Abstract
The myrmecophile cockroach Attaphila fungicola lives in the nests of leaf-cutter ants (Atta texana and A. cephalotes) and uses the female winged reproductives (i.e., female alates) of its host as vectors for the first phase of its dispersal. It is unknown whether A. fungicola remain with vectoring A. texana females after mating flights and throughout A. texana nest founding and subsequent colony development, or if the symbiotic cockroaches disperse to established A. texana colonies, either on their own or while still attached to vectoring A. texana females. We captured A. fungicola attached to A. texana female alates as they prepared for mating flights and measured their survivorship in artificial brood chambers with de-alate, recently mated A. texana queens and their incipient gardens, and in a non-natal established fungal garden tended by A. texana workers. After 13 days, 100% of A. fungicola had died in brood chambers with queens, while 100% of A. fungicola remained alive in the fungal garden chamber. We tested the feasibility of alternative modes of dispersal to established colonies by placing A. fungicola attached and unattached to vectoring female alates in the proximity of an established A. texana colony directly after a mating flight, and recorded whether A. fungicola entered the non-natal nest. A significantly higher proportion of A. fungicola attached to vectoring alates entered the nest compared to unattached A. fungicola. We also placed A. fungicola attached to vectoring alates in a foraging chamber of a laboratory colony to determine if, once in the nest, A. fungicola could navigate to the fungal garden chamber; 100% of A. fungicola detached from their vectoring alates and entered the fungal garden chamber. We tested alate preference of A. fungicola by placing A. fungicola separately in containers with one A. texana female alate and one male alate; after 2 h, 71% of A. fungicola were attached to female alates and 0% to male alates. Finally, we report the first record of a male A. fungicola collected during a mating flight of A. texana. These observations accumulated from field and laboratory studies suggest that A. fungicola vectored by A. texana female alates may not remain with foundresses, but instead disperse between established colonies through one or more alternative mechanisms. This study helps elucidate a tripartite ant-fungus-cockroach interaction, and provides a foundation for future research on Attaphila dispersal and reproductive biology.
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References
Bell WJ, Roth LM, Nalepa CA (2007) Cockroaches: ecology, behavior, and natural history. Johns Hopkins University Press, Baltimore
Bland JM, Altman GD (2004) The logrank test. BMJ 328:1073–1073
Bolívar I (1901) Un nuevo ortóptero mirmecófilo Attaphila Bergi. Común Mus Nac B Aires 1:331–336
Bolívar I (1905) Les blattes myrmécophiles. Mitt Schweiz Entomol Ges 11:134–141
Brossut R (1976) Étude morphologique de la blatte myrmécophile Attaphila fungicola Wheeler. Insect Soc 23:167–174
Cahan S, Julian GE (1999) Fitness consequences of cooperative colony founding in the desert leaf-cutter ant Acromyrmex versicolor. Behav Ecol 10:585–591
Camargo RS, Forti LC, de Matos CAO, Brescovit AD (2015) Phoretic behaviour of Attacobius attarum (Roewer, 1935) (Araneae: Corinnidae: Corinninae) dispersion not associated with predation? J Natl Hist 49:1653–1658
Cole B (2009) The ecological setting of social evolution: the demography of ant populations. In: Gadau J, Fewell J (eds) Organization of insect societies: from genome to sociocomplexity. Harvard University Press, Massachusetts, pp 74–104
Erthal M, Tonhasca A (2001) Attacobius attarum spiders (Corinnidae): myrmecophilous predators of immature forms of the leaf-cutting ant Atta sexdens (Formicidae). Biotropica 33:374–376
Fowler HG (1987) Colonization patterns of the leaf-cutting ant, Atta bisphaerica Forel: evidence for population regulation. J Appl Entomol 104:102–105
Fowler H, Pereira Da Silva V, Forti LC, Saes N (1986) Population dynamics of leaf-cutting ants: a brief review. In: Lofgren CS (ed) Fire ants and leaf-cutting ants: biology and management. Westview Press, Boulder, pp 123–145
Greenwood M (1926) The natural duration of cancer. Rep Public Health Med Subj 33:1–26
Ichinose K, Rinaldi I, Forti LC (2004) Winged leaf-cutting ants on nuptial flights used as transport by Attacobius spiders for dispersal. Ecol Entomol 29:628–631
Jacoby M (1944) Observações e experiências sobre Atta sexdensrubropilosa Forel visando facilitar seu combate. Bol Min Agric Rio 12:1–55
Kaplan EL, Meier P (1958) Nonparametric estimation from incomplete observations. JASA 53:457–481
Krantz GW, Moser JC (2012) A new genus and species of Macrochelidae (Acari: Mesostigmata) associated with the texas leafcutting ant, Atta texana (Buckley) in Louisiana, USA. Int J Acarol 38:576–582
Marti HE, Carlson AL, Brown BV, Mueller UG (2015) Foundress queen mortality and early colony growth of the leafcutter ant, Atta texana (Formicidae: Hymenoptera). Insect Soc 62:357–363
Moser JC (1964) Inquiline roach responds to trail-marking substance of leaf-cutting ants. Science 143:1048–1049
Moser JC (1967) Mating activities of Atta texana (Hymenoptera: Formicidæ). Insect Soc 14:295–312
Moser JC (2006) Complete excavation and mapping of a texas leafcutting ant nest. Ann Entomol Soc Am 99:891–897
Moser JC, Bento JMS, Della Lucia TMC, Cameron RS, Heck NM (2004) Eye size and behaviour of day- and night-flying leaf cutting ant alates. J Zool 264:69–75
Mueller UG, Mikheyev AS, Hong E, Sen R, Warren DL, Solomon SE, Ishak HD, Cooper M, Miller JL, Shaffer KA, Juenger TE (2011) Evolution of cold-tolerant fungal symbionts permits winter fungiculture by leafcutter ants at the northern frontier of a tropical ant-fungus symbiosis. Proc Natl Acad Sci 108:4053–4056
Mueller UG, Mikheyev AS, Solomon SE, Cooper M (2011) Frontier mutualism: coevolutionary patterns at the northern range limit of the leaf-cutter ant-fungus symbiosis. Proc R Soc B Biol Sci 278:3050–3059
Navarrete-Heredia JL (2001) Beetles associated with Atta and Acromyrmex ants (Hymenoptera: Formicidae: Attini). Trans Am Entomol Soc 127:381–429
Nehring V, Dani FR, Calamai L, Turillazzi S, Bohn H, Klass KD, d’Ettore P (2016) Chemical disguise of myrmecophilous cockroaches and its implications for understanding nestmate recognition mechanisms in leaf-cutting ants. BMC Ecol 16:35
Perfecto I, Vandermeer J (1993) Distribution and turnover rate of a population of Atta cephalotes in a tropical rain forest in Costa Rica. Biotropica 25:316
Platnick NI, Baptista RLC (1995) On the spider genus Attacobius (Araneae: Dionycha). Am Mus Novit 3120:1–9
Prugnolle F, de Meeus T (2002) Inferring sex-biased dispersal from population genetic tools: a review. Heredity 88:161–165
Rodríguez JG, Montoya-Lerma J, Calle Z (2013) First record of Attaphila fungicola (Blattaria: Polyphagidae) in Atta cephalotes nests (Hymenoptera: Myrmicinae) in Colombia. Bol Cient Mus Hist Nat Univ Caldas 17:219–225
Roth LM (1995) Pseudoanaplectinia yumotoi, a new ovoviviparous myrmecophilous cockroach genus and species from Sarawak (Blattaria: Blattellidae; Blattellinae). Psyche J Entomol 102: 79–87
Sánchez-Peña SR (2005) Essays on organismal aspects of the fungus-growing ant symbiosis: ecology, experimental symbiont switches and fitness of Atta, and a new theory on the origin of ant fungiculture. Dissertation, University of Texas at Austin
Sánchez-Peña SR, Davis DR, Mueller UG (2003) A gregarious, mycophagous, myrmecophilous moth, Amydria anceps Walsingham (Lepidoptera: Acrolophidae), living in Atta mexicana (F. Smith) (Hymenoptera: Formicidae) spent fungal culture accumulations. Proc Entomol Soc Wash 105:186–194
Verhoeven KJ, Biere A (2013) Geographic parthenogenesis and plant-enemy interactions in the common dandelion. BMC Evol Biol 13:23
Vrijenhoek RC, Parker ED (2009) Geographical parthenogenesis: general purpose genotypes and frozen niche variation. In: Schön I, Martens K, Dijk P (eds) Lost sex: the evolutionary biology of parthenogenesis. Springer Netherlands, Dordrecht, pp 99–131
Waller DA, Moser JC (1990) Invertebrate enemies and nest associates of the leaf-cutting ant Atta texana (Buckley) (Formicidae, Attini). In: Vander Meer RK et al (eds) Applied myrmecology: a world perspective. Westview Press, Boulder, pp 256–273
Weber NA (1972) Gardening ants, the attines. American Philosophical Society, Philadelphia
Wheeler WM (1900) A new myrmecophile from the mushroom gardens of the texan leaf-cutting ant. Am Natl 34:851–862
Wheeler WM (1910) Ants: their structure, development and behavior. Columbia University Press, New York
Zepeda-Paulo F, Lavandero B, Mahéo F, Dion E, Outreman Y, Simon J-C, Figueroa CC (2015) Does sex-biased dispersal account for the lack of geographic and host-associated differentiation in introduced populations of an aphid parasitoid? Ecol Evol 5:2149–2161
Acknowledgements
We thank N. Jones, H. Marti, M. Dixon, T. Olson, and A. Santillana for help with collecting; J. Lee for field and lab assistance; C. Medici for field assistance; R. Plowes for permission to work at the Brackenridge Field Station; A. Wild for permission to include his photographs; K-D. Klass for help with identification of specimens; and D. Friedman, T. Stewart, F. Roces, C. Smith, A. Carlson, and E. Dietrich for comments on the manuscript. The study was funded by a Texas Ecolab award to ZIP and National Science Foundation award DEB-1354666 to UGM.
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Video clip of A. fungicola interacting with A. texana workers in Fungal Garden treatment. (MOV 23435 KB)
Video clip of female A. texana alate with attached A. fungicola entering non-natal A. texana nest in field. (MOV 21146 KB)
Video clip of A. fungicola on vectoring alate in lab colony.sx (MOV 15735 KB)
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Phillips, Z.I., Zhang, M.M. & Mueller, U.G. Dispersal of Attaphila fungicola, a symbiotic cockroach of leaf-cutter ants. Insect. Soc. 64, 277–284 (2017). https://doi.org/10.1007/s00040-016-0535-6
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DOI: https://doi.org/10.1007/s00040-016-0535-6