Maternal androgens in avian brood parasites and their hosts: Responses to parasitism and competition?

In the coevolutionary dynamic of avian brood parasites and their hosts, maternal (or transgenerational) effects have rarely been investigated. We examined the potential role of elevated yolk testosterone in eggs of the principal brood parasite in North America, the brown-headed cowbird, and three of its frequent host species. Elevated maternal androgens in eggs are a common maternal effect observed in many avian species when breeding conditions are unfavorable. These steroids accelerate embryo development, shorten incubation period, increase nestling growth rate, and enhance begging vigor, all traits that can increase the survival of offspring. We hypothesized that elevated maternal androgens in host eggs are a defense against brood parasitism. Our second hypothesis was that elevated maternal androgens in cowbird eggs are a defense against intra-specific competition. For host species, we found that elevated yolk testosterone was correlated with parasitized nests of small species, those whose nest success is most reduced by cowbird parasitism. For cowbirds, we found that elevated yolk testosterone was correlated with eggs in multiply-parasitized nests, which indicate intra-specific competition for nests due to high cowbird density. We propose experimental work to further examine the use of maternal effects by cowbirds and their hosts.

Seasonal variation and correlation between corticosterone and the antioxidant uric acid during stress in the Northern Cardinal (Cardinalis cardinalis).

Glucocorticoids modify metabolism and other physiological processes in order to mount an appropriate response to stress. This stress response is affected by a combination of seasonal changes, life-history events, and environmental factors. Determining seasonal variability and the potential connection between stress hormones and metabolism is fundamental in understanding seasonal physiological changes in animals. Here, we compared an indicator of stress (corticosterone) with an indicator of metabolic activity (uric acid-a non-enzymatic antioxidant and end product of protein metabolism) during capture and restraint in Northern Cardinals (Cardinalis cardinalis) during fall, winter, spring, and summer. Baseline corticosterone, the acute change in corticosterone (Δ10-corticosterone), and integrated corticosterone during capture stress were significantly different among seasons. For all corticosterone measurements birds captured in summer consistently had the lowest values while spring birds were highest. The lower corticosterone stress response in summer may decrease the likelihood of abandonment and thus protect investment in eggs/chicks. Higher glucocorticoid secretion in spring may benefit birds competing for nesting sites. No differences in uric acid levels (baseline, 60 min, and acute change over 60 min- Δ60-uric acid) were found among seasons. While plasma uric acid significantly decreased over an hour in all seasons examined, there were no significant correlations between baseline corticosterone and uric acid, time-60 corticosterone and uric acid, and Δ10-corticosterone and Δ60-uric acid. We conclude that the relationship between corticosterone and metabolism, as measured by uric acid, is indirect, and seasonal variation occurs with corticosterone secretion but not with uric acid, as measured here.

Breeding on the extreme edge: modulation of the adrenocortical response to acute stress in two High Arctic passerines.

Arctic weather in spring is unpredictable and can also be extreme, so Arctic-breeding birds must be flexible in their breeding to deal with such variability. Unpredictability in weather conditions will only intensify with climate change and this in turn could affect reproductive capability of migratory birds. Adjustments to coping strategies are therefore crucial, so here we examined the plasticity of the adrenocorticotropic stress response in two Arctic songbird species-the snow bunting (Plectrophenax nivalis) and Lapland longspur (Calcarius lapponicus)-breeding in northwest Greenland. Across the breeding season, the stress response was strongest at arrival and least robust during molt in male snow buntings. Snow bunting females had higher baseline but similar stress-induced corticosterone levels compared to males. Modification of the stress response was not due to adrenal insensitivity, but likely regulated at the anterior pituitary gland. Compared to independent nestlings and adult snow buntings, parental-dependent chicks had a more robust stress response. For Lapland longspurs, baseline corticosterone was highest at arrival in both male and females, and arriving males displayed a higher stress response compared to arriving females. Comparison of male corticosterone profiles collected at arrival in Greenland (76°N) and Alaska (67-71°N;) reveal that both species have higher stress responses at the more northern location. Flexibility in the stress response may be typical for birds nesting at the leading edges of their range and this ability will become more relevant as global climate change results in major shifts of breeding habitat and phenology for migratory birds.

Fish on Prozac: a simple, noninvasive physiology laboratory investigating the mechanisms of aggressive behavior in Betta splendens.

The neuromodulator serotonin is an important regulator of aggressive behavior in vertebrates. Experimentally increasing synaptic levels of serotonin with fluoxetine, a selective serotonin reuptake inhibitor, has been shown to reliably decrease the expression of aggressive behavior. Here, we describe a method by which fluoxetine can be noninvasively administered to male Betta splendens (an attractive model for the study of aggressive behavior) and describe a simple laboratory exercise that allows students to experimentally investigate the physiological mechanisms of aggressive behavior. We demonstrate that relatively short-term exposure (3 h) of male bettas to as little as 3 microg/ml of fluoxetine-treated aquarium water is sufficient to reduce the expression of specific aggressive behaviors. We emphasize the physiological concepts that can be addressed with this exercise, including the role of the serotonergic system in regulating aggression, and the interplay of environmental contaminants and physiology in regulating the expression of behavior. We also highlight important aspects of experimental design. This exercise can be flexibly altered to accommodate one or several laboratory periods. It is also low cost, is low impact to the animals, and requires minimal preparation time for instructors.

Habituation of adult Magellanic penguins to human visitation as expressed through behavior and corticosterone secretion.

Ecotourism is increasing worldwide; hence, it is important to know how wildlife are affected behaviorally and physiologically by human visitation. We studied the effects of human visitation on the Magellanic Penguins (Spheniscus magellanicus) at Punta Tombo, Argentina, by monitoring changes in defensive head turns and plasma corticosterone (a hormone secreted in response to stress) for penguins with and without a history of tourist visitation. Habituation to human visitation was rapid. In penguins with no previous exposure to tourists, the number of defensive head turns and level of plasma corticosterone decreased significantly within 5 days of one 15-minute visit/day. Penguins living in tourist-visited and undisturbed areas secreted more corticosterone when captured and restrained than penguins visited by a person. Penguins in tourist areas, however did not show as strong a corticosterone response to capture and restraint as did penguins in areas without tourists. This difference was due to a decreased capability of the adrenocortical tissue to secrete corticosterone in tourist-visited birds. Although our data show no direct negative effects of tourism on Magellanic Penguins at Punta Tombo, consequences of a modification of physiological capabilities (e.g., adrenocortical function) may not become apparent until much later in life. The physiological differences between tourist-visited and undisturbed groups of Magellanic Penguins emphasize the importance of monitoring the effects of anthropogenic disturbances on wildlife at multiple levels.

Age and food deprivation affects expression of the glucocorticosteroid stress response in Magellanic penguin (Spheniscus magellanicus) chicks.

We examined how the glucocortical stress response in free-living Magellanic penguin (Spheniscus magellanicus) chicks changes with age and whether adrenocortical function of chicks within a brood varies in relation to food provisioned by adults. Chicks showed little corticosterone response to capture stress shortly after hatching, an intermediate response around 45-d posthatch, and a robust stress response near fledging. However, in response to an adrenocorticotropic hormone (ACTH) challenge, hatchlings were capable of secreting corticosterone at adult-like levels. The larger sibling in broods of two showed a similar gradual stress-response development pattern. In contrast, by day 45, when differences in body condition were well established between siblings, the smaller, food-deprived chicks significantly increased baseline levels of corticosterone but showed normal stress-induced levels. Near fledging, baseline levels had returned to normal, but stress-induced levels were lower than expected. Similar to altricial species, normally developing semialtricial Magellanic penguin chicks do not express a robust corticosterone stress response until near fledging. Chronic stressors such as food deprivation cause corticosterone use to be up-regulated earlier than expected. However, in cases of extended chronic stress, down-regulation may ensue, thus avoiding the negative effects of chronically elevated levels of corticosterone.

A phylogenetically controlled test of hypotheses for behavioral insensitivity to testosterone in birds.

In most male birds that exhibit paternal care, extending the spring testosterone (T) peak throughout the breeding season reduces nestling provisioning. However, in some species, this trade-off between high T and expression of paternal care is absent. For example, during some or all of the nestling period, T did not affect paternal behavior in Male Lapland longspurs (Calcarius lapponicus), chestnut-collared longspurs (Calcarius ornatus), and great tits (Parus major). Two ecological constraints have been hypothesized to drive insensitivity to T after eggs hatch: (1) a short breeding season that limits breeding opportunities, and (2) a need for paternal care to ensure reproductive success. However, because two of the three species that exhibit T insensitivity are closely related, potential phylogenetic confounds limit determination of which, if either, factor constrains some males to T insensitivity. We examined the effects of supplementary T on paternal behavior in the Snow Bunting (Plectrophenax nivalis), a member of the monophyletic Calcarius/Plectrophenax clade. Male Snow Buntings are constrained to a short breeding season, but paternal care is not essential for survival of nestlings. We administered exogenous T during the parental phase to mimic the early spring T peak. T treatment increased song rates and interfered with paternal behavior such that nestlings of T-implanted males grew more slowly than controls. Our data suggest that T insensitivity in this clade is related to relatively recent constraints of the breeding environment (i.e., not simply common ancestry) and that the necessity of paternal care in some species may be a strong selective factor driving behavioral insensitivity to T during the parental phase.

Field endocrinology and conservation biology.

Field endocrinology techniques allow the collection of samples (i.e., blood, urine, feces, tissues) from free-living animals for analysis of hormones, receptors, enzymes, etc. These data reveal mechanisms by which individuals respond to environmental challenges, breed, migrate and regulate all aspects of their life cycles. Field endocrinology techniques can also be used to address many issues in conservation biology. We briefly review past and current ways in which endocrine methods are used to monitor threatened species, identify potential stressors and record responses to environmental disturbance. We then focus on one important aspect of conservation: how free-living populations respond to human disturbance, particularly in relation to ecotourism. Breeding adult Magellanic penguins, Spheniscus magellanicus, appear to habituate well to tourists, and breed in an area where about 70,000 people visit during the season. Baseline levels of corticosterone return to normal after exposure of naïve birds to humans. However, penguin chicks appear to show a heightened adrenocortical response to handling stress in nests exposed to tourists, compared to chicks living in areas isolated from human intrusions. Given that developmental exposure to stress can have profound influences on how individuals cope with stress as adults, this potential effect of tourists on chicks could have long-term consequences. This field endocrine approach identified a stressor not observed through monitoring behavior alone.

The effects of combined aromatase inhibitor and anti-androgen on male territorial aggression in a tropical population of rufous-collared sparrows, Zonotrichia capensis.

Territorial aggression, exhibited by male vertebrates in a reproductive context, is generally thought to be mediated by elevated levels of the gonadal steroid hormone testosterone. Rufous-collared sparrows from Papallacta, Ecuador are only aggressive during the breeding season when plasma testosterone concentrations are elevated. However, previous experiments have determined that during the breeding season testosterone does not increase in response to territorial challenges and testosterone implants do not make males more aggressive. This relationship between testosterone and aggression is different from closely related northern latitude species. We conducted another experiment investigating the role of testosterone in mediating territorial aggression, during the breeding season, in male rufous-collared sparrows. We predicted that blocking the actions of the testosterone would suppress aggression in response to territorial challenges. During the early breeding season males were captured using a simulated territorial intrusion and there was no relationship between time to capture and plasma testosterone, dihydrotestosterone, and corticosterone concentrations. Individual males were then implanted with both the aromatase inhibitor ATD and the anti-androgen Flutamide or empty implants as a control. After one week, birds were challenged with a simulated territorial intrusion and the aggressive responses measured. There were no differences in individual behavioral responses (number of songs, flights, closest approach, or time within 5 m) or overall aggression between the two groups. Androgen levels were elevated, post-implant, in the experimental group suggesting that the treatment was successful by blocking the negative feedback system. We conclude that pharmacologically inhibiting testosterone during the breeding season does not affect territorial aggression in these birds.