Stephan J. Schoech

Reproductive endocrinology and mechanisms of breeding inhibition in cooperatively breeding Florida Scrub Jays Aphelocoma C. coerulescens)

Although the ecological and evolutionary bases of cooperative breeding have received close scrutiny, few studies have explored the physiological mechanisms responsible for delayed breeding by helpers. We chose the Florida Scrub Jay, Aphelocoma c. coerulescens, to determine whether breeders and nonbreeders have different hormone profiles during the reproductive season. We found that male nonbreeders had significantly lower testosterone levels and higher progesterone levels than did male breeders. Nonbreeder and breeder males had similar plasma levels of corticosterone. Elevated plasma levels of progesterone in nonbreeder males may interfere with the reproductive activity at the behavioral or physiological level. Alternatively, progesterone may enable these nonbreeding males to express parental behavior in the absence of a parent/offspring relationship, but the occurrence of the highest levels of progesterone during nest building and egg laying supports the former interpretation. In females, we found that nonbreeders had significantly lower levels of estradiol and corticosterone than breeders. The low levels of primary sex steroid hormones in male and female nonbreeders may physiologically and behaviorally inhibit reproductive activity and suggest hat these individuals are reproductively incompetent. The absence of high levels of corticosterone in nonbreeders suggests that this reproductive inhibition is not due to glucocorticoid-mediated stress imposed by dominant breeders.

EXOGENOUS TESTOSTERONE AND THE ADRENOCORTICAL RESPONSE IN DARK-EYED JUNCOS

Hormonal manipulations with implants allow examination of the costs and benefits of behaviors and physiologic states mediated by a given hormone. As a part of on- going research into the effects of the steroid hormone testosterone (T) in Dark-eyed Juncos (Junco hyemalis), we measured the corticosterone (B, a steroid hormone secreted by the ad- renal in response to stress ) response to the stress of capture and handling in males treated with T (T-males) and in control males (C-males). Although B may be essential for energy mobilization, chronic or repeated exposure to elevated levels of B can have many negative effects. Because T mediates many behaviors that may increase the likelihood that an indi- vidual will encounter stressors, we predicted that plasma B would rise more rapidly in T- males than in controls. In the first few minutes post-capture, the increase in B levels was significantly higher in T-males than in controls. B levels in samples collected 10, 30, and 60 min post-capture were consistently higher in T-males than in C-males; however, the differ- ence was not statistically significant. Because previous work has shown that T-males reduce their parental contribution, we compared females that were mated to T-males and C-males (hereafter T- and C-females). B levels of T-females increased sharply in the first few minutes post-capture, whereas in C-females they did not; however, the responses were not statisti- cally different. Males had higher initial levels and a greater B-response to stress than females when data were compared irrespective of treatment. Our results suggest that the behaviors or physiological changes induced by T are potentially costly and that such costs may in part be incurred through elevated B. Received 25 November 1997, accepted 5 May 1998. IN MOST NORTH-TEMPERATE BIRDS, circulating levels of testosterone (T) in males are elevated during the sexual phase of the breeding season

Prolactin and helping behaviour in the cooperatively breeding Florida scrub-jay,Aphelocoma c. coerulescens

The relationship between parental and alloparental behaviours and prolactin was examined by measuring plasma levels of prolactin in cooperatively breeding Florida scrub-jays during three breeding seasons. The seasonal trends were similar to those in several other avian species, with low prolactin titres during the pre-nesting phase that steadily increased to a maximum during the incubation and nestling periods. Females had higher prolactin levels than males, and breeders had higher levels than non-breeders. Circulating prolactin in non-breeders was elevated prior to the time when they were exposed to a nest or young, suggesting that high prolactin levels were not a simple response to the stimulus of begging young. To further assess correlations between prolactin and parent-like behaviours, the number of nest visits and the amount of food delivered to focal nests was monitored. Prolactin levels were significantly correlated with the number of visits to the nest, as well as the amount of food delivered to the young. Non-breeders that fed nestlings had higher prolactin titres than non-breeders that did not help, lending further support to the hypothesis that helping behaviours are mediated by prolactin.

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.

The Effect of Exogenous Testosterone on Parental Behavior, Plasma Prolactin, and Prolactin Binding Sites in Dark-Eyed Juncos ☆

Numerous studies have shown that parental behaviors are mediated by prolactin (PRL), while testosterone (T) interferes with their full expression. The limited data available suggest that reduced parental behavior induced by T is not mediated by reduced concentrations of plasma PRL. We hypothesized that T reduces parental behaviors by reducing PRL receptor binding activity at central neural sites that promote the expression of parental behaviors. To test this hypothesis we implanted male dark-eyed juncos (Junco hyemalis) with testosterone-filled or empty implants and measured T and PRL levels, paternal behavior, and specific binding of radio-labeled PRL at selected brain regions that have been implicated in the mediation of parental behaviors. Our findings concurred with previous studies in that T-treated males reduced their parental contributions, had higher levels of T, and had equivalent levels of PRL compared with controls. We found no differences in the capacity to bind 125I-oPRL in three brain regions previously implicated in the mediation of parental care in birds, i.e., the preoptic area, ventromedial nucleus of the hypothalamus, and paraventricular nucleus of the hypothalamus. Thus our findings do not support the hypothesis that T interferes with the expression of parental behavior by reducing PRL receptor binding activity at central sites.

Delayed breeding in the cooperatively breeding Florida scrub-jay ( Aphelocoma coerulescens): inhibition or the absence of stimulation?

Abstract To determine whether fundamental differences exist in the reproductive physiology of breeder and nonbreeder Florida scrub-jays (Aphelocoma coerulescens), we compared plasma levels of testosterone (T) and luteinizing hormone (LH) in males, and estradiol (E2) and LH in females. Although male breeders had higher overall T and larger testes, nonbreeders’ T paralleled that of breeders, and their testes were more than an order of magnitude larger than regressed testes. Breeder and nonbreeder males had equivalent baseline LH, and equivalent changes in LH following a gonadotropin-releasing hormone (cGnRH-I) challenge. The T, LH and GnRH challenge data indicate that nonbreeder males have functional hypothalamo-pituitary-gonadal (HPG) axes. We found no hormonal evidence of inbreeding suppression in males: nonbreeders that did not live with their mothers and those that did had similar T. Male nonbreeders that were exposed to E2-implanted females had higher T than did controls, suggesting that the lack of within-pair stimulation is a key factor in whether an individual delays breeding. Female nonbreeders had E2 titres equal to or higher than breeders and neither basal LH nor LH following GnRH challenge differed by breeding status. Nonbreeders’ ovarian follicles were smaller than breeders’, but were larger than they would be during the non-breeding season. These data suggest that nonbreeders were primed for breeding and were simply waiting for an opportunity or a required stimulus. Female nonbreeders that lived in a territory with an unrelated male breeder had significantly higher E2 than those that remained with their fathers. Similarly, nonbreeders that were captured away from their home territories had elevated E2. However, nonbreeders that lived with their fathers had E2 that was equivalent to breeding females, suggesting that inbreeding avoidance may not be the primary factor leading to delayed breeding in females.

CONTEXT-SPECIFIC RESPONSE OF FLORIDA SCRUB-JAY PAIRS TO NORTHERN MOCKINGBIRD VOCAL MIMICRY

Abstract It is well established that vocal mimicry serves an intraspecific function in birds by increasing repertoire size. On an interspecific level, territorial exclusion of other species by deceptive mimicry may occur if the model (i.e., mimicked) species song is effectively reproduced by the mimicking species. Few studies have effectively demonstrated deceptive mimicry because they did not use the context of the mimics song as a control stimulus. We addressed this shortcoming by using isolated and context-dependent playback stimuli to assess the response of Florida Scrub-Jay (Aphelocoma coerulescens) pairs to Northern Mockingbird (Mimus polyglottos) imitation. Scrub-jay pairs responded more aggressively to isolated scrub-jay weep calls than to playbacks consisting of either isolated imitation calls, imitated calls embedded in mockingbird song, or control mockingbird song. These results fail to support the hypothesis that mimicry deceives the model species. Whether mockingbird imitation of scrub-jays deceives other species requires further investigation. Respuesta Contexto-Específica de Aphelocoma coerulescens a las Vocalizaciones Miméticas de Mimus polyglottos Resumen. Se conoce que el mimetismo vocal en las aves tiene la función de incrementar el repertorio de vocalización a nivel intraespecífico. A nivel interespecífico, la exclusión territorial de una especie por parte de otra por medio del “mimetismo de engaño” puede suceder si el canto de la especie modela (i.e., aquella que es imitada) es emulado con precisión. Pocos estudios han demostrado el uso de “mimetismo de engaño” debido a que no han analizado el contexto en el que occurre la vocalización mimética. En este estudio utilizamos grabaciones de cantos, tanto aislados como dependientes del contexto de la vocalización, para investigar cómo las parejas de Aphelocoma coerulescens responden a las emulaciones de Mimus polyglottos. Las parejas de A. coerulescens respondieron de manera más agresiva al escuchar grabaciones de sus propios gemidos que al escuchar imitaciones a sus llamadas, imitaciones mezcladas con vocalizaciones propias de M. polyglottos, o vocalizaciones exclusivas de M. polyglottos (control). Estos resultados no apoyan la hipótesis del “mimetismo de engaño.” Sin embargo, se desconoce si M. polyglottos engaña a otras especies cuando imita a A. coerulescens.