Phenotypically Plastic Responses of Larval Tiger Salamanders, Ambystoma tigrinum, to Different Predators
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1 Phenotypically Plastic Responses of Larval Tiger Salamanders, Ambystoma tigrinum, to Different Predators Author(s) :Andrew Storfer and Candace White Source: Journal of Herpetology, 38(4): Published By: The Society for the Study of Amphibians and Reptiles DOI: URL: BioOne ( is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne s Terms of Use, available at terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. PersonIdentityServiceImpl
2 Journal of Herpetology, Vol. 38, No. 4, pp , 2004 Copyright 2004 Society for the Study of Amphibians and Reptiles SHORTER COMMUNICATIONS Phenotypically Plastic Responses of Larval Tiger Salamanders, Ambystoma tigrinum, to Different Predators ANDREW STORFER 1,2 AND CANDACE WHITE 3 1 School of Biological Sciences, Washington State University, Pullman, Washington 99164, USA 3 Department of Biology, Arizona State University, Tempe, Arizona , USA ABSTRACT. Studies of prey responses to different predators are needed to investigate costs and benefits of particular antipredator responses and to unravel community-level effects on phenotypic plasticity. We reared laboratory-bred larvae of Arizona Tiger Salamanders, Ambystoma tigrinum nebulosum with either of two common predators, diving beetle larvae (Dytiscus sp.) or dragonfly naiads (Anax junius). Relative to controls, salamander larvae in both predator treatments had shorter snout vent lengths and deeper tails; these differences may be related to increased swimming ability. In addition, larvae reared with dragonfly naiads had shorter tails than those reared with diving beetle larvae, possibly in response to different predator foraging strategies or differences in strength of selection imposed by each. Salamander larvae from predator treatments weighed less than controls, with salamanders reared with dragonflies weighing the least. This suggests that salamanders respond more strongly to dragonfly naiads than diving beetles and that dragonflies may be a more important predator. Thus, salamander larvae may distinguish between different predators, highlighting the utility of studying effects of multiple predators on phenotypic plasticity of prey. 2 Corresponding Author. astorfer@wsu.edu Environmental variation often drives the evolution of phenotypic plasticity, which is common throughout the plant and animal kingdoms (Stearns, 1989). Inducible defenses are a form of phenotypic plasticity driven by selection pressures imposed by predators (Harvell, 1990). Prey exhibit a broad array of inducible defenses, including changes in the chemical composition of plants in response to herbivory (Karban and Baldwin, 1997), spines and other morphological structures in marine and freshwater invertebrates (Harvell, 1984, 1986; Havel, 1987; Spitze, 1992), and changes in tail morphology in anurans (VanBuskirk et al., 1997; VanBuskirk and McCollum, 1999; Relyea, 2001). Amphibians have been the focus of several recent studies of predator-induced defenses (Smith and VanBuskirk, 1995; McCollum and VanBuskirk, 1996; VanBuskirk et al., 1997). Most such studies have been with single-predators, where several species of amphibian larvae show induced changes in shape and color when exposed to predatory dragonfly naiads (McCollum and Leimberger, 1997; VanBuskirk et al., 1997; VanBuskirk and McCollum, 1999; VanBuskirk and Schmidt, 2000). Studying prey responses to single predators, however, may not give an accurate picture of the true costs and benefits of a predator-induced morphology (Relyea, 2003). For example, predator avoidance by Daphnia also increased susceptibility to parasites (Decaestecker et al., 2002). Further, prey may show different responses to different predators, as in the Common Frog (Rana temporaria), whereby tadpoles exhibit a strong behavioral response to predatory dragonfly naiads, but no response to predatory newts (VanBuskirk, 2001). Tadpoles of Wood Frog (Rana sylvatica) produced predator-specific phenotypes when reared with single predators (Relyea, 2003). However, when reared with predator pairs, tadpoles of R. sylvatica developed a phenotype resembling the response when reared with the more dangerous predator alone (Relyea, 2003). Predator-induced changes can also be reflected in larval growth rates, which may be increased or decreased in the presence of predators. Growth rates may be accelerated because larger larvae may remove entirely the threat imposed by gape-limited predators (Alford, 1986; Semlitsch, 1990). In addition, rapid larval growth may allow larvae to increase predator handling time earlier than with slower growth (Formanowicz, 1986). Amphibian larvae with high growth rates can also metamorphose early to minimize their exposure to aquatic predators (Wilbur and Collins, 1973; Werner, 1986). Conversely, growth rate may be inhibited because of decreased activity level, which is a generalized antipredator response in amphibians (Sih, 1992). Decreased activity level commonly leads to reduced feeding, which often translates to decreased growth rate (Sih, 1992; VanBuskirk and Yurewicz, 1998). Herein, we present results of experiments to address phenotypic responses among larvae of the Arizona Tiger Salamander (Ambystoma tigrinum nebulosum) to two common invertebrate predators: dragonfly naiads (Anax junius) and predacious larvae of diving beetles (Dytiscus sp.). We predict differences in tail morphology in Tiger Salamanders in the two predator treatments because dragonflies and diving beetles have different predation strategies. Dragonflies are often sit-andwait predators (Corbett, 1980), where initial prey burst speed may be most important for escape. Diving beetles attempt to eat potential prey items upon contact and possibly chase them (AS, pers. obs.); thus, prey endurance may also be important (Nilsson and Svensson, 1994). In addition, we expect that larval growth will be different in both predator treatments relative to a predator-free control, because amphibian larval growth rates have been increased (e.g., to decrease time of vulnerability) or decreased (e.g., because of stress and lowered activity level) in previous studies.
3 SHORTER COMMUNICATIONS 613 FIG. 1. Snout vent length (A), tail length (B), tail depth (C), and mass (D) of larvae of Ambystoma tigrinum nebulosum in each of three treatments (control, with caged larvae of Dytiscus, or with caged Anax larvae) five weeks posthatching. Means and (þ) standard errors are presented; different letters above treatment means represent significant differences among treatments by ANOVA with Fisher s LSD multiple comparison test. MATERIALS AND METHODS Salamander Rearing. Larvae were full-sibs from a laboratory-bred pair of A. t. nebulosum. Eggs were separated into individual containers within 24 h of laying and reared in dechlorinated water with aeration until hatching. After hatching, 40 salamander larvae were reared individually in each of three treatments (a total of 120 larvae): control container (with cage but no predator present), with caged Anax naiad, or with caged Dytiscid larvae. Both predator treatments thus provided chemical and visual predator cues but precluded physical contact. Salamanders were reared individually in 4 liter white plastic ice cream buckets filled with 3.5 liters of dechlorinated water and fed g of brine shrimp daily throughout the experiment at temperatures (16 188C) and light cycle (12:12 L:D) that mimicked natural conditions. Container placement was randomized among shelves in the laboratory. We changed water once per week. Anax naiads and Dytiscid larvae were fed one salamander larva weekly that was genetically unrelated to experimental salamanders. Snout vent lengths (SVL) and masses of salamanders were measured five weeks posthatching with calipers and a top loading digital balance, respectively. Then, a digital image of each salamander was captured using a Sanyo CCD Video Camera (Model VDC-2524) interfaced with a Wild dissecting microscope and attached to a Pentium computer via an Imagenation digitizing card. We measured tail length (from the cloaca to the tail tip), maximum tail depth (width of tail at its widest point), and maximum width of tail musculature in each salamander with Optimas Version 6.0 software (Media Cybernetics, Inc. Silver Springs, MD, 1998). Salamanders were then euthanized in 0.1% MS-222 and fixed in 10% formalin. Statistical Analyses. Statistical analyses were performed with SAS Version 8.1 for Windows. We performed a MANOVA on SVL, tail length, tail depth, depth of tail muscle and mass. We then performed individual ANCOVAS, where snout vent length was used as a covariate for the four remaining variables (tail length, tail depth, depth of tail muscle, and mass). Sequential Bonferroni corrections were performed on individual ANCOVA P-values (because of nonindependence of multiple variables), and for those that were significant, we conducted Fisher s Least-Significant- Difference multiple comparisons to test for significant differences among the three treatments. RESULTS The overall MANOVA was significant (Wilks Lambda F 10, , P, 0.001), indicating an overall significant difference in measurement variables among treatments. Four of the five variables measured were significantly different among treatments, with the exception being width of tail muscle (F 2, , P ). Animals reared in either predator treatment had significantly shorter snout vent lengths (F 2, , P, 0.001; Fig. 1A) than controls. Tail length
4 614 SHORTER COMMUNICATIONS of larva was also significantly different among treatments, with salamanders reared in the presence of Anax having shorter tails than animals reared with either controls or Dytiscus (F 2, , P, 0.007; Fig. 1B), which did not differ. Both predator treatments also had deeper tails (F 2, , P, 0.001; Fig. 1C) than those reared in predator-free controls. Finally, larval mass also differed among treatments (F 2, , P, 0.001; Fig. 1D), with animals reared with Anax weighing the least, followed by Dytiscus-reared larvae weighing significantly more, and control animals weighing the most (see Fig. 1D). DISCUSSION We investigated effects of rearing salamander larvae in the presence of two predators with different foraging strategies. Salamander larvae in both predator treatments had deeper tails relative to control salamanders. This result is consistent with that of previous work in which larval amphibians reared with predatory dragonfly nymphs developed deeper tails than those in predator-free environments (VanBuskirk et al., 1997; VanBuskirk and McCollum, 1999; Van Buskirk and Schmidt, 2000; Relyea, 2001). Deeper tails should allow an individual to displace more water when swimming and consequently may increase initial burst speed and turn speed relative to animals with shallower tails (Webb, 1984; Hoff et al., 1989; Hale, 1996). Yet, in Gray Treefrog (Hyla versicolor), larvae with longer tails and shallow bodies swim faster than those with deeper tails and bodies (VanBuskirk and McCollum, 2000a,b). Thus, tail depth may be more important for increased initial burst speed in caudates relative to anurans. Caudates, and specifically Ambystoma, have generally been shown to have higher maximum amplitude of tail beat (tail tip side-to-side movements are as high as 0.35 times the total length of the animal) than anurans (rarely above one-fourth the length of the animal; Hoff et al., 1989), and more water is displaced as a result. Ambystoma also tend to have higher tail beat frequencies than some anurans, suggesting that increased tail depth may also be important for sustained swimming speed. However, tail depth, and more specifically, overall tail area is positively correlated with speed only at high tail beat frequencies in A. tigrinum (Fitzpatrick et al., 2003). Thus, how variation in tail depth and length translates to variation in swimming speed likely depends on the interaction of morphology and behavior. Salamanders reared with dragonfly naiads also had significantly shorter tails than salamanders reared with either diving beetle larvae or control animals (which did not differ). Shorter, wider tails may allow for faster initial (burst) swimming speed, which is perhaps more important for salamanders to escape dragonfly larvae, that attack via ambush, than diving beetles, which actively forage (AS, pers. obs.). A longer tail may be necessary for better sustained swimming during a chase event from diving beetles (Formanowicz, 1986; VanBuskirk and McCollum, 2000b), although overall tail area is perhaps most important characteristic for swimming speed (Fitzpatrick et al., 2003). Further tests are needed to investigate how these morphological differences influence swimming speed and predator escape ability. Salamanders reared with predators weighed less than those reared without predators. This may reflect a foraging-antipredator trade-off, whereby avoiding predation by hiding in refugia where food is often unavailable conflicts with feeding, which increases predation risk through exposure (Werner, 1986; Sih, 1992; Werner and Anholt, 1993). However, effects of predators on amphibian growth rate are contradictory. Studies by McCollum and VanBuskirk (1996) showed increased growth of tadpoles of Hyla chrysoscelis in presence of dragonfly naiads, but reduced growth occurred among several other species of tadpoles reared in presence of predators (Skelly, 1992; Van Burskirk, 2000). Reduced growth may also be a cost of devoting more energy to antipredator features as opposed to increasing overall growth (VanBuskirk, 2000). VanBuskirk and McCollum (1996) showed that tadpoles with induced tail morphology survived well in the presence of predators, but did not survive as well as control animals in predator-free environments, suggesting a cost to their antipredator response. A predator-induced phenotype in newt larvae (Triturus) also grew more slowly than those reared without predators a cost in ephemeral habitats (Van Buskirk and Schmidt, 2000). Salamander larvae reared with dragonflies weighed less than those reared with diving beetles. This could be caused by the fact that Anax sp. are more important (e.g., more efficient or more common) predators than Dytiscus and thus, larvae reduce feeding rate more in presence of dragonfly naiads relative to Dytiscus. Field surveys throughout Arizona suggest that dragonfly naiads are more common than diving beetles and at higher densities when both predators are found (AS, unpubl.). Wood Frog tadpoles exhibited phenotypes in predator combinations that resembled those induced when reared with the more dangerous predator alone (Relyea, 2003). Thus, amphibians may be able to discern among predators and respond accordingly by developing a morphology appropriate for the most important predator type. Studies of prey responses to multiple predators thus give a more complete picture of community dynamics than studies on single predators, and can guide future experiments designed to detect the relative strengths of selection imposed by different predator species and emergent multiple predator effects. Acknowledgments. We thank P. Verrell, C, Steele, S. Mech, K. Lew, M. Reudink, and two anonymous reviewers for valuable comments that helped improve this manuscript. This work was supported by a Maytag Postdoctoral Fellowship to AS. The experiments herein were approved under the Arizona State University IACUC. LITERATURE CITED ALFORD, R. A Effects of parentage on competitive ability and vulnerability to predation in Hyla chrysoscelis tadpoles. Oecologia 68: CORBETT, Biology of odonata. Annual Reviews of Entomology 25: DECAESTECKER, E., L. DE MEESTER, AND D. EBERT In deep trouble: habitat selection constrained by multiple enemies n zooplankton. 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