Print version ISSN 1519-566X
Neotrop. entomol. vol.37 no.5 Londrina Sept./Oct. 2008
Conopid flies (Diptera: Conopidae) parasitizing Centris (Heterocentris) analis (Fabricius) (Hymenoptera: Apidae, Centridini)
Conopídeos (Diptera: Conopidae) parasitando Centris (Heterocentris) analis (Fabricius) (Hymenoptera: Apidae, Centridini)
Alex M. SantosI; José C. SerranoI; Ricardo M. CoutoI; Leonardo S.G. RochaII; Cátia A. Mello-PatiuII; Carlos A. GarófaloI
IDepto. Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, USP, 14040-901, Ribeirão Preto, SP; email@example.com
IIDepto. Entomologia, Museu Nacional, Univ. Federal do Rio de Janeiro, 20940-040 Rio de Janeiro, RJ; firstname.lastname@example.org
Parasites of adult bees are almost exclusively flies and the most important of them are conopids. This note registers for the first time the association of species of Physocephala (Diptera: Conopidae) with Centris (Heterocentris) analis (Fabricius). From 26 females and nine males of the host species found dead inside trap-nests on the campus of the University of São Paulo, Ribeirão Preto, Brazil, 35 parasitoids were obtained belonging to nine species of Physocephala. The data show that C. analis is a host to several conopid flies, and suggest that such parasitoids can play an important role in population control of this bee species.
Key words: Parasitism, parasite-host association, bee, trap-nest
Parasitas de abelhas adultas são quase exclusivamente moscas e dentre os mais importantes estão os conopídeos. Nesta comunicação relata-se pela primeira vez a associação de espécies de Physocephala (Diptera: Conopidae) com Centris (Heterocentris) analis (Fabricius). De uma amostra de 26 fêmeas e nove machos da espécie hospedeira encontrados mortos em ninhos-armadilha vazios, no campus da Universidade de São Paulo, Ribeirão Preto, SP, emergiram 35 parasitóides pertencentes a nove espécies de Physocephala. Os dados mostram que C. analis é hospedeiro para várias espécies de conopídeos e sugerem que tais parasitóides podem desempenhar um papel importante na regulação populacional dessa espécie de abelha.
Palavras-chave: Parasitismo, associação parasita-hospedeiro, abelha, ninhos-armadilha
Conopid flies are parasitoids of insects, usually aculeate Hymenoptera, with a worldwide distribution (Askew 1971, Smith & Peterson 1987). Probably, they are the most important of dipterous parasitoids of adult bees, both females and males. Female flies attack the bees inserting an egg on or within the bee's abdomen while they are foraging at flowers or while in flight. The larva develops inside the abdomen of the host by feeding on internal tissue and hemolymph (Pouvreau 1974, Müller et al. 1996). Development of the larval parasitoid takes about 10-12 days after oviposition when the host is killed and the parasite pupates in situ (Smith 1966, Pouvreau 1974). The pupa remains inside the host and, for temperate species, the parasitoid hibernates where its host dies, usually outside the nest (Smith & Van Someren 1970, Schmid-Hempel & Müller 1991), before emerging at the following spring. Species of the conopid genus Physocephala have been recorded in association with bee species of several genera such as Anthidium, Anthophora, Eucera, Megachile, Halictus, Apis, Xylocopa, Bombus, and Eulaema (Linsley 1958, Hurd 1978, Katayama & Maeta 1998, Schmid-Hempel 2001, Otterstatter et al. 2002, Rasmussen & Cameron 2004). Recently, two Physocephala species, Physocephala bipunctata Macquart and Physocephala inhabilis Walker, were recorded in association with Epicharis bicolor Smith e Centris vittata Lepeletier (Vilhena & Rocha-Filho inf. pes.).
Centris (Heterocentris) analis Fabricius is a solitary bee that has a broad geographic range extending from Mexico to Brazil (Moure 1960). Like other species of Heterocentris, nesting by C. analis occurs on a variety of preexisting cavities (Camillo et al. 1995, Vieira de Jesus & Garófalo 2000). In a detailed study of the nesting behavior of C. analis in trap-nests, Vieira de Jesus & Garófalo (2000) observed that the bees construct their nests with plant material and an oily substance. Completed nests have one to four brood cells arranged in a linear series, usually followed by a vestibular cell, an empty cell found between the last brood cell and the nest plug. The innermost cells of the nests produce females, and the outermost cells produce males. Nests are parasitized by the wasp Leucospis cayennensis Westwood, the most frequent parasite, and by the bees Coelioxys sp. (Megachilidae) and Mesocheira bicolor Fabricius (Apidae) (Gazola & Garófalo 2003). Nesting activities occur with higher frequency in the hot and wet season (September-April), and several generations per year can be produced. The goal of this note is to register for the first time the association of species of Physocephala with C. analis.
While monitoring the nesting activities of C. analis females on the campus of the University of São Paulo Ribeirão Preto (between 21°05'- 21°15'S and 47°50'- 47°55'W), state of São Paulo, Brazil, the trap-nests, tubes made with black cardboard, with one of the end closed with the same material, were inspected daily with an otoscope and those occupied by females were recorded. The tubes were inserted into horizontal holes drilled into eight wooden plates (28 x 24 x 4 cm) and they were 5.8 cm in length and 0.6 cm in internal diameter. The plates were placed along shelves in a shelter built near the laboratory. The shelves were 1.2 and 1.5 m above the ground. During the inspections of trap-nests, several females and some males that utilized the trap-nests as a place to rest during the night were found dead within empty trap-nests. These individuals were immediately collected, transferred to small glass vials and taken to the laboratory. In the laboratory, the vials were kept at room temperature (21°C-29°C) and observed daily to verify the occurrence of parasitoids attacking such bees. When a parasitoid emerged, it was left in the same vial for 24h. Thereafter, it was killed with ethyl acetate. Voucher specimens were deposited at the Entomological Collection of the Departamento de Biologia, Faculdade de Filosofia, Ciências e Letras de Ribeirão Preto, USP, and duplicates of some specimens are deposited in the Entomological Collection of the Museu Nacional, Universidade Federal do Rio de Janeiro, RJ.
From December 2004 to May 2005 and from January to June 2006, when C. analis females were nesting, 26 females and nine males were found dead and all had been parasitized by conopid flies. Most individuals (19 females and five males) were attacked from December 2004 to April 2005 (Table 1). The interval between the collection date of the dead female or male and the parasitoid emergence ranged from 19 to 53 days. The largest intervals were observed for parasitoids that emerged from males attacked in June/2006 and females that nested in May/2006 (Table 1). This result must be related with the temperature which decreases as the cold and dry season approaches. Of the 35 parasitoids emerged, 10 were Physocephala soror Kröber (five males, four females and one not sexed), one was P. bipunctata (not sexed), six were P. inhabilis (three males and three females), five were Physocephala rufithorax Kröber (four males and one female), two were Physocephala cayennensis Macquart (one female and one male), one was Physocephala aurifrons Walker (one male), one was Physocephala bennetti Camras (not sexed), three were Physocephala spheniformis Camras (one male and two females), and six other individuals were not identified (Physocephala sp.) (four males and two females). Except for P. aurifrons, P. bipunctata and P. bennetti, which were represented by only one individual, specimens of all other species attacked both females and males of C. analis.
To date, besides the association of P. bipunctata with E. bicolor and P. inhabilis with C. vittata (Vilhena & Rocha-Filho inf. pes.) an other available information indicate P. bennetti associated with Xylocopa submordax Cockerell and Xylocopa frontalis Olivier, in Trinidad (Camras 1996), and P. rufithorax attacking Eulaema sp. males attracted to chemical baits, in Peru (Rasmussen & Cameron 2004). The observations reported here show that C. analis is a host to a large number of conopid flies and an alternative host for P. bipunctata, P. inhabilis, P. bennetti and P. rufithorax. From the relationship between the period of host death and conopid fly emergence it can be concluded that all parasitoid species are multivoltine and have their phenologies synchronized with that of the host.
Conopid parasitism in natural population of bumblebees (Bombus sp.) is very commom in Europe, where incidence of parasitism range between 30% and 70% (Schmid-Hempel et al. 1990). This parasitic association has been studied under several aspects and some results have shown that the parasitoid increases the worker mortality (Schmid-Hempel & Schmid-Hempel 1988, 1990), alters foraging behavior (Heinrich & Heinrich 1983, Muller & Schmid-Hempel 1993) and, consequently reduces the size of colonies (Müller & Schmid-Hempel 1992, MacFarlane et al. 1995). Work to clarify similar aspects in the C. analis-conopid interaction is currently in progress.
We are grateful to Vera C. Silva and Elieser Azevedo (UNESP-ASSIS) for the identification of some specimens of parasitoids. This study was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq). A.M. Santos was sponsored by CNPq (PIBIC Processo nº 803070/87.0).
Askew, R.R. 1971. Parasitic insects. American Elsevier Publishing, Inc., New York, 316p. [ Links ]
Camillo, E., C.A. Garófalo, J.C. Serrano & G. Muccillo. 1995. Diversidade e abundância sazonal de abelhas e vespas solitárias em ninhos armadilhas. Rev. Bras. Entomol. 39: 459-470. [ Links ]
Camras, S. 1996. New information on the New World Physocephala (Diptera: Conopidae). Entomol. News 107: 104-112. [ Links ]
Gazola, A.L. & C.A. Garófalo. 2003. Parasitic behavior of Leucospis cayennensis Westwood (Hymenoptera, Leucospidae) and rates of parasitism in populations of Centris (Heterocentris) analis (Fabricius) (Hymenoptera, Apidae, Centridini). J. Kansas Entomol. Soc. 76: 131-142. [ Links ]
Heinrich, B. & M.J.E. Heinrich. 1983. Heterothermia in foraging workers and drones of the bumble-bee Bombus terricola. Physiol. Zool. 56: 563-567. [ Links ]
Hurd, P.D. 1978. An annotated catalog of the carpenter bees (genus Xylocopa Latreille) of the Western Hemisphere. Smithsonian Institution Press, Washington, D.C., 106p. [ Links ]
Katayama, E. & Y. Maeta. 1998. The fourth host of Physocephala obscura Kröber found in Japan (Diptera, Conopidae). Chugoku Kontyu 12: 23. [ Links ]
Linsley, E.G. 1958. The ecology of solitary bees. Hilgardia 27: 543-599. [ Links ]
MacFarlane, R.P., J.J. Lipa & H.J. Liu. 1995. Bumble bee pathogens and internal enemies. Bee World 76: 130-148. [ Links ]
Moure, J.S. 1960. Notes on the types of the neotropical bees described by Fabricius (Hymenoptera: Apoidea). Studia Entomol. 3: 97-160. [ Links ]
Müller, C.B. & P. Schmid-Hempel. 1992. Correlates of reproductive success among field colonies of Bombus lucorum: The importance of growth and parasites. Ecol. Entomol. 17: 343-353. [ Links ]
Müller, C.B. & P. Schmid-Hempel. 1993. Exploitation of cold temperature as defense against parasitoids in bumblebees. Nature 363: 65-67. [ Links ]
Müller, C.B., T.M. Blackburn & P. Schmid-Hempel. 1996. Field evidence that host selection by conopid parasitoids is related to host body size. Insectes Soc. 43: 227-233. [ Links ]
Otterstatter, M.C., T.L. Whidden & R.E. Owen. 2002. Contrasting frequencies of parasitism and host mortality among phorid and conopid parasitoids of bumble-bees. Ecol. Entomol. 27: 229-237. [ Links ]
Pouvreau, A. 1974. Les enemies des bourdons. II. Organismes affectant les adultes. Apidologie 5: 39-62. [ Links ]
Rasmussen, C & S.A. Cameron. 2004. Conopid fly (Diptera: Conopidae) attacking large orchid bees (Hymenoptera: Apidae: Eulaema). J. Kansas Entomol. Soc. 77: 61-62. [ Links ]
Schmid-Hempel, P. 2001. On the evolutionary ecology of host-parasite interactions: Addressing the question with regard to bumble bees and their parasites. Naturwissenschaften 88: 147-158. [ Links ]
Schmid-Hempel, P. & C.B. Müller. 1991. Do parasitized bumblebees forage for their colony ? Anim. Behav. 41: 910-912. [ Links ]
Schmid-Hempel, P., C. Müller, R. Schmid-Hempel & J.A. Shykoff. 1990. Frequency and ecological correlates of parasitisation by conopid flies (Conopidae, Diptera) in populations of bumblebees. Insectes Soc. 37: 14-30. [ Links ]
Schmid-Hempel, P. & R. Schmid-Hempel. 1990. Endoparasitic larvae of conopid flies alter pollination behaviour of bumblebees. Naturwissenschaften 27: 50-52. [ Links ]
Schmid-Hempel, R. & P. Schmid-Hempel. 1988. Parasitic flies (Conopidae, Diptera) may be important stress factors for the ergonomics of their bumblebee hosts. Ecol. Entomol. 13: 469-472. [ Links ]
Smith, K.G.V. 1966. The larva of Thecophora occidensis, with comments upon the biology of Conopidae (Diptera). J. Zool. 149:263-276. [ Links ]
Smith, K.G.V. & B.V. Peterson. 1987. Conopidae. In J. F. McAlpine et al. (eds.), Manual of Nearctic Diptera, vol. 2. Research Branch Agriculture, Monog. 28, Ottawa, 1332p. [ Links ]
Smith, K.G.V. & G.R.C. Van Someren. 1970. The identity of Physocephala bimarginipennis Karsch (Diptera, Conopidae) with notes on the immature stages and biology. J. Nat. Hist. 4: 439-446. [ Links ]
Viera de Jesus, B.M. & C.A. Garófalo. 2000. Nesting behavior of Centris (Heterocentris) analis (Fabricius) in southeastern Brazil (Hymenoptera, Apidae, Centridini). Apidologie 31: 503-515 [ Links ]
Received 14/I/08. Accepted 11/IX/08.