Variation in the Pattern of Predator-Induced Damage to Tadpole Tails
Abstract
Tadpoles in nature are often found with injured tails. We introduce a planimetric technique for compiling data on the injuries sustained by individual tadpoles, which allows us to visualize and quantify the tail damage sustained by a population as a whole. We have used this technique to compare the pattern and severity of damage in tadpoles from seven species (Ascaphus truei, Bufo americanus, Phyllomedusa tomopterna, Pseudacris crucifer, Rana catesbeiana, Rana sylvatica, and Rhinophrynus dorsalis) that differ in microhabitat use (benthic vs pelagic), tail morphology (filamentous vs nonfilamentous) and palatability to predators. We also examined differences in tail damage across developmental stages. Finally, we compared interpopulation variation for R. sylvatica tadpoles from six separate ponds. The tail tip was the most commonly damaged area in all tadpoles, although the pattern and severity of injury varied greatly across species. Unpalatable, benthic larvae sustained small nicks around the margin of the tail, whereas pelagic and palatable species more often had the tail tip sheared off caudally. Little damage was found in any species in the anterior portion of the tail, where most thrust is generated during swimming. Only one species, A. truei, exhibited increased tail damage as the tadpoles aged. Later stage P. crucifer and R. sylvatica larvae in contrast, had significantly less tail damage than younger stage conspecifics. Although this could be the result of different healing rates at different stages, alternatively it suggests that for these species, survivorship is ultimately reduced in individuals that lose a substantial part of the tail when they are young.
Anurans face numerous predators during the aquatic stage of their lifecycle. Fishes, birds, snakes, turtles, salamanders, crayfishes, newts, insect larvae, and even other anuran larvae attack tadpoles (e.g., Heyer et al., 1975; Arnold and Wassersug, 1978; Wassersug, 1997). As a result, one often finds injured tadpoles in nature. In this study, we evaluate and compare how much tail injury populations of tadpoles receive and endure under natural conditions.
Circumstantial evidence suggests that tadpoles can survive with substantial tail damage. In experiments where 0, 25, 50, and 75% of the tails of hylid Hyla chrysoscelis tadpoles were ablated, larval sprint velocity and distance traveled was not affected until more than 50% of the tail was removed (Figiel and Semlitsch, 1991). Surprisingly, Wilbur and Semlitsch (1990) found that tail loss of this magnitude did not increase the tadpoles vulnerability to predation by newts in laboratory experiments.
Consistent with this observation are kinematic data which show that tadpoles do not need all of their tail for propulsion (Wassersug and Hoff, 1985; Hoff, 1987). Propulsive thrust in most species is produced predominantly rostral to the tallest part on the tail. The more caudal end of the tail is used by tadpoles in turning but contributes little to thrust (Liu et al., 1997; K. vS. Hoff and R. J. Wassersug, unpublished data).
Although tadpoles do not necessarily need the entire tail for movement, experimental studies indicate that there is a cost associated with tail loss. Tadpoles with tail damage tend to develop more slowly than tadpoles with intact tails (Morin, 1985; Wilbur and Semlitsch, 1990; Parichy and Kaplan, 1992).
Retarded growth can lead to increased predation in tadpoles because size plays a role in successfully escaping predators. More small tadpoles than large tadpoles are vulnerable to predation by insect larvae (e.g., Travis et al., 1985; Formanowicz, 1986; Caldwell, 1994). In staged experiments, Brodie and Formanowicz (1983) found that smaller tadpoles exhibited less injury than larger ones simply because small ones were more often completely consumed when attacked. This has implications for the degree of tail damage that one might find in tadpoles of different sizes and ages. An absence of tail damage in a size cohort of tadpoles may indicate that those tadpoles are consumed completely once captured, rather than indicating that the tadpoles are good at avoiding or escaping capture.
It is clearly in the best interest of tadpoles to avoid predators altogether, that is, to be well camouflaged. Indeed most tadpoles are cryptically colored. However, some are conspicuous (Wassersug, 1973). In tadpoles of several species, the end of the tail contrasts sharply with the rest of the tadpole. A conspicuous tail tip may draw the attention of visually oriented predators away from the head (Smith and Van Buskirk, 1995; McCollum and Van Buskirk, 1996; McCollum and Leimberger, 1997). Caldwell (1982) found that tadpoles were more likely to have darkened tail tips when in ponds with dragonfly larvae and that tadpoles with black tail tips were both struck on the tail and survived exposure to dragonfly larvae more frequently than conspecifics without the black tail tip. If color spots on tadpole tail tips serve to deflect predator attacks to that part of the tail, then we would expect to find tail damage concentrated at the tail tip. We would also expect that tadpoles would have more damage the longer they are exposed to predators.
A recent study on the biomechanical properties of the tadpole tail fin shows that it is viscoelastic and fragile (Doherty et al., 1998). When grasped, the tail fin stretches, then tears. Consistent with the idea that the fin is designed to fail easily under small tensile loads are observations by Morin (1985) that tadpoles grabbed by salamanders often escaped with parts of their tails missing.
The literature on tadpole tail damage does not address the questions of (1) how much of their tail tadpoles can lose in the wild and still survive, and (2) how much variation there is in the pattern and intensity of damage among populations and species. In the present study, we examine the patterns of damage among several species whose tadpoles differ in tail shape (filamentous vs nonfilamentous), microhabitat use (benthic vs pelagic) and palatability. We also examine intraspecific differences in the patterns of tail damage with developmental stage.
Because of limited sample sizes and the fact that we examined interpopulation variation for only one species and over a relatively narrow range of developmental stages, the results of our interspecific comparisons must be considered tentative. However, this study validates the method introduced here for comparing tail damage among sets of tadpoles. It also provides insight into the relative success of different antipredator strategies employed by tadpoles.
Materials and Methods
Tadpoles from seven New World species form the core of this study (Appendix, Table 1). For six of the seven species, the tadpoles were collected from a single location to limit variation within samples due to habitat differences. Intraspecific variation between populations was examined in one species, R. sylvatica which was collected from five different ponds in Nova Scotia and one in Maryland.
Rana catesbeiana larvae were caught using funnel nets set overnight in Bennet Lake, Fundy National Park, New Brunswick, in May 1997. Five ponds were sampled with dipnets for R. sylvatica larvae in Nova Scotia in May 1998. These ponds ranged from 0.25 to > 1 m deep and were 100 m to 40 km apart. Preserved specimens of the other species were obtained from the National Museum of Natural History (NMNH), Smithsonian Institution, Washington, DC (Appendix). For each specimen, tail and snout–vent length (SVL) were measured to the nearest 0.5 mm. Developmental stage was determined using the staging table of Gosner (1960). The locations of tail damage were recorded on standardized templates made from an outline drawing of the tadpole of each species (sources for the drawings are given in Figs. 1–2). All parts of the tail that were missing or scarred were colored in black on the template for each specimen. Areas of obvious regeneration were also scored as damage for each specimen. Tail damage that appeared to be postmortem artifact, such as bent tails, was noted but not marked on the templates. All of the scoring for the NMNH specimens was done by J. Blair. The scoring for the Nova Scotia R. sylvatica specimens was done by T. Rolle.
Citation: Ichthyology & Herpetology 2000, 2; 10.1643/0045-8511(2000)000[0390:VITPOP]2.0.CO;2
To visualize the pattern of tail damage for each species, all templates were scanned into a computer using Adobe Photoshop®. The images for each species were then layered one on top of another to arrive at a composite picture of the tail damage common to the entire sample. The opacity of the damaged area in each template was reduced to 5–8% so that the damaged area for each specimen appeared as a light gray. When overlaid, the darkest areas in the composite image indicated where damage occurred repetitively within the population. To further enhance the visual display, compiled images for each species were falsely colored in NIH Image® (http://rsb.info.nih.gov/nih-image) using a 32-increment color spectrum, where violet indicated the least frequently and red indicated the most frequently damaged areas of the tail (Fig. 2).
Citation: Ichthyology & Herpetology 2000, 2; 10.1643/0045-8511(2000)000[0390:VITPOP]2.0.CO;2
To quantify the differences between populations and species, the percentage of the total tail area that was damaged for each specimen was measured using NIH Image®. Regression analysis was then used to determine the relationship between stage and amount of tail damage for each population and species.
Reliability assessment
The results from the preserved specimens may not be entirely representative of what occurs in natural populations because of artifacts due to damage during capture or introduced after preservation. However, we conducted a rudimentary examination of the effects of capture methods on tail damage which indicated that our own dipnetting caused negligible damage to tadpole tails.
Because the assessment of tail damage may be subjective, a blinded study was conducted to determine the scoring bias between two observers. J. Glos, of the University of Würzburg, Germany, scored the tail damage of the tadpoles of the African species, Kassina sp. (n = 9) and Phrynomantis microps (n = 17) and sent the scored templates plus the preserved tadpoles to our laboratory. Blair independently rescored the tail damage for the same specimens without examining the previously marked templates.
Results
The reliability study showed some variation between the two observers in scoring the location of marginal damage on the tails of the two species, Kassina sp. and P. microps. Qualitatively, the overall pattern of damage appears to be the same for the independently scored images (Fig. 1). Quantitatively, the two observers independently recorded an average amount of damage that differed by less than 0.6% for each species. This suggests that our planimetric method for assessing tail damage at the population level should be reliable for interpopulation comparisons, if sample size is large enough and care is taken in recording precisely the damage.
Our survey of over a thousand tadpoles confirmed how common tail fin injury is for tadpoles in the field: nearly half (48.4%) of all tadpoles had some damage. For all of the species in this study, the tail tip was the most frequently damaged area (Fig. 2A); however, there was great variation in the severity of the damage sustained by each species. A few R. sylvatica (n = 3) and P. crucifer (n = 4) tadpoles were found with tail damage exceeding 50% (Tables 2–3). No tadpoles of the other five species (totaling nearly 500 specimens) were found with greater than 25% of the tail damaged, suggesting that they either do not receive or cannot endure such extensive injury. The R. sylvatica and P. crucifer larvae had nearly twice, to more than 10 times, as much of their tail missing as any of the other species.
The benthic and unpalatable species, B. americanus and R. catesbeiana, showed more damage, in the form of small nicks, around the margin of the tail than did the other species (Fig. 2A). The more toxic Bufo tadpoles individually sustained little overall damage to their tails (i.e., average area of damage was < 0.6% and no specimen had more than 5% of the tail missing) despite the fact that 48% of the individuals had some damage (Table 2). Ascaphus truei, which has an eye spot at the tip of its tail, showed a marked concentration of damage at the tail tip. The taxa that lived midwater and had filamentous tails, that is, P. tomopterna and R. dorsalis, also were rarely found with more than 5% of their tail missing (average area of damage per tadpole = 0.5%, for both species). In both species, damage was highly concentrated on the terminal tail filament.
The patterns of damage for the six R. sylvatica populations were similar, though not identical (Figs. 2A–3). Shearing of the caudal end of the tail was evident in all of the populations. Damage of the most caudal 25% of the tail was common in all six populations (Tables 2–3). Damage that exceeds 50% of the tail was also observed, although infrequently in the Maryland population and in only one Nova Scotia population. The average amount of tail missing or damaged for individual tadpoles in the six populations ranged from 1.6% to 5.8%.
The average amount of tail damage for the Nova Scotia R. sylvatica population was approximately half that found in the Maryland sample (Table 2). However, all R. sylvatica populations, regardless of the pond from which they came, had substantially higher average tail damage per individual compared to other species, excluding P. crucifer and R. catesbeiana (Table 2). Although we did not find a positive correlation between the average amount of tail damage per individual and the percentage of individuals within each population that were injured across species (n = 7, r2 = 0.19, P = 0.33), we did find it among populations within R. sylvatica (n = 6, r2 = 0.81, P = 0.04).
Stage effects
Rana sylvatica from Maryland and P. crucifer (Fig. 2B; Table 4) had significant inverse relationships between developmental stage and percent of tail with damage (P < 0.05 and P < 0.01 respectively; Figs. 4–5). In contrast, the correlation coefficients for stage versus tail damage for B. americanus, P. tomopterna, R. catesbeiana, and R. dorsalis were all not significant. Only A. truei had a significant positive relationship (P < 0.005) between stage and amount of tail damage.
Citation: Ichthyology & Herpetology 2000, 2; 10.1643/0045-8511(2000)000[0390:VITPOP]2.0.CO;2
The five Nova Scotia samples of R. sylvatica (each with n = 100) do not show a significant correlation between stage and amount of tail damage (Fig. 5). However, the range of stages represented in these collections is only about half that of the Maryland population. Although not significant, all Nova Scotia populations show a negative slope, suggesting a decrease in the amount of tail damage for tadpoles in later developmental stages. When the five Nova Scotia populations are pooled, there is a significant (P < 0.05) inverse relationship of tail damage with developmental stage, similar to that seen in the Maryland population (Fig. 5).
Citation: Ichthyology & Herpetology 2000, 2; 10.1643/0045-8511(2000)000[0390:VITPOP]2.0.CO;2
Discussion
The common loss of the tail tip in all species examined has implications for the importance of the tail tip in tadpole locomotion. The tail tip is used by tadpoles in turning (Wassersug, 1989), but our data indicate that it is expendable—tadpoles, whether benthic or pelagic, can survive in the short term at least without it.
Across all species, fin damage is rare along the ventral margin of the most rostral portion of the tail, where the vent is located. Almost no damage is seen in this area, presumably because tadpoles that lose this part of their tail do not survive attacks.
The pattern of tail damage differs among species. Benthic tadpoles have small nicks in both the dorsal and ventral margins of their tails, whereas pelagic species have larger pieces of the tail fully sheared off the caudal end. This suggests that pelagic species are attacked by pelagic predators that are large enough to chase down and dissect the end of the tail. The benthic species, in contrast, may be sustaining the nicks from proportionately smaller predators that live in the substratum and ambush rather than chase and dissect tadpoles. Phrynomantis microps, one of the two African species that we examined, is unusual in having larvae that live just below the water's surface. Although we had few tadpoles of this species (and consequently excluded it from our main interspecific comparison), it was the only taxa to exhibit conspicuously greater damage to its ventral than dorsal fin. This is consistent with this tadpole being attacked more often from below.
The many small marginal nicks in the fins of B. americanus and R. catesbeiana suggests that some predators attack but then reject these tadpoles. This is consistent with these tadpoles being unpalatable to many predators (e.g., Wassersug, 1973; Kats et al., 1988; Werner and McPeek, 1994). The fact that nearly half of all Bufo tadpoles had some tail damage, yet the average amount of damage per individual is very low (0.6%), suggests that tail damage is not an important contributor to mortality in these unpalatable larvae. However, one cannot discount the possibility that, when predators attack B. americanus tadpoles, the tadpoles are more often caught and completely ingested rather than escaping with substantial (i.e., > 5%) damage. Evidently, individual B. americanus tadpoles either do not sustain, or cannot tolerate, much tail damage.
Rana catesbeiana also had small pieces of the tail lost around the margins. However, R. catesbeiana larvae endure much more tail damage than B. americanus consistent with the fact that they are more palatable than B. americanus (RJW, pers. obs.). Rana catesbeiana larvae overwinter and are subjected to predation pressure for a longer period of time than B. americanus, which may also account for the higher degree of damage per individual and the greater number of individuals (88%) with some amount of tail damage.
In contrast, the brevity of the larval period may explain the small degree of damage in R. dorsalis, which has the shortest time from hatching to metamorphosis (18–60 days) of all of the species examined. We believe that the slight injury observed in R. dorsalis may be a positive consequence of breeding in newly formed temporary pools, which are likely to have few large resident predators.
The pattern of tail damage in A. truei is consistent with Caldwell's (1982, 1986) hypothesis that a pigment patch at the tip of a tadpole's tail is an adaptive feature that draws the attack of predators away from a tadpole's head. The area that we found most frequently damaged in A. truei larvae bears a remarkable resemblance to the white spot at the tip of its tail. Ascaphus truei (see Hoff and Wassersug, 000: fig. 8) is the only one of the seven main species examined here where the amount of tail damage increased as the tadpole aged. This positive relationship between developmental stage and percent damage in A. truei strongly suggests that not only does the color spot attract predators but the longer the tadpoles are in the stream the more “hits” their tail tips sustain.
Similarly, the tadpoles with filamentous tails sustain damage almost exclusively to that structure. The undulating filament in P. tomopterna and R. dorsalis may thus act like the tail spot in A. truei—attracting predators through movement rather than color—and drawing attacks away from the tadpole's head.
The anterior portion of the tail sustains little damage in any of the species studied. Even R. sylvatica and P. crucifer, whose tadpoles were the most severely injured, do not lose or else do not survive damage to the most anterior portion of their tails.
Although Figiel and Semlitsch (1991) found that tadpoles with up to 75% tail loss were no more vulnerable to predators than tadpoles with intact tails, our findings suggest otherwise, at least for R. sylvatica and P. crucifer. In those species, the amount of tail damage found in the population seemed to decrease with age. This negative relationship, we believe, implies that individuals that are heavily damaged at an early stage may survive the initial attack, but only for a short time and not to metamorphosis. We recognize, however, alternative interpretations (see below).
The severity of damage in P. crucifer and R. sylvatica may reflect the success of their respective predator avoidance strategies. Pseudacris crucifer is known to be a relatively inactive tadpole that swims short distances then hides in refugia for long periods of time (Semlitsch, 1990; Skelly, 1997). Semlitsch (1990) suggested that tadpoles that use crypsis as a predator avoidance strategy would be less affected by tail loss because they would not encounter sit-and-wait predators as often as active tadpoles. This may also hold for R. sylvatica tadpoles that occasionally swim in schools (Waldman, 1984, 1991), since injured tadpoles may be able to hide within the school (the selfish herd phenomenon; Hamilton, 1971).
Surprisingly, not only do P. crucifer tadpoles show a greater frequency of damage in the younger stages, but the severity of the damage is far greater in the younger tadpoles (Fig. 2B, Table 4). Brodie and Formanowicz (1983), Crump (1984) and Caldwell (1994) all found that larger tadpoles escaped predator attacks more often than smaller ones, so we anticipated a greater frequency of damage in older tadpoles, assuming attacks on small (or young) individuals are lethal. M.-O. Rödel (pers. comm.) independently found a positive correlation between tadpole size and frequency of damage to the tail in certain African tadpoles. Our results for P. crucifer tadpoles suggest that in nature there is an increased risk of mortality once tadpoles lose more than 25% of their tail. However, alternative explanations involving improved healing rates and decreased predator attacks as tadpoles grow could account for these results.
In summary, our study shows that tadpoles with substantial damage to their tails do exist in the wild—and that it is possible to overlay images of the injuries from individual tadpoles, to produce a composite illustration of the damage in a population as a whole. Tail damage varies among species, but the damage in the seven species we studied was always concentrated on the tail tip. The pattern of tail damage between species shows some correlation with microhabitat. Specifically, benthic forms, without a color spot at the tail tip, are more likely than pelagic tadpoles to show small nicks along the whole fin margin. Tail form (i.e., filamentous vs nonfilamentous) and predator avoidance strategy (unpalatability) may also predict the severity and location of tail damage that a species sustains. The results with A. truei suggest that a color spot at the tip of tadpole tails draws predator attacks. Finally, tail loss of 25% appears to exert a cost to tadpoles in natural populations.
Citation: Ichthyology & Herpetology 2000, 2; 10.1643/0045-8511(2000)000[0390:VITPOP]2.0.CO;2
Repeatability in scoring tail damage, showing good agreement between two observers in the pattern and amount of tail damage. (A–B) Composite images from Kassina sp. (n = 9); (C–D) Phrynomantis microps (n = 19). Tail damage was scored independently by J. Glos (A,C) and by J. Blair (B,D). The average percent of tail area damaged recorded are (A) 4.1 ± 2.8, (B) 3.5 ± 1.7, (C) 2.5 ± 0.8, (D) 2.8 ± 1.1. Because of the smaller sample size, the opacity was set at a higher level (20% for Kassina and 15% for Phrynomantis) than in the following figures (Tadpole drawings provided by M.-O. Rödel)
(A) False colored composite images of tail damage for seven species, arranged from the species with the most (Pseudacris crucifer) to the species with the least (Bufo americanus) severely damaged tails. Sample sizes for each species are given in the Appendix. Source of outline drawings: Johnson (1987) for P. crucifer, Rana sylvatica, Rana catesbeiana, and B. americanus; Stebbins (1966) for Ascaphus truei; Duellman and Trueb (1986) for Rhinophrynus dorsalis; and Cannatella (1982) for Phyllomedusa tomopterna. (B) Intraspecific comparison of injury in younger, stage 26–34 (A), versus older, stage 35–43 (B), P. crucifer tadpoles
Scatterplots of percent of the tadpole tail with damage across developmental stage for Rana sylvatica collected at five sites in Nova Scotia and one site in Maryland
Scatterplots of the percent of the tadpole tail damaged versus developmental stage for each species. Sample sizes are given in the Appendix
Composite images of tail damage for Rana sylvatica tadpoles collected in five Nova Scotia ponds (n = 100 for each population)