The palatability of Neotropical poison frogs in predator‐prey systems: do alkaloids make the difference?

Neotropical poison frogs sequester alkaloid‐based chemical defenses from their diet, which seem to repel invertebrate predators after contact. In this study, we tested the reaction of predatory ants toward skin secretions of captive‐bred poison frogs without alkaloids. Although the secretions had a smell and taste similar to those of wild‐caught frogs, the ants did not avoid them, but actually preferred them. We infer that amphibian secretions are attractive to invertebrate predators (probably due to palatable nutritive components), but that this attraction is overridden when unpalatable alkaloids are present.     

Experimental transmission of cutaneous chytridiomycosis in dendrobatid frogs

In a series of three experiments during March-October, 1998, two species of captive-bred poison dart frogs (Dendrobates tinctorius and D. auratus) were exposed to Batrachochytrium dendrobatidis, a recently-described chytridiomycete fungus (chytrid) that was originally isolated from a blue poison dart frog (D. azureus). All frogs exposed to the chytrids developed a fatal skin disease, whereas none of the control frogs developed skin lesions. The most consistent clinical sign in chytrid-exposed frogs was excessive shedding of skin. Gross lesions were subtle, usually affected the legs and ventrum, and consisted of mild skin thickening and discoloration. Microscopic examination of shed skin pieces and/or skin imprints demonstrated the presence of chytrids and was used for ante mortem and post mortem confirmation of chytrid infection. Histologically, there was epidermal hyperkeratosis, hyperplasia, and hypertrophy associated with low to moderate numbers of chytrids in the keratinized layers. These experiments demonstrated that Batrachochytrium dendrobatidis can be a fatal pathogen in poison dart frogs. The experimentally-induced disease in these frogs resembled cases of cutaneous chytridiomycosis that have recently been described in several other species of captive and wild amphibians.     

Batrachochytrium dendrobatidis in Darwin's frog Rhinoderma spp. in Chile

The presence of the chytrid fungus Batrachochytrium dendrobatidis in Chile was evaluated in 2 endangered frog species of the genus Rhinoderma. Specimens from a captive rearing facility, wild populations and preserved collection material were analyzed using histological and molecular techniques. The fungus was identified in the rearing facility and in wild populations, but not in the archived frogs. This study confirms, for first time, the presence of chytridiomycosis in Rhinoderma darwinii in Chile.     

Development of restoration techniques for Hawaiian thrushes: Collection of wild eggs,artificial incubation,hand‐rearing,captive‐breeding,and re‐introduction to the wild

From 1995 to 1999, two species of endemic Hawaiian thrushes, `Oma`o (Myadestes obscurus) and Puaiohi (M. palmeri), were captive‐reared and re‐introduced into their historic range in Hawai`i by The Peregrine Fund, in collaboration with the U.S. Geological Survey–Biological Resources Division (BRD) and the Hawai`i State Department of Land and Natural Resources. This paper describes the management techniques that were developed (collection of wild eggs, artificial incubation, hand‐rearing, captive propagation, and release) with the non‐endangered surrogate species, the `Oma`o; techniques that are now being used for recovery of the endangered Puaiohi. In 1995 and 1996, 29 viable `Oma`o eggs were collected from the wild. Of 27 chicks hatched, 25 were hand‐reared and released into Pu`u Wa`awa`a Wildlife Reserve. Using the techniques developed for the `Oma`o, a captive propagation and release program was initiated in 1996 to aid the recovery of the endangered Puaiohi. Fifteen viable Puaiohi eggs were collected from the wild (1996–1997) to establish a captive breeding flock to produce birds for re‐introduction. These Puaiohi reproduced for the first time in captivity in 1998 (total Puaiohi chicks reared in captivity 1996–1998 = 41). In 1999, 14 captive‐bred Puaiohi were re‐introduced into the Alaka`i Swamp, Kaua`i. These captive‐bred birds reproduced and fledged seven chicks in the wild after release. This is the first endangered passerine recovery program using this broad spectrum of management techniques (collection of wild eggs, artificial incubation, hand‐rearing, captive‐breeding, and release) in which re‐introduced birds survived and bred in the wild. Long‐term population monitoring will be published separately [BRD, in preparation]. Zoo Biol 19:263–277, 2000. © 2000 Wiley‐Liss, Inc.     

A study of ovarian follicular kinetics, oviduct, fat body, and liver mass cycles in laboratory-maintained Rana cyanophlyctis in comparison with wild-caught frogs.

Ovarian follicular dynamics and fluctuations in fat body, oviducal, and liver masses were studied in captive Rana cyanophlyctis in comparison with wild-caught frogs, sampled at monthly intervals over a period of 12 months. In both the captive and wild-caught frogs first growth phase (FGP) and second growth phase (SGP) or vitellogenic oocytes were produced throughout the period examined; however, changes in ovarian and oviducal weights were less marked in the former group. In the captive frogs SGP oocyte production was reduced by 50%, and, maximum ovarian weight and SGP oocyte number were attained 2-3 months earlier than in wild-caught controls. The FGP oocyte pool in laboratory-maintained frogs, however, was comparable with that of the corresponding wild-caught frogs. Captivity caused a threefold increase in atresia and reduced the number of oocytes reaching SGP. The depletion of fat stores in fat bodies during the later phases of captivity suggests that the deposition of lipids into oocytes (for SGP) was given priority over storage in the fat bodies. The low oviducal weights of captive frogs was correlated with a reduced number of SGP oocytes, which are the source of estrogen. On the other hand, liver weight remained high, indicating adequate hepatic vitellogenin synthesis. Possible reduction in its output was not detected, possibly due to the reduced number of follicles reaching SGP. The findings indicate that stress of captivity decreases gonadotrophins and estrogen levels. Oviducal growth is reduced in captive frogs.(ABSTRACT TRUNCATED AT 250 WORDS)     

Investigating signal modalities of aposematism in a poison frog

Aposematic species combine a conspicuous signal with a secondary defence, the majority of which are studied in the context of a visual signal. While multimodality of the aposematic signal appears to be common in invertebrate species, we know very little about the presence or absence of multimodality in vertebrates. Here, we examine the possibility of multimodality of aposematism in the green-and-black poison frog, Dendrobates auratus. Using a non-visual predator (the cat-eyed snake, Leptodeira annulata) and extractions of chemicals in frog skins, we test whether there is sufficient non-visual information for predators to avoid this aposematic species without using visual cues. We found that experienced predators avoid chemicals in this poison frog's skin by olfactory cues alone in trials with live frogs and extracts from captive poison frogs, whereas extracts from wild poison frogs did not lead to avoidance behaviours in predators. Further, in our limited sampling, naïve predators demonstrate no avoidance. This not only indicates that predators can make informed decisions from the frog's odour, but also indicates that avoidance based on olfactory cue is a learned response.     

Divergence in parental care, habitat selection and larval life history between two species of Peruvian poison frogs: an experimental analysis

Changes in the nature of the ecological resources exploited by a species can lead to the evolution of novel suites of behaviours. We identified a case in which the transition from large pool use to the use of very small breeding pools in neotropical poison frogs (family Dendrobatidae) is associated with the evolution of a suite of behaviours, including biparental care (from uniparental care) and social monogamy (from promiscuity). We manipulated breeding pool size in order to demonstrate experimentally that breeding habitat selection strategy has evolved in concert with changes in parental care and mating system. We also manipulated intra- and interspecific larval interactions to demonstrate that larval adaptation to the use of very small pools for breeding affected the evolution of larval competition and cannibalism. Our results illustrate the intimate connection between breeding pool ecology, parental care and mating strategies in Peruvian poison frogs.     

The cost of polygyny and the evolution of female care in poison frogs

Previous research on a variety of organisms indicates that polygyny can impose a cost on the reproductive success of females. Some authors have hypothesized that this cost may have caused the evolution of female parental care from paternal or biparental care in some lineages, particularly in poison frogs of the genus Dendrobates. In this paper, we evaluate the assumptions and theoretical implications of this hypothesis and present several game-theoretic models that clarify some of the issues. We conclude that a cost of polygyny is unlikely to drive a female care strategy to fixation on its own; however, if caring males suffer a cost of lost mating opportunities then a cost of polygyny may destabilize male care and result in the evolution of uniparental female care. A cost of polygyny on its own may be able to drive a transition from male care to biparental care. We also discuss other factors that may have influenced the evolution of parental care in the poison frogs, including results from recent field and laboratory research, and we evaluate the possibility that female care evolved from biparental, as opposed to male care.     

Amazon poison frogs (Ranitomeya amazonica) use different phytotelm characteristics to determine their suitability for egg and tadpole deposition

Parents have to assess the multivariate characteristics of their reproductive sites to maximize their reproductive success through offspring performance. In addition, they may provide care to ensure optimal performance of their offspring. In poison frogs it has been identified that ecological characteristics of reproductive sites may underlie transitions in the involvement of parental sexes in care for offspring. To elucidate the ecological factors that may drive these transitions, it is important to understand which characteristics poison frogs use to assess the quality of their reproductive site. We studied the use of small water bodies in leaf axils of bromeliads, phytotelmata, for egg and tadpole deposition by Amazon poison frogs (Ranitomeya amazonica). We compared phytotelm quality characteristics for preferred egg and tadpole deposition sites and used two choice tests with plastic cups to study the causal relationship with tadpole deposition for the identified characteristics. The differences among quality characteristics of deposition sites were largest among bromeliad species, and for egg or tadpole deposition different bromeliad species were preferred. However, males were also selective in the leaf axils within a bromeliad species that they used for egg or tadpole deposition. Eggs were deposited in small, resource limited water bodies that were close to the forest floor. Tadpoles were deposited in leaf axils holding resource-rich phytotelmata with larger water volumes. Preference of detritus containing water over clear water in choice tests confirmed that Amazon poison frogs assess quality of their tadpole deposition sites on food availability. We conclude that preference for large water volume and resource rich phytotelmata plays an important role in determining male involvement in parental care and speculate that distribution of preferred resources may bring about selection on female involvement in parental care.     

Conservation of deer: contributions from molecular biology, evolutionary ecology, and reproductive physiology

Molecular phylogenetics, interspecific comparisons, and assisted reproductive techniques are recent approaches to understanding and facilitating conservation of endangered species. This paper reviews the contribution of these approaches to a small but well-studied group of mammals, deer, many of which are endangered in the wild. Conservation efforts require a comprehensive understanding of the biology and history of these animals. The value of assisted reproductive technologies for conservation of deer has received increased awareness especially for captive populations. Such breeding programmes are designed to assist propagation of threatened species and to maximize genetic diversity within populations through the movement of genetic material across the globe, but will only be successful if we understand the genetic and reproductive potential of various lineages. Here we discuss the phylogenetic status of deer, the distinctiveness and evolution of their reproductive patterns, and current approaches for improving the success of controlled breeding programmes for the conservation of endangered lineages. Only by combining both theoretical and practical approaches to conservation efforts can we hope to salvage the remaining organismal diversity of our planet.     

Multivariate species boundaries and conservation of harlequin poison frogs

In this study, we present an iterative method for delimiting species under the general lineage concept (GLC) based on the multivariate clustering of morphological, ecological and genetic data. Our rationale is that distinct multivariate groups correspond to evolutionarily independent metapopulation lineages because they reflect the common signal of different secondary defining properties (environmental and genetic distinctiveness, phenotypic diagnosability, etc.) that imply the existence of barriers preventing or limiting gene exchange. We applied this method to study a group of endangered poison frogs, the Oophaga histrionica complex. In our study case, we used next‐generation targeted amplicon sequencing to obtain a robust genetic data set that we combined with patterns of morphological and ecological features. Our analyses revealed the existence of at least five different species in the histrionica complex (three, new to science), some of them, occurring in small isolated populations outside any protected areas. The lineage delimitation proposed here has important conservation implications as it revealed that some of the Oophaga species should be considered among the most vulnerable of the Neotropical frogs. More broadly, our study exemplifies how multiple‐amplicon and multivariate statistical techniques can be integrated to successfully identify species and their boundaries.     

Use of immunohistochemistry to diagnose chytridiomycosis in dyeing poison dart frogs (Dendrobates tinctorius)

Chytridiomycosis, caused by Batrachochytrium dendrobatidis, is an emerging disease of both wild and captive amphibians, posing a threat to their survival in many parts of the world. As the disease can be difficult to diagnose on routine pathologic sections, the purpose of this study was to develop an additional method for visualization. To accomplish this, immunohistochemical staining was applied to histologic skin sections from four experimentally infected Dyeing poison dart frogs (Dendrobates tinctorius). Staining of the positive tissue sections was distinct and readily visualized, making this technique a valuable ancillary diagnostic test for this important disease.     

Rapid quantitative detection of chytridiomycosis (Batrachochytrium dendrobatidis) in amphibian samples using real-time Taqman PCR assay

Batrachochytrium dendrobatidis is a major pathogen of frogs worldwide, associated with declines in amphibian populations. Diagnosis of chytridiomycosis to date has largely relied upon histological and immunohistochemical examination of toe clips. This technique is invasive and insensitive particularly at early stages of infection when treatment may be possible. We have developed a real-time PCR Taqman assay that can accurately detect and quantify one zoospore in a diagnostic sample. This assay will assist the early detection of B. dendrobatidis in both captive and wild populations, with a high degree of sensitivity and specificity, thus facilitating treatment and protection of endangered populations, monitoring of pristine environments and preventing further global spread via amphibian trade.     

Seasonal behavioral patterns of captive alpine musk deer (<Emphasis Type="Italic">Moschus sifanicus</Emphasis>): Rut and pre-rut comparisons

Alpine musk deer (Moschus sifanicus), well-known for their musk production, are endemic to western China. Due to historical unrestricted illegal hunting and habitat loss, captive farming has been employed as a means of conserving this endangered species and developing sustainable musk harvesting techniques. For captive animals, an understanding of behavioral characteristics is vital to improve management practices. This study addressed a lack of information regarding the behavioral characteristics of alpine musk deer; specifically daily activity patterns in respect to gender and reproductive season. From August 2002 to January 2003, focal sampling was employed to observe 32 adult captive alpine musk deer (13 females and 19 males), at Xinglongshan Musk Deer Farm (XMDF), located at Xinglongshan National Nature Reserve, Gansu Province, China. Results indicated that the general behavioral patterns were similar between female and male captive alpine musk deer throughout both reproductive and non-reproductive seasons (rut and pre-rut season). Both male and female alpine musk deer demonstrated tail-pasting behavior during rut season, a previously male-only behavior trait. Female musk deer also rested comparatively more than males during pre-rut season.     

A captive breeding experiment reveals no evidence of reproductive isolation among lineages of a polytypic poison frog

Reproductive isolation is central to the generation of biodiversity, yet a clear understanding of the contributions of alternative reproductive barriers to this process remains elusive. Studies of young lineages that have diverged in ecologically important traits can offer insights into the chronology and relative importance of various isolating mechanisms during speciation. In poison frogs (Dendrobatidae), within‐species lineages often differ dramatically in coloration, a trait subject to natural and sexual selection. Coloration in the strawberry poison frog (Oophaga pumilio) is particularly diverse and previous work suggests the potential for reproductive isolation. We used a captive breeding experiment to assess the extent of reproductive isolation among three allopatric, genetically distinct O. pumilio lineages that differ in coloration. We compared reproduction of within‐ and between‐lineage pairs, predicting that if lineages are isolated, within‐lineage pairs would be most successful. We also examined the fertility and productivity of F1 backcrosses of admixed offspring. We found no evidence suggesting behavioural pre‐zygotic or post‐zygotic reproductive isolation, indicating that isolation would not be maintained by intrinsic mechanisms in the event of secondary contact. Future work should address costs of between‐lineage matings exerted by extrinsic natural and/or sexual selection against admixed offspring.     

Canopy Closure,Competition, and the Endangered Dusky Gopher Frog

Abstract: A major challenge facing wildlife biologists is understanding why some species go extinct while others persist in the same habitat. To address this question, we investigated whether tree canopy closure over ponds affects growth and survival of rare and common tadpoles within ponds and mediates competitive interactions among species. We conducted 2 experiments to test whether canopy closure and competition may have contributed to the decline of the endangered dusky gopher frog (Rana sevosa), but allowed the persistence of the southern leopard frog (R. sphenocephala). We explored the response of both species to canopy closure in single-species and mixed- (1:1) species treatments of identical total tadpole density. An experiment using aquatic enclosures in temporary ponds showed that canopy closure reduced tadpole growth approximately 20% for both species. Survival of dusky gopher frog tadpoles was higher in mixed-species enclosures than in single-species enclosures. In a complementary experiment using artificial ponds, dusky gopher frogs had lower survival to metamorphosis, reduced size at metamorphosis, and produced a lower total biomass of metamorphosed juveniles in shaded ponds. Southern leopard frogs exhibited reduced body size at metamorphosis only when shaded. These studies suggest that pond canopy closure, not larval competition, may be contributing to the decline of the dusky gopher frog. The different responses to canopy closure suggest a potential mechanism for the loss of dusky gopher frogs and the persistence of southern leopard frogs. Removal of trees from historically open-canopy ponds may help facilitate the recovery of dusky gopher frogs and benefit similar species.     

Development, validation, and application of a urinary relaxin radioimmunoassay for the diagnosis and monitoring of pregnancy in felids

Many nondomestic felids are highly endangered, and captive breeding programs have become essential components of holistic conservation efforts for these species. The ability to diagnose pregnancy early in gestation is fundamental to developing effective breeding programs. The purpose of this study was to develop a radioimmunoassay (RIA) for the detection of urinary relaxin in felids and assess its applicability for early, noninvasive pregnancy diagnosis in domestic cats (Felis silvestris catus) and leopards (Panthera pardus). Urine was collected from pregnant and nonpregnant domestic cats and leopards at mating, and then weekly thereafter for the duration of gestation. Paired serum samples were also collected from the domestic cats. A RIA for relaxin that uses an antiserum against synthetic canine relaxin was validated for felid urine and shown to detect relaxin immunoreactivity in pregnant cat urine subjected to acid-acetone extraction. In the cat, urinary relaxin was first detected between Days 21 and 28 of gestation; levels peaked at 42-49 days, and the concentrations then declined over 2 wk prior to parturition. The urinary relaxin profiles of the cat mirrored those in serum. In the leopard, urinary relaxin was first detected at Day 25-28 of gestation; levels peaked at Day 60-64 and declined in the last 3-4 wk of pregnancy. These results indicate that measurement of urinary relaxin in the cat and leopard provides a reliable method for pregnancy determination from as early as 3-4 wk of gestation. This method of pregnancy diagnosis and monitoring may prove useful in the breeding management of domestic cats and other felid and canid species, and provides a foundation for future studies on pregnancy in captive exotic carnivores.     

Poison frogs rely on experience to find the way home in the rainforest

Among vertebrates, comparable spatial learning abilities have been found in birds, mammals, turtles and fishes, but virtually nothing is known about such abilities in amphibians. Overall, amphibians are the most sedentary vertebrates, but poison frogs (Dendrobatidae) routinely shuttle tadpoles from terrestrial territories to dispersed aquatic deposition sites. We hypothesize that dendrobatid frogs rely on learning for flexible navigation. We tested the role of experience with the local cues for poison frog way-finding by (i) experimentally displacing territorial males of Allobates femoralis over several hundred metres, (ii) using a harmonic direction finder with miniature transponders to track these small frogs, and (iii) using a natural river barrier to separate the translocated frogs from any familiar landmarks. We found that homeward orientation was disrupted by the translocation to the unfamiliar area but frogs translocated over similar distances in their local area showed significant homeward orientation and returned to their territories via a direct path. We suggest that poison frogs rely on spatial learning for way-finding in their local area.     

A preliminary study assessing risk to Tasmanian devils from poisoning for red foxes

The recent introduction of red foxes (Vulpes vulpes) to Australia's island state of Tasmania represents a major threat to native fauna. In response, the Tasmanian government has begun a fox eradication program using Foxoff®, a bait containing the poison sodium monofluoroacetate (commonly known as 1080). The bait is potentially attractive to native Tasmanian carnivores as well as to foxes. Of particular concern is the endangered Tasmanian devil (Sarcophilus harrisii), which is already at risk from an emergent infectious disease, devil facial tumor disease (DFTD). In both a captive and a field study using non-toxic Foxoff bait, we assessed bait palatability and possible effects of demographics, hunger level, bait age, and bait burial method on the likelihood of bait uptake by Tasmanian devils. Captive devils showed varying interest in the bait, but wild devils appeared to find it uniformly palatable. In the captive study, males and younger, captive-born animals were more likely to excavate and remove bait. Subterranean burial at 15 cm was the most effective deterrent to bait excavation; effectiveness decreased at shallower depths and with surface-level bait buried beneath soil mounds. Our findings suggest that the current fox-baiting campaign may negatively impact individual devils. More extensive study is necessary to assess potential risk at the population level. © 2011 The Wildlife Society.     

Putting the Spotlight on Internally Displaced Animals (IDAs): A Survey of Primate Sanctuaries in Africa,Asia, and the Americas

As anthropogenic activity makes deeper incursions into forests, fragmenting habitat, wildlife is forced into closer proximity to humans leading to increased incidences of human–wildlife conflict and wildlife displacement. These same incursions facilitate poaching for the commercial trade in dead and live animals. As a direct result, the number of sanctuaries and internally displaced animals (IDAs) in need of sanctuary placement and rehabilitation are increasing. We focus on internally displaced primates given the prevalence of primate‐focused facilities and anthropomorphic considerations surrounding this taxonomic group. Surveys were distributed globally to map the extent and range of native primate sanctuaries and species. Over 70 facilities care for more than 6,000 native primates comprising 64 species, with almost half listed as endangered or critically endangered. As not all sanctuaries were identified at the time of the survey distribution, we estimate that the actual number of facilities is closer to double this number with a captive population in excess of 10,000 individual primates. Native primate sanctuaries hold significant numbers of primates in long‐term captive care, with less than half (37%) identified as candidates for release. The surveyed sanctuary population accounts for 35% of the world's captive primates, as compared to ISIS‐registered (where ISIS is International Species Information System) zoological facilities, although we estimate that the actual population is closer to 58%. For some species, the sanctuary population represents the only population in captivity. We discuss the prevalence of range‐state sanctuaries and their primate populations, and issues surrounding their future development and management. Am. J. Primatol. 75:116‐134, 2013. © 2012 Wiley Periodicals, Inc.