Claire W. Varian-Ramos

Mercury Reduces Avian Reproductive Success and Imposes Selection: An Experimental Study with Adult- or Lifetime-Exposure in Zebra Finch

Mercury is a global pollutant that biomagnifies in food webs, placing wildlife at risk of reduced reproductive fitness and survival. Songbirds are the most diverse branch of the avian evolutionary tree; many are suffering persistent and serious population declines and we know that songbirds are frequently exposed to mercury pollution. Our objective was to determine the effects of environmentally relevant doses of mercury on reproductive success of songbirds exposed throughout their lives or only as adults. The two modes of exposure simulated philopatric species versus dispersive species, and are particularly relevant because of the heightened mercury-sensitivity of developing nervous systems. We performed a dosing study with dietary methylmercury in a model songbird species, the zebra finch (Taeniopygia guttata), at doses from 0.3 – 2.4 parts per million. Birds were exposed to mercury either as adults only or throughout their lives. All doses of mercury reduced reproductive success, with the lowest dose reducing the number of independent offspring produced in one year by 16% and the highest dose, representing approximately half the lethal dose for this species, causing a 50% reduction. While mercury did not affect clutch size or survivorship, it had the most consistent effect on the proportion of chicks that fledged from the nest, regardless of mode of exposure. Among birds exposed as adults, mercury caused a steep increase in the latency to re-nest after loss of a clutch. Birds exposed for their entire lifetimes, which were necessarily the offspring of dosed parents, had up to 50% lower reproductive success than adult-exposed birds at low doses of methylmercury, but increased reproductive success at high doses, suggesting selection for mercury tolerance at the highest level of exposure. Our results indicate that mercury levels in prey items at contaminated sites pose a significant threat to populations of songbirds through reduced reproductive success.

Embryological staging of the Zebra Finch, Taeniopygia guttata

Zebra Finches (Taeniopygia guttata) are the most commonly used laboratory songbird species, yet their embryological development has been poorly characterized. Most studies to date apply Hamburger and Hamilton stages derived from chicken development; however, significant differences in development between precocial and altricial species suggest that they may not be directly comparable. We provide the first detailed description of embryological development in the Zebra Finch under standard artificial incubation. These descriptions confirm that some of the features used to classify chicken embryos into stages are not applicable in an altricial bird such as the Zebra Finch. This staging protocol will help to standardize future studies of embryological development in the Zebra Finch. J. Morphol. 274:1090–1110, 2013.

Decreased Immune Response in Zebra Finches Exposed to Sublethal Doses of Mercury

Mercury (Hg) is a ubiquitous contaminant with deleterious effects on many wildlife species. Most studies to date have focused on fish-eating birds and mammals because much historical Hg pollution is aquatic. Recently, however, comparable blood-Hg levels have been found in terrestrial insectivorous songbirds. As a result, research is needed to clarify the effects of Hg exposure on songbirds. One fundamental end point that is still poorly understood is the effect of Hg on the songbird immune system. If Hg affects the functioning of the immune system, exposed songbirds may be less able to mount an appropriate immune response against invading pathogens. To gain insight into how Hg affects songbird immune function on a cellular level, a flow cytometric assay was developed to measure lipopolysaccharide-induced B-lymphocyte proliferation in zebra finches (Taeniopygia guttata). This is the first experimental (dosing) study of the potential effect of Hg on songbird immune system functioning. Decreased B cell proliferation was observed after lipopolysaccharide exposure in individuals with greater concentrations of Hg in their blood and tissues. In addition, these individuals had decreased ratios of proliferating-to-resting B cells. This decrease in lymphocyte proliferation in response to an effective mitogen suggests that environmental exposure to sublethal levels of Hg may inhibit or delay B cell proliferation in songbirds, potentially increasing susceptibility to disease and decreasing survivorship.

Lifelong exposure to methylmercury disrupts stress‐induced corticosterone response in zebra finches (Taeniopygia guttata)

Mercury can disrupt the endocrine systems of mammals and fish, but little is known about its effects on avian hormones. The authors employed an experimental manipulation to show that methylmercury suppresses the stress-induced corticosterone response in birds, an effect previously unreported in the literature. Corticosterone regulates many normal metabolic processes, such as the maintenance of proper blood glucose levels during stressful daily fasting; an inability to increase corticosterone levels in response to stressors renders a bird less able to face a wide array of environmental challenges. The authors studied reproductively mature zebra finches that had been exposed to 0.0 µg/g, 0.3 µg/g, 0.6 µg/g, 1.2 µg/g, or 2.4 µg/g (wet wt) dietary methylmercury throughout their life (i.e., from the egg onward). In contrast to some field studies, the present study found no significant change in baseline plasma corticosterone concentrations attributable to chronic methylmercury exposure. However, a comparison between the baseline corticosterone levels and levels after 30 min of handling stress revealed that the ability of birds to mount a stress response was reduced with increasing blood total mercury concentration. These results are consistent with adrenal corticoid disruption caused by chronic mercury exposure and mirror a similar study on free-living nestling songbirds exposed to environmental mercury.

Familial differences in the effects of mercury on reproduction in zebra finches

Ecotoxicologists often implicitly assume that populations are homogenous entities in which all individuals have similar responses to a contaminant. However, genetically variable responses occur within populations. This variation can be visualized using dose-response curves of genetically related groups, similar to the way that evolutionary biologists construct reaction norms. We assessed the variation in reproductive success of full-sibling families of captive zebra finches (Taeniopygia guttata) experimentally exposed to methylmercury. We found significant variation among families in the effects of methylmercury on several reproductive parameters. This variation suggests that there may be strong responses to selection for resistant genotypes in contaminated areas. This has important implications for the evolution of tolerance as well as risk assessment and wildlife conservation efforts on sites with legacy contamination.

Mercury levels of Nelson’s and saltmarsh sparrows at wintering grounds in Virginia, USA

Nelson’s and saltmarsh sparrows (Ammodramus nelsoni and A. caudacutus) have recently been recognized as separate species, and because of their limited distributions and the susceptibility of their wetland habitats to climate change, these two new species are of conservation concern. Both species are known to bioaccumulate mercury at breeding sites in New England, USA where their ranges overlap, with the saltmarsh sparrow reported to have twice the concentration of blood total mercury. In this study we sampled both species on their shared wintering grounds, and documented that mercury exposure is lower than that reported for the breeding range, with saltmarsh sparrow blood mercury 2.6 times higher than in Nelson’s sparrow. Feather mercury, which is incorporated on the breeding grounds, confirmed that saltmarsh sparrows had incorporated 2.3 times more mercury than Nelson’s sparrows during the previous breeding season. A comparison of stable isotopes of nitrogen and carbon suggests that the higher exposure of saltmarsh sparrows may be not due to feeding at a higher trophic level, as previously hypothesized, but rather could be related to a difference in the carbon source at the base of each species’ food chain. This study, along with recently published data from both species on additional breeding and wintering grounds, provides a more complete picture of relative mercury exposure. Saltmarsh sparrows are exposed to mercury levels that warrant concern, with the highest exposure being during the breeding season. Areas set aside for the long-term conservation of this species should be carefully assessed for mercury bioaccumulation.

Female Red-Backed Fairy-Wrens (Malurus Melanocephalus) Do Not Appear to Pay a Cost For High Rates of Promiscuity

ABSTRACT. Males of monogamous species are expected to increase their overall fitness by engaging in extrapair copulations, but the fitness implications of this behavior for females are somewhat less clear. Numerous studies have examined the potential benefits of extrapair mating to females, but the costs of extrapair mating, which may be substantial, are less well studied. Quantifying these costs is critical to understanding the evolution of extrapair mating behavior in females. We examined the costs of extrapair paternity to female Red-backed Fairy-wrens (Malurus melanocephalus) using an 8-year data set that allowed us to examine both short-term and long-term costs. The variability of individual extrapair mating behavior in female Red-backed Fairy-wrens allowed us to compare the parental care, fecundity, and apparent survival of faithful and promiscuous females. We found no effect of the presence of extrapair offspring on the rate at which males provisioned broods. We also found that promiscuous and faithful females did not differ with respect to apparent annual survival and four indices of reproductive success. These findings suggest that there are few or no costs to extrapair mating in females in this population. Low costs, as documented here, may contribute to the evolution of high extrapair paternity rates observed in many species; thus, our results underscore the importance of both costs and benefits in explaining the evolution of extrapair mating behavior in females.

Effect of laying sequence on egg mercury in captive zebra finches: An interpretation considering individual variation

Bird eggs are used widely as noninvasive bioindicators for environmental mercury availability. Previous studies, however, have found varying relationships between laying sequence and egg mercury concentrations. Some studies have reported that the mercury concentration was higher in first-laid eggs or declined across the laying sequence, whereas in other studies mercury concentration was not related to egg order. Approximately 300 eggs (61 clutches) were collected from captive zebra finches dosed throughout their reproductive lives with methylmercury (0.3 μg/g, 0.6 μg/g, 1.2 μg/g, or 2.4 μg/g wet wt in diet); the total mercury concentration (mean ± standard deviation [SD] dry wt basis) of their eggs was 7.03 ± 1.38 μg/g, 14.15 ± 2.52 μg/g, 26.85 ± 5.85 μg/g, and 49.76 ± 10.37 μg/g, respectively (equivalent to fresh wt egg mercury concentrations of 1.24 μg/g, 2.50 μg/g, 4.74 μg/g, and 8.79 μg/g). The authors observed a significant decrease in the mercury concentration of successive eggs when compared with the first egg and notable variation between clutches within treatments. The mercury level of individual females within and among treatments did not alter this relationship. Based on the results, sampling of a single egg in each clutch from any position in the laying sequence is sufficient for purposes of population risk assessment, but it is not recommended as a proxy for individual female exposure or as an estimate of average mercury level within the clutch.

Multiple hypotheses explain variation in extra-pair paternity at different levels in a single bird family

Extra‐pair paternity (EPP), where offspring are sired by a male other than the social male, varies enormously both within and among species. Trying to explain this variation has proved difficult because the majority of the interspecific variation is phylogenetically based. Ideally, variation in EPP should be investigated in closely related species, but clades with sufficient variation are rare. We present a comprehensive multifactorial test to explain variation in EPP among individuals in 20 populations of nine species over 89 years from a single bird family (Maluridae). Females had higher EPP in the presence of more helpers, more neighbours or if paired incestuously. Furthermore, higher EPP occurred in years with many incestuous pairs, populations with many helpers and species with high male density or in which males provide less care. Altogether, these variables accounted for 48% of the total and 89% of the interspecific and interpopulation variation in EPP. These findings indicate why consistent patterns in EPP have been so challenging to detect and suggest that a single predictor is unlikely to account for the enormous variation in EPP across levels of analysis. Nevertheless, it also shows that existing hypotheses can explain the variation in EPP well and that the density of males in particular is a good predictor to explain variation in EPP among species when a large part of the confounding effect of phylogeny is excluded.

Integrative behavioral ecotoxicology: bringing together fields to establish new insight to behavioral ecology, toxicology, and conservation

Abstract The fields of behavioral ecology, conservation science, and environmental toxicology individually aim to protect and manage the conservation of wildlife in response to anthropogenic stressors, including widespread anthropogenic pollution. Although great emphasis in the field of toxicology has been placed on understanding how single pollutants affect survival, a comprehensive, interdisciplinary approach that includes behavioral ecology is essential to address how anthropogenic compounds are a risk for the survival of species and populations in an increasingly polluted world. We provide an integrative framework for behavioral ecotoxicology using Tinbergen’s four postulates (causation and mechanism, development and ontogeny, function and fitness, and evolutionary history and phylogenetic patterns). The aims of this review are: 1) to promote an integrative view and re-define the field of integrative behavioral ecotoxicology; 2) to demonstrate how studying ecotoxicology can promote behavior research; and 3) to identify areas of behavioral ecotoxicology that require further attention to promote the integration and growth of the field.