The genus Pyxicephalus currently comprises four species distributed throughout sub-Saharan Africa: the Giant African Bullfrog (Pyxicephalus adspersus Tschudi, 1838), Narrow-headed Bullfrog (P. angusticeps Parry, 1982), Edible Bullfrog (P. edulis Peters, 1854) and Calabresi’s Bullfrog (P. obbianus Calabresi, 1927) (Scott et al., 2013). With the exception of the latter, the other three species have been at the centre of taxonomic debate for many years and their species boundaries and distribution are poorly known, with some authors suggesting introgression is occuring in some areas (Poynton, 1964; Parry, 1982; Poynton and Broadley, 1985; Channing et al., 1994).

According to Channing et al. (1994) and Channing (2001), P. adspersus and P. edulis occur sympatrically in places, but this notion was disputed by Scott et al. (2013) who maintained that P. adspersus is an inland species and does not occur on the Mozambique coastal plain. Although P. edulis and P. angusticeps occur sympatrically on the Mozambique coastal plain, the two species seem to occupy different micro-habitats (Scott et al., 2013). Pickersgill (2007) evidently found these species so confusing that he concluded that the differences were unfathomable. The taxonomic confusion has led to seemingly conflicting reports regarding the breeding biology of the Edible Bullfrog.

The first description of the breeding biology of P. edulis revealed a species that breeds at night after light rain with well-spaced males calling in relatively

deep water (300 mm), no inter-male aggression, and amplexing pairs floating and laying eggs like typical Rana [Afrana] species (Channing et al., 1994). These observations were made near Beira, Mozambique. Braack and Maguire (2005) observed P. edulis breeding in the lowveld of South Africa’s Limpopo Province. Their observations could not have been more different from those reported by Channing et al. (1994). Firstly, Braack and Maguire (2005) observed breeding during the day following heavy overnight rain (72 and 188 mm respectively). Secondly, they reported males aggregating in shallow water (<10 cm) at several leks, each with a dominant male which is in contrast to the isolated males calling from deep water as reported by Channing et al. (1994). Thirdly, the lowveld males were extremely aggressive to other males and charging, tossing and biting was common, sometimes resulting in fatalities. This aggressive behaviour, albeit more muted compared to P. adspersus, was also reported by Cook and Minter (2004). Finally, amplexus and egg-laying were similar to that of P. adspersus in that this occurred in shallow water with the female arching her back to expose her cloaca above the water surface, which is different to the floating, Afrana-[Rana] like amplexus described by Channing et al. (1994). It is clear from the foregoing that there are contrasting breeding strategies in Pyxicephalus. Scott et al. (2013) suggested that the observations reported by Channing et al. (1994) were actually of P. angusticeps and those by Braack and Maguire (2005) of P. edulis. It is clear that more details are required about the breeding biology of these species to resolve the uncertainty regarding the seemingly conflicting breeding strategies of the smaller Pyxicephalus species in southern Africa.

Recording Pyxicephalus breeding behaviour is not easy and therefore most of our present knowledge of P. edulis behaviour is based on anecdotal observations.

Herpetology Notes, volume 8: 365-369 (2015) (published online on 30 June 2015)

Notes on the breeding behaviour and ecology of Edible Bullfrogs Pyxicephalus edulis Peters, 1854

in the Limpopo Province, South Africa

Derek Engelbrecht*, Mmatjie Mashao and Ali Halajian

Department of Biodiversity, University of Limpopo, Private Bag X1106, Sovenga, 0727, South Africa.

* Corresponding author e-mail: derek.engelbrecht@ul.ac.za

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The species spends approximately 10 months of the year below the soil surface (Mitchell, 1946) and only seems to breed in numbers if sufficiently heavy rain (>70 mm) fell within a short period (Braack and Maguire, 2005; DE, pers. obs.). Following the main breeding event, calling is sporadic and it can be difficult to determine if the species is present in a given area.

Here we report on observations made during two breeding events of P. edulis, with notes on predation and the diet of adults in the Limpopo Province, South Africa. Specimens were identified based on the presence of a pale spot on the tympanum, the vertebral stripe in the adults, their distinctive advertisement calls and the key provided by Scott et al. (2013). Both breeding events occurred on the farm De Loskop (23°30.706’S, 29°19.019’E; 1090 masl), approximately 45 km north of the city of Polokwane. The farm is situated in the savannah biome and the vegetation is described as Polokwane Plateau Bushveld (Mucina and Rutherford, 2006). The first breeding event occurred on the 4th December 2009 following heavy rain (>80 mm) the night before, and the second occurred on the 21st January 2013 after in excess of 110 mm rain fell in the late afternoon and night of the 20th January 2013, resulting in extensive flooding of grassy plains.

Both events included several hundred frogs, and with the January 2013 breeding event in particular, males were seen and heard calling on the inundated floodplain of an earth dam and the adjacent flooded grassland (0.2–0.3 km2) as well as many small, temporary pools at various localities all over the farm. These temporary pools included roadside ditches, shallow excavations and small, natural depressions ranging in size from approximately 1 m2 to >100 m2. They were all shallow (< 200 mm) and characterised by flooded grasses and forbs. Since there were no good follow-up rains, these temporary pools all dried up within 2–3 days and it was only at the larger floodplain and inundated grassland area where juveniles were later recorded. Although some swarms of tadpoles were observed, we found no evidence of channel construction or guarding of tadpoles. Admittedly our visits to the area were brief and sporadic after the breeding event and it is possible that we may have missed such behaviour. It should be noted that channel construction on the floodplain of the earth dam and the adjacent grassland would probably not have been required as the area remained flooded for several weeks as a result of a slow but steady inflow into the dam. On both occasions breeding took place during the day and by noon breeding activity and calling

Figure 1. Aggressive behaviour of adult male Edible Bullfrogs (Pyxicephalus edulis). (A) A lunge to knock a rival over; (B) Attack with the mouth open to bite a rival.

had decreased substantially. Despite an intensive night-time survey on the 24th January 2013 during favourable weather conditions, no adults were heard or seen in the area.

Our observations confirm the observations of Braack and Maguire (2005). Males aggregated in loose groups in shallow water, with an apparently dominant male charging, biting and even tossing other males that got too close (Figures 1A and B). However, males sometimes wandered into a territory and headed straight for the dominant male. Aggressive encounters frequently resulted in some serious injuries and even a few fatalities. Interestingly, one male was observed amplexing a corpse for several minutes (Figure 2). Females seemed to move freely within and between these aggregations with males chasing them. The events immediately preceding amplexus was uncomplicated and oviposition commenced immediately after amplexus. Amplexing pairs were generally not disturbed by others, but amplexus displacement was observed on two occasions. Some females produced notably smaller clutches suggesting that they had spawned earlier already. Spawning occurred in shallow water (Figure 3) and was as described by Braack and Maguire (2005) and is like that of P. adspersus (Channing et al., 1994; Du Preez and Cook 2004).

Males called in shallow water with their heads and vocal sacs above the water, their deep calls causing a rippling effect in the water (Figure 4). A spectrogram of a series of three calls is presented in Figure 5. In addition to an auditory clue provided by calling males, the pale bulging vocal sac contrasting with the bright yellow axillary and ventrolateral regions may also provide valuable clues about the breeding status of an individual as suggested by Oliver and Scott-Prendini (2011). It would be interesting to establish if females and rival males use the ripples as sensory cues to determine a male’s fitness like in the Neotropical Túngara Frog (Halfwerk et al., 2014). As mentioned above, there was a marked decrease in calling as the day progressed and we heard no calling frogs when we returned three days later.

To obtain data on the diet of adults, we collected the carcasses of five adults that were killed when crossing a road near the breeding site and which were still in relatively good condition. The stomachs were cut open and the contents sorted in a petri dish and examined under a stereo-microscope in the laboratory. The following prey items were recorded and the percentage of stomachs that contained the items is given in parentheses: Coleoptera (100%), Orthoptera (100%),

Notes on the breeding behaviour and ecology of Edible Bullfrogs in South Africa 367

Figure 2. A male Edible Bullfrog (Pyxicephalus edulis) attempting amplexus with a corpse.

Figure 3. Amplexus in the Edible Bullfrog (Pyxicephalus edulis). Note the raised cloaca of the female above the surface of the water.

Isoptera (40%), Diplopoda (20%), Hymenoptera (20%) and Arachnida (20%). Interestingly, most stomachs (60%) contained plant material, e.g. seeds, a small twig and grass blades, as well as grit. Plant material and grit was also recorded in the stomachs of recently

metamorphosed African Bullfrogs (Conradie et al., 2010). However, we concur with these authors that these materials may have been swallowed accidentally while capturing their prey.

Several avian predators were recorded feeding on adult frogs during the breeding events (Figure 6). These included Yellow-billed Kite (Milvus aegyptius), Marabou Stork (Leptoptilos crumeniferus), Saddle-billed Stork (Ephippiorhynchus senegalensis), Yellow-billed Egret (Egretta intermedia), Grey Heron (Ardea cinerea) and Black-headed Heron (Ardea melanocephala). During these events, some Edible Bull Frog individuals were rather bold and lunged at water birds that got too

Figure 4. A calling male Edible Bullfrog (Pyxicephalus edulis) does not only provide an auditory clue, but also visual and possibly sensory tactile clues.

Figure 6. Predation of Edible Bullfrogs (Pyxicephalus edulis) by: (A) Saddle-billed Stork (Ephippiorhynchus senegalensis); (B) Marabou Stork (Leptoptilos crumeniferus); (C) Yellow-billed Kite (Milvus aegyptius).

Figure 5. A spectrogram of the calls of the Edible Bullfrog (Pyxicephalus edulis) recorded at a breeding event on the farm De Loskop, Limpopo Province, South Africa on 21 January 2013.

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close to them. As there were no tadpoles present at the time, it is possible that these may have been territorial males defending their territories.

To conclude, this study has confirmed the observations of the breeding behaviour described by Braack and Maguire (2005) and lends further support to the assertion by Scott et al. (2013) that the breeding behaviour reported by Channing et al. (1994) was indeed that of P. angusticeps. A more detailed study of the breeding behaviour and ecology of the Edible Bullfrog will hopefully provide further insight into this enigmatic species.

Acknowledgements. We wish to express our gratitude to Elizabeth Scott-Prendini for commenting on an early version of this paper and for confirming the identification of the species. The management of the farm Al3 De Loskop for allowing us access to their property.

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Accepted by Maximilian Dehling

Notes on the breeding behaviour and ecology of Edible Bullfrogs in South Africa 369