Physiological Condition of Juvenile Wading Birds in Relation to Multiple Landscape Stressors in the Florida Everglades: Effects of Hydrology, Prey Availability, and Mercury Bioaccumulation

and Mercury Bioaccumulation. PLoS ONE 9(9): e106447. doi:10.1371/journal. pone.0106447 Physiological Condition of Juvenile Wading Birds in Relation to Multiple Landscape Stressors in the Florida Everglades: Effects of Hydrology, Prey Availability, and Mercury Bioaccumulation Garth Herring 0 Collin A. Eagles-Smith 0 Dale E. Gawlik 0 James M. Beerens 0 Joshua T. Ackerman 0 Chang-Qing Gao, Central South University, China 0 1 United States Geological Survey, Forest and Rangeland Ecosystem Science Center , Corvallis, Oregon , United States of America, 2 Department of Biological Sciences, Florida Atlantic University , Boca Raton , Florida, United States of America, 3 United States Geological Survey, Western Ecological Research Center, Dixon Field Station , Dixon, California , United States of America The physiological condition of juvenile birds can be influenced by multiple ecological stressors, and few studies have concurrently considered the effects of environmental contaminants in combination with ecological attributes that can influence foraging conditions and prey availability. Using three temporally distinct indices of physiological condition, we compared the physiological response of nestling great egrets (Ardea alba) and white ibises (Eudocimus albus) to changing prey availability, hydrology (water depth, recession rate), and mercury exposure in the Florida Everglades. We found that the physiological response of chicks varied between species and among environmental variables. Chick body condition (shortterm index) and fecal corticosterone levels (medium-term) were influenced by wetland water depth, prey availability, region, and age, but not by mercury contamination. However, mercury exposure did influence heat shock protein 70 (HSP70) in egret chicks, indicating a longer-term physiological response to contamination. Our results indicate that the physiological condition of egret and ibis chicks were influenced by several environmental stressors, and the time frame of the effect may depend on the specialized foraging behavior of the adults provisioning the chicks. - Data Availability: The authors confirm that all data underlying the findings are fully available without restriction. All relevant data are within the paper and its Supporting Information files. Funding: Financial or inkind support was provided by the U.S. This work received support from the Fish and Wildlife Service (grant/contract number: 401815G028) and U.S. Geological Survey. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Environmental stressors, such as contaminants, prey availability, and adverse weather, can elicit strong physiological responses from wild birds in order to help them overcome short-term challenges. These responses can be particularly harmful during the early stages of life if the response exceeds physiological norms [13]. Physiological [4] and behavioral [5] responses can manifest throughout the annual cycle by many avian species in order to cope with seasonal environmental stochasticity. Understanding avian responses to multiple environmental stressors, when one of those stressors is an environmental contaminant, is poorly understood, yet this situation is prevalent in many anthropogenically-impacted environments [6,7]. Mercury (Hg) contamination and subsequent bioaccumulation in waterbirds is problematic in wetlands throughout the world. Inorganic Hg is converted into the toxic and bioaccumulative form methylmercury (MeHg) under biogeochemical conditions that are common in wetland ecosystems [6,7]. Once methylated, MeHg biomagnifies as it is transferred through the food chain [810]. Environmentally relevant Hg concentrations in birds have been associated with a suite of impaired physiological and reproductive responses, including altered reproductive hormone levels [11,12], compromised hypothalamic-pituitary-adrenal axis [1315], and reduced reproductive performance [16]. The decline of several species of Everglades wading bird between the 1930s and 2001 has been related to changes in prey availability and alterations to the ecosystems hydrology [1719] and possibly due to Hg exposure [20,21]. Great egrets (Ardea alba; hereafter egret) and white ibis (Eudocimus albus; hereafter ibis) are two of the most common breeding waterbirds in the Everglades, and they exhibit different foraging strategies that influence their exposure to ecological stressors. Ibis are more limited in their use of habitats and available prey than egrets [22]. Specifically, Ibis select highquality foraging patches that they then abandon relatively quickly once prey availability drops, whereas egrets tend to remain at foraging sites even when prey densities are low [22]. Although both species select different foraging habitats [23] nest survival for both species is similarly influenced by hydrological conditions and prey availability [24]. Furthermore, Hg concentrations differ between egrets and ibises in the Florida Everglades [10,2528], which is likely a function of their foraging ecology and prey selection [28]. Herein, we assessed the physiological response of juvenile egrets and ibis to changing prey availability, hydrology (water depth, recession rate), and mercury exposure. We measured physiological biomarkers and body condition for egret and ibis nestlings in two consecutive years that differed greatly in hydrologic conditions, prey availability, and Hg exposure. Additionally, we measured physiological biomarkers of environmental stressors that manifest across a range of different time frames. In particular, we used measures of physiological condition that we expected would represent a temporal continuum of responses relative to the age of wading bird chicks in our study, including a body-condition index (short-time frame; 12 days; [29]), fecal corticosterone metabolites [FCORT] (medium-time frame; 27 days; [30,31]), and heat shock proteins 60 and 70 [HSP60, HSP70] (long-time frame: weeks - .1 month; [28,3234]). Corticosterone (CORT) is a hormone that serves as a signal to modify both behavior and metabolism during a period of acute stress. Corticosterone is released by the hypothalamo-pituitary-adrenal axis into the blood stream when birds experience acute stress, facilitating a rapid response to overcome the stressor [2,35]. Variation in CORT levels in waterbirds have been correlated with a variety of factors including prey availability [31,36], Hg exposure [12,15], and changing hydrological conditions [37]. In contrast, heat shock proteins are highly conserved molecular chaperones that function to maintain optimal cell function and homeostasis [38,39] by being amplified through up-regulation during periods of stress to minimize cell protein damage [40,41]. Elevated heat shock proteins are commonly associated with responses to da (...truncated)