Kristen M. Hart

Severe mammal declines coincide with proliferation of invasive Burmese pythons in Everglades National Park

Invasive species represent a significant threat to global biodiversity and a substantial economic burden. Burmese pythons, giant constricting snakes native to Asia, now are found throughout much of southern Florida, including all of Everglades National Park (ENP). Pythons have increased dramatically in both abundance and geographic range since 2000 and consume a wide variety of mammals and birds. Here we report severe apparent declines in mammal populations that coincide temporally and spatially with the proliferation of pythons in ENP. Before 2000, mammals were encountered frequently during nocturnal road surveys within ENP. In contrast, road surveys totaling 56,971 km from 2003–2011 documented a 99.3% decrease in the frequency of raccoon observations, decreases of 98.9% and 87.5% for opossum and bobcat observations, respectively, and failed to detect rabbits. Road surveys also revealed that these species are more common in areas where pythons have been discovered only recently and are most abundant outside the pythons current introduced range. These findings suggest that predation by pythons has resulted in dramatic declines in mammals within ENP and that introduced apex predators, such as giant constrictors, can exert significant top-down pressure on prey populations. Severe declines in easily observed and/or common mammals, such as raccoons and bobcats, bode poorly for species of conservation concern, which often are more difficult to sample and occur at lower densities.

Environmental DNA (eDNA) Sampling Improves Occurrence and Detection Estimates of Invasive Burmese Pythons

Environmental DNA (eDNA) methods are used to detect DNA that is shed into the aquatic environment by cryptic or low density species. Applied in eDNA studies, occupancy models can be used to estimate occurrence and detection probabilities and thereby account for imperfect detection. However, occupancy terminology has been applied inconsistently in eDNA studies, and many have calculated occurrence probabilities while not considering the effects of imperfect detection. Low detection of invasive giant constrictors using visual surveys and traps has hampered the estimation of occupancy and detection estimates needed for population management in southern Florida, USA. Giant constrictor snakes pose a threat to native species and the ecological restoration of the Florida Everglades. To assist with detection, we developed species-specific eDNA assays using quantitative PCR (qPCR) for the Burmese python (Python molurus bivittatus), Northern African python (P. sebae), boa constrictor (Boa constrictor), and the green (Eunectes murinus) and yellow anaconda (E. notaeus). Burmese pythons, Northern African pythons, and boa constrictors are established and reproducing, while the green and yellow anaconda have the potential to become established. We validated the python and boa constrictor assays using laboratory trials and tested all species in 21 field locations distributed in eight southern Florida regions. Burmese python eDNA was detected in 37 of 63 field sampling events; however, the other species were not detected. Although eDNA was heterogeneously distributed in the environment, occupancy models were able to provide the first estimates of detection probabilities, which were greater than 91%. Burmese python eDNA was detected along the leading northern edge of the known population boundary. The development of informative detection tools and eDNA occupancy models can improve conservation efforts in southern Florida and support more extensive studies of invasive constrictors. Generic sampling design and terminology are proposed to standardize and clarify interpretations of eDNA-based occupancy models.

Mitigating By-Catch of Diamondback Terrapins in Crab Pots

ABSTRACT Chronic by-catch of diamondback terrapins (Malaclemys terrapin) in blue crab (Callinectes sapidus) pots is a concern for terrapin conservation along the United States Atlantic and Gulf of Mexico coasts. Despite the availability of by-catch reduction devices (BRDs) for crab pots, adoption of BRDs has not been mandated and by-catch of terrapins continues. We conducted experimental fishing studies in North Carolinas year-round blue crab fishery from 2000 to 2004 to evaluate the ability of various BRDs to reduce terrapin by-catch without a concomitant reduction in the catch of blue crabs. In 4,822 crab pot days fished, we recorded only 21 terrapin captures. Estimated capture rates were 0.003 terrapins/pot per day in hard crab experimental fishing and 0.008 terrapins/pot per day in peeler experimental fishing. All terrapin captures occurred from April to mid-May within 321.4 m of the shoreline. Longer soak times produced more dead terrapins, with 4 live and 4 dead during hard crab experimental fishing and 11 live and 2 dead during peeler experimental fishing. The 4.0-cm BRDs in fall and 4.5-cm and 5.0-cm BRDs in spring reduced the catch of legal-sized male hard crabs by 26.6%, 21.2%, and 5.7%, respectively. Only the 5.0-cm BRDs did not significantly affect the catch of legal-sized hard male crabs. However, BRDs had no measurable effect on catch of target crabs in the peeler crab fishery. Our results identify 3 complementary and economically feasible tools for blue crab fishery managers to exclude terrapins from commercially fished crab pots in North Carolina: 1) gear modifications (e.g., BRDs); 2) distance-to-shore restrictions; and 3) time-of-year regulations. These measures combined could provide a reduction in terrapin by-catch of up to 95% without a significant reduction in target crab catch.

Marsh rabbit mortalities tie pythons to the precipitous decline of mammals in the Everglades

To address the ongoing debate over the impact of invasive species on native terrestrial wildlife, we conducted a large-scale experiment to test the hypothesis that invasive Burmese pythons (Python molurus bivittatus) were a cause of the precipitous decline of mammals in Everglades National Park (ENP). Evidence linking pythons to mammal declines has been indirect and there are reasons to question whether pythons, or any predator, could have caused the precipitous declines seen across a range of mammalian functional groups. Experimentally manipulating marsh rabbits, we found that pythons accounted for 77% of rabbit mortalities within 11 months of their translocation to ENP and that python predation appeared to preclude the persistence of rabbit populations in ENP. On control sites, outside of the park, no rabbits were killed by pythons and 71% of attributable marsh rabbit mortalities were classified as mammal predations. Burmese pythons pose a serious threat to the faunal communities and ecological functioning of the Greater Everglades Ecosystem, which will probably spread as python populations expand their range.

Determining origin in a migratory marine vertebrate: a novel method to integrate stable isotopes and satellite tracking

Stable isotope analysis is a useful tool to track animal movements in both terrestrial and marine environments. These intrinsic markers are assimilated through the diet and may exhibit spatial gradients as a result of biogeochemical processes at the base of the food web. In the marine environment, maps to predict the spatial distribution of stable isotopes are limited, and thus determining geographic origin has been reliant upon integrating satellite telemetry and stable isotope data. Migratory sea turtles regularly move between foraging and reproductive areas. Whereas most nesting populations can be easily accessed and regularly monitored, little is known about the demographic trends in foraging populations. The purpose of the present study was to examine migration patterns of loggerhead nesting aggregations in the Gulf of Mexico (GoM), where sea turtles have been historically understudied. Two methods of geographic assignment using stable isotope values in known-origin samples from satellite telemetry were compared: (1) a nominal approach through discriminant analysis and (2) a novel continuous-surface approach using bivariate carbon and nitrogen isoscapes (isotopic landscapes) developed for this study. Tissue samples for stable isotope analysis were obtained from 60 satellite-tracked individuals at five nesting beaches within the GoM. Both methodological approaches for assignment resulted in high accuracy of foraging area determination, though each has advantages and disadvantages. The nominal approach is more appropriate when defined boundaries are necessary, but up to 42% of the individuals could not be considered in this approach. All individuals can be included in the continuous-surface approach, and individual results can be aggregated to identify geographic hotspots of foraging area use, though the accuracy rate was lower than nominal assignment. The methodological validation provides a foundation for future sea turtle studies in the region to inexpensively determine geographic origin for large numbers of untracked individuals. Regular monitoring of sea turtle nesting aggregations with stable isotope sampling can be used to fill critical data gaps regarding habitat use and migration patterns. Probabilistic assignment to origin with isoscapes has not been previously used in the marine environment, but the methods presented here could also be applied to other migratory marine species.

Risk assessment of potential invasiveness of exotic reptiles imported to south Florida

The recent explosion of exotic reptiles in south Florida requires effective management strategies. The objective of this study is to bring knowledge of ecological correlates and quantitative modeling methods into management by providing the foundation for a screening procedure that will identify potentially invasive species and assess adverse impacts associated with these species. We considered 17 variables and, based on model selection procedures, we identified the following significant predictors of establishment success: taxonomic order, maximum temperature match between a species’ native range and Florida, animal sale price, and manageability (defined as a species’ maintenance cost, aggressiveness, proneness to escape, and venomousness). Applying the models to predict establishment success of 33 reptiles that were most frequently imported through Miami and St. Petersburg ports from 2000 to 2005 and two additional reptiles of concern in Florida, we identified eight lizards and four snakes as potentially successful invaders. We further assessed adverse impacts associated with potential invaders, should they become established, by identifying species that are (1) dangerous to humans, (2) dangerous to the ecosystem (upper trophic-level predators), and (3) rapidly spreading. Controlling exotic reptiles can be expensive and labor intensive once they are established. Information on which species are potential invaders based on screening procedures and what impacts these species might cause will be a valuable contribution to the development of proactive management strategies.

Movements and Habitat-Use of Loggerhead Sea Turtles in the Northern Gulf of Mexico during the Reproductive Period

Nesting strategies and use of important in-water habitats for far-ranging marine turtles can be determined using satellite telemetry. Because of a lack of information on habitat-use by marine turtles in the northern Gulf of Mexico, we used satellite transmitters in 2010 through 2012 to track movements of 39 adult female breeding loggerhead turtles (Caretta caretta) tagged on nesting beaches at three sites in Florida and Alabama. During the nesting season, recaptured turtles emerged to nest 1 to 5 times, with mean distance between emergences of 27.5 km; however, several turtles nested on beaches separated by ∼250 km within a single season. Mean total distances traveled throughout inter-nesting periods for all turtles was 1422.0±930.8 km. In-water inter-nesting sites, delineated using 50% kernel density estimation (KDE), were located a mean distance of 33.0 km from land, in water with mean depth of −31.6 m; other in-water inter-nesting sites, delineated using minimum convex polygon (MCP) approach, were located a mean 13.8 km from land and in water with a mean depth of −15.8 m. Mean size of in-water inter-nesting habitats were 61.9 km2 (50% KDEs, n = 10) and 741.4 km2 (MCPs, n = 30); these areas overlapped significantly with trawling and oil and gas extraction activities. Abundance estimates for this nesting subpopulation may be inaccurate in light of how much spread there is between nests of the same individual. Further, our results also have consequences for critical habitat designations for northern Gulf loggerheads, as protection of one nesting beach would not encompass the entire range used by turtles during breeding seasons.

Foraging area fidelity for Kemp's ridleys in the Gulf of Mexico.

For many marine species, locations of key foraging areas are not well defined. We used satellite telemetry and switching state-space modeling (SSM) to identify distinct foraging areas used by Kemps ridley turtles (Lepidochelys kempii) tagged after nesting during 1998–2011 at Padre Island National Seashore, Texas, USA (PAIS; N = 22), and Rancho Nuevo, Tamaulipas, Mexico (RN; N = 9). Overall, turtles traveled a mean distance of 793.1 km (±347.8 SD) to foraging sites, where 24 of 31 turtles showed foraging area fidelity (FAF) over time (N = 22 in USA, N = 2 in Mexico). Multiple turtles foraged along their migratory route, prior to arrival at their “final” foraging sites. We identified new foraging “hotspots” where adult female Kemps ridley turtles spent 44% of their time during tracking (i.e., 2641/6009 tracking days in foraging mode). Nearshore Gulf of Mexico waters served as foraging habitat for all turtles tracked in this study; final foraging sites were located in water <68 m deep and a mean distance of 33.2 km (±25.3 SD) from the nearest mainland coast. Distance to release site, distance to mainland shore, annual mean sea surface temperature, bathymetry, and net primary production were significant predictors of sites where turtles spent large numbers of days in foraging mode. Spatial similarity of particular foraging sites selected by different turtles over the 13-year tracking period indicates that these areas represent critical foraging habitat, particularly in waters off Louisiana. Furthermore, the wide distribution of foraging sites indicates that a foraging corridor exists for Kemps ridleys in the Gulf. Our results highlight the need for further study of environmental and bathymetric components of foraging sites and prey resources contained therein, as well as international cooperation to protect essential at-sea foraging habitats for this imperiled species.

Migration, foraging, and residency patterns for Northern Gulf loggerheads: implications of local threats and international movements.

Northern Gulf of Mexico (NGoM) loggerheads (Caretta caretta) make up one of the smallest subpopulations of this threatened species and have declining nest numbers. We used satellite telemetry and a switching state-space model to identify distinct foraging areas used by 59 NGoM loggerheads tagged during 2010–2013. We tagged turtles after nesting at three sites, 1 in Alabama (Gulf Shores; n = 37) and 2 in Florida (St. Joseph Peninsula; n = 20 and Eglin Air Force Base; n = 2). Peak migration time was 22 July to 9 August during which >40% of turtles were in migration mode; the mean post-nesting migration period was 23.0 d (±13.8 d SD). After displacement from nesting beaches, 44 turtles traveled to foraging sites where they remained resident throughout tracking durations. Selected foraging locations were variable distances from tagging sites, and in 5 geographic regions; no turtles selected foraging sites outside the Gulf of Mexico (GoM). Foraging sites delineated using 50% kernel density estimation were located a mean distance of 47.6 km from land and in water with mean depth of −32.5 m; other foraging sites, delineated using minimum convex polygons, were located a mean distance of 43.0 km from land and in water with a mean depth of −24.9 m. Foraging sites overlapped with known trawling activities, oil and gas extraction activities, and the footprint of surface oiling during the 2010 Deepwater Horizon oil spill (n = 10). Our results highlight the year-round use of habitats in the GoM by loggerheads that nest in the NGoM. Our findings indicate that protection of females in this subpopulation requires both international collaborations and management of threats that spatially overlap with distinct foraging habitats.

Using Scenario Planning to Evaluate the Impacts of Climate Change on Wildlife Populations and Communities in the Florida Everglades

It is uncertain how climate change will impact hydrologic drivers of wildlife population dynamics in freshwater wetlands of the Florida Everglades, or how to accommodate this uncertainty in restoration decisions. Using projections of climate scenarios for the year 2060, we evaluated how several possible futures could affect wildlife populations (wading birds, fish, alligators, native apple snails, amphibians, threatened and invasive species) across the Everglades landscape and inform planning already underway. We used data collected from prior research and monitoring to parameterize our wildlife population models. Hydrologic data were simulated using a spatially explicit, regional-scale model. Our scenario evaluations show that expected changes in temperature, precipitation, and sea level could significantly alter important ecological functions. All of our wildlife indicators were negatively affected by scenarios with less rainfall and more evapotranspiration. Under such scenarios, habitat suitability was substantially reduced for iconic animals such as wading birds and alligators. Conversely, the increased rainfall scenario benefited aquatic prey productivity and apex predators. Cascading impacts on non-native species is speculative, but increasing temperatures could increase the time between cold events that currently limit expansion and abundance of non-native fishes, amphibians, and reptiles with natural ranges in the tropics. This scenario planning framework underscored the benefits of proceeding with Everglades restoration plans that capture and clean more freshwater with the potential to mitigate rainfall loss and postpone impacts of sea level rise.