Effects of metamorphosis on the aquatic escape response of the two-lined salamander (Eurycea bislineata)
1 Graduate Program in Organismic and Evolutionary Biology and
2 Biology Department, University of Massachusetts, Amherst, MA 01003-9297, USA
*e-mail: mannya{at}bio.umass.edu
Accepted 4 January 2002
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Summary |
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Movie available on-line: http://www.biologists.com/JEB/movies/jeb3978.html.
Key words: amphibian metamorphosis, salamander, escape response, kinematics, C-start, tail morphology, locomotion, swimming, Eurycea bislineata, Plethodontidae, Caudata.
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Introduction |
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While there has been some interest in the terrestrial escape responses of salamanders (e.g. Dowdey and Brodie, 1989; Whiteman and Wissinger, 1991
) and a few investigators have studied the aquatic escape behavior of anuran tadpoles (Will, 1991
; von Seckendorf Hoff, 1989
; von Seckendorf Hoff and Wassersug, 2000
), the aquatic escape responses of salamanders remain largely unexplored. The escape response literature is dominated by studies of fishes. These focus on kinematics (for a review, see Domenici and Blake, 1997
), motor pattern (Jayne and Lauder, 1993
; Westneat et al., 1998
) and neural control (Eaton et al., 1977
; Eaton and Bombardieri, 1978
; Fetcho, 1991
; Zottoli, 1978
, 1995
). Often referred to as a C-start or fast-start, the escape response of most fishes is a rapid movement consisting of two distinct stages. A variety of different criteria have been used to define the two stages, including acceleration profiles and muscle activation patterns, but, in common with many previous studies, we will use a kinematic definition (e.g. Domenici and Blake, 1993b
; Hale, 1999
). Stage 1 represents the preparatory stroke, characterized by a high degree of axial bending with little movement of the center of mass. Stage 2 represents the propulsive stroke in which a large-amplitude propulsive wave is passed down the body, moving the animals center of mass away from the stimulus (Weihs, 1973
).
Eurycea bislineata was chosen for this study because it is a common local species whose propensity for aquatic escape behavior was well known to us from previous experience in the field. Both adults and larvae spend their lives in close proximity to streams. The larvae are entirely aquatic, while the adults inhabit the edges and splash zone of streams (Petranka, 1998). In addition, adults may spend up to 4 months of the year in a stream during the breeding season (Petranka, 1998
). Predator avoidance in streams is therefore assumed to be a critical aspect of the ecology of both larval and adult E. bislineata.
The two main goals of this study are to provide a kinematic description of the escape response of Eurycea bislineata and to examine the effects of metamorphosis on aquatic escape performance. We quantify and compare the following three aspects of escape performance: the duration of both stages of the escape, the final escape trajectory (at the end of stage 2) and the distance traveled during the propulsive phase of the escape (stage 2). On the basis of general scaling models (e.g. Schmidt-Nielsen, 1993), we predict that total escape duration will increase with body length. However, this scaling trend is not likely to shift significantly as a result of metamorphosis. On the basis of both empirical data (Eaton and Emberley, 1991
; Domenici and Blake, 1993a
; Hale, 1999
) and theoretical predictions (Weihs and Webb, 1984
) of optimal escape trajectory, we predict that both life stages of E. bislineata will have a final escape angle that is directed away from the stimulus. This escape trajectory places the most vulnerable parts of the body farthest from a predator. We will also test the hypothesis that the distance traveled during the propulsive phase of the escape will be a function of the relative depth of the thrust-producing segment (Weihs, 1973
). Because of changes in tail shape associated with metamorphosis, we predict that, for a given size, adults will travel significantly shorter distances than larvae during stage 2 of the escape response. Finally, by comparing escape performance between larvae and adults, we will test the hypothesis (Carrier, 1996
) that higher levels of predation on the early life stages of a species result in young individuals exhibiting better locomotor performance for their size than adults.
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Materials and methods |
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Morphometric data were gathered from digital images captured on a Nikon Coolpix 990 digital camera, calibrated with a ruler and analyzed using NIH Image 1.62. Animal collection, care and experimental procedures were approved by the University of Massachusetts Amherst Institutional Animal Care and Use Committee. All specimens were killed in a buffered solution of 2 g l1 tricaine methanesulfonate (MS222) in water prior to being photographed for morphometric measurements and later deposited in the Massachusetts Museum of Natural History at UMASS Amherst.
High-speed videography
Escape responses were filmed in dorsal view in a 40 cmx50 cmx10 cm plastic tank half-filled with RO water. To eliminate interference from the walls (such as the animals pushing off or fluid boundary effects), the field of view was limited to the center area (30 cmx30 cm) of the tank. Prior to eliciting escape responses, salamanders were placed near the center of the field of view to maintain a minimum of 10 cm (at least 1 body length) from the closest wall. High-speed video of escape responses was recorded at 250 frames s1 and 1/250 s shutter speed using a Kodak Ektapro EM processor and was downloaded to SVHS videotapes. Video sequences were converted to TIFF files using Adobe Premiere 5.1 and analyzed using NIH image 1.62. Distances in the video sequences were calibrated by filming a 16 cm ruler before each salamander was placed in the tank and after any adjustments to the camera. Water temperature in the filming tank was maintained at 10±1°C to match the temperature of the holding tanks and that of the salamanders natural environment.
Filming trials were limited to a maximum of 15 min and five escapes per individual per day to avoid fatigue and acclimation to the stimulus. After each filming trial, salamanders were allowed a minimum of 3 days of recovery prior to the subsequent filming trial. To test whether the salamanders were fatiguing during the 15 min filming period, we performed a one-factor analysis of covariance (ANCOVA) comparing the distance and duration of the first and last escape response recorded on each day by each salamander. We found no significant difference in escape distance (P=0.984) or duration (P=0.843) between the initial and final escape responses recorded on a given day, indicating that the salamanders did not fatigue during the course of the 15 min filming trial. To look for possible long-term acclimation of the salamanders to our experimental protocol, we compared the initial filming trials of each salamander with all subsequent days of data collection using a one-factor analysis of variance (ANOVA). We found that previous exposure to our experimental protocol did not significantly affect the distance (P=0.216) or duration (P=0.392) of the escape response. This suggests that long-term acclimation to both captivity and our experimental protocol did not have a significant effect on escape behavior.
Stimulus
To elicit escape responses, we oriented a glass stirring rod (4 mm in diameter) perpendicular to the long axis of the body and delivered a tactile stimulus to the forelimb or the pectoral region of the salamanders. We were occasionally able to elicit escape responses by directing a tactile stimulus to the hind limb or trunk region, but this was not consistently effective. Prior to the adoption of our experimental protocol, we tested the efficacy of various stimulus types used in previous studies to elicit escape responses. Pressure waves created by tapping the side or bottom of a tank have been effective as a method of inducing escape responses in fishes (e.g. Eaton and Emberley, 1991) and anuran tadpoles (Yamashita et al., 2000
). In contrast, we were unable consistently to induce an escape response in Eurycea bislineata using this stimulus. However, since immobility has been shown to be a defensive response in amphibians, it cannot be considered a lack of response (Brodie et al., 1974
; Caldwell et al., 1980
). The use of immobility in combination with cryptic coloration may be an important predator avoidance strategy, but in this study we will focus on escape behavior induced by tactile stimuli. While it is consistent with our observations that a vibratory (pressure wave) stimulus induces immobility in E. bislineata, we have performed no specific tests of this behavior. Responses to all the various types of stimuli described above were largely consistent across both life stages and all individuals.
Kinematic analysis
We analyzed 711 escape responses per individual for a total of 159 escapes. All escape responses that included obvious movement in the vertical direction or did not include both kinematic stages were removed from our sample. In this study, stage 1 is defined as beginning at the first detectable movement and ending when the body reaches maximum curvature. Stage 2 is defined as beginning at maximum body curvature and ending at the frame in which the first propulsive wave has been propagated off the body. The duration of each kinematic stage was calculated by multiplying the total number of frames by the time interval (4 ms) between adjacent frames.
Body curvature was quantified using a variation of curvature coefficient as defined by Webb (1978). Curvature coefficient has previously been defined as the linear distance from the center of mass to the trailing edge of the tail at maximum curvature divided by that same distance at rest. Thus, curvature coefficient decreases with higher body curvature. In an attempt to use a more intuitive measure of curvature, we define a variable that increases with increasing body curvature. To avoid confusion, we call this parameter bending coefficient (Fig. 1) and define it as the linear distance (chord length) from the tip of the snout to the tip of the tail divided by total length and subtracted from 1. The escape kinematics of Eurycea bislineata is unique when compared with published results from fishes performing C-starts because the salamanders head can pass over its tail during high-curvature responses. Similar high-curvature movements have also been observed during the air-breathing maneuvers of Xenopus laevis tadpoles (Wassersug, 2001
). In escapes in which the head passes over the tail, the distance between the snout and the tip of the tail is measured as negative, resulting in a bending coefficient greater than 1.
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The distance that salamanders traveled during stage 2 was measured as the linear displacement of a digitized landmark on the pectoral girdle between the time at maximum curvature and the end of stage 2.
Statistical analyses
To compare the duration, distance and curvature parameters between the two ontogenetic stages, overall differences in total length were accounted for using a one-factor ANCOVA. Life stage was set as the factor, total length was set as the covariate and escape parameters were treated as the dependent variables. Mean values for each individual were used in the ANCOVA test. Significance levels are reported after the non-significant interaction terms have been removed. SuperAnova 1.11 was used for all non-polar statistical tests.
In our analysis of escape angles, we used a one-factor ANOVA to test for individual effects within each life stage. No significant difference in escape angle was detected among individuals. This allowed us to pool all escapes within each life stage prior to running polar statistics. A WatsonWilliams test was used to compare stage 1 and final escape angles between the two life stages (Zar, 1996). Mean values and 95 % confidence intervals for stage 1 angles and final escape angles were also calculated for both life stages (Zar, 1996
).
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Results |
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Tail morphology
The change in tail shape of salamanders at metamorphosis is a morphological transition likely to affect aquatic locomotor performance. Tail aspect ratio, defined as the ratio of maximum tail height squared to tail area, is an important morphological determinant of swimming hydrodynamics and performance and is used in this study as our measure of tail shape (Fig. 2) (Vogel, 1994). A significant difference in aspect ratio was found between the two life stages using a one-factor ANCOVA (P=0.0007). Aspect ratio ranged from 0.16 to 0.25 for larvae and from 0.09 to 0.16 for adults. Tail aspect ratio was not found to be significantly correlated with total length (P=0.4593). See Table 1 for a summary of morphometric data.
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Discussion |
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In contrast to the results predicted by this hypothesis, we found that the distance traveled in stage 2 did not differ significantly between larvae and adults (Table 2). Although the adults in our sample had tails with lower aspect ratio, they perform escapes with significantly higher maximum curvature (Fig. 3). With an increase in the maximum curvature, a corresponding increase in the wave amplitude and therefore the rearward thrust component of the propulsive wave should occur in stage 2. Support for this comes from Andraso (1997), who found that higher maximum curvature increases the distance traveled during C-starts in the brook stickleback Culaea inconstans. It is possible that the decreased tail aspect ratio of adult Eurycea bislineata is compensated for by an increase in maximum curvature, thereby maintaining a mean stage 2 escape distance that is similar to that of larvae. Thus, our initial performance predictions based on morphological differences are complicated by kinematic variation in the behavior.
The function of the amphibian tail fin as an effective thrust-generating surface remains somewhat contentious. Despite a lack of ossified support elements, the tail fin of bullfrog (Rana catesbeiana) tadpoles does not undergo passive lateral deflection during steady swimming and may therefore contribute to thrust production (Wassersug and von Seckendorf Hoff, 1985; Doherty et al., 1998
). However, experimental tail fin ablations of up to 30 % in depth have no significant effect on maximum swimming velocity or the time needed to travel 2.5 cm in the gray treefrog Hyla versicolor (Van Buskirk and McCollum, 2000
). Understanding the locomotor contributions of the larval tail fin in salamanders will require ablation experiments comparing locomotor performance within individuals.
The final escape trajectory (measured at the end of stage 2) of the prey relative to a stimulus has been considered an important measure of escape performance (Eaton and Emberley, 1991; Domenici and Blake, 1993a
; Hale, 1999
). Although values for the final trajectory of fast-starts in fishes are variable when the stimulus is directed at the cranial or caudal end of the animal, laterally directed stimuli often result in an escape trajectory directly away from the stimulus (Eaton and Emberley, 1991
; Domenici and Blake, 1993a
; Hale, 1999
). Theoretical predictions of predator avoidance strategies suggest that the optimal escape angle lies within 21° of a predators approach angle (Weihs and Webb, 1984
). Consistent with theoretical predictions and the observed behavior of fishes, we found that the mean final escape angle (end of stage 2) for both life stages did not differ significantly from 90° (which is directly away from the stimulus). This final escape angle positions the tail closest to and the head farthest from the stimulus direction. This escape trajectory is also consistent with observations that tadpoles and salamanders often suffer tail loss or damage during interactions with predators (e.g. Caldwell et al., 1980
; Whiteman and Wissinger, 1991
).
In one laboratory experiment, adult Eurycea bislineata utilized tail autotomy in 59 % of encounters with a predatory snake (Thamnophis sirtalis), and 33 % of individuals collected in the field had damaged, autotomized or regenerated tails (Whiteman and Wissinger, 1991). Wake and Dresner (1967
) reported that 8.3 % of museum specimens of E. bislineata were either missing or had regenerated more than half the length of their tails. Although adults in our study utilize higher curvature and greater net angular rotation during the escape, both life stages use an escape trajectory that is directly away from a laterally directed stimulus (Fig. 6).
Given the limited size range of our sample, we will only discuss the general scaling trends observed in our data, with no reference to various scaling models. We found that stage 1, stage 2 and total escape duration had significant positive correlations with total length. These results are consistent with previous studies investigating escape performance across a size range (Webb, 1977, 1978
; Domenici and Blake, 1993b
; Hale, 1999
). Although the mean total escape durations for both life stages of Eurycea bislineata are considerably higher than for fish of similar body length, no comparable data are currently available for C-starts in fish with a similarly elongate body shape (Domenici and Blake, 1997
). An elongate body shape may be correlated with increased overall body flexibility, allowing for higher maximum curvature during the escape response (Brainerd and Patek, 1998
). In support of this, E. bislineata (with its elongate shape) utilizes higher-curvature escape responses than previously observed in fishes performing C-starts. Westneat et al. (1998
) observed that, in high-curvature responses, the head and the caudal fin of Polypterus palamas made contact at maximum curvature. Lacking a caudal fin, the tapering tails of adult E. bislineata may allow for greater maximum curvature by permitting the head to pass over the tail during stage 1 of the escape. Given the high-curvature responses of adult E. bislineata, it is likely that relatively more time is required to reach maximum curvature, thereby increasing the total duration of the escape.
The distance that Eurycea bislineata travels during stage 2 of the escape is positively correlated with total length. Similar scaling trends for this performance parameter have been observed in fishes (Webb, 1977, 1978
; Domenici and Blake, 1993b
). Despite the relatively shallow body of E. bislineata, the range of distances traveled in stage 2 is comparable with values reported for fish of similar body length (Webb, 1978
; Hale, 1999
; Domenici and Blake, 1993b
). The decrease in potential thrust production due to a lower maximum body depth may be counteracted by the high-amplitude propulsive wave associated with the high-curvature responses of E. bislineata.
It is possible that the neural mechanism initiating an escape response in Eurycea bislineata differs from the Mauthner-initiated response described in fishes (Eaton et al., 1977; Eaton and Bombardieri, 1978
; Fetcho, 1991
; Zottoli, 1978
, 1995
). Although numerous studies have correlated C-start behavior with the presence and activity of Mauthner neurons (Zottoli, 1977
), Eaton et al. (1982
) showed that alternative neural mechanisms can also induce kinematically similar escape responses. Alternative neural mechanisms or variations in Mauthner cell morphology could affect both the latency of a response and the type of stimulus that induces a response. Although it is not known whether Mauthner cells are present in E. bislineata, they have been described in larvae and adults of numerous amphibian species, including several other plethodontid salamanders (Will, 1991
; Zottoli, 1978
).
Carrier (1996) hypothesized that, as a result of heavy predation on the early life stages of individuals, selection will favor relatively better locomotor performance early in ontogeny. In the case of Eurycea bislineata, the testing of such predictions is complicated by morphological and ecological changes at metamorphosis. We found no evidence to support the hypothesis that aquatic escape performance decreases after metamorphosis in E. bislineata. It is likely that kinematic modulation of the escape response allows adults to sustain an effective level of escape performance despite changes in morphology and ecology.
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Acknowledgments |
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