Current Herpetology 36(1): 54–57, February 2017 © 2017 by The Herpetological Society of Japan
doi 10.5358/hsj.36.54
No Experimental Evidence for Cannibalism in Tadpoles of a Rhacophorid Treefrog, Polypedates braueri Richard M. LEHTINEN1* and Yeong-Choy KAM2 1
The College of Wooster, Department of Biology, 931 College Mall, Wooster, Ohio 44691, USA 2 Tunghai University, Department of Life Science, Taichung, Taiwan 407, ROC
Abstract: In recent years, cannibalism has been increasingly documented in larval amphibians and anecdotal observations suggested that tadpoles of Polypedates braueri (Rhacophoridae) exhibit this unusual feeding behavior. To test these observations, we conducted a laboratory experiment where we manipulated both density and food quantity in P. braueri tadpoles. However, there were no significant differences in survival among treatments and no instances of cannibalism were observed during the course of the experiment in any treatments. Despite using conditions that might facilitate cannibalism (low food, high density), we were unable to experimentally confirm its existence under the conditions examined. Key words: Conspecific interactions; Density; Food limitation; Necrophagy; Tadpole diet
Introduction Acquiring adequate food for physiological needs is very important for most animal species. While rare in vertebrates, cannibalism can be an important strategy to acquire food. Individuals killing and eating conspecifics can gain an energy-rich food source and at the same time eliminate potential competitors or predators (Meffe and Crump, 1987; Babbit and Meshaka, 2000; Crossland et al., 2011; Jefferson et al., 2014). However, possible drawbacks of cannibalistic behavior include risk of injury or death (Wildy et al., 2001), increased probability of disease transmission (Pfennig et al., 1998), and a decrease in inclu* Corresponding author. Tel: +1–330–263–2271; Fax: +1–330–263–2378; E-mail address:
[email protected]
sive fitness by consuming a close relative (Fox, 1975; Crump, 1992). In amphibians, a number of well-documented examples of cannibalism are known, especially in salamander larvae. For example, larvae of the tiger salamander (Ambystoma tigrinum) commonly consume conspecifics and some populations have ‘cannibal morph’ individuals which differ from normal individuals in having enlarged heads and vomerine teeth (Collins and Cheek, 1983). Larval cannibalism may take the form of a larva killing and consuming another larva, hatchling, or fertilized egg but oophagy (a larva consuming an unfertilized egg) is not regarded as cannibalism as the egg is non-viable (Lehtinen, 2004). Cannibalistic interactions are thought to most often occur between unrelated individuals (heterocannibalism), but are also known among siblings (sibling cannibalism, Alford, 1999).
LEHTINEN & KAM—NO CANNIBALISM OF POLYPEDATES BRAUERI TA DPOLES 55 In frogs, most species have tadpoles that are primarily or entirely herbivorous or detritivorous. Yet a growing number of species are known to exploit animal food sources when available (Schiesari et al., 2009). For example, Alford (1999) listed thirty species known to consume the eggs or tadpoles of conspecifics. Cannibalism in tadpoles is thought to be more common in species that breed in ephemeral waterbodies and in conditions of high density and low food (Crump, 1992; Caldwell and Araújo, 1998; Babbit and Meshaka, 2000). Some species, such as spadefoot toads, have an inducible carnivore tadpole phenotype (Pfennig, 1992). Cannibalism has also been reported to be most frequent when larger and more developmentally advanced tadpoles encounter newly deposited eggs or recently hatched tadpoles (Petranka and Thomas, 1995). Nonetheless, detailed empirical examples of bona fide cannibalism in tadpoles are not very common. Field observations of cannibalism may sometimes actually be necrophagy (the consumption of dead or dying conspecifics; Rudolf and Antonovics, 2007). Distinguishing between cannibalism and related behaviors such as predation, necrophagy and oophagy is important as these are different processes with different outcomes. For this reason, studies investigating cannibalism in an experimental context using appropriate controls and replication are most likely to advance our knowledge on this important topic. Here, we explore the possibility of cannibalistic behavior in tadpoles of the treefrog Polypedates braueri (Rhacophoridae). Chou and Lin (1997) briefly reported on suspected cannibalism in this species (as P. megacephalus) and our own observations also suggested it (Y-C. Kam, unpublished data) but, to our knowledge, this claim has not been investigated further. In this experiment, we experimentally manipulated both food levels and tadpole density to investigate the conditions under which cannibalism might occur in this species.
Materials and Methods Polypedates braueri tadpoles were collected from a natural population breeding in concrete tanks at Bagua Terrace (Changhua County, Taiwan) on 5 October 2006. Tadpoles were transported to Tunghai University and randomly allocated to one of four treatments: normal food/low density, normal food/high density, low food/low density and low food/ high density. Tadpoles were placed in plastic containers (12.6 cm wide×9.8 cm high×7.4 cm deep), and filled with 500 mL of aged well water. Each treatment was replicated five times for a total of twenty containers. Low density treatments had five tadpoles per container, high density treatments had 10 tadpoles per container. Based on our field observations at Bagua Terrace, these are not abnormally high densities for this species. Because of the multiple cohorts present at our collection site, tadpoles were available in a wide variety of sizes (Gosner stage range 25–39 (mean 26.8, SD= 2.7); Gosner, 1960). Random allocation of these tadpoles to treatments resulted in all replicates having a variety of ontogenetic stages. This was done intentionally, to maximize our chance of detecting cannibalism. A ll containers were kept in an indoor laboratory at room temperature (~22 C) under fluorescent lights on a 12/12 light-dark cycle. Tadpoles were fed tadpole food pellets in amounts of 0.01 g per tadpole per day in the normal food treatments and at 0.0025 g per tadpole per day in the low food treatments. The food amount in the normal food treatments was previously found to support adequate growth and development in P. braueri tadpoles (Hsu et al., 2012). Water in each container was changed every other day. The experiment was continued for 14 days, starting on 7 October and ending on 20 October, 2006. One individual metamorphosed during the experiment. This individual was removed and replaced with a late stage tadpole. We tested for statistically significant differences in survival among treatments using a non-parametric Kruskal-Wallis test implemented in SPSS version 23.0.
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Fig. 1. Mean proportion of P. braueri tadpoles surviving until the end of the experiment (±2 SE) in the four treatments. Each treatment was replicated five times. Some treatments lack error bars since all replicates had 100% survival.
Results Tadpole survival was high overall and was not significantly different among any of the treatments (χ2=2.12, df=3, P=0.549; Fig. 1). One replicate in the high food/high density treatment had 100% percent mortality due to unknown causes. One individual from the low food/high density treatment also died of unknown causes. However, none of these dead tadpoles were consumed by conspecifics and were found intact in their containers. No other mortality was noted during the experiment.
Discussion While dietary diversity in tadpoles is increasingly recognized (Altig et al., 2007; Schiesari et al., 2009) and reports of cannibalism in tadpoles continue to grow (Alford, 1999), we found no evidence for cannibalism in tadpoles of P. braueri in our experimental conditions. Other studies have shown that the occurrence of cannibalism is often related to resource availability, with cannibalism being more likely under low food and high density conditions (Collins and Cheek, 1983; Wildy et al., 2001). However, in our study, tadpoles of P. braueri did not engage in cannibalism even when these conditions were present and
smaller individuals were available as prey to larger ones. While this experiment was relatively short (14 days), the digestive tract clearance time of many tadpoles is only a few hours (Liang et al., 2002). Based on this and previous data on feeding and growth in this species (Hsu et al., 2012), it seems very likely that food was limiting in our experiment. The lack of observed cannibalistic behavior suggests that P. braueri tadpoles may be either unwilling or unable to utilize conspecifics as a food source. While recent studies have suggested substantial plasticity and adaptability in food use in tadpoles (Schiesari et al., 2009), there may still be limitations or constraints in some taxa in the types of food that are taken. One factor that may help explain these results is habitat permanence. Other studies have found that cannibalism in tadpoles is often associated with reproduction in temporary water bodies (Crump, 1983). In such habitats, rapid growth may be especially necessary to achieve metamorphosis before the pond dries. Polypedates braueri is considered to be a habitat generalist and is not tied particularly to temporary water bodies (Karraker, 2013). Thus, in a species that often breeds in more permanent water bodies, the costs of cannibalism may outweigh its benefits. While cannibalism or other sorts of carnivory are noteworthy in tadpoles, experiments that fail to find evidence of cannibalism may be under-reported in the literature. To have an accurate estimate of the frequency, distribution and importance of cannibalism in amphibians and other taxa, we encourage the reporting of both positive and negative experimental results.
Acknowledgments We thank the Taiwan National Science Council for providing funds for RML to visit Taiwan. RML also thanks the College of Wooster for the research leave that supported this work. The College of Wooster IACUC approved the methods used in this study.
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Accepted: 25 August 2016
