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Explosive breeding reduces egg and tadpole cannibalism in the wood frog, Rana sylvatica
Anim. Behav.,
1995, 50, 731-739
Explosivebreedingreducesegg and tadpole cannibalismin the wood frog, Rana sylvatica JAMES W. PETRANKA Department
of Biology,
& DAPHNE University
A. G. THOMAS
of North
Carolina
(Received 10 August 1994; initial acceptance 24 October 1994; final acceptance 4 January 1995; MS. number: a7060j
Abstract. Cannibalism of anuran eggs and hatchlings by larger tadpoles has been documented in many speciesthat inhabit seasonally ephemeral habitats and has been hypothesized to play an important role in favouring synchronized breeding. Using the wood frog, this hypothesis was tested by determining whetheroffspring of non-synchronized breeders were more vulnerable to cannibalism than offspring of synchronizedbreeders. In a laboratory experiment, small tadpoles of similar size did not cannibalize eachother. However, large tadpoles preyed heavily on the eggs and hatchlings of conspecifics, and the incidenceof predation increased with cannibal size. In natural populations, over 80% of adults bred explosivelyduring a 3-day period, and their offspring were not cannibalized because hatching was synchronized and tadpoles varied only slightly in size. About 5% of adults oviposited late in the breedingseason, and the resulting embryos hatched when tadpoles of synchronized breeders averaged 0.6-1.3g. Larger tadpoles in the ponds cannibalized the eggs and hatchlings of these late breeders. In a field experiment conducted at a natural breeding site, eggs that were added 7 days after embryos of late breeders hatched suffered complete mortality within 19 h. Similarly, more than 50% of hatchlings werecannibalized within 15 min after they were placed in the pond. These results are consistent with the view that synchronized breeding is an adaptation that reduces cannibalism in anurans that breed in temporary ponds. 0 1995 The Association for the Study of Animal Behaviour Breeding phenologies are important elements of amphibian life-history strategies that can affect community composition, population size and structure, and larval life-history traits (Keen 1975; Rose& Armentrout 1976; Harris 1980; Alford & Wilbur 1985; Kats et al. 1994). Aspects of breeding phenology that can potentially influence adult fitness include the frequency and duration of individual breeding bouts as well as the seasonal time of breeding (Blair 1961; Dixon & Heyer 1968). Comparative studies suggest that speciesspecificbreeding phenologies are adaptive and often correlate with breeding habitat, seasonal changesin climate, or the presence of potential competitors or predators (Bragg 1945; Wilbur & Alford 1985; Duellman & Trueb 1986). One well-documented dichotomy in amphibian breeding phenology is the explosive or synchronous breeding pattern of many species,compared to the more continuous pattern of others. The Correspondence: J. ogy, University 2299,U.S.A.
W. of North
0003-3472/95/090731+09
Petranka,Department Carolina,
$12.0010
Asheville,
of BiolNC 28804-
degree of breeding synchrony may be viewed as a continuum that ranges from species such as spadefoot toads, Scaphiopus spp., in which a local population may restrict its breeding to a single day, to those such as the red-spotted newt, Notophthalmus viridescens, which breeds continuously over several months. Explosive breeding is common in many species that use seasonally ephemeral habitats such as vernal ponds and tropical rain pools, and may involve a single annual bout, or several explosive bouts over a prolonged breeding season (Heyer et al. 1975; Crump 1983; Newman 1987). Changes in climate or weather often provide narrow windows of opportunity for individuals to exploit seasonally ephemeral habitats, and individuals typically arrive en masse at breeding sites shortly after ponds fill or conditions become suitable for migrations. The widespread occurrence of explosive breeding in many temporary pond breeders suggests that individuals that breed relatively late during a breeding bout have lower fitness than synchronized breeders. The selection pressuresthat favour
Q 1995 The Association
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for the Study
of Animal
Behaviour
132
Animal
Behaviour,
early, synchronized breeding in temporary pond breeders are complex and probably operate on both the adult and larval stages. Tadpoles that hatch early, for example, may minimize predation risk because of predator lags (Wilbur 1980) and have more time to complete the larva1 period before habitats dry (Newman 1987). Where sizespecific competition and priority effects occur, tadpoles of early breeders may be competitively superior to those of late arrivers (Travis 1983; Alford & Wilbur 1985; Wilbur & Alford 1985). Factors that relate to the adult stage, such as sexual competition, the ability to find a mate, and predation risk to breeding or migrating adults, may also influence breeding phenologies (Greer & Wells 1980; Godwin & Roble 1983; Woodward & Mitchell 1990). Crump (1992) and Heusser (1970) hypothesized that cannibalism could potentially play an important role in favouring explosive breeding in amphibians that use seasonally ephemeral habitats. Because cannibalism by larva1 amphibians often involves larger individuals preying on eggs or smaller larvae, the frequency of cannibalism often increaseswith sizevariation in a population (Degani et al. 1980; Kusano et al. 1985; Nyman et al. 1993). Synchronized breeding produces weakly size-structured populations and could potentially reduce cannibalism by size-selective predators. Here, we test this hypothesis using the wood frog. The wood frog occurs from Alaska to New England and south through the southern Appalachians to Alabama and Georgia. Although this widely distributed speciesfavours moist forests, it also inhabits western grasslandsand northern tundra (Berven & Grudzien 1990). Adults emerge from winter hibernacula to breed in winter or early spring and deposit egg massesin communal groups in seasonally ephemeral habitats that lack fish (Waldman 1982; Berven & Grudzien 1990). Breeding is explosive and most oviposition within local populations occurs during a I-2-week period (Waldman 1982). Tadpole densities are often very high in breeding ponds (Biesterfeldt et al. 1993), and the tadpole stage normally lasts from 2 to 5 months. Cannibalism has not been documented in R. sylvatica, although Bleakney (1958) observed hundreds of tadpoles that appeared to have eaten portions of each others’ tails. Petranka et al. (1994) reported that R. sylvatica tadpoles are voracious predators on the eggs and hatchlings of
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American toads, Bufo americanus. The propensity of R. sylvatica tadpoles to prey on toad eggs and hatchlings suggeststhat tadpoles would also can. nibalize the eggs or hatchlings of late breeders. This, in turn, might select for synchronized breeding and hatching, which would minimize cannibal. ism risk. To test this hypothesis, we conducted studies to determine whether R sylvatica tadpoles are cannibalistic and whether cannibalism rate varies with cannibal size and prey developmental stage. In addition, we monitored breeding and hatching periods in natural breeding sites to deter. mine whether late breeders were vulnerable to egg or hatchling cannibalism. METHODS Experiment 1: Does Cannibalism Frequency Depend on Predator Size and Prey Life-history Stage? We conducted a 2 x 4 factorial experiment to examine size-specificcannibalism of embryos and hatchlings by tadpoles. The two factors were the initial developmental stages of the prey (embryos versus hatchlings) and the level of risk to the prey We manipulated level of risk by using predator treatments that consisted of small, medium and large tadpoles, as well as controls with no tadpoles (minima1 risk). Becausethe frequency of cannibal. ism often increaseswith the average sizedifference between predator and prey, we assumed that risk of cannibalism increased with sizeof the potential tadpole cannibal. To generate three sizecohorts for use as potential cannibals, we collected egg massesfrom breed. ing ponds on 9 February, 20-22 February and 2 March 1994 and grew hatchlings in 38-189~litre~ aquaria for 3-21 days. We reared tadpoles at room temperature with an uncontrolled light:dark cycle and fed all three cohorts powdered rabbit chow ad libitum once or twice daily. Immediately before initiating the experiment, we pooled tadpoles from all tanks and used sieves to sort them into small, medium and large groups. Respective mean masses (&SE; N=20) were 0.44 % 0.01 g, 0.99 f 0.07 g and 1.95 f 0.09 g. A fourth treatment consisted of controls with no tadpoles. The experiment was a randomized blocked design with four replicates. We tested animals at room temperature (ca 21°C) in plastic containers
Petranka
& Thomas: Cannibalism
measuring20 x 10 x 15 cm. Each container held 2.7litresof water and was bubbled with air so that oxygenlevels were near saturation. We arranged containersin four blocks (Iv’=8 containers per block)along two laboratory benches and assigned treatmentsrandomly to containers within each block.We added 20 small, medium or large tadpolesto appropriate containers, then fed tadpoles 14Omgof powdered rabbit chow per g of wet massto assure that hunger levels were approximatelythe same for all size classes.After allowing 1day for tadpoles to acclimatize, we added to eachcontainer either 40 hatchlings (Gosner stages 20-22;mass, XLIZSE= 83 f 3 mg for a sample of 15 hatchlings)or 40 late-term eggs (embryos within theenclosed jelly coats were at Gosner stages K-19). We observed containers during the first hour of the experiment and recorded any instancesof cannibalism. We then checked containersat l-day intervals for 3 days and scored the numberof missing prey. DocumentingBreeding and Hatching Periods in NaturalPopulations We documented the breeding phenology and hatchingdates of wood frogs at six natural and semi-naturalponds within 10 km of Bamardsville, BuncombeCounty, North Carolina. One site was anaturalvernal pond, whereas the remaining sites weresmall (~50 m2) water-filled depressionsin the bedsof old logging roads within the Pisgah National Forest. Pond A was located approximately8 km from the remaining cluster of ponds whichwere within 500 m of each other. We visited sites every l-5 days from the initiation of breeding on 9 February until hatching terminated on 2 April.We visited sites more frequently (l-3 days) duringbreeding and hatching periods to documentmore preciselythe timing of these events. On eachvisit we censusedall egg massesin each pond, then marked and recorded the developmental stagesof a subset (N=l-7 masses per pond) of newlylaid eggs. We marked masses with dowel rodsplaced through each mass, and used marked massesto estimate the incubation period and hatchingdates of eggs from different breeding bouts.Hatching of egg masses laid during l-day breedingbouts sometimes lasted as long as 5-6 daysduring cold weather. Becausethe percentages of embryoshatching on a given day could not be preciselydetermined, we used mid-points of the
in wood frogs
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entire hatching period to approximate the average time of hatching and length of the incubation period. We estimated the wet mass and growth rates of tadpoles in each pond from the initiation of hatching (9 March) through the first week of April by weighing 10-15 tadpoles that were haphazardly collected while wading through each pond. Tadpoles were blotted with paper tissue to remove external water before being weighed to the nearest milligram on an electronic balance. Experiment 2: Are Offspring of Late Breeders Vulnerable to Cannibalism in Nature? To determine whether the offspring of late breeders are vulnerable to cannibalism in the field, we monitored the survival of eggs and hatchlings experimentally added to pond B on 2 April. About 85% of adults deposited eggs at this site during 20-22 February. However, breeding did not terminate until 10 March, when single egg masseswere deposited in pond B and two adjoining ponds. Hatching of the eggs of late breeders ended on 25 March in pond B and 2 April in ponds D-F. To determine whether hatchlings of late-breeders were vulnerable to cannibalism, we conducted 22 trials in which individual hatchlings were added to the pond in the vicinity of resident tadpoles. Test animals were less than 24 h posthatching, were at Gosner stages20-22, and averaged 92*3 mg and 9.3 *0.2mm total length (N= 15). We placed uninjured hatchlings with intact tail fins within 0.5 m of the edge of the pond where we could clearly observe behavioural interactions without disturbing resident tadpoles. We watched each focal animal continuously from the shoreline for a maximum of 15 min and recorded all attacks or kills by conspecifics. We recovered all hatchlings that survived for 15 min and inspected them for injuries such as bites out of the tail fins or yolk sac. We conducted the trials during the afternoon when water temperatures averaged 23.5’C. We visually estimated that the pond contained at least 100 000 tadpoles, with local densities exceeding 2000 tadpoles/m2. Hence, we assumed that the trials were independent and that the probability that a particular resident was involved in more than one attack was very small. To determine whether tadpoles would prey on eggs, we added 50 eggs at Gosner stages 10-16 to each of five locations around the perimeter of the pond. Eggs used in the experiment were teased
734
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Behaviour,
apart from a single mass. We placed eggs in shallow water near the pond edge then observed tadpole feeding responsesfor 30 min. We checked each group after 19 h to determine the number of eggs surviving. We released all surviving tadpoles used in laboratory and field studies in a natural breeding pond.
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ing in frenetic feeding activity in the vicinity of the injured animal. This behaviour appeared to be in response to the release of body fluids or yolk from injured hatchlings, and often resulted in injured animals being cannibalized. During the first hour of observation, 32 hatchlings were cannibalized and 11 other hatchlings sustained visible injuries. Numerous tadpoles were observed feeding on Field Observations of Cannibalism the jelly coat that surrounded the eggs. However, We visited ponds during 20-24 March to docu- we observed only two instances of egg predation ment cannibalism of the offspring of late-term during the first hour of the experiment. In one breeders during the hatching period. Egg masses case a single tadpole penetrated the jelly coat and were inspected for evidence of predation, and a consumed an embryo. In the second instance a preliminary experiment similar to that described group of feeding tadpoles collectively fed upon the in experiment 2 was conducted to determine if jelly coat and embryo of an egg. Patterns of survival varied markedly between hatchlings were vulnerable to cannibalism. treatment groups during the ensuing 3 days (Fig. 1). Mortality of late-term embryos was relatively Statistical Analyses constant for the first 2 days of the experiment and averaged 10% per day overall. Hatching began We analysed the results of the laboratory experiment with ANOVA and repeated-measures near the end of day 2 and 99% of the surviving ANOVA using log-transformed data. Block embryos hatched before the termination of the effects were not significant and were excluded experiment. Age-specific mortality increased dur. from the model. Mean survival in control groups ing day 3 for all three size treatments. This was 100% and there was no variation in the data. increase in mortality corresponded to the time Becauseuse of control data would grossly violate when most embryos hatched. In the hatchling the assumption of homogeneity of variances treatment, mortality was confined almost entirely between treatment groups, we excluded this from to day 1, when hatchlings were immobile and the analysis and only compared the three tadpole responded to attacks with relatively weak uncoordinated swimming. After day 1 mos size classes. tadpoles exhibited coordinated swimming and rapidly fled when approached by potential cannibals. RESULTS Mortality of eggs and hatchlings increased win mean sizeof the predatory tadpoles (Fig. 1). After Experiment 1 2 days, 15, 18 and 27% of embryos were consumed~ We observed 22 instances of larger tadpoles in the small, medium and large tadpole treatment\’ attacking conspecific hatchlings during the first respectively. Similarly, mortality of hatchlingr hour of the laboratory experiment. Typically, after 3 days was 12, 18 and 39%, respectively. Na individuals would tilt the body and orient the mortality occurred in any of the control contains head downward, then thrust with the tail while ers, which indicates that deaths in other containen delivering a bite. Bites often resulted in visible were as a result of cannibalism. Repeated, injuries that consisted of U-shaped plugs that measures ANOVA indicated that the overall pat. were most often taken from the belly where yolk terns of survival were significantly affected by reserves were concentrated (42% of injuries) or tadpole size (P=O.OOOS), but not by initial devel. from the tail fin (25% of injuries). In many cases opmental stage (P=O.72; Table I). The interaction tadpoles that bit hatchlings rapidly consumed of the two factors was significant (P=O.OOl)which them within 5-20 s after an attack began. In other presumably reflects variation in the shapes of the cases,hatchlings were injured but were not con- survivorship curves for the egg and hatchling sumed by the attacker. Neighbouring tadpoles treatments (Fig. 1). An ANOVA conducted at the responded to severelyinjured hatchlings by engag- termination of the experiment (day 3) indicated
Petranka
Egg stage
40
, Hatchlings I
2
, Free-swimming I
Source of variation
3
tadpoles
09 0
I 1
I
I _
2
3
Time (days) Figure 1. Age-specific survivorship for (a) egg and (b) hatchling treatments in the presence of small (W), medium (0), large (a), or no (0) tadpoles. Intervals abovegraphs indicate the approximate time when individuals began hatching or reached free-swimming stages in the respective treatments. that initial developmental stage (P=O.OOZ) and tadpole size (P=O.O04) significantly affected prey survival. The interaction of the two factors was not significant (P=O.78). Analysis of withintreatment (subjects) effects of the repeatedmeasures ANOVA indicated a significant day effect. In addition, all of the interaction terms were significant (PjO.02; Table I). Breeding and Hatching
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Table I. Summary statistics for repeated-measures ANOVA for experiment 1
, -‘ii 1
1 Hatchlings
in wood frogs
Between-subjects effects Stage Size Stage x size Error Within-subjects effects Day Day x stage Day x size Day x stage x size Error (day)
4ok; , 0
& Thomas: Cannibalism
Periods
Adults at most ponds engaged in three to four breeding bouts during the season which were
Between-subjects effects, whereas related trends in stage; size: mean
4
F 1
0.13
2 2 18
12.18 6.03
2 2 4 4 36
57.88 50.01 3.34 3.86
P
0.72
0~0005 0.0099
0~0001 0~0001 0.0201 0.0103
effects test for overall treatment within-subjects effects test for timesurvival. Stage: Initial developmental tadpole size; day: day of experiment.
interrupted by periods of cold weather in which breeding activity ceased. Breeding began on 9-13 February and continued until 10 March (Fig. 2). Although the overall breeding season lasted nearly 1 month, breeding was highly synchronized both within and between ponds. Overall, 81% of females oviposited on either 20 or 22 February (range=59-94% among ponds). A small percentage (2-14%) of late arrivers bred on 2 March (ponds A and D) and 10 March (ponds A, B, E and F). Hatching occurred during 6 March-2 April, and the incubation period was inversely related to time of oviposition. The day of the year that eggs were laid explained 56% of the variation in length of the incubation period of cohorts of marked egg masses (linear regression; r* = 0.56, F, ,22= 26.85, P=O.O002). As a result, embryos of very early breeders hatched within a few days of those laid during the major breeding bout of 20-22 February. Embryos from clutches deposited during 20-22 February hatched during 11-22 March. Hatchings from this cohort did not appear to be vulnerable to cannibalism because tadpoles in ponds generally averaged less than 0.2 g (Fig. 2). In contrast, offspring of late arrivers that bred in early March hatched between 22 March and 2 April when tadpoles in ponds averaged between 0.6 and 1.3 g. Mean masses of tadpoles in ponds at this time were slightly larger than the small and medium tadpoles used in the laboratory
Animal
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Behaviour,
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Figure 2. Relationship between breeding phenology, hatching dates and mean tadpole sizes in six natural breediq sites of the wood frog. n : % of the total egg massesdeposited in 1994; 0: mid-points of the hatching periods for eact cohort which, for simplicity of illustration, assume equal hatching successbetween cohorts. Lines indicate changer in the mean ( f SE) of tadpoles from the initiation of hatching onward.
experiment, and tadpoles were sufficiently large to cannibalize both the eggs and hatchlings of late breeders. Experiment
2
Of 22 hatchlings that were introduced into pond B, 12 (55%) were cannibalized during the 15min trial periods. Cannibals showed the typical feeding
behaviour that involved tilting the body down. ward into a feeding position and thrusting witi the tail while delivering a forceful bite. Feedink frenzies often ensued after a hatchling was initial11 attacked. Typically, hundreds of tadpoles began feeding frenetically in the immediate area where an animal was injured in apparent response to the release of body fluids from injured hatchlings. 01 the remaining 10 tadpoles that survived for
Petranka
& Thomas: Cannibalism
15min, 80% sustained visible injuries, including 60%with large plugs bitten out of the ventral bodywall and yolk sac. Tadpoles began feeding on eggs immediately after they were added to ponds. Within 30 min, large aggregates of tadpoles had formed in the vicinityof the eggs and hundreds of tadpoles were observedfeeding on the jelly coats. After 19 h, we wereunable to locate either eggs or the remnants of thejelly coats at any of the five siteswhere eggs wereadded to the pond.
in wood frogs
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seasonally ephemeral habitats. Our data provide support for this hypothesis and suggest that cannibalism is an important factor favouring explosive breeding in R. sylvatica. Adults at our field sites exhibited highly synchronized breeding in which 8 1% of eggswere laid during a 3-day period. Embryos from this primary breeding bout hatched relatively synchronously and sizevariation at hatching was minimal. In our laboratory experiment, variation in tadpole size in the control group was similar to that of individuals that hatched synchronously in ponds. Tadpoles in control groups that lacked larger Field Observations of Cannibalism tadpoles did not cannibalize each other during the Field observations were made on 20-24 March experiment, presumably because size variation to document natural occurrences of cannibalism. was not sufficient to allow cannibalism. ConseOn20 March we observed large tadpoles feeding quently, risk of cannibalism was minimal for on a single egg mass in pond B that was laid highly synchronized breeders in natural ponds. duringa final breeding bout on 10 March. On 22 Embryos of late breeders did not hatch until March large tadpoles were feeding on the egg tadpoles of synchronized breeders were 24 weeks massand most of the outer jelly coats had been old and averaged 061.3 g. Our laboratory eaten.Hatching of this mass occurred on 23-24 experiment indicates that the risk of cannibalism March. During this hatching period we moved increases with predator size and that tadpoles eightrecently hatched embryos to the edge of the within this size range will readily cannibalize eggs pondto observe them. In the ensuing 15 min, two and hatchlings. Our field experiment further demwerecannibalized and two sustained major in- onstrates that offspring of late arrivers are highly juries.Egg massesof late breeders in ponds C-F vulnerable to cannibalism. Eggs and hatchlings alsohad much of the outer jelly coats eaten, and that were added 7 days after embryos of late numerousembryos were missing from the masses breeders hatched had extremely high mortality thatwere presumably cannibalized. In pond A, 18 rates. Cannibalism rates for the field experiment masses were laid during a final breeding bout on were much higher than those observed for similar10March. When examined on 20-23 March, we sized tadpoles in the laboratory (i.e. large tadpole observedtadpoles feeding on most of these masses treatment) and may reflect differences in food andnumerous embryos were missing from the egg level or tadpole densities. Tadpole densities in our capsules. laboratory experiment were 666 tadpoles/m* of container, whereas Biesterfeldt et al. (1993) recorded average densities of 1816 tadpoles/m’ of DISCUSSION pond bottom for samples taken from our study sites in late March and early April. The results Cannibalism is widespread among anurans and of our field experiment suggest that offspring of hasbeen reported in at least 12 of 21 families of individuals breeding even a few days beyond the frogs(Polis & Myers 1985; Crump 1986, 1992). normal termination of breeding would suffer Nonethe less, surprisingly few data are available catastrophic mortality from cannibalism. onthe evolutionary significance of cannibalism in Wood frog tadpoles have generalized trophic naturalpopulations of anurans. Cannibalism may morphologies that are typical of microphagous bean important selection pressure favouring kin suspension-feeders. Although they lack specialrecognition in tadpoles, and could potentially ized structures such as enlarged jaws, modified favour terrestrial reproduction in adults (Crump beaks and teeth, and shortened digestive tracts 1983;Pfennig et al. 1993). Crump (1992) sum- that are often seen in highly carnivorous tadpoles marizedmany of the costs and benefits of canni- (Wassersug 1980; Wassersug et al. 1981; Crump balismand hypothesized that cannibalism might 1983) they are surprisingly efficient predators on alsofavour explosive breeding in anurans that use the eggs and hatchlings of many amphibians.
738
Petranka
Animul
Behuviour,
et al. (1994) found that predation of tadpoles on American toad eggs and hatchlings is sufficient to exclude toads from many wood frog breeding sites. We have also observed R. sylvatica tadpoles feeding on the eggs of grey tree frogs, Hyla chrysoscelis, and spotted salamanders, Ambystoma maculatum, in natural ponds. Thus, this species appears to be a major predator structuring amphibian communities in vernal ponds in the southern Appalachian Mountains. Cannibalism is undoubtedly not the only factor favouring explosive breeding in wood frogs. Waldman (1982), for example, found that eggs of early breeders that were deposited in the middle of communal rafts had higher survival than those of late breeders that laid near the periphery of rafts. Early, synchronized breeding in R. sylvatica may also be favoured because it enhances size-specific competitive ability (Wilbur 1980, 1984) and maximizes the time available for offspring to exploit productive, but transient pond communities. Cannibalism is common in natural populations where conspecific densities are high, food is limiting, and survival rates are low (Fox 1975; Polis 1981; Polis & Myers 1985). Scientists have documented a growing number of anuran tadpoles that prey on conspecific and heterospecific eggs and tadpoles (Crump 1983, 1992; Petranka et al. 1994), and most live in seasonally ephemeral habitats. Although seasonally ephemeral ponds are often highly productive (Wilbur 1980, 1984), high densities of amphibian larvae often result in intense competition for food that can slow growth, lengthen the larval period and reduce survival (Wilbur 1972, 1976; Wilbur et al. 1983). This, coupled with pond drying, should favour mechanisms such as cannibalism that accelerate growth and development rates (Crump 1983, 1992). Local densities of wood frog tadpoles at our study sites sometimes reach nearly 9000 tadpoles/m* of pond bottom (Biesterfeldt et al. 1993). At these densities, intense competition for food seems likely and cannibalism of frog eggs and the yolk reserves of hatchlings would provide a nutritive, energy-rich food source in an otherwise nutrient-poor environment. Cannibals always run the risk of reducing their inclusive fitness by eating relatives, and kin recognition may play a role in minimizing cannibalism of close relatives (Blaustein & O’Hara 1982; Pfennig et al. R. sylvatica
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1993). Rana sylvaticu tadpoles can recognize kin (Waldman 1984; Cornell et al. 1989; Rautio et al. 1991); however, it is uncertain whether they use this in a context-dependent manner to cannibalize conspecifics selectively based on genetic relatedness. Studies along these lines would be useful to elucidate the evolutionary significance of cannibalism in shaping anuran life-history strategies. ACKNOWLEDGMENTS Special appreciation is extended to Becky Barwick, Chris Crawford, Randy Durren, Mark Hopey, Michelle MacMillan and Ruth Urand for assisting in the laboratory and field work, and to two anonymous referees for their helpful criticisms.
REFERENCES Alford, R. A. & Wilbur, H. M. 1985. Priority effects in experimental pond communities: competition between Bufo and Rana. Ecology, 66, 1097-I 105. Berven, K. A. & Grudzien, T. A. 1990. Dispersal in tht wood frog (Rana sylvatica): implications for genetic population structure. Evolution, 44, 2047-2056. Biesterfeldt, J. M., Petranka, J. W. & Sherbondy, S. 1993. Prevalence of chemical interference competition in natural populations of wood frogs, Rana sy/vatica Copeia, 1993; 688-695. Blair. W. F. 1961. Calling and soawning seasons in I mixed population of anirans. I%ology,42, 99-l 10. Blaustein, A. R. & O’Hara, R. K. 1982. Kin recognition in Rana cascadae tadpoles: maternal and paternal effects. Anim. Behav., 30, 1151-l 157. Bleakney, S. C. 1958. Cannibalism in Rana sylvatica tadpoles. Herpetologica, 14, 34. Bragg, A. N. 1945. The spadefoot toads in Oklahoma with summary of our knowledge of the group II. Anr Nat., 19, 52-72. Cornell, T. J., Berven, K. A. & Gamboa, G. J. 1989. Kin recognition by tadpoles and froglets of the wood frog Rana svlvatica. Oecolopia I Beri. ). 18, 3 12-3 16. Crump, M. L. 1983. r)pportu&tic cannibalism by amphibian larvae in temporary aquatic environments. Am. Nat., 121, 281-287. Crump, M. L. 1986. Cannibalism by younger tadpoles another hazard of metamorphosis. Copeia, 1986, 1007-1009. Crump, M. L. 1992. Cannibalism in amphibians. In Carkbalism: Ecology and Evolution among Divers Taxa (Ed. bv M. A. Elgar & B. J. Cresoi). DO 256-27i. New York: OxfoFd University Press. .’ Degani, G., Goldenberg, S. & Warburg, M. R. 1980. Cannibalistic phenomena in Salamandra Salamandr larvae in certain water bodies and under experimenta conditions. Hydrobiologia, IS, 123-128.
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Dixon, J. R. & Heyer, W. R. 1968. Anuran succession in a temporary pond in Colima, Mexico. Bull. Sth. Calif: Ad Sci., 61, 129-137. Duellman, W. E. & Trueb, L. 1986. Biology of Amphibians. New York: McGraw-Hill. Fox, L. R. 1975. Factors influencing cannibalism, a mechanism of population limitation in the predator Notonecta hoffmanni. Ecology, 56, 9333941. Godwin, G. J. & Roble, S. 1983. Mating success in male treefrogs, Hyla chrysoscelis (Anura: Hylidae). Herpetologica, 39, 141-146. Greer, B. J. & Wells, K. D. 1980. Territorial and reproductive behavior of the tropical American frog (Centrolennafleishmanni). Herpetologica, 36, 318-326. Harris, R. N. 1980. The consequences of within-year timing of breeding in Ambystoma maculatum. Copeia, 1980, 719-722. Heusser, H. 1970. Spawn eating by tadpoles as possible cause of specific biotype preferences and short breeding times in European anurans (Amphibia: Anura). Oecologia (Bed), 4, 83-88. Heyer, W. R., McDiarmid, R. W. & Weigmann, D. L. 1975. Tadpoles, predation, and pond habitats in the tropics. Biotropica, 7, 100-l 11. Kats, L. B., Breeding, J. A. & Hanson, K. M. 1994. Ontogenetic changes in California newts (Taricha forosa) in response to chemical cues from conspecific predators. Jl N. Am. benthol. Sot., 13, 321-325. Keen, W. H. 1975. Breeding and larval development of three species of Ambystoma in central Kentucky (Amphibia: Urodela). Herpetologica, 31, 18-21. Kusano, T., Kusano, H. & Miyashita, K. 1985. Sizerelated cannibalism among larval Hynobius nebulosus. Copeia, 1985, 472476. Newman, R. A. 1987. Effects of density and predation on Scaphiopus couchi tadpoles in desert ponds. Oecologia (Bed), 71, 301-307. Nyman, S., Wilkinson, R. F. & Hutcherson, J. E. 1993. Cannibalism and size relations in a cohort of larval ringed salamanders (Ambystoma anndatum). J. Herpetol., 27, 78-84. Petranka, 3. W., Hopey, M. E., Jennings, B. T., Baird, S. D. & Boone, S. J. 1994. Breeding habitat segregation of wood frogs and American toads: the role of interspecific tadpole predation and adult choice. Copeia, 1994, 691-697. Pfennig, D. W., Reeve, H. K. & Sherman, P. W. 1993. Kin recognition and cannibalism in spadefoot toad tadpoles. Anim. Behav., 46, 87-94. Polis, G. A. 1981. The evolution and dynamics of intraspecific predation. A. Rev. Ecol. Syst., 12, 225-25 1.
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Polis, G. A. & Myers C. A. 1985. A survey of intraspecific predation among reptiles and amphibians. J. Herpetol., 19, 99-107. Rautio, S. A., Bura, E. A., Berven, K. A. & Gamboa, G. J. 1991. Kin recognition in wood frog tadpoles (Rana sylvatica): factors affecting spatial proximity to siblings. Can. J. Zool., 69, 256992571. Rose, F. L. & Armentrout, D. 1976. Adaptive strategies of Ambystoma tigrinum Green inhabiting the Llano Estacado of West Texas. J. Anim. Eeol., 45, 713-129. Travis, J. 1983. Variation in development patterns of larval anurans in temporary ponds. I. Persistent variation within a Hyla gratiosa population. Evolution, 37, 496512. Waldman, B. 1982. Adaptive significance of communal oviposition in wood frogs (Rana sylvatica). Behav. Ecol. Sociobiol., 10, 1699174. Waldman, B. 1984. Kin recognition and sibling association among wood frog (Rana sylvatica) tadpoles. Behav. Ecol. Sociobiol., 14, 171-180. Wassersug, R. J. 1980. Internal oral features of larvae from eight anuran families: functional, systematic, evolutionary and ecological considerations. Misc. Pubis MUX nat. Hist. Univ. Kans., 68, I-146. Wassersug, R. J., Frogner, K. J. & Inger, R. F. 1981. Adaptations for life in tree holes by rhycophorid tadpoles from Thailand. J. Heruetol.. 15. 41-52. Wilbur, H. M. 1972. Competition, predation, and the structure of the Ambystoma-Rana sylvatica community. Ecology, 53, 3-21. Wilbur, H. M. 1976. Density-dependent aspects of metamorphosis in Ambystoma and Rana sylvatica. Ecology, 57, 1289-1296. Wilbur, H. M. 1980. Complex life cycles. A. Rev. Ed. Syst., 11, 67-93. Wilbur, H. M. 1984. Complex life cycles and community organization in amphibians. In: A New Ecology: Novel Approaches to Interactive Systems (Ed. by P. W. Price, C: W. Slobodchikoff &. W. S. Gauh), pp. 1955224. New York: John Wilev. Wilbur, H. M. & Alford, R. A. 1985. Priority effects in experimental pond communities: responses of Hyla to Bufo and Rana. Ecology, 66, 1106-l 114. Wilbur, H. M., Morin, P. J. & Harris, R. N. 1983. Salamander predation and the structure of experimental communities: anuran responses. Ecology, 64, 1423-1429. Woodward, B. D. & Mitchell, S. 1990. Predation of frogs in breeding choruses. SWest. Nat., 35, 449450.
1995, 50, 731-739
Explosivebreedingreducesegg and tadpole cannibalismin the wood frog, Rana sylvatica JAMES W. PETRANKA Department
of Biology,
& DAPHNE University
A. G. THOMAS
of North
Carolina
(Received 10 August 1994; initial acceptance 24 October 1994; final acceptance 4 January 1995; MS. number: a7060j
Abstract. Cannibalism of anuran eggs and hatchlings by larger tadpoles has been documented in many speciesthat inhabit seasonally ephemeral habitats and has been hypothesized to play an important role in favouring synchronized breeding. Using the wood frog, this hypothesis was tested by determining whetheroffspring of non-synchronized breeders were more vulnerable to cannibalism than offspring of synchronizedbreeders. In a laboratory experiment, small tadpoles of similar size did not cannibalize eachother. However, large tadpoles preyed heavily on the eggs and hatchlings of conspecifics, and the incidenceof predation increased with cannibal size. In natural populations, over 80% of adults bred explosivelyduring a 3-day period, and their offspring were not cannibalized because hatching was synchronized and tadpoles varied only slightly in size. About 5% of adults oviposited late in the breedingseason, and the resulting embryos hatched when tadpoles of synchronized breeders averaged 0.6-1.3g. Larger tadpoles in the ponds cannibalized the eggs and hatchlings of these late breeders. In a field experiment conducted at a natural breeding site, eggs that were added 7 days after embryos of late breeders hatched suffered complete mortality within 19 h. Similarly, more than 50% of hatchlings werecannibalized within 15 min after they were placed in the pond. These results are consistent with the view that synchronized breeding is an adaptation that reduces cannibalism in anurans that breed in temporary ponds. 0 1995 The Association for the Study of Animal Behaviour Breeding phenologies are important elements of amphibian life-history strategies that can affect community composition, population size and structure, and larval life-history traits (Keen 1975; Rose& Armentrout 1976; Harris 1980; Alford & Wilbur 1985; Kats et al. 1994). Aspects of breeding phenology that can potentially influence adult fitness include the frequency and duration of individual breeding bouts as well as the seasonal time of breeding (Blair 1961; Dixon & Heyer 1968). Comparative studies suggest that speciesspecificbreeding phenologies are adaptive and often correlate with breeding habitat, seasonal changesin climate, or the presence of potential competitors or predators (Bragg 1945; Wilbur & Alford 1985; Duellman & Trueb 1986). One well-documented dichotomy in amphibian breeding phenology is the explosive or synchronous breeding pattern of many species,compared to the more continuous pattern of others. The Correspondence: J. ogy, University 2299,U.S.A.
W. of North
0003-3472/95/090731+09
Petranka,Department Carolina,
$12.0010
Asheville,
of BiolNC 28804-
degree of breeding synchrony may be viewed as a continuum that ranges from species such as spadefoot toads, Scaphiopus spp., in which a local population may restrict its breeding to a single day, to those such as the red-spotted newt, Notophthalmus viridescens, which breeds continuously over several months. Explosive breeding is common in many species that use seasonally ephemeral habitats such as vernal ponds and tropical rain pools, and may involve a single annual bout, or several explosive bouts over a prolonged breeding season (Heyer et al. 1975; Crump 1983; Newman 1987). Changes in climate or weather often provide narrow windows of opportunity for individuals to exploit seasonally ephemeral habitats, and individuals typically arrive en masse at breeding sites shortly after ponds fill or conditions become suitable for migrations. The widespread occurrence of explosive breeding in many temporary pond breeders suggests that individuals that breed relatively late during a breeding bout have lower fitness than synchronized breeders. The selection pressuresthat favour
Q 1995 The Association
731
for the Study
of Animal
Behaviour
132
Animal
Behaviour,
early, synchronized breeding in temporary pond breeders are complex and probably operate on both the adult and larval stages. Tadpoles that hatch early, for example, may minimize predation risk because of predator lags (Wilbur 1980) and have more time to complete the larva1 period before habitats dry (Newman 1987). Where sizespecific competition and priority effects occur, tadpoles of early breeders may be competitively superior to those of late arrivers (Travis 1983; Alford & Wilbur 1985; Wilbur & Alford 1985). Factors that relate to the adult stage, such as sexual competition, the ability to find a mate, and predation risk to breeding or migrating adults, may also influence breeding phenologies (Greer & Wells 1980; Godwin & Roble 1983; Woodward & Mitchell 1990). Crump (1992) and Heusser (1970) hypothesized that cannibalism could potentially play an important role in favouring explosive breeding in amphibians that use seasonally ephemeral habitats. Because cannibalism by larva1 amphibians often involves larger individuals preying on eggs or smaller larvae, the frequency of cannibalism often increaseswith sizevariation in a population (Degani et al. 1980; Kusano et al. 1985; Nyman et al. 1993). Synchronized breeding produces weakly size-structured populations and could potentially reduce cannibalism by size-selective predators. Here, we test this hypothesis using the wood frog. The wood frog occurs from Alaska to New England and south through the southern Appalachians to Alabama and Georgia. Although this widely distributed speciesfavours moist forests, it also inhabits western grasslandsand northern tundra (Berven & Grudzien 1990). Adults emerge from winter hibernacula to breed in winter or early spring and deposit egg massesin communal groups in seasonally ephemeral habitats that lack fish (Waldman 1982; Berven & Grudzien 1990). Breeding is explosive and most oviposition within local populations occurs during a I-2-week period (Waldman 1982). Tadpole densities are often very high in breeding ponds (Biesterfeldt et al. 1993), and the tadpole stage normally lasts from 2 to 5 months. Cannibalism has not been documented in R. sylvatica, although Bleakney (1958) observed hundreds of tadpoles that appeared to have eaten portions of each others’ tails. Petranka et al. (1994) reported that R. sylvatica tadpoles are voracious predators on the eggs and hatchlings of
50, 3
American toads, Bufo americanus. The propensity of R. sylvatica tadpoles to prey on toad eggs and hatchlings suggeststhat tadpoles would also can. nibalize the eggs or hatchlings of late breeders. This, in turn, might select for synchronized breeding and hatching, which would minimize cannibal. ism risk. To test this hypothesis, we conducted studies to determine whether R sylvatica tadpoles are cannibalistic and whether cannibalism rate varies with cannibal size and prey developmental stage. In addition, we monitored breeding and hatching periods in natural breeding sites to deter. mine whether late breeders were vulnerable to egg or hatchling cannibalism. METHODS Experiment 1: Does Cannibalism Frequency Depend on Predator Size and Prey Life-history Stage? We conducted a 2 x 4 factorial experiment to examine size-specificcannibalism of embryos and hatchlings by tadpoles. The two factors were the initial developmental stages of the prey (embryos versus hatchlings) and the level of risk to the prey We manipulated level of risk by using predator treatments that consisted of small, medium and large tadpoles, as well as controls with no tadpoles (minima1 risk). Becausethe frequency of cannibal. ism often increaseswith the average sizedifference between predator and prey, we assumed that risk of cannibalism increased with sizeof the potential tadpole cannibal. To generate three sizecohorts for use as potential cannibals, we collected egg massesfrom breed. ing ponds on 9 February, 20-22 February and 2 March 1994 and grew hatchlings in 38-189~litre~ aquaria for 3-21 days. We reared tadpoles at room temperature with an uncontrolled light:dark cycle and fed all three cohorts powdered rabbit chow ad libitum once or twice daily. Immediately before initiating the experiment, we pooled tadpoles from all tanks and used sieves to sort them into small, medium and large groups. Respective mean masses (&SE; N=20) were 0.44 % 0.01 g, 0.99 f 0.07 g and 1.95 f 0.09 g. A fourth treatment consisted of controls with no tadpoles. The experiment was a randomized blocked design with four replicates. We tested animals at room temperature (ca 21°C) in plastic containers
Petranka
& Thomas: Cannibalism
measuring20 x 10 x 15 cm. Each container held 2.7litresof water and was bubbled with air so that oxygenlevels were near saturation. We arranged containersin four blocks (Iv’=8 containers per block)along two laboratory benches and assigned treatmentsrandomly to containers within each block.We added 20 small, medium or large tadpolesto appropriate containers, then fed tadpoles 14Omgof powdered rabbit chow per g of wet massto assure that hunger levels were approximatelythe same for all size classes.After allowing 1day for tadpoles to acclimatize, we added to eachcontainer either 40 hatchlings (Gosner stages 20-22;mass, XLIZSE= 83 f 3 mg for a sample of 15 hatchlings)or 40 late-term eggs (embryos within theenclosed jelly coats were at Gosner stages K-19). We observed containers during the first hour of the experiment and recorded any instancesof cannibalism. We then checked containersat l-day intervals for 3 days and scored the numberof missing prey. DocumentingBreeding and Hatching Periods in NaturalPopulations We documented the breeding phenology and hatchingdates of wood frogs at six natural and semi-naturalponds within 10 km of Bamardsville, BuncombeCounty, North Carolina. One site was anaturalvernal pond, whereas the remaining sites weresmall (~50 m2) water-filled depressionsin the bedsof old logging roads within the Pisgah National Forest. Pond A was located approximately8 km from the remaining cluster of ponds whichwere within 500 m of each other. We visited sites every l-5 days from the initiation of breeding on 9 February until hatching terminated on 2 April.We visited sites more frequently (l-3 days) duringbreeding and hatching periods to documentmore preciselythe timing of these events. On eachvisit we censusedall egg massesin each pond, then marked and recorded the developmental stagesof a subset (N=l-7 masses per pond) of newlylaid eggs. We marked masses with dowel rodsplaced through each mass, and used marked massesto estimate the incubation period and hatchingdates of eggs from different breeding bouts.Hatching of egg masses laid during l-day breedingbouts sometimes lasted as long as 5-6 daysduring cold weather. Becausethe percentages of embryoshatching on a given day could not be preciselydetermined, we used mid-points of the
in wood frogs
733
entire hatching period to approximate the average time of hatching and length of the incubation period. We estimated the wet mass and growth rates of tadpoles in each pond from the initiation of hatching (9 March) through the first week of April by weighing 10-15 tadpoles that were haphazardly collected while wading through each pond. Tadpoles were blotted with paper tissue to remove external water before being weighed to the nearest milligram on an electronic balance. Experiment 2: Are Offspring of Late Breeders Vulnerable to Cannibalism in Nature? To determine whether the offspring of late breeders are vulnerable to cannibalism in the field, we monitored the survival of eggs and hatchlings experimentally added to pond B on 2 April. About 85% of adults deposited eggs at this site during 20-22 February. However, breeding did not terminate until 10 March, when single egg masseswere deposited in pond B and two adjoining ponds. Hatching of the eggs of late breeders ended on 25 March in pond B and 2 April in ponds D-F. To determine whether hatchlings of late-breeders were vulnerable to cannibalism, we conducted 22 trials in which individual hatchlings were added to the pond in the vicinity of resident tadpoles. Test animals were less than 24 h posthatching, were at Gosner stages20-22, and averaged 92*3 mg and 9.3 *0.2mm total length (N= 15). We placed uninjured hatchlings with intact tail fins within 0.5 m of the edge of the pond where we could clearly observe behavioural interactions without disturbing resident tadpoles. We watched each focal animal continuously from the shoreline for a maximum of 15 min and recorded all attacks or kills by conspecifics. We recovered all hatchlings that survived for 15 min and inspected them for injuries such as bites out of the tail fins or yolk sac. We conducted the trials during the afternoon when water temperatures averaged 23.5’C. We visually estimated that the pond contained at least 100 000 tadpoles, with local densities exceeding 2000 tadpoles/m2. Hence, we assumed that the trials were independent and that the probability that a particular resident was involved in more than one attack was very small. To determine whether tadpoles would prey on eggs, we added 50 eggs at Gosner stages 10-16 to each of five locations around the perimeter of the pond. Eggs used in the experiment were teased
734
Animal
Behaviour,
apart from a single mass. We placed eggs in shallow water near the pond edge then observed tadpole feeding responsesfor 30 min. We checked each group after 19 h to determine the number of eggs surviving. We released all surviving tadpoles used in laboratory and field studies in a natural breeding pond.
50, 3
ing in frenetic feeding activity in the vicinity of the injured animal. This behaviour appeared to be in response to the release of body fluids or yolk from injured hatchlings, and often resulted in injured animals being cannibalized. During the first hour of observation, 32 hatchlings were cannibalized and 11 other hatchlings sustained visible injuries. Numerous tadpoles were observed feeding on Field Observations of Cannibalism the jelly coat that surrounded the eggs. However, We visited ponds during 20-24 March to docu- we observed only two instances of egg predation ment cannibalism of the offspring of late-term during the first hour of the experiment. In one breeders during the hatching period. Egg masses case a single tadpole penetrated the jelly coat and were inspected for evidence of predation, and a consumed an embryo. In the second instance a preliminary experiment similar to that described group of feeding tadpoles collectively fed upon the in experiment 2 was conducted to determine if jelly coat and embryo of an egg. Patterns of survival varied markedly between hatchlings were vulnerable to cannibalism. treatment groups during the ensuing 3 days (Fig. 1). Mortality of late-term embryos was relatively Statistical Analyses constant for the first 2 days of the experiment and averaged 10% per day overall. Hatching began We analysed the results of the laboratory experiment with ANOVA and repeated-measures near the end of day 2 and 99% of the surviving ANOVA using log-transformed data. Block embryos hatched before the termination of the effects were not significant and were excluded experiment. Age-specific mortality increased dur. from the model. Mean survival in control groups ing day 3 for all three size treatments. This was 100% and there was no variation in the data. increase in mortality corresponded to the time Becauseuse of control data would grossly violate when most embryos hatched. In the hatchling the assumption of homogeneity of variances treatment, mortality was confined almost entirely between treatment groups, we excluded this from to day 1, when hatchlings were immobile and the analysis and only compared the three tadpole responded to attacks with relatively weak uncoordinated swimming. After day 1 mos size classes. tadpoles exhibited coordinated swimming and rapidly fled when approached by potential cannibals. RESULTS Mortality of eggs and hatchlings increased win mean sizeof the predatory tadpoles (Fig. 1). After Experiment 1 2 days, 15, 18 and 27% of embryos were consumed~ We observed 22 instances of larger tadpoles in the small, medium and large tadpole treatment\’ attacking conspecific hatchlings during the first respectively. Similarly, mortality of hatchlingr hour of the laboratory experiment. Typically, after 3 days was 12, 18 and 39%, respectively. Na individuals would tilt the body and orient the mortality occurred in any of the control contains head downward, then thrust with the tail while ers, which indicates that deaths in other containen delivering a bite. Bites often resulted in visible were as a result of cannibalism. Repeated, injuries that consisted of U-shaped plugs that measures ANOVA indicated that the overall pat. were most often taken from the belly where yolk terns of survival were significantly affected by reserves were concentrated (42% of injuries) or tadpole size (P=O.OOOS), but not by initial devel. from the tail fin (25% of injuries). In many cases opmental stage (P=O.72; Table I). The interaction tadpoles that bit hatchlings rapidly consumed of the two factors was significant (P=O.OOl)which them within 5-20 s after an attack began. In other presumably reflects variation in the shapes of the cases,hatchlings were injured but were not con- survivorship curves for the egg and hatchling sumed by the attacker. Neighbouring tadpoles treatments (Fig. 1). An ANOVA conducted at the responded to severelyinjured hatchlings by engag- termination of the experiment (day 3) indicated
Petranka
Egg stage
40
, Hatchlings I
2
, Free-swimming I
Source of variation
3
tadpoles
09 0
I 1
I
I _
2
3
Time (days) Figure 1. Age-specific survivorship for (a) egg and (b) hatchling treatments in the presence of small (W), medium (0), large (a), or no (0) tadpoles. Intervals abovegraphs indicate the approximate time when individuals began hatching or reached free-swimming stages in the respective treatments. that initial developmental stage (P=O.OOZ) and tadpole size (P=O.O04) significantly affected prey survival. The interaction of the two factors was not significant (P=O.78). Analysis of withintreatment (subjects) effects of the repeatedmeasures ANOVA indicated a significant day effect. In addition, all of the interaction terms were significant (PjO.02; Table I). Breeding and Hatching
735
Table I. Summary statistics for repeated-measures ANOVA for experiment 1
, -‘ii 1
1 Hatchlings
in wood frogs
Between-subjects effects Stage Size Stage x size Error Within-subjects effects Day Day x stage Day x size Day x stage x size Error (day)
4ok; , 0
& Thomas: Cannibalism
Periods
Adults at most ponds engaged in three to four breeding bouts during the season which were
Between-subjects effects, whereas related trends in stage; size: mean
4
F 1
0.13
2 2 18
12.18 6.03
2 2 4 4 36
57.88 50.01 3.34 3.86
P
0.72
0~0005 0.0099
0~0001 0~0001 0.0201 0.0103
effects test for overall treatment within-subjects effects test for timesurvival. Stage: Initial developmental tadpole size; day: day of experiment.
interrupted by periods of cold weather in which breeding activity ceased. Breeding began on 9-13 February and continued until 10 March (Fig. 2). Although the overall breeding season lasted nearly 1 month, breeding was highly synchronized both within and between ponds. Overall, 81% of females oviposited on either 20 or 22 February (range=59-94% among ponds). A small percentage (2-14%) of late arrivers bred on 2 March (ponds A and D) and 10 March (ponds A, B, E and F). Hatching occurred during 6 March-2 April, and the incubation period was inversely related to time of oviposition. The day of the year that eggs were laid explained 56% of the variation in length of the incubation period of cohorts of marked egg masses (linear regression; r* = 0.56, F, ,22= 26.85, P=O.O002). As a result, embryos of very early breeders hatched within a few days of those laid during the major breeding bout of 20-22 February. Embryos from clutches deposited during 20-22 February hatched during 11-22 March. Hatchings from this cohort did not appear to be vulnerable to cannibalism because tadpoles in ponds generally averaged less than 0.2 g (Fig. 2). In contrast, offspring of late arrivers that bred in early March hatched between 22 March and 2 April when tadpoles in ponds averaged between 0.6 and 1.3 g. Mean masses of tadpoles in ponds at this time were slightly larger than the small and medium tadpoles used in the laboratory
Animal
736
Behaviour,
I
Pond A
Pond B
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1.4 1.0
1.0
2CI-
0.6
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% L 1 7 14 February 3 B 0” nk 50
1 7 14 21 28 1 7 March April
1 7 14 21 February
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1 30
1.0
1 20
0.6
8 10
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Pond E
1 7 14 21 28 1 7 March April End of
I
40
I
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2.2
Bb 40
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% 2b; Es
50, 3
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% 1.8 4
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1 7 14 21 28 1 7 March April
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1.0
0.6
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0.2
0.2
1 7 14 21 28 1 7 March April
3
1 7 14 21 February
1 7 14 21 28 1 7 March April
Figure 2. Relationship between breeding phenology, hatching dates and mean tadpole sizes in six natural breediq sites of the wood frog. n : % of the total egg massesdeposited in 1994; 0: mid-points of the hatching periods for eact cohort which, for simplicity of illustration, assume equal hatching successbetween cohorts. Lines indicate changer in the mean ( f SE) of tadpoles from the initiation of hatching onward.
experiment, and tadpoles were sufficiently large to cannibalize both the eggs and hatchlings of late breeders. Experiment
2
Of 22 hatchlings that were introduced into pond B, 12 (55%) were cannibalized during the 15min trial periods. Cannibals showed the typical feeding
behaviour that involved tilting the body down. ward into a feeding position and thrusting witi the tail while delivering a forceful bite. Feedink frenzies often ensued after a hatchling was initial11 attacked. Typically, hundreds of tadpoles began feeding frenetically in the immediate area where an animal was injured in apparent response to the release of body fluids from injured hatchlings. 01 the remaining 10 tadpoles that survived for
Petranka
& Thomas: Cannibalism
15min, 80% sustained visible injuries, including 60%with large plugs bitten out of the ventral bodywall and yolk sac. Tadpoles began feeding on eggs immediately after they were added to ponds. Within 30 min, large aggregates of tadpoles had formed in the vicinityof the eggs and hundreds of tadpoles were observedfeeding on the jelly coats. After 19 h, we wereunable to locate either eggs or the remnants of thejelly coats at any of the five siteswhere eggs wereadded to the pond.
in wood frogs
131
seasonally ephemeral habitats. Our data provide support for this hypothesis and suggest that cannibalism is an important factor favouring explosive breeding in R. sylvatica. Adults at our field sites exhibited highly synchronized breeding in which 8 1% of eggswere laid during a 3-day period. Embryos from this primary breeding bout hatched relatively synchronously and sizevariation at hatching was minimal. In our laboratory experiment, variation in tadpole size in the control group was similar to that of individuals that hatched synchronously in ponds. Tadpoles in control groups that lacked larger Field Observations of Cannibalism tadpoles did not cannibalize each other during the Field observations were made on 20-24 March experiment, presumably because size variation to document natural occurrences of cannibalism. was not sufficient to allow cannibalism. ConseOn20 March we observed large tadpoles feeding quently, risk of cannibalism was minimal for on a single egg mass in pond B that was laid highly synchronized breeders in natural ponds. duringa final breeding bout on 10 March. On 22 Embryos of late breeders did not hatch until March large tadpoles were feeding on the egg tadpoles of synchronized breeders were 24 weeks massand most of the outer jelly coats had been old and averaged 061.3 g. Our laboratory eaten.Hatching of this mass occurred on 23-24 experiment indicates that the risk of cannibalism March. During this hatching period we moved increases with predator size and that tadpoles eightrecently hatched embryos to the edge of the within this size range will readily cannibalize eggs pondto observe them. In the ensuing 15 min, two and hatchlings. Our field experiment further demwerecannibalized and two sustained major in- onstrates that offspring of late arrivers are highly juries.Egg massesof late breeders in ponds C-F vulnerable to cannibalism. Eggs and hatchlings alsohad much of the outer jelly coats eaten, and that were added 7 days after embryos of late numerousembryos were missing from the masses breeders hatched had extremely high mortality thatwere presumably cannibalized. In pond A, 18 rates. Cannibalism rates for the field experiment masses were laid during a final breeding bout on were much higher than those observed for similar10March. When examined on 20-23 March, we sized tadpoles in the laboratory (i.e. large tadpole observedtadpoles feeding on most of these masses treatment) and may reflect differences in food andnumerous embryos were missing from the egg level or tadpole densities. Tadpole densities in our capsules. laboratory experiment were 666 tadpoles/m* of container, whereas Biesterfeldt et al. (1993) recorded average densities of 1816 tadpoles/m’ of DISCUSSION pond bottom for samples taken from our study sites in late March and early April. The results Cannibalism is widespread among anurans and of our field experiment suggest that offspring of hasbeen reported in at least 12 of 21 families of individuals breeding even a few days beyond the frogs(Polis & Myers 1985; Crump 1986, 1992). normal termination of breeding would suffer Nonethe less, surprisingly few data are available catastrophic mortality from cannibalism. onthe evolutionary significance of cannibalism in Wood frog tadpoles have generalized trophic naturalpopulations of anurans. Cannibalism may morphologies that are typical of microphagous bean important selection pressure favouring kin suspension-feeders. Although they lack specialrecognition in tadpoles, and could potentially ized structures such as enlarged jaws, modified favour terrestrial reproduction in adults (Crump beaks and teeth, and shortened digestive tracts 1983;Pfennig et al. 1993). Crump (1992) sum- that are often seen in highly carnivorous tadpoles marizedmany of the costs and benefits of canni- (Wassersug 1980; Wassersug et al. 1981; Crump balismand hypothesized that cannibalism might 1983) they are surprisingly efficient predators on alsofavour explosive breeding in anurans that use the eggs and hatchlings of many amphibians.
738
Petranka
Animul
Behuviour,
et al. (1994) found that predation of tadpoles on American toad eggs and hatchlings is sufficient to exclude toads from many wood frog breeding sites. We have also observed R. sylvatica tadpoles feeding on the eggs of grey tree frogs, Hyla chrysoscelis, and spotted salamanders, Ambystoma maculatum, in natural ponds. Thus, this species appears to be a major predator structuring amphibian communities in vernal ponds in the southern Appalachian Mountains. Cannibalism is undoubtedly not the only factor favouring explosive breeding in wood frogs. Waldman (1982), for example, found that eggs of early breeders that were deposited in the middle of communal rafts had higher survival than those of late breeders that laid near the periphery of rafts. Early, synchronized breeding in R. sylvatica may also be favoured because it enhances size-specific competitive ability (Wilbur 1980, 1984) and maximizes the time available for offspring to exploit productive, but transient pond communities. Cannibalism is common in natural populations where conspecific densities are high, food is limiting, and survival rates are low (Fox 1975; Polis 1981; Polis & Myers 1985). Scientists have documented a growing number of anuran tadpoles that prey on conspecific and heterospecific eggs and tadpoles (Crump 1983, 1992; Petranka et al. 1994), and most live in seasonally ephemeral habitats. Although seasonally ephemeral ponds are often highly productive (Wilbur 1980, 1984), high densities of amphibian larvae often result in intense competition for food that can slow growth, lengthen the larval period and reduce survival (Wilbur 1972, 1976; Wilbur et al. 1983). This, coupled with pond drying, should favour mechanisms such as cannibalism that accelerate growth and development rates (Crump 1983, 1992). Local densities of wood frog tadpoles at our study sites sometimes reach nearly 9000 tadpoles/m* of pond bottom (Biesterfeldt et al. 1993). At these densities, intense competition for food seems likely and cannibalism of frog eggs and the yolk reserves of hatchlings would provide a nutritive, energy-rich food source in an otherwise nutrient-poor environment. Cannibals always run the risk of reducing their inclusive fitness by eating relatives, and kin recognition may play a role in minimizing cannibalism of close relatives (Blaustein & O’Hara 1982; Pfennig et al. R. sylvatica
50. 3
1993). Rana sylvaticu tadpoles can recognize kin (Waldman 1984; Cornell et al. 1989; Rautio et al. 1991); however, it is uncertain whether they use this in a context-dependent manner to cannibalize conspecifics selectively based on genetic relatedness. Studies along these lines would be useful to elucidate the evolutionary significance of cannibalism in shaping anuran life-history strategies. ACKNOWLEDGMENTS Special appreciation is extended to Becky Barwick, Chris Crawford, Randy Durren, Mark Hopey, Michelle MacMillan and Ruth Urand for assisting in the laboratory and field work, and to two anonymous referees for their helpful criticisms.
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