Jennifer C. Owen

SEASONAL DIFFERENCES IN IMMUNOLOGICAL CONDITION OF THREE SPECIES OF THRUSHES

Abstract Migratory birds are exposed to a diverse pathogen fauna by virtue of their long-distance travels. Although the immune system is an organisms primary defense against pathogenic microorganisms, few studies have investigated avian immune function during migration, much less shown seasonal differences in immune function. We describe the immunological condition of three intercontinental migratory species, Swainsons Thrush (Catharus ustulatus), Veery (C. fuscescens), and Wood Thrush (Hylocichla mustelina) during spring migration. In addition, we compare their immunological condition with conspecifics captured during fall migration and during the breeding season to provide a frame of reference for the spring immunological data. Measures of immunological condition presented include total leukocyte count, heterophil:lymphocyte (H:L) ratio, heterophil and lymphocyte counts, hematocrit, and IgG titers. In addition, we assessed each birds energetic condition by measuring body mass and calculating a size-corrected condition index. Migrating birds had lower leukocyte and lymphocyte counts, lower hematocrit, reduced fat stores, and higher H:L ratios relative to nonmigrating individuals sampled during the breeding season. We also found that birds sampled during spring migration had lower lymphocyte counts and reduced fat stores, and higher heterophil counts and H:L ratios than fall migrants. Our results suggest that migrating birds are immunocompromised compared with conspecifics during the breeding season. Furthermore, compared with conspecifics sampled after a shorter overland flight, migrants sampled after crossing the Gulf of Mexico exhibited higher H:L ratios, which is indicative of heightened energetic stress.

Migrating Birds as Dispersal Vehicles for West Nile Virus

Whereas migrating birds have been implicated in the spread of West Nile virus (WNV), there is no direct evidence of birds actively migrating while infectious. The role of birds in WNV dispersal is difficult to assess in the field. However, this role can be evaluated experimentally because birds in migratory disposition display increased locomotor activity or restlessness under captive conditions. We tested the following hypotheses: (1) migrating passerine birds continue to exhibit migratory activity while infectious with WNV and (2) the migratory state of the individual affects the magnitude of viremia. We examined the migratory activity of two neoarctic-neotropical passerine migrants, Swainson’s thrush (Catharus ustulatus) and gray catbird (Dumetella carolinensis), during acute WNV infection. All gray catbirds and six of nine Swainson’s thrushes exhibited migratory activity while infectious. Moreover, migratory status did not appear to influence viremia titers, as might be expected if individuals were immunosuppressed during migration. Therefore, we demonstrate that migrating passerine birds are potential dispersal vehicles for WNV.

HABITAT AND SEX DIFFERENCES IN PHYSIOLOGICAL CONDITION OF BREEDING SOUTHWESTERN WILLOW FLYCATCHERS (EMPIDONAX TRAILLII EXTIMUS)

Abstract The Southwestern Willow Flycatcher (Empidonax traillii extimus; here- after “flycatcher”) is a federally listed endangered species that breeds in densely vegetated riparian habitats dominated by native and exotic plants, including introduced monotypic saltcedar (Tamarix ramosissima). Some workers have theorized that saltcedar is unsuitable habitat for the flycatcher, primarily because it generally supports a smaller and less diverse invertebrate community (the flycatchers food base) than native habitats (e.g. Salix spp.). However, differences in insect communities between native and saltcedar habitats are not proof that saltcedar habitats are inferior. The only way to evaluate whether the habitats differ in dietary or energetic quality is to document actual food limitation or its manifestations. Measurements of an individuals body condition and metabolic state can serve as indicators of environmental stressors, such as food limitation and environmental extremes. We captured 130 flycatchers breeding in native and saltcedar habitats in Arizona and New Mexico and measured 12 variables of physiological condition. These variables included body mass, fat level, body condition index, hematocrit, plasma triglycerides, plasma free fatty acids and glycerol, plasma glucose and beta-hydroxybutyrate, plasma uric acid, total leukocyte count, and heterophil-to-lymphocyte ratio. We found substantial sex-based differences in the condition of male and female flycatchers. Ten of the 12 measures of physiological condition differed significantly between the sexes. In all cases where male and female condition differed (except mass), the differences suggest that males were in poorer condition than females. We found few habitat-based differences in flycatcher condition. Only 3 of the 12 physiological condition indices differed significantly between habitats. Our data show that, at least in some parts of the flycatchers range, there is no evidence that flycatchers breeding in saltcedar habitats exhibit poorer nutritional condition or are suffering negative physiological affects. Diferencias entre Hábitats y Sexos en la Condición Fisiológica de Individuos Reproductivos en Empidonax traillii extimus

Swainson’s thrushes in migratory disposition exhibit reduced immune function

Evidence indicates that the immune system, which protects an organism from parasitic and pathogenic infections, is frequently suppressed when animals are engaged in activities involving strenuous exercise. We tested the hypothesis that birds reduce immune function during the migratory period in preparation for the anticipated heightened energetic demands of long flights. Swainson’s thrushes (Catharus ustulatus), captured in fall, were held in an indoor aviary until January, when migratory disposition was induced in half of the birds with an artificially prolonged daylength. Experimental birds became hyperphagic and deposited fat stores, and then displayed nocturnal activity (Zugunruhe) characteristic of the spring migratory period. Cell-mediated immunity was measured by intradermal injection of phytohemagglutinin in the wing patagium of both control and experimental birds. Birds exhibiting migratory restlessness had a reduced cell-mediated immune response compared to control birds. Our results suggest that birds are immunosuppressed during the migratory period. The suppression may be a nonadaptive response due to unrelated physiological processes, or it may be an adaptive response to the physiological demands associated with migration, such as high energetic demands and the negative consequences of a hyperactive immune system.

Influence of body condition on influenza A virus infection in mallard ducks: experimental infection data.

Migrating waterfowl are implicated in the global spread of influenza A viruses (IAVs), and mallards (Anas platyrhynchos) are considered a particularly important IAV reservoir. Prevalence of IAV infection in waterfowl peaks during autumn pre-migration staging and then declines as birds reach wintering areas. Migration is energetically costly and birds often experience declines in body condition that may suppress immune function. We assessed how body condition affects susceptibility to infection, viral shedding and antibody production in wild-caught and captive-bred juvenile mallards challenged with low pathogenic avian influenza virus (LPAIV) H5N9. Wild mallards (n = 30) were separated into three experimental groups; each manipulated through food availability to a different condition level (−20%, −10%, and normal ±5% original body condition), and captive-bred mallards (n = 10) were maintained at normal condition. We found that wild mallards in normal condition were more susceptible to LPAIV infection, shed higher peak viral loads and shed viral RNA more frequently compared to birds in poor condition. Antibody production did not differ according to condition. We found that wild mallards did not differ from captive-bred mallards in viral intensity and duration of infection, but they did exhibit lower antibody titers and greater variation in viral load. Our findings suggest that reduced body condition negatively influences waterfowl host competence to LPAIV infection. This observation is contradictory to the recently proposed condition-dependent hypothesis, according to which birds in reduced condition would be more susceptible to IAV infection. The mechanisms responsible for reducing host competency among birds in poor condition remain unknown. Our research indicates body condition may influence the maintenance and spread of LPAIV by migrating waterfowl.

The effect of exogenous corticosterone on West Nile virus infection in Northern Cardinals (Cardinalis cardinalis)

The relationship between stress and disease is thought to be unambiguous: chronic stress induces immunosuppression, which likely increases the risk of infection. However, this link has not been firmly established in wild animals, particularly whether stress hormones affect host responses to zoonotic pathogens, which can be transmitted to domesticated animal, wildlife and human populations. Due to the dynamic effects of stress hormones on immune functions, stress hormones may make hosts better or poorer amplifying hosts for a pathogen contingent on context and the host species evaluated. Using an important zoonotic pathogen, West Nile virus (WNV) and a competent host, the Northern Cardinal (Cardinalis cardinalis), we tested the effects of exogenous corticosterone on response to WNV infection. Corticosterone was administered at levels that individuals enduring chronic stressors (i.e., long-term inclement weather, food shortage, anthropogenic pollution) might experience in the wild. Corticosterone greatly impacted mortality: half of the corticosterone-implanted cardinals died between five - 11 days post-inoculation whereas only one of nine empty-implanted (control) birds died. No differences were found in viral titer between corticosterone- and empty-implanted birds. However, cardinals that survived infections had significantly higher average body temperatures during peak infection than individuals that died. In sum, this study indicates that elevated corticosterone could affect the survival of WNV-infected wild birds, suggesting that populations may be disproportionately at-risk to disease in stressful environments.

Arrival timing and hematological parameters in Gray Catbirds (Dumetella carolinensis)

Early arrival at the breeding grounds for migratory birds is associated with greater reproductive success. According to the condition-dependent arrival hypothesis, only those individuals in superior physiological condition are able to bear the costs (e.g., poor environmental conditions, limited food availability) of early arrival. Condition has usually been measured in terms of energy reserves or mass but other physiological measures of condition such as hematocrit and immune function have been gaining attention. We examined several measures of condition and their association with date of first capture in Gray Catbirds (Dumetella carolinensis) arriving at breeding grounds in northeastern Pennsylvania. Earlier arrivals had higher hematocrit and H/L ratios and lower lymphocyte counts. Arrival date was also negatively associated with fat score. Fat score was positively related to hematocrit, total number of leukocytes, and number of lymphocytes, but the other hematological parameters were not associated with traditional measures of condition (keel score, fat score, or a body condition index). Our results provide some support for the condition-dependent arrival hypothesis and suggest that there may be immunological differences between early- and late-arriving birds.

Short-chain carboxylic acids from gray catbird (Dumetella carolinensis) uropygial secretions vary with testosterone levels and photoperiod

The uropygial gland of birds produces secretions that are important in maintaining the health and structural integrity of feathers. Non-volatile components of uropygial secretions are believed to serve a number of functions including waterproofing and conditioning the feathers. Volatile components have been characterized in fewer species, but are particularly interesting because of their potential importance in olfactory interactions within and across species. We used solid-phase microextraction headspace sampling with gas chromatography-mass spectrometry to detect and identify volatiles in uropygial secretions of gray catbirds (Dumetella carolinensis), a North American migratory bird. We consistently detected the following carboxylic acids: acetic, propanoic, 2-methylpropanoic, butanoic, and 3-methylbutanoic. We tested for the effect of lengthened photoperiod and/or exogenous testosterone on volatile signal strength and found a negative effect of lengthened photoperiod on the signal strength of propanoic, 2-methylpropanoic, and butanoic acids, suggesting a trade-off between their production and heightened night-time activity associated with lengthened photoperiod. Signal strength of propanoic and 2-methylpropanoic acids was lower in birds treated with exogenous testosterone than in birds treated with placebos. Sex did not affect signal strength of any of the volatile compounds.

Test of Recrudescence Hypothesis for Overwintering of West Nile Virus in Gray Catbirds

ABSTRACT West Nile virus is a pathogen of concern for both human and wildlife health, Although many aspects of the ecology of West Nile virus are well understood, the mechanisms by which this and similar mosquito-borne viruses overwinter and become reinitiated each spring in temperate regions is not known. A thorough understanding of this mechanism is crucial to risk assessment and development of control strategies. One of the hypotheses to explain the mechanism by which this virus persists from year to year is the spring recrudescence of latent virus in avian reservoir hosts. Stress-related immunosuppression is implicated in the recrudescence of latent viruses in birds. We tested the spring recrudescence hypothesis in a controlled laboratory experiment using hatching-year gray catbirds (Dumatella carolinensis) captured in northern Ohio (July–August 2006), Catbirds (n = 60) were experimentally infected (September 2006) and later examined for the effects of immuno-suppression through exogenous hormones and artificially induced migratory disposition, We found no effect of either testosterone or migratory behavior on infection status in any of the treatment birds. Moreover, we detected no viral RNA in the kidney, spleen, brain, or liver upon necropsy at 24 wk postinfection.

Mathematical modeling of viral zoonoses in wildlife

abstract Zoonoses are a worldwide public health concern, accounting for approximately 75% of human infectious diseases. In addition, zoonoses adversely affect agricultural production and wildlife. We review some mathematical models developed for the study of viral zoonoses in wildlife and identify areas where further modeling efforts are needed.