Sexual Behavior and the Enlarged Hind Legs of Male armatus (Coleoptera, Chrysomelidae, Megalopodinae) Author(s): William G. Eberhard and Mary Carmen Marin Source: Journal of the Kansas Entomological Society, Vol. 69, No. 1 (Jan., 1996), pp. 1-8 Published by: Allen Press on behalf of Kansas (Central States) Entomological Society Stable URL: http://www.jstor.org/stable/25085643 . Accessed: 08/09/2011 20:07

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http://www.jstor.org JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY 69(1), 1996, pp. 1-8

Sexual Behavior and the Enlarged Hind Legs of Male Megalopus armatus (Cole?ptera, Chrysomelidae, Megalopodinae)

William G. Eberhard12 and Mary Carmen Marin2 1 Smithsonian Tropical Research Institute 2 Escuela de Biolog?a, Universidad de Costa Rica, Ciudad Universitaria, Costa Rica

abstract: Behavioral observations indicate the giant hind legs of male Magalopus ar matus function as weapons in battles between males over sites where feeding and mating occur; they are not used to court females. Males court females actively during copulation.

When male and female morphology show clear differences, it is reasonable to suspect that the sexually dimorphic male characters have evolved under sexual selection (Darwin, 1872). It is not so easy, however, to deduce whether a given male character has been under sexual selection by female choice, or by direct male combat. Given characters can, in fact, be under both types of selection. A first step in deciphering the function of a sexually dimorphic male structure is to observe the 's behavior. If, for example, the structure is displayed prominently during male-female interactions in a way likely to increase the fem ale's perception of it, the male trait may play a role in sexual selection by female choice. If the structure is employed in aggressive interactions between males in a as to a such way apparently increase male's chances of defeating rival males, then a role in sexual selection by male combat is indicated. Males of the chrysomelid Megalopus armatus Lacordaire have giant hind legs, with large spines on the femur and a curved tibia. This brief study indicates that these legs are used as weapons in fights between males over mating sites, and are probably not used in the context of female choice.

Materials and Methods

Megalopus armatus beetles were observed on 1 and 4 June, 1994 in the field on a Solanum sp. near americanum (Solanaceae) plant near the edge of the Rio Agres, about 2.5 km S of San Antonio de Escazu, San Jose Province, Costa Rica (el. about 1450 m). Four matings and four aggressive interactions were videotaped in the field using a Sony Hi8 camcorder with closeup lenses at 30 images/sec. An additional nine matings (one recorded with a National Omnipro camera, also with closeup lenses) and nine aggressive interactions (all recorded) between bee tles collected at about 1500 m on a second species of Solanum were observed in captivity. Feeding, mating (seven more times), and fighting were also observed in captivity under a dissecting microscope on 5 June, when an additional mating was taped. All drawings were traced from videotaped images. Voucher specimens are de posited in the Museum of Comparative Zoology, Harvard University, and the Museo de Entomolog?a of the Universidad de Costa Rica.

Accepted for publication 25 August 1995. 2 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Results

Feeding

All of the approximately ten beetles seen on the Solanum sp. near americanum plant 1 June, and the nine beetles seen on 4 June were resting near the tips of shoots which had been broken or chewed off. In every case the beetle was facing the tip. When disturbed by a movement nearby, the beetle quickly swung sideways on the stem so as to place the stem between itself and the object which had moved. Each of the four females was accompanied by a male. The females were all near the tip of a broken shoot, at the basal edge of a portion which had apparently been chewed and where there were many small masses of plant tissue, while the male was just behind the female (Fig. 1 ). Observations in captivity confirmed that both male and female beetles produced this type of damage to plants by chewing on them. Under the microscope a feeding female repeatedly bit the shoot or (more often) a piece of plant tissue which had already been loosened. Just as the beetle seized the plant tissue, an area of the plant very near the beetle's mouthparts became appreciably wetter for a moment, and then immediately drier; it then remained this way for the approx imately 1-2 sec until the beetle released her hold. The beetle usually seized the plant again immediately in a slightly different place. In a pair observed for about an hour in the field, the male repeatedly fed briefly at the tip of the stem. The male moved forward and onto the side of the stem opposite the female, executed low level aggressive behavior such as one or more ventral leg swings (see below); the female (sometimes after a few swings of her own) backed 1-2 body lengths down the stem, and the male moved to the dorsal side of the tip and began to feed. Within 1-5 min the female moved forward again on the opposite side of the stem from the male, jerked her body and swung her hind legs, and the male backed down the stem, allowing her to resume feeding.

Courtship and copulation

Males and females copulated repeatedly. In two pairs which were observed for 1?1.5 hrs in the field, the male mated, moved back behind the female for up to 30 min, then moved forward and mated again. One pair mated three times in about 90 min. All observations in captivity and in the field were consistent with the following sequence of events. The male approached the female slowly from the rear, raised his anterior end slightly from the stalk, and lunged forward quickly to mount the female (Fig. 1). In at least some cases the male jerked his body several times and stridulated in the period just prior to mounting. With no preliminaries other than perhaps brief contact with his mouthparts against her elytra, the male flexed the tip of his abdomen ventrally and anteriorly until it encountered the female's abdomen. In two cases it was clear that the tip of the male's genitalia first contacted the female's pygidium, and then slid smoothly to its tip, and the male then inserted his geni talia. In no case was there any sign of resistance to intromission by the female. During the first portion of copulation the male repeatedly made sharp jerking movements of his body forward and dorsally (Fig. 2), but was otherwise quiet. Each jerk was accompanied by a small ventral movement of the male's antennae which never brought them into contact with the female (Fig. 2). In captivity body VOLUME 69, NUMBER 1

Fig. 1. A male Macropus armatus mounts a female with little or no preliminary courtship. After slowly moving about one half body length closer to the female from behind, he raised the anterior portion of his body (top), lunged forward (middle?0.07 sec after previous drawing), and mounted her (bottom?0.40 sec after previous drawing). Within 10 sec after the bottom drawing the male inserted his genitalia in the female. 4 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Body jerks

intromission intromission begins ends

J_L

intromission begins intromission ends

2 min. Mouthparts tap |

Taps with mouthparts

i_4 sec.

Fig. 2. A male Macropus armatus jerks his body forward and dorsally and lowers his antennae while copulating with the female (dotted lines indicate position 0.07 sec after solid lines). The pattern of body jerks and tapping with the mouthparts during two different copulations of the same pair are shown in the graphs in the middle (each vertical line is a body jerk). The bottom graph shows the pattern of taps with the maxillary palps during a period of mouthpart tapping.

jerks were accompanied by stridulation (the noise of a nearby stream precluded observation of stridulation in the field). Toward the end of this first period of the move copulation male's mouthparts began to actively. During the second portion of copulation, the male leaned ventrally to bring his mouthparts into rhythmic contact with the female's elytra, and continued to jerk his body periodically (Fig. 2). Observation of mating pairs under a dissecting VOLUME 69, NUMBER 1 5

microscope showed that tapping with the mouthparts involved stereotyped, rhyth mic ventro-lateral extensions of the male's maxillae. With each extension the tips of the maxillary palps made a single, brief tapping contact with the female's elytra or the setae on their dorsal surfaces. Each cycle lasted about 0.5-1.0 sec (deter mined from video records of two pairs, one in the field, one in captivity). Most of the tapping movement was produced by movements of the mouthparts them selves, but sometimes the male's head also moved ventrally with each tap. The labial palps also tapped the female's elytra. In one pair under the microscope it was clear that the labial palps moved synchronously in a ventro-anterior direction to tap almost immediately after each tap with the maxillary palps. The sites on the elytra touched by the labial palps were just posterior to those tapped by the maxillary palps. The labial palps tapped more rapidly, and contacted the female several times for each tap with the maxillary palps. A large male copulating with a small female tapped near the anterior edge of her elytra, while a small male copulating with a medium-sized female tapped near the middle of her elytra. The temporal pattern of bursts of tapping behavior varied. In some cases the male ceased tapping one or more times, then resumed. In some cases he ceased tapping and raised his head away from the female for the last 10-30 sec of copulation before withdrawing his genitalia. Immediately after copulation the male slowly backed off the female, dragging his mouthparts along her elytra for 1-2 sec. The male and female genitalia made minor rhythmic movements during cop ulation. One type of movement, brief anterior flexions of the tips of both male and female abdomen, seemed to be produced by the female. In one pair observed under the microscope the interstices at the tip of the male were rhythmically filled and drained of tiny amounts of liquid on the order of once/sec, as if the hydrostatic pressure within the female were rhythmically increasing and decreasing. In all five cases in which the female was watched carefully after copulation ended (three were videotaped), she rubbed the tip of her abdomen against the plant within about a minute of the end of copulation. In at least three cases it appeared that a whitish substance emerged from her abdomen and was rubbed mass off at this time. The white then seemed to enter the female again, and then a few seconds later a larger mass emerged and was apparently rubbed off on the plant. One mass was collected from a copulating pair in captivity (unfortunately the copulation was atypical in that the male reinserted his genitalia repeatedly without dismounting). Under the compound scope the mass proved to be amorphic and slightly rubbery, without any sperm. These masses were not feces, which were much larger (about 3 mm long) and spindle-shaped. In one video recording, a powerful jet of liquid emerged from a white mass and squirted horizontally for 1/30 sec or less; this was probably the elimination of waste material (Peiyu and Xingke 1994).

Aggressive behavior

Males and females used their hind legs in several ways in aggressive interac tions. All aggression in the field occurred on stems of the food plant, with both beetles facing the same direction (usually toward the tip). In order of increasing intensity, aggression included the following (females performed the first two types, while males performed all four): 6 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY

Fig. 3. Aggressive interactions between two Macropus armatus males in the field at a feeding site. A) Both males raise their hind legs in a threat display. B) The upper male swings one hind leg ventrally (arrow shows displacement which occurred in the space of 0.03 sec). C) The lower male swings his hind leg ventrally, and it is parried by the hind leg of the upper male. D) The upper male flexes his hind tibia after swinging the leg ventrally, thereby clamping the lower male. The clamp lasted only 0.15 sec, but the smaller male almost immediately abandoned the twig (1.3 sec later) by flying away.

Warning Display: The beetle raised and spread its partially extended, poste riorly directed hind legs (Fig. 3A). Ventral Swing: The beetle briskly swung its partly extended hind legs ven trally (Fig. 3B). Most movement was at the coxatrochanter-femur articulation. Sometimes the beetle swung both legs simultaneously, others only one (Fig. 3B). In captivity each swing was accompanied by vigorous stridulation. When there was another beetle on the other side of the stem, it usually responded to a swing by slipping sideways out of the way, positioning itself on the opposite side of the stem from the swinging beetle. push or spar: The male pushed ventrally with his hind legs while they were in contact with the legs or body of another beetle on the other side of the stem. Some pushing movements appeared to be forceful. These movements were not stereotyped. Probably in some cases the other male used his hind legs to parry a push by his opponent (Fig. 3C). clamp: In two intense fights a period of sparring culminated when one male seized his opponent's body using the tibia and femur of one of his hind legs as a clamp (Fig. 3D). One clamp lasted 16.27 sec, the other (after a less intense interaction) 0.15 sec. In both cases the opponent ceased struggling soon after being clamped. Both males that had been clamped walked or flew away imme diately with no further aggression. VOLUME 69, NUMBER 1 7

One additional apparently aggressive behavior was body jerking, which oc curred both before and following fights, and was accompanied by stridulation in captivity. When the mouthparts of a male and a female were detached and mounted on no a slide and then examined with a compound microscope, obvious sexual di morphism was noted.

Discussion

The enlarged hind legs of male M. armatus played no apparent role in male female interactions immediately before or during copulation. There was, in fact, often little or no apparent courtship prior to copulation. Females showed no sign of resistance to copulation attempts, and copulated readily with both the smallest = male (body length 9 mm) and the largest male (body length =15 mm) seen. In contrast, the hind legs of males played a variety of prominent roles during aggressive interactions. They were used to perform both apparent threats, and physical attacks. Their giant size facilitated both forceful pushing and clamping. Clamping was the most forceful aggressive behavior, and a strong clamp appeared capable of resolving a fight over a feeding and mating site in a male's favor. Enlarged hind legs are also used as weapons in the coreid bug Acanthocephala femorata and the zoropteran Zorotypus gurneyi, though in a slightly different manners (Mitchell, 1980; Choe, 1994). As is true in many other species of and spiders (Eberhard, 1991; 1994), male M. armatus perform stereotyped behavior during copulation that appears designed to stimulate the female (copulatory courtship). The tapping movements of the male mouthparts occurred consistently and were of similar form in every copulation observed. Presumably they function to induce the female to perform some process (ovulate, allow the male's genitalia to penetrate more deeply, refrain - from discarding his sperm, transport sperm, etc. see Eberhard, 1991; 1994). soon Females of this species may sometimes emit sperm after copulation ends, as occurs in some other chrysomelid beetles (Rodriguez 1994; Eberhard, 1994), as well as in other beetles (Rodriguez and Eberhard, in prep.), but our observa were on tions unfortunately inconclusive this point. All aggressive interactions occurred at feeding sites at the tips of chewed-off twigs. The losing beetle always left that branch of the plant. Females both feed and copulate at these sites. There were more chewed-off branches than there were on near beetles the Solanum sp. americanum plant in the field. Some appeared to have been chewed off more recently, however, so it is possible that some sites were more attractive or better food sources than others. Stridulating beetles produced a variety of chirps, squeaks, and chittering sounds. Sounds were produced by very rapid, almost imperceptible anterior-posterior movements of the pronotum over the finely striated mesonotum. These move ments were too subtle to be resolved with confidence in many of the video records. Both males and females produced sounds. Relatively loud chirps occurred during body jerks in brief aggressive interactions between males in captivity, and when a beetle was grasped with a forceps. Stridulation also occurred in other situations; for instance a feeding female made nearly continuous chittering sounds without any body jerks while at the tip of a branch, accompanied by a male. It appears that the beetles feed at least partly by sucking on plant juices. The 8 JOURNAL OF THE KANSAS ENTOMOLOGICAL SOCIETY apparent wetting of plant material near their mouthparts may imply that they dissolve plant tissues extra-orally; alternatively, the brief wetting may have oc curred as as result of the beetle's mouthparts exerting pressure on the plant. Use of liquid food is in accord with the relatively thin, pointed form of the mandibles, and also agrees with observation of sap feeding by other megalopodine species (Peiyu and Xingke, 1994). The solid fecal pellets indicate that the beetles also ingest some solid material. Perhaps the bright, apparently aposematic colors of these beetles (black, white, and yellow, with the orange dorsum of the abdomen exposed in flight) is explained by their acquiring defensive compounds from their host plants. Several observations of M. armatus can be compared with published accounts of other megalopodines. The lack of pre-mounting courtship contrasts with Aga thomerus sellatus, in which the beetle vibrates his body and moves his body dorsally (jer^s?) (dos Santos, 1981). Copulation was much shorter than in A. - sellatus (which averaged 86 min dos Santos, 1981) and Temnaspis nankinea ... ("several minutes up to more than an hour") (Peiyu and Xingke, 1994). mate once Females more than in all three of these species. Males of T. nankinea also stridulate with the same mechanism (Peiyu and Xingke, 1994).

Acknowledgments Jorge Gomez L. kindly identified the plants, and David Furth the beetles. We received financial support from the Smithsonian Tropical Research Institute and the Vicerrector?a de Investigation of the Universidad de Costa Rica.

Literature Cited

Choe, J. 1994. Sexual selection and mating system in Zorotypus gurneyi Choe (Insecta: Zoraptera): I. Dominance hierarchy and mating success. Behav. Ecol. Sociobiol. 34:87-93. Darwin, C. 1871. The Descent of Man and Selection in Relation to Sex (reprinted). Random House, New York. dos Santos, H. R. 1981. Biologia de Agathomerus sellatus (Germar, 1824) (Cole?ptera, Chrysomel idae, Megalopodinae) broca do tomateiro. Rev. Bras. Entomol. 25:165-170. Eberhard, W. G. 1991. Copulatory courtship and cryptic female choice in insects. Biol. Rev. 66:1-31. 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. Mitchell, R L. 1980. Combat and territorial defense of Acanthocephala femorata (Hemiptera: Core idae). Ann. Entomol. Soc. Am. 73:404-408. Peiyu, Y, and Y Xingke. 1994. Biological studies on Temnaspis nankinea (Pic) (Chrysomelidae: Megalopodinae). In P. H. Jolivet, M. L. Cox and E. Petitpierre (eds.), Novel Aspects of the Biology of Chrysomelidae, pp. 527-531. Kluwer Academic, The Netherlands. Rodriguez, V. 1994. Function of the spermathecal muscle in Chelymorpha alternans Boheman (Co le?ptera: Chrysomelidae: Cassidinae). Physiol. Entomol. 19:198-202. Rodriguez, R. L., and Eberhard, W. G. in prep. Mating behavior of two species of Pseudoxychila beetles (Cole?ptera: Cicindellidae).