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Predator escape success in tailed versus tailless Scinella lateralis (Sauria: Scincidae)
SHORT C O M M U N I C A T I O N S logy of oystercatchers Haematopus ostralegus wintering on the Exe estuary, Devon. Ibis, 125, 155-171. Goss-Custard, J. D, Durell, S. E. A. le V. dit & Ens, B. J. 1982a. Individual differences in aggressiveness and food stealing among wintering oystercatchers, Haematopus ostralegus L. Anim. Behav., 30, 917-928. Goss-Custard, J. D., Durell, S. E. A. le V. dit, McGrorty, S. & Reading, C. J. 1982b. Use of mussel Mytilus edulis beds by oystercatchers Haematopus ostraIegus according to age and population size. J. Anim. EcoL, 51, 543-554. Heinrich, B. 1976. Foraging specialisations of individual bumblebees. Ecol. Monogr., 46, 105-128. Norton-Griffiths, M. 1967. Some ecological aspects of the feeding behaviour of the oystercatcher Haematopus ostralegus on the edible mussel Mytilus edulis, lbis, 109, 412-424. Norton-Griffiths, M. 1968. The feeding behaviour of the oystercatcher Haematopus ostralegus. Ph.D. thesis, University of Oxford.
(Received 2 September 1983; revised 25 October 1983; MS. number: sc-175). Predator Escape Success in Tailed Versus Tailless Scincella lateralis (Sauria: Scincidae) The selective agent of predation has produced a wide variety of behavioural .and morphological avoidance and/or escape tactics including autotomy, in which the mechanical release of body parts facilitates escape. Tail autotomy has evolved as a major predator escape tactic in 13 of the 20 or so lizard families (Etheridge 1967; Congdon et al. 1974; Johnson & Brodie 1974; Vitt et al. 1977), despite the fact that many species use their tails for energy storage (Derickson 1976; Dial & Fitzpatrick 1981) and/or locomotion (Urban 1965; Ballinger 1973; Pond 1978; Ballinger et at. 1979). Elsewhere we reported the effects of energy loss through tail autotomy on reproduction (Dial & Fitzpatrick 1981), and the physiological and functional bases of autotomized tail movement (Dial & Fitzpatrick 1983). Here, we report on the relation between tail presence and flight success from predators in a lizard (Scincella lateralis) that uses autotomy as a principal escape mechanism, but also relies heavily on its intact tail for locomotion (Dial 1981). We examined the effects of tail absence on flight success from predators by staging encounters between tailed (control) and tailless (experimental) S. lateralis and a principal predator, the snake Lampropeltis triangulum (Blanchard 1921). Adult lizards ( N = 62; X snoutvent length = 43.5 mm; )? tail length = 70.6 m m ; )? mass = 1.5 g), which we collected from Dallas and Harris counties, Texas in the spring of 1980, were divided randomly into contr61 and experimental groups. We induced autotomy in the latter, several days before the experiments, by gripping the tails with forceps at the most proximal caudal fracture plane (Etheridge 1967). There was negligible loss of blood after autotomy, and healing occurred rapidly. All lizards were in good health during the experiments. The snakes that we used were subadults (N = 3; )? SVL = 28.4 cm) and were obtained commercially. Each was fed one lizard per week until 3-4 days before the experiments. A n experimental trial consisted of choosing two tailed and two tailless lizards at random from a terrarium housing all of the lizards, placing them in a glass arena (76 • 45 • 50 cm) with a
301
mixed leaf litter substrate (1-2 cm), and introducing a snake 30 min later. In each trial the snake actively foraged and attempted to catch the lizards. Generally, a snake would move slowly through the leaf litter, moving its head laterally and examining the substrate with tongue flicks. When it detected a lizard, apparently by the lizard's movement, the snake would accelerate in short bursts towards the lizard. This usually caused the lizard to flee. A trial was terminated when a lizard was captured, at which time the remaining lizards and the snake were returned to holding terraria. Trials were conducted at 3-h intervals for 12 h per day. Room temperature was 29~ during all trials. We scored the encounters between snakes and tailed versus tailless lizards according to (i) flight success, (ii) escape success through autotomy, and (iii) which part of the anatomy was attacked by the snake. In a total of 42 attempted attacks on both tailed and tailless lizards, the snakes captured and ingested 20 lizards (47.6 %). All lizards (both tailed and tailless) that were captured and ingested were struck between the head and hind limbs. Snakes were 100% successful (12 attempts, 12 captures) in capturing tailless lizards (Table I). None of the tailless lizards that were attacked escaped after the attack. In contrast, snakes were successful in only 2 6 . 7 ~ (30 attempts, eight captures) of the attacks on tailed lizards (Table I). Fifty per cent (11 of 22) of the tailed lizards that escaped did so by fleeing with tails intact, and 50% escaped via tail autotomy. All autotomized tails were consumed by the snakes. Thus our data show that tailed lizards were considerably more successful in escaping predation than their tailless counterparts. Tails of S. lateralis represent a considerable portion of an individual's biomass ( X = 30 ~ , wet) and total length O? = 62 ~o). The presence of a tail in S. lateralis not only allows for escape through autotomy, but apparently the intact tail enhances flight success as well. However, an intact tail may simply misdirect the snake's attack to the tail and not aid in actual flight. We examined that possibility by staging encounters between tailed lizards and snakes in the arena lined with paper instead of leaf litter. The substrate paper was dark bown in colour, closely approximating the colour of S.lateralis. All (N = 12) of the lizards were captured with midbody strikes and were eaten. Lizards appeared to move more slowly on the paper substrate compared to leaf litter, whereas snake movement appeared to be unaffected by the paper substrate. Presumably, the smooth surface reduced the effectiveness of the tail in locomotion and neutralized the advantage tailed lizards have in flight over tailless ones. The results of our laboratory experiments suggest that the consequences of tail autotomy include reduced
Table I. Escape Success of Tailed Versus Tailless S. lateralis during Encounters with the Predatory Snake L. triangulum
Attempted captures Captures Escapes With tail autotomy With tail intact
Tailed
Tailless
30 8 22 11 11
12 12 0
The difference in escape success between tailed and tailless lizards was significant (Xa = 18.51, d f = 1, P < 0.001).
302
ANIMAL
BEHAVIOUR,
mechanical efficiency in locomotion during flight. Quantitative analysis of the escape success of tailed versus tailless lizard prey in natural encounters with predators must await further study. In addition, our study suggests that tail loss might affect other aspects of a lizard's behaviour. Snakes pursued all (tailed and tailless) lizards that were encountered. Although sample sizes of tailed and tailless lizards per test were equal (N = 2 and 2), snakes attempted more attacks on tailed than tailless lizards (30 versus 12, respectively), suggesting that tailed lizards were encountered more frequently than tailless ones. Are tailless lizards more restricted in their movements than tailed ones? Conceivably, tail loss might temporarily affect several behavioural aspects of a lizard's biology, including foraging behaviour (time spent foraging, area covered during foraging) and flight distance. Thus, tail autotomy might alter a lizard's position on the 'sit-and-wait-active-foraging' predatorymode continuum (see Tollestrup 1980). Future studies of both foraging behaviour and predator-prey relations of lizards should address the behavioural as well as the physiological (see Dial & Fitzpatrick 1981) consequences of tail autotomy. We thank H. Erie Rawlins, Jr. and Robert J. Kosinski for their assistance, and we gratefully acknowledge financial support to B.E.D. from the American Museum of Natural History (Theodore Roosevelt Memorial Fund), the American Society of Ichthyologists and Herpetologists (Gaige Fund) and Sigma Xi, and to L.C.F. from the Faculty Research Fund (NTSU). Funds for manuscript preparation were provided by the Department of Biology, Texas A & M University. BENJAMIN E. DIAL* LLOYD C. FITZPAaa~ICK'~
*Department of Biology, Texas A & M University, College Station, TX 77843, U.S.A. t Department of Biological Sciences, North Texas State University, Denton, TX 76203, U.S.A. References Ba!linger, R. E. 1973. Experimental evidence of the tail as a balancing organ in the lizard, Anolis carolinensis. Herpetologica, 29, 65-66. Ballinger, R. E., Neitfeldt, J. W. & Koupe, J. J. 1979. An experimental analysis of the role of the tail in attaining high running speed in Cnemidophorus sexlineatus (Reptilia: Squamata: Lacertilia). He~Tetologica, 35, 114-116 Blanehard, F. N. 1921. A revision of the kingsnakes: genus Lampropeltis. U.S. Nat. Mus. Bull., 114, 1-260. Congdon, J. D., Vitt, L. J. & King, W. W. 1974. Geckos: adaptive significance and energetics of tail autotomy. Science, N.Y., 184, 1379-1380. Derickson, W. K. 1976. Lipid storage and utilization in reptiles. Am. ZooL, 16, 711-723. Dial, B. E. 1981, Lizard tail autotomy: some aspects of its ecology and energetics. Ph.D. thesis, N o r t h Texas State University. Dial, B. E. & Fitzpatrick, L. C. 1981. The energetic costs of tail autotomy to reproduction in the lizard Coleonyx brevis (Sauria: Gekkonidae). Oecologia, 51, 310-317. Dial, B. E. & Fitzpatrick, L. C. 1983. Lizard tail autotomy: function and energetics of postautotomy tail movement in Scincella lateralis. Science, N. Y., 219, 391-393.
32,
1
Etheridge, R. 1967. Lizard caudal vertebrae. Copeia, 1967, 699-721. Johnson, J. A. & Brodie, E. D. 1974. Defensive behavinur of the western banded gecko, Coleonyx variegatus. Anim. Behav., 22, 684-687. Pond, C. M. 1978. The effect of tail loss on rapid running in Dipsosaurus dorsalis. Am. Zool., 18, 612. Tol!estrup, K. 1980. Sit-and-wait predators vs. active foragers: do they exist ? Am. ZooL, 20, 809. Urban, E. K. 1965. Quantitative study of locomotion in teiid lizards. Anita. Behav., 13, 513-529. Vitt, L. J., Congdon, J. D. & Dickson, N. A. 1977. Adaptive strategies and energeties of tail autotomy in lizards. Ecology, 58, 326-337.
(Received 25 July 1983 ; revised 4 October 1983 ; MS. number: AS-194) A Payoff Asymmetry in Resident-Resident Disputes between Shrews In species which defend territories, residents usually defeat intruders in disputes over ownership (e.g. Bamard & Brown 1982; Krebs 1982). There are several reasons why residents should be at an advantage and these have been discussed at length by, e.g. Maynard Smith & Parker (1976). In an earlier study of the resident advantage in common shrews (Sorex araneus), Bamard & Brown (1982) showed that, although prior residence itself conferred an advantage (and was therefore an uncorrelated asymmetry in Maynard Smith & Parker's terminology), the degree of advantage depended on the relative competitive ability of resident and intruder (RHP asymmetry) and the availability of food experienced by the resident in the disputed area (payoff asymmetx'y). Residents did better against weaker intruders and when there was less food available. A n interesting question not considered by Barnard & Brown (1982), however, was h o w an asymmetry in food availability would influence the outcome of disputes when both contestants were resident in the disputed area and there was no resident/intruder uncorrelated asymmetry. F r o m the results of Barnard & Brown's study, we would predict that the resident experiencing the lower food density should tend to win most disputes. We tested this by allowing two common shrews to reside on a foraging grid at different times and experience different food densities during their periods of residence. The experiment was carried out during November and December 1982. Wild-caught adult common shrews which had been kept in captivity for several weeks were introduced in pairs to a grid apparatus. The apparatus consisted of two identical 150 • 60 cm wooden grids with 1-cm-diameter wells drilled to a depth of 1 cm every 5 cm. Each grid was surrounded by Perspex wall supporting a Perspex roof and had a 6 0 • 2 1 5 'home' tank containing peat, nest material and water attached to either end. Full details of the grid apparatus are given by Barnard & Brown (1982). A n important addition used here, however, was a perforated Perspex barrier running diagonally across each grid. During tests, when both animals of a pair were on the grid together (see below), the barriers allowed visual and olfactory contact but prevented physical contact and therefore the possibility of injury. Twelve shrews were arbitrarily divided (see Barnard & Brown 1982) into 6 pairs. A pair was allocated to grid 1 and a pair to grid 2 with one animal being introduced to each home tank. Except overnight, food (fly pupae) was available only on the grids. Pairs were allowed to settle
(Received 2 September 1983; revised 25 October 1983; MS. number: sc-175). Predator Escape Success in Tailed Versus Tailless Scincella lateralis (Sauria: Scincidae) The selective agent of predation has produced a wide variety of behavioural .and morphological avoidance and/or escape tactics including autotomy, in which the mechanical release of body parts facilitates escape. Tail autotomy has evolved as a major predator escape tactic in 13 of the 20 or so lizard families (Etheridge 1967; Congdon et al. 1974; Johnson & Brodie 1974; Vitt et al. 1977), despite the fact that many species use their tails for energy storage (Derickson 1976; Dial & Fitzpatrick 1981) and/or locomotion (Urban 1965; Ballinger 1973; Pond 1978; Ballinger et at. 1979). Elsewhere we reported the effects of energy loss through tail autotomy on reproduction (Dial & Fitzpatrick 1981), and the physiological and functional bases of autotomized tail movement (Dial & Fitzpatrick 1983). Here, we report on the relation between tail presence and flight success from predators in a lizard (Scincella lateralis) that uses autotomy as a principal escape mechanism, but also relies heavily on its intact tail for locomotion (Dial 1981). We examined the effects of tail absence on flight success from predators by staging encounters between tailed (control) and tailless (experimental) S. lateralis and a principal predator, the snake Lampropeltis triangulum (Blanchard 1921). Adult lizards ( N = 62; X snoutvent length = 43.5 mm; )? tail length = 70.6 m m ; )? mass = 1.5 g), which we collected from Dallas and Harris counties, Texas in the spring of 1980, were divided randomly into contr61 and experimental groups. We induced autotomy in the latter, several days before the experiments, by gripping the tails with forceps at the most proximal caudal fracture plane (Etheridge 1967). There was negligible loss of blood after autotomy, and healing occurred rapidly. All lizards were in good health during the experiments. The snakes that we used were subadults (N = 3; )? SVL = 28.4 cm) and were obtained commercially. Each was fed one lizard per week until 3-4 days before the experiments. A n experimental trial consisted of choosing two tailed and two tailless lizards at random from a terrarium housing all of the lizards, placing them in a glass arena (76 • 45 • 50 cm) with a
301
mixed leaf litter substrate (1-2 cm), and introducing a snake 30 min later. In each trial the snake actively foraged and attempted to catch the lizards. Generally, a snake would move slowly through the leaf litter, moving its head laterally and examining the substrate with tongue flicks. When it detected a lizard, apparently by the lizard's movement, the snake would accelerate in short bursts towards the lizard. This usually caused the lizard to flee. A trial was terminated when a lizard was captured, at which time the remaining lizards and the snake were returned to holding terraria. Trials were conducted at 3-h intervals for 12 h per day. Room temperature was 29~ during all trials. We scored the encounters between snakes and tailed versus tailless lizards according to (i) flight success, (ii) escape success through autotomy, and (iii) which part of the anatomy was attacked by the snake. In a total of 42 attempted attacks on both tailed and tailless lizards, the snakes captured and ingested 20 lizards (47.6 %). All lizards (both tailed and tailless) that were captured and ingested were struck between the head and hind limbs. Snakes were 100% successful (12 attempts, 12 captures) in capturing tailless lizards (Table I). None of the tailless lizards that were attacked escaped after the attack. In contrast, snakes were successful in only 2 6 . 7 ~ (30 attempts, eight captures) of the attacks on tailed lizards (Table I). Fifty per cent (11 of 22) of the tailed lizards that escaped did so by fleeing with tails intact, and 50% escaped via tail autotomy. All autotomized tails were consumed by the snakes. Thus our data show that tailed lizards were considerably more successful in escaping predation than their tailless counterparts. Tails of S. lateralis represent a considerable portion of an individual's biomass ( X = 30 ~ , wet) and total length O? = 62 ~o). The presence of a tail in S. lateralis not only allows for escape through autotomy, but apparently the intact tail enhances flight success as well. However, an intact tail may simply misdirect the snake's attack to the tail and not aid in actual flight. We examined that possibility by staging encounters between tailed lizards and snakes in the arena lined with paper instead of leaf litter. The substrate paper was dark bown in colour, closely approximating the colour of S.lateralis. All (N = 12) of the lizards were captured with midbody strikes and were eaten. Lizards appeared to move more slowly on the paper substrate compared to leaf litter, whereas snake movement appeared to be unaffected by the paper substrate. Presumably, the smooth surface reduced the effectiveness of the tail in locomotion and neutralized the advantage tailed lizards have in flight over tailless ones. The results of our laboratory experiments suggest that the consequences of tail autotomy include reduced
Table I. Escape Success of Tailed Versus Tailless S. lateralis during Encounters with the Predatory Snake L. triangulum
Attempted captures Captures Escapes With tail autotomy With tail intact
Tailed
Tailless
30 8 22 11 11
12 12 0
The difference in escape success between tailed and tailless lizards was significant (Xa = 18.51, d f = 1, P < 0.001).
302
ANIMAL
BEHAVIOUR,
mechanical efficiency in locomotion during flight. Quantitative analysis of the escape success of tailed versus tailless lizard prey in natural encounters with predators must await further study. In addition, our study suggests that tail loss might affect other aspects of a lizard's behaviour. Snakes pursued all (tailed and tailless) lizards that were encountered. Although sample sizes of tailed and tailless lizards per test were equal (N = 2 and 2), snakes attempted more attacks on tailed than tailless lizards (30 versus 12, respectively), suggesting that tailed lizards were encountered more frequently than tailless ones. Are tailless lizards more restricted in their movements than tailed ones? Conceivably, tail loss might temporarily affect several behavioural aspects of a lizard's biology, including foraging behaviour (time spent foraging, area covered during foraging) and flight distance. Thus, tail autotomy might alter a lizard's position on the 'sit-and-wait-active-foraging' predatorymode continuum (see Tollestrup 1980). Future studies of both foraging behaviour and predator-prey relations of lizards should address the behavioural as well as the physiological (see Dial & Fitzpatrick 1981) consequences of tail autotomy. We thank H. Erie Rawlins, Jr. and Robert J. Kosinski for their assistance, and we gratefully acknowledge financial support to B.E.D. from the American Museum of Natural History (Theodore Roosevelt Memorial Fund), the American Society of Ichthyologists and Herpetologists (Gaige Fund) and Sigma Xi, and to L.C.F. from the Faculty Research Fund (NTSU). Funds for manuscript preparation were provided by the Department of Biology, Texas A & M University. BENJAMIN E. DIAL* LLOYD C. FITZPAaa~ICK'~
*Department of Biology, Texas A & M University, College Station, TX 77843, U.S.A. t Department of Biological Sciences, North Texas State University, Denton, TX 76203, U.S.A. References Ba!linger, R. E. 1973. Experimental evidence of the tail as a balancing organ in the lizard, Anolis carolinensis. Herpetologica, 29, 65-66. Ballinger, R. E., Neitfeldt, J. W. & Koupe, J. J. 1979. An experimental analysis of the role of the tail in attaining high running speed in Cnemidophorus sexlineatus (Reptilia: Squamata: Lacertilia). He~Tetologica, 35, 114-116 Blanehard, F. N. 1921. A revision of the kingsnakes: genus Lampropeltis. U.S. Nat. Mus. Bull., 114, 1-260. Congdon, J. D., Vitt, L. J. & King, W. W. 1974. Geckos: adaptive significance and energetics of tail autotomy. Science, N.Y., 184, 1379-1380. Derickson, W. K. 1976. Lipid storage and utilization in reptiles. Am. ZooL, 16, 711-723. Dial, B. E. 1981, Lizard tail autotomy: some aspects of its ecology and energetics. Ph.D. thesis, N o r t h Texas State University. Dial, B. E. & Fitzpatrick, L. C. 1981. The energetic costs of tail autotomy to reproduction in the lizard Coleonyx brevis (Sauria: Gekkonidae). Oecologia, 51, 310-317. Dial, B. E. & Fitzpatrick, L. C. 1983. Lizard tail autotomy: function and energetics of postautotomy tail movement in Scincella lateralis. Science, N. Y., 219, 391-393.
32,
1
Etheridge, R. 1967. Lizard caudal vertebrae. Copeia, 1967, 699-721. Johnson, J. A. & Brodie, E. D. 1974. Defensive behavinur of the western banded gecko, Coleonyx variegatus. Anim. Behav., 22, 684-687. Pond, C. M. 1978. The effect of tail loss on rapid running in Dipsosaurus dorsalis. Am. Zool., 18, 612. Tol!estrup, K. 1980. Sit-and-wait predators vs. active foragers: do they exist ? Am. ZooL, 20, 809. Urban, E. K. 1965. Quantitative study of locomotion in teiid lizards. Anita. Behav., 13, 513-529. Vitt, L. J., Congdon, J. D. & Dickson, N. A. 1977. Adaptive strategies and energeties of tail autotomy in lizards. Ecology, 58, 326-337.
(Received 25 July 1983 ; revised 4 October 1983 ; MS. number: AS-194) A Payoff Asymmetry in Resident-Resident Disputes between Shrews In species which defend territories, residents usually defeat intruders in disputes over ownership (e.g. Bamard & Brown 1982; Krebs 1982). There are several reasons why residents should be at an advantage and these have been discussed at length by, e.g. Maynard Smith & Parker (1976). In an earlier study of the resident advantage in common shrews (Sorex araneus), Bamard & Brown (1982) showed that, although prior residence itself conferred an advantage (and was therefore an uncorrelated asymmetry in Maynard Smith & Parker's terminology), the degree of advantage depended on the relative competitive ability of resident and intruder (RHP asymmetry) and the availability of food experienced by the resident in the disputed area (payoff asymmetx'y). Residents did better against weaker intruders and when there was less food available. A n interesting question not considered by Barnard & Brown (1982), however, was h o w an asymmetry in food availability would influence the outcome of disputes when both contestants were resident in the disputed area and there was no resident/intruder uncorrelated asymmetry. F r o m the results of Barnard & Brown's study, we would predict that the resident experiencing the lower food density should tend to win most disputes. We tested this by allowing two common shrews to reside on a foraging grid at different times and experience different food densities during their periods of residence. The experiment was carried out during November and December 1982. Wild-caught adult common shrews which had been kept in captivity for several weeks were introduced in pairs to a grid apparatus. The apparatus consisted of two identical 150 • 60 cm wooden grids with 1-cm-diameter wells drilled to a depth of 1 cm every 5 cm. Each grid was surrounded by Perspex wall supporting a Perspex roof and had a 6 0 • 2 1 5 'home' tank containing peat, nest material and water attached to either end. Full details of the grid apparatus are given by Barnard & Brown (1982). A n important addition used here, however, was a perforated Perspex barrier running diagonally across each grid. During tests, when both animals of a pair were on the grid together (see below), the barriers allowed visual and olfactory contact but prevented physical contact and therefore the possibility of injury. Twelve shrews were arbitrarily divided (see Barnard & Brown 1982) into 6 pairs. A pair was allocated to grid 1 and a pair to grid 2 with one animal being introduced to each home tank. Except overnight, food (fly pupae) was available only on the grids. Pairs were allowed to settle