What does a Pacman eat? Macrophagy and necrophagy in a generalist predator (Ceratophrys stolzmanni)

Introduction

A critical first step in understanding the ecology of a predator is to have knowledge of its food preferences and foraging strategy. Data regarding the type of prey consumed improves our understanding of the feeding strategy of the species, and uncovers its position in the trophic network (Jiang & Morin, 2005). In many ecosystems, especially in the tropics, amphibians are the most abundant vertebrates (Stebbins & Cohen, 1995), so they can have an important impact on food-webs, both as predators and prey (Semlitsch, O’Donnell & Thompson, 2014).

Frogs and toads swallow their prey whole, so they are considered gape-limited predators (Wells, 2010). Therefore, the width of their head constitutes a good predictor of the size of prey they are able to ingest (Emerson, 1986). As a result, a tendency for larger individuals or animals with wider mouths to consume larger prey items exists both between differently sized individuals of the same species (Lima & Moreira, 1993; Wu et al., 2005), but to some extent also between different species (Toft, 1980; Lima & Magnusson, 1998; Isacch & Barg, 2002). Among anurans, one family that seems to benefit from a series of morphological features associated with macrophagy is the Ceratophryidae (Emerson, 1985). Species belonging to this family have a disproportionately large, robust skull relative to their body size (hence the name of Pacman frogs vernacularly used for Ceratophrys species), a reduced skull length associated with an increase in skull width (Fabrezi, 2006) and fangs (Fabrezi & Emerson, 2003; Fig. S1). The capacity to ingest very large prey allows these animals to exploit diverse dietary resources, which results in a diet that consists, along with diverse invertebrates, of reptiles (Chávez, Venegas & Lescano, 2011), small birds and mammals (Duellman & Lizana, 1994; Schalk et al., 2014), and a large proportion of amphibians (Hulse, 1978; Pueta & Perotti, 2013; Stănescu, Marangoni & Reinko, 2014).

Among horned frogs, one species for which information regarding the feeding habits is lacking is the Pacific horned frog, Ceratophrys stolzmanni, a burrowing amphibian known from just a few locations in the coastal dry forests in Peru and Ecuador (IUCN Amphibian Specialist Group, 2018). The species is fossorial and nocturnal. Individuals remain buried in the ground most of their lives, and come out of their burrows only after heavy rains. Owing to its infrequent activity and small distribution, few studies concerning the ecology of the species have been carried out (Székely et al., 2017, 2018b). Pacific horned frogs inhabit seasonal environments, with a dry season consisting of at least 4 months with less than 10 mm monthly precipitation (Espinosa et al., 2016). The frogs aestivate during this interval, and return to activity and breed immediately after the first heavy rains of the rainy season (Székely et al., 2018a). However, even during the rainy season, they are essentially active above ground only during humid nights. First juveniles start to metamorphose at the end of March through April, depending on the precipitation regime; they have less than 3 months, generally until the end of June, to feed and grow enough that they can survive the subsequent aestivation. A previous study revealed that juveniles of this species double in size and reach sexual maturity less than a year after metamorphosis (Székely et al., 2018b), despite the short season in which they are active.

We describe here the first observations of the diet of the Pacific horned frog, obtained during the rainy season (January–April) of 2 years (2015–2016) in the natural habitat of the species. Additionally to reporting the variety of prey consumed, we also investigated the way the size of the predator influenced its diet; we hypothesize that individuals with wider heads would ingest larger prey (Quiroga, Sanabria & Acosta, 2009). We also expected a positive correlation between predator size and its ingested food in terms of either number of items or volume of food (Basso, 1988; Biavati, Wiederhecker & Colli, 2004), and that larger individuals would tend to avoid eating small items (Whitfield & Donnelly, 2006).

Materials and Methods

Results

GIT content analysis. From the 37 collected dead horned frogs (19 females, 18 males, SVL ranging between 51.6 and 81.2 mm), six (16%) had no detectable food in their GIT. From the remaining 31 frogs, we retrieved 197 prey items, belonging to 12 taxa (Table 1), including three vertebrate items (two anurans, Trachycephalus jordani and Leptodactylus labrosus, and a juvenile snake, Leptodeira septentrionalis; Fig. 1). The average number of prey items per individual was 6.4 ± 3.8, ranging between 1 and 121.

Insects, gastropods, and arachnids represented the most important prey as revealed by the relative importance index; in terms of volume, gastropods (Pulmonata) and centipedes (Chilopoda) represented a large proportion, while numerically mites (Acari) and non-ant Hymenoptera dominated the diet of horned frogs (Fig. 2). Ingested invertebrate prey varied in length between 1 and 65 mm (mean ± S.E. = 13.2 ± 1.6 mm) and in width between 1 and 16 mm (5.6 ± 0.6 mm). In the 31 frogs that had prey items, we found no statistically significant relationship between the predator size and the ingested prey size. The total length (SVL) of the predator was not correlated with the number of prey items it contained (Pearson correlation; r = −0.108, p = 0.564, n = 31), the total volume of GIT contents (Pearson correlation; r = 0.197, p = 0.345, n = 25), or the minimum volume of any individual ingested item (Pearson correlation; r = −0.005, p = 0.981, n = 25). The HW was not correlated with the maximum width of ingested prey (Pearson correlation; r = 0.192, p = 0.357, n = 25).

Direct observation of feeding behaviour. Observed behaviours included both predation and scavenging on anuran species (Fig. 3). We witnessed 22 instances of juveniles (Gosner stage 46, tail completely resorbed, average SVL = 29.6 ± 1.3 mm) performing cannibalistic attacks on similar or younger froglets (tail in various stages of resorption, SVL = 23.8 ± 1.2 mm, n = 18, the rest being too far ingested to estimate the size). The average ratio between predator and prey SVL was 1.26 (Table S2). The prey was always caught head-first. In one additional case, we did not witness the predation event, but the dorsal pattern of a Pacific horned frog was evident by transparency through the stretched skin of the cannibal juvenile’s abdomen.

We encountered five instances of adult C. stolzmanni (mean SVL = 55.9 ± 2.4 mm) feeding on Leptodactylus labrosus (45.7 ± 3.2 mm, n = 4, one escaped before it could be photographed or measured). The average ratio between predator and prey SVL was 1.24 (Table S2). The prey was bitten by the posterior part, and the horned frogs used their forelimbs to subdue it and secure a better position for ingestion (Fig. 3C). As a defence mechanism, the white-lipped frogs were inflated and emitted a high-pitched distress call.

Necrophagy. On March 19, 2015 at around 23:00 on a dirt road inside the reserve, we encountered a male C. stolzmanni (SVL = 58 mm), attempting to ingest a male T. jordani (SVL = 73 mm) that was dead on the road (Fig. 3D). The condition of the carcass, which was flattened and partially dried out, indicated that the road-killed treefrog had been dead for several hours. We observed the pair for about 10 min. During this interval, the horned frog, having bitten the treefrog by the head, jumped and used its forelegs to attempt to position its evidently larger prey for an easier ingestion (Video S1). Since the horned frog was noticeably disturbed by our presence and tried to hide under the vegetation by the side of the road, we left. We cannot know whether the feeding attempt was successful.

Discussion

The few studies concerning the dietary habits of Ceratophrys species in their natural habitat reveal them as generalist and opportunistic predators (Pueta & Perotti, 2013; Schalk et al., 2014). Our study shows that, similar to its larger congeners, the Pacific horned frogs hunt and consume diverse resources. Generalist feeders, switching between invertebrates and vertebrates, have more feeding opportunities and thus higher growth rates compared to more specialized competitors (Caley & Munday, 2003; Berumen & Pratchett, 2008).

For other species of this genus, vertebrate prey represent a predominant part of their diet. The more in-depth studies concerning the diet of C. cornuta (Duellman & Lizana, 1994), C. joazeirensis (Da Silva Jorge et al., 2015) and C. ornata (Basso, 1988) show that vertebrates represent a high volumetric (up to 98%) and numeric (up to 69%) proportion of the their food. In the case of the Pacific horned frog, only approximately 10% of the individuals had preyed upon amphibians and reptiles, and vertebrates represented 1.5% of all ingested prey items. However, although the advanced state of digestion did not allow us to accurately estimate their volume, they constitute a large part of the total consumed volume. The additional direct observations of anurophagy confirm that such events are not accidental. Other vertebrates, such as rodents and birds, which were reported from the diet of large Ceratophrys species such as C. cornuta (Duellman & Lizana, 1994), C. cranwelli (Schalk et al., 2014) and C. ornata (Basso, 1988), are less likely to be feasible to the smaller sized Pacific horned frog. The differences in the amount of vertebrate prey consumed are likely a consequence of the smaller size of C. stolzmanni as well.

In amphibians, the width of the mouth limits the size of items that can be ingested (Emerson, 1985). Indeed, a number of studies show that as individuals grow in size, their diet also shifts towards larger prey (Lima & Moreira, 1993; Hirai, 2002). As a result, we expected to find that larger Pacific horned frogs consumed larger prey. However, no relation between the predator gape and the maximum prey item ingested was evident in our study. The lack of correlation between predator and prey is probably due to the lack of juveniles in our sample. A study carried out across size classes would probably confirm that larger individuals have access to and consistently eat larger food items. On the other hand, our results show that even large individuals capture and consume very small prey items, such as mites and small insects. Eating small prey may be beneficial because of lower behavioural costs and risks (e.g. handling time and energy expenditure; risk of injury), even in larger adults (Simon & Toft, 1991).

In some aspects, the taxonomic composition of invertebrate prey in C. stolzmanni showed some differences compared to other horned frogs for which data is available. An important proportion of their diet consisted of molluscs (Gastropoda), which were consumed by almost half of the sampled frogs. This contrasts with the rare occurrence of gastropods in other Ceratophrys (Schalk et al., 2014). The dominance of ants (Formicidae), which was reported for C. cornuta (Duellman & Lizana, 1994) and C. aurita (Schalk et al., 2014), is also not shared by the Pacific horned frogs, as ants did not represent a substantial part of their diet. Although amphibians are capable of distinguishing between prey characteristics, resulting in consistent selectivity of prey (Freed, 1982), these differences in diet may simply reflect the discrepancies in resource availability rather than an active choice. Future studies focusing on diet vs. site-specific prey availability should clarify these questions (Cogălniceanu et al., 2018).

Anurophagy and cannibalism. The majority of anurans feed mostly on invertebrates (Pough et al., 2016), but some species occasionally consume post-metamorphic anurans (Toledo, Ribeiro & Haddad, 2007). This occurs with a much higher frequency in a few genera (Measey et al., 2015), such as Lithobates (Bolek & Janvy, 2004; Silva et al., 2009), Leptodactylus (Rodrigues et al., 2011; Costa-Pereira et al., 2015), and Ceratophrys (Schalk et al., 2014). At least two species of the genus Ceratophrys exhibit complex pedal luring behaviour (Murphy, 1976; Radcliffe et al., 1986), which presumably evolved to attract visually hunting prey, such as other anurans (Hagman & Shine, 2008; Sloggett & Zeilstra, 2008). Feeding on vertebrates is beneficial: they are a source of energy that is easier to digest compared to most groups of invertebrates, which have a tough exoskeleton (Secor, Wooten & Cox, 2007). Additionally, the higher protein of vertebrates promotes rapid growth (Grayson et al., 2005), while the high water content of anuran prey compared to invertebrates can be especially advantageous in a xeric environment.

Intra-guild predation can be considered as an opportunistic form of predation (Toledo, Ribeiro & Haddad, 2007). Additional to a phylogenetic predisposition (Measey et al., 2015), this behaviour is favoured by several environmental conditions, such as overlap in habitat use amongst various size classes (Wissinger et al., 2010), a scarcity in alternative prey (Pizzatto & Shine, 2008), and a high amphibian density (Polis & Myers, 1985). The conditions favouring cannibalism are met especially in highly seasonal environments (Blayneh, 1999). In the study area, shortly after metamorphosis, the density of C. stolzmanni juveniles in the vicinity of breeding ponds can be as high as 25 individuals/m² (D. Székely, personal observation, 2016), and their capacity to ingest large prey increases the probability for cannibalism. Along with providing a nutritious source of food, consuming other anurans found in the same habitat can also be beneficial by eliminating potential competitors (Polis, Myers & Holt, 1989; Finke & Denno, 2003).

Necrophagy. Scavenging is common in some anuran species during their larval stage (Heinen & Abdella, 2005; Silva & Muniz, 2005; Kirchmeyer et al., 2015), since tadpoles base the recognition of food items on chemical cues and are typically grazing feeders (Altig, Whiles & Taylor, 2007). However, reports of adults consuming any type of carcass are exceptional (Beane & Pusser, 2005; Tupper, Adams & Timm, 2009; Oda & Landgraf, 2012). In post-metamorphic anurans, a certain pattern of movement is necessary for prey recognition and thus for triggering an attack (Ewert, Burghagen & Schurg-Pfeiffer, 1983), so that cadavers are generally disregarded. Even if scavenging is occasional in C. stolzmanni, our report suggests that some anuran species have greater dietary flexibility than often believed.

Conclusions

We found that the Pacific horned frog has a relatively diverse diet, both in terms of prey diversity and size. The ability to feed on a wide variety of prey types indicates that the species has the capacity to take advantage of a variety of feeding opportunities. However, we acknowledge that the number of individuals used in this study is low and we are still far from having a complete understanding of this species’ feeding habits. Further research on the subject is needed. Additionally, studies testing consumed vs available resources and competitive interactions with other species would allow for conclusions regarding the selectivity (or lack thereof) in prey choice. Such studies would also permit testing for the active inclusion of vertebrates in their diet (Toft, 1981). A lack of selection in prey can have important conservation implications, suggesting that the species might be more resilient to shifts in community composition caused by habitat change (Raubenheimer, Simpson & Tait, 2012) or change in prey diversity (Lister & Garcia, 2018). Also, generalist feeders, especially higher-order consumers, can have a stabilizing effect on food-webs (Rooney et al., 2006). On the other hand, it can be speculated that species which frequently engage in intra-guild predation, cannibalism and necrophagy might be especially at risk in the case of an emerging disease or parasite, since such behaviour increases the risk of transmission of different diseases (Pfennig, 2000; Harp & Petranka, 2006; Brunner, Schock & Collins, 2007).

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