Forced Copulation and Costly Female Resistance

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ABSTRACT: Male Lake Eyre dragons (Ctenophorus maculosus) have evolved behaviors to over- ... also develop a bright red ventral coloration after theĀ ...
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Forced Copulation and Costly Female Resistance Behavior in the Lake Eyre Dragon, Ctenophorus maculosus Author(s): Mats Olsson Source: Herpetologica, Vol. 51, No. 1 (Mar., 1995), pp. 19-24 Published by: Herpetologists' League Stable URL: http://www.jstor.org/stable/3892780 . Accessed: 16/08/2013 19:02 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp

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Herpetologica,51(1), 1995, 19-24 ? 1995 by The Herpetologists' League, Inc.

FORCED COPULATION AND COSTLY FEMALE RESISTANCE BEHAVIOR IN THE LAKE EYRE DRAGON, CTENOPHORUS MACULOSUS MATS OLSSON' University of Goteborg,Department of Zoology, Medicinaregatan 18, 413 90 Gdteborg,Sweden ABSTRACT: Male Lake Eyre dragons (Ctenophorus maculosus) have evolved behaviors to overcome female resistance to copulation. Males press rejecting females to the ground before they try to intromit; males that press females longer to the ground also copulate longer. Unreceptive females have a repertoire of three rejection behaviors that they use singly or in combination to expel males. Large females threaten with a lateral posture, small females predominantly flee, and all females eventually flip over onto their backs when resisting copulations. The size ratio of the sexes has a significant effect on the extent to which flip-over behavior is used by females. The female rejection of males incurs high costs to the females, such as open wounds and perhaps increased predation. The benefits of female mate rejection are not clear, but one hypothesis is that females may benefit from avoiding copulations with non-preferred males.

Key words:

Female rejection; Forced copulation; Lizard; Ctenophorus maculosus

is selected to copulate while the other sex ultimately benefits from refusing to do so. However, only a few studies have been able to demonstrate behavioral and morphological adaptations resulting from selection in such situations (e.g., Thornhill and Sauer, 1991). In some species, males coerce matings with unreceptive females [e.g., in birds (McKinney et al., 1983), insects (Arnqvist, 1989; Thornhill, 1980; Thornhill and Sauer, 1991), and lizards (Werner,1978)].In two species, males have even evolved morphological adaptations specifically designed to obtain matings by force. In a water strider (Gerris odontogaster), males coerce copulationsby using a clasperon the abdomen (Arnqvist,1979). In the scorpionfly (Panorpa vulgaris), the clamplike notal organ makes it possiblefor males to coerce copulations when lack of food preventsthe male from producingthe nuptial gift needed to induce female receptivity (Thornhill and Sauer, 1991). In two phylogenetically widely separate taxa, a water strider (Gerrisodontogaster) (Arnqvist, 1989) and a lizard (Ctenophorus maculosus) (Mitchell, 1973), females flip over onto their backs when resisting attempts at forced copulation. In C. maculosus (the Lake Eyre dragon), females also develop a bright red ventral coloration after the receptive period, which is ex-

A MALE'S advantage from multiple copulations is not controversial:more matings often yield more offspring (Darwin, 1871). However, in several situations females are expected not to mate (Thornhill, 1980). The mechanism explaining female mate rejection can be proximate: e.g., a female may refuse to mate with all males simply because she is not yet physiologically and behaviorally ready to mate. This occurs, for instance, when females emerge after males from a period of inactivity preceding the mating season and initially reject courting males (Carpenter and Ferguson, 1977; Thornhill and Alcock, 1983; Wittenberger, 1981). In other species, the mechanism is ultimate and females have evolved mate rejection as a form of mate choice, avoiding copulations with non-preferred males (e.g., Cox and LeBouef, 1977). When female mate rejection is costly (e.g., by being time consuming or by exposing females to danger), one expects a selective advantage to offset its costs. Conflicting interests of the sexes may lead to sexual conflict over matings (Williams, 1966), a situation in which one sex

' PRESENT ADDRESS: The University of Sydney, School of Biological Sciences, Zoology Building AO8, N.S.W. 2006, Australia.

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posed when females flip over. In this study, I investigated resistance behavior in C. maculosus; the objectives of this paper were to (1) investigate the circumstances in which females use "flip-over"and other rejection behaviors, (2) describe male behaviors that facilitate forced copulation, (3) examine the relationship between the male: female size ratio and the occurrence or avoidance of forced copulation, (4) identify costs that females may suffer by rejecting males, and (5) discuss what benefits may result from female mate rejection. Ctenophorus maculosus (Agamidae) lives on dry saltlakes in the South Australian interior. A detailed description of its general ecology and morphology was provided by Mitchell (1973). The species is sexually dimorphic; mature males are approximately 55-70 mm snout-vent length (SVL) and mature females are 52-64 mm SVL. In late August, the dominant males have established territories. Females emerge from hibernationabout 2 wk after the males and situate themselves within the territories of dominant males (Mitchell, 1973). METHODS

Field Methods I performed a field study of Lake Eyre dragons (Ctenophorus maculosus) for 3 mo/yr in 1986 and 1987. The study site was a dry saltlake (Lake Eyre, Prescott Point) in South Australia. The climatic conditions were extremely harsh. Duststorms occurred every third to fourth day and the maximum recorded temperature when lizards were still active was 46 C in the shade. The behavioral data were collected in 1987 by studying animals in a fenced 100 x 100 m area of natural habitat. The fence was made by digging a 50cm deep trench around the circumference of the area into which plastic sheeting was secured by refilling the trench. The upper part of the plastic was stapled around a wire strung between 50 cm high poles. Into this enclosure, I introduced 14 mature males and 27 females from the surrounding area. The lizards were caught arbi-

[Vol. 51, No. 1

trarily, and their size distributionreflected that of the mature wild population. I measured each individual to the nearest 1 mm SVL, weighed it to the nearest 0.1 g on a Pesola scale, and painted an identification number on its back. I observed mating behaviors and agonistic encounters through binoculars from the shore of the dry saltlake and by walking around the circumference of the enclosure. All copulationattempts(n = 31) by males (n = 7) included in the analyses were directed at post-receptive females (n = 9): i.e., females that had developed red ventral coloration. I noted repertoires of female behaviors during the attempts at forced copulation and I timed them with a stop-watch (mean number of observations per pair = 2.6 ? 3.2 SD). Statistical Methods In males, I calculated the mean size ratio

between a male and all of the females with which he had attempted to copulate (male SVL/female SVL). I also calculated the mean values of the time that he was engaged in displaying behaviors.These mean values were used to analyze the importance of the relative size of the sexes for coercing copulations. I arcsine-transformed all ratiosand log-transformedmale SVL'sbefore statisticalanalyses (Sokaland Rohlf, 1981). In females, I calculated the average time that a female spent on a given rejection behavior as a proportion of the total time that she was observed rejecting a male. Also for females I arcsine-transformedall ratios, and log-transformed SVL's before statisticalanalyses (Sokaland Rohlf, 1981). In an analysis of covariance, using the proportionof "flip-over"as the dependent variable, I used female identificationnumber (class variable) and size ratio as the independent variables.In the case of three females, two males of identical SVL had been observed attempting to copulate. To avoid pseudoreplication, I randomly selected one of these males for each female for the statistical analysis of the influence of size ratio on incidence of "flip-over" behavior.

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March 1995]

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RESULTS

All females that I observed in interactions with males refused to copulate. A male mating attempt involved no courtship; the male rushed up to the female and grasped her by the nape, after which he rolled her onto her side and tried to intromit. The unreceptive female responded with rejection in one of three ways; (1) initially she tried to run away, pursued by the male, or (2) arched her back and turned the flattened body side towards the approaching male; (3) eventually, she flipped over onto her back, which prevented copulation and exposed her bright red abdomen. These behaviors will henceforth be referred to as "run", "lateral threat", and "flip-over,"respectively. I made no observations of females using "flip-over" behavior in other contexts than when deterring males. Male Behavior As soon as a female rolled back to a normal position after a "flip-over" rejection, the male threw himself on top of her, pressed the female to the ground, and thereby made it impossible for her to flip over on to her back again. On average, males pressed females to the ground for 12.9 s (?8.4 SD, n = 20). Five of the seven males were observed attempting to copulate with different females more than once (mean number of observationsper male = 2.86 ? 1.86 SD). These males did not differ in either how long they pressed females to the ground or in copulation duration (Kruskal-Wallis analysis of variance by ranks,Chi-squareapproximation,x2= 2.2, P = 0.70, and x2 = 2.0, P = 0.74, df = 4 respectively). Male SVL was not significantly correlated with pressingdurationor copulation duration (r = 0.28, P = 0.54 and r = 0.26, P = 0.58, respectively, n = 7). However, the size ratio between the male and female was significantly correlated with both pressingduration (r = 0.76, P < 0.05, n = 7: Fig. 1) and copulation duration (r = 0.78, P = 0.04, n = 7). The importance of the male: female size ratio for successful forced copulation became even more evident when male SVL was

21

0

25 U)

0

20

E 15

0

CD

0~

@ 10 (L

L

5 0

0.102

0.104

0.106

Male SVL/Female

0.108

0.110

SVL (arcsine,

mm)

FIG. 1.-Mean time that a male pressed females to the ground plotted against the mean size ratio between the male and the females that he attempted to mate (r = 0.76, P < 0.05, n = 7).

held constant at its mean in a partial correlation (r = 0.86, P = 0.03 and r = 0.90, P = 0.02 respectively, n = 7). The mean time that females were pressed to the ground was positively correlated with mean copulation time (r = 0.83, P = 0.02, n =

7). Female Behavior Females responded to attempts at forced copulation by employing the three rejection behaviors singly or in combination (the proportion of each rejection behavior of the total rejection time was: run = 17%, lateral threat = 24%, flip-over = 59%, n

=

31). To look for differences among females in the use of the three rejection behaviors, I performed an unbalanced analysis of variance. I used the female's identification number as the class variable and the proportion of the analyzed behavior as the response variable (Table 1, mean number of observations per female = 3.1 ? 1.4, range 2-6). Females differed significantly in "lateral threat" (P < 0.01), and the results of "run" bordered on significant (P = 0.06). "Flip-over" could not be demonstrated to vary significantly among females (P = 0.18).

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[Vol. 51, No. 1

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TABLE 1.-Results of analysisof variance, using female identificationnumber as class variable.

Dependent variable "Lateralthreat" Error Correctedtotal Dependent variable "Run" Error Correctedtotal Dependent variable "Flip-over" Error Correctedtotal

R2

df

SS

MS

F

P

0.71

8 22 30

6.16 2.55 8.71

0.76 0.12

6.6

0.002

0.45

8 22 30

4.68 5.65 10.33

0.58 0.26

2.28

0.06

0.37

8 22 30

4.41 7.63 12.04

0.55 0.35

1.59

0.18

"Lateralthreat"and "run"were the be- employed "flip-over"more often when the haviors first used to deter and or escape size difference between the sexes was great from a male's forced copulation attempt. (R2 = 0.59, Model, df = 9, error = 18, SS These behaviors appeared to be size-de- = 6.28, MS = 0.67, F = 2.84, P = 0.03; size pendent; this was analyzed by correlating ratio, df = 1, SS = 1.39, MS = 1.39, F = arcsine-transformedmean ratios of these 5.66, P = 0.03). behaviors with female SVL (r = -0.83, P Costs of Rejection < 0.01, n = 9: Fig. 2); small females used more "run"and fewer "lateralthreats"for One female died after an unusually mate rejection. fierce forced copulation.The cause of death The result of the analysis of covariance appeared to be that one of the male's endemonstrated a significant effect of size larged teeth penetrated her spine. Several ratio on "flip over" behavior; thus females of the other females had open wounds due to the ferocious male copulation attempts. I observed successful attacks on wild Lake Eyre dragons by hawks (Accipiter) and by Gould's monitor lizards (Varanus gouldii) C _ on several occasions. 01

0.8

DISCUSSION

a)

Unlike rejected males in most other liza0.2 ards (Stamps, 1983), a male Lake Eyre dragon continues his mating attempt de0.4 spite the persistentrejectionby the female. 0 The unusually fierce male mating behavior in this species, and the pressing of the :3 0 0.2_ -J female to the ground before attempts at intromission, seems to have evolved be, 0.0 _ @0* 00 cause it enhances forced copulations.Even if the female has alreadyovulated,the male 3.85 3.90 3.95 4.00 4.05 4.10 4.15 may experience some gain in reproductive success if females store sperm between Female SVL (log mm) FIG. 2.-The ratio between the durationsof "lat- ovulations.Female sperm storagehas been eral threat" and "run" in a female's rejection rep- demonstrated in the iguanid lizard Holbrookia propinqua (Adams and Cooper, ertoire plotted against her SVL (r = -0.83, P < 0.01, n = 9). 1988), and in the Lake Eyre dragon, fe-

4-

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March 1995]

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HERPETOLOGICA

males can store sperm for at least 3 mo within a reproductive cycle (Mitchell, 1973). Females may avoid copulations by using size-dependent "lateral threat'' and "run," and size-independent "flip-over" behaviors when avoiding forced copulations. Why do females evolve such dramatic rejection behaviors? First, female rejection cannot be an artefact of the experimental design; in a natural population, rejections and copulation attempts are not preceded by prolonged courtship, even when involving receptive females (Mitchell, 1973). The open habitat makes lizard movements eye-catching to the human observer and probably also to predators. It seems likely that male movements around the female may attract the attention of predators. One reason for female mate rejection after the period of receptivity could thus be minimization of nearby movements by males and, consequently, reduction of the likelihood of attracting predators to her vicinity. If so, mean rejection time for forced copulation would be predicted to be significantly shorter than the mean time of a copulation with a receptive female. Mitchell (1973) reported that this time is, on average, 25 s (no variance given). Thus, by mate rejection, a female does not appear to reduce substantially the interaction time with a male (mean rejection time in this study was 26.7 s, mean forced copulation time was 31.2 s). Thus, the hypothesis that females reduce the risk of predation by rejecting males is not supported by my data. Female Lake Eyre dragons live in one of the most, if not the most, exposed environments inhabited by lizards. Thus, at a relatively low cost, females can possibly observe and compare several males simultaneously. According to Mitchell (1973), females situate themselves on the boundaries between the adjoining territories of dominant males, which may facilitate an active choice of males by females. However, my data do not allow an analysis of mate choice in C. maculosus. Female choice on a male quantitative trait has been convincingly demonstrated only once in reptiles (Eumeces laticeps: Cooper

and Vitt, 1993), and hence appears to be rare. Williams (1966) discussed the evolutionary implications of sexual conflictsand concluded that "inevitably there is a kind of evolutionary battle of the sexes". In essence, he captured the idea of an intersexual evolutionaryarms race between the sexes (Dawkins and Krebs, 1979). In several respects, the sexual conflict over matings between males and females in the Lake Eyre dragon seems to conform to the idea of sexual behavior as such an evolutionary arms race. My data do not include information of female rejection in temporal relation to ovulation, multiple mating, and sperm competition between males. Thus, how the sex-specific costs and benefits of forcing and resistingcopulationsaffects reproductivesuccess,and what bearingsthey may have for evolution of, for example, body size, is outside the scope of this study. Acknowledgments. -I am grateful to L. Bak for enduring very trying working conditions and to the Mitchell families for their help and encouragement. I am also most grateful to M. Andersson for valuable discussions and to R. Thornhill, R. Swain, and two anonymous reviewers for critically commenting on an earlier draft of this manuscript. The Swedish Institute and Helge Ax:son Johnsson's foundation gave financial support.

LITERATURE CITED ADAMS, C. S., AND W. E. COOPER. 1988. Oviductal

morphology and sperm storage in the keeled earless lizard, Holbrookia propinqua. Herpetologica 44: 190-197. ARNQVIST, G. 1989. Multiple mating in a water strider: Mutual benefits or intersexual conflict. Anim. Behav. 38:749-756. CARPENTER, C. C., AND G. W. FERGUSON. 1977. Variation and evolution of stereotyped behavior in reptiles. Pp. 335-554. In C. Gans and D. Tinkle (Eds.), Biology of the Reptilia, Vol. 7. Academic Press, New York. COOPER, W. E., AND L. VITT. 1993. Female choice of large male broad-headed skinks. Anim. Behav. 45:683-693. Cox, C. R., AND B. J. LEBoUEF. 1977. Female incitation of male competition: A mechanism in sexual selection. Am. Nat. 111:317-335. DARWIN, C. 1871. The Descent of Man and Selection in Relation to Sex. John Murray, London. DAWKINS, R., AND J. KREBS. 1979. Arms races between and within species. Proc. R. Soc. Lond. 205: 489-511. McKINNEY, F., S. R. DERRICKSON, AND P. MINEAU.

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[Vol. 51, No. 1

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1983. Forced copulation in waterfowl. Behaviour 86:250-294. MITCHELL, F. J. 1973. Studies on the ecology of the agamid lizard Amphibolorus maculosus. Trans. R. Soc. S. Aust. 97:47-76. SOKAL, R. R., AND F. J. ROHLF. 1981. Biometry, 2nd ed. W. H. Freeman, San Francisco. STAMPS, J. 1983. Sexual selection, sexual dimorphism, and territoriality. Pp. 169-204. In R. Huey, E. Pianka, and T. Schoener (Eds.), Lizard Ecology-Studies of a Model Organism. Harvard University Press, Cambridge, Massachusetts. THORNHILL, R. 1980. Rape in Panorpa scorpionflies and a general rape hypothesis. Anim. Behav. 28: 52-59. THORNHILL, R., AND J. ALCOCK. 1983. The Evolution of Insect Mating Systems. Harvard University Press, Cambridge, Massachusetts.

THORNHILL, R., AND K. P. SAUER. 1991.

The notal organ of the scorpionfly Panorpa vulgaris: An adaptation to coerce mating duration. Behav. Ecol. 2:156-164. WERNER, D. I. 1978. On the biology of Tropidurus delanonis, Baur, (Iguanidae). Z. Tierpsychol. 47: 337-395. WILLIAMS, G. C. 1966. Adaptation and Natural Selection: A Critique of Some Current Evolutionary Thought. Princeton University Press, Princeton, New Jersey. WITTENBERGER, J. F. 1981. Animal Social Behavior. Duxbury Press, Boston. Accepted: 10 March 1994 Associate Editor: Richard Howard

Herpetologsca, 51(1), 1995, 24-38 ? 1995 by The Herpetologists' League, Inc.

REPRODUCTIVE BIOLOGY OF THE LIZARD UROSAURUS BICARINATUS BICARINATUS (REPTILIA:PHRYNOSOMATIDAE)FROM RIO BALSASBASIN, MEXICO AURELIO RAMiREZ-BAUTISTA,' ZEFERINO URIBE-PErA,' AND Louis J. GUILLETTE, JR.2 'Laboratoriode herpetolog(a,Departamento de Zoologia, Instituto de Biologfa, UNAM, A. P. 70-153 C. U., C.P. 04510, Mexico 20, Distrito Federal, Mexico 2Departmentof Zoology, University of Florida, Gainesville, FL 32611, USA ABSTRACT: We studied the reproductive biology of two populations of the arboreal lizard Urosaurus b. bicarinatus from 1980-1984 in western Mexico. One population is located in the elevated portion of the Rio Balsas Basin, in the state of Morelos, and the other at a lowland site of the basin in the state of Michoacin. Data were obtained from specimens collected in the field and from museum collections. Females and males of both populations exhibit a pattern of late spring and summer reproduction. Males show maximal testicular volume and activity during the late spring and summer months in Michoacin and during the spring and summer months in Morelos. Vitellogenesis begins in April in both populations, with most females ovulating in the summer. Incubation occurs during the summer with hatching in late summer and early fall. Individuals reach sexual maturity within a year. Mean clutch size for oviductal eggs was 7.7 ? 2.4 and 6.7 + 1.8 in populations from Morelos and Michoacin respectively. No correlation between snout-vent length of females and clutch size was found.

Key words: Reptilia; Sauria; Phrynosomatidae; Urosaurus bicarinatus; Reproduction; Oviparity; Life-history; Mexico

VARIATION in reproductive patterns in numerous reptilian species has been well documented, and a great diversity of life history characteristics has been recorded

(Dunham and Miles, 1985; Licht, 1984;

Vitt, 1986). Since the classic studies of Tinkle (1969) and Tinkle et al. (1970) on life historyevolutionof lizards,additionalideas have been formulated to explain life history patterns. These patterns have been

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