Kristen J. Navara

The dark side of light at night: physiological, epidemiological, and ecological consequences

Abstract:  Organisms must adapt to the temporal characteristics of their surroundings to successfully survive and reproduce. Variation in the daily light cycle, for example, acts through endocrine and neurobiological mechanisms to control several downstream physiological and behavioral processes. Interruptions in normal circadian light cycles and the resulting disruption of normal melatonin rhythms cause widespread disruptive effects involving multiple body systems, the results of which can have serious medical consequences for individuals, as well as large‐scale ecological implications for populations. With the invention of electrical lights about a century ago, the temporal organization of the environment has been drastically altered for many species, including humans. In addition to the incidental exposure to light at night through light pollution, humans also engage in increasing amounts of shift‐work, resulting in repeated and often long‐term circadian disruption. The increasing prevalence of exposure to light at night has significant social, ecological, behavioral, and health consequences that are only now becoming apparent. This review addresses the complicated web of potential behavioral and physiological consequences resulting from exposure to light at night, as well as the large‐scale medical and ecological implications that may result.

Variable Effects of Yolk Androgens on Growth, Survival, and Immunity in Eastern Bluebird Nestlings

Female birds allocate androgens differentially within and among clutches, and it has been suggested that this is a strategy to maximize reproductive success. Only a few studies, however, have examined the effects of yolk testosterone (T) on the growth and development of nestlings, and none have reported on the immunological effects of yolk T nor have they examined several different effects in the same nestlings. To examine the effects of yolk T on nestling eastern bluebirds, we administered two doses of exogenous T to bluebird eggs and measured the growth and immunological responsiveness in the resulting nestlings. We found that yolk T is detrimental to developing embryos, with hatching success decreasing with increasing doses of yolk T. Moderate doses of yolk T stimulated skeletal growth during the embryonic period, while high doses of yolk T resulted in nestlings that weighed more and were more mature at fledging but had a compromised T‐cell immune response to phytohemagglutinin. These data suggest that the alteration of reproductive success through the allocation of yolk T is a complicated phenomenon that involves the integration of several physiological effects.

Evolution of sex-biased maternal effects in birds: III. Adjustment of ovulation order can enable sex-specific allocation of hormones, carotenoids, and vitamins

Overlap in growth of offspring should constrain the opportunity for sex‐biased maternal effects, yet sex‐specific allocation of maternal resources among simultaneously growing ova is often observed in vertebrates. In birds, such allocation can be accomplished either by temporal clustering of ova that become the same sex, resulting in sex‐biased egg‐laying order, or by follicle‐specific delivery of maternal resources. Two house finch populations at the northern and southern boundaries of the species range have opposite ovulation sequences of male and female eggs, and thus, in the absence of sex differences in ova growth or sex‐specific maternal strategies, would be expected to have opposite sex‐specific accumulation of maternal products. We found that the populations had strong and similar gradients of steroid distribution in relation to ovulation order, whereas distribution of carotenoids and vitamins correlated with each follicles accumulation of steroids. In both populations, temporal bias in production of sons and daughters within a clutch enabled strongly sex‐specific acquisition of maternal products, and oocytes of the same sex were highly interdependent in their accumulation of steroids. Moreover, in nests where the sex‐bias in relation to ovulation order deviated from population‐specific patterns, eggs had highly distinct concentrations of steroids, carotenoids and vitamins. These results and previous findings of sex‐specific yolk partitioning among oocytes suggest that oocytes that become males and females are temporally or spatially clustered during their ovarian growth. We discuss the implication of these findings for the evolution of sex‐specific maternal resource allocation.

Yolk Testosterone Stimulates Growth and Immunity in House Finch Chicks

Female birds deposit variable amounts of androgens, such as testosterone, into the yolks of their eggs. Evidence suggests that yolk androgens play an important role in the determination of offspring phenotype. While androgens are generally regarded as anabolic and immunosuppressive, studies of the behavioral and physiological effects of yolk androgens on offspring of several avian species have been conflicting, leaving the adaptive significance associated with deposition patterns of yolk androgens unclear. We injected either a physiological dose of testosterone or a control vehicle into house finch (Carpodacus mexicanus) eggs and examined the effects of these injections on offspring growth and immunity. Two days after hatching, nestlings from eggs treated with testosterone were significantly larger than nestlings from eggs treated with a control injection, suggesting a stimulatory effect of yolk androgens in early development. By 8 d after hatching, however, this effect disappeared, and chicks from the two treatment groups were similar in size. Nestlings in the testosterone treatment group showed a significantly larger swelling response to phytohemagglutinin than control nestlings 15 d after hatching, which is close to fledging. Overall, our observations show that when food resources are abundant, testosterone stimulates both early growth and immunity in developing house finches.

Yolk androgen deposition as a compensatory strategy

The deposition of androgens into the yolks of eggs can have long-lasting effects on the growth and development of young birds. It has been proposed that female birds and reptiles deposit yolk androgens according to the differential allocation hypothesis (DAH), which posits the allocation of more resources to offspring sired by more attractive, higher-quality males. We examined deposition patterns of yolk androgens in relation to mate attractiveness in the house finch Carpodacus mexicanus. Contrary to the predictions of the DAH, female house finches deposited significantly more androgens into eggs sired by less attractive males. We propose that, rather than serving as resources, androgens are used as mediators in a compensatory distribution strategy, enabling females to improve the quality of young produced with less attractive males.

Differential Accumulation and Pigmenting Ability of Dietary Carotenoids in Colorful Finches

Many animals develop bright red, orange, or yellow carotenoid pigmentation that they use to attract mates. Colorful carotenoid pigments are acquired from the diet and are either directly incorporated as integumentary colorants or metabolized into other forms before deposition. Because animals often obtain several different carotenoids from plant and animal food sources, it is possible that these pigments are accumulated at different levels in the body and may play unique roles in shaping the ultimate color expression of individuals. We studied patterns of carotenoid accumulation and integumentary pigmentation in two colorful finch species—the American goldfinch (Carduelis tristis) and the zebra finch (Taeniopygia guttata). Both species acquire two main hydroxycarotenoids, lutein and zeaxanthin, from their seed diet but transform these into a series of metabolites that are used as colorful pigments in the plumage (goldfinches only) and beak (both species). We conducted a series of carotenoid‐supplementation experiments to investigate the relative extent to which lutein and zeaxanthin are accumulated in blood and increase carotenoid coloration in feathers and bare parts. First, we supplemented the diets of both species with either lutein or zeaxanthin and measured plasma pigment status, feather carotenoid concentration (goldfinches only), and integumentary color. Zeaxanthin‐supplemented males grew more colorful feathers and beaks than lutein‐supplemented males, and in goldfinches incorporated a different ratio of carotenoids in feathers (favoring the accumulation of canary xanthophyll B). We also fed goldfinches different concentrations of a standard lutein‐zeaxanthin mix and found that at physiologically normal and high concentrations, birds circulated proportionally more zeaxanthin over lutein than occurred in the diet. Collectively, these results demonstrate that zeaxanthin is preferentially accumulated in the body and serves as a more potent substrate for pigmentation than lutein in these finches.

Roosting ecology and variation in adaptive and innate immune system function in the Brazilian free-tailed bat (Tadarida brasiliensis)

Bats have recently been implicated as reservoirs of important emerging diseases. However, few studies have examined immune responses in bats, and even fewer have evaluated these responses in an ecological context. We examined aspects of both innate and adaptive immune response in adult female Brazilian free-tailed bats (Tadarida brasiliensis) at four maternity roosts (two natural caves and two human-made bridges) in south-central Texas. Immune measurements included in vitro bactericidal ability of whole blood and in vivo T cell mediated response to mitogenic challenge. Bactericidal activity in T. brasiliensis varied with roosting ecology, but appears to be sensitive to colony-level effects. Blood from females living at one cave had significantly lower bactericidal ability than blood from females at three other sites. T cell mediated response in this species was associated with variation in roost ecology, with females from two caves having greater responses than females from two bridges. T cell mediated response and bactericidal activity were negatively correlated with one another within individuals that were tested for both. Variation in immunological response of T. brasiliensis is important for understanding the influence of the environment on the frequency and distribution of immunologically competent individuals and for understanding disease-host dynamics in this and other colonial species.

Yolk Antioxidants Vary with Male Attractiveness and Female Condition in the House Finch (Carpodacus mexicanus)

The manipulation of egg content is one of the few ways by which female birds can alter offspring quality before hatch. Lipid‐soluble vitamins and carotenoids are potent antioxidants. Female birds deposit these antioxidants into eggs in variable amounts according to environmental and social conditions, and the quantities deposited into eggs can have effects on offspring health and immunological condition. Allocation theory posits that females will alter the distribution of resources according to mate quality, sometimes allocating resources according to the differential allocation hypothesis (DAH), investing more in offspring sired by better‐quality males, and other times allocating resources according to a compensatory strategy, enhancing the quality of offspring sired by lower‐quality males. It is unknown, however, whether antioxidants are deposited into eggs according to the DAH or a compensatory strategy. We examined deposition patterns of yolk antioxidants (including vitamin E and three carotenoids) in relation to laying order, mate attractiveness, female condition, and yolk androgen content in the house finch (Carpodacus mexicanus). Female house finches deposited significantly more total antioxidants into eggs sired by less attractive males. Additionally, yolk antioxidant content was significantly positively correlated with female condition, which suggests a cost associated with the deposition of antioxidants into eggs. Finally, concentrations of antioxidants in egg yolks were positively correlated with total yolk androgen content. We suggest that yolk antioxidants are deposited according to a compensatory deposition strategy, enabling females to improve the quality of young produced with less attractive males. Additionally, yolk antioxidants may act to counter some of the detrimental effects associated with high levels of yolk androgens in eggs and, thus, may exert a complementary effect to yolk androgens.