Tropical snake diversity collapses after widespread amphibian loss.

Biodiversity is declining at unprecedented rates worldwide. Yet cascading effects of biodiversity loss on other taxa are largely unknown because baseline data are often unavailable. We document the collapse of a Neotropical snake community after the invasive fungal pathogen Batrachochytrium dendrobatidis caused a chytridiomycosis epizootic leading to the catastrophic loss of amphibians, a food source for snakes. After mass mortality of amphibians, the snake community contained fewer species and was more homogeneous across the study site, with several species in poorer body condition, despite no other systematic changes in the environment. The demise of the snake community after amphibian loss demonstrates the repercussive and often unnoticed consequences of the biodiversity crisis and calls attention to the invisible declines of rare and data-deficient species.

Disentangling data discrepancies with integrated population models.

A common challenge for studying wildlife populations occurs when different survey methods provide inconsistent or incomplete inference on the trend, dynamics, or viability of a population. A potential solution to the challenge of conflicting or piecemeal data relies on the integration of multiple data types into a unified modeling framework, such as integrated population models (IPMs). IPMs are a powerful approach for species that inhabit spatially and seasonally complex environments. We provide guidance on exploiting the capabilities of IPMs to address inferential discrepancies that stem from spatiotemporal data mismatches. We illustrate this issue with analysis of a migratory species, the American Woodcock (Scolopax minor), in which individual monitoring programs suggest differing population trends. To address this discrepancy, we synthesized several long-term data sets (1963-2015) within an IPM to estimate continental-scale population trends, and link dynamic drivers across the full annual cycle and complete extent of the woodcock's geographic range in eastern North America. Our analysis reveals the limiting portions of the life cycle by identifying time periods and regions where vital rates are lowest and most variable, as well as which demographic parameters constitute the main drivers of population change. We conclude by providing recommendations for resolving conflicting population estimates within an integrated modeling approach, and discuss how strategies (e.g., data thinning, expert opinion elicitation) from other disciplines could be incorporated into ecological analyses when attempting to combine multiple, incongruent data types.

Trophic declines and decadal-scale foraging segregation in three pelagic seabirds.

We investigated how foraging habits vary among three ecologically distinct wide-ranging seabirds. Using amino acid δ15N proxies for nutrient regime (δ15NPhe) and trophic position (Δδ15NGlu-Phe), we compared Newell's shearwater (Puffinus newelli) and Laysan albatross (Phoebastria immutabilis) foraging habits over the past 50-100 years, respectively, to published records for the Hawaiian petrel (Pterodroma sandwichensis). Standard ellipses constructed from the isotope proxies show that inter-population and interspecific foraging segregation have persisted for several decades. We found no evidence of a shift in nutrient regime at the base of the food web for the three species. However, our data identify a trophic decline during the past century for Newell's shearwater and Laysan albatross (probability ≥ 0.97), echoing a similar decline observed in the Hawaiian petrel. During this time, Newell's shearwaters and Hawaiian petrels have experienced population declines and Laysan albatross has experienced range extension and apparent population stability. Counting other recent studies, a pattern of trophic decline over the past century has now been identified in eight species of pelagic seabirds that breed in the Hawaiian Islands. Because our study species forage broadly across the North Pacific Ocean and differ in morphological and behavioral traits and feeding methods, the identified trophic declines suggest a pervasive shift in food web architecture within the past century.

Integrating count and detection-nondetection data to model population dynamics.

There is increasing need for methods that integrate multiple data types into a single analytical framework as the spatial and temporal scale of ecological research expands. Current work on this topic primarily focuses on combining capture-recapture data from marked individuals with other data types into integrated population models. Yet, studies of species distributions and trends often rely on data from unmarked individuals across broad scales where local abundance and environmental variables may vary. We present a modeling framework for integrating detection-nondetection and count data into a single analysis to estimate population dynamics, abundance, and individual detection probabilities during sampling. Our dynamic population model assumes that site-specific abundance can change over time according to survival of individuals and gains through reproduction and immigration. The observation process for each data type is modeled by assuming that every individual present at a site has an equal probability of being detected during sampling processes. We examine our modeling approach through a series of simulations illustrating the relative value of count vs. detection-nondetection data under a variety of parameter values and survey configurations. We also provide an empirical example of the model by combining long-term detection-nondetection data (1995-2014) with newly collected count data (2015-2016) from a growing population of Barred Owl (Strix varia) in the Pacific Northwest to examine the factors influencing population abundance over time. Our model provides a foundation for incorporating unmarked data within a single framework, even in cases where sampling processes yield different detection probabilities. This approach will be useful for survey design and to researchers interested in incorporating historical or citizen science data into analyses focused on understanding how demographic rates drive population abundance.

Broad-scale trophic shift in the pelagic North Pacific revealed by an oceanic seabird.

Human-induced ecological change in the open oceans appears to be accelerating. Fisheries, climate change and elevated nutrient inputs are variously blamed, at least in part, for altering oceanic ecosystems. Yet it is challenging to assess the extent of anthropogenic change in the open oceans, where historical records of ecological conditions are sparse, and the geographical scale is immense. We developed millennial-scale amino acid nitrogen isotope records preserved in ancient animal remains to understand changes in food web structure and nutrient regimes in the oceanic realm of the North Pacific Ocean (NPO). Our millennial-scale isotope records of amino acids in bone collagen in a wide-ranging oceanic seabird, the Hawaiian petrel (Pterodroma sandwichensis), showed that trophic level declined over time. The amino acid records do not support a broad-scale increase in nitrogen fixation in the North Pacific subtropical gyre, rejecting an earlier interpretation based on bulk and amino acid specific δ15N chronologies for Hawaiian deep-sea corals and bulk δ15N chronologies for the Hawaiian petrel. Rather, our work suggests that the food web structure in the NPO has shifted at a broad geographical scale, a phenomenon potentially related to industrial fishing.

Dynamic N-occupancy models: estimating demographic rates and local abundance from detection-nondetection data.

Occupancy modeling is a widely used analytical technique for assessing species distributions and range dynamics. However, occupancy analyses frequently ignore variation in abundance of occupied sites, even though site abundances affect many of the parameters being estimated (e.g., extinction, colonization, detection probability). We introduce a new model ("dynamic N-occupancy") capable of providing accurate estimates of local abundance, population gains (reproduction/immigration), and apparent survival probabilities while accounting for imperfect detection using only detection/nondetection data. Our model utilizes heterogeneity in detection based on variations in site abundances to estimate latent demographic rates via a dynamic N-mixture modeling framework. We validate our model using simulations across a wide range of values and examine the data requirements, including the number of years and survey sites needed, for unbiased and precise estimation of parameters. We apply our model to estimate spatiotemporal heterogeneity in abundances of barred owls (Strix varia) within a recently invaded region in Oregon (USA). Estimates of apparent survival and population gains are consistent with those from a nearby radio-tracking study and elucidate how barred owl abundances have increased dramatically over time. The dynamic N-occupancy model greatly improves inferences on individual-level population processes from occupancy data by explicitly modeling the latent population structure.

Beyond carbon and nitrogen: guidelines for estimating three-dimensional isotopic niche space.

Isotopic niche has typically been characterized through carbon and nitrogen ratios and most modeling approaches are limited to two dimensions. Yet, other stable isotopes can provide additional power to resolve questions associated with foraging, migration, dispersal and variations in resource use. The ellipse niche model was recently generalized to n-dimensions. We present an analogous methodology which incorporates variation across three stable dimensions to estimate the significant features of a population's isotopic niche space including: 1) niche volume (referred to as standard ellipsoid volume, SEV), 2) relative centroid location (CL), 3) shape and 4) area of overlap between multiple ellipsoids and 5) distance between two CLs. We conducted a simulation study showing the accuracy and precision of three dimensional niche models across a range of values. Importantly, the model correctly identifies differences in SEV and CL among populations, even with small sample sizes and in cases where the absolute values cannot precisely be recovered. We use these results to provide guidelines for sample size in conducting multivariate isotopic niche modeling. We demonstrate the utility of our approach with a case study of three bottlenose dolphin populations which appear to possess largely overlapping niches when analyzed with only carbon and nitrogen isotopes. Upon inclusion of sulfur, we see that the three dolphin ecotypes are in fact segregated on the basis of salinity and find the stable isotope niche of inshore bottlenose dolphins significantly larger than coastal and offshore populations.

Individual specialization in the foraging habits of female bottlenose dolphins living in a trophically diverse and habitat rich estuary.

We examine individual specialization in foraging habits (foraging habitat and trophic level) of female bottlenose dolphins (Tursiops truncatus) resident in Sarasota Bay, Florida, USA, by analyzing time series of stable isotope (δ(15)N and δ(13)C) values in sequential growth layer groups within teeth. The isotope data provide a chronology of foraging habits over the lifetime of the individual and allowed us to show that female bottlenose dolphins exhibit a high degree of individual specialization in both foraging habitat and trophic level. The foraging habits used by adult females are similar to those they used as calves and may be passed down from mother to calf through social learning. We also characterized the foraging habits and home range of each individual by constructing standard ellipses from isotope values and dolphin sightings data (latitude and longitude), respectively. These data show that Sarasota Bay bottlenose dolphins forage within a subset of the habitats in which they are observed. Moreover, females with similar observational standard ellipses often possessed different foraging specializations. Female bottlenose dolphins may demonstrate individual specialization in foraging habits because it reduces some of the cost of living in groups, such as competition for prey.

Unexpected hydrogen isotope variation in oceanic pelagic seabirds.

Hydrogen isotopes have significantly enhanced our understanding of the biogeography of migratory animals. The basis for this methodology lies in predictable, continental patterns of precipitation δD values that are often reflected in an organism's tissues. δD variation is not expected for oceanic pelagic organisms whose dietary hydrogen (water and organic hydrogen in prey) is transferred up the food web from an isotopically homogeneous water source. We report a 142‰ range in the δD values of flight feathers from the Hawaiian petrel (Pterodroma sandwichensis), an oceanic pelagic North Pacific species, and inquire about the source of that variation. We show δD variation between and within four other oceanic pelagic species: Newell's shearwater (Puffinus auricularis newellii), Black-footed albatross (Phoebastria nigripes), Laysan albatross (Phoebastria immutabilis) and Buller's shearwater (Puffinus bulleri). The similarity between muscle δD values of hatch-year Hawaiian petrels and their prey suggests that trophic fractionation does not influence δD values of muscle. We hypothesize that isotopic discrimination is associated with water loss during salt excretion through salt glands. Salt load differs between seabirds that consume isosmotic squid and crustaceans and those that feed on hyposmotic teleost fish. In support of the salt gland hypothesis, we show an inverse relationship between δD and percent teleost fish in diet for three seabird species. Our results demonstrate the utility of δD in the study of oceanic consumers, while also contributing to a better understanding of δD systematics, the basis for one of the most commonly utilized isotope tools in avian ecology.

Levels of chlorinated, brominated, and perfluorinated contaminants in birds of prey spanning multiple trophic levels.

Birds of prey occupy high trophic levels and can consequently bioaccumulate high levels of environmental contaminants. To evaluate exposure to past- and current-use pollutants, we measured legacy contaminants (i.e., polychlorinated biphenyls [PCBs]; organochlorine pesticides, e.g., DDT), contaminants of emerging concern (polybrominated diphenyl ethers [PBDEs]; perfluorinated compounds [PFCs]), and stable isotopes (δ(13)C, δ(15)N) in 26 birds of prey (10 species) from coastal South Carolina (USA) sampled in 2009 and 2010. Nitrogen isotope ratios (δ(15)N) ranged from 5.2% to 13.7%, indicating the birds of prey spanned two to three trophic levels. Legacy contaminant levels were highly variable but generally comparable to levels reported previously for birds of prey in the southeast US, suggesting exposure has not declined substantially over the past 40 yr. Despite their status as newly emerging environmental contaminants, PFC levels were within the same order of magnitude as legacy contaminants. Although PBDEs were less prevalent, levels were among the greatest observed in wildlife to date (∑PBDEs max. 200 µg/g lipid). Relative contaminant profiles also varied between birds of prey utilizing low and high trophic levels; specifically PFCs contributed to a larger proportion of the contaminant burden in birds utilizing high trophic levels, whereas the legacy pesticide mirex was a larger contributor in low-trophic-level birds, indicating that relative exposure is in part dependent on foraging ecology. This study demonstrates that birds of prey continue to face exposure to legacy contaminants as well as newly emerging contaminants at levels of concern.