Thomas P. Hahn

In search of relationships between the acute adrenocortical response and fitness

The assumption that the acute response to stress is adaptive is pervasive in the literature, but there is little direct evidence regarding potential positive fitness consequences of an acute stress response. If acute glucocorticoid (GC) elevation increases lifetime reproductive success (fitness), in what contexts does this occur, and through what combination of effects on annual reproductive output and interannual survival? Here we examine the framework under which most comparative acute GC studies fall, evaluate the commonalities of those studies in the light of expected fitness effects, and suggest methods to better examine the potentially beneficial effects of the acute GC response for free living animals. An overwhelming majority of papers from this area examine environmental-physiological-social effects on GC reactivity. Fewer evaluate intermediate performance measures (fitness proxies). We could only find 11 that directly examine GC effects on reproductive output and survival. The environment-GC-performance papers suggest that greater GC reactivity favors self-maintenance behavior (survival) at the expense of current reproduction. However, the two studies that directly address GC reactivity and fitness (2 of the 11) find the opposite effect (greater GC reactivity predicts lower annual survival). We suggest that it is time to move past simple evaluation of factors regulating GC secretion. These studies will be much richer and informative if researchers include performance and fitness measures. We especially support incorporating and testing ideas of context dependency, coping strategies, and possible fluctuating selection pressures when considering the fitness benefits of the acute GC response.

Testosterone and territorial behaviour in sedentary and migratory sparrows

Abstract Abstract. Free-living male song sparrows, Melospiza melodia morphna, showed marked aggressive behaviour in response to simulated territorial intrusions throughout most of the year. Only during the prebasic moult, and during inclement winter weather, was territorial aggression suppressed. In contrast, free-living male white-crowned sparrows, Zonotrichia leucophrys pugetensis , showed the highest behavioural responses to simulated territorial intrusions in spring when territories were established. Responses then declined as the breeding season progressed, reaching a minimum during the prebasic moult. The latter species migrates to wintering grounds and does not show territorial aggression until the following spring. Plasma levels of testosterone paralleled changes in territorial aggression in white-crowned sparrows, but not song sparrows. The resurgence of autumnal territoriality was independent of any increase in circulating testosterone levels. Males of both species showed increases in testosterone levels in response to simulated territorial intrusions, but this was only significant in white-crowned sparrows. However, male song sparrows had higher levels of testosterone in spring in areas with a high density of territories than males in areas with a low density of territories. These data suggest that although territorial behaviour in the non-breeding season was independent of testosterone in song sparrows, such behaviour in the breeding season may be influenced by this steroid hormone. Finally, it appears that young, first summer, song sparrows were also able to establish a territory in early autumn with no changes in testosterone or luteinizing hormone.

Integrating stress physiology, environmental change, and behavior in free-living sparrows

As weather deteriorates, breeding animals have a diverse array of options to ensure survival. Because of their mobility, birds can easily abandon territories to seek out benign conditions away from the breeding site. The timing of abandonment, however, may have repercussions for territory size, mate quality, reproductive success, and survival. There is a large body of evidence indicating that the adrenocortical response to stress plays a role in mediating the onset and maintenance of this behavioral switch. Here we develop a model describing the interactions of weather, food availability, body condition, and stress physiology in initiating departure from the breeding site. We tested the model using a population of white-crowned sparrows breeding at high elevation in the Sierra Nevada, where severe weather at the beginning of the breeding season often induces temporary abandonment of breeding territories and facultative altitudinal migration to lower elevation refugia. The data show that (1). during inclement weather, exogenous corticosterone delays return to the breeding site after territory abandonment; (2). during good weather, exogenous corticosterone alone does not induce territory abandonment, but does increase activity range around the breeding site; and (3). the magnitude of the corticosteroid response to stress is inversely related to body condition of the sparrow.

Hormonal, behavioral, and thermoregulatory responses to bacterial lipopolysaccharide in captive and free-living white-crowned sparrows (Zonotrichia leucophrys gambelii).

Exposing vertebrates to pathogenic organisms or inflammatory stimuli, such as bacterial lipopolysaccharide (LPS), activates the immune system and triggers the acute phase response. This response involves fever, alterations in neuroendocrine circuits, such as hypothalamo-pituitary-adrenal (HPA) and -gonadal (HPG) axes, and stereotypical sickness behaviors that include lethargy, anorexia, adipsia, and a disinterest in social activities. We investigated the hormonal, behavioral, and thermoregulatory effects of acute LPS treatment in a seasonally breeding songbird, the white-crowned sparrow (Zonotrichia leucophrys gambelii) using laboratory and field experiments. Captive male and female sparrows were housed on short (8L:16D) or long (20L:4D) day lengths and injected subcutaneously with LPS or saline (control). LPS treatment activated the HPA axis, causing a rapid increase in plasma corticosterone titers over 24 h compared to controls. Suppression of the HPG axis occurred in long-day LPS birds as measured by a decline in luteinizing hormone levels. Instead of a rise in body temperature, LPS-injected birds experienced short-term hypothermia compared to controls. Birds treated with LPS decreased activity and reduced food and water intake, resulting in weight loss. LPS males on long days experienced more weight loss than LPS males on short days, but this seasonal effect was not observed in females. These results paralleled seasonal differences in body condition, suggesting that modulation of the acute phase response is linked to energy reserves. In free-living males, LPS treatment decreased song and several measures of territorial aggression. These studies highlight immune-endocrine-behavior interrelationships that may proximately mediate life-history tradeoffs between reproduction and defense against pathogens.

Effects of temperature on photoperiodically induced reproductive development, circulating plasma luteinizing hormone and thyroid hormones, body mass, fat deposition and molt in mountain white-crowned sparrows, Zonotrichia leucophrys oriantha.

The mountain white-crowned sparrow, Zonotrichia leucophrys oriantha, breeds in subalpine meadows throughout many mountainous regions of western North America. Mathematical analysis of 20 years of egg-laying dates at Tioga Pass, California (3030m elevation) indicated a highly predictable breeding season suggesting that precise environmental cues such as the annual change in day length were important for regulating reproductive function. Additionally, it appeared that there was sufficient yearly variation in the timing of breeding to suggest that other environmental cues may also be important for regulating adjustments in reproductive development and regression. Captive populations of Z. l. oriantha showed strong responses in gonadal development following transfer to longs days (15L 9D) and low temperature (5 degrees C) slowed down photoperiodically induced gonadal growth and subsequent regression, in both males and females. High temperature of 30 degrees C tended to accelerate gonadal development and regression whereas gonadal development was intermediate in a group exposed to 20 degrees C. Prior exposure to these temperature regimes while on short days (9L 15D) had no effect on body mass, fat, or plasma levels of luteinizing hormone (LH) and thyroid hormones. Curiously there was no effect of temperature on photoperiodically induced rises in LH in either sex despite marked effects on gonadal growth. Brood patch development was also enhanced in females exposed to 30 degrees C. Corticosterone levels measured in a subset of plasma samples from this experiment indicated no effect of temperature suggesting that the retarded gonadal development at 5 degrees C was not a result of thermal stress. Although there was a robust effect of photostimulation on thyroid hormone levels in blood of both sexes, temperature treatment had no effect on tri-iodothyronine (T3) concentrations. However, plasma levels of thyroxine (T4) were lower initially at 5 degrees C versus 20 and 30 degrees C treatments. This may be related to the protracted gonadal cycle at 5 degrees C versus the truncated gonadal cycle at 30 degrees C. Molt score, an indication of post-reproductive state and onset of photorefractoriness, was delayed in birds exposed to 5 degrees C. Body mass, and to a lesser extent fat score, tended to be lowest in birds exposed to 5 degrees C compared with those at 20 and 30 degrees C. These results demonstrate that ambient temperature significantly affected photoperiodically induced gonadal development and regression in these birds. The endocrine mechanisms underlying these effects require further study.

Endocrine influences on parental care during a short breeding season: testosterone and male parental care in Lapland longspurs (Calcarius lapponicus)

Abstract In males of socially monogamous birds, plasma testosterone (T) typically declines to low levels during the parental phase. Studies on multiple-brooded species indicate that high T may be incompatible with high-quality paternal care. The length of the breeding season may affect the costs and benefits of high T and its effect on paternal care. We studied the effect of experimentally elevated T on paternal care in a single-brooded species with a short breeding season, the Lapland longspur (Calcarius lapponicus). We monitored T levels and parental behavior in 16 males with subcutaneous T implants, 14 males with empty implants, and 14 unimplanted males. We videotaped nests when nestlings were 2–3 days old and again at 4–5 days. T males with 2- to 3-day-old young visited nests and fed young less often than control males, and the mates of the T males compensated with elevated visits and feedings. However, when nestlings were 4–5 days old, T males visited their nests at normal rates – though feeding movements remained below normal – and T females visited and fed at normal rates. Nestling mass and nest success were similar in both groups. Overall, high T suppresses paternal care in Lapland longspur males. The partial improvement of paternal care when nestlings are older, despite high T, may be related to the short 6-week breeding season of this arctic species, and the consequently reduced benefits of sexual behavior late in the breeding season.

REPRODUCTIVE SEASONALITY IN AN OPPORTUNISTIC BREEDER, THE RED CROSSBILL, LOXIA CURVIROSTRA

Crossbills (genus Loxia) are thought to breed opportunistically whenever food is abundant. If strictly true, this would distinguish them from most temperate zone birds that use photoperiod and supplementary cues (e.g., temperature, food supply) to time changes in reproductive physiology and behavior. I describe patterns of changing repro- ductive physiology in free-living Red Crossbills (Loxia curvirostra) as functions of season and conifer phonology. Nonbreeding spring migrants had elevated plasma luteinizing hor- mone (LH) and began gonadal development prior to finding a summer breeding site. The birds began breeding in July while feeding on maturing seeds of western hemlock (Tsuga heterophylla). Circulating LH declined in August, and gonads regressed completely as molt accelerated in September, although seed availability was at an annual high. Slight gonadal growth occurred after molt in late autumn and early winter, but reproductive maturation and nesting did not occur during winter in this study, possibly because western hemlock cones had shed most of their seeds. Winter/spring breeding (reproductive opportunism) at other locations was inferred from the presence of independent juveniles in early summer. Thus, activation of the reproductive system in summer and termination of breeding during molt in autumn appear to be regular seasonal phenomena in Red Crossbills, as in other temperate zone birds. Their opportunistic capabilities are superimposed on this underlying pattern.

Territoriality and testosterone in an equatorial population of rufous-collared sparrows, Zonotrichia capensis

Territorial aggression, displayed by male vertebrates in a reproductive context, is generally thought to be mediated by testosterone. The challenge hypothesis predicts that in socially monogamous species, territorial challenges should induce an increase in plasma testosterone concentrations, which will enhance aggressive behaviour and territory defence. This hypothesis is based on northern latitude birds and needs to be tested in tropical birds before it can be universally accepted. We tested the challenge hypothesis in an equatorial population of rufous-collared sparrows in Papallacta, Ecuador. This population shows an extended breeding period during which males aggressively guard territories. During the early breeding season, males were challenged with conspecific or heterospecific simulated territorial intrusions (STIs) lasting 10 min. Conspecific-challenged males responded more aggressively than heterospecific-challenged males. However, there was no increase in plasma testosterone in response to the conspecific STI. During the breeding season, males were challenged with conspecific STIs lasting 0, 10 or 30 min. Males behaved aggressively regardless of STI duration, and did not differ in plasma testosterone or luteinizing hormone concentrations. During the breeding season, males were implanted with testosterone-filled or empty silastic tubes and subsequently challenged with a conspecific STI. Testosterone implants significantly raised plasma testosterone concentrations, but testosterone-implanted males were not more aggressive than blank-implanted controls. Combined, these findings suggest that testosterone concentrations above breeding baseline are not related to territorial aggression in this population and therefore do not support the challenge hypothesis.

Temporal Flexibility in Avian Reproduction

In changing environments, birds time reproduction to optimize survival of young (e.g., Wingfield, 1983; Perrins, 1970; Lack, 1968). Selective features of the environment (ultimate factors; Baker, 1938) favor those individuals that breed in reasonably close synchrony with the changes occurring in the environment. These ultimate factors include food availability, weather, competition, predation, or any other feature of the physical or biotic environment that has direct effects on the success of a reproductive attempt. Animals prepare for changes in ultimate factors by responding to proximate factors, or cues, from the environment (Baker, 1938). These cues provide reliable information either in the long or short term about the suitability of the environment for breeding. Proximate cues, then, are the features of the environment that actually influence the physiology, morphology, and behavior of individuals.

Recent advances in behavioral neuroendocrinology: Insights from studies on birds

Ever since investigations in the field of behavioral endocrinology were hatched with experiments on roosters, birds have provided original insights into issues of fundamental importance for all vertebrate groups. Here we focus on more recent advances that continue this tradition, including (1) environmental regulation of neuroendocrine and behavioral systems, (2) steroidogenic enzyme functions that are related to intracrine processes and de novo production of neurosteroids, and (3) hormonal regulation of neuroplasticity. We also review recent findings on the anatomical and functional organization of steroid-sensitive circuits in the basal forebrain and midbrain. A burgeoning body of data now demonstrates that these circuits comprise an evolutionarily conserved network, thus numerous novel insights obtained from birds can be used (in a relatively straightforward manner) to generate predictions for other taxa as well. We close by using birdsong as an example that links these areas together, thereby highlighting the exceptional opportunities that birds offer for integrative studies of behavioral neuroendocrinology and behavioral biology in general.