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Dispersal of Attaphila Fungicola, a Symbiotic Cockroach of Leaf-Cutter Ants Enter Older, Established Colonies, While Still Attached to Attaphila Fungicola and A

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Dispersal of Attaphila Fungicola, a Symbiotic Cockroach of Leaf-Cutter Ants Enter Older, Established Colonies, While Still Attached to Attaphila Fungicola and A Insect. Soc. (2017) 64:277–284 DOI 10.1007/s00040-016-0535-6 Insectes Sociaux RESEARCH ARTICLE Dispersal of Attaphila fungicola, a symbiotic cockroach of leaf- cutter ants Z. I. Phillips1 · M. M. Zhang2 · U. G. Mueller1 Received: 9 October 2015 / Revised: 9 November 2016 / Accepted: 1 December 2016 / Published online: 11 February 2017 © International Union for the Study of Social Insects (IUSSI) 2017 Abstract The myrmecophile cockroach Attaphila fungi- to vectoring alates entered the nest compared to unat- cola lives in the nests of leaf-cutter ants (Atta texana and tached A. fungicola. We also placed A. fungicola attached A. cephalotes) and uses the female winged reproductives to vectoring alates in a foraging chamber of a laboratory (i.e., female alates) of its host as vectors for the frst phase colony to determine if, once in the nest, A. fungicola could of its dispersal. It is unknown whether A. fungicola remain navigate to the fungal garden chamber; 100% of A. fungi- with vectoring A. texana females after mating fights and cola detached from their vectoring alates and entered the throughout A. texana nest founding and subsequent colony fungal garden chamber. We tested alate preference of A. development, or if the symbiotic cockroaches disperse fungicola by placing A. fungicola separately in containers to established A. texana colonies, either on their own or with one A. texana female alate and one male alate; after while still attached to vectoring A. texana females. We cap- 2 h, 71% of A. fungicola were attached to female alates tured A. fungicola attached to A. texana female alates as and 0% to male alates. Finally, we report the frst record they prepared for mating fights and measured their survi- of a male A. fungicola collected during a mating fight of vorship in artifcial brood chambers with de-alate, recently A. texana. These observations accumulated from feld and mated A. texana queens and their incipient gardens, and in laboratory studies suggest that A. fungicola vectored by A. a non-natal established fungal garden tended by A. texana texana female alates may not remain with foundresses, but workers. After 13 days, 100% of A. fungicola had died in instead disperse between established colonies through one brood chambers with queens, while 100% of A. fungicola or more alternative mechanisms. This study helps elucidate remained alive in the fungal garden chamber. We tested the a tripartite ant-fungus-cockroach interaction, and provides feasibility of alternative modes of dispersal to established a foundation for future research on Attaphila dispersal and colonies by placing A. fungicola attached and unattached reproductive biology. to vectoring female alates in the proximity of an estab- lished A. texana colony directly after a mating fight, and Keywords Attaphila · Atta texana · Dispersal · Inquiline · recorded whether A. fungicola entered the non-natal nest. Myrmecophile · Phoretic · Social parasitism · Symbiosis A signifcantly higher proportion of A. fungicola attached Introduction Electronic supplementary material The online version of this article (doi:10.1007/s00040-016-0535-6) contains supplementary material, which is available to authorized users. Nests of leaf-cutter ants (Atta and Acromyrmex) are inhab- ited by diverse arthropods, such as mites, spiders, beetles, * Z. I. Phillips fies, moths, and other insects (Waller and Moser 1990; [email protected] Erthal and Tonhasca 2001; Navarrete-Heredia 2001; 1 Department of Integrative Biology, University of Texas, Sánchez-Peñaet al. 2003; Krantz and Moser 2012), but the Austin, TX 78712, USA nature of the associations between ant host and arthropod 2 Department of Statistics and Data Science, University “guests” is not well understood. Frequent guests inhab- of Texas, Austin, TX 78712, USA iting leaf-cutter fungus-garden chambers are Attaphila Vol.:(0123456789)1 3 278 Z. I. Phillips et al. cockroaches (Wheeler 1910; Moser 1967), a genus of six mating fight just before dawn, individuals of A. fungicola described species (Rodríguez et al. 2013). Attaphila are can be readily observed riding on female alates (Fig. 2) small (up to 3.5 mm in length), wingless, possess well- aggregating on the nest mound (Moser 1967) and also on developed arolia (i.e., tarsal pads) that aid in attaching to female alates when they depart from their natal mound to the cuticle of the ants, and appear to use modifed maxil- begin their mating fight (Phillips and Mueller unpublished lary palps to follow the chemical trails produced by leaf- observation). We are unaware of any observation of A. fun- cutter workers (Wheeler 1900; Moser 1964; Brossut 1976). gicola riding on male alates. The specialized morphology and behavior of Attaphila, and These accumulated observations suggest that A. fungi- the absence of any observations of free-living individuals cola use female alates of A. texana as vectors to disperse (i.e., not in association with leaf-cutter ants) suggest that from their natal host colony. However, following success- Attaphila is an obligate symbiont of leaf-cutter colonies. ful departure by dispersing A. texana female alates, it is Attaphila fungicola Wheeler (Wheeler 1900) inhabits unclear whether A. fungicola remain with their vector- colonies of Atta texana in Texas and Louisiana at the north- ing A. texana females as these aspiring queens attempt to ern range limit of the leaf-cutter distribution (Mueller et al. found new colonies, or if A. fungicola enter previously 2011a, b). A. fungicola spends almost its entire life inside established leaf-cutter colonies. Previous observations pro- the host nest, apparently within the fungal garden chambers vide limited support for either possibility. In one report, tended by the ants (Fig. 1) (Wheeler 1900; Moser 2006; Attaphila was observed “running on the ground…like tiny Rodríguez et al. 2013). Nearly all observations of A. fun- beetles” (Sánchez-Peña 2005) in close proximity to foun- gicola outside of the nest have occurred during the early dresses of Atta mexicana that had alighted away from their phase of the mating fights of A. texana when a colony’s natal nest, indicating the cockroaches had detached from winged reproductives (i.e., alates) gather on the nest mound the foundresses after the mating fight to disperse inde- in aggregations of several thousand individuals (Moser pendently before nest founding was complete. We are also 1964, 1967; Phillips and Mueller unpublished observa- unaware of any observations of A. fungicola attached to tions). During predawn preparations and during the actual nest-excavating foundresses, and we have found so far no A. fungicola in approximately 150 incipient A. texana nests excavated in Texas (Mueller unpublished observation). In contrast, Moser (1967, p. 304) reports that A. fungicola can be found in “new burrows made by queens”, but the fre- quency and location of these observations are not reported. Although the destination of A. fungicola directly after A. texana mating fights is unresolved, their likely obli- gate association with leaf-cutter colonies suggests three non-exclusive alternatives for their dispersal: (1) A. fungi- cola accompany foundresses into their sealed (i.e., claus- tral) brood chambers, where they remain as the incipient colony develops; (2) A. fungicola abandon foundresses soon after mating fights and disperse to the fungal gar- dens of older, established colonies; and (3) A. fungicola Fig. 1 A. fungicola in fungal garden of A. texana Fig. 2 A. fungicola attached to A. texana female alate 1 3 279 Dispersal of Attaphila fungicola, a symbiotic cockroach of leaf-cutter ants enter older, established colonies, while still attached to Attaphila fungicola and A. texana queen survivorship vectoring female alates. The costs associated with the frst strategy include remaining with young A. texana col- Atta texana foundresses (n = 52) searching for nest sites onies subject to high mortality rates, and the costs of the were collected from a parking lot in Cedar Park, TX second and third strategy include the challenge of landing (30°19′5.86"N 97°39′34.72″W) on 7 May 2015 and trans- in the proximity of, locating and integrating into estab- ported to the laboratory. We transferred each foundress into lished A. texana colonies, and specifcally into a fungal an artifcial brood chamber constructed from a 5-dram vial garden chamber. In this study, as a test of the viability flled 75% with moistened dental plaster. In addition, we of dispersal mechanism (1), we compared the survi- constructed an artifcial fungal garden chamber by trans- vorship of A. fungicola captured during mating fights ferring approximately 207 cm³ of fungal garden, includ- between those placed with foundresses, in isolation, and ing the workers tending it, from a lab colony of A. texana in a fungus garden maintained by workers. To test disper- into a round translucent plastic container (4 cm × 11 cm sal mechanisms (2) and (3), we conducted a feld and lab diameter). We used a digital microscope camera (Dino- experiment representing these possible strategies used Lite AM3111T) to flm interactions between A. fungicola by A. fungicola to move from an alighting female alate and A. texana workers in the artifcial garden (see Online into the nest and fungal garden of a non-natal established Resource 1). colony. In addition, we conducted the frst test of A. fun- Within 48 h of alate capture, we randomly assigned A. gicola preference to associate with either female or male fungicola to diferent treatments by transferring 26 A. fun- alates of A. texana. gicola into separate artifcial brood chambers, each housing an A. texana foundress captured after mating fights (Queen treatment), 26 A. fungicola into separate artifcial brood chambers without A. texana (Isolation treatment, Control), Methods and 23 A. fungicola together into the artifcial fungal gar- den chamber (Fungal Garden treatment). The number of Collection of Atta texana and Attaphila fungicola A. fungicola placed in the Fungal Garden treatment was based approximately on W.
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