Predation of Foam Nests of Physalaemus Ephippifer (Anura: Leptodactylidae) by Platemys Platycephala (Testudines: Chelidae) in Central Guyana
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SALAMANDRA 50(1) 57–62 30 April 2014 ISSNCorrespondence 0036–3375 Correspondence Whipped cream cravings in the rainforest: predation of foam nests of Physalaemus ephippifer (Anura: Leptodactylidae) by Platemys platycephala (Testudines: Chelidae) in central Guyana Raffael Ernst1, Stephan Böhm2, Monique Hölting1 & Tillmann Konrad3 1) Museum of Zoology, Senckenberg Natural History Collections Dresden, Königsbrücker Landstr. 159, 01109 Dresden, Germany 2) Department of Integrative Zoology, Universität Wien, Althanstr. 14, 1090 Wien, Austria 3) World Wide Fund for Nature Germany, Reinhardtstr. 14, 10117 Berlin, Germany Correspondence author: Raffael Ernst, e-mail: [email protected] Manuscript received: 9 December 2013 Accepted: 13 December 2013 by Jörn Köhler Non-aquatic oviposition has long been recognized as a The use of foam nests as incubation environments for major trend in amphibian evolution (Lutz 1947, Duell- anuran eggs and larvae is probably one of the most fas- man & Trueb 1986, Wells 2007) and the selective pres- cinating examples of an adaptation to the various selec- sures that drive the evolution of non-aquatic reproduc- tive pressures associated with terrestrial reproduction. It is tion, particularly in anurans, have long been a subject of also a striking example of convergent evolution of life his- speculation (e.g., Gomez-Mestre et al. 2012, Müller et tory strategies, as it appears to have evolved independent- al. 2013). The most widely accepted explanation for this re- ly in several major anuran lineages. At least seven anuran curring trend is predator avoidance during the most vul- families (Hylidae, Hyperoliidae, Leptodactylidae, Limno- nerable life-history phases (i.e., egg and early larval devel- dynasti dae, Microhylidae, Myobatrachidae, and Rhaco- opment) in aquatic environments. However, this theory phori dae) with representatives on all continents that sup- ignores the fact that terrestrial eggs and subsequent ear- port amphibians are currently known to make use of foam ly ontogenetic stages are preyed upon by a wide range of nests. Members of the mainly Neotropical family Lepto- both vertebrate and invertebrate predators, often at rates dactylidae generally deposit their eggs in foam nests, but similar to those reported for aquatic breeders (e.g., Menin construction and deposition as well as the extent to which & Giaretta 2003). Several alternative driving factors for larval development is confined to these nests differ among terrestrial anuran reproduction have therefore been dis- genera and even between species within the same genus cussed, including reduced larval competition, reduction (Hödl 1986, Prado et al. 2002, Haddad & Prado 2005). of the risk of unpredictable drying-up of aquatic sites, Leptodactylid foam nests are thought to protect eggs and limited oxygen availability in tropical ponds, avoidance of developing embryos from predation and desiccation (Hey- strong currents in lotic environments (reviewed in Wells er 1969, Downie 1988). The materials used for foam nest 2007), and a range of habitat factors that are considered construction must therefore be environmentally resilient promoting terrestrial reproduction (Magnusson & Hero and comparatively resistant to physical and chemical dam- 1991, Müller et al. 2013). Given the observed diversity of age (e.g., imposed through invertebrate and vertebrate amphibian reproductive modes that, particularly in the predators as well as bacteria and fungi), yet compatible tropics, co-occur in the same general habitat, it seems with naked eggs and sperm. These are properties that seem challenging if not unlikely to find a universal explanation to be mutually exclusive, but a recent study on the com- for the evolution of non-aquatic reproduction in amphib- ponents of foam nests of the Túngara frog (Engystomops ians. Different species or lineages simply seem to have de- pustulosus) showed how this seemingly paradox situation veloped different strategies to cope with similar selective is resolved through a combination of several proteins that pressures. predominate in foam nests (Fleming et al. 2009). The noc- © 2014 Deutsche Gesellschaft für Herpetologie und Terrarienkunde e.V. (DGHT), Mannheim, Germany All articles available online at http://www.salamandra-journal.com 57 Correspondence turnal Neotropical frog Physalaemus ephippifer, closely re- ity of nests (75%, N = 32) were located at the edge of the lated to the Túngara frog, which was previously placed in water surface of the respective aquatic sites and usually the same genus, exhibits a reproductive strategy that can attached to, or covered by, plant structures, such as large be characterised as r-selected reproduction (high number Cecropia sp. leaves (88% of all recorded cases, N = 32). The of small eggs, fast larval development) that likely evolved foam nests of P. ephippifer exhibit the typical hemispheri- in response to the unpredictable and high-risk environ- cal shape as reported for other members of the genus. The ments in which the species occurs. At our study sites in mean nest diameter observed at Mabura Hill was 6.33 cm central Guyana (Mabura Hill Forest Reserve, MHFR, (sd = 2.6, N = 28) and nests contained an average of 500 05°09’19.30’’ N, 58°41’58.96’’ W; and Iwokrama Forest, tadpoles (sd = 172, N = 20). Embryogenesis was found to be 04°40’17.5’’ N, 58°41’06.6’’ W), where all observations pre- rather rapid, and tadpoles were usually ready to leave the sented in this paper were made, the species is either most nest after two days at Gosner stage 21. However, tadpoles abundant in disturbed habitats (Iwokrama Forest) or ex- could still be retrieved from nests on consecutive days after clusively occurs at heavily disturbed sites (Mabura). Here the first “hatching” was observed. Environmental persist- it reproduces in puddles and ditches mainly along log- ence time of nests depended largely on prevailing weather ging roads and skid trails. Nest densities can be very high. conditions and occurrence of predation. After two to four At Iwokrama, up to 50 foam nests per search hour were days, the majority of nests would show signs of partial dam- recorded in a single night in the main rainy season (July age, i.e., collapsed foam hemisphere or missing segments, 2004), along a single stretch of approximately 2 km of ac- and had completely dissolved or vanished after four to six cess road connecting the field station with the main road days. These observations largely correspond to previous that crosses the forest. Throughout a short observational observations of developmental times and environmental period from May to July 2004, 32 nests were recorded at a persistence of foam nests in Engystomops pustulosus with single site, a small, shallow puddle (app. 50 cm diameter, the exception that here, persistence times were reported maximum depth 20 cm) located at an access road close to to extend to 10 days in tropical conditions (Downie 1993, the field station in the Mabura Hill Forest Reserve. In Guy- Fleming et al. 2009). ana, P. ephippifer can be regarded as a prolonged breeder While a comparatively small percentage of nests were that reproduces throughout the year, even during the dry found to have been partially or completely damaged, none season, but with reproductive and calling activity peaks at of the recovered nests showed clear signs of desiccation. the onset and throughout the core rainy season (May to Further evidence for the assumed protective function of July in average years). foam nests that prevent eggs and larvae from desiccation Foam nests are produced at night, at the edges of small and lethal overheating (Gorzula 1977) was obtained from to medium temporary bodies of water (see above). The thermal buffering experiments, in which internal tempera- construction behaviour of P. ephippifer from Belém, state tures of ten P. ephippifer nests and ambient air tempera- of Pará (Brazil), has previously been described in detail by tures were monitored at continuous intervals (mean tem- Hödl (1990). Our own observations largely correspond to peratures in °C integrated for three time-increments: [1] these descriptions (Fig. 1). However, while several nests (up 02:00–10:00 h, [2] 10:00–18:00 h, [3] 18:00–02:00 h) over to three) could be observed at the same time in a single lo- the course of three days (from shortly after the production cality, communal nests as reported by Hödl (1990) were of foam nests to first hatching of tadpoles). Temperatures not observed in either of the two study sites. The major- were recorded using thermobutton data loggers (i-Button- TMEX, Version 3.12 ± 0.1 °C). Pairs of data loggers were placed in the centre of each nest and on a wooden pedestal at approximately the same height outside nests, respective- ly. All tested nests (N = 10) showed significant differenc- es between the internal nest temperature and ambient air temperature, with internal nest temperatures being gener- ally lower than the ambient air temperatures (mean 0.5 °C, sd = 0.1, N = 90, p < 0.01). The majority of observed devia- tions (55%) were recorded for time-increment two (time of the day with the highest ambient temperatures and most intense solar exposure), while the remainder (45%) were distributed across time-increments one and three (periods with lower ambient temperatures). Temperature increases of as little as 0.5°C have previously been shown to result in increased mortality in tadpoles of the leptodactylid frog Leptodactylus petersii (Ernst et al. 2007). In terrestrial eggs that are exposed to higher temperatures, metabolic rates Figure 1. Amplectant pair of Physalaemus ephippifer constructing and development of embryos are limited by rates of gas a foam nest, observed on 02 May 2003 between 01:00 and 01:30 h, diffusion (Seymour & Loveridge 1994). The buffering ca- Mabura Hill Forest Reserve, Guyana. Photo: RE. pacity provided by P. ephippifer foam nests may therefore 58 Correspondence represent an effective protection during periods with in- and L. rhodomystax) that were found to be unaffected by creased temperatures.