Dana M. Hawley

Compromised immune competence in free-living tree swallows exposed to mercury

Mercury is a pervasive environmental contaminant and a well-documented immunosuppressor. However, little is known about the effects of mercury contamination on health of free-living vertebrate populations. The South River in Virginia, USA was heavily contaminated with industrial mercury from 1929 to 1950, and recent studies have documented high levels of circulating mercury in riparian songbirds breeding below the site of contamination. Here we used two standardized immune assays, mitogen-induced swelling in response to phytohaemagglutinin (PHA) and antibody response to sheep red blood cells (SRBCs), to test for effects of mercury toxicity on the immune system of female tree swallows (Tachycineta bicolor) which feed on terrestrial and aquatic insects along the contaminated waterway. We found that females breeding at mercury-contaminated sites mounted significantly weaker PHA-induced swelling responses than those at reference sites in both years of study. However, among females on the contaminated sites, individual bloodstream mercury concentration did not predict the extent of mitogen-induced swelling. We did not detect any differences between reference and contaminated females in the strength of antibody responses to SRBCs, but sample sizes for this assay were significantly smaller. Overall, our results suggest that mercury toxicity can exert sub-lethal immunosuppression in free-living, insectivorous songbirds. The potential fitness consequences of the detected differences in immunocompetence caused by mercury toxicity warrant further study.

Experimental evidence for transmission of Mycoplasma gallisepticum in house finches by fomites.

Ever since Mycoplasma gallisepticum emerged among house finches in North America, it has been suggested that bird aggregations at feeders are an important cause of the epidemic of mycoplasmal conjunctivitis because diseased birds could deposit droplets of pathogen onto the feeders and thereby promote indirect transmission by fomites. In this paper we bring the first experimental evidence that such transmission (bird-to-feeder-to-bird) does actually take place. House finches infected via this route, however, developed only mild disease and recovered much more rapidly than birds infected from the same source birds but directly into the conjunctiva. While it is certainly probable that house finch aggregations at artificial feeders enhance pathogen transmission, to some degree transmission of M. gallisepticum by fomites may serve to immunize birds against developing more severe infections. Some such birds develop M. gallisepticum antibodies, providing indication of an immune response, although no direct evidence of protection.

House Finch Populations Differ in Early Inflammatory Signaling and Pathogen Tolerance at the Peak of Mycoplasma gallisepticum Infection

Host individuals and populations often vary in their responses to infection, with direct consequences for pathogen spread and evolution. While considerable work has focused on the mechanisms underlying differences in resistance—the ability to kill pathogens—we know little about the mechanisms underlying tolerance—the ability to minimize fitness losses per unit pathogen. Here, we examine patterns and mechanisms of tolerance between two populations of house finches (Haemorhous [formerly Carpodacus] mexicanus) with different histories with the bacterial pathogen Mycoplasma gallisepticum (MG). After infection in a common environment, we assessed two metrics of pathology, mass loss and eye lesion severity, as proxies for fitness. We calculated tolerance using two methods, one based on pathology and pathogen load at the peak of infection (point tolerance) and the other based on the integrals of these metrics over time (range tolerance). Alabama birds, which have a significantly longer history of exposure to MG, showed more pronounced point tolerance than Arizona birds, while range tolerance did not differ between populations. Alabama birds also displayed lower inflammatory cytokine signaling and lower fever early in infection. These results suggest that differences in inflammatory processes, which can significantly damage host tissues, may contribute to variation in tolerance among house finch individuals and populations. Such variation can affect pathogen spread and evolution in ways not predictable by resistance alone and sheds light on the costs and benefits of inflammation in wild animals.

Incubation temperature affects multiple measures of immunocompetence in young wood ducks (Aix Sponsa)

Parental effects play a vital role in shaping offspring phenotype. In birds, incubation behaviour is a critical parental effect because it influences the early developmental environment and can therefore have lifelong consequences for offspring phenotype. Recent studies that manipulated incubation temperature found effects on hatchling body composition, condition and growth, suggesting that incubation temperature could also affect energetically costly physiological processes of young birds that are important to survival (e.g. immune responses). We artificially incubated wood duck (Aix sponsa) eggs at three biologically relevant temperatures. Following incubation, we used two immunoassays to measure acquired immune responses of ducklings. Ducklings incubated at the lowest temperature had reduced growth, body condition and responses to both of our immune challenges, compared with those from the higher temperatures. Our results show that incubation temperatures can be an important driver of phenotypic variation in avian populations.

Parallel Patterns of Increased Virulence in a Recently Emerged Wildlife Pathogen

A bacterial pathogen of wild songbirds evolved higher virulence following its emergence in two separate regions of the host range.

Feeder use predicts both acquisition and transmission of a contagious pathogen in a North American songbird

Individual heterogeneity can influence the dynamics of infectious diseases in wildlife and humans alike. Thus, recent work has sought to identify behavioural characteristics that contribute disproportionately to individual variation in pathogen acquisition (super-receiving) or transmission (super-spreading). However, it remains unknown whether the same behaviours enhance both acquisition and transmission, a scenario likely to result in explosive epidemics. Here, we examined this possibility in an ecologically relevant host–pathogen system: house finches and their bacterial pathogen, Mycoplasma gallisepticum, which causes severe conjunctivitis. We examined behaviours likely to influence disease acquisition (feeder use, aggression, social network affiliations) in an observational field study, finding that the time an individual spends on bird feeders best predicted the risk of conjunctivitis. To test whether this behaviour also influences the likelihood of transmitting M. gallisepticum, we experimentally inoculated individuals based on feeding behaviour and tracked epidemics within captive flocks. As predicted, transmission was fastest when birds that spent the most time on feeders initiated the epidemic. Our results suggest that the same behaviour underlies both pathogen acquisition and transmission in this system and potentially others. Identifying individuals that exhibit such behaviours is critical for disease management.

Sickness behaviour acting as an evolutionary trap? Male house finches preferentially feed near diseased conspecifics.

Host behaviour towards infectious conspecifics is a crucial yet overlooked component of pathogen dynamics. Selection is expected to favour individuals who can recognize and avoid infected conspecifics in order to reduce their own risk of infection. However, evidence is scarce and limited to species employing chemical cues. Here, we experimentally examine whether healthy captive house finches (Carpodacus mexicanus) preferentially forage near a same-sex, healthy conspecific versus one infected with the directly transmissible pathogen Mycoplasma gallisepticum (MG), which causes lethargy and visible conjunctivitis. Interestingly, male house finches strongly preferred feeding near diseased conspecifics, while females showed no preference. This sex difference appeared to be the result of lower aggression rates in diseased males, but not in females. The reduced aggression of diseased males may act as an ‘evolutionary trap’ by presenting a historically beneficial behavioural cue in the context of a new environment, which now includes a recently emerged, potentially fatal pathogen. Since MG can be directly transmitted during feeding, healthy males may inadvertently increase their risk of contracting MG. This behaviour is likely to significantly contribute to the continued persistence of MG epidemics in wild populations.

Characterization of Experimental Mycoplasma gallisepticum Infection in Captive House Finch Flocks

Abstract The use of controlled, horizontal-transmission experiments provides detailed information on the spread of disease within fixed social groups, which informs our understanding of disease dynamics both in an empirical and theoretical context. For that reason, we characterized in 2002, horizontal transmission of Mycoplasma gallisepticum (MG) in two flocks of 11 wild-caught house finches housed in outdoor aviaries over a 6-mo period. All birds were initially free of MG by a polymerase chain reaction (PCR)-based test, rapid plate agglutination (RPA), and the scoring of physical signs. We inoculated one flock member bilaterally in the palpebral conjunctiva and reintroduced it into its cage. Index birds developed conjunctivitis within 3 to 5 days but died 13 and 20 days postinfection (PI) possibly because of very severe weather. The proportion of birds with physical signs increased gradually, reached 40% at 6 wk PI, and fluctuated around 40% until 21 wk PI. By the time our experiment ended at 24.5 wk PI, 28% of the birds still exhibited physical signs. Across both flocks, 80% of the birds developed unilateral or bilateral conjunctivitis, and several birds relapsed. The appearance of physical signs in new individuals occurred between 10 and 144 days PI (median 41 days PI). Physical signs lasted 1–172 days (median 42 days). Birds that became infected earlier during the experiment developed more severe conjunctivitis, and there was a tendency for birds that developed bilateral conjunctivitis to develop physical signs earlier. Most birds that developed physical signs of MG were also PCR- and RPA-positive, although we detected a single asymptomatic carrier and a single symptomatic false negative. No birds died as a result of secondary MG infection.

PTILOCHRONOLOGY REVEALS DIFFERENCES IN CONDITION OF CAPTIVE WHITE-THROATED SPARROWS

Abstract Ptilochronology is a technique in which the growth rate of a feather is used as an assay of a birds condition. Two important questions remain regarding this decade-old technique: (1) Does the daily rate of feather growth correspond very closely with changes in nutritional status during feather growth? and (2) For which stressors can ptilochronology be used as a reliable assay? Using an experimental manipulation of diet, we tested the effectiveness of ptilochronology for assessing nutritional condition in male White-throated Sparrows (Zonotrichia albicollis). Our hypothesis was that birds given an ample diet would be in better condition than those given a subsistence diet, as indicated by faster feather growth. In a second experiment, we examined the effect of a stressor, low social status, on feather growth. We expected that dominant birds would be in better condition and regrow feathers faster than subordinates because of their priority of access to food. Birds fed an enriched diet weighed more, grew longer feathers, and had wider growth bars than birds receiving a diet lower in protein and calories. Dominants retained more fat than subordinates, but did not grow significantly longer feathers or wider growth bars. However, within flocks, the differences in social status between the birds corresponded to differences in growth-bar width. Our results support the validity of ptilochronology for directly detecting differences in nutritional status during feather regrowth, and point to a likely influence of social status, a density-dependent ecological stressor, on feather growth rates. La Ptilocronología Revela Diferencias en la Condición de Individuos de Zonotrichia albicollis en Cautiverio Resumen. La ptilocronología es una técnica en la que la tasa de crecimiento de una pluma se utiliza para examinar la condición física de un ave. Dos preguntas sobre esta técnica desarrollada hace una década permanecen abiertas. Primero, ¿está la tasa diaria de crecimiento de las plumas relacionada estrechamente con cambios en el estatus nutricional de las aves durante el crecimiento de las plumas? Segundo, ¿para cuáles agentes causantes de estrés puede usarse la ptilocronología como un examinador confiable? Mediante una manipulación experimental de la dieta, pusimos a prueba la efectividad de la ptilocronología para determinar la condición nutricional de machos de Zonotrichia albicollis. Nuestra hipótesis era que aves con una dieta rica estarían en mejor condición que aves con una dieta de subsistencia, lo que sería indicado por un crecimiento más rápido de las plumas. En un segundo experimento, evaluamos el efecto de un factor de estrés (bajo estatus social) en el crecimiento de las plumas. Esperábamos que las aves dominantes estuvieran en mejor condición y que sus plumas crecieran más rápidamente que las de aves subordinadas debido a su acceso prioritario al alimento. Las aves con dieta rica pesaron más, desarrollaron plumas más largas y tuvieron barras de crecimiento más amplias que las aves que recibieron una dieta con menor contenido de proteínas y calorías. Las aves dominantes retuvieron más grasa que las subordinadas pero no desarrollaron plumas significativamente más largas ni barras de crecimiento más amplias. Sin embargo, al interior de bandadas, las diferencias en estatus social entre las aves se reflejaron en diferencias en la amplitud de las barras de crecimiento. Nuestros resultados apoyan la validez de la ptilocronología para detectar diferencias en estatus nutricional durante el período de crecimiento de las plumas directamente y apuntan a una probable influencia del estatus social (un factor ecológico denso-dependiente causante de estrés) sobre las tasas de crecimiento de las plumas.

Common garden experiment reveals pathogen isolate but no host genetic diversity effect on the dynamics of an emerging wildlife disease

Host genetic diversity can mediate pathogen resistance within and among populations. Here we test whether the lower prevalence of Mycoplasmal conjunctivitis in native North American house finch populations results from greater resistance to the causative agent, Mycoplasma gallisepticum (MG), than introduced, recently‐bottlenecked populations that lack genetic diversity. In a common garden experiment, we challenged wild‐caught western (native) and eastern (introduced) North American finches with a representative eastern or western MG isolate. Although introduced finches in our study had lower neutral genetic diversity than native finches, we found no support for a population‐level genetic diversity effect on host resistance. Instead we detected strong support for isolate differences: the MG isolate circulating in western house finch populations produced lower virulence, but higher pathogen loads, in both native and introduced hosts. Our results indicate that contemporary differences in host genetic diversity likely do not explain the lower conjunctivitis prevalence in native house finches, but isolate‐level differences in virulence may play an important role.