Four species of Collembola were found in nests of the ant genera Myrmicocrypta, Trachymyrmex and Sericomyrmex of the tribe Attini (Formicidae: Myrmicinae). The panmyrmecophilic collembolan Cyphoderus (Lepidocyrtidae: Cyphoderinae) was the most abundant and was associated with all the ants. The collembolan genus Mucrosomia (Isotomidae: Anurophorinae) was found for the first time in ant nests. This is the first list of springtails found in nests of fungus-growing ants other than those belonging to the genera Atta and Acromyrmex (Formicidae: Myrmicinae).
Fungus-growing ants (Formicidae: Myrmicinae: Attini) are distributed exclusively in the New World, with more than 230 species described. They are obligately dependent on the fungi they grow, though displaying great variation in their ecology (Mehdiabadi & Schultz 2010). Conditions in the nests of fungus-growing ants are extremely stable in time and space, and nests possess considerable resources that are available for the diverse fauna associated with such ants (Kistner 1982; Waller & Moser 1990; Hughes et al. 2008). Most genera, previously considered to be the “lower” attines in an earlier system of classification (before Ward et al. 2015), form small colonies with fewer than 3,000 workers. In contrast, the species of the related genus Atta form very large colonies that can include several million workers (Hölldobler & Wilson 1990). Most research on the fauna associated with fungus-growing ant nests has been focused on the genera Atta and Acromyrmex, particularly on some groups of inquilines such as Coleoptera and Araneae (Cushing 1997; Vazde-Mello et al. 1998; Navarrete-Heredia 2001).
Springtails are common inhabitants of fungus-growing ant nests, and in some cases they can be considered to be pests of the fungal gardens maintained by the ants. Even the peculiar behavior known as “jigging”, described as rhythmic rocking behavior displayed by Cyphomyrmex and Myrmicocrypta ants (Formicidae: Myrmicinae), has been attributed to driving away the collembolans from fungus gardens (Kweskin 2004). Nevertheless, until now only 3 species of collembolans have been reported to be associated with fungus-growing ants, all in the genera Atta and Acromyrmex (Formicidae: Myrmicinae): Cyphoderus inaequalis Folsom (Lepidocyrtidae: Cyphoderinae) with Acromyrmex octospinosus (Reich) (Weber 1958), Pseudosinella violenta (Folsom) (Lepidocyrtidae) with Atta texana (Buckley) (Waller & Moser 1990), and Seira edmanni (Stach) (Seiridae) with A. sexdens (L) (Eidmann 1937). The occurrence of springtails of the family Sminthuridae have been reported in laboratory colonies of Cyphomyrmex costatus Mann (Formicidae: Myrmiciane) (Kweskin 2004), but there are no records of this group of microarthropods in any other fungusgrowing ant nests. Here we report information on springtails living in the nests of fungus-growing ants in different localities of southern Bahia, Brazil.
Collecting sites in the southeast of Bahia State, Brazil, 2012–2013.
Materials and Methods
Entire nests of fungus-growing ants, including ants of the genera Apterostigma, Cyphomyrmex, Mycocepurus, Myrmicocrypta, Sericomyrmex, and Trachymyrmex (Formicidae: Myrmicinae) were collected in the localities of Ubatã, Ubaitaba, Itajuípe, and Ilhéus, in the southeast of the state of Bahia, Brazil, during different periods of 2012 and 2013, during the project “Biology of fungus-growing ants in Southern Bahia, Brazil: associated fauna and nesting strategy”. They were obtained from cocoa plantations and areas of secondary growth of tropical rain forest. These nests were examined for associated fauna. Springtails were obtained directly using a paint brush or entomological forceps. The springtails were sorted and mounted in Hoyer's solution for identification. Table 1 shows the main characteristics of the nests examined.
A total of 74 nests of the different ant species were examined for associated fauna. Springtails were found in only 17 nests, which belonged to the ants Sericomyrmex saussurei Emery (Formicidae: Myrmicinae) (5 nests), S. bondari Borgmeier (Formicidae: Myrmicinae) (4 nests), S. parvulus Forel (Formicidae: Myrmicinae) 2 nests), Myrmicocrypta sp. (5 nests), and Trachymyrmex cornetzi (Forel) (Formicidae: Myrmicinae) (1 nest). No collembolans were found in the nests of Apterostigma, Cyphomyrmex and Mycocepurus. A total of 106 springtails representing 4 species were recorded, the most common being Cyphoderus agnotus Börner (Cyphoderidae: Cyphoderus) (Table 2).
Springtails associated with the nests of fungus-growing ants in southeastern Bahia State, Brazil.
Springtails were found in only 24% of the nests, and were associated with 3 genera of fungus-growing ants among the 6 we studied. Cyphoderus was present in all the ant species nests, confirming its panmyrmecophily (Wasmann 1894). Nevertheless, we found that C. agnotus was associated with S. bondari (Hymentopera: Formicidae), whereas C. similis was associated with T. cornetzi. Mucrosomia (Iso tomidae: Anurophorinae) was recorded for the first time in ant nests; until now this genus has been found in Brazil only by Mendonça and Queiroz (2013) in mountains of the southeast of the country, whereas the other 3 known species occur in Europe (Potapov 2001). The species Proisotoma minima (Collembola: Isotomidae) has been recorded once previously associated with Ponerinae (Hymenoptera: Formicidae) ant nests found in cacao pods (Castaño-Meneses et al. 2014).
Within attine “agricultural systems,” Myrmicocrypta display a “lower agriculture” system, whereas Trachymyrmex and Sericomyrmex show a “generalized higher agriculture” system (Mehdiabadi & Schultz 2010). All of these ants cultivate their symbiotic fungus with plant detritus, flower fragments, seeds, and arthropod feces as substrates, which are suitable for growth of the leucocoprineous fungi grown by the ants (Brandão & Mayhé-Nunes 2007; Mehdiabadi & Schultz 2010). These fungi are common decomposers of the leaf litter, and also are consumed by the Collembola (Vellinga 2004; Takahashi et al. 2005). The availability of this food source can explain the abundance of springtails such as Cyphoderus in the nests of these ants. Collembola were already recorded as commensals in nests of different fungus growing ants, but without discrimination of the host ant species (Mehdiabadi & Schultz 2010). This is the first record of springtails associated with known species of the genera Myrmicocrypta, Trachymyrmex and Sericomyrmex. The occurrence of collembolans in the nests of fungusgrowing ants is possibly beneficial to the growth of the symbiotic fungus. It has been observed that grazing activity of collembolans is able to increase the growth and respiration rate of fungal hyphae (Hedlund et al. 1991), and for this reason, the host ants tolerate them in their nests.
The authors would like to thank the Programa de Apoyos para la Superación del Personal Académico, DGAPA, UNAM that gave support to sabbatical leave to GCM and research visit of DZ. CNPq is acknowledged for the grant concession to CSFM and JHCD. We are deeply thankful to José Raimundo Maia Santos's support in the field work, and to Karina Alves (In Memoriam) and Evelyn Fróes for ant nest collection and sorting of the associated fauna. Luis Parra (ENAP-UNAM) corrected the English composition of the final manuscript.