and female spotted antbirds can produce DHEA during the non-breeding season and DHEA may serve as a precursor of sex steroids for the regulation of year-round territorial behavior in both sexes.

Within seasons and among years: When are corticosterone levels repeatable?

Hormones play a central role in integrating internal and external cues to help mediate life-history decisions as well as changes in behavior and physiology of individuals. Describing the consistency of endocrine traits within and among individuals is an important step for understanding whether hormonal traits are dependable predictors of phenotypes that selection could act upon. However, few long-term field studies have investigated the individual consistency of hormonal traits. Glucocorticoid hormones mediate homeostatic responses to environmental variation as well as stress responses to acute, unpredictable disturbances. We characterized the repeatability of plasma corticosterone concentrations in two species of free-living passerines across multiple years. We found repeatability in baseline corticosterone concentrations in both sexes of great tits (Parus major) and in female tree swallows (Tachycineta bicolor) within the breeding season but no repeatability of this trait among seasons or across years. Stress-induced levels of corticosterone were only assessed in great tits and were not repeatable in either sex. Our data suggest that in line with their function in mediating responses of individuals to longer-term and acute demands, both baseline and stress-induced plasma corticosterone concentrations are rather plastic traits. However, individuals may differ in their degree of trait plasticity and hence in behavioral and physiological responses to a variety of organismal challenges.

Hormonal mechanisms of cooperative behaviour

Research on the diversity, evolution and stability of cooperative behaviour has generated a considerable body of work. As concepts simplify the real world, theoretical solutions are typically also simple. Real behaviour, in contrast, is often much more diverse. Such diversity, which is increasingly acknowledged to help in stabilizing cooperative outcomes, warrants detailed research about the proximate mechanisms underlying decision-making. Our aim here is to focus on the potential role of neuroendocrine mechanisms on the regulation of the expression of cooperative behaviour in vertebrates. We first provide a brief introduction into the neuroendocrine basis of social behaviour. We then evaluate how hormones may influence known cognitive modules that are involved in decision-making processes that may lead to cooperative behaviour. Based on this evaluation, we will discuss specific examples of how hormones may contribute to the variability of cooperative behaviour at three different levels: (i) within an individual; (ii) between individuals and (iii) between species. We hope that these ideas spur increased research on the behavioural endocrinology of cooperation.

REPRODUCTIVE SEASONALITY OF SEVEN NEOTROPICAL PASSERINE SPECIES

Abstract We investigated gonad sizes, nesting patterns, and plasma hormone concentrations of seven Neotropical passerine species in a lowland tropical rainforest (Panama) at 9°N latitude over at least one annual cycle. All species had entirely regressed gonads for several months of the year (October to January), coinciding with the end of heavy rainfall. Gonadal recrudescence started in the dry season between January and March. Nesting began earlier (March) for open-habitat species than for forest-interior species (April), and lasted until August or December, respectively. Species differed widely in maximal relative testes sizes and reproductive hormone concentrations, but both measures were lower than in most temperate-zone species. Although we cannot provide a phylogenetically controlled comparison, polygynous and group-living species appeared to have larger testes than monogamous species, possibly indicating sperm competition. Testosterone concentrations were highest in polygynous species, intermediate in socially monogamous species, and lowest in a group-living species, indicating that testosterone is more influenced by social systems than by gonad cycles. Tropical birds may generally maintain low testosterone concentrations and relatively small gonads to decrease overall energy expenditure compared to temperate-zone relatives. Estacionalidad Reproductiva de Siete Especies Passeriformes Neotropicales Resumen. Investigamos los tamaños de las gónadas, los patrones de nidificación y las concentraciones hormonales plasmáticas de siete especies de aves paserinas Neotropicales en una selva lluviosa tropical de tierras bajas en Panamá (9°N) durante por lo menos un ciclo anual. Todas las especies tenían gónadas enteramente retraídas por varios meses del año (octubre a enero), coincidiendo con el fin del periodo de precipitación lluviosa pesada. El crecimiento gonadal comenzó en la estación seca, entre enero y marzo. La nidificación comenzó primero en las especies de hábitat abierto (marzo) que en las especies de interior de bosque (abril) y duró hasta agosto y diciembre, respectivamente. Las especies difirieron extensamente en los tamaños relativos máximos de las gónadas y en las concentraciones de la hormona reproductiva, aunque ambas medidas fueron menores que para la mayoría de las especies de la zona templada. Aunque no podemos proveer una comparación controlada por filogenia, las especies poliginias y las especies que viven en grupo tenían testículos más grandes que las especies monógamas, lo que posiblemente podría estar indicando competencia espermática. Las concentraciones de testosterona fueron mayores en las especies poliginias, intermedias en las socialmente monógamas, y menores en las especies que viven en grupo, indicando que la testosterona estaría más influenciada por el sistema social que por los ciclos de las gónadas. Las aves tropicales podrían generalmente mantener niveles bajos de testosterona y tamaños relativamente pequeños de gónadas con el fin de disminuir los gastos energéticos totales en comparación a las especies emparentadas de las zonas templadas.

Sexual signal exaggeration affects physiological state in male barn swallows

Summary A prevailing view in sexual selection theory is that costly physiological processes underlie the development, maintenance and expression of sexual signals, and that the costs of these signals enforce their honesty [1,2]. However, this unidirectional view of how physiology governs signal expression is narrow, because many of the putative physiological underpinnings of signals, such as health status, are themselves dynamic [3]. As such, we predicted that physiological parameters should be affected by sexual signal expression. We therefore manipulated a known sexual signal — plumage coloration — in male barn swallows (Hirundo rustica erythrogaster) and measured circulating androgen levels and body mass before and after the manipulation. We found that androgen concentrations increased in color-enhanced males, but decreased in control males, as expected due to typical seasonal androgen declines [4,5]. Color-enhanced males also lost body mass, whereas control males gained weight between successive captures one week apart. These results indicate the existence of feedbacks between an individuals morphological signals and physiology — a finding that is not currently explained by honest signaling theory.

Reproductive State, but Not Testosterone, Reduces Immune Function in Male House Sparrows (Passer domesticus)

The immune system requires energetic and nutritional resources to optimally defend organisms against pathogens and parasites. Because resources are typically limited, immune function may require a trade‐off with other physiologically demanding activities. Here, we examined whether photoperiodically induced seasonal states (breeding, molting, or nonbreeding) affected the cutaneous immune response of captive male house sparrows (Passer domesticus). To assess immune function in these birds, we injected the mitogen phytohemagglutinin (PHA) into the patagium and measured the resulting wing web swelling. Molting and nonbreeding birds had similar immune responses to PHA injection. However, males in a breeding state showed lower immune responses than both molting and nonbreeding birds even though they did not actually breed. We tested whether this decrease in the PHA swelling response in birds in a breeding state was due to elevated plasma concentrations of testosterone (T) by administering T to birds in a nonbreeding state. Contrary to some evidence in the literature, T did not suppress the response to PHA in house sparrows. Our data show that passerine birds show seasonal modulation in immune function, even in benign environmental conditions. However, even though T is often cited as a strong immunosuppressant, it is not fully responsible for this seasonal modulation.