Pierre Deviche

Corticosterone and corticosteroid binding globulin in birds: Relation to urbanization in a desert city

As cities expand worldwide, understanding how species adapt to novel urban habitats will become increasingly important to conservation. The adrenocortical stress response enables vertebrates to cope with novel environmental challenges to homeostasis. We examined total and estimates of free baseline and stress-induced corticosterone (CORT) concentrations and CORT binding globulin (CBG) levels in five passerine species within and around Phoenix, Arizona. We tested whether baseline and stress-induced CORT patterns differed among species living at varying densities in Phoenix and tested the hypothesis that, for species capable of successfully colonizing cities, individuals living in urban areas have a decreased acute stress response compared to individuals living in native desert. Baseline total CORT levels were generally similar in urban and rural birds. Capture and handling stress typically produced greater total CORT responses in urban birds than in rural birds, although these responses differed as a function of the life history stage (non-breeding, breeding or molt). CBG binding capacity did not change with life history stage or locality. Estimated free CORT concentrations differed less between groups than total CORT concentrations. Urban birds showed less variability in stress responses across life history stages than rural birds. We propose that more predictable resources in the city than in rural areas may decrease the need to vary stress responsiveness across life history stages. The results highlight the species-specific effects of urbanization on stress physiology and the difficulty to predict how urbanization impacts organisms.

Acute stress rapidly decreases plasma testosterone in a free-ranging male songbird: Potential site of action and mechanism

We used a free-ranging, seasonally breeding adult male songbird, the rufous-winged sparrow, Aimophila carpalis, to investigate the effects of acute stress-induced by capture followed by restraint, on the hypothalamo-pituitary-testicular axis. Intra- and interindividual comparisons revealed that males decreased their plasma testosterone (T) by 37-52% in response to acute stress. The decrease occurred within 15 min of capture and persisted for at least another 15 min. Within 15 min, the decrease in plasma T was not associated with a reduction in plasma luteinizing hormone (LH). Thirty minutes after capture and restraint, the decrease in plasma T either was likewise not associated with decreased plasma LH (intraindividual comparison) or concurred with a reduction in plasma LH (interindividual comparison). These observations indicate that effects of stress may have been mediated at the pituitary gland and also directly at the testicular levels. To address this question, we measured the hormonal response to an injection of the glutamate receptor agonist N-methyl-d,l-aspartate (NMA) to stimulate to stimulate the release of gonadotropin-releasing hormone (GnRH) or of GnRH to stimulate the release of LH. Treatment with NMA did not change plasma LH, presumably because the birds were in breeding condition and already secreting GnRH at a maximum rate. Administration of GnRH increased plasma LH equally in birds that were or were not stressed before the treatment. An injection of purified ovine LH (oLH) increased plasma T equally in birds that were or were not acutely stressed before the hormone injection. Thus, the observed acute stress-induced decrease in plasma T was apparently not mediated by decreased responsiveness of the pituitary gland to GnRH or of the testes to LH. Decreased plasma T following stress may involve a direct impairment of the testicular endocrine function.

Effects of Captivity and Body Condition on Plasma Corticosterone, Locomotor Behavior, and Plasma Metabolites in Curve-Billed Thrashers

The acute stress response involves the secretion of catabolic glucocorticoids, such as corticosterone (CORT) in birds, that mobilize intrinsic energy stores primarily through a gluconeogenic pathway involving fat breakdown, thus linking body condition and stress. We measured changes in CORT and gluconeogenic metabolites (triglycerides, free glycerols, glucose) during handling stress in curve-billed thrashers Toxostoma curvirostre from two habitats (urban vs. desert) that may differ in food abundance in the wild, in captivity, and in response to both food restriction and subsequent recovery. Urban thrashers were heavier and secreted more CORT than desert birds in the field, but differences did not persist in captivity. Decreased access to food resulted in decreased body mass and a diminished ability to elevate plasma CORT in response to handling stress. However, the opposite effect was observed as these birds recovered from food restriction. Plasma levels of glucose and triglycerides did not change with stress. Food restriction also increased locomotor activity, which likely further exacerbated energy loss. These observations suggest that body condition and stress differences between urban and desert birds may be related to differences in their relative energetic states, possibly due to food availability. Body condition may affect the extent to which an individual can elevate CORT and use free glycerol as energy during acute stress.

Androgen control of immunocompetence in the male house finch,Carpodacus mexicanus Müller

SUMMARY The immunocompetence handicap (ICH) hypothesis predicts that elevated levels of the gonadal androgen testosterone (T) entail obligatory costs, such as immunosuppression, but evidence supporting this immunosuppressive influence is equivocal. To investigate this question, adult males house finches, Carpodacus mexicanus, were exposed to short days and chronically treated with T-filled (T males; N=10) or empty (C males; N=10) Silastic capsules. Testosterone administration increased plasma T levels and the size of the cloacal protuberance, an androgen-dependent secondary sexual characteristic. To study humoral immunity, finches received injections of sheep red blood cells (SRBC) and we measured circulating concentrations of antibodies to these cells with a hemagglutination test. All males produced antibodies following four SRBC injections at weekly intervals. Antibody titers in T and C males did not differ 5 days after the fourth injection, but were 59% lower in T than C males 2 weeks later. To study cell-mediated immunity, we measured the local inflammatory response to an injection of phytohemaglutinin (PHA). This response in T and C males was similar 1 day after PHA injection, but was 58% less in T than C males 2 days following the injection. Thus, T and C males mounted similar humoral and cell-mediated immune responses, but T treatment compromised maintenance of these responses. The results, demonstrating immunosuppressive effects of elevated T, are consistent with the ICH hypothesis.

Photoperiod-Independent Hypothalamic Regulation of Luteinizing Hormone Secretion in a Free-Living Sonoran Desert Bird, the Rufous-Winged Sparrow (Aimophila carpalis)

We investigated the regulation of luteinizing hormone (LH) in the male Rufous-winged Sparrow,Aimophila carpalis, a resident of the Sonoran desert that breeds after irregular summer rains. Although the testes develop in March due to increasing photoperiod and regress in September due to decreasing photoperiod, LH does not consistently increase in the spring as in other photoperiodic birds. However, throughout the year increased plasma LH is correlated with rainfall. To investigate this rainfall-associated regulation of LH secretion, we quantified immunocytochemical labeling for gonadotropin-releasing hormone I (GnRH-I), proGnRH (the GnRH precursor), and gonadotropin-inhibitory hormone (GnIH) in the hypothalamus of free-living adult males caught before (low LH), and during (high LH) the monsoon rainy season. Compared to pre-monsoon birds, birds caught during the monsoon season had larger immunoreactive GnRH-I (GnRH-I-ir) and proGnRH-ir cell bodies, as well as fewer, less densely labeled proGnRH-ir cell bodies. Birds caught during the monsoon had fewer, less densely labeled GnIH-ir cell bodies than birds caught before the monsoon. Further, there was no GnIH-ir labeling in the median eminence on either capture dates, suggesting that GnIH is not released to the pituitary gland via the portal vein at this time of year, but there were fewer GnIH-ir fibers in the preoptic area of birds caught during the monsoon season. Our data support the hypothesis that environmental factors associated with increased rainfall during the monsoon season stimulate GnRH synthesis and release to increase LH secretion. These data also suggest that GnIH could inhibit GnRH neuronal activity prior to the monsoon season.

Central vasotocin‐immunoreactive system in a male passerine bird (Junco hyemalis)

Previous investigations have identified regions of the avian brain that contain immunoreactive vasotocinergic (VT‐ir) cell bodies and fibers. These studies exclusively used domesticated species, and the relevance of the findings for free‐living birds has not been established. The present study used immunocytochemistry to determine the neuroanatomical distribution of the VT‐ir system in the brain of a well‐studied male passerine bird (dark‐eyed junco, Junco hyemalis) obtained from a natural population in interior Alaska (65°N, 147°W). VT‐ir cell bodies were observed in several brain regions (paraventricular and supraoptic nuclei, nucleus of the stria terminalis), where they have been described in other oscine species. VT‐ir fibers were widespread in many brain regions and were especially abundant in the medial preoptic nucleus, the basal region of the septum, and the hypothalamic–neurohypophyseal tract. Fibers were also present in brain regions that are involved in the control of vocal behavior including the ventromedial capsular region of the nucleus robustus archistriatalis and the dorsomedial portion of the mesencephalic nucleus intercollicularis. The widespread brain distribution of VT‐ir cell bodies and fibers in juncos generally resembles that of domestic birds and suggests a role for this neuropeptide in the control of reproductive behavior and physiology. J. Comp. Neurol. 409:105–117, 1999.

Environmental regulation of the reproductive system in a flexibly breeding Sonoran Desert bird, the Rufous-winged Sparrow, Aimophila carpalis

We investigated reproductive regulation in male Rufous-winged Sparrows, Aimophila carpalis, a Sonoran Desert passerine that breeds after irregular summer rains. Field and captive data demonstrate that increased photoperiod stimulates testicular development in March and maintains it until early September. Free-living birds caught in July and placed on captive long days (16L: 8D) maintained developed testes for up to 7 months, and free-living birds caught in September, during testicular regression, redeveloped testes when placed on captive long days, indicating that these birds were still photosensitive. Captive birds on long days maintained testicular development when exposed to temperatures mimicking those occurring during regression in free-living birds. In free-living birds, testicular development was observed during spring and summer, but unless this was associated with rainfall, breeding (indicated by juveniles) did not occur. Large increases in plasma luteinizing hormone (LH) in free-living males were correlated with heavy rainfall in July/August, when the birds bred, and in November, when they did not breed. In captive birds, plasma LH concentrations were unresponsive to photoperiodic changes, but may have responded to social cues. Plasma prolactin concentrations were directly correlated with photoperiod in free-living birds, but an effect of photoperiod on prolactin secretion was not seen in captive birds. It is concluded that male Rufous-winged Sparrows use long photoperiods to stimulate and maintain testicular development, but exposure to long photoperiods does not terminate breeding by inducing absolute photorefractoriness. The specific timing of reproductive behaviors is apparently determined by elevated plasma LH coinciding with long day stimulated gonad development.

Effects of testosterone and photoperiodic condition on song production and vocal control region volumes in adult male dark-eyed juncos (Junco hyemalis)

In seasonally breeding male oscines, song learning and expression are controlled by brain regions (vocal control regions, VCRs) that exhibit seasonal neural plasticity in adulthood. Several VCRs contain androgen receptors, and gonadal androgens play important roles in the control of seasonal structural and functional changes of VCRs. Recent studies also found that adult VCRs are influenced by factors other than gonadal hormones, including photoperiod, but the relative importance of these factors and their mechanisms of action are poorly understood. To address this issue, we investigated the contributions of photoperiod and testicular androgens to the regulation of VCR volumes and to the control of song expression in adult dark-eyed juncos, Junco hyemalis. Exposing castrated (CX) photosensitive males to long days (LD) enhanced their high vocal center (HVc) volumes compared to those of males held on short days (SD). These volumes were not further increased by concurrent testosterone (T) treatment, revealing a marked and gonadal androgen-independent stimulatory influence of photoperiod on the size of this brain region. HVc sizes were smaller in LD-exposed photorefractory than photosensitive males irrespective of whether birds were intact or had been castrated before photoperiodic manipulations, but HVc sizes increased in response to T treatment in intact photorefractory males. Thus, LD exposure can increase HVc volumes in the absence of gonadal T, but large volume induction in photorefractory males requires elevated plasma T levels. Testosterone treatment of SD-exposed photosensitive males increased HVc, but not Area X, MAN, or RA volumes. Only T-treated males sang and this treatment given to castrates was equally effective behaviorally when administered to photosensitive, photostimulated, or photorefractory juncos. This result indicates that the stimulating influence of LD exposure on HVc volumes is insufficient to induce song in the absence of elevated plasma T levels.

Photoperiod and testosterone independently affect vocal control region volumes in adolescent male songbirds

Previously, we found that, unlike adults, adolescent male dark-eyed juncos (Junco hyemalis) maintained large Area X volumes despite having low plasma testosterone concentrations. Other studies indicate that photoperiod may act independently of testosterone to modulate vocal control region (VCR) volumes in adult songbirds. In the present study, we investigated the effects of testosterone and photoperiod on the volumes of four VCRs in adolescent male juncos. To test the hypothesis that VCR volumes in these males are testosterone independent, we treated birds exposed to short days with testosterone and later compared their VCR volumes with those of birds exposed to short days without testosterone. To examine whether photoperiod alone could affect VCR volumes independent of testosterone, we measured these volumes in photorefractory birds exposed to long photoperiod without testosterone. Administering testosterone induced singing, yet increased the volume of only one VCR, the robust nucleus of the anterior neostriatum (RA). In contrast, long photoperiod increased several VCR volumes (Area X, higher vocal center, and RA) despite low testosterone levels, but did not induce singing. Our results suggest a limited role for testosterone, but an important role for photoperiod, in controlling VCR volumes in adolescent male juncos. In addition, the results demonstrate that singing behavior can be induced in adolescent males without a concomitant increase in most VCR volumes.

INTERSPECIFIC VARIABILITY OF PREVALENCE IN BLOOD PARASITES OF ADULT PASSERINE BIRDS DURING THE BREEDING SEASON IN ALASKA

Blood parasite prevalence based on microscopic examination of stained blood smears was determined in adults of 11 passerine bird species sampled during their breeding season (May and June 1997–98) in interior Alaska (USA). These species included primarily Nearctic migratory species such as the dark-eyed junco (Junco hyemalis) and neotropical migratory species such as the blackpoll warbler (Dendroica striata), alder flycatcher (Empidonax alnorum), Swainsons thrush (Catharus ustulatus), northern waterthrush (Seiurus noveboracensis), and bank swallow (Riparia riparia) as well as one long-distance palearctic migrant, the arctic warbler (Phylloscopus borealis). The more prevalent parasites were Leucocytozoon dubreuili (73% of the sampled turdinids), L. fringillinarum (42% of the sampled fringillids and parulids), and Trypanosoma avium (39% of the sampled hosts). Other parasites (H. fallisi: 18% of the sampled turdinids; Haemoproteus paruli: 14% of the sampled parulids; H. fringillae: 5% of the sampled fringillids; microfilariae: 4% of the sampled hosts) were observed less frequently. Plasmodium vaughani was found only in two yellow warblers (Dendroica petechia). Overall parasite prevalence varied between 0% in the alder flycatcher to >80% in Swainsons thrush, arctic warbler, and Townsends warbler (Dendroica townsendi). Prevalence of various hematozoa also was bird species-dependent. No relationship was observed between prevalence and either foraging (aerial versus trees/shrubs) or nesting habits (ground versus arboreal) or general location of the wintering area of the different species examined. Prevalence also was unrelated to average dates of arrival on breeding grounds and, therefore, to potential duration of exposure to local insect vectors before capture. Differences in blood parasite prevalence among species breeding in a same region and in the same type of habitat may result from differences in host specificity such as immunological resistance to infection or blood meal preference by potential vectors and/or in behavioral adjustments/physiological traits that alter exposure to vectors.