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Amphibian population declines: 30 Years of progress in confronting a complex problem

In 1989, it dawned on participants at the First World Congress of Herpetology that observed declines in amphibian populations might actually be global in scope and unprecedented in severity. Three decades of research since then has produced an enormous increase in our knowledge of amphibian ecology and appreciation of the complexity of possible causes for amphibian population declines. In September 2019, 30 yr after the First World Congress ended, a day-long, international symposium on amphibian population declines was held at the Redpath Museum of McGill University in Montreal, Canada. Symposium participants drew upon the knowledge gained over three decades of study to look ahead with fresh ideas to address this vital aspect of the global decline of biodiversity. Despite tremendous progress over the past three decades there is still much about amphibian ecology, population biology, and pathology that remains unknown. Amphibian declines have turned out to be more complex than originally expected and the result of multiple possible causes acting across landscapes, among taxa, or between populations in ways that are not at all uniform. The papers in this special issue of Herpetologica , which stem from the symposium, explore much of our current understanding of amphibian declines and their causes.

Herpetologica

Malaclemys terrapin rhizophorarum (mangrove diamond-backed terrapin)

MALACLEMYS TERRAPIN RHIZOPHORARUM (Mangrove Diamond-backed Terrapin). DIET. Malaclemys terrapin rhizophorarum, one of seven subspecies of M. terrapin, inhabits subtropical mangrove habitats in South Florida, USA. In temperate climates M. terrapin is largely carnivorous, feeding primarily on gastropods, bivalves, and decapod crustaceans (Tucker et. al. 1995. Herpetologica 51:167–181; Butler et. al. 2012. Chelon. Conserv. Biol. 11:124–128). In addition to its preferred prey, M. t. rhizophorarum has also been reported to consume barnacles, fish, and vegetation (Tucker et. al. 1995, op. cit.; Butler et. al. 2012, op. cit.; Tulipani 2013. Ph.D. Dissertation. The College of William and Mary, Williamsburg, Virginia. 224 pp.). Herein, we report observations regarding the diet of M. t. rhizophorarum from the southernmost extent of their range in the Florida Keys, USA.

Herpetological Review

Crocodylus acutus (American Crocodile). Long distance juvenile movement

Crocodylus acutus (American Crocodile) is the most widely distributed New World crocodilian species with its range extending from Peru in the south to the southern tip of peninsular Florida in the north. Crocodylus acutus occupies primarily coastal brackish water habitat, however it also occurs in freshwater to hypersaline habitats (Thorbjarnarson 2010. In Crocodiles. Status Survey and Conservation Action Plan. [Third Edition], American Crocodile Crocodylus acutus, pp. 46–53 S.C. Manolis and C. Stevenson. Crocodile Specialist Group, Darwin). There is limited literature on long distance movements of juvenile crocodilians worldwide and no literature on juvenile crocodiles in Florida. However, adult C. acutus in Florida have been documented to make seasonal movements of 5–15 km from preferred foraging habitat to nesting beaches (Mazzotti 1983. The Ecology of Crocodylus acutus in Florida. PhD Dissertation. The Pennsylvania State University, University Park, Pennsylvania. 161pp), and one adult was documented making a 35 km trip from her nest site to preferred foraging habitat (Cherkiss et. al. 2006. Herpetol. Rev. 38:72–73). Rodda (1984. Herpetologica 40:444–451) reported on juvenile C. acutus movement in Gatun Lake, Panama, and found that juveniles stayed within 1 km of their nest site for the first month. Movements of juvenile Crocodylus porosus (Saltwater Crocodile) in a river system in Northern Australia showed a maximum movement of 38.9 km from a known nest site, with the majority of the crocodiles staying within 15.6 km downstream to 6.8 km upstream (Webb and Messel 1978. Aust. Wildlife Res. 5:263–283). Juvenile movement of Crocodylus niloticus (Nile Crocodile) in Lake Ngezi, Zimbabwe showed crocodiles restricted their movements from 1.0 km up to 4.5 km through the wet and dry seasons (Hutton 1989. Am. Zool. 29:1033–1049). Long distance movements of alligators were recorded for sizes ranging from 28 cm to 361 cm in a coastal refuge in Louisiana, where the distance traveled ranged from 0.3 km to 90.2 km. The data showed that the smaller alligators moved greater distance than larger ones (Lance et al. 2011. Southeast Nat. 10:389–398). An ongoing 30 year mark and recapture study for Crocodylus acutus in Florida allowed us to look at long distance movement (>30 km) of juveniles (30km). Initial and most recent captures as a juvenile were used to analyze distances moved (Fig. 1). These distances were measured linearly between capture locations. Maximum linear distances of 76.3 km and 69.6 km were recorded for animals 4838 and 6662. All crocodiles moved from nesting habitat through potentially optimal nursery habitat prior to reaching their recapture locations. These juvenile long distance movements could be due to larger crocodiles facilitating their dispersal from the nest location (Lance et al. 2011. op. cit.). These data (Table 1.) support that there is exchange of individuals among the nesting colonies and our ongoing efforts to monitor this threatened species allow us to make observations of how juvenile crocodiles are moving throughout the landscape in an ecosystem currently undergoing restoration.

Herpetological Review

Locality note for rubber boa

CHARINA BOTTAE BOTTAE (N. Rubber Boa), USA: CALIFORNIA: Monterey Co.: Landels-Hill Big Creek Reserve, east side of Hwy. 1, 80 km (50 miles) south of Carmel, Calif., (36.0719055 N 121.5991555 W) 19 June, 2009; (36.0703611 N 121.5982222 W) 06 July 2009; (36.9516666 N 121.5991944 W) 27 July 2009. In chronological order, photo vouchers MVZObs:Herp:26, MVZObs:Herp:27, MVZObs:Herp:28. Verified by Mitchell Mulks, formerly of 84 Redondo Ave. Suisun City, Calif., Michelle Koo, Staff Curator, Biodiversity Informatics & GIS and Researcher, MVZ, U.C., Berkeley, Calif. New southern extension of the species in the Santa Lucia Range of Monterey Co. approximately 48 km. (30 miles) south of previous range extension south of Carmel in Bixby Canyon (Burger, L.W., Herpetologica, Vol. 8. Part 1. March 22, 1952), and approximately 4 km. (2.5 miles) south of MVZ #229876 found 20 miles north of Nacimiento Road, at approximate coordinates of 36.10033 N 121.62026 W.

California

Lampropeltis californiae (California kingsnake) behavior, male-male combat

There are few published descriptions of male-male combat in Lampropeltis spp. under natural conditions. Shaw (1951. Herpetologica 7:149-168) briefly described aggressive interactions between two captive male L. annulata (Mexican Milksnakes) that appeared to be associated with feeding, and Moehn (1967. Copeia 1967:480–481) described the "combat dance" between two male L. calligaster (Prairie Kingsnakes) in the field over a period of 30 minutes, with the snakes "completely intertwined..." and "...in constant motion." Carpenter and Gillingham (1977. Southwest. Nat. 22:517–524) described and illustrated interactions of two male L. holbrooki (Speckled Kingsnake) in a small artificial enclosure. Tabulated categories of male–male combat behaviors in Boid, Colubrid, and Viperid snakes (including Lampropeltis spp.) have been compared in an attempt to relate behavior patterns to phylogenetic relationships (Senter et al. 2014. PLoS ONE 9(9): e107528).

Herpetological Review

Portrait of a small population of boreal toads ( Anaxyrus boreas )

Much attention has been given to the conservation of small populations, those that are small because of decline, and those that are naturally small. Small populations are of particular interest because ecological theory suggests that they are vulnerable to the deleterious effects of environmental, demographic, and genetic stochasticity as well as natural and human-induced catastrophes. However, testing theory and developing applicable conservation measures for small populations is hampered by sparse data. This lack of information is frequently driven by computational issues with small data sets that can be confounded by the impacts of stressors. We present estimates of demographic parameters from a small population of Boreal Toads (Anaxyrus boreas) that has been surveyed since 2001 by using capture-recapture methods. Estimates of annual adult survival probability are high relative to other Boreal Toad populations, whereas estimates of recruitment rate are low. Despite using simple models, clear patterns emerged from the analyses, suggesting that population size is constrained by low recruitment of adults and is declining slowly. These patterns provide insights that are useful in developing management directions for this small population, and this study serves as an example of the potential for small populations to yield robust and useful information despite sample size constraints.

Herpetologica

Estimating superpopulation size and annual probability of breeding for pond-breeding salamanders

It has long been accepted that amphibians can skip breeding in any given year, and environmental conditions act as a cue for breeding. In this paper, we quantify temporary emigration or nonbreeding probability for mole and spotted salamanders (Ambystoma talpoideum and A. maculatum). We estimated that 70% of mole salamanders may skip breeding during an average rainfall year and 90% may skip during a drought year. Spotted salamanders may be more likely to breed, with only 17% avoiding the breeding pond during an average rainfall year. We illustrate how superpopulations can be estimated using temporary emigration probability estimates. The superpopulation is the total number of salamanders associated with a given breeding pond. Although most salamanders stay within a certain distance of a breeding pond for the majority of their life spans, it is difficult to determine true overall population sizes for a given site if animals are only captured during a brief time frame each year with some animals unavailable for capture at any time during a given year. ?? 2007 by The Herpetologists' League, Inc.

Herpetologica

Where has turtle ecology been, and where is it going?

Over 9000 articles have been published on turtles and tortoises (excluding sea turtles) since 1950 according to the Web of Science, including over 8000 contained in a personal bibliography that we analyze in this paper. Research had a slow start from 1900 to 1950, with mostly anecdotal additions to our knowledge until the contributions of F. Cagle and A. Carr took turtle research to new levels as the cofathers of turtle ecology in the middle of the last century. Books written in 1939, 1952, and 1972 that compiled existing literature on turtles in the United States and Canada set the stage for growing interest in turtles. The first global compilation of turtle species did not become available until 1961. Publication frequency increased in the 1960s and especially the 1970s as interest in turtles grew, and a wave of turtle biologists emerged from doctoral degree programs. We briefly review the contributions of scientists who published extensively on turtle ecology in those and later decades up to the present. We also review advances in our knowledge of various topics, including the global distribution of turtle research efforts; changes in our perceptions of turtle species diversity over time; turtle community ecology; sex ratios, sex-determination, and climate change; overwintering behavior; sexual size dimorphism and sexual dichromatism; analyses of population genetics; turtles and vocalization; and the emergence of turtle conservation biology efforts. We conclude with a discussion of future opportunities and challenges for working with turtles.

Herpetologica

A synthesis of evidence of drivers of amphibian declines

Early calls for robust long-term time series of amphibian population data, stemming from discussion following the first World Congress of Herpetology, are now being realized after 25 yr of focused research. Inference from individual studies and locations have contributed to a basic consensus on drivers of amphibian declines. Until recently there were no large-scale syntheses of long-term time series data to test hypotheses about the generality of factors driving population dynamics at broad spatial scales. Through the U.S. Geological Survey's Powell Center for Analysis and Synthesis, we brought together a group of scientists to elucidate mechanisms underlying amphibian declines in North America and Europe. We used time series of field data collected across dozens of study areas to make inferences with these combined data using hierarchical and spatial models. We bring together results from four syntheses of these data to summarize our state of knowledge of amphibian declines, identify commonalities that suggest further avenues of study, and suggest a way forward in addressing amphibian declines—by looking beyond specific drivers to how to achieve stability in remaining populations. The common thread of the syntheses is that declines are real but not ubiquitous, and that multiple factors drive declines but the relative importance of each factor varies among species, populations, and regions. We also found that climate is an important driver of amphibian population dynamics. However, the direction and magnitude of sensitivity to change vary among species in ways unlikely to explain overall rates of decline. Thirty years after the initial identification of a major catastrophe for global biodiversity, the scientific community has empirically demonstrated the reality of the problem, identified putative causes, provided evidence of their impacts, invested in broader-scale actions, and attempted meta-analyses to search out global drivers. We suggest an approach that focuses on key demographic rates that may improve amphibian population trends at multiple sites across the landscape.

Herpetologica

Effects of snowpack, temperature, and disease on the demography of a wild population of amphibians

Understanding the demographic consequences of interactions among pathogens, hosts, and weather conditions is critical in determining how amphibian populations respond to disease and in identifying site-specific conservation actions that can be developed to bolster persistence of amphibian populations. We investigated population dynamics in Boreal Toads ( Anaxyrus boreas ) relative to abiotic (fall temperatures and snowpack) and biotic (the abundance of another anuran host and disease) characteristics of the local environment in Wyoming, USA. We used capture–recapture data and a multistate model where state was treated as a hidden Markov process to incorporate disease state uncertainty and assess our a priori hypotheses. Our results indicated that snowpack during the coldest week of winter is more influential to toad survival, disease transition probabilities, and the population-level prevalence of the amphibian chytrid fungus ( Batrachochytrium dendrobatidis ) in the spring, than temperatures in the fall or the presence of another host. As hypothesized, apparent survival at low (i.e., <25 cm) snowpack (0.22; confidence interval [CI] = 0.15–0.31) was lower than apparent survival at high snowpack (90.65; CI = 0.50–0.78). Our findings highlight the potential for local environmental factors, like snowpack, to influence disease and host persistence, and demonstrate the ecological complexity of disease effects on population demography in natural environments. This work further emphasizes the need for improved understanding of how climate change may influence the relationships among pathogens, hosts, and their environment for wild animal populations challenged by disease.

Wyoming

Informing amphibian conservation efforts with abundance-based metapopulation models

Science-based management strategies are needed to halt or reverse the global decline of amphibians. In many cases, sound management requires reliable models built using monitoring data. Historically, monitoring and statistical modeling efforts have focused on estimating occupancy using detection–nondetection data. Spatial occupancy models are useful for studying colonization–extinction dynamics, but richer insights can be gained from estimating abundance and density-dependent demographic rates. We developed an integrated abundance-based metapopulation model of the processes contributing to spatiotemporal variation in patch population density. We fit our model to a combination of detection–nondetection and count data from a 14-yr study of a reintroduced metapopulation of federally threatened Chiricahua Leopard Frogs (Lithobates chiricahuensis). Pond-specific population growth rate was influenced by pond hydroperiod and frog density, such that permanent and semipermanent ponds with low densities of adult frogs experienced the highest annual population growth rates. Immigration rate declined as the distance among ponds increased. After reintroduction in 2003, metapopulation-level abundance increased and appeared to stabilize around 1300 adult frogs (95% CI = 1192–1471) by year 2015. Further, changes in metapopulation abundance were driven mostly by changes in abundance at a few ponds. These high-density populations, which would not have been identifiable with traditional occupancy-based metapopulation models, are likely especially important for species recovery in the area. Abundance-based metapopulation models can be widely applied to inform conservation efforts, by providing higher quality information needed to prioritize habitat patches for management and can be used to make more accurate predictions of metapopulation extinction risk.

Herpetologica

Divergence among barking frogs ( Eleutherodactylus augusti ) in the southwestern United States

Barking frogs ( Eleutherodactylus augusti ) are distributed from southern Mexico along the Sierra Madre Occidental into Arizona and the Sierra Madre Oriental into Texas and New Mexico. Barking frogs in Arizona and most of Texas live in rocky areas in oak woodland, while those in New Mexico and far western Texas live in rodent burrows in desertscrub. Barking frogs in each of the three states have distinct coloration and differ in sexually dimorphic characters, female vocalization, and skin toxicity. We analyzed advertisement call variation and conducted a phylogenetic analysis using mitochondrial DNA sequences (ND2 and tRNA regions) for barking frogs from these three states. Advertisement calls of frogs from Arizona were significantly longer in duration, higher in frequency, and had longer duration pulses than those of frogs from either New Mexico or Texas; frogs from these latter two sites were indistinguishable in these call variables. Phylogenetic analysis showed deep divisions among barking frogs from the three states. Differences in call structure, coloration, and mitochondrial DNA sequences strongly suggest that barking frogs in Arizona are reproductively isolated from those in New Mexico and Texas. Our results indicate that either northern populations are connected via gene flow through southern Mexico (i.e., they are subspecies as currently recognized), or represent independent lineages as originally described (i.e., western barking frogs, E. cactorum in AZ, and the eastern barking frogs, E. latrans in NM, TX).

Arizona, New Mexico, Texas

Phylogeography and genetic identification of the newly-discovered populations of torrent salamanders (Rhyacotriton cascade and R. variegatus) in the central Cascades (USA)

Newly discovered populations of Rhyacotritonidae were investigated for taxonomic identity, hybridization, and sympatry. Species in the genus Rhyacotriton have been historically difficult to identify using morphological characters. Mitochondrial (mtDNA) 16S ribosomal RNA sequences (491 bp) and allozymes (6 loci) were used to identify the distribution of populations occurring intermediate between the previously described ranges of R. variegatus and R. cascadae in the central Cascade Mountain region of Oregon. Allozyme and mitochondrial sequence data both indicated the presence of two distinct evolutionary lineages, with each lineage corresponding to the allopatric distribution of R. cascadae and R. variegatus . Results suggest the Willamette River acts as a phylogeographic barrier limiting the distribution of both species, although we cannot exclude the possibility that reproductive isolation also exists that reinforces species' distributions. This study extends the previously described geographical ranges of both R. cascadae and R. variegatus and defines an eastern range limit for R. variegatus conservation efforts.

Washington

Behavior of amphibians on the road in response to car traffic

Nocturnal car traffic often results in amphibian casualties, especially during rainy nights. The behavior of amphibians presumably influences their vulnerability to mortality on the road, but this hypothesis remains untested. We investigated the behavioral response of individuals of six species of amphibians on roads when confronted by an approaching vehicle. We first conducted a field study consisting of 50 night-driving surveys over 4 yr during which we recorded the behavior (i.e., moving or immobile) of frogs, toads, tree frogs, and salamanders encountered on a 20-km stretch of road. In an effort to tease apart the effects of headlights and the sound of motors on amphibian behavior, we carried out a field experiment on a test road where we exposed individuals to different car-associated stimuli. Here, we tested the hypothesis that simultaneous exposure to headlights and the sound of a car motor would elicit a stronger response than exposure to a single stimulus or a control. Based on the observations of the 2767 individuals in the field survey, immobility was the most common response to the approach of a car (mean probability of 0.82 of remaining immobile); the response differed across species but depended on the season of the survey (May-June vs. July-September). Similarly, the 91 individuals included in the field experiment were more likely to move during the control treatment than during any of the car-associated treatments. The combined stimuli elicited the strongest response, followed by the headlights-only and the motor-only treatments. Spring peepers (Pseudacris crucifer) tended to move more often than the other species we tested in the field experiment, which suggests they spend less time on the road and are less vulnerable to traffic mortality than other species. Both the field survey and field experiment consistently indicated that amphibians tend to remain immobile at the approach of a vehicle. This behavior highlights the vulnerability of amphibians to road traffic and should be considered in measures to mitigate road impacts. ?? 2005 by The Herpetologists' League, Inc.

Herpetologica

Survival of radio-implanted drymarchon couperi (Eastern Indigo Snake) in relation to body size and sex

Drymarchon couperi (eastern indigo snake) has experienced population declines across its range primarily as a result of extensive habitat loss, fragmentation, and degradation. Conservation efforts for D. couperi have been hindered, in part, because of informational gaps regarding the species, including a lack of data on population ecology and estimates of demographic parameters such as survival. We conducted a 2- year radiotelemetry study of D. couperi on Fort Stewart Military Reservation and adjacent private lands located in southeastern Georgia to assess individual characteristics associated with probability of survival. We used known-fate modeling to estimate survival, and an information-theoretic approach, based on a priori hypotheses, to examine intraspecific differences in survival probabilities relative to individual covariates (sex, size, size standardized by sex, and overwintering location). Annual survival in 2003 and 2004 was 0.89 (95% CI = 0.73-0.97, n = 25) and 0.72 (95% CI = 0.52-0.86; n = 27), respectively. Results indicated that body size, standardized by sex, was the most important covariate determining survival of adult D. couperi, suggesting lower survival for larger individuals within each sex. We are uncertain of the mechanisms underlying this result, but possibilities may include greater resource needs for larger individuals within each sex, necessitating larger or more frequent movements, or a population with older individuals. Our results may also have been influenced by analysis limitations because of sample size, other sources of individual variation, or environmental conditions. ?? 2009 by The Herpetologists' League, Inc.

Herpetologica

Optimizing walking pace to maximize snake detection rate: A visual encounter survey experiment

Visual encounter survey efforts can be defined and constrained by duration, distance, or both duration and distance simultaneously. This study examines the optimal walking pace that will maximize the number of animal detections within a limited time frame. We predicted that animal sighting rate per unit of distance would decline with increasing pace, but that maximal sighting rate per unit of time would occur at some intermediate pace because walking faster means covering more ground and passing more animals that could potentially be detected. We conducted a controlled experiment during which we searched for Brown Treesnakes ( Boiga irregularis ) while walking 220-m-long transects at three different speeds. For transects inside the forest, detection rate per unit distance decreased (nonlinearly) with increasing pace. When considering catch per unit time, however, we found 5% more snakes at the medium pace compared with the slow pace, and 63% more snakes at the fast pace compared with the slow pace. The pattern appeared different for surveys along forest edges with higher vegetation density, in which snakes might be more difficult to spot. Surprisingly, pace had no detectable effect on the body sizes or perch heights of snakes successfully detected. Finding the optimal search pace for a particular study organism in a focal habitat has the potential to substantially increase survey cost-efficacy.

Herpetologica

Sexual dimorphism and feeding ecology of Diamond-backed Terrapins ( Malaclemys terrapin )

Natural and sexual selection are frequently invoked as causes of sexual size dimorphism in animals. Many species of turtles, including the Diamond-backed Terrapin (Malaclemys terrapin), exhibit sexual dimorphism in body size, possibly enabling the sexes to exploit different resources and reduce intraspecific competition. Female terrapins not only have larger body sizes but also disproportionately larger skulls and jaws relative to males. To better understand the relationship between skull morphology and terrapin feeding ecology, we measured the in-lever to out-lever ratios of 27 male and 33 female terrapin jaws to evaluate biomechanics of the trophic apparatus. In addition, we measured prey handling times by feeding Fiddler Crabs (Uca pugnax), a natural prey item, to 24 terrapins in the laboratory. Our results indicate that although females have disproportionately larger heads, they have similar in:out lever ratios to males, suggesting that differences in adductor muscle mass are more important in determining bite force than jaw in:out lever ratios. Females also had considerably reduced prey handling times. Understanding the factors affecting terrapin feeding ecology can illuminate the potential roles male and female terrapins play as top-down predators that regulate grazing of Periwinkle Snails (Littorina irrorata) on Cord Grass (Spartina alterniflora).

Herpetologica

Mortality of American alligators attributed to cannibalism

Mortality of juvenile (<122 cm total length; TL) American Alligators ( Alligator mississippiensis ) attributed to cannibalism on Orange Lake, Florida was examined. Alligator web tags used in mark&ndash;recapture studies were found in 12% of 267 stomachs sampled from alligators &ge;168 cm TL. Captive alligators retained 76% of force-fed tags during a 588-d tag-retention trial. Models relating the probability of tag recovery to the annual probabilities of juvenile survival, cannibalism, tag retention, adult survival, and adult harvest suggested that cannibalism may on average remove 6&ndash;7% of the juvenile alligator population annually. Vulnerability continued to 140 cm TL (age 6&ndash;8 yr). Cannibalism of juveniles may serve to regulate the alligator population on Orange Lake. Alligator cannibalism may vary widely among populations, depending on demography and environmental conditions. The role and importance of cannibalism in alligator population dynamics should be more fully assessed and environmental and population factors that influence cannibalism identified to better evaluate management programs.

Florida