1 Effects of competition on copulatory behaviors in Pseudoxychila tarsalis (Coleoptera: Cicindelidae) Hilary Wilson Department of Biology, Indiana University ABSTRACT This study examines the effects of competition on copulatory behaviors of the tiger bee tle Pseudoxychila tarsalis I tested the hypothesis that copulatory behavior of a P. tarsalis mating pair in the presence of an additional male would induce significant behavioral changes, including longer amplexus time and increased frequency of a variet y of copulatory behaviors. Trials were conducted with either one male and one female, or two males and one female, and the behaviors of one copulatory amplexus recorded per trial. No statistical differences were found for the male behaviors of time until mount, amplexus duration, or number of intromissions, but means tended to decline in each for the two male trials. Rocking and tapping behaviors in males decreased significantly in the presence of a second male, indicating a response to competition. The general downward trend in the two male trials may be explained by interruption of copulatory behaviors by the non copulating male. Female batting showed a slight but not significant increase in the presence of a second male, which may be intended as a de terrent so that she may gain access to the second male. RESUMEN Este estudio examina los efectos de la competencia en comportamientos de copulacin en el escarabajo tigre, Pseudoxychila tarsalis Prob la hiptesis que las conductas de una pareja de P. tarsalis en la presencia de otro macho inducira cambios conductistas significativos de comportamientos, inclusivo tiempo ms largo de amplexo y aumentos en la frecuencia de una variedad de comportamientos de copulacin. Las pruebas se realizaron con un macho y una hembra, o dos machos y una hembra, y los comportamientos durante el amplexo se registraron por cada prueba. No se encontraron diferencias estadsticas en los comportamientos masculinos de tiempo hasta la monta, la duracin de amplexo, ni el n mero de copulacines, pero las tendencias bajan en las pruebas con con dos machos. Los comportamientos de mecer y golpear bajan apreciablemente en la presencia de un segundo macho, lo que indica una respuesta a la competencia. La tendencia decreciente en las pruebas con dos machos puede ser explicada por la interrupcin de conductas de sexualidad por el macho nocopulatorio. El golpeteo de la hembra mostr un leveaumento, pero no fue significativo, en la presencia de un segundo macho, que posiblimente pue de ser dirigido como impedimento de tal manera que ella pueda tener acceso al segundo macho. INTRODUCTION Reproductive success is of paramount importance for every living organism passed on to subsequent generations. Among sexually reproducing species, there should thus be strong selection to choose or compete for the best or most mates, as this will largely ween two kinds
2 Otte 1979). Epigamic selection, the result of one sex selecting on the o ther, is best epitomized by situations in which mating is solely a function of female choice between or among males, and females determine which males reproduce. Intrasexual selection operates within members of the same sex, often manifested by male male competition for females, and hence males themselves determine which males mate. However, these selection mechanisms are not necessarily mutually exclusive. Gould (1989) cites an example of an English migratory bird species that displays both epigamic and intrasexual selection. Males arrive in the spring before females in order to compete for and secure the choicest territories. When females arrive soon after, they choose mates based on the territories they hold. Epigamic selection (female choice of mal es with superior territories) causes the males to compete (intrasexual selection). Bateman proposed that, in most species, differential reproductive strategies between the sexes are a function of fertility limitations based on number of gametes and capacit y for offspring production. In females, producing offspring is more energetically expensive, and females have a finite capacity for egg production. Therefore, females should be interested in generating the highest quality of offspring, because quantity i s limited. However, males are not limited in this way because of the low cost of sperm production, and are instead more limited by the number of inseminations during their lifetime. Hence, male reproductive strategy focuses more highly on quantity rather than quality (Bateman 1948, in Otte 1979). The net result is competition for limited female gametes by the abundant male gametes. When male parental investment is nothing but genetic material, as in most insects, male reproductive effort should be channe led into competition between males, and females may select between competing males (Thornhill 1979). Pseudoxychila tarsalis is a virtually blind, flightless tiger beetle found in the highlands of Costa Rica, between 600 and 2000 meters elevation. This sp ecies is recognized by a single yellow dot ringed in black on each elytra on an otherwise iridescent blue green body. They are generally found in open clay areas, disturbed vegetation, and steep clay embankments (Palmer 1983; Pearson 2001). These beetles exhibit a range of observable copulatory behaviors and transfer sperm in discrete packets called spermatophores. In P. tarsalis paternal investment in offspring includes only copulatory behavior, and theory thus predicts that males would compete for ac cess to females, which may favor the evolution of traits that give males a chance to copulate. However, this is Pearson and Vogler 2001) in which females are able to reje ct and expel the spermatophore during or after copulation (Rodrguez 1998, 2000 in Pearson and Vogler 2001). Because copulation does not ensure paternity, males must compete not only to access the female, they must also convince her to accept the spermato phore. Here, epigamic and intrasexual are working in concert to influence male copulatory behavior. I asked the question, how does this competition affect reproductive behaviors? In a study of Indian tiger beetles, two of five species showed longer post copulatory amplexus (in which the male rides the female after sperm transfer has taken place) in the presence of another male. This suggests that post copulatory amplexus may be a mate guarding behavior to help confer the highest probability of fertiliza tion by his own sperm (Shivashankar and Pearson 1994).
3 This study examines a range of copulatory behaviors in mating pairs of P. tarsalis in the presence and absence of an additional male. I hypothesized that competition, in the form of the additional mal e, would result in significant differences in the behaviors of the two groups. Specifically, I predicted that intrasexual selection would induce males to mount more quickly and remain in amplexus longer, and epigamic selection would effect an increase in f requency of a range of other copulatory behaviors. METHODS This study took place between October 25th and November 12th, 2004, near Monteverde, Costa Rica. This area is classified as a Lower Montane Wet Forest Holdridge Life Zone and is located at an e levation of approximately 1525 meters. Pseudoxychila tarsalis were collected between 9 a.m. and 12:00 p.m. on clay roads, embankments, and ditches, including the road leading to the Estacin Biolgica Monteverde and the nearby Cerro Amigos road. Individua ls were retrieved using forceps and placed in small plastic bags where they were sexed by presence (male) or absence (female) of setal pads on the tarsi of the first pair of legs (Pearson and Vogler 2001). Females and males were kept in two separate, smal l, open terrariums (30 x 20 x 20 cm) with a small amount of the clay dirt on which they were found, and supplied with water and numerous dead moths each day as fodder. Specimens were kept up to three days and released after testing; thus no individual was tested more than once. All trials were conducted between 10:00 a.m. and 4:00 p.m. Trials consisted of either one male and one female (n = 20), or two males and one female (n = 20) placed in a nine centimeter diameter covered Petri dish. Males were placed in the Petri dish first, and time started when the female was added. Time was recorded at the initial mount, copulatory behaviors recorded (see below), and time again recorded at dismount. Trials ended when the male dismounted, at which point individual s were removed from the Petri dish. Thus, even in two male trials, only one male was given the opportunity to mount. If a male did not mount within five minutes of start, the trial was terminated and individuals replaced in the terrariums. The followin g copulatory behaviors were observed and quantified: Mount: Male grasps female from behind by clasping her thorax with his mandibles. Amplexus: Continued mounted position of male before, during, and after copulation. Rocking: Pumping motion of male with body, abdomen, and/or aedeagus during intromission. Tapping: Male repeatedly hits thorax and/or abdomen of female while in amplexus. Female Batting: Female taps the male on the head with tarsi of front legs during amplexus. Dismount: Male releases the thorax of the female from his mandibles, terminating amplexus.
4 RESULTS General Observations of Copulatory Behavior After the female was placed in the Petri dish, copulatory behav ior began with the male mounting the female, usually followed immediately by intromission. Intromission was generally, although not always, accompanied by rocking. After a period of intromission, males withdrew the aedeagus, and a period of amplexus with out intromission would follow. Tapping and female batting occurred either during or after intromission, often in series, although these behaviors did not occur in every trial. In addition, several other behaviors occurred that were not quantified. Freque ntly females were observed repeatedly exposing the hypogynal valve from the tip of the abdomen (n = 12/40), which may be evidence for the rejection of the spermatophore (Rodstrom 1998). This behavior occurred either during or after amplexus. Trials inclu ding two males often included attacking behavior from the non copulating male (n = 13/20). This usually took the form of the non copulating male mounting the copulating male, either in standard mounting position or oriented in the opposite direction (abdo men facing the head of the female), although sometimes the interference was continual climbing over and around the copulating pair. When a non copulating male mounted a copulating male, the copulating male would often display batting behavior (tapping the head of the other male) similar to female batting during amplexus (n = 9/13). Statistical Analyses and Comparisons Data regarding time until mount, amplexus duration, number of intromissions, rocking, tapping, and female batting were analyzed using a Ma nn Whitney U test to compare means between the one male (n = 20) and two male (n = 20) groups. Mean amplexus time was shorter in the two male group (501 492 seconds) compared to the one male group (689 496 seconds), although the difference was not sign ificant (U = 267, p = 0.070). Analysis showed no significant differences for time to mount (U = 250.5, p = 0.172), or number of intromissions (U = 236.0, p = 0.310), although downward trends can be observed in each from the one male to two male groups. M ales in the one male group exhibited significantly more rocking (U = 290.5, p = 0.014) and tapping (U = 282.5, p = 0.024) than those in the two male group. Female batting showed a slight but not significant increase (U = 216, p = 0.649) in the two male gr oup (2.15 3.03) as compared to the one male group (1.75 2.49) (Figure 1). To assess the possibility that the greater rocking and tapping times in the one male group were merely a function of greater time, a Spearman Rank Correlation was run to determ ine whether or not a relationship occurred between amplexus duration and tapping and/or rocking (Figure 2). Amplexus duration was significantly correlated with tapping (r = 0.552, p = 0.001, n = 20), but not with rocking (r = 0.271, p = 0.098, n = 20). D ISCUSSION Contrary to my hypothesis, most elements of copulatory behavior in P. tarsalis did not change significantly in the presence of an additional male. However, a trend is shown
5 that males mounted the female faster in the presence of a competitor. This behavioral response was expected based on intrasexual selection because mounting the female faster may help the male preferentially gain access to the female, thus potentially increasing the number of offspring he produces. Based on intrasexual selec tion, I predicted that the frequency of various copulatory behaviors would increase with competition; however, every male behavior actually tended to decrease in the presence of a second male. Mean amplexus tended to be shorter in the two male group compa red to the one male group, although the difference was not significant. The attacking behaviors observed in many of the two male trials suggest that many behaviors were interrupted or hindered, which explains the decrease in mean amplexus duration, number of intromissions, and the significant differences in rocking and tapping. These behaviors are part of a normal copulatory sequence that is apparently impeded by competition. Although Shivashankar and Pearson (1994) report longer amplexus time in the pres ence of a second male, my results may be related to the small size of the mating area in comparison to the large area considered in this previous study. The more limited area may have induced more interactions and attacks, thus interrupting behaviors of t he mounted male. In addition, Shivashankar and Pearson (1994) report that only two out of five species display this increased post copulatory amplexus, meaning that this is not necessarily a ubiquitous behavior. The only female behavior quantified, battin g, tended to increase slightly in the two male group. Exhibition of male batting (males batting other males) during attacks, as well as batting displays by individuals of both sexes when transported by forceps, lead me to believe that batting may be inten ded as a deterrent. The increased frequency of batting in the presence of second male supports this hypothesis, as the female may want a chance to copulate with a the other, potentially superior, male in the area. The effectiveness of this behavior, howe ver, is questionable, as I did not detect an observable change in male behavior in response to female batting. My data show that some copulatory behaviors in P. tarsalis indicate a response to the presence of a competitor, but do not address the consequenc es of these changed behaviors, nor do they examine these behaviors in a natural setting. Future studies could address factors that influence the acceptance or rejection of the spermatophore, and effects of behaviors on the paternity of offspring. Additio nally, they could study these behaviors in the wild, or in laboratory conditions that more closely simulate a natural environment. In conclusion, epigamic selection, at least on small spatial scales, appears to operate not by changing male behaviors during copulation, but instead by cryptic female choice. Epigamic factors may also influence the tendency toward increased female batting in the presence of a second male, although this behavior and its function need further study. Intrasexual selection explai ns the tendency toward shorter mounting time in the presence of competition, but it appears that the most important factor changing behaviors in this study was interference by the competitor, which itself may be a product of intrasexual selection.
6 ACKNOW LEDGMENTS Thanks to Karen and Alan Masters for their guidance, direction, inspiration, and most of all patience. Thanks to Ollie Hyman and Matt Gasner for assistance in collecting samples and answering all my tedious questions, the Estacin Biolgica Mont everde for use of their wonderful facilities, Javier Mendez for translation assistance, and Missy Senf for additional collection help and, more importantly, comic relief. LITERATURE CITED Bateman, A. J. 1948. Intra sexual selection in Drosophila. Her edity 2: 349 368. Eberhard, W.G. 1994. Evidence for widespread courtship during copulation in 131 species of insects and spiders, and implications for cryptic female choice. Evolution 48:711 733. Gould, J.L. and C.G. Gould. 1989. Sexual Selection. Sci entific American Library, New York. Amer. Nat. 72:416 433. Otte, D. 1979. Historical Development of Sexual Selection Theory. In: Sexual Selection and Reproductive Competition in Insects, M.S. Blum an d N.A. Blum, ed. Academic Press, New York, NY, p.8. Palmer, M.K. 1983. Pseudoxychila tarsalis (Abejn Tigre, Tiger Beetle). In: Costa Rican Natural History, D.H. Janzen, ed. The University of Chicago Press, Chicago, IL, pp. 765 766. Pearson, D.L. and A. P. Vogler. 2001. Tiger Beetles: The Evolution, Ecology, and Diversity of the Cicindelids. Cornell University Press, New York. Rodrguez, R.L. 1998. Mating behavior of two Pseudoxychila beetles (Coleoptera: Cicindelidae). Can Entomol. 130:735 750. --------. 2000. Spermatophore transfer and ejection in the beetle Pseudoxychila tarsalis (Coleoptera: Cicindelidae). J. Kans. Entomol. Soc. 72:1 9. Rodstrom, R.A. 1998. Mating Behavior of the Tiger Beetle, Pseudoxychila tarsalis (Cicindelidae). CIEE Fall, T ropical Ecology and Conservation. Shivashankar, T. and D.L. Pearson. 1994. A Comparison of Mate Guarding Among Five Syntopic Tiger Beetle Species from Peninsular India (Coleoptera: Cicindelidae). Biotropica 26(4): 436 442. Thornhill, R. 1979. Male and Female Sexual Selection and the Evolution of Mating Strategies in Insects. In: Sexual Selection and Reproductive Competition in Insects, M.S. Blum and N.A. Blum, ed. Academic Press, New York, NY, p. 84.
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Efectos de la competencia sobre los comportamientos de copulacin en Pseudoxychila tarsalis (Coleoptera: Cicindelidae)
Effects of competition on copulatory behaviors in Pseudoxychila tarsalis (Coleoptera: Cicindelidae)
This study examines the effects of competition on copulatory behaviors of the tiger beetle Pseudoxychila tarsalis. I tested the hypothesis that copulatory behavior of a P. tarsalis mating pair in the presence of an additional male would induce significant behavioral changes, including longer amplexus time and increased frequency of a variety of copulatory behaviors. Trials were conducted with either one male and one
female, or two males and one female, and the behaviors of one copulatory amplexus recorded per trial. No statistical differences were found for the male behaviors of time until mount, amplexus duration, or number of intromissions, but means tended to decline in each for the two-male trials. Rocking and tapping behaviors in males decreased significantly in the presence of a second male, indicating a response to competition. The general downward trend in the two-male trials may be explained by interruption of
copulatory behaviors by the non-copulating male. Female batting showed a slight but not significant increase in the presence of a second male, which may be intended as a deterrent so that she may gain access to the second male.
Este estudio examina los efectos de la competencia en comportamientos de copulacin en el escarabajo tigre, Pseudoxychila tarsalis. Prob la hiptesis que las conductas de una pareja de P. tarsalis en la presencia de otro macho inducira cambios conductistas significativos de comportamientos, inclusive tiempo ms largo de amplexo y aumentos en la frecuencia de una variedad de comportamientos de copulacin. Las pruebas se realizaron con un macho y una hembra, o dos machos y una hembra, y los comportamientos durante el amplexo se registraron por cada prueba. No se encontraron diferencias estadsticas en los comportamientos masculinos de tiempo hasta la monta, la duracin de amplexo, ni el nmero de copulaciones, pero las tendencias bajan en las pruebas con dos machos. Los comportamientos de mecer y golpear bajan apreciablemente en la presencia de un segundo macho, lo que indica una respuesta a la competencia. La tendencia decreciente en las pruebas con dos machos puede ser explicada por la interrupcin de conductas de sexualidad por el macho no copulatorio. El golpeteo de la hembra mostr un leve aumento, pero no fue significativo, en la presencia de un segundo macho, que posiblemente puede ser dirigido como impedimento de tal manera que ella pueda tener acceso al segundo macho.
Text in English.
Courtship in animals
Costa Rica--Puntarenas--Monteverde Zone
Apareamiento en animales
Costa Rica--Puntarenas--Zona de Monteverde
Tropical Ecology Fall 2004
Ecologa Tropical Otoo 2004
t Monteverde Institute : Tropical Ecology