Behavioral Ecology Vol. 14 No. 2: 288-293
© 2003 International Society for Behavioral Ecology
Effects of risk, cost, and their interaction on optimal escape by nonrefuging Bonaire whiptail lizards, Cnemidophorus murinus
a Department of Biology, Indiana University-Purdue University at Fort Wayne, Fort Wayne, IN 46805, USA b Departamento de Biologia Animal, Universidad de Salamanca, 37071 Salamanca, Spain c Oklahoma City–County Health Department, 921 NE 23rd Street, Oklahoma City, OK 73105, USA d Department of Biology, University of Central Oklahoma, 100 N. University Drive, Edmond, OK 73034, USA e Sam Noble Oklahoma Museum of Natural History and Department of Zoology, University of Oklahoma, 2401 Chautauqua Avenue, Norman, OK 73072, USA
Address correspondence to W.E. Cooper. E-mail: cooperw{at}ipfw.edu.
Received 15 February 2002; revised 26 June 2002; accepted 22 August 2002.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Optimal escape theory seeks to explain variation in the distance to an approaching predator at which the prey initiates escape (flight initiation distance). Flight initiation distance increases when predators pose a greater threat and decreases when escape costs increase. Although optimal escape theory has been highly successful, its predictions have been tested primarily for species that escape to discrete refuges, and most studies have focused on single risk or cost factors. We present data from two experiments in which two risks or a risk and a cost varied in Bonaire whiptail lizards (Cnemidophorus murinus) that escaped without entering refuges. Our data verify several predictions about optimal escape for nonrefuging lizard prey. Two risk factors, speed and directness of approach by the predator, interacted. Directly approached lizards had greater flight initiation distances than did indirectly approached lizards when approached rapidly, but shorter flight initiation distances when approached slowly. Flight initiation distance was shorter in the presence of food and during slow versus rapid approaches, but contrary to expectation, food presence and approach speed did not interact. This would be explained if cost curves are nonlinear or if they are parallel rather than intersecting when the predator reaches the prey. More empirical work is needed to determine which risk and cost factors act additively and which act synergistically. The absence of interaction between the risk and cost factors suggests that cost curves were nonlinear.
Key words: antipredatory behavior, behavior, escape theory, refuge, Squamata.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Optimal escape theory (Ydenberg and Dill, 1986
) predicts that a prey should begin to escape from an approaching predator when the predator reaches a point at which the risk of predation equals the cost of escape. This distance from the predator at which prey are predicted to initiate flight is the optimal flight initiation distance. Optimal escape theory has been strongly supported by experimental tests of the effects of numerous risk and cost factors in a wide range of prey taxa (see below). Effects of simultaneous variation in more than one risk factor or in a risk factor and a cost factor have not been considered theoretically and have received very little empirical attention. This is surprising because prey are typically faced with multiple risks and costs that operate simultaneously. For example, prey should be able to respond to the dangerousness of the predator, its speed, the distance from and security of a refuge, the cost of giving up feeding opportunities, and other risks and costs that may affect a single encounter with a predator. Another aspect of optimal escape theory that has not has been widely tested is its applicability to nonmammalian prey that flee in the open rather than enter a refuge.
Flight initiation distance increases with magnitude of risk for several risk factors, including dangerousness of the predator (McLean and Godin, 1989; Walther, 1969); predator approach speed (Cooper, 1997c), directness of the predator's approach (Bulova, 1994; Burger and Gochfeld, 1981, 1990; Cooper, 1997c), direction of predator's approach relative to the refuge (Cooper, 1997a; Kramer and Bonenfant, 1997), distance to nearest refuge (Bulova, 1994; Bonenfant and Kramer, 1996; Cooper, 1997b; Dill, 1990), availability of cover (Grant and Noakes, 1987; LaGory, 1987), persistence by the predator (Cooper, 1997b), changes in a predator's path to a direct approach (Cooper, 1997b, 1998a), and lowered body temperature that results in lower escape speed in ectotherms (Rand, 1964; Smith, 1997).
As predicted by optimal escape theory, increases in escape costs are accompanied by decreases in flight initiation distance. Energetic expenditure and increased likelihood of injury during escape have the potential to be substantial, but are likely relatively small for prey that flee short distances to refuges. Loss of opportunities to forage and engage in fitness-enhancing social behavior while in refuge are major costs of hiding that affect escape decisions. Prey permit closer approach by predators when escape requires them to forego a feeding opportunity (Cooper, 2000) or opportunities to court or fight with rivals (Cooper, 2000). Ectothermic prey may be reluctant to enter cool refuges where decrease in body temperature may be costly owing to loss of social or foraging opportunities, whereas basking to reach a body temperature allows efficient locomotion on emerging from refuge, resulting in a shorter flight initiation distance (Cooper, 2000; Martín and Lopéz, 1999b).
Theoretically, multiple risks might have additive or interactive effects, as might multiple costs. Risks and costs might have additive or interactive effects with each other. However, little is known about such relationships. Optimal escape theory does not specify whether the joint risk curve for two simultaneous risk factors should be determined additively or interactively. Thus, we made no prediction regarding interaction between two risk factors. Between simultaneously operating risk and cost factors, optimal escape theory predicts interaction if risk has a curvilinear relationship and cost a linear relationship with distance between predator and prey, as in Ydenberg and Dill's (1986) model. In Figure 1, two curvilinear risk curves and two linear cost curves have four intersections. An optimal flight initiation distance is specified by each of the four intersections. The difference in optimal flight initiation distances between the two cost curves is greater for the upper risk curve in Figure 1 than for the lower one, implying interaction between risk and cost. Although costs were linear in Ydenberg and Dill's (1986) graphical model, their shapes have not been determined empirically for any species.
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Optimal escape theory has been tested primarily for prey that flee to distinct refuges, yet many prey escape by fleeing long distances without entering refuges or by fleeing to nonspecific refuges. Prey may use refuges facultatively, presumably depending on availability of safe refuges, relative speeds of prey and predator, and relative costs of entering refuges and remaining exposed. Some lizards flee in the open. Others that do not enter obvious refuges may flee over rocky terrain or through plants or other objects that may impede the progress of predators. These may be, in effect, using less secure refuges. Optimality considerations apply to time spent in refuge and to flight initiation distance (Dill and Fraser, 1997
; Martín and Lopéz, 1999a,b; Sih, 1992). From an optimality perspective, distance from refuge is merely one of several potential risk factors that may affect escape decisions by prey that use distinct refuges. This factor does not apply to nonrefuging prey, but other risk factors remain effective. Ydenberg and Dill (1986) cited several studies showing that escape by nonrefuging ungulates conforms to predictions of optimal escape theory.
Our goals in the present study were to examine relationships between two risk factors and between a risk factor and a cost factor and to test the predictions of optimal escape theory for nonmammalian prey that rely on speed to escape without entering refuge. Lizards are excellent subjects for field studies of optimal escape theory because many of them reliably flee from approaching biologists and are abundant enough to facilitate data collection. Consequently, more is known about factors affecting escape decisions in relation to optimal escape theory for lizards than for any other animal. Several risk factors affect flight initiation distance by lizards. Flight initiation distance of lizards decreases when they are closer to refuge (Bulova, 1994; Cooper, 1997a), when more cover is available (Martín and López, 1995), when the predator approaches more slowly and less directly (Bulova, 1994; Burger and Gochfeld, 1990; Cooper, 1997b), and when the lizards can flee to a refuge directly away form the predator's path (Cooper, 1997a). Because the running speed of lizards decreases at low body temperatures, placing them at greater risk at a fixed distance from refuge, the fact that flight initiation distance increases as body temperature decreases (Rand, 1964; Smith, 1997) is consistent with escape theory. Flight initiation distance also increases when predators are persistent (approach more than once) or change path toward the prey and when lizards are in open locations where they are conspicuous (Cooper, 1997a,c, 1998a,b). Less is known about effects of costs of escape in lizards, but the flight initiation distance is shorter when food is present, when males are guarding or courting females, and when rival males are present (Cooper, 1999; Martín and Lopéz, 1999a).
We studied escape behavior by Bonaire whiptail lizards, Cnemidophorus murinus, teiid omnivores that forage actively for prey and plant food (Dearing and Schall, 1992) and, in many areas, do not enter refuges, but escape on the surface in the open or through a varied terrain containing obstructive rocks and plants. We tested responses by the lizards to two simultaneous risk factors, predator approach speed and directness of approach, and to simultaneous operating risk (approach speed) and cost (presence of food) factors. The difference in optimal flight initiation distance between the food and no food treatments should be greater for rapid approach than for slow approach by the predator if risk curves are curvilinear and cost curves linear.
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METHODS |
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Adult C. murinus were observed in semiarid areas on Bonaire Island (Netherlands Antilles), where this species is endemic, during 1–7 March 2001 on warm sunny days when the lizards were fully active. In the experiment on effects of speed and directness of approach on escape, lizards were observed at a site east of and inland from Boka Onima, near the north coast where human beings were infrequently present. In this area, the lizards did not flee to discrete refuges and stopped in the open. However, at Boka Onima, where we collected similar data not presented here, the lizards frequently used holes in the ground often associated with rocks as refuges. In the experiment on effects of speed of approach and presence of food on flight initiation distance, the lizards were observed in open areas at several sites within the Washington Slagbaai National Park, where they were habituated to human presence. The habitat was open in these sites, lacking dense vegetation that might serve as refuges.
In both experiments, biologists served as simulated predators. Using human beings as predators has the advantages of allowing rapid data collection and of not requiring maintenance and use of experimental predators that may not behave as desired or of operating models in the field under variable, often adverse conditions. It has two disadvantages. One is that because human beings are not frequent predators of many lizard species, it is questionable whether lizards react to approaching experimenters as if they are predators. Field workers with lizards know that many species are wary and difficult to capture, including typical species in the genus Cnemidophorus. Lizards specialists have long noted that lizards routinely flee when approached by people, and the specialists have used themselves as simulated predators in numerous studies to test various hypotheses (see Bulova, 1994; Burger and Gochfeld, 1990; Dial, 1986; Heatwole, 1968; Rand, 1964). Another strong indication that lizards treat approaching biologists as predators is that the behavior of lizards conforms to predictions of optimal escape theory for effects of many variables on flight initiation distance (see Cooper, 1997a,b,c, 1998a), including tradeoffs between risk of predation and costs of escape (Cooper, 1999, 2000). The other disadvantage is potential bias owing to unintentional differences in approach among treatments by investigators, especially because the same individual approached and recorded data. We attempted to minimize this possibility by using standardized walking speeds and movement style during approaches.
The primary response variable in both experiments was flight initiation distance, a different term for the same variable used in other studies. In the seminal paper on optimal escape theory (Ydenberg and Dill, 1986), the flight initiation distance was called flight distance. This term should be avoided because it can be confused with the distance fled. Approach distance, another synonym of flight initiation distance (see Cooper, 1999, 2000), is less cumbersome but can be confusing because the predator approaches, whereas the prey decides when to flee.
Experiment 1 had a 2 x 3 factorial design to test the effects of speed of approach and directness of approach on flight initiation distance. The factorial design is useful because it permits assessment of the effects of both factors and of any interaction between them. Previous experiments testing predictions of optimal escape theory have focused on single factors affecting risk of predation or cost of escape. The two levels of predator approach speed were fast (139 ± 6 m/min, expressed as mean ± 1 SE, n = 6) and slow (46 ± 1 m/min). Directness of approach was measured as the closest possible distance between the lizard along the linear path being walked by the approaching investigator. This distance was 0 m for direct approaches and 5 or 10 m for indirect approaches (approaches bypassing the lizards at the stated minimum distances). In each trial, we recorded air temperature at 1 m above ground, whether the lizard fled or not, and flight initiation distance if it fled.
Experiment 2 examined the effects of variation in a risk factor, predator approach speed, and a cost of escape, leaving food that could not be carried away in order to escape. In the 2 x 2 factorial design, there were two levels of approach speed, as in experiment 1, and two levels of food presence. The food presented was ripe pear, which the lizards eat readily in the field and can be used effectively to bait live traps for C. murinus. To prepare for a trial, an investigator placed a chunk of pear large enough to prevent the lizard from running away with it or a rock of similar size on the ground where a lizard could see it. The investigator then withdrew to let the lizard approach. The rock served as a control for response to a nonfood object placed in the habitat. When the lizard reached and examined the pear or rock, an investigator approached it directly at one of the two speeds and recorded whether or not it fled and, if it fled, the flight initiation distance. The color morph of each lizard was recorded as blue or brown to allow examination of possible differences in boldness.
Lizards were located visually by walking slowly through the habitat in most cases, but at two sites in the Slagbaai National Park, the lizards were so abundant that a new individual sometimes was detected immediately when investigators finished the previous trial. Because independent groups designs were used in experiments, we walked through a given area only once during each experiment to ensure that each lizard was tested only once. No data from the Boka Onima site, where lizards used burrows under rocks as refuges, or from Boka Kokolishi, where they often fled beneath dense bushes, were included.
Data on approach speed were analyzed by using factorial ANOVA with all factors and levels being independent groups (Zar, 1996). Before conducting the tests, the assumption of homogeneity of variance was examined by using Levene's tests (Statistica 5.5, 1999). When significant heterogeneity of variance was detected, it was eliminated by appropriate transformations of the raw data before analysis. Differences among treatments in frequency of fleeing were examined by using chi-square tests. Significance tests were two-tailed, with 
= 0.05. Data are presented in the text as mean ± 1.0 SE.
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RESULTS |
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Experiment 1: approach speed and directness
Air temperatures during data collection were 32.6 ± 1.1°C (n = 150). Temperature did not differ significantly among experimental conditions, although the difference in temperature approached significance for directness of approach (speed: F1,144 = 0.7, p =.40; directness of approach: F2,144 = 3.0, p =.054; speed x directness: F2,144 = 0.4, p =.68). Temperature did not differ between lizards that fled and those that did not flee (F1,94 = 0.007, p >.10).
Numbers of individuals that fled when approached varied greatly among treatments (Table 1). The number that fled was strongly affected by directness of approach (
22 = 57.4, p <<.001), with all individuals fleeing on being approached directly, slightly over half fleeing when approached indirectly with a 5-m-minimum bypass distance (18 of 32), and only two of 31 when approached indirectly with a 10-m-minimum bypass distance. A slightly higher proportion of individuals fled when approached rapidly (29 of 48) than slowly (22 of 48), but the effect of speed of approach on numbers of individuals that fled was not significant (21 = 2.0, p >.10). The overall effect of approach speed was not significant because speed had no effect for direct approaches and 10-m bypasses. However, among lizards approached with a 5-m bypass distance, significantly more lizards fled when approached rapidly than slowly (21 = 4.67, p <.03).
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Because only two lizards fled at the 10-m bypass distance, analysis of the joint effect of approach speed and directness of approach was restricted to data on direct approaches and 5-m bypass for which lizards actually fled. The only effects of adding the data for lizards that did not flee would be to decrease the variances and lower the means slightly for both groups of lizards that were bypassed.
Among lizards that fled, the flight initiation distance was greater when lizards were approached rapidly than slowly. The effect of directness for these lizards was unclear because for lizards approached slowly, flight initiation distance was greater for bypassed than for directly approached lizards, whereas for lizards approached rapidly, the flight initiation distance was less for bypassed than for directly approached individuals (Figure 2). For the logarithmically transformed data, approach speed significantly affected flight initiation distance (F1,45 = 33.5, p = 1 x 10–6). For lizards that fled, approach distance was 3.8 ± 0.3 (range, 2.0–8.0; n = 21) for slow approaches and 7.3 ± 0.5 (range, 4.7–14.5; n = 29) for fast approaches. Flight initiation distance did not differ significantly with directness of approach (F1,45 = 2.8, p =.10) and was only slightly greater for 5-m bypasses (6.0 ± 0.4; range, 5.0–11.0; n = 18) than for direct approaches (5.5 ± 0.5; range, 2.0–14.5, n = 31). The single lizard that fled when approached on a 10-m bypass had a flight initiation distance of 13.5 m. The interaction between speed and directness of approach was significant (F1,45 = 14.2, p < 4.7 x 10–4).
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Experiment 2: approach speed and presence of food
All lizards fled when approached, and the lizards clearly responded differentially to approach speed and presence of food (Figure 3). Color morph had no effect on flight initiation distance (F1,75 = 0.1, p >.10) and did not interact significantly with the other factors (color x speed: F1,75 = 0.01, p >.10; color x food presence: F1,75 = 2.3, p >.10; color x speed x food: F1,75 = 0.1, p >.10 ).
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In the 2 x 2 analysis for effects of approach speed and presence of food using the transformed data, rapid approach elicited escape at a significantly greater flight initiation distance than did slow approach (F1,79 = 8.1, p <.00056). The flight initiation distance was significantly shorter in the presence of food than in its absence (F1,79 = 44.29, p < 1.0 x 10–6). The interaction between approach speed and presence of food was not significant (F1,79 = 1.3, p >.25).
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DISCUSSION |
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Risks, costs, and their interaction
The significant interaction between speed and directness of approach suggests that the level of one risk factor can affect responses to the level of another, so that the overall assessed risk is not determined additively by the two risks. This finding is limited to the particular combination of approach speed and directness of approach, and may not apply to some other pairs of risk factors. The threat-sensitivity hypothesis (Helfman, 1989
) states that risk is traded off against cost in a graded manner. Smith and Belk (2001) considered that simultaneously acting risk factors must have additive effects under the threat-sensitivity hypothesis. They showed that predator diet and predator hunger level additively affected avoidance of green sunfish (Lepomis cyanellus) by mosquitofish (Gambusia affinis), but that predator size and hunger interactively affected predator inspection. Smith and Belk (2001) suggested that for mosquitofish, avoidance may be determined by additive risks, but they implied that risks may interact for riskier behaviors such as predator inspection. Our data for whiptail lizards show that risk factors may interact for less risky behaviors such as escape. For refuging prey, Kramer and Bonenfant (1997) hypothesized that prey maintain a margin of safety by simultaneously considering distance from refuge and the direction of approach by the predator. Their model, which specifies linear risk curves, predicts interaction between distance to refuge and another risk factor, but does not apply directly to prey that do not use refuges. Optimal escape theory could predict whether risks and costs are additive or interactive if the shapes of the risk curves were known. Theoretical predictions about interactions are not currently possible because the relationship between distance from the predator and risk in fitness units is not known for the various risk factors. Development of methods for determining shapes of risk and cost curves would be extremely valuable for testing predictions about relationships involving risk-cost combinations. In the absence of such methods, empirical studies of combinations of several risk factors are needed to determine which operate independently and which interact.
The predicted interaction between the risk and cost factors was not observed. This finding contradicts the prediction of optimal escape theory based on the linear cost curves presented graphically by Ydenberg and Dill (1986). As shown in Figure 1, a greater difference in flight initiation distance for high and low cost curves is predicted for higher than lower risk curves. Nevertheless, the lack of interaction between risk and cost does not contradict the more general interpretation that Ydenberg and Dill (1986) undoubtedly intended. If cost curves, as well as risk curves are curvilinear, the relative differences in optimal flight initiation distance between cost curves for higher and lower risk curves cannot be specified a priori. Thus, the lack of interaction between risk and cost that we observed suggests that the cost curves for presence of food might be nonlinear although reasons for this are unclear.
Another likely possibility is that costs of fleeing are not equal when food is present or absent and the predator and prey are in the same position (at the origin in Figure 1). Cost curves may often be parallel rather than intersecting when the predator is at zero distance from the prey. Such cases seem very likely to exist and contradict the original formulation of optimal escape theory.
An alternative explanation for the lack of significant interaction between risk and cost might be that a small interaction with nonlinear costs existed but was not detected owing to small sample size relative to effect size, variability of flight initiation distances, random differences in wariness among individuals chosen in the four experimental groups, or a combination of these factors. Another consideration is that the optimal escape model is based on actual risks and costs, but prey must assess these indirectly. Differences in the ability of prey to assess various risk and cost variables could affect interaction. Studies of additional risk-cost combinations using larger samples, strongly contrasting risk and cost levels, and perhaps repeated-measures designs to control for individuals differences in wariness are needed to further evaluate the effects of combinations of risk and cost factors on escape behavior.
Optimal escape without refuge
Predictions of optimal escape theory were verified for lizard prey that did not escape to refuges. The findings for approach speed, direction of approach, and presence of food are similar to those for previously studied prey that use refuges. In C. murinus, flight initiation distance increased with predator approach speed, as in E. laticeps (Cooper, 1997a). Flight initiation distance increased with directness of approach at high approach speed, as it did in several other lizard species (Bulova, 1994; Burger and Gochfeld, 1990; Cooper, 1997a). The tradeoff between predation risk and loss of opportunity to feed by C. murinus is similar to that observed in E. laticeps (Cooper, 2000). Although refuge use has been a prominent feature in studies of escape behavior, limited data for ungulates and lizards suggest that optimal escape theory applies equally well to nonrefuging prey. Theoretically, optimal escape theory should apply equally to refuging and nonrefuging prey, because distance from refuge is a risk factor for species that use them, whereas it is not a consideration for those that do not.
Predictions regarding individual factors
Optimal escape theory accurately predicted that risk and cost factors affected flight initiation distance. Flight initiation distance increased with predator approach speed in both experiments, indicating its importance for escape decisions. Because a rapidly approaching predator poses a much greater immediate threat at a given distance than does a slowly approaching predator, approach speed must be an important cue to a wide range of prey taxa, and is known to be so in two lizard families, Teiidae and Scincidae (Cooper, 1997c; this paper).
Directness of approach also affected escape decisions by lizards that fled, the flight initiation distance being was slightly greater for lizards approached directly than indirectly. At the 5-m bypass distance, nearly half of lizards did not flee at all. Because the proportion of individuals that fled increased greatly with directness of approach, lizards likely perceived more direct approach as indicating greater threat, and increased their flight initiation distance accordingly. Depending on the rate of increase in risk with directness of approach, a range of distances may exist in which closer approach is permitted on indirect than direct paths. This result has been demonstrated for several lizard species (Bulova, 1994; Burger and Gochfeld, 1990; Cooper, 1997a) and is extended here.
Bonaire whiptail lizards reacted to the presence of food as predicted, as shown by the decrease in flight initiation distance in trials in which food was present. This finding suggest that the lizards took the cost of leaving food into account in deciding when to flee, permitting the predator to draw nearer before fleeing when the cost of escaping was higher.
Flight initiation distances were notably greater in experiment 1 than in experiment 2, presumably reflecting the more frequent contact between human beings and lizards in the Slagbaai National Park (experiment 2) than in experiment 1. Frequent human presence is known to be associated with decreased flight initiation distance in species from three other lizards families: Iguanidae, Tropiduridae, and Scincidae (Burger and Gochfeld, 1981; Eifler, 2001; Labra and Leonard, 1999); presumably because of habituation to human presence without being attacked.
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ACKNOWLEDGEMENTS |
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This work was partially supported by a grant from the Cleveland Metroparks Zoo and by travel funds from our universities.
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REFERENCES |
|---|
|
TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
|---|
Bonenfant M, Kramer DL, 1996. The influence of distance to burrow on flight initiation distance in the woodchuck, Marmota monax. Behav Ecol 7:299-303.
Bulova SJ, 1994. Ecological correlates of population and individual variation in antipredator behavior of two species of desert lizards. Copeia 1994:980–992.
Burger J, Gochfeld M, 1981. Discrimination of the threat of direct versus tangential approach to the nest by incubating herring and great black-backed gulls. J Comp Physiol Psychol 95:676-684.[CrossRef]
Burger J, Gochfeld M, 1990. Risk discrimination of direct versus tangential approach by basking black iguana (Ctenosaura similis): variation as a function of human exposure. J Comp Psychol 104:388-394.[CrossRef]
Cooper WE, Jr, 1997a. Escape by a refuging prey: the broad-headed skink (Eumeces laticeps). Can J Zool 75:943-947.
Cooper WE, Jr, 1997b. Factors affecting risk and cost of escape by the broad-headed skink (Eumeces laticeps): predator speed, directness of approach, and female presence. Herpetologica 53:464-474.[ISI]
Cooper WE, Jr, 1997c. Threat factors affecting antipredatory behavior in the broad-headed skink (Eumeces laticeps): repeated approach, change in predator path, and predator's field of view. Copeia 1997:613–619.
Cooper WE, Jr, 1998a. Direction of predator turning, a neglected cue to predation risk. Behaviour 135:55-64.
Cooper WE, Jr, 1998b. Risk factors and emergence from refuge in the lizard Eumeces laticeps. Behaviour 135:1065-1076.
Cooper WE, Jr, 1999. Tradeoffs between courtship, fighting, and antipredatory behavior by a lizard, Eumeces laticeps. Behav Ecol Sociobiol 47:54-59.[CrossRef]
Cooper WE, Jr, 2000. Tradeoffs between predation risk and feeding in a lizard, the broad-headed skink (Eumeces laticeps). Behaviour 137:1175-1189.[CrossRef]
Dearing MD, Schall JJ, 1992. Testing models of optimal diet assembly by the generalist herbivorous lizard Cnemidophorus murinus. Ecology 73:845-858.[CrossRef]
Dial BE, 1986. Tail display in two species of iguanid lizards: a test of the "predator signal" hypothesis. Am Nat 127:103-111.[CrossRef]
Dill LM, 1990. Distance-to-cover and the escape decisions of an African cichlid fish, Melanochromis chipokae. Envl Biol Fish 27:147-152.[CrossRef]
Dill LM, Fraser AHG, 1997. The worm re-turns: hiding behavior of a tube-dwelling marine polychaete, Serpula vermicularis. Behav Ecol 8:186-193.
Eifler D, 2001. Egernia cunninghami (Cunningham's skink) escape behavior. Herp Rev 32:40.
Grant JW, Noakes DLG, 1987. Escape behaviour and use of cover by young-of-the-year brook trout, Salvelinus fontinalis. Can J Fish Aquat Sci 44:1390-1396.
Heatwole H, 1968. Relationship of escape behavior and camouflage in anoline lizards. Copeia 1968:109–113.
Helfman GS, 1989. Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47-58.
Kramer DL, Bonenfant M, 1997. Direction of predator approach and the decision to flee to a refuge. Anim Behav 54:289-295.[CrossRef][ISI][Medline]
Labra A, Leonard R, 1999. Intraspecific variation in antipredator response of three species of lizards (Liolaemus): possible effects of human presence. J Herpetol 33:441-448.
LaGory KE, 1987. The influence of habitat and group characteristics in the alarm and flight response of white-tailed deer. Anim Behav 35:20-25.[CrossRef]
Martín J, Lopéz P, 1995. Influence of habitat structure on the escape tactics of the lizard Psammodromus algirus. Can J Zool 73:129-132.
Martín J, Lopéz P, 1999a. An experimental test of the costs of antipredatory refuge use in the wall lizard, Podarcis muralis. Oikos 84:499-505.[CrossRef][ISI]
Martín J, Lopéz P, 1999b. When to come out from a refuge: risk-sensitive and state-dependent decisions in an alpine lizard. Behav Ecol 10:487-492.
McLean EB, Godin J-GJ, 1989. Distance to cover and fleeing from predators in fish with different amounts of defensive armour. Oikos 55:281-290.[CrossRef]
Rand AS, 1964. Inverse relationship between temperature and shyness in the lizardAnolis lineatopus. Ecology 45:863-864.[CrossRef]
Sih A, 1992. Prey uncertainty and the balancing of antipredator and foraging needs. Am Nat 139:1052-1069.[CrossRef]
Smith DG, 1997. Ecological factors influencing the antipredator behaviors of the ground skink, Scincella lateralis. Behav Ecol 8:622-629.
Smith ME, Belk MC, 2001. Risk assessment in western mosquitofish (Gambusia affinis): do multiple cues have additive effects? Behav Ecol Sociobiol 51:101-107.[CrossRef]
Statistica,, 1999. User guide, version 5.5. Tulsa, Oklahoma: Statsoft.
Walther FR, 1969. Flight behaviour and avoidance of predators in Thomson's gazelle (Gazella thomsoni Guenther 1884). Behaviour 34:184-221.
Ydenberg RC, Dill LM, 1986. The economics of fleeing from predators. Adv Stud Behav 16:229-249.
Zar JH, 1996. Biostatistical analysis, 3rd ed. Upper Saddle River, New Jersey: Prentice Hall.
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