This review updates and summarizes the current knowledge about the interaction of leaf-cutter ants and their parasitoids by providing comparable data for Acromyrmex and Atta ants. First, an overview of the relevant aspects of the biology and taxonomy of leaf cutters and of their parasitoids is provided. Second, I show the peculiarities of the parasitoids attacking behaviors towards their host as well as the responses or ant defenses against the phorids exhibited by their hosts. Third, I discuss relevant aspects of the interactions between hosts and parasitoids. Finally, the review ends demonstrating why these phorids could be promising biological control agents of leaf-cutter pests and suggests priority lines of research for the future. 1. Introduction Since the Feener Jr. and Brown [1] review discussion on flies as parasitoids, there has not been a comprehensive review on Phoridae (Diptera) parasitoids specialized on attacking adult ant workers. Phorids attacking fire ants are the ones most extensively studied due to their application in biological control. The literature is vast and dispersed although there is a review about Pseudacteon biology and interaction with fire ants [2]. Other scarce studies were done on other ant-phorid systems such as Pheidole [3, 4], Azteca [5, 6], and Paraponera [7]. Until more information is gathered, generalizations will not be possible for these groups. Hsun-Yi and Perfecto [8] have done an interesting review on indirect trait mediated effects of parasitoids on ants showing general patterns such as a reduction in ant’s foraging activity, body sizes as well as the amount of food retrieved by colonies. A compilation of leaf-cutter phorid species with their known and/or potential host species has been recently made [9]. The mentioned work includes some biological data about parasitoids of Atta, mainly from the laboratory, but a comprehensive review about their biology and ecological interaction with their hosts, including data of Acromyrmex, has not been done. Furthermore, Bragan？a [9] has not updated the scientific names of 14 species (called as Neodohrniphora) according to the status change of the subgenus Eibesfeldtphora to genus, proposed by Disney et al. [10]. Although the great majority of data available is limited to the southern portion of South America and therefore more work is needed, it is enough to observe general patterns. This review will summarize the current information about this system and will identify key questions and gaps of knowledge where researchers should focus attention. 2. Leaf-Cutter Ants The
References
[1]
D. H. Feener Jr. and B. V. Brown, “Diptera as parasitoids,” Annual Review of Entomology, vol. 42, pp. 73–97, 1997.
[2]
L. W. Morrison, “Biology of Pseudacteon (Diptera: Phoridae) ant parasitoids and their potential to control imported Solenopsis fire ants (Hymenoptera: Formicidae),” Recent Research and Development in Entomology, vol. 3, pp. 1–13, 2000.
[3]
D. H. Feener Jr., “Competition between ant species: outcome controlled by parasitic flies,” Science, vol. 214, no. 4522, pp. 815–817, 1981.
[4]
E. G. LeBrun and D. H. Feener Jr., “Linked indirect effects in ant-phorid interactions: impacts on ant assemblage structure,” Oecologia, vol. 133, no. 4, pp. 599–607, 2002.
[5]
S. M. Philpott, I. Perfecto, J. Vandermeer, and S. Uno, “Spatial scale and density dependence in a host parasitoid system: an arboreal ant, Azteca instabilis, and its Pseudacteon phorid parasitoid,” Environmental Entomology, vol. 38, no. 3, pp. 790–796, 2009.
[6]
G. L. Pardee and S. M. Philpott, “Cascading indirect effects in a coffee agroecosystem: effects of parasitic phorid flies on ants and the coffee berry borer in a high-shade and low-shade habitat,” Environmental Entomology, vol. 40, no. 3, pp. 581–588, 2011.
[7]
B. V. Brown and D. H. Feener Jr., “Life history parameters and description of the larva of Apocephalus paraponerae (Diptera: Phoridae), a parasitoid of the giant tropical ant Paraponera clavata (Hymenoptera: Formicidae),” Journal of Natural History, vol. 25, no. 1, pp. 221–231, 1991.
[8]
H. Hsun-Yi and I. Perfecto, “Trait mediated indirect effects of phorid flies on ants,” Psyche, vol. 2012, Article ID 380474, 11 pages, 2012.
[9]
M. A. L. Bragan？a, “Parasitoides de formigas cortadeiras,” in Formigas-Cortadeiras: da Bioecologia ao Manejo, T. M. Castro Della Lucia, Ed., pp. 321–343, Universidade Federal de Vi？osa, Vi？osa, Brasil, 2011.
[10]
R. H. L. Disney, L. Elizalde, and P. J. Folgarait, “New species and new records of scuttle flies (diptera: Phoridae) that parasitize leaf-cutter and army ants (Hymenoptera: Formicidae),” Sociobiology, vol. 54, no. 2, pp. 601–631, 2009.
[11]
J. H. Delabie, H. S. Rodrigues Alves, G. M. Reuss-Strenzel, A. F. Ribeiro do Carmo, and I. Cardoso do Nascimento, “Distribucao das formigas-cortadeiras Acromyrmex e Atta no Novo Mundo,” in Formigas-Cortadeiras: da Bioecologia ao Manejo, T. M. Castro Della Lucia, Ed., pp. 80–101, Universidade Federal de Vi？osa, Vi？osa, Brasil, 2011.
[12]
L. Elizalde and P. J. Folgarait, “Host diversity and environmental variables as determinants of the species richness of the parasitoids of leaf-cutting ants,” Journal of Biogeography, vol. 37, no. 12, pp. 2305–2316, 2010.
[13]
C. R. Ferreira Brandao, A. J. Mayhe-Nunes, and C. E. Dias Sanhudo, “Taxonomia e filogenia das formigas-cortadeiras,” in Formigas-Cortadeiras: da Bioecologia ao Manejo, T. M. Castro Della Lucia, Ed., pp. 27–48, Universidade Federal de Vi？osa, Vi？osa, Brasil, 2011.
[14]
B. Holldobler and E. O. Wilson, The Ants, Cambridge University Press, New York, NY, USA, 1990.
[15]
A. A. Bonetto, Las Hormigas “Cortadoras” de la Provincia de Santa Fé (Géneros: Atta y AcromYrmex), Ministerio de Agricultura y Ganaderia, Provincia de Santa Fe, Argentina, 1959.
[16]
L. C. Forti, M. L. de Andrade, A. P. P. Andrade, J. F. S. Lopes, and V. M. Ramos, “Bionomics and identification of Acromyrmex (Hymenoptera: Formicidae) through an illustrated key,” Sociobiology, vol. 48, no. 1, pp. 135–153, 2006.
[17]
L. C. Forti, A. Alves Moreira, A. P. Protti Andrade, M. A. Castellani, and N. Caldato, “Nidifica？ao e arquitetura de ninhos de formigas -cortadeiras,” in Formigas-Cortadeiras: da Bioecologia ao Manejo, T. M. Castro Della Lucia, Ed., pp. 102–125, Universidade Federal de Vi？osa, Vi？osa, Brasil, 2011.
[18]
M. Bollazzi, J. Kronenbitter, and F. Roces, “Soil temperature, digging behaviour, and the adaptive value of nest depth in South American species of Acromyrmex leaf-cutting ants,” Oecologia, vol. 158, no. 1, pp. 165–175, 2008.
[19]
L. Elizalde and P. J. Folgarait, “Behavioral strategies of phorid parasitoids and responses of their hosts, the leaf-cutting ants,” Journal of Insect Science, vol. 12, article 135, 2012.
[20]
L. Elizalde, Biogeografía y comunidades de fóridos parasitoides de hormigas cortadoras de hojas. Diversidad del sistema y partición del recurso hospedador [Ph.D. thesis], Universidad Nacional de Quilmes, Buenos Aires, Argentina, 2009.
[21]
P. Eggleton and R. Belshaw, “Insect parasitoids: an evolutionary overview,” Philosophical Transactions of the Royal Society of London B, vol. 337, no. 1279, pp. 1–20, 1992.
[22]
R. H. L. Disney, Scuttle Flies: The Phoridae, Chapman and Hall, London, UK, 1994.
[23]
R. H. L. Disney, L. Elizalde, and P. J. Folgarait, “New species and records of scuttle flies (Diptera: Phoridae) associated with leaf-cutter ants and army ants (Hymenoptera: Formicidae) in Argentina,” Sociobiology, vol. 51, no. 1, pp. 95–117, 2008.
[24]
L. Elizalde and P. J. Folgarait, “Primeros registros de foridos parasitoides (Phoridae: Diptera) de hormigas cortadoras de hojas (Atta y Acromyrmex) para Argentina y Paraguay, incluyendo su distribución en el área total donde se encuentran los hospedadores,” in VI Congreso Argentino de Entomología, San Miguel del Tucuman, Argentina, 2005.
[25]
A. C. Guillade and P. J. Folgarait, “Life-history traits and parasitism rates of four phorid species (Diptera: Phoridae), parasitoids of Atta vollenweideri (Hymenoptera: Formicidae) in Argentina,” Journal of Economic Entomology, vol. 104, no. 1, pp. 32–40, 2011.
[26]
B. V. Brown, “Revision of the Apocephalus attophilus-group of ant-decapitaiting flies (Diptera: Phoridae),” Contribution in Science, vol. 468, pp. 1–60, 1997.
[27]
B. V. Brown, “Taxonomic revision of Neodohrniphora, subgenus Eibesfeldtphora (Diptera: Phoridae),” Insect Systematics and Evolution, vol. 32, no. 4, pp. 393–409, 2001.
[28]
T. Borgmeier, “Investigacoes sobre Phorideos myrmecophilos (Diptera, Phoridae),” Archivos do Instituto Biologico de Defesa Agricola e Animal S？o Paulo, vol. 1, pp. 159–192, 1928.
[29]
R. H. L. Disney, L. Elizalde, and P. J. Folgarait, “New species and revision of Myrmosicarius (Diptera: Phoridae) that parasitize leaf-cutter ants (Hymenoptera: Formicidae),” Sociobiology, vol. 47, no. 3, pp. 771–810, 2006.
[30]
B. V. Brown, R. H. L. Disney, L. Elizalde, and P. J. Folgarait, “New species and new records of Apocephalus Coquillett (Diptera: Phoridae) that parasitize ants (Hymenoptera: Formicidae) in America,” Sociobiology, vol. 55, no. 1 B, pp. 165–190, 2010.
[31]
R. H. L. Disney, “A key to Neodohrniphora (Diptera: Phoridae), parasites of leaf-cutter ants (Hymenoptera: Formicidae),” Journal of Natural History, vol. 30, no. 9, pp. 1377–1389, 1996.
[32]
L. Elizalde and P. J. Folgarait, “Biological attributes of Argentinian phorid parasitoids (Insecta: Diptera: Phoridae) of leaf-cutting ants, Acromyrmex and Atta,” Journal of Natural History, vol. 45, no. 43-44, pp. 2701–2723, 2011.
[33]
A. Tonhasca Jr, “Interactions between a parasitic fly, Neodhorniphora declinata (Diptera: Phoridae) and its host, the leaf-cutting ant Atta sexdens rubropilosa (Hymenoptera: Formicidae),” Ecotropica, vol. 2, pp. 157–164, 1996.
[34]
M. Erthal Jr. and A. Tonhasca Jr., “Biology and oviposition behavior of the phorid Apocephalus attophilus and the response of its host, the leaf-cutting ant Atta laevigata,” Entomologia Experimentalis et Applicata, vol. 95, no. 1, pp. 71–75, 2000.
[35]
M. A. L. Bragan？a, A. Tonhasca Jr., and T. M. C. Delia Lucia, “Reduction in the foraging activity of the leaf-cutting ant Atta sexdens caused by the phorid Neodohrniphora sp,” Entomologia Experimentalis et Applicata, vol. 89, no. 3, pp. 305–311, 1998.
[36]
M. A. L. Bragan？a and Z. C. S. Medeiros, “Ocorrência e Características Biológicas de Forídeos Parasitóides (Diptera: Phoridae) da Saúva Atta laevigata (Smith) (Hymenoptera: Formicidae) em Porto Nacional, TO,” Neotropical Entomology, vol. 35, pp. 408–411, 2006.
[37]
D. H. Feener Jr. and K. A. G. Moss, “Defense against parasites by hitchhikers in leaf-cutting ants: a quantitative assessment,” Behavioral Ecology and Sociobiology, vol. 26, no. 1, pp. 17–29, 1990.
[38]
J. Tonhasca Jr., M. A. L. Bragan？a, and J. Erthal Jr., “Parasitism and biology of Myrmosicarius grandicornis (Diptera, Phoridae) in relationship to its host, the leaf-cutting ant Atta sexdens (Hymenoptera, Formicidae),” Insectes Sociaux, vol. 48, no. 2, pp. 154–158, 2001.
[39]
M. A. L. Bragan？a, A. Tonhasca Jr., and T. M. C. Della Lucia, “Biological and behavioral characteristics of Neodohrniphora elongata Brown (Diptera, Phoridae), a parasitic fly of the leaf-cutting ant Atta sexdens rubropilosa Forel (Hymenoptera, Formicidae),” Revista Brasileira de Entomologia, vol. 53, no. 4, pp. 600–606, 2009.
[40]
D. H. Feener Jr. and B. V. Brown, “Oviposition behavior of an ant-parasitizing fly, Neodohrniphora curvinervis (Diptera: Phoridae), and defense behavior by its leaf-cutting ant host Atta cephalotes (Hymenoptera: Formicidae),” Journal of Insect Behavior, vol. 6, no. 6, pp. 675–688, 1993.
[41]
V. Gazal, O. Bailez, and A. M. Viana-Bailez, “Mechanism of host recognition in Neodohrniphora elongata (Brown) (Diptera: Phoridae),” Animal Behaviour, vol. 78, no. 5, pp. 1177–1182, 2009.
[42]
L. W. Morrison and J. R. King, “Host location behavior in a parasitoid of imported fire ants,” Journal of Insect Behavior, vol. 17, no. 3, pp. 367–383, 2004.
[43]
K. A. Mathis and S. M. Philpott, “Current understanding and future prospects of host selection, acceptance, discrimination, and regulation of phorid fly parasitoids that attack ants,” Psyche, vol. 2012, Article ID 895424, 2012.
[44]
L. W. Morrison and L. E. Gilbert, “Parasitoid-host relationships when host size varies: the case of Pseudacteon flies and Solenopsis fire ants,” Ecological Entomology, vol. 23, no. 4, pp. 409–416, 1998.
[45]
P. J. Folgarait, O. A. Bruzzone, R. J. W. Patrock, and L. E. Gilbert, “Developmental rates and host specificity for Pseudacteon parasitoids (Diptera: Phoridae) of fire ants (Hymenoptera: Formicidae) in Argentina,” Journal of Economic Entomology, vol. 95, no. 6, pp. 1151–1158, 2002.
[46]
M. R. Orr, “Parasitic flies (Diptera: Phoridae) influence foraging rhythms and caste division of labor in the leaf-cutter ant, Atta cephalotes (Hymenoptera: Formicidae),” Behavioral Ecology and Sociobiology, vol. 30, no. 6, pp. 395–402, 1992.
[47]
E. H. M. Vieira-Neto, F. M. Mundim, and H. L. Vasconcelos, “Hitchhiking behaviour in leaf-cutter ants: an experimental evaluation of three hypotheses,” Insectes Sociaux, vol. 53, no. 3, pp. 326–332, 2006.
[48]
T. A. Linksvayer, A. C. McCall, R. M. Jensen, C. M. Marshall, J. W. Miner, and M. J. McKone, “The function of hitchhiking behavior in the leaf-cutting ant Atta cephalotes,” Biotropica, vol. 34, no. 1, pp. 93–100, 2002.
[49]
H. M. Griffiths and W. O. H. Hughes, “Hitchhiking and the removal of microbial contaminants by the leaf-cutting ant Atta colombica,” Ecological Entomology, vol. 35, no. 4, pp. 529–537, 2010.
[50]
A. Lenoir, D. Fresneau, C. Errard, and A. Hefetz, “The individuality and the colonial identity in ants: the emergence of the social representation concept,” in Information Processing in Social Insects, C. Detrain, J. L. Deneubourg, and J. Pasteels, Eds., pp. 219–237, Birkhauser, Basel, Switzerland, 1999.
[51]
A. Clavijo McCormick, S. B. Unsicker, and J. Gershenzon, “The specificity of herbivore-induced plant volatiles in attracting herbivore enemies,” Trends in Plant Science, vol. 17, pp. 303–310, 2012.
[52]
E. Goncalvez Paterson Fox, A. Pianaro, D. Russ Solis et al., “Intraspecific and intracolonial variation in the profile of venom alkaloids and cuticular hydrocarbons of the fire Ant Solenopsis saevissima Smith (Hymenoptera: Formicidae),” Psyche, vol. 2012, Article ID 398061, 10 pages, 2012.
[53]
D. J. de Souza, A. Lenoir, M. C. Megumi Kasuya et al., “Ectosymbionts and immunity in the leaf-cutting ant Acromyrmex subterraneus subterraneus,” Brain Behavior, and Immunity, vol. 28, pp. 182–187, 2013.
[54]
L. Lapchin and T. Guillemaud, “Asymmetry in host and parasitoid diffuse coevolution: when the red queen has to keep a finger in more than one pie,” Frontiers in Zoology, vol. 2, article 4, 2005.
[55]
L. Elizalde L and P. J. Folgarait, “Diversity of interactions among leaf-cutting ants and their phorid parasitoids: a community approach,” in Primer Encuentro de Mirmecologistas de las Américas y XX Simpósio de Mirmecologia, Petropolis, Brasil, 2011.
