Insectes soc. 47 (2000) 84–91 0020-1812/00/010084-08 $ 1.50+0.20/0 © Birkhäuser Verlag, Basel, 2000
Insectes Sociaux
Research article
Colony foundation and acquisition of coccoid trophobionts by Aphomomyrmex afer (Formicinae): co-dispersal of queens and phoretic mealybugs in an ant-plant-homopteran mutualism? L. Gaume 1, 2, D. Matile-Ferrero 3 and D. McKey 1, 2 1
2
3
Institut des Sciences de l’Evolution, Université Montpellier II, Place Eugène Bataillon, F-34095 Montpellier, France, e-mail:
[email protected] CEFE (Centre d’Ecologie Fonctionnelle et Evolutive) – CNRS, 1919 route de Mende, F-34293 Montpellier cedex 5, France, e-mail:
[email protected] Laboratoire d’Entomologie, Museum National d’Histoire Naturelle, 45, rue de Buffon, F-75005 Paris, France, e-mail:
[email protected]
Received 25 January 1999; revised 21 August 1999; accepted 8 September 1999.
Summary. In coastal forests of Cameroon, colonies of the ant Aphomomyrmex afer are found in hollowed twigs of two species of trees, most commonly the myrmecophyte Leonardoxa africana T3. Established colonies of this ant are always associated with coccoid homopterans (the pseudococcid Paraputo anomala or the coccid Houardia abdita, or both) within hollow twigs, and ants appear to be dependent on these sap-sucking trophobionts. We dissected domatia of juvenile host-plants that had not yet acquired an established colony to determine (1) how colonies are founded, and (2) when and how trophobionts are acquired. Colony foundation is claustral. A single queen chews an entrance hole into an unoccupied domatium that serves as the founding chamber. The entrance hole is partially closed by debris and later by callus growth. Nineteen foundresses were located while still in the claustral phase, with no workers or a few nanitic workers. Of the 19 foundresses, 12 had at least a single Paraputo anomala individual in the same domatium. One of the queens had two female P. anomala nymphs attached to her body. The remaining 7 foundresses were not associated with coccoids. These results indicate that mealybug and ant may codisperse by phoresis of juvenile female mealybugs on founding queens. Association with mealybugs should provide foundresses with a food source during claustral foundation. The coccid Houardia does not seem to co-disperse with ants, and foundresses originating from adult colonies that tend only coccids must acquire trophobionts later. Key words: Ant-plant-homopteran mutualisms, trophobionts, colony foundation, co-dispersal, phoresis.
Introduction Specialised relationships between myrmecophytes and plant-ants in tropical ecosystems are often mediated by homopterans, especially sap-sucking coccoids (Davidson and McKey, 1993). These include both soft scales (Coccidae) and mealybugs (Pseudococcidae) tended by ants inside specialised hollowed structures of myrmecophytes, the domatia. Most of these tripartite ant-plant-homopteran relationships are mutualisms, in which each partner obtains a net benefit. Benefits for ants are quite evident: the plant provides nest sites and food resources, either directly through extrafloral nectaries or specialised food bodies or indirectly via the homopterans. Homopterans are tended by ants mostly for their honeydew and exceptionally as direct food resources (Way, 1963; Sakata, 1994). Homopterans benefit by having exclusive access to the host’s sap in sheltered sites protected from predation (Buckley, 1987; Gullan, 1997). The main advantage for the plant is protection provided by ants against herbivores, against competing plants (reviewed by Beattie, 1985; Davidson and McKey, 1993), or even against fungi (Letourneau, 1998). Associations between the different partners vary in their species richness and degree of specificity. One or several species of homopteran may be found in an individual hostplant (Heckroth et al., 1998; Gaume et al., 1998). Homopterans may also have several host-plants or may be confined to just one species of myrmecophyte. They may be tended by several species of ants or associated with only one species upon which they are completely dependent (Gullan and Kosztarab, 1997).
Insectes soc. Vol. 47, 2000
Specialised mutualisms between ants and their homopteran trophobionts may involve extensive coadaptations. For myrmecophilous homopterans, these include behavioural and morphological modifications as well as modification of the life-cycle (Way, 1963; Williams, 1978; Gullan, 1997). For the ants, primarily behavioural modifications are involved. For example, a small number of ants have been reported to carry their mealybug trophobionts (reviewed by Hölldobler and Wilson, 1990). These include workers which transport symbionts to the appropriate parts of the food plant (Way, 1954) or which carry phoretic symbionts on their backs to new nest sites (for nomad species, see Reyne, 1954; Williams, 1978; Maschwitz and Hänel, 1985; Dill and Maschwitz, 1994). In other cases, founding queens carry their mealybug symbionts in their mandibles during the nuptial flight and colony foundation, thus establishing a honeydew source for the newly founded nest (Gullan, 1997; Williams, 1998). Recorded cases of transport of homopterans by founding queens are from south-east Asia, concerning the genera Acropyga (Formicinae: Plagiolepidini) (Bünzli, 1935; Brown, 1945; Williams, 1998) and Tetraponera (Pseudomyrmecinae) (Klein et al., 1992); from South America, concerning the genus Rhizomyrma (Flanders, 1957); and from Europe (Buschinger et al., 1987). The ant in this last example was originally thought to be a species of Plagiolepis but is now identified as Acropyga nearctica (Hölldobler and Wilson, 1990). An additional south-east Asian record concerns a formicine ant recorded by Roepke (1930) as Cladomyrma sp., but Reyne (1965) examined this specimen and reported this to be a misidentification of an Acropyga (Atopodon) sp. queen. In all these cases, the homopterans involved are mealybugs (Pseudococcidae), which appear to be the coccoids having morphological adaptations best suited to this type of transport (Williams, 1978; Gullan, 1997). The associate of Rhizomyrma (Eumyrmococcus smithii) reported by Flanders (1957) is a mealybug of the subfamily Rhizoecinae (Williams, 1978). Although suspected in some plant-ants (Stout, 1979; Schremmer, 1984), transport of homopteran trophobionts by founding queens of plant-specialist ants has only been confirmed once, by Klein et al. (1992) in a bamboo-dwelling Tetraponera species. An explanation offered for the rarity of such behaviour in plant-ants is that queens of myrmecophyte-nesting ants need unencumbered mandibles to chew into plant tissue (Gullan et al., 1993). However, in view of the very risky period of dispersal and foundation (McKey, 1988), caused in part by low availability of food resources during foundation, which is usually claustral, the transport of trophobionts by foundresses might still be expected to occur more frequently in plant-ants than current literature suggests. In this manuscript, we describe colony foundation by a plant-ant that is associated with two species of homopterans, and whose establishment and reproduction are dependent on these trophobionts. We present preliminary evidence for codispersal of founding queens and one of these homopteran trophobionts, a mealybug. If our results are confirmed by
Research article
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other field observations, this would be the second recorded case of co-dispersal of foundresses and trophobionts in a plant-specialist ant, and the first record worldwide of phoresis of mealybugs on ant foundresses. Materials and methods Aphomomyrmex afer Emery (Formicinae, Myrmelachistini) is a plantant associated with the forest-understorey myrmecophyte Leonardoxa africana T3 (Leguminosae, Caesalpinioideae) in Cameroon (McKey, 1991; Gaume and McKey, 1998). The plant possesses swollen hollowed internodes, the domatia, that shelter ants. Each domatium is a discrete cavity extending over 1 – 3 internodes, separated from others by a woody septum, and each domatium has at least one entrance hole. Once a domatium is produced, the volume of the cavity does not change; the wall merely thickens with secondary growth. While small trees of L. africana T3 are occupied by other species of ants, Aphomomyrmex occupies most of the trees over 1m tall and is the exclusive occupant of all trees taller than 7m (n = 116 trees, Gaume and McKey, 1998). Aphomomyrmex tends two kinds of homopterans inside the domatia of the host-plant: a coccid (Houardia abdita De Lotto) and/or a pseudococcid (Paraputo anomala Newstead). Of 21 entirely dissected trees (ranging in height from 1.6 m to 8 m) whose ant and homopteran colonies were also completely counted), 11 were found with the coccid as sole (4 trees) or dominant trophobionts (7 trees), while the remainder (10 trees) were found with pseudococcids as the sole trophobiont (Gaume et al., 1998). Such homopterans are necessary partners of Aphomomyrmex in Leonardoxa africana T3. None of the numerous colonies we have studied (even incipient colonies beyond the stage of foundation) lack such partners. Paraputo anomala is oval to heart-shaped and has a white to grey body covered with white wax. Adult females may be up to 4.5 mm long. Individuals of this species possess developed legs in all stages, adult female included (Fig. 1, 2). Houardia abdita has a flat-topped redcoloured body. Adult females are up to 3mm long. Second and all succeeding nymphal instars, as well as adult females, are legless (Fig. 3), while the first instar nymph has developed legs (Fig. 4). Neither P. anomala nor H. abdita is host-specific. Both species are exclusively afrotropical. Paraputo anomala is a polyphagous species known from several countries in tropical Africa (Ben-Dov, 1994). It is also known to live with ants under bark (Williams, 1958). Houardia abdita is a rarely collected species, hitherto known only from South Africa and Zimbabwe, where it has been found living in galleries (probably made by woodboring insects) in stems of Burkea africana and B. spiciformis (Leguminosae) (Hodgson, 1990; Ben-Dov, 1993). Aphomomyrmex afer also has another host-plant, Vitex grandifolia (Verbenaceae) (McKey, 1991), but in our study site Leonardoxa is by far the more frequent host (Meunier et al., 1999). The relationship between L. africana T3 and Aphomomyrmex afer is globally a protective mutualism (Gaume and McKey, 1998), but the identity of the homopteran partner affects the outcome of the interaction. It has been demonstrated to be a strong protective mutualism when the ants tend pseudococcids, but benefits to the plant are lower, and costs to the plant appear to be higher, when the ants tend coccids (Gaume et al., 1998). The studied trees and their occupant colonies were taken from a population of Leonardoxa africana T3 in Korup National Park (Southwest Province of Cameroon, latitude 5° 00’ N, longitude 8° 05¢ E). A total of 116 trees were checked for identity of their ant-occupant by partially opening one (when the tree obviously was host to a large established colony of A. afer) to several domatia (when no large colony fully occupied the tree). Inside such studied domatia, we sometimes found by chance foundress queens of Aphomomyrmex. When a partially opened domatium contained a foundress, we quickly closed it shut and put each domatium separately into a vial containing ethanol to kill the occupants. For each such foundress encountered, we recorded whether the domatium contained a queen alone (with or without brood)
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L. Gaume et al.
Trophobionts and colony foundation by Aphomomyrmex
Results Evidence for claustral foundation Founding queens of Aphomomyrmex chewed their entrance holes at the prostoma. This is a highly localised, unlignified spot on the domatium wall, specialised to facilitate entry of suitably adapted ants. Sometimes (two domatia), the hole was partially blocked by debris, presumably deposited by the foundress, and the margins of the holes of all domatia bore wound callus that had begun to narrow the entrance. As a result, entrances of these domatia had become too narrow to permit passage of a queen. This indicates that the queen, once entered inside the domatium, does not leave it. This “closing” behaviour is characteristic of claustral colony foundation. Not only does the queen remain within the domatium throughout foundation, it appears that she may remain within this domatium throughout her life. Indeed, although almost all the founding queens we recorded were found within young domatia, the strongly physogastric queens of old established colonies were found mostly in domatia in the trunk or old branches (Multiple Fisher’s exact test [see Raymond and Rousset, 1995]: p
