The Enigmatic Decline of Rose's Mountain Toad Capensibufo Rosei
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Fading out of view: the enigmatic decline of Rose’s mountain toad Capensibufo rosei E. R. CRESSEY,G.J.MEASEY and K . A . T OLLEY Abstract Rose’s mountain toad Capensibufo rosei survives Introduction in a few isolated montane populations in the south-western Cape of South Africa. It comprises several cryptic species midst growing concern over the biodiversity crisis but it is uncertain whether the lineage on the Cape Aand the suggestion that we are currently experiencing Peninsula is distinct. We tested the hypothesis that toads the sixth mass extinction, declines in amphibian species fi from the Peninsula form a single genetic lineage but that are signi cant. More than one third of amphibians are different breeding sites are divergent at a population level in decline, with proportionately more species at risk of as a result of limited dispersal abilities. Directed surveys extinction than any other taxonomic group (Stuart et al., 2004 were carried out to locate breeding sites and samples ob- ). Furthermore, data pertaining to amphibian declines tained were analysed in a phylogenetic and population are probably underestimates because of the large number 2004 genetic framework, using two mitochondrial markers. We of poorly studied species (Stuart et al., ). Although found toads breeding at only one of five known historical there is no single factor that explains amphibian declines, breeding sites, although one new breeding site was also habitat destruction and alteration are commonly cited as fi 2003 recorded. No toads were observed at 15 other non-breeding the most signi cant threat (Collins & Storfer, ; Beebee ffi 2005 2011 localities where they were historically observed. Toads from &Gri ths, ; Measey, ). Some declines represent the two active breeding sites formed a single lineage that a phenomenon that goes beyond these observable causes, was sufficiently distinct to be given species status. However, occurring in areas that are protected and/or relatively 2004 these were discrete at a population level, with no shared pristine (Stuart et al., ). Such enigmatic declines are ffi haplotypes, suggesting no gene flow between sites. One more di cult to redress and reveal inadequacies in our site was particularly low in genetic diversity, implying understanding of species as well as our approaches towards 2003 increased vulnerability to stochastic events and elevated risk habitat protection (Collins & Storfer, ). of extinction. These results, coupled with the failure to A dearth of baseline data on the population dynamics locate historically known sites on the Cape Peninsula, make of amphibians and the relatively brief and anecdotal nature ffi this newly recognized Peninsula endemic a conservation of many studies have led to di culties in discerning fl priority. Efforts should focus on the protection and between natural population uctuations and human- 1990 1991 expansion of the two known surviving populations and induced declines (Barinaga, ; Pechmann et al., ). the patches of habitat upon which they rely. As a result, mitigation measures are often delayed and this has probably led to the demise of numerous amphibian Keywords Amphibian, Bufonidae, Cape Floristic Region, populations and in some cases entire species (Pounds & Cape Fold Mountains, dwarf toads, extinction risk, fynbos Crump, 1994). In the absence of long-term quantitative data biome biologists use information on historical distribution and This paper contains supplementary material that can be abundance garnered from museum records or natural- 2001 found online at http://journals.cambridge.org history databases (Kress et al., ). Although such data typically lack information on observed absences, historical presences can direct current search efforts (Skelly et al., 2003). Capensibufo Grandison, 1980 (Anura: Bufonidae) is a E. R. CRESSEY* Applied Biodiversity Research Division, South African National genus of African dwarf toad that consists of two recognized Biodiversity Institute, Claremont, South Africa species, C. rosei and the allopatric C. tradouwi. Both species G. J. MEASEY Department of Zoology, Nelson Mandela Metropolitan University, are isolated on montane plateaux in the Cape Fold Port Elizabeth, South Africa Mountains of South Africa, within the fynbos habitat, a K. A. TOLLEY† (Corresponding author) Applied Biodiversity Research Division, South African National Biodiversity Institute, Private Bag X7, Claremont 7735, Mediterranean-type heathland that characterizes these South Africa. E-mail: [email protected] mountains (Fig. 1). C. rosei is categorized as Vulnerable on *Also at: Percy FitzPatrick Institute of African Ornithology, University of Cape the IUCN Red List (SA-FRoG, 2010) and a recent national Town, Rondebosch, South Africa strategic exercise prioritized this species for conservation †Also at: Department of Botany and Zoology, University of Stellenbosch, Matieland, South Africa work relating to surveying, monitoring and taxonomy 2011 Received 7 February 2013. Revision requested 22 May 2013. (Measey et al., ). A recent phylogeny of C. rosei and its Accepted 15 July 2013. First published online 11 February 2014. congener C. tradouwi shows divergences consistent with Oryx, 2015, 49(3), 521–528 © 2014 Fauna & Flora International doi:10.1017/S0030605313001051 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 30 Sep 2021 at 14:54:16, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605313001051 522 E. R. Cressey et al. (a) Legend (b) Approximate extent of breeding site Disturbed breeding site Pristine breeding site Disturbed individual locality Pristine individual locality 34o S (c) 34o 15’ S South Africa 036912km 18o 30’ E FIG. 1 (a) Historical breeding sites of Rose’s mountain toad Capensibufo rosei on the Cape Peninsula, South Africa. (b) The horizontal cross-hatching shows the presumed distribution of C. tradouwi and the vertical cross-hatching shows the presumed distribution of C. rosei incertae sedis, with C. rosei distributed only on the Cape Peninsula. The rectangle on (c) indicates the location of (b) and the rectangle on (b) indicates the location of (a). multiple species and suggests that C. rosei sensu lato these breeding sites are distinct at the population level. comprises cryptic species (Tolley et al., 2010). Presumably Levels of genetic diversity at each breeding site were assessed all populations on the isolated Cape Peninsula represent a to highlight the potential vulnerability of Capensibufo spp. single clade but this conclusion is based on only two to environmental change (e.g. stochastic events) and risk of individuals from a single breeding site (Tolley et al., 2010). It extinction. The combination of phylogenetic and popu- appears that the current conservation status of C. rosei was lation genetic analyses, with the examination of historical assessed using insufficient taxonomic knowledge, exacer- records, allowed a critical assessment of the current bated by the lack of distributional data as a result of the distribution of C. rosei, which has implications for setting cryptic nature of these toads. Unlike most other anurans conservation priorities for this species. C. rosei has no call (Grandison, 1980) so all records are based on direct observations of individuals. Its montane distri- Methods bution, small body size (,2 cm) and cryptic colouration coupled with densely vegetated habitat and a short breeding To direct the search effort, historical records from museums season (c. 2 weeks in late August) have resulted in a paucity and the literature were compiled from the Global Bio- of records (Minter et al., 2004). diversity Information Facility as well as directly from To verify the geographical distribution of C. rosei on relevant institutions. Records from the Atlas and Red Data the Cape Peninsula and to examine possible trends of Book of the Frogs of South Africa, Lesotho and Swaziland population persistence, gain and loss we compiled all (Minter et al., 2004) were also included, as were field notes historical records from the Cape Peninsula and carried out and anecdotal information from local herpetologists. We dedicated surveys to locate breeding populations. We also assumed that records of individual adults probably rep- examined the hypothesis that all breeding sites on the resented nearby breeding populations at the time they Cape Peninsula form a monophyletic clade at the species were recorded. Teams of 1–8 people searched 12 historically level (using mitochondrial markers, ND2 and 16S) but that recorded sites (Supplementary Table 1) on at least 26 Oryx, 2015, 49(3), 521–528 © 2014 Fauna & Flora International doi:10.1017/S0030605313001051 Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.14, on 30 Sep 2021 at 14:54:16, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1017/S0030605313001051 Rose’s mountain toad 523 occasions over 4 years (2008–2011). Each search lasted c. 4 v. 3 (Ronquist & Huelsenbeck, 2003). The data were hours and was carried out during daylight, when the likeli- partitioned by marker, with priors specifying six rate hood of sighting toads or tadpoles was greatest (Fig. 1). This categories plus gamma. Markov chain Monte Carlo was toad does not produce any breeding call and therefore the run twice in parallel with four independent chains starting breeding aggregations are silent both day and night (GJM & from different initial random trees, for 10 million genera- KAT, pers. obs.). C. rosei breeds in ephemeral pools filled by tions. Trees were sampled every 1,000 generations and the winter rainfall (de Villiers, 2004), typically located on first 3 million generations were removed as burn-in. Burn-in mountain plateaux (Supplementary Table 1). The sites on was determined by examining the standard deviation of the Cape Peninsula are characterized by low fynbos veget- split frequencies for stabilization and whether the effective ation (, 0.5 m) and observers were able to look directly into sample size was .200 for all parameters, using Tracer v. 1.4.1 any small seepage pools. Target areas were scoured, such (Rambaut & Drummond, 2007).