Experimental demonstration of a parasite‐induced immune response in wild birds: Darwin's finches and introduced nest flies

Abstract

Ecological immunology aims to explain variation among hosts in the strength and efficacy of immunological defenses. However, a shortcoming has been the failure to link host immune responses to actual parasites under natural conditions. Here, we present one of the first experimental demonstrations of a parasiteinduced immune response in a wild bird population. The recently introduced ectoparasitic nest fly Philornis downsi severely impacts the fitness of Darwin's finches and other land birds in the Gal apagos Islands. An earlier study showed that female medium ground finches (Geospiza fortis) had P. downsi-binding antibodies correlating with presumed variation in fly exposure over time. In the current study, we experimentally manipulated fly abundance to test whether the fly does, in fact, cause changes in antibody levels. We manipulated P. downsi abundance in nests and quantified P. downsi-binding antibody levels of medium ground finch mothers, fathers, and nestlings. We also quantified host behaviors, such as preening, which can integrate with antibody-mediated defenses against ectoparasites. Philornis downsi-binding antibody levels were significantly higher among mothers at parasitized nests, compared to mothers at (fumigated) nonparasitized nests. Mothers with higher antibody levels tended to have fewer parasites in their nests, suggesting that antibodies play a role in defense against parasites. Mothers showed no behavioral changes that would enhance the effectiveness of the immune response. Neither adult males, nor nestlings, had P. downsi-induced immunological or behavioral responses that would enhance defense against flies. None of the parasitized nests fledged any offspring, despite the immune response by mothers. Thus, this study shows that, while the immune response of mothers appeared to be defensive, it was not sufficient to rescue current reproductive fitness. This study further shows the importance of testing the fitness consequences of immune defenses, rather than assuming that such responses increase host fitness.

Experimental test of the effect of introduced hematophagous flies on corticosterone levels of breeding Darwin’s finches

“…P. downsi had a significant negative effect on the reproductive success of birds in this study; see Koop et al (2013) for details. However, neither the body condition nor hematocrit of adult females differed significantly between parasite treatments.…”

“…The simplest explanation is that P. downsi is not a significant stressor for adult female birds. While previous studies suggest that female finches are bitten by P. downsi (Huber et al, 2010; Koop et al, 2013), the frequency with which this occurs is unknown. Our study did not find a significant difference in hematocrit values between females sitting on parasitized and non-parasitized nests.…”

“…P. downsi can cause nests to fail within a week of the eggs hatching (Koop et al, 2013). We therefore sampled adult female birds for blood relatively quickly (within 4–6 days of the eggs hatching).…”

“…When nestlings were 3–6 days old, a mist net was placed in the nest territory to catch the attending adult female. This time period was chosen to minimize sample loss due to the failure of parasitized nests, which often happens less than a week after hatching of the first egg (Koop et al, 2013). Once opened, nets were under constant surveillance.…”

Galápagos mockingbirds tolerate introduced parasites that affect Darwin's finches

“…Adult flies, which are not parasitic, lay their eggs in the nests of finches and other land birds in the Galápagos. In some years, 100% of finch nests fail to produce fledglings due to P. downsi (Koop et al 2011, 2013a, O'Connor et al 2013. Several studies have shown that P. downsi reduces the reproductive success of the medium ground finch (Geospiza fortis) and other species of Darwin's finches (reviewed in Koop et al 2011).…”