Analysis of movement recursions to detect reproductive events and estimate their fate in central place foragers.

BACKGROUND: Recursive movement patterns have been used to detect behavioral structure within individual movement trajectories in the context of foraging ecology, home-ranging behavior, and predator avoidance. Some animals exhibit movement recursions to locations that are tied to reproductive functions, including nests and dens; while existing literature recognizes that, no method is currently available to explicitly target different types of revisited locations. Moreover, the temporal persistence of recursive movements to a breeding location can carry information regarding the fate of breeding attempts, but it has never been used as a metric to quantify recursive movement patterns. Here, we introduce a method to locate breeding attempts and estimate their fate from GPS-tracking data of central place foragers. We tested the performance of our method in three bird species differing in breeding ecology (wood stork (Mycteria americana), lesser kestrel (Falco naumanni), Mediterranean gull (Ichthyaetus melanocephalus)) and implemented it in the R package 'nestR'. METHODS: We identified breeding sites based on the analysis of recursive movements within individual tracks. Using trajectories with known breeding attempts, we estimated a set of species-specific criteria for the identification of nest sites, which we further validated using non-reproductive individuals as controls. We then estimated individual nest survival as a binary measure of reproductive fate (success, corresponding to fledging of at least one chick, or failure) from nest-site revisitation histories during breeding attempts, using a Bayesian hierarchical modeling approach that accounted for temporally variable revisitation patterns, probability of visit detection, and missing data. RESULTS: Across the three species, positive predictive value of the nest-site detection algorithm varied between 87 and 100% and sensitivity between 88 and 92%, and we correctly estimated the fate of 86-100% breeding attempts. CONCLUSIONS: By providing a method to formally distinguish among revisited locations that serve different ecological functions and introducing a probabilistic framework to quantify temporal persistence of movement recursions, we demonstrated how the analysis of recursive movement patterns can be applied to estimate reproduction in central place foragers. Beyond avian species, the principles of our method can be applied to other central place foraging breeders such as denning mammals. Our method estimates a component of individual fitness from movement data and will help bridge the gap between movement behavior, environmental factors, and their fitness consequences.

Mercury bioaccumulation in tropical bats from a region of active artisanal and small-scale gold mining.

Mercury negatively affects human and animal health. Artisanal and small-scale gold mining can be a major local source of mercury contamination, especially into aquatic systems in tropical areas. Animals associated with mercury-contaminated aquatic systems are at high risk of experiencing effects of this heavy metal, but it is not clear how far the effects may extend into nearby terrestrial systems. We report mercury contamination levels in bats in agricultural areas at increasing distances from gold mining (~3-89 km of distance). We hypothesized that bat mercury concentrations would differ between feeding guilds, land use types, and be higher at sites closer to gold mining areas. We collected 112 fur samples from 30 bat species and eight guilds, and provide the first reports of concentrations in 12 species. All mercury concentrations were below the level at which health is likely to be affected (10 ppm). We found guild-influenced differences among mercury concentration levels, with the highest concentrations in aerial insectivores and carnivores, and the lowest in canopy frugivores. Our results suggest insectivorous and carnivorous bats may still be at some risk even at sites distant from aquatic mercury contamination. We did not find an effect of agricultural land-use type on mercury concentrations within species or guilds, suggesting mercury contamination did not extend to agricultural sites from areas of gold mining activities, and that these agricultural activities themselves were not an important source of mercury. We conclude bats did not demonstrate a signature of mercury risk either as a result of proximity of gold mining, or as a result of agricultural activities.

Environmental DNA sampling reveals high occupancy rates of invasive Burmese pythons at wading bird breeding aggregations in the central Everglades.

The Burmese python (Python bivittatus) is now established as a breeding population throughout south Florida, USA. However, the extent of the invasion, and the ecological impacts of this novel apex predator on animal communities are incompletely known, in large part because Burmese pythons (hereafter "pythons") are extremely cryptic and there has been no efficient way to detect them. Pythons are recently confirmed nest predators of long-legged wading bird breeding colonies (orders Ciconiiformes and Pelecaniformes). Pythons can consume large quantities of prey and may not be recognized as predators by wading birds, therefore they could be a particular threat to colonies. To quantify python occupancy rates at tree islands where wading birds breed, we utilized environmental DNA (eDNA) analysis-a genetic tool which detects shed DNA in water samples and provides high detection probabilities. We fitted multi-scale Bayesian occupancy models to test the prediction that pythons occupy islands with wading bird colonies at higher rates compared to representative control islands containing no breeding birds. Our results suggest that pythons are widely distributed across the central Everglades in proximity to active wading bird colonies. In support of our prediction that pythons are attracted to colonies, site-level python eDNA occupancy rates were higher at wading bird colonies (ψ = 0.88, 95% credible interval [0.59-1.00]) than at the control islands (ψ = 0.42 [0.16-0.80]) in April through June (n = 15 colony-control pairs). We found our water temperature proxy (time of day) to be informative of detection probability, in accordance with other studies demonstrating an effect of temperature on eDNA degradation in occupied samples. Individual sample concentrations ranged from 0.26 to 38.29 copies/µL and we generally detected higher concentrations of python eDNA in colony sites. Continued monitoring of wading bird colonies is warranted to determine the effect pythons are having on populations and investigate putative management activities.

Presence of Breeding Birds Improves Body Condition for a Crocodilian Nest Protector.

Ecological associations where one species enhances habitat for another nearby species (facilitations) shape fundamental community dynamics and can promote niche expansion, thereby influencing how and where species persist and coexist. For the many breeding birds facing high nest-predation pressure, enemy-free space can be gained by nesting near more formidable animals for physical protection. While the benefits to protected species seem well documented, very few studies have explored whether and how protector species are affected by nest protection associations. Long-legged wading birds (Pelecaniformes and Ciconiiformes) actively choose nesting sites above resident American alligators (Alligator mississippiensis), apparently to take advantage of the protection from mammalian nest predators that alligator presence offers. Previous research has shown that wading bird nesting colonies could provide substantial food for alligators in the form of dropped chicks. We compared alligator body condition in similar habitat with and without wading bird nesting colonies present. Alligator morphometric body condition indices were significantly higher in colony than in non-colony locations, an effect that was statistically independent of a range of environmental variables. Since colonially nesting birds and crocodilians co-occur in many tropical and subtropical wetlands, our results highlight a potentially widespread keystone process between two ecologically important species-groups. These findings suggest the interaction is highly beneficial for both groups of actors, and illustrate how selective pressures may have acted to form and reinforce a strongly positive ecological interaction.

Wading bird guano enrichment of soil nutrients in tree islands of the Florida Everglades.

Differential distribution of nutrients within an ecosystem can offer insight of ecological and physical processes that are otherwise unclear. This study was conducted to determine if enrichment of phosphorus (P) in tree island soils of the Florida Everglades can be explained by bird guano deposition. Concentrations of total carbon, nitrogen (N), and P, and N stable isotope ratio (δ(15)N) were determined on soil samples from 46 tree islands. Total elemental concentrations and δ(15)N were determined on wading bird guano. Sequential chemical extraction of P pools was also performed on guano. Guano contained between 53.1 and 123.7 g-N kg(-1) and 20.7 and 56.7 g-P kg(-1). Most of the P present in guano was extractable by HCl, which ranged from 82 to 97% of the total P. Total P of tree islands classified as having low or high P soils averaged 0.71 and 40.6 g kg(-1), respectively. Tree island soil with high total P concentration was found to have a similar δ(15)N signature and total P concentration as bird guano. Phosphorus concentrations and δ(15)N were positively correlated in tree island soils (r = 0.83, p< 0.0001). Potential input of guano with elevated concentrations of N and P, and (15)N enriched N, relative to other sources suggests that guano deposition in tree island soils is a mechanism contributing to this pattern.

Determining habitat quality for species that demonstrate dynamic habitat selection.

Determining habitat quality for wildlife populations requires relating a species' habitat to its survival and reproduction. Within a season, species occurrence and density can be disconnected from measures of habitat quality when resources are highly seasonal, unpredictable over time, and patchy. Here we establish an explicit link among dynamic selection of changing resources, spatio-temporal species distributions, and fitness for predictive abundance and occurrence models that are used for short-term water management and long-term restoration planning. We used the wading bird distribution and evaluation models (WADEM) that estimate (1) daily changes in selection across resource gradients, (2) landscape abundance of flocks and individuals, (3) conspecific foraging aggregation, and (4) resource unit occurrence (at fixed 400 m cells) to quantify habitat quality and its consequences on reproduction for wetland indicator species. We linked maximum annual numbers of nests detected across the study area and nesting success of Great Egrets (Ardea alba), White Ibises (Eudocimus albus), and Wood Storks (Mycteria americana) over a 20-year period to estimated daily dynamics of food resources produced by WADEM over a 7490 km(2) area. For all species, increases in predicted species abundance in March and high abundance in April were strongly linked to breeding responses. Great Egret nesting effort and success were higher when birds also showed greater conspecific foraging aggregation. Synthesis and applications: This study provides the first empirical evidence that dynamic habitat selection processes and distributions of wading birds over environmental gradients are linked with reproductive measures over periods of decades. Further, predictor variables at a variety of temporal (daily-multiannual) resolutions and spatial (400 m to regional) scales effectively explained variation in ecological processes that change habitat quality. The process used here allows managers to develop short- and long-term conservation strategies that (1) consider flexible behavioral patterns and (2) are robust to environmental variation over time.

Endocrine disruption in white ibises (Eudocimus albus) caused by exposure to environmentally relevant levels of methylmercury.

Methylmercury is a globally distributed pollutant and upper trophic level aquatic fauna are at particularly high risk of exposure. Although methylmercury is known to have a number of neurological and developmental effects, relatively little is known about effects on endocrine disruption and reproduction in aquatic fauna, particularly in response to chronic exposure at low concentrations. We experimentally exposed captive white ibises for 3.5 years (2005-2008) to dietary methylmercury at three environmentally relevant concentrations (0.05, 0.1 and 0.3 ppm wet weight in diet). We measured fecal concentrations of estradiol and testosterone metabolites in two consecutive breeding seasons (2007 and 2008). When effects were controlled for stage of breeding, this resulted in altered estradiol and testosterone concentrations in adult breeders of both sexes. Changes in endocrine expression were not consistent over both years, and a clear dose-response relationship was not always present. Endocrine changes were, however, associated at all dose levels with changes in reproductive behavior, reduced reproductive success and altered mate choice in males. Male-male pairing and altered courtship behavior in males were related both to dose treatment and, in 2008, to a demasculinized pattern of endocrine expression. Changes in hormone concentrations of dosed homosexually paired males, when present, were in the same direction but at a higher magnitude than those in heterosexual dosed males. Dosed homosexual males showed decreased testosterone during nest-building and elevated testosterone during incubation when compared with their dosed heterosexual counterparts during the 2008 breeding season. In the same year, exposed males had elevated estradiol during courtship, but had decreased estradiol during other stages in comparison with controls. Dosed females generally showed decreased estradiol and testosterone concentrations compared to controls, albeit not with a clear dose-response effect. Our findings suggest that endocrine disruption due to chronic exposure to even low concentrations of dietary methylmercury may be a widespread mechanism by which reproduction is impaired in wild bird populations.

Use of the superpopulation approach to estimate breeding population size: an example in asynchronously breeding birds.

Many populations of animals are fluid in both space and time, making estimation of numbers difficult. Much attention has been devoted to estimation of bias in detection of animals that are present at the time of survey. However, an equally important problem is estimation of population size when all animals are not present on all survey occasions. Here, we showcase use of the superpopulation approach to capture-recapture modeling for estimating populations where group membership is asynchronous, and where considerable overlap in group membership among sampling occasions may occur. We estimate total population size of long-legged wading bird (Great Egret and White Ibis) breeding colonies from aerial observations of individually identifiable nests at various times in the nesting season. Initiation and termination of nests were analogous to entry and departure from a population. Estimates using the superpopulation approach were 47-382% larger than peak aerial counts of the same colonies. Our results indicate that the use of the superpopulation approach to model nesting asynchrony provides a considerably less biased and more efficient estimate of nesting activity than traditional methods. We suggest that this approach may also be used to derive population estimates in a variety of situations where group membership is fluid.

Sublethal effects of methylmercury on fecal metabolites of testosterone, estradiol, and corticosterone in captive juvenile white ibises (Eudocimus albus).

Methylmercury (MeHg) is a globally distributed neurotoxin, endocrine disruptor, and teratogen, and its effects on birds are poorly understood, especially within an environmentally relevant exposure range. In an effort to understand the potential causal relationship between MeHg exposure and endocrine development, we established four dietary exposure groups (0 [control], 0.05, 0.1, and 0.3 mg/kg wet wt/d of MeHg) of postfledging white ibises (Eudocimus albus) in a divided, free-flight aviary that spanned the estimated range of environmental exposure for this species. Fecal samples were collected from individually identified ibises over six months in 2005 and processed for hormone evaluation. Significant sex-related differences in fecal estradiol concentrations, though unpredicted in direction, suggest that this steroid could be related to juvenile development in this species. Using repeated-measures general linear models, we tested a set of candidate models to explain variation in endocrine expression. We found that MeHg exposure led to significant differences in fecal estradiol concentrations between the control and medium-dose groups, whereas differences in fecal corticosterone concentrations were observed between the control and both the low- and high-dose groups. These results suggest highly nonlinear dose-response patterns for MeHg. Many endocrine-disrupting contaminants are theorized to affect multiple endpoints in a nonlinear manner, making results difficult to interpret using a traditional toxicological approach. The evidence presented here suggests that endocrine effects of MeHg exposure could behave similarly.

Effects of methylmercury and spatial complexity on foraging behavior and foraging efficiency in juvenile white ibises (Eudocimus albus).

Methylmercury is a globally distributed neurotoxin, endocrine disruptor, and teratogen, the effects of which on wildlife at environmentally relevant levels are largely unknown. In birds, foraging efficiency and learning may be sensitive endpoints for sublethal methylmercury toxicity, and these endpoints also may be biologically relevant at the population level. In the present study, groups of wild-caught, prefledgling white ibises (Eudocimus albus) were raised in a free-flight, open-air aviary on diets that approximated the measured range of methylmercury exposure in the Everglades ecosystem (0, 0.05, 0.1, and 0.3 mg/kg/d). The effect of methylmercury exposure on group foraging efficiency was examined by allowing birds to forage on 200 fathead minnows (Pimephales promelas) in artificial ponds for 15 min by straining the arenas' contents through a seine net and counting all remaining prey. Additionally, we varied the difficulty of foraging by these tactile feeding birds by adding multiple levels of structural complexity (e.g., increased vegetation and prey refugia) to the pond. Structural complexity affected both foraging efficiency and the rate of increase in efficiency over time (improvement). Methylmercury exposure affected foraging efficiency (p = 0.03). It did not affect foraging improvement in the face of increasingly challenging environments, however, and the dose-response relationship was nonlinear (e.g., the control and high-exposure groups were the least efficient foragers). Evidence for an effect of methylmercury on foraging efficiency therefore was inconclusive because of unpredicted results and no interaction with time or habitat complexity. These data suggest a nonlinear dose-response relationship at low levels of methylmercury exposure; future research is needed to verify this hypothesis. This appears to be the first experimental demonstration of the effects of habitat complexity on foraging efficiency in long-legged wading birds.

Phenology of body mass changes during reproduction in a nomadic, tropical waterbird, the Scarlet Ibis (Eudocimus ruber).

In birds, the prereproductive buildup of endogenous energy reserves (e.g. body fat) is highly variable and is often thought to be a strategy evolving in response to either seasonal and/or unpredictable changes in breeding conditions. Nomadic behavior is also thought to be an adaptation to unpredictable resource distribution in both space and time. Because of the difficultly in obtaining a longitudinal time series of body masses for free-living individuals of highly nomadic species, the relationship between nomadism and endogenous energy storage has not been explored. In this study, we investigated prereproductive energy storage in a large free-flighted captive colony of highly nomadic waterbird, the Scarlet Ibis, Eudocimus ruber. We used size-corrected body mass as an index of body condition both earlier to and during breeding. We compared both breeders and nonbreeders body condition earlier to nesting. We also prevented a subsample of the birds from gaining mass earlier to nesting and compared their nesting success with a control group that was allowed to feed freely. Although significant differences were found in prereproductive body conditions of breeders and nonbreeders, we were unable to control breeding by manipulating prereproductive condition, most likely because of the ability of some birds to rapidly change body condition within several days or weeks earlier to nesting. We conclude that prereproductive energy storage is important for nesting success in both sexes of this highly nomadic species, however energy stores are highly labile and can be rapidly obtained through prenesting hyperphagia. Zoo Biol 27:360-370, 2008. (c) 2008 Wiley-Liss, Inc.

Subchronic effects of methylmercury on plasma and organ biochemistries in great egret nestlings.

In recent years, high concentrations of mercury have been found in wading birds in Florida, USA. Great egret (Ardea alba) chicks (2 weeks old) were dosed orally daily with the equivalent of 0, 0.5, or 5 microg/g Hg as methylmercury chloride in the diet for up to 12 weeks. Weakness of the legs or paralysis occurred in all high-dosed birds. Geometric mean blood Hg concentrations were 0.17, 10.3, and 78.5 microg/g (wet wt), respectively. Mercury concentrations for organs (microg/g wet wt), including brain (0.22, 3.4, and 35, respectively), liver (0.34, 15.1, 138, respectively), and kidney (0.28, 8.1, and 120, respectively), increased in a dose-dependent manner. Total glutathione (GSH) peroxidase activity was significantly lower in the plasma, brain, liver, and kidney of the high-dosed group. Plasma aspartate aminotransferase activity increased with mercury treatment, whereas lactate dehydrogenase activity decreased. Four other plasma chemistries were decreased significantly in the high-dosed group and included uric acid, total protein, albumin, and inorganic phosphorus. Lipid peroxidation increased in liver (low and high dose) and brain (high dose). Tissue changes in concentrations of reduced thiols included decreased total thiols and protein-bound thiols in liver, decreased protein-bound thiols in kidney, and increased GSH in kidney and brain. Activities of GSH S-transferase and oxidized glutathione reductase increased in liver. In kidney, GSH S-transferase and glucose-6-phosphate dehydrogenase activities increased with mercury dose. These findings, including apparent compensatory changes, are compared to other Hg studies where oxidative stress was reported in egrets, herons, and diving ducks in the field and mallards in the laboratory.

A historical record of mercury contamination in Southern Florida (USA) as inferred from avian feather tissue.

During the late 1980s, the upper trophic-level biota of the Everglades (FL, USA) was recognized as being highly contaminated with mercury (Hg). However, the timing and pattern of that increase is poorly known, and no information is available about mercury contamination in Everglades wildlife prior to 1974. We measured methylmercury concentrations in feathers of white ibises (n = 33), great egrets (n = 7), anhingas (n = 21), and great blue herons (n = 12) from museum specimens collected from 1910 through 1980 and combined them with more recent feather samples collected from live birds (1985-2000, n = 98, 37, 49, and 7, respectively). We found no evidence of contamination of museum samples with inorganic mercuric preservatives (0.01-0.28% of total Hg in feathers). All species showed relatively low concentrations of mercury through the 1970s (<5 microl/L dry wt for anhingas, ibises, and egrets, <10 microl/L for herons). Samples from all species taken during the 1990s showed a large and significant increase (4-5X) in MeHg concentration. This evidence suggests that most of the increase in Hg deposition during the 20th century in south Florida occurred during the last two to three decades, which is consistent with information about local source deposition. Contamination levels prior to the 1970s appear to have been associated with normal reproduction in these birds, suggesting partial evidence for a threshold of reproductive impairment.

Reproductive physiology of free-living White Ibises (Eudocimus albus) in the Florida Everglades.

We measured plasma concentrations of testosterone, estradiol, progesterone, and corticosterone; and recorded changes in gonad size, body condition, molt, and brood patch development of free-living adult White Ibises (Eudocimus albus) during the breeding season in the Florida Everglades. White Ibises are colonially breeding, long-legged wading birds that inhabit freshwater and estuarine wetlands. They have flexible breeding schedules (nest initiation dates can range from January to September) and onset of nesting is usually associated with increased prey availability caused by concentration of small fish in pools during periods of wetland drying. In this paper, we present the hormonal and physical characteristics of White Ibis reproductive physiology. We classified White Ibis breeding into five stages: pre-breeding, display, copulation/egg production, incubation, and chick rearing. White Ibises showed cyclic gonadal development which corresponded to reproductive stage. Male and female testosterone concentrations increased during the display stage and decreased during copulation, incubation, and chick rearing. Female estradiol concentrations were highest during display and chick rearing and male estradiol concentrations were lowest during copulation. Female progesterone concentrations increased during display and remained high throughout the breeding season. Female ibises had low corticosterone concentrations that increased during incubation and were highest during chick rearing, concomitant with lower body condition and flight muscle-mass scores. Male ibis progesterone and corticosterone concentrations did not show seasonal changes and were more variable than concentrations in female ibises at similar stages. Males and females had elevated body condition scores during the display stage, which were depleted by the onset of incubation. Increased energy stores during display may be used later for fasting in male birds that do not eat during the 10-day copulation/egg production stage, and for egg production in female birds. During incubation, male and female ibises developed brood patches. Ibises molted in all stages of reproduction, indicating that ibis molt and reproductive physiology may not inhibit each other as in most temperate bird species. White Ibises showed similar patterns in reproductive physiology to other monogamous, seasonally breeding bird species in which both sexes incubate and care for the young.

Wading birds as bioindicators of mercury contamination in Florida, USA: annual and geographic variation.

Mercury contamination in wetland biota is often dynamic, difficult to predict, and costly to track. In this paper, we present results from a six-year study of growing feathers of piscivorous birds as monitors of wetland Hg exposure in Florida, USA, wetlands. Between 1994 and 2000, we collected feathers of growing great egret (Ardea alba) nestlings from colonies in the freshwater Everglades of southern Florida, and during 1998, feathers were collected from chicks of both great egrets and white ibises (Eudocimus albus) at a variety of colonies throughout peninsular Florida. Coastal colonies showed significantly lower feather Hg concentrations than did inland sites. Within the Everglades, we found significant effects of both geographic location and year on age-adjusted mean total Hg concentrations in feathers. Over the course of our study, Everglades colonies maintained their Hg concentration rankings relative to one another, but all showed strongly declining Hg concentrations (mean of 73% averaged across colonies, between 1994 and 2000). Using a previously established predictive relationship between Hg consumption in food and feather Hg for great egrets, we estimated that Hg concentrations in the aggregate diet of egrets have been reduced by an average of 67%. We conclude that the Everglades has undergone a biologically significant decline in Hg availability in the wetland food web, possibly because of decreased local inputs.