On the Advantages of Putative Cannibalism in American Toad Tadpoles (Bufo A. Americanus): Is It Active or Passive and Why?

By Heinen, Joel T.; Abdella, Jennifer A. | The American Midland Naturalist, April 2005 | Go to article overview

On the Advantages of Putative Cannibalism in American Toad Tadpoles (Bufo A. Americanus): Is It Active or Passive and Why?


Heinen, Joel T., Abdella, Jennifer A., The American Midland Naturalist


ABSTRACT.-

We performed two experiments to address the questions of whether toad tadpoles (Bufo a. americanus): (1) gain an advantage from consuming conspecifics and (2) engage in active cannibalism as opposed to scavenging. Our results show that tadpoles fed algal mats (and associated debris found within them) from their natal pond and supplemented on the bodies of dead tadpoles for 28 d attained an average of 5 more stages of development than tadpoles fed only on algal mats, which suggests a strong advantage to eating conspecifics. No tadpoles fed algal mats died, which suggests that this is an adequate food source. In a series of trials used to address the second question, we found no indication that tadpoles engage in active cannibalism. We tested this under conditions of hunger and using injured tadpoles as potential prey and progressively older tadpoles as potential cannibals. In no cases did we observe any tadpole attacking living tadpoles (even if injured) within 1-h after being placed in experimental tanks. Although some tadpoles were missing from tanks after 3-d periods, our results suggest that some (e.g., injured) tadpoles may succumb and are eaten thereafter. Test tadpoles began consuming dead crushed tadpoles significantly more quickly than dead intact tadpoles, suggesting that cues used to induce feeding are chemical and perhaps a result of some bacterial decomposition. We suggest that toad tadpoles have not evolved active cannibalism because of energetic and other costs and because mortality rates of tadpoles are naturally high in shallow ephemeral breeding ponds. Living tadpoles thus have access to dead tadpoles as a food source in such circumstances without incurring some costs of cannibalism.

INTRODUCTION

Cannibalism is recognized across a wide variety of animal taxa under various conditions (Elgar and Crespi, 1992). Benefits of this behavior are a ready food source that contains proper lipid, protein and mineral components (e.g., Christie, 1982; Wildy et al., 1998; Arts and Wainman, 1999). Studies demonstrate growth and developmental advantages to cannibalism for many taxa (e.g., Meffe and Crump, 1987; Crump, 1990), but costs can be numerous. They include risk of injury or death, parasite or disease transmission and the possibility of eating close relatives (Crump, 1992; Pfennig et al., 1998). Larval amphibians are highly variable with respect to the known incidence and types of cannibalistic behavior (Polis, 1981; Crump, 1986; Caldwell and Arujo, 1998). Both obligate and facultative cannibalism are known across various amphibian taxa (Crump, 1983; Pfennig and Frankino, 1997) and morphological and physiological adaptations related to cannibalism have been studied across many taxa under different ecological circumstances (e.g., Newman, 1987; Petranka and Thomas, 1995; Kam et al., 1997; Grassland, 1998a; Petranka et al., 1998).

Many generalized anuran larvae from temperate habitats such as toads (Bufo) feed on conspecifics (below), but it is not known whether this is active cannibalism or if the behavior consists only of feeding on dead animals. This is more-appropriately defined as scavenging (Elgar and Crespi, 1992). Such species are predominantly grazers and filter feeders that lack the mouth structures of actively predatory tadpoles, but this may not preclude active facultative cannibalism if conspecifics are injured or significantly smaller than those feeding on them (e.g., Kusano et al., 1985). Most such temperate species breed in large wetland complexes containing thousands of conspecific tadpoles that may represent an important food source. Some (e.g., Bufo) school in sibling groups, metamorphose synchronously and recognize kin (Arnold and Wassersug, 1978; Waldman, 1985, 1991; Heinen, 1993a) although chemical mechanisms for kin recognition are poorly known in most taxa (e.g., Cornell et al., 1989; Gamboa et al., 1991; Wakahara, 1997). Toxicity of both eggs and tadpoles promote predator avoidance and have been proposed as reasons for sibling aggregations in toads (Crossland, 1998b). Studies suggest that more cannibalistic forms are also more likely to be able to recognize kin in various amphibian taxa (Walls and Roudebush, 1991; Pfennig, 1998, 1999).

Incidental observations show that Bufo americanus tadpoles, which presumably aggregate in kin-based schools (Waldman, 1985), can be frequently found in small groups feeding on dead conspecifics. It is not known whether this constitutes cannibalism as opposed to scavenging. Even if such behavior is not actively cannibalistic, it may be selected for if tadpoles gain some advantage in growth and development. Here we perform several experiments to test the hypotheses that: (1) there is an advantage to feeding on conspecifics and, if so, (2) toad tadpoles engage in active cannibalism.

METHODS

Two experiments are reported (Table 1). All tadpoles were captured from Van Pond, located 2 km N of Pellston, Emmet County, Michigan, adjacent to the property of the University of Michigan Biological Station. The pond covers >0.5 ha in Spring and <0.2 ha in Summer; extensive algal mats are found throughout where water is present. Depth in the permanent section of the pond is about 1.5 m in Spring and <0.75 m in Summer (Heinen, 1993a, b, 1994). Here we report methods and results separately for each experiment.

Experiment 1.-In order to test the hypothesis that toad tadpoles gain an advantage by eating conspecifics, we placed 40 randomly-selected tadpoles in each often 40-1 aquaria (400 tadpoles total) for 4 wk (24 May to 21 June 2000). Tap water was used and depth was maintained at 7 cm. Broken clay pots were placed in each aquarium so that individuals had shallow water, hiding places and a terrestrial refuge available post-metamorphosis. Algal mats and their associated debris from Van Pond were placed in all aquaria; mats were cut to 100 sq cm and averaged 1 cm thick. Half of the water in each aquarium was replaced daily and algal mats were replaced every 3 d. Five aquaria served as controls and five served as treatments. Ten previously frozen and thawed tadpoles were placed in each of the treatment tanks daily throughout the time period. Any remaining dead tadpoles or parts were removed daily from treatment tanks. Algal mats, including all organisms found within them (see below), were the only food source in control tanks. All remaining tadpoles were assigned Gosner (1960) development stages at the end of 4 wk; a Mann-Whitney U test was used to test the hypothesis that tadpoles supplemented with dead tadpoles had attained greater development over the time period than did those fed algal mats alone.

Experiment 2.-We tested the hypothesis that toad tadpoles actively cannibalize-and (if so) under what conditions-by varying degree of hunger and by using injured and dead tadpoles as potential food sources. We hypothesized that if tadpoles engage in active cannibalism, they are more likely to do so with injured individuals or when food is limited. If tadpoles only scavenge, then they should feed only on dead conspecih'cs under any circumstances. Because cannibalistic behavior can change with the age and development stage in other species (e.g., Crump 1986, 1992), we replicated the experiment five times at 4-d intervals beginning 23 May and ending 10 June 2000, using progressively older tadpoles. We assigned Gosner (1960) development stages to 20 randomly selected tadpoles captured for each time period to measure whether more-developed tadpoles were, in fact, used over time.

We tested controls and five different treatments in 20-1 aquaria in which tap water was used and algal mats were placed ('fed' tadpoles) and controls and three different treatments in aquaria in which reverse osmotic water was used and no algal mats were placed ('hungry' tadpoles; Table 1). Three replicates were performed for each control and each treatment during each time period. In total, we used 30, 20-1 aquaria: 18 for the fed controls and treatments and 12 for the hungry controls and treatments (see below). Twenty-five tadpoles were placed into each aquarium at the start of each trial, to which two additional tadpoles were added; the latter determined the treatment.

For controls, two living non-injured tadpoles were placed in each tank. For treatments, two injured tadpoles, with one of three different types of injuries, or two dead tadpoles that had been manipulated differently, were placed into each tank. We hypothesized that if toads engage in active cannibalism, they are likely to detect and attack injured conspecifics but we had no a priori idea of what kinds of cues they may use. Therefore, we simulated injuries to which tadpoles might be exposed in the wild if they are attacked by, for example, a turtle, carnivorous beetle or fish. We also required that injuries should not in themselves be fatal (to test the main question of cannibalism), but that injuries should break the skin and provide chemical cues via the release of some body fluids. We, thus, injured 40 tadpoles for each of the three types of injuries as controls and placed them separately in 100 ml beakers with tap water and algal mats as a food source for 3 d to assess whether the injuries themselves caused mortality.

The treatments we simulated (for fed tadpoles) were: (1) injured, caudal (tail cut off with a razor blade at half its length), (2) injured, poked (a pin was used to poke the tadpole once through the skin on the ventral surface, halfway between the cloaca and the gill slits), (3) injured, cut (a razor blade was used to make a 2 mm incision through the ventral skin), (4) dead, intact (previously frozen and thawed tadpoles were placed in the tank) and (5) dead, crushed (previously frozen and thawed tadpoles were crushed and then placed in the tank). For these treatments, the control or manipulated tadpoles were placed in the tanks on the first day of the trial. For 1-h thereafter we observed tanks to determine whether there were any attacks or cannibalistic behavior and we counted the number of tadpoles to see if any were missing after three days, which could imply cannibalism (see below).

In the case of hungry tadpoles (those placed in tanks with no algal mats and reverse osmotic water) we used controls and the three injured treatments (above) as our observations suggested that fed tadpoles would feed on dead conspecifics, so it is obvious that hungry individuals would as well. Thus, we did not test the hungry tadpoles with dead, intact or dead, crushed tadpoles. There was one other deviation between the hungry and the fed treatments: in the hungry treatments, we placed the additional two tadpoles in the tanks with 25 conspecifics on the third dav of the trial-and kept them in for only 1 d-to assure that the original 25 were, in fact, hungry when they were exposed to either control (non-injured) or experimental (injured) tadpoles. As in fed treatments, we observed tanks for 1-h after placing the additional tadpoles to determine if there were any attacks or cannibalistic behavior. In this case, we counted the number of individuals left after 4 d of the experiment, which was only one day after placement of the additional two tadpoles. We also placed 40 tadpoles separately into 100 ml beakers with reverse osmotic water and no food source for 3 d as hunger controls because starvation over the trial period would complicate statistical analyses.

Trials for all treatments were replicated five times. These were: (1) 23 to 27 May, (2) 27 to 31 May, (3) 31 May to 3 June, (4) 3 to 7June and (5) 7 to 10 June 2000. In all cases, new tadpoles were captured from Van Pond for each trial, and tadpoles previously used were released after capturing new specimens. Since the density of tadpoles was consistently very high in all shallow areas of Van Pond and we spread our capture efforts widely, we assume that new tadpoles captured had not been previously used. All tadpoles were randomized for use in all treatments across the time period. ANOVAs (below) were used to test the effects of treatment (non-injured versus injured versus dead) and time of trial over the entire period (and interactions therein) on cannibalistic behaviors either directly observed within 1 h of placing the additional two tadpoles in each tank or inferred based on the number of individuals left in each tank after 3 d for the fed treatments and after 1 d for the hungry treatments. Lastly, we collected samples of algal mats from Van Pond and had all recognizable taxa, and rank-order abundance, identified and counted to document (generally) what food sources are widely available to tadpoles at this site.

RESULTS AND DISCUSSION

The results of Experiment 1 were highly significant. Those tadpoles supplied ad lib. with algal mats and daily supplemented with dead tadpoles averaged 5.2 Gosner developmental stages more than those supplied ad lib. with algal mats alone (U = 3; n^sub 1^ = n^sub 2^ = 5; P < 0.01). Based on Gosner (1960), tadpoles supplemented with dead tadpoles reached an average stage of 41.7 ± 3.2, compared to 36.5 ± 3.4 for those fed algal mats alone (mean ± 1 SD in both cases). Of 200 individuals in each group, more of those supplemented with dead tadpoles had metamorphosed by the time the experiment was complete, compared with those fed algal mats only (44 or 22% compared to 14 or 7%). Other work completed in freshwater aquatic systems has shown similar results for both larval amphibians and fish (e.g., Meffe and Crump, 1987). It is likely that lipids from conspecifics are important in these findings (Arts and Wainman, 1999), but other components such as proteins and inorganic nutrients may also play a role in allowing higher rates of development. Of the original 400 tadpoles in both experimental and control tanks, none died. There is, thus, no indication that withholding dead tadpoles (in controls) as a food source resulted in mortality, although differences in developmental stage were strong.

The results of Experiment 2 gave no indication that toad tadpoles engage in active cannibalism. In no cases, with either algal mat-fed tadpoles (fed treatments) or tadpoles kept in reverse osmotic water for 3 d (hungry treatments), did we observe tadpoles attacking living but injured tadpoles within the first 1-h observation period. This was true regardless of the type of injury, and throughout the time period, so there was no indication that age or developmental stage correlated with a propensity to cannibalize.

Quantitatively, diatoms of eight genera and blue-green algae of six genera dominated the composition of algal mats (i.e., >60% of all biomass) collected at Van Pond, the primary food source for toad tadpoles. Many other organisms were also identified. These included two genera of green algae, four genera of desmids and parts of insects or other invertebrates such as mosquito larvae, chironomids and ostracods (Table 2). Both small flagellate and large ciliate protozoa were also identified, as were two genera of rotifers. Finally, algal mats contained detritus such as terrestrial plant matter, pollen grains, fungal spores and bacteriallycolonized dead organic matter. We observed on many occasions, both in field and lab, tadpoles feeding on both algae and parts of dead insects. Presumably, they are taking in all components of algal mats while feeding, but may prefer animal parts when available because of the likely higher lipid and protein components compared to the more abundant algae.

In all cases, dead tadpoles placed in tanks with tadpoles fed with algal mats were fed upon; feeding in all cases began within the initial 1-h observation period. Feeding on tadpoles that had been crushed began an average of 6 min earlier compared to those placed dead but intact in tanks with live tadpoles (t = 1.98; df = 28; P < 0.05; Table 3). From one-way ANOVAs, we determined that older tadpoles fed upon dead tadpoles (both intact and crushed) more quickly than did younger tadpoles (f^sub (intact)^ =21.5; f^sub (crushed)^ = 28.8; P < 0.05 in both case; Table 3), but there were no other significant relationships based on treatment, age of tadpoles over time, or types of injuries received and the propensity to cannibalize. The hungry controls showed that hunger did not cause mortality. Of 40 tadpoles kept in reverse-osmotic water (and no algal mats) alone for 3-d periods, none died. Of 40 tadpoles kept alone in each of the three injured controls (caudal, poked and cut) none died within 1 h, although three (of 120) died over the 3-d period; two had received the cut injury and one had received the poked injury. No tadpoles that received the caudal injury died in these controls.

Thus, very few animals died over 3-d periods as a result of injury in the mortality controls for Experiment 2. Results from multi-way ANOVAs showed no relationships or interaction terms consistent with the primary question of differential cannibalism under conditions of hunger, or using injured tadpoles, over time. Thus, the most parsimonious explanation for our results collectively is that those few injured tadpoles that were missing after 3 d in trials in Experiment 2 (a total of 7 individuals for all trials, treatments and replicates combined) had died sometime over the 3-d time period as a result of injury or some natural mortality factor (i.e., not as a result of attack) and were later eaten. Our results, thus, suggest that toad tadpoles readily engage in scavenging but not cannibalism. Given that dead crushed tadpoles were fed upon significantly more quickly that dead intact tadpoles, it is likely that tadpoles receive some chemical cues from skin or from internal organs after conspecifics die (Table 3). Given that tadpoles showed no propensity to attack injured tadpoles, it is also likely that any chemical cue results from dead tissue, or lack of movement, and not from internal body fluids of live tadpoles. Many of the injured caudal tadpoles, for example, visibly bled small amounts around the wound. Yet none were attacked within 1-h observation periods (and none died in controls for this injury).

There is a demonstrable advantage in growth and development to eating conspecifics (Experiment 1), and tadpoles are able to get through the skin of dead intact tadpoles rather quickly (Experiments). They could presumably do so with injured tadpoles-or perhaps with uninjured tadpoles of smaller size-yet we found no evidence for this. Although size was not a primary factor of analysis in these experiments, all tadpoles were randomized and there were visible differences in the sizes of animals placed in all treatments for both experiments (Table 3). As a consequence, large tadpoles were regularly placed with smaller tadpoles. Given that we observed tanks for 1-h at the start of each trial and recorded all losses over 3 d, we would have observed cannibalistic behaviors directed towards smaller tadpoles if they occurred. Thus, we found no evidence for active cannibalism in Experiment 2 as described in the Introduction under any circumstances, despite the developmental advantages shown in Experiment 1.

The reasons for this result are perhaps related to the overall ecology of toad tadpoles and to environmental conditions in and around the breeding ponds themselves. Here we will consider each in turn. Given that toad tadpoles have mouth parts appropriate for filter feeding and algal grazing typical of anuran larvae that are primarily algal feeders, it is likely that piercing the skin of live conspecifics is a slow and inefficient process and that the process is simplified with dead conspecifics if bacterial breakdown begins shortly after death. Thus, attacking live tadpoles of smaller size, or injured tadpoles that are still able to move, would be energetically costly. We know of no work that shows this directly but it seems likely based on the type of breeding ponds toads use. They tend to be shallow, highly productive and warm and, thus, bacterial breakdown begins more quickly than in deeper and cooler environments. Within such ponds toad tadpoles prefer shallow warmer areas, suggesting that they behaviorally thermoregulate to enhance growth rates (Dupre and Petranka, 1985). Toad tadpoles presumably prefer such sites to attain higher developmental rates, thus permitting more post-metamorphic development before the first hibernation period. This is consistent with work that shows that newly-metamorphosed toads are diurnal (in contrast to adults of many species), thus attaining high growth rates by maintaining high levels of activity and feeding (Lillywhite et al., 1973). This is in contrast to the some ranid frogs in the region (e.g., Rana catesbeiana, R. clamitans and R. pipiens) that frequently over-winter as tadpoles. The latter two species also breed in Van Pond (Heinen and Hammond, 1997), but their tadpoles are generally seen in permanent parts of the pond and virtually never in water less than about 5 cm deep (field observations). Toad tadpoles are generally seen in water less than 5 cm deep and frequently in water less than 2 cm deep.

Some natural mortality is associated with the propensity of toad tadpoles to remain in very shallow water. It is common around Van and other breeding ponds to find dead tadpoles that had been stranded in areas that had dried. With so little relief around these shallow ponds, one rainfall can reconnect such areas to other portions of the pond and, thus, dead tadpoles are regularly available as a food source to live tadpoles under these circumstances. From field observations, we found that raccoons (Procyon lotor), white-tailed deer (Odocoileus virginiana) and large wading birds such as Great Blue Heron (Ardea herodius) frequented the pond and regularly walked through shallow areas. Since toad tadpoles congregate in great numbers in very shallow water, some are trampled inadvertently. We witnessed small groups of tadpoles (up to eight individuals) feeding on dead conspecifics each time we visited Van Pond (every 3 to 4 d throughout the experimental period); in all cases, they were seen in shallow water, 2 cm or less in depth. Our results suggest that toad tadpoles feed only on conspecifics that succumb to desiccation, trampling or other natural mortality factors. Thus the behaviors we observed constitute scavenging and not cannibalism.

Finally, several aspects of the experimental results reported here are preliminary and raise numerous questions for further study. For example, we kept densities constant and relatively low compared to the situation in most breeding ponds. This was done because we had to count each individual and, in the case of Experiment 2, watch all tadpoles for 1-h periods to assess whether cannibalism was occurring. Further experiments with density as a main variable could yield different results. We also kept water depth and temperature constant, whereas repeating Experiment 2 under varying water depths and temperatures may show, for example, that toad tadpoles may actively cannibalize under stressful conditions of shallow depths and very warm water indicative of a rapidly-deteriorating larval environment. Also, our results show that tadpoles fed readily on dead tadpoles under all circumstances, and yet there are potential direct costs to this behavior (e.g., disease transmission; Pfennig et al., 1998). Our results presumably mean that the risk is generally low compared to the developmental advantage. However, tadpoles also may have some mechanism to discern if a dead tadpole were diseased. The dead tadpoles used here (both intact and crushed) were all healthy, painlessly killed by freezing and fed fresh (after a 10-min thawing period) to tadpoles. Experimenting with carcasses killed by disease-and/or in varying stages of decomposition-may shed light on the acceptability of this food source and to what degree olfactory or other cues are important in deciding when, and whether, to feed on dead tadpoles. Further work will be needed to assess these various possibilities.

In summary, our results show that there is a strong advantage to eating conspecifics in that toad tadpoles attained significantly higher rates of development when supplemented with dead tadpoles. In light of other work, it is likely that lipids play a major role in this advantage (e.g., Arts and Wainman, 1999), but other components such as proteins or inorganic nutrients may also be important; more research on this particular question is needed. However, there is no indication that toad tadpoles actively cannibalize injured or smaller conspecifics, whether fed or hungry and in spite of this advantage. We suggest that this is because the most easily available food sources are algal mats and animal remnants found therein for which grazing mouthparts are most efficient. Although toad tadpoles fed ad lib. on algal mats fed readily on dead tadpoles when they were available, no tadpoles in the controls in Experiment 1 (i.e., those fed on algal mats alone) died over the 1-mo time period, and some (14 of 200) metamorphosed. This indicates that algal mats are adequate, but not optimal, food sources. Our results are preliminary and don't address other possibilities such as the potential effects of varying tadpole density, water depth and temperature on the propensity to cannibalize. Under very extreme conditions (e.g., hungry and at high densities in very shallow, warm water) it is possible that toad tadpoles will cannibalize; we found no evidence for this under relatively less-stressful circumstances explored here. Specific cues tadpoles may use to assess whether a dead tadpole is edible or not (e.g., due to death by disease or the degree of decomposition) are also unknown. Thus, a great deal more work could be done on this system to shed light on sensory mechanisms and environmental conditions that may elicit putatively-cannibalistic behaviors.

Acknowledgments.-We thank Bob Vande Kopple and Sherry Webster for supplying us with laboratory space and equipment, especially for the timely procurement of a number of new aquaria. Nancy Tuchman graciously identified organisms found in algal mats from Van Pond and Jay Sah helped with statistical analyses. Comments from several anonymous reviewers and the Editor improved earlier drafts. This work was approved by the University of Michigan's Committee on the Use and Care of Animals and was completed at the University of Michigan Biological Station, Pellston, Michigan in May and June 2000.

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SUBMITTED 13 FEBRUARY 2004 ACCEPTED 16 JULY 2004

[Author Affiliation]

JOEL T. HEINEN1

Department of Environmental Studies, Florida International University, Miami 33199

AND

JENNIFER A. ABDELLA2

School of Natural Resources and Environment, University of Michigan, Ann Arbor 48109

[Author Affiliation]

1 Corresponding author: e-mail: heinenj@fiu.edu

2 Present address: Vermont Law School, P.O. Box 96, South Royalton 05068

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On the Advantages of Putative Cannibalism in American Toad Tadpoles (Bufo A. Americanus): Is It Active or Passive and Why?
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    1. Lois J. Einhorn, Abraham Lincoln, the Orator: Penetrating the Lincoln Legend (Westport, CT: Greenwood Press, 1992), 25, http://www.questia.com/read/27419298.

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