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My research on anurans has been diverse: biogeography, speciation, acoustics, polyandry, sperm competition, and conservation. My interests in biology started in natural history but, in the late 1960s as an undergraduate student, I was receptive to emerging new ideas in biogeography and evolutionary biology: continental drift and neutral theory. My focus in this “Perspective” is an explanation of how diversity has evolved in the frog fauna of southwestern Australia, where I have worked since 1978. I discuss the roles of range fragmentation, genetic drift, directional sexual selection, polyploidy, and simultaneous polyandry as processes driving the evolution of diversity in the sometimes-bizarre frog fauna of southwestern Australia. I identify features that can characterize polyandrous anurans: e.g., large testes, sperm morphology, and, possibly, complex calls with an example of the latter in Geocrinia leai. I discuss how current anuran life histories vary across rainfall and temperature gradients and how derivation of more-arid adapted forms is a well-defined historic biogeographic pattern in southwestern Australia. My observations over time leave me cautiously optimistic about the prospects for frogs affected by global warming.
Taylor L. Cooper, Caroline L. Zabinski, Emily J. Adams, Savannah M. Berry, Juanita Pardo-Sanchez, Emma M. Reinhardt, Katherine M. Roberts, Julia Watzek, Sarah F. Brosnan, Robert L. Hill, Emily G. Weigel, Joseph R. Mendelson III
Procedural memory allows animals to solve previously encountered tasks over weeks, months, or years efficiently. Although thoroughly documented in vertebrate clades such as mammals and birds, studies of procedural memory in squamate reptiles are lacking. Filling the gap in knowledge regarding procedural memory in squamates is important to understanding the degree to which procedural memory is unique to birds and mammals, as it is related to their unique cognitive abilities. We tested for memory of a problem-solving task in two species of monitor lizard (Varanus spp.) and a beaded lizard (Heloderma sp.) after a 20-mo hiatus in exposure, representing approximately 25% of their ages at the time of testing. All the monitor lizards had lower initial latencies to solve the task upon re-exposure posthiatus than they had as naïve individuals during the prehiatus trials and reached minimum latencies in fewer trials than when previously tested. Our results indicate procedural memory of puzzle-solving behaviors on the time scales of years. Our results add to an emerging literature suggesting that squamate and other nonavian reptiles share a number of cognitive traits with birds and mammals, suggesting that such traits are far more widespread across taxa than previously recognized. We also discuss a framework for studying cognition in squamates that would allow tests of cognition across a great diversity of body forms and ecologies.
Pesticides have been identified as one of the major reasons for the worldwide decline of amphibian populations. In terms of aquatic amphibian exposure, most ecotoxicological studies concentrate on testing tadpoles in Gosner stage (GS) 25. To examine the representativeness of GS25, we exposed five aquatic stages of European common frogs (Rana temporaria) to the viticultural fungicide folpet (Folpan® 80 WDG) in a dose–response setup. The 96-h mortality data identified the hatchling stage GS20 as the most sensitive aquatic stage (LC50 of GS15: 2.68 mg/L, GS20: 1.01 mg/L, GS25: 1.22 mg/L, GS36: 2.11 mg/L, GS42: > 2.6 mg/L). Because these results suggest that the commonly used stage is not sufficient for a protective environmental risk assessment of pesticides, comprehensive investigations are needed to provide adequate regulatory guidance.
Infectious pathogens threaten wildlife populations through effects on host growth, reproduction, and survival. The amphibian chytrid fungus Batrachochytrium dendrobatidis (Bd), the cause of the disease chytridiomycosis, has been implicated in worldwide declines of amphibian populations. Documenting conditions under which amphibians are threatened by Bd will allow us to pinpoint at-risk populations, especially in the midwestern United States, an understudied region. We investigated how distributions of Bd differ across host life stages, land cover types, and spatial extents in a susceptible temperate host, the American Toad (Anaxyrus americanus). We surveyed a total of 232 adults at 14 sites and 430 metamorphs at 15 sites in southwestern Ohio, USA, and analyzed associations among land use type, Bd prevalence, and Bd load by using model selection. We found Bd infection prevalence in metamorphs was dramatically lower than in adults; only 1.6% of metamorphs were infected compared with 28.0% of adults. These results suggest that Bd transmission occurs after metamorphosis in this species or that infections vary with season, given that we surveyed adults in the spring during breeding events and metamorphs in the summer as they emerged from ponds. In adults, infection prevalence was reduced with increasing open-canopy habitats across spatial scales (from 100 to 1,000 m), whereas infection load increased with the proportion of forested habitats at small spatial scales (100 m). Our study shows that Bd infection risk in a temperate system can be influenced by host life stage and land cover types across local spatial scales.
The natural histories of parasites and their hosts are intertwined, and intensity of parasitism depends on parasite abundance and host behavior as well as potential effects of sex/age. To characterize potential effects of parasite abundance and host sex/ age on chigger mite (Eutrombicula alfreddugesi) ectoparasitism on Eastern Fence Lizards (Sceloporus undulatus), we measured 1) the abundance of mites in the environment as well as mite load and prevalence on lizards throughout the activity season, 2) sex- and age-specific patterns of ectoparasitism, and 3) week-to-week consistency of mite loads on lizards. Environmental mite abundance varied seasonally in close association with mean monthly temperatures and was the main driver of pronounced seasonal variation in mite loads on lizards. Mite loads were almost always higher on yearlings than on adults and, somewhat unexpectedly, were never higher on adult males than any of the other age-sex classes. As adults, females had higher mite loads than did males in June–July, but as yearlings, males had higher mite loads than did females in July–September. Despite considerable week-to-week variation, rank-ordering of lizard mite loads was highly consistent. These findings indicate that 1) consistent, age-specific sex biases are superimposed on strong seasonal variation in mite loads, and 2) detrimental effects of mites are expected to be consistently stronger in some individuals than in others.
Males tend to experience higher rates of parasitism compared to females, a phenomenon associated with ecological factors, the fact that males engage in risky behaviors, and because testosterone is known to be immunosuppressive. However, females could experience higher rates of parasitism if energy is allocated from costly immune responses towards producing eggs. We used pooled data sets from laboratory experiments to investigate sex-specific differences in salamander (Plethodon cinereus) resistance to the emerging fungal pathogen Batrachochytrium dendrobatidis (“Bd”). Contrary to our predictions, we found that female salamanders had a higher prevalence of infection (∼56%) and carried a higher Bd infection burden (455 zoospores equivalents per sample) compared to male salamanders (which had a Bd infection prevalence of ∼24% and an average infection burden of 58 zoospore equivalents per sample). We also found that female reproductive investment (i.e., mass of eggs) positively correlated with Bd infection burden, suggesting that females who previously invested more into reproduction carried a higher Bd infection burden. Collectively, our findings might indicate that female salamanders experience a cost of reproduction in the form of decreased disease resistance.
For many amphibian species of conservation concern, our understanding of drivers of distribution and abundance are based on data collected at only a few localities. Thus, landscape-scale efforts are needed to better inform management and species conservation. The Streamside Salamander (Ambystoma barbouri) is a global conservation priority because of its restricted geographic distribution and presumed sensitivity to forest loss, yet landscape-scale studies have not occurred. We surveyed a 16-county area in Kentucky (USA) and examined the influence of catchment (forest, agriculture, and urban) and local-scale (water chemistry and sunfish presence) variables on A. barbouri occupancy and abundance. We sampled 80 streams across different land cover types (i.e., 30 agriculture, 34 forested, and 16 urban) over 2 yrs (2017–2018). Within these streams, we identified 56 new localities. Estimated mean occupancy (Ψ = 0.91; credible interval [CI] = 0.76–0.99) was high. Streams with the highest estimated abundances were those without sunfish and containing >50% forested or agricultural land cover within their catchments; urban streams had the lowest estimated abundances. At sites where we did not detect sunfish, there were an estimated 35.25 (95% CI = 32.04–38.67) A. barbouri individuals per 10 m in forested sites, 22.47 (95% CI = 19.86–25.14) in agricultural sites, and 0.66 (95% CI = 0.14–1.59) in urban sites. Water chemistry varied across site types; however, only maximum sodium (β = –0.51, 95% CI = –0.58 to –0.43) was associated with A. barbouri abundance. If managing this species becomes necessary, minimizing urban development within low-order stream catchments should be a priority.
To mitigate habitat loss and increase the reproductive success of threatened Bog Turtles (Glyptemys muhlenbergii), managers often improve or restore open-canopy nesting habitats within or adjacent to occupied habitat. Restoring nesting habitat, however, does not guarantee that Bog Turtles will use these restored habitats; inertial mechanisms such as nest-site fidelity and natal homing may prevent female Bog Turtles from discovering and using restored habitats for many years or even generations. The objective of this study was to improve understanding of the role behavioral inertia may play in female Bog Turtle nest-site selection. From 2008 to 2012, at nine fens in New York and Massachusetts, we compared the average distance between previous and subsequent nests with null distributions assuming no nest-site fidelity. We also assessed whether pairwise genetic relatedness of nesting females was positively associated with geographic distance between nests. We found evidence for strong but incomplete fidelity to nesting-habitat patches within a wetland, likely driven by behavioral inertia. Individuals nesting closer together were not more closely related, and first-degree female relatives did not consistently nest within the same nesting-habitat patch, suggesting that Bog Turtles do not exhibit natal homing. Our results suggest that Bog Turtle populations may be slow to respond to newly restored nesting areas because of behavior inertia. However, testing this hypothesis will require long-term monitoring of habitat-restoration efforts coupled with further investigations of Bog Turtle nest-site selection.
The Golden Mantella (Mantella aurantiaca) is a highly threatened frog species found in east-central Madagascar. They are seasonally active and difficult to observe outside the summer breeding season. We used a captive population maintained within the native range of the species to examine two aspects of life history that otherwise would be impracticable to observe in the field: sheltering behavior and nearest neighbor distance (NND). We made weekly observations on seven groups of frogs for 1 yr, recording NND of each individual and how many individuals were sheltering under cover. We also recorded whether eggs were present in terraria to better define the breeding season and determine how time of year relates to NND and sheltering behavior. Frogs were closer together and more often took shelter during cool winter months. This corresponds to the time of year when fewer egg clutches were recorded. There was no difference between NND and sheltering behavior in wild-caught vs. captive-bred frogs, and there was no significant difference between NND of males and females. Golden Mantellas may be at increased risk from infectious diseases because behavior that increases contact between infected individuals can facilitate disease transmission.
G. C. dos Santos Oliveira, G. Corso, D. M. Medeiros, I. De Mendonça Silva, A. J. B. Santos, M. F. Nakamura, H. M. de Aquino Carmo, G. Z. dos Santos Lima
We studied the nesting behavior of the Hawksbill Turtle (Eretmochelys imbricata) along the northeastern coast of Brazil, specifically in southern Rio Grande do Norte. We compare the peak of nesting activity for several seasons from 2006 to 2016. The raw data consist of daily records of the presence of hawksbill turtle on a beach (N = 3,717). In the statistical analysis, we construct a cumulative sum of data and perform a logistic fitting. Furthermore, we use the derivative of the fitting to find the peak of nesting season. We observed a drift in the oviposition peak of the Hawksbill Turtle. In addition, the peak of maximal sea surface temperature in the nesting area followed a similar drift. The results suggest that the Hawksbill Turtle population has been responding to warming environmental changes.
Intraspecific color pattern polymorphism (CPP) is widely documented in squamate reptiles and thought to contribute to fitness advantages. Dimorphic striped/spotted CPPs (color pattern dimorphisms [CPDs]) are well characterized among colubrid snakes but are apparently rare among macrostoman lineages. Turks and Caicos Boas (Chilabothrus chrysogaster chrysogaster) are the only booids (superfamily Booidea) known to exhibit a dimorphic striped/spotted CPD within a single population. Based on examination of 737 live wild specimens observed over 12 yr within a population of boas on Big Ambergris Cay, Turks and Caicos Islands, we characterized the striped/spotted CPD and examined potential morphological and spatial correlates of this pattern dimorphism. Contrary to predictions based on studies of similar CPD in colubrid snakes, we found no association between striped or spotted morphs and sex, age, size, or potential morphological correlates. We show that, on average, 15% of the individuals in this population are striped during any given year and that the relative frequency of striped individuals does not appear to change through time, suggesting that the relative frequencies of this polymorphism are stable in this population. Spatial correlation analyses suggested that the striped morph is under-dispersed relative to the spotted morph on Big Ambergris Cay, which might be a product of limited postnatal dispersal or differential habitat preferences. Finally, we described a continuum of color-by-pattern morphs within each pattern class (striped/spotted) in this subspecies which represents a much broader range of color and pattern variation in this species than has been previously recognized.
An organism's thermal limits provide valuable insights into species distributions and potential climate change impacts. The critical thermal maximum (CTmax) in particular has been widely used for among-species analyses of thermal tolerances. However, CTmax measurements can depend on important context-dependencies, including acclimation temperature and experimental procedure. We investigated acclimation effects on CTmax in two amphibian species commonly used as laboratory models, Ambystoma mexicanum (Axolotls) and Xenopus laevis (African Clawed Frogs), using the standard dynamic method. Both species exhibited an increased CTmax following acclimation to a warm temperature (24°C) relative to cold acclimation (8°C). We also found that warm-temperature acclimation resulted in significant mass losses in both species, possibly reflecting metabolic costs of living at higher temperatures. Our CTmax measurements for A. mexicanum were consistent with CTmax measurements for closely related salamander species, but CTmax measurements for cold-acclimated X. laevis were inconsistent with a prior study of this species. This might have been because of the earlier study employing a less common curve-fitting method to estimate CTmax. These results highlight the importance of accounting for recent acclimation temperatures when estimating amphibian thermal limits and provide further support for the generalization that most amphibian species exhibit increased CTmax following warm-temperature acclimation.
Male Anolis lizards display their colorful dewlaps in a variety of contexts, ranging from long-distance territorial displays to close-range agonistic and courtship displays. Anoles have eyes of high optical quality and a retina that contains tightly spaced, small-diameter photoreceptors. Highest visual acuity is associated with the center of the retina (=12.5 cycles o-1), whereas acuity is much lower in the periphery. Anoles possess a small eye that creates a small retinal image, which limits their maximum visual spatial acuity to approximately 1/10 that of humans. In animal visual systems spatial resolution falls rapidly with distance from the stimulus. In some species, dewlap color patterns are fairly complex and may transmit various kinds of information. To gain insight into the visual information that conspecifics can potentially extract from dewlap color patterns, we modified high-resolution digital photographs reflecting the limits imposed by the acuity of the Anolis eye. For central retinal vision, from a distance of 0.5 m or less, the finest levels of dewlap pattern spatial detail were visible. At greater distances, and/or for peripheral vision, much less detail could be resolved. When viewed from 1 m away with peripheral vision, only the average color of the large patches could be detected, and all pattern detail was lost. The potential information content of the dewlap patterns changes dramatically with the context in which it is viewed. We show that a clear knowledge of an animal's sensory limitations can lead to greatly improved hypotheses about signal function.
Strawberry Poison Frogs (Oophaga pumilio) are common members of leaf litter lowland communities in Central America and exhibit several color morphs throughout their distribution. Color plays a determinant role during intra- and intermorph interactions in many insular populations, but little is known about the variation and perception of visual signals in mainland populations. In this study, we investigated color variation of four body parts—head, back, belly, and throat—in a bright red O. pumilio population of northeastern Costa Rica. We incorporated frog- and bird-specific visual modeling to evaluate the differences in color and brightness between the sexes, from the perspective of conspecifics and avian predators. Furthermore, we measured the color and brightness contrast against natural backgrounds commonly used by these frogs to forage and patrol within territories. Our results revealed that, from the perspective of conspecifics, there is no dichromatism between males and females. However, females had a greater contrast against green and brown backgrounds than males. The bird visual models indicated that males and females are highly conspicuous against common background substrates but that females are easier to detect than males. This study detailing color variants between sexes within a mainland population of O. pumilio contributes to our understanding of color differences in populations of this species.
Pulchrana rawa is a peat swamp specialist that was described from eastern Sumatra in 2012 based on a single specimen. Since then, no confirmed records have been forthcoming; thus, virtually nothing is known about this species. Recent fieldwork at peat swamp forests in southwestern Peninsular Malaysia led to the discovery of a frog that morphologically resembled P. rawa. Despite having relatively high mitochondrial divergence (6.6%) that was consistent with interspecific divergences of other closely related species, results from species delimitation analyses indicated that the Malaysian specimen was conspecific with P. rawa. In addition to extending the geographic distribution of this species to a different country, we also provide the first quantitative characterization of its call. This study provides novel insights into the distribution and natural history of this enigmatic species that will inevitably aid in threat assessments and conservation efforts.
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