The Relation of Air Breathing and Locomotion to Predation on Tadpoles, Rana berlandieri, by Turtles

Division of Comparative Physiology and Biochemistry, Society for Integrative andComparative Biology

The Relation of Air Breathing and Locomotion to Predation on Tadpoles, Rana berlandieri, byTurtlesAuthor(s): Martin E. FederSource: Physiological Zoology, Vol. 56, No. 4 (Oct., 1983), pp. 522-531Published by: The University of Chicago Press. Sponsored by the Division of ComparativePhysiology and Biochemistry, Society for Integrative and Comparative BiologyStable URL: http://www.jstor.org/stable/30155875 .

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THE RELATION OF AIR BREATHING AND LOCOMOTION TO PREDATION ON TADPOLES, RANA BERLANDIERI, BY

TURTLES'

MARTIN E. FEDER

Department of Anatomy and Committee on Evolutionary Biology, University of Chicago,

Chicago, Illinois 60637

(Accepted 4/18/83)

To examine how air breathing affects susceptibility to predation in anuran larvae, predatory encounters were staged between tadpoles of the frog Rana berlandieri and turtles (Chrysemys picta) in a laboratory setting. Swimming and air-breathing movements of tadpoles increased the distance at which turtles recognized and attacked tadpoles. Turtles attacked only one nonmoving tadpole more than 30 cm distant but attacked moving tadpoles up to 175 cm distant. However, only 5% of tadpoles attacked while moving were actually swimming to breathe air. Locomotor stamina (and hence its enhancement by air breathing) had little bearing on the outcome of predatory encounters. Encounters (no. = 171) averaged 11.4 s (SD = 7.0 s), and fewer than 10% exceeded 20 s. Tadpoles' escapes from turtles involved burst speed or maneuverability rather than stamina. Escaped and captured tadpoles differed in speed and number of abrupt turns, but not in distance swum and swimming time. Lactate concentrations of tadpoles did not change during simulated predatory encounters. Tadpoles increased movement after a predator's attack. The data suggest that air breathing increases tadpole recognition by visually oriented predators and does little to aid a tadpole's escape in a predatory encounter. Thus, the real benefit of air breathing to most tadpoles in nature remains an open question.

INTRODUCTION

Most studies of air breathing in aquatic vertebrates emphasize the advantages of this behavior. Some commonly cited advantages are the ability to exploit hypoxic aquatic environments (Randall et al. 1981), the low energetic cost relative to breathing water (Dejours 1981), and increases in locomotor stamina (Brett 1972; Wassersug and Feder 1983). A critical examination of these supposed advantages, however, often fails to substantiate them (Kramer 1983). For example, most fish in typical hypoxic aquatic habitats breathe only water and not air (Kramer et al. 1978; Burggren 1982), suggesting that air breathing is frequently not necessary for survival in hypoxic

This manuscript benefited greatly from the in- sightful comments of T. Baird, R. Gatten, J. Gra- ham, D. Kramer, R. Wassersug, and several anonymous referees, and grew out of stimulating dis- cussions with R. Wassersug. Allen Gibbs provided technical assistance and ably simulated a tadpole predator. Research was supported by NSF grant DEB 78-23896 and the Louis Block Fund, the University of Chicago.

Physiol. Zool. 56(4):522-531. 1983. C 1983 by The University of Chicago. All

rights reserved. 0031-935X/83/5604-8314$02.00

aquatic environments. The low energetic cost of breathing air instead of water may be offset by the high costs of traveling to the surface to breathe air (Kramer and McClure 1981) and of evading predators that await surfacing prey (e.g., Kramer and Graham 1976; Kramer, Manley, and Burgeois 1983). Air breathing may also in- terrupt activities that occur below the surface (Halliday and Sweatman 1975) and decrease swimming performance due to the increased buoyancy afforded by air-filled lungs (Wassersug and Feder 1983).

A previous study (Wassersug and Feder 1983) sought to examine critically the third advantage cited above, enhanced locomotor performance. In that study, tadpoles of the frog Rana berlandieri increased their rate of air breathing when swimming in a current and thereby improved their locomotor stamina. However, the significance of such increased stamina to tadpoles in nature is unclear for several reasons. (1) Although detailed observations of tadpole behavior in the field are rare, most natu- ralists agree that tadpoles seldom swim at high speeds for long periods (R. J. Was- sersug, personal communication). (2) An obvious context in which stamina may be

522



AIR BREATHING AND PREDATION IN TADPOLES 523

important to tadpoles is in escaping predators. However, encounters between tadpoles and their predators have seldom been observed. (3) In order for air breathing to improve the probability of escaping predators through its effect on stamina, predator-prey encounters must be relatively prolonged. Augmentation of oxygen consumption via air breathing would affect primarily sustained activity and be neutral or negative in terms of burst performance (Bennett 1980; Wassersug and Feder 1983). (4) Even though breathing air might improve a tadpole's capability of eluding a predator, any increase in predatory attacks on tadpoles because of their increased visibility as they swim to the surface to breathe might well offset their improved antipred- ator performance (Kramer 1983; Kramer et al. 1983).

The influence of air breathing on susceptibility to predation in tadpoles is best elucidated through direct observation of tadpoles and their predators in the field. However, several aspects of tadpole habitats frustrate clear observations of behavioral interactions. Such habitats are frequently turbid, structurally complex, and difficult to manipulate; moreover, in the field both tadpoles and their predators are quite wary of human observers. A laboratory setting for observations of predator-prey interactions, although it may simplify or exaggerate aspects of the hab- itat, may yield important insights into the adaptive significance of air breathing and locomotor stamina that are not readily ob- tainable in the field. Therefore, as a first approximation, encounters were staged in the laboratory between tadpoles of Rana berlandieri and the turtle Chrysemys picta, a natural aquatic predator on tadpoles (Heyer and Muedeking 1976). These encounters addressed two questions: (1) Does the increased activity of air breathing itself elicit predatory attacksd (2) Is the outcome of predatory attacks related to a tadpole's stamina, to other factors (e.g., speed, maneuverability, crypsis), or to chanced

MATERIAL AND METHODS

Turtles (Chrysemys picta) and tadpoles (Rana berlandieri) were purchased from NASCO, Ft. Atkinson, Wisconsin. Turtles (no. = 10) had shell lengths between 10

and 15 cm. Tadpoles were reared in the laboratory until they reached 30-60 mm total length and developmental stages 35- 39 (Gosner 1960). Their front limbs had not emerged; their hind limbs were not used to swimming. Tadpoles were fed boiled lettuce daily, were on a 14L:10D photoperiod, and were maintained at room temperature (22 + 2 C). Turtles were maintained at room temperature in a large cage with running water. The turtles were fed commercial dog food, but feeding was halted several days before experimentation.

Predator-prey encounters were staged in a large concrete tank, 260 cm x 260 cm, with a gradually sloping bottom. Water depth ranged from 5 to 35 cm. Except for a standpipe in the deep end of the tank, no obstructions impeded either the line of sight or the swimming of the experimental animals. The tank water was aged for at least 24 h before the animals were intro- duced, and tadpoles suffered no ill effects from the water. Water temperatures were between 24 and 28 C but were relatively constant at any given location in the tank. Oxygen content of the water was measured with a YSI Model 54 dissolved oxygen meter (Yellow Springs Instruments, Antioch, Ohio) and was never less than 80% of saturation.

Except as noted below, both turtles and tadpoles were placed in the tank at least 1 h before observations began. Turtles were allowed to swim freely. Tadpoles were con- fined within a circular screen enclosure, diameter 60 cm. The enclosure allowed the tadpoles to become accustomed to the water and move about freely but prevented them from being attacked prematurely. The turtles apparently did not respond to tadpoles within the enclosure. In a typical trial, a single turtle and six tadpoles were placed in the experimental tank. After at least 1 h, an observer lifted the screen enclosure from the water and noted the subsequent behavior of both predator and prey. The duration of attacks was timed with a stopwatch. Observations were halted when either all tadpoles were eaten or a turtle ceased attempting to capture tadpoles and began attempting to escape from the experimental tank.

This standard protocol was sometimes altered in the following ways: (1) To de-



524 M. E. FEDER

termine tadpole behavior before and after a predator's attack, tadpoles were placed in the experimental tank 4 h before observations began. The screen enclosure was omitted. After 1 h of behavioral observations, the observer chased tadpoles about for 60 s with a wooden rod to simulate a predator's attack. Tadpoles were then observed for an additional hour. (2) To measure anaerobic metabolism during a predator's attack, tadpoles were placed in the tank as in 1. After 4 h, one observer chased individual tadpoles with a small fishnet while a second timed each chase with a stopwatch. At the end of each chase (determined arbitrarily) the tadpole was caught and immediately frozen in liquid nitrogen. While still frozen, the carcass was weighed and homogenized in approximately 5 vol of ice-cold 0.6 N perchloric acid; the tadpole's specific gravity was as- sumed to be 1.0. The lactate content of the homogenate was analyzed enzymatically according to Bennett and Licht (1972) with commercial reagents (Biodynamics-BMC, Indianapolis). Lactate content of tadpoles resting in the experimental tank was determined similarly by freezing them without a prior chase.

Sketches were made of the paths of both tadpole and turtle as each encounter occurred. The paths were converted to distances with a digitizing tablet and a microcomputer. Differences were tested for statistical significance with one-way analysis of variance (lactate data) or Mann- Whitney's U (other data).

RESULTS

GENERAL BEHAVIOR

Turtles swam about the experimental tank slowly and sporadically when not attempting to eat tadpoles. Attacks on tadpoles occurred in two stages: "approach" and "pursuit." A turtle's first response, termed approach, was to swim toward the tadpole at moderate speed with its neck extended. The distance between the turtle and the tadpole when an approach began was recorded. When the turtle was within approximately 10-15 cm, the tadpole usu- ally responded by swimming away rapidly. The turtle would respond by accelerating and attempting to overtake the tadpole.

The simultaneous acceleration of the turtle and the tadpole designated the start of the pursuit. The turtle would match the tadpole's speed and attempt to bite it (fig. 1). Either a tadpole would elude the turtle or it would be eaten. In the latter case, the turtle typically bit off a portion of the tadpole's tail and easily swallowed the hand- icapped tadpole. Soon afterward, turtles resumed swimming about the tank. A tadpole was considered to have escaped a turtle if the turtle returned to slow, sporadic swimming without the tadpole's being eaten or if the turtle attacked another tadpole. Slow swimming, attack, approach, pursuit, and escape were unambiguously identifiable as such. Likewise, the individual tadpole being attacked by a turtle could be identified readily.

FACTORS ELICITING ATTACKS BY TURTLES

Turtles readily attacked moving and motionless tadpoles. However, the object of a turtle's attack was more frequently a

260 B

195 5

% A /

130 D

65 C

0 II I 0 65 130 195 260

FIG. 1.-A typical pursuit of a tadpole (solid line) by a turtle (dashed line). The turtle was at A when

it responded to a tadpole surfacing to breathe air at B. It approached the tadpole during the next 3 s. The tadpole responded to the turtle's approach by swimming toward and then parallel to one wall of the experimental tank. The turtle pursued the tadpole, matching its speed to the speed of the tadpole. At C, the turtle snapped at the tadpole, and the tadpole reversed its direction of swimming abruptly and escaped. By the time the turtle had turned to pursue the tadpole, the tadpole had swum to D and was still. The turtle evidently had lost the tadpole and sub-

sequently pursued other tadpoles. The duration of the pursuit (from B to D) was 8 s; the total distance swum by the tadpole was 385 cm. The scale (in cm) is given alongside the figure.




moving tadpole than a still tadpole. Of 132 encounters in which tadpole behavior before the attack was noted, 72% were on moving tadpoles. Of these, 87 were swimming in the horizontal plane, five were swimming to the surface to breathe air, and four were drifting slowly at the surface.

Both still and moving tadpoles were attacked readily when tadpoles were within 30 cm of a turtle and in its line of sight (fig. 2). The larger number of attacks on moving tadpoles within 30 cm may indi- cate that moving tadpoles were conspicuous to turtles or only that tadpoles were more likely to be moving than still. At greater distances, however, tadpole movement per se was clearly associated with the likelihood of attack by a turtle. Only a single motionless tadpole was attacked from more than 30 cm (40 cm), whereas swimming and air-breathing tadpoles were attacked from up to 175 cm (fig. 2). In two instances when turtles' movements took them directly toward motionless tadpoles from 120 cm and 60 cm away, the turtle

did not respond until the tadpoles were within 30 cm.

Air breathing per se increased the likelihood of attack by a turtle, although this increase was small. For example, a turtle attacked an air-breathing tadpole 100 cm away and attacked two air-breathing tadpoles 50 cm away. Figure 2 suggests that these tadpoles would not have been attacked had they been motionless. Air breathing seemed no more conspicuous or provocative to the turtles than any other movement, but no less so. Air breathing, however, was far less frequently associated with predator attacks than were other movements. Of 96 encounters in which moving tadpoles were attacked, only 5% were on tadpoles swimming to breathe air.

FACTORS AFFECTING TADPOLE ESCAPE

Despite the larger size of the turtles and the absence of sheltered retreats in the experimental tank, the tadpoles were more often successful in eluding a turtle than

15

h 12 A. Still tadpoles

9

+l 3

0 20 40 60 80 100 120 140 160 180

21-

18 B. Moving tadpoles

3r 15

ol 9

EL4 6

0 20 40 60 80 100 120 140 160 180 Distance between turtle and tadpole (cm)

FIG. 2.-Effect of tadpole movement on the distance at which tadpoles were detected by turtles. Distances between tadpoles and turtles when the turtles began to approach the tadpoles are plotted for tadpoles that were motionless (A, no. = 36) or moving (B, no. = 96) at the time of detection.



526 M. E. FEDER

not. Of 171 encounters, 74% ended in escape.

Locomotor stamina appeared not to be an important determinant of the outcome of experimental predatory encounters. The duration of the pursuit (i.e., the time from a tadpole's response to attack until its escape or demise) was recorded in 129 encounters (fig. 3). The mean pursuit lasted 11.4 s (SD = 7.0 s); only one pursuit lasted more than 30 s, and fewer than 10% of the pursuits lasted more than 20 s. Thus predatory encounters seldom involved a prolonged pursuit. Moreover, pursuits of tadpoles that eventually escaped averaged 11.2 s (0.7 s SE)--slightly but not significantly less (P = .57) than pursuits of tadpoles that were caught (12.1 + 1.6 s).

The factors that influenced escape involved not stamina but, rather, the greater burst speed and greater maneuverability of tadpoles in comparison to turtles. Es- capes occurred in 111 encounters. The most common escape tactic (53 % of escapes) was a rapid alteration in the tadpole's heading as it swam (fig. 1). A tadpole would reverse course and swim rapidly in a new direction. The pursuing turtle would turn in the opposite direction (e.g., clockwise instead of counterclockwise), or turn more slowly, or collide with a wall. In any event, the result was often the turtle's losing sight of the tadpole or the tadpole's outdistancing a turtle on its new heading. In the latter case, sometimes a turtle would again overtake a tadpole, prompting yet another reverse by the tadpole. As many as five reverses occurred in a single encounter. Other escapes (41%) transpired because

36

32

28

24

20 o 1

12 8 F4

0 4 8 12 16 20 24 28 32 36 40 44 Duration of pursuit (s)

FIG. 3.-Duration of pursuits of tadpoles by turtles (no. = 129).

tadpoles swam ahead of turtles in a burst of speed and the turtles lost sight of the tadpoles. The distances between a turtle and a tadpole after such a burst of swimming typically were less than the distances at which turtles initially recognized tadpoles (previously summarized in fig. 2), but the turtles seemed unable to locate the escaping tadpoles. These turtles typically moved their heads as if scanning the water ahead and reduced their swimming speed. The remainder of escapes were due either to turtles' colliding with the standpipe (4%) or swimming after a tadpole other than the original target. In no case did a tadpole evade capture because it swam for a longer time than a turtle, with the turtle's becoming fatigued and falling behind.

Chance played an important role in determining the outcome of predatory encounters. The observers' notes record instances of tadpoles reversing course directly into a turtle's mouth or of one tadpole escaping by reversing near a second tadpole-which was then eaten by the turtle before it could respond. At other times, fleeing tadpoles stopped after swimming for only a few seconds and were then eaten, or tadpoles wandered in front of a turtle's head. Likewise, being recognized by a turtle was largely a matter of the direction of the turtle's head and whether a tadpole happened to be swimming or still at the critical instant.

To evaluate the relative importance of the various escape maneuvers and chance in determining the outcome of predatory encounters, measurements of locomotor behavior during the pursuit were com- pared in tadpoles that escaped or were eaten (table 1). The duration of the pursuit and the total distance swum by tadpoles were unrelated to the outcome of an encounter, further substantiating the negligible role of stamina in escape. However, the average speed of tadpoles during the pursuit (cal- culated as total distance swum divided by duration of a pursuit) and the number of reverses (expressed either as per pursuit or per second of swimming) differed significantly in escaped and eaten tadpoles. Cu- riously, the escaping tadpoles reversed less often than tadpoles that were eaten (table 1); apparently a single reverse was more effective in thwarting predation than mul-




tiple reverses. Thus, the outcome of predatory encounters was clearly determined to some extent by the behavior of the tadpoles.

LACTATE PRODUCTION

In trials in which an observer chased tadpoles with a fishnet, the duration of the pursuit (20.6 + 1.7 s; mean + SE), distance swum (547.8 + 35.1 cm), and tadpole velocity(28.0 + 2.2 cm s-')were all greater than in trials with turtles. Thus these trials yielded an overestimate of lactate production by tadpoles during encounters with turtles. Twelve such trials were performed, and the whole-body lactate concentrations of the tadpoles com- pared with lactate concentrations in six undisturbed animals. The mean lactate concentrations (+ SE) for resting and active animals, respectively, were 0.45 + 0.07 and 0.54 + 0.05 mg lactate

d g wet mass -'. These values do not differ significantly (P - .65). Moreover, the lactate concentrations in the active animals showed little correlation with either the duration of the pursuit (Spearman's r = 0.203), the distance swum (- 0.007), or the tadpole velocity (-0.145).

ROUTINE BEHAVIOR OF TADPOLES BEFORE AND

AFTER ATTACK

Tadpoles routinely moved from place to place on an irregular basis when no turtle was present (fig. 4). Because the movement of tadpoles contributes to their visibility by turtles, one might expect tadpoles to reduce routine swimming movements when turtles are present. Contrary to this ex- pectation, tadpoles increased both the number of movements and the total distance traveled after a 1-min simulated predator attack (fig. 4). Even with the small

sample size (total no. = 7), these differences were significant (P < .05).

DISCUSSION

AIR BREATHING AND LOCOMOTOR BEHAVIOR AS A

STIMULUS TO PREDATION

Many predators, including turtles (Granda and Fulbrook 1982), are espe- cially responsive to moving objects. Aquatic vertebrates at risk of predation may deal with increased conspicuousness caused by movement either by reducing movement or by becoming immobile when a predator is present (Wassersug 1972; Brodie, Johnson, and Dodd 1974; Kramer and Graham 1976; Caldwell, Thorp, and Jervey 1980; Baird 1983). If movement is necessary (e.g., breathing), populations of fish, tadpoles, and adult frogs may move synchronously, thereby minimizing the probability of any one individual's being eaten and potentially confusing a predator (Kramer and Graham 1976; Baird 1983; D. L. Kramer, personal communication).

Tadpoles of Rana berlandieri and some other species (Feder 1981a) curtail neither air breathing nor other movements but instead increase activity after a simulated predatory attack. This response is per- plexing in one respect, for many predators of tadpoles (salamander larvae, dragonfly larvae [Caldwell et al. 1980], adult frogs [M. E. Feder, unpublished observations], snakes [Wassersug and Sperry 1977; Ar- nold and Wassersug 1978; Drummond 1980], and at least 15 species of birds [R. J. Wassersug, personal communication]) are visually oriented. In a pond the size of the experimental tank, this increased activity may facilitate predation on tadpoles. In larger bodies of water, however, increased activity may lead a tadpole from the vicinity of a predator.

TABLE 1

DIFFERENCES IN BEHAVIOR OF TADPOLES THAT WERE EATEN

OR ESCAPED PREDATION

Measure of Performance Eaten Escape P

Pursuit duration (s) ........ 12.1+ 1.6 (23) 11.2 + .7 (106) .5684 Pursuit velocity (cms-') .... 23.4+ 1.8 (23) 32.5 + 1.3 (106) .0002 Pursuit distance (cm)....... 322.1 +39.7 (23) 316.4+ 14.0 (109) .8855 Reverses per second ....... .12 . .03 (22) .06+ .01 (104) .0183

NOTE.--Values are means + 1 SE. Numbers in sample are given in parentheses.



528 M. E. FEDER

Many amphibians, in fact, release warning substances when stressed that promote increased activity of conspecifics (Hedberg 1981). As both increased and decreased activity have been suggested as possible an- tipredator behaviors in lower vertebrates, further experiments are necessary to de- termine the circumstances (i.e., water tur- bidity, the visual range of predators, the number and distribution of refugia, predators, and prey) in which either behavior may be more effective, if either is.

Air-breathing behavior may increase predation on tadpoles in two ways. First,

by increasing the locomotor activity and conspicuousness of tadpoles, air breathing may prompt increased attacks by visually oriented predators that frequent the same microhabitats as tadpoles. Air breathing may increase this type of predation neg- ligibly if air breathing constitutes only a small fraction of overall movement, as it does in normoxic Rana tadpoles (Wasser- sug and Seibert 1975; Feder 1983; present study). Indeed, air breathing prompted less than 4% of the predatory attacks in the present study. However, in hypoxic water Rana tadpoles may breathe air every few

A. Before attack 300

o0 0 10 20 30 40 50 60

B. After attack U

1800- - 3600

o 1500 - - 3300

S1200 - - 3000

S900- 2700

S600- - 2400

r)

300- - 2100

0 8 1800 0 10 20 30 40 50 60

Time (min)

FIG. 4.-Routine movements by tadpoles before (A) and after (B) attack by a simulated predator. The cumulative distance moved during 1 h of observation is plotted for each tadpole with a different symbol. Each symbol represents a minute in which a tadpole moved. In B, the movements of the individual represented by the open square are plotted according to the left scale for the first 34 min and according to the right scale for the remaining time.




minutes and do little else and thereby may elicit numerous predatory attacks.

A second way in which air breathing may increase predation on tadpoles is by exposing tadpoles to predators that nor- mally frequent different microhabitats, such as fish dwelling higher in the water column or aerial predators. Many aerial predators (e.g., birds, snakes) lie in wait for fish or tadpoles specifically as they surface to breathe air (Wassersug and Sperry 1977; Kramer et al. 1983). Even modest rates of air breathing may be highly del- eterious in this circumstance. For example, Kramer et al. (1983) have shown that fish that breathe air regularly or remain near the surface are preyed upon more heavily by a heron than are fish that remain near the bottom. Increased dependence upon aquatic respiration, anaerobiosis (Feder 1983), and synchronous air breathing (Kramer and Graham 1976) may be es- pecially valuable in thwarting this second mode of predation.

DOES ENHANCING STAMINA OF TADPOLES THWART

PREDATIONd

The data strongly suggest that stamina had little bearing on the outcome of predatory encounters; hence air breathing, through its effect on stamina (Wassersug and Feder 1983), had little value as a predator deterrent in the laboratory setting of the present study. Predatory encounters were relatively brief (fig. 3). Their outcome was determined primarily by the speed and maneuverability of the prey and not by the relative stamina of the predator and the prey (table 1, figs. 1, 3-4). The low lactate concentrations in tadpoles after an encounter, while also consistent with a major dependence on aerobiosis during activity, probably results from dependence on non- glycolytic anaerobic pathways. Gatten, Caldwell, and Stockard (1983) reported a marked depletion of muscle phosphocrea- tine and only a nonsignificant (15%) increase in lactate in the tails of tadpoles undergoing 30 s of burst activity in the laboratory.

Although burst activity of tadpoles was ineffective in thwarting predation in 26% of the experimental encounters, this pro- portion may be far lower in natural habitats. The experimental tank contained

relatively clean water and few obstructions to vision. In natural habitats of tadpoles, the water is often murky. Vegetation and sediments may serve as refugia. Moreover, tadpoles may easily negotiate vegetation through which large predators cannot pass. Thus, sustained activity may seldom figure in individual predatory encounters, for relatively brief bursts of activity may be all that are needed to escape.

The relative unimportance of stamina in determining the outcome of a given predator-prey encounter may apply to the predator-prey relationships of many vertebrates other than tadpoles. Many analyses of predation on fleeing prey, both tadpoles of other species (Wassersug and Sperry 1977; Huey 1980) and other organisms in air and water (Howland 1974; Webb 1976, 1977; Elliott, Cowan, and Holling 1977; Kim- mel, Eaton, and Powell 1980; Huey and Hertz 1982) implicate burst performance rather than sustained activity as the major determinant of the success of a predator's attack. Contests of the relative staminas of predator and prey seem rare by comparison.

WHY DO TADPOLES BREATHE AIRd

If air breathing has little value in facil- itating escape in any single predatory encounter and in fact contributes to the risk of predation by enhancing conspicuousness, why do tadpoles breathe aird Of four possible answers, the first is least satisfac- tory, and the others deserve further attention.

a) Air-breathing behavior contributes significantly to overall oxygen uptake at all times.-Although aerial oxygen uptake in tadpoles accounts for 15%-20% of total oxygen consumption under routine conditions (Burggren, Feder, and Pinder 1983; Feder 1983), tadpoles are not obligate air breathers. If denied access to air, tadpoles of several species show no ill effects and maintain normal levels of oxygen consumption, even during activity (Feder 1981b, 1983).

b) Air-breathing behavior is an important response to aquatic hypoxia.--Air breathing in fact is crucial to tolerance of aquatic hypoxia. Tadpoles lose oxygen to hypoxic water through their gills and skin and compensate for this loss via increased



530 M. E. FEDER

aerial respiration (Feder 1981b, 1983). Many aquatic habitats similar to those fre- quented by tadpoles regularly become hypoxic (Kramer 1983), and two studies have specifically documented hypoxia in tadpole habitats (Crump 1981; Noland and Ultsch 1981). Some other tadpole habitats seem well aerated. However, tadpoles may encounter hypoxia even in normoxic water; the ventrally directed mouths of tadpoles may inspire mainly poorly oxygenated water in contact with bottom sediment and detritus. One problem with this explanation, however, is that tadpoles breathe air even in well-oxygenated water.

c) Tadpoles are under constant attack by predators; although any given encounter may be brief, the cumulative result is relatively constant activity.-This possibility receives some support from the data. In some cases, each experimental tadpole was attacked multiple times. Sometimes one tadpole would frighten others as it fled from a turtle, and the others startled still more tadpoles in a chain reaction. If tadpoles are moving in frequent bursts, air breathing might well be important in the overall metabolic support of activity. Air breathing may also speed recovery from fatigue (Feder and Olsen 1978) and thereby improve a tadpole's chance of escape from any subsequent predatory encounter. A difficulty with this explanation is the lack of field data. This explanation necessitates a relatively high density of predators and a high probability of frequent attacks on tadpoles. Both these conditions might con- ceivably be met in natural situations. Sal-

amander larvae and dragonfly larvae, just two of the many natural predators of tadpoles, may be as dense as eight per square meter and may outnumber tadpoles in a typical pond (Caldwell et al. 1980). Turtle biomass is also very high in many ponds (Iverson 1982). However, the greater structural diversity of natural habitats and the many opportunities for crypsis may al- ternatively offset the probability of multiple encounters with predators. Further observations of predation upon tadpoles in the field would be most welcome.

d) Air-breathing behavior is not adaptive, but its costs are negligible.-Air breathing in some premetamorphic amphibians might be a historical relict of an- cestral environments or an ontogenetic event that occurs before it is actually necessary. Although air breathing must have some costs (Kramer and McClure 1981; Kramer 1983; present study), the costs in both the energetic support of air breathing and the increased risk of predation might be negligible to a tadpole if its food is abun- dant, if conspicuous activity other than air breathing is frequent, and if many alternative prey items (including other tadpoles) are available to predators. Thus there may be little natural selection to eliminate "un-necessary" air-breathing behavior that is due to a historical or developmental ac- cident. These possibilities are seldom ex- amined in detail (Gould and Lewontin 1979). However, the present study suggests this alternative as a useful null hy- pothesis and point of departure for future work.

LITERATURE CITED

ARNOLD, S. J., AND R. J. WASSERSUG. 1978. Dif- ferential predation by garter snakes (Thamno- phis): social behavior as a possible defense. Ecology 59:1014-1022.

BAIRD, T. A. 1983. Influence of social and predatory stimuli on the air-breathing behavior of the Af- rican clawed frog, Xenopus laevis. Copeia 1983:411-420.

BENNETT, A. F. 1980. The metabolic foundations of vertebrate behavior. BioScience 30:452-456.

BENNETT, A. F., and P. LICHT. 1972. Anaerobic metabolism and activity in lizards. J. Comp. Physiol. 81:277-288.

BRETT, J. R. 1972. The metabolic demand for oxygen in fish, particularly salmonids, and a comparison with other vertebrates. Respiration Physiol. 14:151-170.

BRODIE, E. D., J. A. JOHNSON, and K. C. DODD. 1974. Immobility as a defensive behavior in salamanders. Herpetologica 30:79-85.

BURGGREN, W. W. 1982. "Air gulping" improves blood

oxygen transport during aquatic hypoxia in the

goldfish Carassius auratus. Physiol. Zool. 55:327- 334.

BURGGREN, W. W., M. E. FEDER, and A. W. PIN-

DER. 1983. Temperature and the balance between aerial and aquatic respiration in larvae of Rana berlandieri and Rana catesbeiana. Physiol. Zool. 56:263-273.

CALDWELL, J. P., J. H. THORP, and T. O. JERVEY.

1980. Predator-prey relationships among larval

dragonflies, salamanders, and frogs. Oecologia 46:285-289.

CRUMP, M. L. 1981. Variation in propagule size as




a function of environmental uncertainty for tree frogs. Amer. Natur. 117:724-737.

DEJOURS, P. 1981. Principles of comparative respiratory physiology. 2d ed. North-Holland, Amsterdam.

DRUMMOND, H. M. 1980. Aquatic foraging in some New World natricine snakes: generalists and spe- cialists and their behavioral evolution. Ph.D. diss. University of Tennessee, Knoxville.

ELLIOTT, J. P., I. M. COWAN, and C. S. HOLLING. 1977. Prey capture by the African lion. Can. J. Zool. 55:1811-1828.

FEDER, M. E. 1981a. Effect of body size, trophic state, time of day, and experimental stress on oxygen consumption of anuran larvae: an experimental assessment and evaluation of the literature. Comp. Biochem. Physiol. 70A:497-508. - . 1981b. Responses to acute aquatic hypoxia

in larvae of amphibians, Rana and Xenopus. Amer. Zool. 21:928.

S1983. Responses to acute aquatic hypoxia in larvae of the frog Rana berlandieri. J. Exp. Biol. 104:79-95.

FEDER, M. E., and L. E. OLSEN. 1978. Behavioral and physiological correlates of recovery from ex- haustion in the lungless salamander Batrachoseps attenuatus (Amphibia: Plethodontidae). J. Comp. Physiol. 128:101-107.

GATTEN, R. E., J. P CALDWELL, and M. E. STOCK- ARD. 1982. Anaerobic metabolism during intense swimming in anuran larvae. Forthcoming.

GOSNER, K. L. 1960. A simplified table for staging anuran embryos and larvae with notes on iden- tification. Herpetologica 16:183-190.

GOULD, S. J., and R. C. LEWONTIN. 1979. The span- drels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme. Proc. Roy. Soc. London 205B:581-598.

GRANDA, A. M., and J. E. FULBROOK. 1982. Spatial organization of retinal ganglion cells in turtle, Pseudemys. Color Res. Appl. 7:173-177.

HALLIDAY, T. R., and H. P. A. SWEATMAN. 1975. To breathe or not to breathe: the newt's problem. Anim. Behav. 24:551-561.

HEDBERG, T. G. 1981. A possible stress-warning marker in ambystomatid salamanders. J. Exp. Zool. 216:349-355.

HEYER, W. R., and M. H. MUEDEKING. 1976. Notes on tadpoles as prey for naiads and turtles. J. Washington Acad. Sci. 66:235-239.

HOWLAND, H. C. 1974. Optimal strategies for predator avoidance: the relative importance of speed and maneuverability. J. Theoret. Biol. 47:333- 350.

HUEY, R. B. 1980. Sprint velocity of tadpoles (Bufo boreas) through metamorphosis. Copeia 1980:537- 540.

HUEY, R. B., and P. E. HERTZ. 1982. Effects of body size and slope on sprint speed of a lizard (Stellio

(Agama) stellio). J. Exp. Biol. 97:401-409. IVERSON, J. B. 1982. Biomass in turtle populations:

a neglected subject. Oecologia 55:69-76. KIMMEL, C. B., R. C. EATON, and S. L. POWELL.

1980. Decreased fast-start performance of ze- brafish larvae lacking Mauthner neurons. J. Comp. Physiol. 140:343-350.

KRAMER, D. L. 1983. The evolutionary ecology of respiratory mode in fishes: an analysis based on the costs of breathing. Environmental Biol. Fishes (in press).

KRAMER, D. L., and J. G. GRAHAM. 1976. Syn- chronous air breathing, a social component of respiration in fish. Copeia 1976:689-697.

KRAMER, D. L., C. C. LINDSEY, G. E. E. MOODIE, and E. D. STEVENS. 1978. The fishes and the aquatic environment of the central Amazon basin, with particular reference to respiratory patterns. Can. J. Zool. 58:1984-1991.

KRAMER, D. L., and M. MCCLURE. 1981. The transit cost of aerial respiration in the catfish Corydoras aeneus (Callichthyidae). Physiol. Zool. 54:189- 194.

KRAMER, D. L., D. MANLEY, and R. BURGEOIS. 1983. The risk of respiration in fishes. Can. J. Zool. 61:653-665.

NOLAND, R., and G. R. ULTSCH. 1981. The roles of temperature and dissolved oxygen in microhabi- tat selection by the tadpoles of a frog (Rana pi- piens) and a toad (Bufo terrestris). Copeia 1981:645-652.

RANDALL, D. J., W. W BURGGREN, A. P. FARRELL, and M. S. HASWELL. 1981. The evolution of air breathing in vertebrates. Cambridge University Press, Cambridge.

WASSERSUG, R. J. 1972. On the comparative pal-

atability of some dry-season tadpoles from Costa Rica. Amer. Midland Natur. 86:101-109.

WASSERSUG, R. J., and M. E. FEDER. 1983. The effects of aquatic oxygen concentration, body size, and respiratory behaviors on the stamina of obligate aquatic (Bufo americanus) and facultative air-breathing (Xenopus laevis and Rana berlandieri) anuran larvae. J. Exp. Biol. (in press).

WASSERSUG, R. J., and E. A. SEIBERT. 1975. Be- havioral responses of amphibian larvae to variation in dissolved oxygen. Copeia 1975:87-103.

WASSERSUG, R. J., and D. SPERRY. 1977. The relation of locomotion to differential predation on Pseudacris triseriata (Anura: Hylidae). Ecology 58:830-839.

WEBB, P. W. 1976. The effect of size on the fast-start performance of rainbow trout Salmo gairdneri, and a consideration of piscivorous predator-prey interactions. J. Exp. Biol. 65:157-177.

. 1977. Effects of median-fin amputation on fast-start performance of rainbow trout (Salmo gairdneri). J. Exp. Biol. 68:123-135.



Documents

The Relation of Air Breathing and Locomotion to Predation on Tadpoles, Rana berlandieri, by Turtles