Print version ISSN 1519-566X
Neotrop. Entomol. vol.31 no.2 Londrina Apr./June 2002
Parasitism Characteristics of Two Phorid Fly Species in Relation to Their Host, the Leaf-Cutting Ant Atta laevigata (Smith) (Hymenoptera: Formicidae)
MARCOS A.L. BRAGANÇA1, ATHAYDE TONHASCA JR.2 AND DENISE D.O. MOREIRA2
1Centro Universitário de Porto Nacional, Fundação Universidade do Tocantins, C. postal 25, 77500-000,
Porto Nacional, TO, e-mail: email@example.com
2Centro de Ciências e Tecnologias Agropecuárias, Universidade Estadual do Norte Fluminense, Av. Alberto Lamego 2000, 28015-620, Campos dos Goytacazes, RJ
Características de Parasitismo de Duas Espécies de Forídeos em Relação ao seu Hospedeiro, a Saúva Atta laevigata (Smith) (Hymenoptera: Formicidae)
RESUMO - As saúvas Atta sexdens (L.) e Atta laevigata (Smith) são consideradas sérias pragas para a agricultura e reflorestamento no Brasil. Estas saúvas são parasitadas pelos forídeos Neodohrniphora tonhascai Brown e Neodohrniphora erthali Brown (Diptera: Phoridae), respectivamente. O potencial de parasitismo de N. tonhascai em relação ao seu hospedeiro foi previamente investigado, mas não há informações equivalentes para N. erthali. Os objetivos deste estudo foram avaliar o comportamento de oviposição e algumas características biológicas de N. erthali em relação ao seu hospedeiro e determinar o potencial de oviposição de N. tonhascai para A. laevigata, já que em muitas áreas da região Sudeste ninhos de A. sexdens e A. laevigata são encontrados próximos uns dos outros. Os dados foram obtidos a partir de fêmeas de N. erthali e N. tonhascai coletadas no campo em Viçosa (Minas Gerais) e liberadas em uma câmara de observação colocada entre um ninho de A. laevigata de laboratório e sua arena de forrageamento. N. tonhascai levou menos tempo selecionando seus hospedeiros, atacou mais formigas e causou maiores níveis de parasitismo do que N. erthali. Não foi possível determinar se A. laevigata é parasitada por N. tonhascai no campo, mas o sucesso reprodutivo de N. tonhascai em laboratório demonstrou que A. laevigata é hospedeiro adequado para este parasióide. Os tipos de defesa demonstrados por A. laevigata contra ambas espécies de forídeos foram marcadamente diferentes, o que sugere que forrageadoras tomam medidas defensivas específicas de modo a reduzir a possibilidade de parasitismo por moscas forídeas.
PALAVRAS-CHAVE: Attini, Neodohrniphora tonhascai, Neodohrniphora erthali, parasitóide, controle biológico.
ABSTRACT - The leaf-cutting ants Atta sexdens (L.) and Atta laevigata (Smith) constitute serious pests of agriculture and forestry in Brazil. These ants are parasitized by the phorids Neodohrniphora tonhascai Brown and Neodohrniphora erthali Brown (Diptera: Phoridae), respectively. The parasitic potential of N. tonhascai against its host has been previously investigated, but no equivalent information is available for N. erthali. The objectives of this study were to evaluate the oviposition behavior and some biological characteristics of N. erthali in relation to its host and to determine the parasitic potential of N. tonhascai against A. laevigata, considering that in many parts of southeastern Brazil nests of A. sexdens and A. laevigata are found in close proximity of each other. These data were obtained from female N. erthali and N. tonhascai collected in the field in Viçosa (Minas Gerais State) and released singly in an observation chamber placed between a laboratory nest of A. laevigata and its foraging arena. Neodohrniphora tonhascai took less time selecting its hosts, attacked more ants and had greater rate of parasitism in relation to N. erthali. We could not establish whether A. laevigata is parasitized by N. tonhascai in the field, but the reproductive success of N. tonhascai in the laboratory demonstrated that A. laevigata is a suitable host to this parasitoid. The types of defense displayed by A. laevigata against both phorid species were markedly different, and these results suggest that foragers take specific defensive steps in order to reduce the possibility of parasitism by phorid flies.
KEY WORDS: Attini, Neodohrniphora tonhascai, Neodohrniphora erthali, parasitoid, biological control.
Throughout most of their range, Atta spp. leaf-cutting ants are parasitized by flies of the genus Neodohrniphora (Diptera: Phoridae) (Prado 1976, Disney 1994, Brown 2001). These flies pursue and attack the larger foragers walking along trails, but nearby ants are also disturbed by flies' attacking bouts. Neodohrniphora have been implicated in the diel shift of foraging activity exhibited by Atta cephalotes (L.) (Orr 1992, Feener & Brown 1993) and in the reduction of the forager force size of Atta sexdens (L.) (Bragança et al. 1998, Tonhasca & Bragança 2000). When exposed to a Neodohrniphora species, young A. sexdens colonies (less than 1-year old) stop completely their foraging activity within five minutes of initial contact with the parasitoids (D.D.O. Moreira, unpubl.). In older colonies, A. sexdens foragers react to the presence of these flies by abandoning their loads and returning to the nest (Bragança et al. 1998). Consequently, the occurrence of Neodohrniphora represents a disruptive factor in the foraging of Atta leaf-cutting ants.
Atta sexdens and Atta laevigata (Smith) are two of the most common leaf-cutting ants in Brazil, and both represent serious pests of agriculture and forestry (Fowler et al. 1989). In Viçosa, Minas Gerais State, Brazil (20o45'S, 42o51'W), these ants are parasitized by Neodohrniphora tonhascai Brown and Neodohrniphora erthali Brown, respectively. Like other Atta-parasitizing Neodohrniphora (Eibl-Eibesfeldt & Eibl-Eibesfeldt 1967, Orr 1992, Feener & Brown 1993), N. tonhascai attacks the head of the larger workers. Its behavior and parasitic characteristics in relation to A. sexdens have been investigated by Tonhasca (1996), where it was incorrectly named Neodohrniphora declinata Borgmeier, and by Bragança et al. (1998), where it was referred to as Neodohrniphora sp. No equivalent information is available for N. erthali.
The objectives of this study were to investigate the oviposition behavior and some biological characteristics of N. erthali related to its host and to determine the parasitic potential of N. tonhascai against A. laevigata. Many ant-parasitizing phorids are host specific (Disney 1994), but at least one Neodohrniphora species is believed to attack more than one Atta species (Brown 2001). Because nests of A. sexdens and A. laevigata occur in close proximity to each other in Viçosa as well as in many parts of southeastern Brazil, it could be possible for N. tonhascai, a species whose effects on A. sexdens are known, to utilize A. laevigata workers as host.
Material and Methods
Between 1st and 18th June 1999, 16 N. tonhascai females hovering over A. sexdens foraging trails were collected from several nests in the field. Flies were taken to the laboratory and released individually inside an observation chamber placed between a 2.5-year-old A. laevigata nest and a foraging arena. Bragança et al. (1998) described this experimental setting in detail. Fly's and ants' behavior was observed for 1h, then the fly was removed. Another phorid was released when the ants resumed their normal foraging rhythm. Ants attacked by parasitoids were removed, marked with paint on their thorax and returned to the observation chamber after 20-30 min. The same procedure was used for 15 N. erthali females collected from A. laevigata nests between 3rd and 9th July. Another 10 N. tonhascai were collected between 15th and 18th July, and 13 N. erthali between 3rd and 5th August to repeat the observations with a second A. laevigata nest of similar size and age of the previous one.
All N. tonhascai attacked the ants almost immediately after being released in the chamber, whereas only 10 N. erthali attacked the ants from either nest. To obtain more ants parasitized by this species, several additional releases of two to six N. erthali females were made along with 25 to 70 A. laevigata foragers in an observation chamber that was not connected to a nest. Ants were selected at random from each colony separately, but individuals with head widths smaller than about 1.7 mm (which was the minimum size of ants attacked by both parasitoids) were discarded. Ants and phorids were kept in the chamber for 15-24h. Afterwards, all ants were removed from the chamber, marked with paint on the thorax and returned to their nests after 20 to 30 min. In a 8-day period, 32 phorids and 325 ants from the two nests were released.
Dead ants parasitized by phorids in the laboratory are deposited by nestmates in the colony's refuse pile (Tonhasca et al. 2001). For 15 days subsequent to the parasitoid releases, dead ants with head widths larger than 1.7 mm were removed daily from the refuse pile and placed in an environmental chamber (26.5 ± 0.5oC, 85 ± 5% RH, L00:D24). Parasitism by both species was detected by the presence of a single puparium between the ant's mandibles (Tonhasca 1996). Parasitized ants were placed individually in glass tubes stopped with cotton, which were kept inside the environmental chamber until emergence of adult flies.
In the field, N. erthali are clearly larger than N. tonhascai. Ant-parasitizing phorids prefer larger individuals, a possible adaptation to increase their chances of survival and reproductive success (Feener 1987). To evaluate the effect of host size on the emergence performance of both phorid species, a factorial analysis of variance (with species and presence of puparium as factors) was performed on the data on size of dead ants recovered from the refuse pile. These variables were obtained by measuring ants' head width to the nearest 0.1 mm.
Results and Discussion
The attacking behavior of N. tonhascai and defensive behavior of threatened ants were similar to those described for A. sexdens (Tonhasca 1996, Bragança et al. 1998). This fly approaches the ant from its front or sides, apparently introducing the ovipositor in the posterior part of the host's head. Threatened ants may run away, try to fend off attacking bouts or protect the back of their heads with their legs. N. erthali on the other hand approaches the host only from its back and introduces the ovipositor in the final portion of the ant's gaster, apparently in the anal opening. Ants threatened by N. erthali lean on their middle and posterior legs, lift their bodies and curl their gaster inward to avoid oviposition while remaining stationary or walking slowly. They also try to "kick" the approaching fly with the posterior legs. We did not observe attacks by N. tonhascai against loaded ants, but six of the 31 observed attacks by N. erthali were made against ants carrying leaf fragments. However, N. tonhascai was a more efficient parasitoid. Of the 127 attacks registered for the 26 flies released in the chamber, 46.5% resulted in puparia. There were only 31 attacks for the 28 N. erthali, of which 19.4% resulted in puparia.
The presence of N. erthali puparia between the ant mandibles indicates that the larvae migrate from the gaster to the head capsule, where resources for larval development are abundant. Adult flies emerged about 35 days after oviposition. The interaction effect between phorid species and the presence of puparium was not statistically significant, but N. erthali selected significantly larger ants (F = 45.20, P<0.001, d.f. = 1,269) in comparison with N. tonhascai (Table 1). The analysis also indicated that head widths of ants parasitized by both phorid species were larger (F = 17.49, P<0.01, d.f. = 1,269) than head sizes of ants attacked but not parasitized (Table 1). The results from both nests were combined for this analysis because the average forager size in the first nest (2.2±0.7 mm) and second nest (2.4±0.7 mm) were not significantly different according to a t-test (t = 1.05, P = 0.30, d.f. = 61).
Two important conclusions were reached from this research. First, N. tonhascai collected from A. sexdens trails not only were able to parasitize A. laevigata, but were also more efficient parasitoids than N. erthali. Despite avoiding ants carrying leaf fragments, N. tonhascai took less time selecting hosts, attacked more ants and had greater rate of parasitism in relation to N. erthali. Because A. laevigata was the only host available to N. tonhascai in these tests, we could not conclude that A. laevigata is parasitized by this phorid in the field. Nonetheless, the reproductive success of N. tonhascai demonstrated that A. laevigata is a suitable host for this parasitoid. Both Neodohrniphora species selected larger foragers for oviposition, a common trend among phorids. In fact, success of puparia formation for both species was related to host size. Because the average size of Atta workers in laboratory is smaller than in the field (unpubl.), N. erthali may have been less efficient because of reduced availability of hosts of adequate size.
The second noteworthy conclusion of this study is that the type of defense displayed by individual foragers depends on the attacking phorid species. Although the defensive behaviors of leaf-cutting ants are similar when foragers are threatened by Neodohrniphora spp. that parasitize their heads (Eibl-Eibesfeldt & Eibl-Eibesfeldt 1967, Orr 1992, Feener & Brown 1993, Tonhasca 1996), the response of A. laevigata to N. erthali was remarkably different. Porter et al. (1995) suggested that ants' protective behavior is triggered by the detection of parasitoid's wing buzzing at short range. This hypothesis implies that defenses against phorids are stereotypical responses to a generic signal such as air vibrations. However, our results indicated that ants take specific defensive steps in order to reduce the possibility of parasitism.
We thank T. Della Lucia for logistical support, D. Coracini, M. Erthal Jr. and M. Ferreira for helping with field and laboratory work, and B.V. Brown for identifying the phorids. M. Bragança was supported by a grant from FAPERJ and A. Tonhasca received funds from the International Foundation for Science.
Bragança, M.A.L., A. Tonhasca Jr. & T.M.C. Della Lucia. 1998. Reduction in the foraging activity of the leaf-cutting ant Atta sexdens caused by the phorid Neodohrniphora sp. Entomol. Exp. Appl. 89: 305-311. [ Links ]
Brown, B.V. 2001. Taxonomic revision of Neodohrniphora, subgenus Eibesfeldtphora (Diptera: Phoridae). Ins. Syst. Evol. 32: 393-409. [ Links ]
Disney, R.H.L. 1994. Scuttle flies: the Phoridae. London, Chapman & Hall, 467p. [ Links ]
Eibl-Eibesfeldt, I. & E. Eibl-Eibesfeldt. 1967. Das parasitenabwehren der minima-arbeiterinnen der blattschneider-ameise (Atta cephalotes). Z. Tierpsychol. 24: 278-281. [ Links ]
Feener Jr., D.H. 1987. Size-selective oviposition in Pseudacteon crawfordi (Diptera: Phoridae), a parasite of fire ants. Ann. Entomol. Soc. Am. 80: 148-151. [ Links ]
Feener Jr., D.H. & B.V. Brown. 1993. Oviposition behavior of an ant-parasitizing fly, Neodohrniphora curvinervis (Diptera: Phoridae), and defense behavior by its leaf-cutting ant host Atta cephalotes (Hymenoptera: Formicidae). J. Ins. Behav. 6: 675-688. [ Links ]
Fowler, H.G., M.I. Pagani, O.A. da Silva, L.C. Forti, V.P. da Silva & H.L. de Vasconcelos. 1989. A pest is a pest is a pest The dilemma of Neotropical leaf-cutting ants: keystone taxa of natural ecosystems. Environ. Manag. 13: 71-675. [ Links ]
Orr, M.R. 1992. Parasitic flies (Diptera: Phoridae) influence foraging rhythms and caste division of labor in the leaf-cutter ant, Atta cephalotes (Hymenoptera: Formicidae). Behav. Ecol. Sociobiol. 30: 395-402. [ Links ]
Porter, S.D., R.K. van der Meer, M.A. Pesquero, S. Campiolo, H.G. Fowler. 1995. Solenopsis (Hymenoptera: Formicidae) fire ant reactions to attacks of Pseudacteon flies (Diptera: Phoridae) in Southeastern Brazil. Ann. Entomol. Soc. Am. 88: 570-575. [ Links ]
Prado, A.P. 1976. Records and descriptions of Phorid flies, mainly of the Neotropical region (Diptera; Phoridae). Stud. Entomol. 19: 561-609. [ Links ]
Tonhasca Jr., A. 1996. Interactions between a parasitic fly, Neodohrniphora declinata (Diptera: Phoridae), and its host, the leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae). Ecotropica 2: 157-164. [ Links ]
Tonhasca Jr., A. & M.A.L. Bragança. 2000. Effect of leaf toughness on the susceptibility of the leaf-cutting ant Atta sexdens to attacks of a phorid parasitoid. Insectes Soc. 47: 220-222. [ Links ]
Tonhasca Jr., A., M.A.L. Bragança & M. Erthal Jr.. 2001. Parasitism and biology of Myrmosicarius grandicornis (Diptera, Phoridae) in relationship to its host, the leaf-cutting ant Atta sexdens (Hymenoptera, Formicidae). Insectes Soc. 48: 154-158. [ Links ]
Received 24/07/01. Accepted 01/05/02.