C 2005) Journal of Insect Behavior, Vol. 18, No. 1, January 2005 ( DOI: 10.1007/s10905-005-9343-y
Behavioural Interactions Between Crematogaster brevispinosa rochai Forel (Hymenoptera: Formicidae) and Two Nasutitermes Species (Isoptera: Termitidae) Y. Quinet,1,3 N. Tekule,2 and J. C. de Biseau2 Accepted March 17, 2004; revised July 27, 2004
In the savanna-like Brazilian biome “caatinga,” the arboreal and polydomous ant Crematogaster brevispinosa rochai can be found cohabiting with two closely related Nasutitermes species (N. corniger and N. ephratae). This ant occupies variably sized portions of the termite nests and maintains a physical separation with its hosts by plugging the cells of the boundary areas with fibrous material. Although all the analysed cohabiting C. b. rochai nests were queenless, they always contained brood, especially from male and female reproductive castes. Interaction experiments between workers of C. b. rochai and workers or soldiers of N. ephratae revealed a low level of aggressiveness between the two species that contrasts with the aggressiveness of both C. b. rochai and N. ephratae in encounters with other ant (Azteca cf. chartifex, Cephalotes pusillus) or termite (M. cf. indistinctus) species. The association could benefit both ants (additional nesting sites, brood rearing places) and termites (protection against predators, dead ants or ant refuses as source of nitrogen). KEY WORDS: ant-termite interactions; Formicidae; Isoptera; Crematogaster brevispinosa rochai; Nasutitermes.
1Laboratorio ´
´ Fortaleza-Ceara, ´ Brazil. de Entomologia, Universidade Estadual do Ceara, ´ ´ d’Eco-ethologie evolutive, Universite´ Libre de Bruxelles, Brussels, Belgium. 3To whom correspondence should be addressed. e-mail:
[email protected] 2Service
1 C 2005 Springer Science+Business Media, Inc. 0892-7553/05/0100-0001/0
2
Quinet, Tekule, and de Biseau
INTRODUCTION Ants (Hymenoptera: Formicidae) and termites (Isoptera), with about 11,000 and 2,600 described species, respectively (Bolton, 1995a,b; Kambhampati and Eggleton, 2000), are two ecologically dominant groups in terrestrial ecosystems, particularly in tropical regions where they ¨ show their highest level of diversification (Holldobler and Wilson, 1990; Eggleton, 2000). The interactions that exist between the two groups are a well-known fact and are almost always described as agonistic ones, ants being considered as the main enemies and predators of termites (Bugnion, 1927; ¨ Wheeler, 1936; Wilson, 1971; Deligne et al., 1981; Holldobler and Wilson, 1990). However, although many ant species occasionally prey on termites (during the termites’ nuptial flights or after an accidental breaking of the termite nest for example), there are few ant species specialized in termite predation. The best known example is the African ponerine Megaponera foetens that forms columns of 200–500 workers to attack foraging workers of various termite species of the Macrotermitinae subfamily (Wheeler, 1936; Sheppe, 1970; Longhurst et al., 1978; Lepage, 1981). The African myrmicine Decamorium uelense that attacks primarily termites of the Microtermes genus is another example (Longhurst et al., 1979). Predation is also observed in ant species whose colonies settle in portions of termite nests and whose workers, generally small and blind, steal the eggs of their hosts and even attack the nymphs and adults. Several species of the Solenopsis, Carebara, Centromyrmex and Hypoponera genera provide examples of this parasitic/predatory relationship with their termite hosts (Wheeler, 1936; ¨ Lemaire et al., 1986; Holldobler and Wilson, 1990; Delabie, 1995; Dejean ´ eron, ´ and Fen 1999). In all these cases, however, the impact of the predation is low with regard to the biomass of the termite nests (0.537 termites/m2 /day in the case of Megaponera foetens) and does not represent a danger for mature nests (Darlington, 1985; Lepage, 1981). According to some authors, predation is only one aspect, generally overestimated, of the ecological interactions between ants and termites, that have developed more varied relations (Sennepin, 1996). Nearly 200 ant species were recorded by Wheeler (1936) as temporarily or permanently cohabitating with its host termites, without exerting any predation. Generally, the cohabitating species occupy distinct portions of termite nests and show varied degrees of tolerance towards each other, although in most cases, little is known about the exact nature of the relations between the ants and their termite hosts. The inverse cohabitation, i.e. termites that occupy parts of ant nests, has also been described, although this kind of interaction is less known
Behavioural Interactions Between Crematogaster b. rochai and Nasutitermes spp.
3
(Wheeler, 1936, Gray, 1974; Sennepin, 1999; Shelton et al., 1999). The total integration of ants and termites to form true mixed colonies is known in only one case, the Australian formicine Stigmacros termitoxenus that lives in nests of the termite Nasutitermes peracutus (Wheeler, 1936). In some cases, the cohabitation can take the form of a true mutualism. Higashi and Ito (1989) showed that the different ant species that live in the nests of Amitermes laurensis (Termitidae) actively defend them against invasions of the ant Iridomyrmex sanguineus and that the termite nests with ant guests better withstand the attacks of I. sanguineus. Some benefit with respect to the food supply was also observed. This was shown with the termite Nasutitermes corniger that benefits from cohabiting ants by feeding on dead ants and ant middens, thereby increasing their nitrogen pool in an environment otherwise relatively poor in nitrogen containing compounds (Jaffe et al., 1995). According to the authors, the association could represent an incipient form of facultative or opportunistic mutualism. In the present work, we investigated the cohabitation and the behavioural interactions between two closely related arboreal neotropical species of Nasutitermes (N. corniger and N. ephratae) (Termitidae: Nasutiterminae) and the myrmicine Crematogaster brevispinosa rochai Forel, which is found living within the nest of either of the termite species. Crematogaster is the fourth biggest ant genus, with 427 described species and a world-wide distribution, although most of the species live in tropical regions (Bolton, 1995a,b). In tropical ant communities, many Cre´ 1960; de Marneffe, 1999; Richard matogaster species are dominant (Soulie, et al., 2001), and may even constitute a limiting factor for arboreal termite assemblages (Leponce et al., 1999). C. brevispinosa rochai is an arboreal species typical of the savanna-like Brazilian ecosystem (“caatinga”) that covers most of the Ceara state territory. It forms large polydomous, probably monogynous, colonies that are generally formed by one or more principal nest(s) and several smaller ones (de Marneffe, 1999; Longino, 2003). The nests of a single colony can occupy several trees where the workers tend homopterous colonies and from which all competitors are excluded, with columns of workers patrolling the trees day and night and moving between the nests (de Marneffe, 1999). As it is the rule in the genus, the venom is produced in the Dufour’s gland and is applied topically on the enemies’ body with a spatulate sting. In C. b. rochai, the main compounds of the venom were found to be unusual furanocembrenoid diterpenes (Leclercq et al., 2000). Nasutitermes is a dominant element of the “caatinga” where arboreal nests of some species can reach impressive dimensions (some nests can reach up to 1 m in length and 0.6 m in diameter, personal observation). The characteristic feature of the genus is the defensive system of the soldiers.
4
Quinet, Tekule, and de Biseau
They possess a pear-shaped head from which they can project a sticky defensive secretion produced by the frontal gland and consisting primarily of light monoterpenes and heavier diterpenes (Braekman et al., 1983; Noirot and Darlington, 2000).
MATERIAL AND METHODS Analysis of Compound Termite Nests Eight Nasutitermes nests of two closely related species (6 nests of N. corniger and 2 nests of N. ephratae), were collected at Pentecoste (state of ´ Ceara—Brazil), in December 2000 (end of the dry season), in trees where foraging activity of both C. brevispinosa rochai and Nasutitermes corniger (or N. ephratae) was verified. N. corniger and N. ephratae are very similar species, whose soldiers and workers are difficult to distinguish from each other (Constantino, personnal communication), with apparently identical defensive behaviours and internal nest architecture. All the collected nests were made of carton, had a nearly ovoid shape, with height varying from 35 to 40 cm and a maximum circumference of 85 to 110 cm, and were attached to branches of small trees, at a height of 1–2 m. Nest removal from the tree was made by gently sawing the branch(es) that sustained it, in order to cause the smallest possible disturbance of the nest inhabitants. Immediately after its removal, the nest was placed in a plastic bag with a cotton ball moistened with ether, whereafter the air was removed from the bag with an air pump, before closing it with a string. This procedure aimed at killing the nest inhabitants as quickly as possible, in order to fix their spatial distribution. In the laboratory, the nests were kept in a freezer until analysed. Each nest was cut into 2–4 cm thick slices with a fine saw, beginning from the superior pole and going to the inferior one. After the removal of a slice, the exposed area of the nest was scanned for posterior image analysis of the ants and/or termites distribution within the nest. Before it was scanned, each area was carefully examined, marking the boundaries of the zones occupied by the ants or the termites with white paint and annoting any relevant feature of the occupied zones.
Interactions Between Ants and Termites The experiments were all realised with laboratory ant and termite nests. Ten C. brevispinosa rochai colonies were collected at Pentecoste
Behavioural Interactions Between Crematogaster b. rochai and Nasutitermes spp.
5
and placed each in a round plastic containers (20 cm deep and 30 cm in diameter) with tubes of water and 1 M sucrose solution. Cockroaches or shrimp were given to the colonies once a week. Three Nasutitermes ephratae colonies were collected on the campus of the State University of Ceara´ in Fortaleza, and placed each in a closed tub (28 cm long, 21 cm wide, and 14 cm deep). Each colony was connected by way of a plastic tube to another similar tub with rotting wood as a food source and tubes of water. In order to compare the behavioural interactions between C. b. rochai and N. ephratae with other interspecific situations of interference, two other ant species (Azteca cf. chartifex and Cephalotes pusillus) and another termite species (Microcerotermes cf. indistinctus) were used in the experiments. The colonies (one of A. cf. chartifex, one of C. pusillus, and two of M. cf. indistinctus) were collected on the campus of the State University of Ceara´ and cultured as described above. Those species were chosen so as to allow comparisons with ants characterized by very high or very weak level of aggressiveness, and with termites of a different subfamily. Azteca cf. chartifex. (Dolichoderinae) is a territorial and very aggressive arboreal species with populous colonies whose workers, similar in size to C. b. rochai workers, quickly respond to the slightest disturbance by mass recruitment. Cephalotes pusillus (Myrmicinae) is a polymorphic species with heavily armoured workers, whose relatively small colonies nest in hollow branches. Unlike Azteca cf. chartifex, C. pusillus is a subordinate species which responds to aggression by immobilization, retraction of the antennae in the antennal scrobes, and flattening of the body to the ground, or else by flight. In the interactions experiments, only small workers, with a size roughly similar to that of the C. b. rochai workers (
