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Tadpoles: the biology of anuran larvae

Amphibians are facing an extinction crisis, and conservation breeding pro- grammes are a tool used to prevent imminent species extinctions. Compared to mammals and birds, amphibians are considered ideal candidates for these programmes due to their small body size and low space requirements, high fecundity, applicability of reproductive technologies, short generation time, lack of parental care, hard wired behaviour, low maintenance requirements, relative cost effectiveness of such programmes, the success of several amphibian conservation breeding programmes and because captive husbandry capacity exists. Superficially, these reasons appear sound and conservation breeding has improved the conservation status of several amphibian species, however it is impossible to make generalisations about the biology or geo-political context of an entire class. Many threatened amphibian species fail to meet criteria that are commonly cited as reasons why amphibians are suitable for conservation breeding programmes. There are also limitations associated with maintaining populations of amphibians in the zoo and private sectors, and these could potentially undermine the success of conservation breeding programmes and reintroductions. We recommend that species that have been assessed as high priorities for ex situ conservation action are subsequently individually reassessed to determine their suitability for inclusion in conservation breeding programmes. The limitations and risks of maintaining ex situ populations of amphibians need to be considered from the outset and, where possible, mitigated. This should improve programme success rates and ensure that the limited funds dedicated to ex situ amphibian conservation are allocated to projects which have the greatest chance of success.

Amphibians and conservation breeding programmes: do all threatened amphibians belong on the ark?

A captive 'survival assurance' population of 56 endangered boreal toads Anaxyrus boreas boreas, housed within a cosmopolitan collection of amphibians originating from Southeast Asia and other locations, experienced high mortality (91%) in April to July 2010. Histological examination demonstrated lesions consistent with ranaviral disease, including multicentric necrosis of skin, kidney, liver, spleen, and hematopoietic tissue, vasculitis, and myriad basophilic intracytoplasmic inclusion bodies. Initial confirmation of ranavirus infection was made by Taqman real-time PCR analysis of a portion of the major capsid protein (MCP) gene and detection of iridovirus-like particles by transmission electron microscopy. Preliminary DNA sequence analysis of the MCP, DNA polymerase, and neurofilament protein (NFP) genes demonstrated highest identity with Bohle iridovirus (BIV). A virus, tentatively designated zoo ranavirus (ZRV), was subsequently isolated, and viral protein profiles, restriction fragment length polymorphism analysis, and next generation DNA sequencing were performed. Comparison of a concatenated set of 4 ZRV genes, for which BIV sequence data are available, with sequence data from representative ranaviruses confirmed that ZRV was most similar to BIV. This is the first report of a BIV-like agent outside of Australia. However, it is not clear whether ZRV is a novel North American variant of BIV or whether it was acquired by exposure to amphibians co-inhabiting the same facility and originating from different geographic locations. Lastly, several surviving toads remained PCR-positive 10 wk after the conclusion of the outbreak. This finding has implications for the management of amphibians destined for use in reintroduction programs, as their release may inadvertently lead to viral dissemination.

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Isolation of a Bohle-like iridovirus from boreal toads housed within a cosmopolitan aquarium collection

To test the hypothesis that subtle differences in abiotic requirements can result in almost total spatial segregation, we sampled two species of diurnal frogs, Atelopus spumarius and Allobates sumtuosus, in a primary forest reserve in central Brazilian Amazonia. We conducted visual and acoustic surveys on three occasions over 2 months, in 40 streamside (riparian) plots distributed throughout the reserve's two major drainage basins, using a grid system that covers 64 km2. On average, drainages differed in the pH of stream water and the number of connected and isolated streamside pools. Differences in abiotic characteristics of drainages were associated with the spatial distribution of frog species. The occurrence and density of Allobates sumtuosus was negatively related to stream pH and discharge and positively related to the number of isolated pools in plots. The occurrence and density of Atelopus spumarius was associated with streams with high discharge and pH near neutral. These results indicate that although very large reserves will probably contain sufficient landscape heterogeneity to accommodate different species of diurnal frogs, due to strongly patchy distributions, in situ studies using fine-scale species-distribution models will be necessary to assess the adequacy of small reserves in Amazonia that cover hundreds of square kilometers or less for the conservation of some anuran species.

Fine‐scale habitat heterogeneity explains the local distribution of two Amazonian frog species of concern for conservation

The late Paleogene to early Neogene salamander Chelotriton paradoxus is redescribed on the basis of new and excellent material from two deposits, the late Oligocene Enspel locality and the Miocene Randeck Maar. C. paradoxus is characterised by the following features: (1) skull outline broad and parabolic, (2) snout abbreviated, with nasal only half the length of the frontal, (3) quadratojugal with a series of 3–5 spikes on the lateral margin, and (4) osteoderms larger than in other genera. Like extant Echinotriton, its trunk ribs bear extensive spikes (epipleural processes), with an elongated one on the 3rd rib. The Enspel sample of C. paradoxus shows greater variation in the size and number of quadratojugal spikes, whereas the best-preserved Randeck specimen bears exceptionally tall tubercles on all dermal bones and osteoderms and has a larger quadratojugal. Based on preliminary taphonomical data, we suggest that C. paradoxus probably led a predominantly aquatic life.

The salamandrid Chelotriton paradoxus from Enspel and Randeck Maars (Oligocene–Miocene, Germany)

We report on our experiences with the captive management and ex situ reproduction of the Harlequin toad from Suriname (Atelopus flavescens ) at the amphibian breeding unit of the Cologne Zoo. Egg deposition was stimulated by maintaining A. flavescens in a drier environment followed by a period of intensive irrigation. Here we provide for the first time an overview of the larval development from oviposition to metamorphosis, including diagnostic morphological char- acters according to Gosner. Eggs were arranged in strings and attached to the substrate below the water surface. Larvae hatched about five days after egg deposition and the characteristic abdomi- nal suctorial disc developed about two days later (stages 20-21). Tadpoles are gastromyzophorous and were observed rasping algae. The average time for larval development to stage 41 was 100-130 days. Larval development appears to be dependent on water temperature with faster development at higher temperatures. Concerning color pattern in adults, we observed a slight sexual dimorphism and we were able to recognize individuals due to a constant color pattern. However, color was ob- served to slightly change over time.

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Is there a chance for conservation breeding? Ex situ management, reproduction, and early life stages of the Harlequin toad Atelopus flavescens Duméril & Bibron, 1841 (Amphibia: Anura: Bufonidae)

2 Naturhistorisches Museum der Burgergemeinde Bern, Berne, SWITZERLAND Abstract.—We report long-term experience with the successful keeping and breeding of Megoph- rys nasuta at the Cologne Zoo's Amphibian Breeding Unit and compare data with other breeding reports. In addition, we document the development and morphology of different larval stages of M. nasuta. Diagnostic morphological characters are provided for Gosner (1960) larval stages 18- 22 and 25-46. Ovipositions were not seasonal and took place after a drier phase in the terrarium followed by intensive spraying to simulate the natural rain period. The larvae hatched about one week after egg deposition. The characteristic funnel-shaped oral disc became discernible about two weeks after egg deposition at Gosner stage 21 and degenerated at Gosner stage 42. The mean total developmental time observed for M. nasuta was 2.5-3.5 months. Larvae developed faster at higher temperatures and lower densities. The triangular projections at the upper eyelids, which are char- acteristic for advanced terrestrial stages, began to develop two or three weeks after completion of metamorphosis.

Husbandry, captive breeding, larval development and stages of the Malayan horned frog Megophrys nasuta (Schlegel, 1858) (Amphibia: Anura: Megophryidae)

Captive breeding and larval morphology of Tylototriton shanjing Nussbaum, Brodie & Yang, 1995, with an updated key of the genus Tylototriton (Amphibia: Salamandridae)

The aim of this study was to gain a better understanding of the social and in particular reproductive behaviour of the Critically Endangered Philippine crocodile. Crocodylus mindorensis has been a focus for international conservation breeding measures for about two decades. Since little scientific data have been gathered on the biology and ecology of the species so far, its breeding remains a challenge. In order to identify behavioural patterns that trigger courtship behaviour, and to determine when sociopositive interactions increase and the animals are ready for reproduction, a pair of two adult C. mindorensis at Cologne Zoo was systematically observed between August 2011 and July 2012 for a total of 583 hours. Observations took place using all occurrences recording and scan sampling, focusing on pre-, post- and actual mating behaviour. We present a detailed documentation of copulations with behaviours such as growling, roaring, and bubbling. Bubbling in both sexes was observed prior to copulations and decreased with the end of the mating season, supporting the assumption that it can be referred to as courtship behaviour. Behaviours that indicate the approach of the breeding season, such as approaches to the dividing slide, bubbling and nest building, could be distinguished. Our findings should help to improve breeding efforts under captive husbandry conditions and thus contribute to the conservation breeding of this highly endangered and difficult to keep crocodilian species.

Detlef Karbe

Papers

Is there a chance for conservation breeding? Ex situ management, reproduction, and early life stages of the Harlequin toad Atelopus flavescens Duméril & Bibron, 1841 (Amphibia: Anura: Bufonidae)

Husbandry, captive breeding, larval development and stages of the Malayan horned frog Megophrys nasuta (Schlegel, 1858) (Amphibia: Anura: Megophryidae)

Captive breeding and larval morphology of Tylototriton shanjing Nussbaum, Brodie & Yang, 1995, with an updated key of the genus Tylototriton (Amphibia: Salamandridae)

First observations on the courtship, mating, and nest visit behaviour of the Philippine crocodile (Crocodylus mindorensis) at the Cologne Zoo