Conservation biology of the giant bullfrog, Pyxicephalus adspersus (Tschudi, 1838) by Caroline Angela Yetman Submitted in partial fulfilment of the requirements for the degree Doctor of Philosophy (Zoology) in the Faculty of Natural and Agricultural Sciences Department of Zoology and Entomology University of Pretoria, Pretoria South Africa April 2012 © University of Pretoria Conservation biology of the giant bullfrog, Pyxicephalus adspersus (Tschudi, 1838) Student: Caroline A. Yetman1 Supervisor: J. Willem H. Ferguson2 Department: 2Centre For Environmental Studies, 1,2Department of Zoology and Entomology, University of Pretoria, Pretoria, 0002, South Africa Degree: Doctor of Philosophy (Zoology) Abstract The giant bullfrog, Pyxicephalus adspersus, is a large, explosive-breeding anuran from southern Africa, which spends most of the year buried in a state of torpor. In South Africa this species is considered to be Near-Threatened by habitat loss and other factors, especially in the densely human populated Gauteng Province. The aim of this thesis was to obtain essential outstanding information about the ecology of P. adspersus to contribute towards improved conservation management of this species. A model was used to predict the geographic range of P. adspersus in southern Africa, and recent land cover data were used to determine the amount of suitable habitat remaining for this species in Gauteng. As a step towards identifying P. adspersus conservation management units, genetic structure and gene flow for populations from 23 localities in Gauteng and seven additional localities in the north-eastern interior of South Africa was i © University of Pretoria quantified using 708 base pairs of the mitochondrial gene cytochrome b. To investigate the unpredictable activity and unknown spatial habitat requirements of P. adspersus, a population’s spawning and non-breeding activity was monitored, and the movements of 70 adult frogs were radio- or spool-tracked during five summers at a site in Diepsloot, Gauteng. Using skeletohronology, the age distribution of breeding P. adspersus at this and two other peri-urban sites near Johannesburg, Gauteng, was examined. Bioclimatic conditions were predicted to be suitable for P. adspersus in the temperate to semi-arid interior, but not the low-lying eastern subtropical and arid western sides of southern Africa. Limited genetic data suggested that P. adspersus was common in the north-eastern interior of South Africa, and that populations in the Free State Province represent an evolutionary significant unit of this species. In central Gauteng, where P. adspersus may have declined by > 90%, populations < 20 km apart exhibited significant genetic differentiation, possibly as a result of genetic drift. At Diepsloot, both annual numbers of spawning events and numbers of spawning males were positively correlated with rainfall, although other meteorological variables also affected the activity of P. adspersus. Radio- or spool-tracked frogs showed high fidelity to their breeding site and burrows, which were situated up to 1 km away from the water. Male P. adspersus probably live ≥ 20 years in the wild, but at some peri-urban breeding sites adult life expectancy and body size may be declining. The geographic range of P. adspersus was predicted to be slightly smaller than that reported by other authors, and deserves phylogeographic validation. The main ii © University of Pretoria conservation priority for P. adspersus in South Africa should be the protection of terrestrial habitat for adult foraging and aestivation around, and for juvenile dispersal and gene flow between, breeding sites. In Gauteng, the conservation of a P. adspersus meta- population is critical, and could most likely be achieved in the northern region of this province. Populations in the Free State Province deserve improved protection given their reported genetic uniqueness. At local spatial scales specific threats (e.g. pollution) should be ameliorated, and long-term monitoring should be implemented to detect real population trends. Keywords amphibian, Anura, biology, Gauteng, grassland, Pyxicephalidae, southern Africa, threatened, wetland iii © University of Pretoria Acknowledgements I am eternally indebted to Jimmy my father, Alice my mother, Johan Lötter my fiancé and Mark my brother for their immeasurable support and assistance, morally, financially and in the field. I have yet to find the caliber of your character in other mortals. I regret and apologize deeply that this project took almost a decade to complete. There are infinitely more profitable ways that your money and my time could have been spent. I sincerely thank Wendy Duncan for assisting with field work in Diepsloot and Peter Mokonoto for helping with the histology component of this project. I also thank others who made a small but significant contribution to this research. The Endangered Wildlife Trust sourced funding for a large portion of this project, which was gratefully received from Rand Merchant Bank and the Pretoria East branch of the South African Hunter’s and Game Conservation Association. Arrow Bulk Marketing is thanked for funding fuel during the first three seasons of field work, and Cellar Rats Wine Club, Diaz Films, and the late Bill Flynn are kindly acknowledged for collectively sponsoring several radio-transmitters. iv © University of Pretoria Disclaimer This dissertation was written as a collection of five manuscripts to simplify the process of publication of the results, as recommended by the Department of Zoology and Entomology. There has consequently been duplication of some information between the chapters. Chapters 2, 3 and 4 have been published and are, respectively, cited below. Chapters 5 and 6 might be submitted for peer-review in the future. Chapter 2 Yetman, C.A. & J.W.H. Ferguson (2011a). Spawning and non-breeding activity of adult giant bullfrogs (Pyxicephalus adspersus). African Journal of Herpetology 60: 13- 29. Chapter 3 Yetman, C.A. & J.W.H. Ferguson (2011b). Conservation implications of spatial habitat use by adult giant bullfrogs (Pyxicephalus adspersus). Journal of Herpetology 45: 56-62. Chapter 4 Yetman, C.A., P. Mokonoto & J.W.H. Ferguson (2012). Conservation implications of the age/size distribution of giant bullfrogs (Pyxicephalus adspersus) at three peri-urban breeding sites. Herpetological Journal 22: 23-32. v © University of Pretoria Declaration I, Caroline Angela Yetman declare that the thesis, which I hereby submit for the degree Ph.D. (Zoology) at the University of Pretoria, is my own work and has not been submitted by me for a degree at this or any other tertiary institution. Caroline A. Yetman: _________________________ Date: _______________________ vi © University of Pretoria Table of contents Abstract .............................................................................................................................. i Acknowledgements .......................................................................................................... iv Disclaimer ......................................................................................................................... v Declaration ....................................................................................................................... vi Table of contents ............................................................................................................. vii Chapter 1 Introduction Global decline of amphibians .................................................................... 1 Conservation status of South African anurans .......................................... 2 Biology of Pyxicephalus adspersus .......................................................... 3 Relevance and objectives of this thesis ..................................................... 5 Chapter 2 Spawning and non-breeding activity of adult giant bullfrogs (Pyxicephalus adspersus) Abstract ..................................................................................................... 9 Introduction ............................................................................................. 11 Materials and Methods ............................................................................ 13 Results ..................................................................................................... 19 Discussion ............................................................................................... 23 Tables ...................................................................................................... 30 Figures ..................................................................................................... 34 vii © University of Pretoria Chapter 3 Conservation implications of spatial habitat use by adult giant bullfrogs (Pyxicephalus adspersus) Abstract ................................................................................................... 37 Introduction ............................................................................................. 39 Materials and Methods ............................................................................ 41 Results ..................................................................................................... 45 Discussion ............................................................................................... 49 Tables ...................................................................................................... 55 Figures ....................................................................................................