Journal of Insect Physiology 50 (2004) 539–546 www.elsevier.com/locate/jinsphys
Factors affecting post-flight behavior in primary reproductives of the Formosan subterranean termite, Coptotermes formosanus (Isoptera: Rhinotermitidae) Yong Ihl Park , John M. Bland, Ashok K. Raina Formosan Subterranean Termite Research Unit, Agricultural Research Service, USDA, SRRC, 1100 Robert E. Lee Boulevard, New Orleans, LA 70124, USA Received 13 November 2003; received in revised form 15 March 2004; accepted 18 March 2004
Abstract After swarming, reproductive dealates of the Formosan subterranean termite, Coptotermes formosanus, run together in tandem. The tandem running is an age-related behavioral activity in C. formosanus. This behavior was not evoked in pre-flight alates less than 6-d-old that were artificially dealated. Female age was more important than male age for evoking tandem behavior. Females and males, older than 35 days, did not exhibit this behavior. Mating status was not important for female and male dealates to form the tandem pairs. The titers of the major tergal gland component, trilinolein, did not decline significantly and remained high, not only in virgin females, but also in mated females for a period of time after swarming. On the other hand, increasing amounts of the female-specific compound trilinolein were detected in male dealates 7, 14, and 42 days after pairing. This suggests that trilinolein in the females might be transferred to the males as a nuptial gift in C. formosanus. In addition, females have structurally different lateral setae that may constitute a morphological factor involved in the tandem behavior in this species. Covering the setae with dimethyl sulfoxide prevented the tandem behavior. Published by Elsevier Ltd. Keywords: Coptotermes formosanus; Tergal glands; Tandem behavior; Trilinolein; Lateral setae
1. Introduction Most subterranean termites are serious pests of wooden structures throughout the world. The Formosan subterranean termite, Coptotermes formosanus, was introduced into the southern states over 50 years ago (Woodson et al., 2001). C. formosanus became a serious urban pest, infesting historical buildings and live trees in New Orleans, Louisiana. Mature colonies of C. formosanus contain several hundred thousand to a few million foraging workers, and because of these large numbers, can do significant structural damage in a very short period (Haverty, 1976). Most of the attention in termite management has focused on foraging workers of mature colonies. However, every year Corresponding author. Tel.: +1-504-286-4297; fax: +1-504-2864235. E-mail address:
[email protected] (Y.I. Park).
0022-1910/$ - see front matter Published by Elsevier Ltd. doi:10.1016/j.jinsphys.2004.03.010
swarming alates have the potential to establish new incipient colonies, giving rise to mature colonies within 5–8 years (Higa, 1981; Huang and Chen, 1984). Swarming season varies depending on location: April to July in China (Wang et al., 2002), April to June and September to October in Florida (Nan-Yao Su, personal communication) and every month in Hawaii (Julian Yates, personal communication). Different termite species showed different swarming characters in dispersing either diurnally or nocturnally and in forming new colonies away from the parent colony (Nutting, 1969). In Louisiana, alates of C. formosanus swarm after sunset from late April to June (King and Spink, 1974). Alates land on the ground, after about a 20–30 min flight to the closest light source, and shed their wings. After dealation, the females lead the males, forming tandem pairs (Raina et al., 2003a). However, dealated females of different termite species are known to exhibit different post-flight behaviors such as calling
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or tandem running, or both. Tandem running was not observed in Cryptotermes havilandi (Wilkinson, 1962; Stuart, 1969), but was present in C. cynocephalus (Stuart, 1970). In some species of termites, both calling and tandem running were observed, e.g. Incisitermes snyderi (Kalotermitidae), Reticulitermes flavipes and R. virginicus (Rhinotermitidae) (unpublished observations). In C. formosanus, dealated females did not call or produce a sex pheromone to attract males, but they showed tandem behavior (Raina et al., 2003a). Earlier work suggested that the sternal gland(s) in different termite species produced sex pheromone to attract dealated males (Buchli, 1960; Stuart, 1969; Wall, 1971; Pasteels, 1972; McDowell and Oloo, 1984; Bordereau et al., 1991; Laduguie et al., 1994) and to form tandem pairs with the female in the lead. In addition, tergal glands in several species of termites have been implicated in post-flight behavior (Noirot, 1969; Ampion and Quennedey, 1981). Bordereau et al. (2002) reported that females of Cornitermes bequarerti released a pheromone from their tergal glands for attracting males during calling. The pheromone was further identified to be the same as the commonly known termite trail pheromone. The tergal glands were first observed by Montalenti (1928) in Kalotermes, and by Barth (1955) in Syntermes dirus. In Kalotermes flavicollis, these glands were reported to be present in both males and females (Noirot, 1969). The location and the number of tergal glands in many different termite species have been described (Noirot, 1969; Ampion and Quennedey, 1981; Cle´ment and Bagne`res, 1998). However, these glands have not been found in several termite species such as Pseudacanthotermes spiniger (Bordereau et al., 1991), Zootermopsis nevadensis (Pasteels, 1972), Reticulitermes lucifugus (Noirot, 1969), R. flavipes and R. virginicus (unpublished observations). In C. formosanus, a pair of tergal glands are found only in females. Recently, Bland et al. (2004) reported that trilinolein was the major component in extracts of tergal glands of this species. The post-flight behaviors in termites are much more complicated than previously suggested. For example, R. flavipes and R. virginicus, with only a sternal gland, showed both calling and tandem behaviors, but C. formosanus with only tergal glands showed only tandem running after dealation. In C. formosanus, Raina et al. (2003a) suggested that the first contact between sexes is accidental and leads to tandem running with the male maintaining constant contact with the posterior region of the female abdomen. Thus, post-flight behaviors in termites appear to be species-specific. We investigated the tandem behavior and possible factors that may influence this behavior in C. formosanus. We also investigated the role of mating and age on titers of trilinolein and that of the female specific lateral setae in post-flight behavior.
2. Materials and methods 2.1. Insects Female and male alates were collected following swarming in New Orleans and Metairie, Louisiana, for three years from 2001 to 2003 during the period from late April to June. The post-flight dealates were immediately sexed, and pairs were kept in 50 9 mm Petri dishes (Falcon, Fisher Scientific, Suwanee, GA) containing 9 ml sawdust–agar mixture (Raina et al., 2003b) and a 4 4 cm piece of southern yellow pine (Pinus taeda) veneer. In addition, either two virgin female dealates or two virgin male dealates were separately kept in diet Petri dishes for future use. Because it is impossible to determine the exact age of alates at swarming, we obtained termite-infested garden ties containing last stage brachypterous nymphs. The nymphs were removed from the ties and kept in an v incubator maintained at 28 1 C, 60% relative humidity and constant darkness. From these, alates of known ages were collected after their final molt. These pre-flight alates did not voluntarily dealate, so the wings were removed by snapping these back with a pair of forceps before use. In one set of experiments, 6-d-old pre-flight females and males obtained from the garden ties were used. Pre-flight virgin females of unknown age, ready for swarming, were directly collected from field nests. All other insects of different ages were obtained from dealated females and males after swarming. Fertilized eggs laid by a female of a pair provided an indication that it had mated. 2.2. Effect of age and mating status on tandem behavior To determine the effect of age on tandem behavior, males and females of specific ages were paired in Petri dishes (50 9 mm) and observed for tandem formation for 30 min. The pairings were: (a) 6-d-old pre-flight virgin males and females after molting from brachypterous nymphs; (b) 6-d-old pre-flight virgin males and
