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Gomez-Mestre, I., & Keller, C. (2003). Experimental assessment of turtle predation on larval anurans. Copeia, 2003(2), 349–356.
Added by: Admin (14 Aug 2008 20:36:22 UTC) |
| Resource type: Journal Article BibTeX citation key: GomezMestre2003 View all bibliographic details  |
Categories: General Keywords: Emydidae, Emys, Emys orbicularis, Ernährung = nutrition, Fressfeinde = predators, Geoemydidae, Habitat = habitat, Mauremys, Mauremys leprosa, Schildkröten = turtles + tortoises, Südwesteuropa = South-Western Europe Creators: Gomez-Mestre, Keller Collection: Copeia |
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| Abstract |
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Emys orbicularis, Mauremys Effect of predator species and sex.- Emys orbicularis was a more efficient predator than M. leprosa in all cases, causing significant decreases in survivorship rates of B. calamita, H. meridionalis, and P. cultripes (Table 2 ). Emys orbicularis consistently eliminated all P. cultripes in all trials but had a more variable behavior with the other species. The lower survivorship of B. calamita exposed to E. orbicularis was caused by three turtles that predated upon 90-100% of the tadpole sample, all remaining tadpole survivorship rates varying from 0.57-0.99. Likewise the lower survivorship of R. perezi exposed to E. orbicularis was caused by two individuals that consumed 100% of tadpoles, the remaining survivorship rates (0.70-1.00) being similar to those obtained for M. leprosa. No differences were observed in tadpole survivorship when comparing males and females within predator species, except for a significantly lower survivorship of P. cultripes exposed to female M. leprosa (12 = 7.15, P = 0.0075). Evidence for size selection.- Pelobates cultripes surviving exposure to M. leprosa were significantly smaller (F1,9 = 71.09, P < 0.0001), while R. perezi exposed to E. orbicularis were significantly larger (F1,8 = 6.04, P = 0.039) than tadpoles from the initial pool (Fig. 1 ). No evidence for size selection was observed for B. calamita and H. meridionalis, nor for R. perezi exposed to M. leprosa. Evidence for tadpole unpalatability.- With the exception of B. calamita, significant differences were observed in rejection rates between turtle species (Table 2 , Fig. 2 ), whereas rejection rates were < 1% in all cases for E. orbicularis, M. leprosa rejected, on average, from 50% to almost 90% of tadpoles killed. As a consequence, consumption rates differed more between predator species than tadpole survivorship rates. Notably, all R. perezi tadpoles killed were rejected by M. leprosa except for two females that swallowed one tadpole each. For H. meridionalis and P. cultripes individual rejection responses of M. leprosa were more variable, ranging from 100% rejection to nearly 100% consumption of the preclated tadpoles. Discussion Return to TOC Effect of predator species and sex.- Emys orbicularis was a more efficient predator than M. leprosa in all cases. Emys orbicularis is an almost exclusive consumer of animal prey in Doñana, whereas M. leprosa feeds predominantly on plants (Keller and Busack, 2001 ). Direct observations in the experimental pools also indicated that, although E. orbicularis made frequent capture attempts, M. leprosa tended to ignore tadpoles more often. In nature, nearly 30% of live animal biomass ingested by E. orbicularis is composed of small invertebrates, whereas M. leprosa favors crayfish and fish as animal prey (C. Keller and J. L. Garcia-Mudarra, unpubl. data). The habit of capturing small animals may explain why E. orbicularis was a more efficient consumer of smaller tadpoles like B. calamita. Lower survivorship rates of P. cultripes (the largest tadpole species tested) when exposed to female M. leprosa as compared to males, seemed to indicate that females favored larger, probably energetically more rewarding prey, which may be caused by females being in the demanding egg-producing phase. Consumption rates of all tadpole species for female E. orbicularis (also in egg-maturing phase) were higher than those of female M. leprosa, but, unlike male M. leprosa, male E. orbicularis were as voracious as females. The intraspecific individual variability in predatory efficiency of turtles observed in our experiments is likely to reflect differential foraging strategies or abilities. This might be related to distinct habits of microhabitat use, to individual differences in reaction time and sprint capacity or even different sensitivity to unpalatability (as suggested by the variance in rejection rates of Hyla and Pelobates tadpoles by M. leprosa). Studies concerning foraging habits of vertebrate species in the wild are traditionally standardized on the population level and usually overlook individual variation. However, individual variation in foraging strategies may cause considerable fitness differences among individuals (Grant and Grant, 1996 ; Annett and Pierotti, 1999 ; Fedriani and Kohn, 2001 ) and may, in turn, differentially affect prey fitness at the local scale. Evidence for size selection.- Pelobates cultripes was predated upon frequently and consumed more frequently. The complete eradication of all P. cultripes by E. orbicularis, and the selection of larger tadpoles by M. leprosa both indicate that turtles tended to favor the capture of larger prey, in agreement with predictions of optimal foraging theory. In contrast with our predictions, however, R. perezi (the second largest prey species in body size), was the least consumed. Moreover, E. orbicularis predated more heavily on smaller R. perezi tadpoles. Pelobates tadpoles of the same length as Rana are bulkier, whereas Rana has a more streamlined profile and more powerful tail muscles, higher speed and greater maneuverability, which makes them less susceptible to predation than Bufo and Hyla (Chovanec, 1992 ; Richardson, 2001 ). Likewise, successful escapes of other tadpole species were related more to burst speed and maneuverability than to stamina (Feder, 1983 ). Frustrated predation attempts of E. orbicularis on R. perezi occurred when tadpoles outmaneuvered the turtle, performing fast and short strokes in a direction other than the persecution line. Thus, the capture of R. perezi tadpoles probably has a higher energetic cost to turtles compared to slower species, and the enhancement of the escape performance associated with an increase in body size probably outbalances the benefits obtained from capturing larger prey. The higher predation rates upon H. meridionalis tadpoles in comparison with R. perezi were likely a consequence of the resemblance between the Hyla and Pelobates morphotypes as well as of the lower amount of Hyla biomass offered to turtles. Evidence for unpalatability.- Besides being difficult to catch, all but two R. perezi tadpoles killed by M. leprosa were rejected. The same reaction was observed for Ambystoma newts predating upon Rana sphenocephala (Morin, 1983 ). These observations indicate that Rana tadpoles may be unpalatable to some vertebrates. Yet the fact that practically all R. perezi captured by E. orbicularis were readily consumed suggests that tadpole palatability may vary even among taxonomically close predator species, which was also observed by Banks and Beebee (1988) for predation of B. calamita and Bufo bufo tadpoles by three Triturus species. These observations suggest that the defensive value of producing substances aimed at distastefulness in terms of tadpole fitness may be highly dependent on the local composition of the predator guild at different ponds. Contrary to expectations based on reports of unpalatability of Bufo embryos and tadpoles to vertebrate predators (Heyer et al., 1975 ; Denton and Beebee, 1991 ; Azevedo-Ramos and Magnusson, 1999 ) unpalatability seemed to be no deterrent to predation of B. calamita by E. orbicularis and M. leprosa, judged by the absence of rejected tadpoles. Bufo calamita have weaker axial musculature and are slower swimmers than comparable sized Rana tadpoles (Wassersug and Hoff, 1985 ), and their aggregation behavior and tendency to continous activity makes them particularly vulnerable to visually oriented predators (Wassersug, 1973 ; Heyer et al., 1975 ; Chovanec, 1992 ). Thus higher evasiveness is unlikely to have been the cause of Bufo experiencing lower predation by turtles than either Hyla or Pelobates. Possibly the small size of B. calamita tadpoles, which was below the minimum sizes of all other tadpole species tested, made them less attractive to most turtles. The 100% predation rates observed for B. calamita by some E. orbicularis, however, indicate that individual E. orbicularis may be highly efficient predators of B. calamita in its usual breeding pools, which bear a closer resemblence with the experimental pools than most other amphibian breeding habitats. The adaptive advantage attributed to the use of very small ephemeral ponds as breeding sites by anurans is the reduction of predation pressure on larvae by aquatic predators (Woodward, 1983 ; Roth and Jackson, 1987 ; Pearman, 1995 ). In the present context, the robustness of this hypotheses deserves to be tested with relation to large vertebrate predators that are not bound to water, which have a much higher potential for consumption and for which the crowding and higher exposure of tadpoles in small pools may act as a facilitator of predation success. Newman (1987) found indirect evidence of turtles acting as total eradication agents of tadpole populations in small desert pools. Although the biological significance of our results in natural conditions will be mediated by other factors, like availability and abundance of other food resources for turtles, habitat complexity, and the previous experience of tadpoles with predators, the evidence produced favors the notion that the impact of both turtle species-especially E. orbicularis-on tadpole populations is substantial. Our results suggest that turtles are generally keen on larger tadpoles, either because they are easier to see when they move, or because they represent a higher energy reward per unit of effort (as for P. cultripes) and, otherwise, that limitations like visual accuracy and sprint speed or maneuverability may impose prey size limitations even to predators that are not gape-size limited. Moreover, tadpole traits widely accepted as defensive strategies against vertebrate predators, like unpalatability, may vary in efficiency among predators of the same guild. Therefore, the presence of turtles in anuran breeding areas should not be overlooked in studies concerned with the conservation and ecological dynamics of tadpole assemblages. Abstract: The effect of predation by large non-gape-limited vertebrates on the survivorship and size distribution of larvae of four anuran species was assessed using two syntopic freshwater turtle species, Emys orbicularis and Mauremys leprosa. Predator species and predator sex within species were used as treatments in replicated, factorial experiments for predation trials on tadpoles of Bufo calamita, Hyla meridionalis, Rana perezi, and Pelobates cultripes. Tadpole consumption rates were significantly higher for the carnivorous E. orbicularis than for M. leprosa. Rana perezi tadpoles were the least consumed, whereas P. cultripes and H. meridionalis had the lowest survivorship rates, being relatively easier to catch than R. perezi. Significant size selection occured for larger tadpoles of P. cultripes, whereas predation upon R. perezi tended to concentrate on the smaller size classes. The results point to an overall tendency of turtles to predate upon large tadpoles, yet the outcome of size selection by large vertebrates may depend on phenotypic traits that enhance the escape potential of tadoles. Mauremys leprosa had a high rejection rate of tadpoles, suggesting a higher sensitivity to unpalatability as compared to E. orbicularis, especially with relation to R. perezi. The results indicate that the effect of unpalatability as a predation deterrent may vary even among taxonomically close predator species.
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