Life history, nest longevity, sex ratio, and nest architecture of the fungus-growing ant Mycetosoritis hartmanni (Formicidae: Attina)

PLOS ONE RESEARCH ARTICLE Life history, nest longevity, sex ratio, and nest architecture of the fungus-growing ant Mycetosoritis hartmanni (Formicidae: Attina) Ulrich G. Mueller ID1*, Anna G. Himler1,2, Caroline E. Farrior1 1 Department of Integrative Biology, University of Texas at Austin, Austin, TX, United States of America, 2 Department of Biology, College of Idaho, Caldwell, ID, United States of America a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Mueller UG, Himler AG, Farrior CE (2023) Life history, nest longevity, sex ratio, and nest architecture of the fungus-growing ant Mycetosoritis hartmanni (Formicidae: Attina). PLoS ONE 18(7): e0289146. https://doi.org/10.1371/ journal.pone.0289146 Editor: Volker Nehring, Albert-Ludwigs-Universitat Freiburg, GERMANY Received: November 23, 2022 Accepted: July 12, 2023 Published: July 26, 2023 Peer Review History: PLOS recognizes the benefits of transparency in the peer review process; therefore, we enable the publication of all of the content of peer review and author responses alongside final, published articles. The editorial history of this article is available here: https://doi.org/10.1371/journal.pone.0289146 Copyright: © 2023 Mueller et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: The Supporting Information contains all raw data and metadata in an Excel file, as well as the R-script used in the analyses of colony lifespan. * Abstract Mycetosoritis hartmanni is a rarely collected fungus-farming ant of North America. We describe life history and nest architecture for a M. hartmanni population in central Texas, USA. Colonies are monogynous with typically less than 100 workers (average 47.6 workers, maximum 148 workers). Nests occur always in sand and have a uniform architecture with 1–3 underground garden chambers arranged along a vertical tunnel, with the deepest gardens 50–70 cm deep. Foragers are active primarily between April and October. After reduced activity between November and February, egg laying by queens resumes in April, and the first worker pupae develop in early June. Reproductive females and males are reared primarily in July and August, with proportionally more females produced early in summer (protogyny). Mating flights and founding of new nests by mated females occur in late June to August, but may extend through September. For a cohort of 150 established nests (nests that had survived at least one year after nest founding), the estimated mortality rate was 0.41–0.53, the estimated average lifespan for these nests was 1.9–2.5 years, and the longest-living nests were observed to live for 6 years. These life-history parameters for M. hartmanni in central Texas are consistent with information from additional M. hartmanni nests observed throughout the range of this species from eastern Louisiana to southern Texas. Throughout its range in the USA, M. hartmanni can be locally very abundant in sunexposed, sandy soil. Abundance of M. hartmanni seems so far relatively unaffected by invasive fire ants, and at present M. hartmanni does not appear to be an endangered species. Introduction Mycetosoritis is among the least-studied genera of fungus-growing ants (tribe Attina), appearing typically as single, stray workers in surveys of ground-dwelling ants [1–14]. Since the original species description of M. hartmanni over 100 years ago [15], no reports have been published elucidating the biology of M. hartmanni, leading to the general belief that this fungus-growing ant species is exceedingly rare or difficult to find [2,16, 17]. Fungus-growing ants (subtribe Attina) are partners in an obligate symbiosis with fungi that they cultivate for food [15, 16, 18–20]. Phylogenetically, Attina ants are subdivided into two PLOS ONE | https://doi.org/10.1371/journal.pone.0289146 July 26, 2023 1 / 23 PLOS ONE Funding: The research was supported by funding from the National Science Foundation (Doctoral Dissertation Improvement Grant DEB-0206372 to AGH; CAREER award DEB-998379 and OPUS award DEB-1911443 to UGM); and the W.M. Wheeler Lost Pines Endowment from the University of Texas at Austin. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. There was no additional external funding received for this study. Competing interests: The authors have declared that no competing interests exist. Natural history of the fungus-farming ant Mycetosoritis hartmanni groups, a monophyletic group of higher Attina that include the well-researched leaf-cutter ants plus five genera closely related to leaf-cutters, and a second group called the lower Attina that includes less-studied, often cryptic, and phylogenetically more diverse genera. Mycetosoritis is one such understudied lower-Attina genus, the likely sister genus of the South American genus Mycetarotes [21–23]. The genus Mycetosoritis includes currently two described species, M. hartmanni [15] and M. vinsoni Mackay [2]. Mycetosoritis hartmanni ranges from the USA (Louisiana, Texas) across eastern Mexico to at least Honduras (Project LLAMA, [14]). Collections identified as M. vinsoni have been reported only from north-west Costa Rica [2, 6] and south-east Mexico [9], but the Mexican collections of M vinsoni could be misidentified M. hartmanni. Whether M vinsoni is a separate species from M. hartmanni is unclear [24, 25], as the morphological characters used by Mackay [2] to identify M. vinsoni are rather subtle and fall within the morphological variation known for M. hartmanni [24]. For example, workers from four nests collected by one of the authors (UGM) in 1995 in the Naranjo Valley in Parque Nacional Santa Rosa, Costa Rica, appear to be M. hartmanni, not M. vinsoni (UG Mueller, unpublished observations; [26]). Although future phylogenomic analyses may confirm the species status of M. vinsoni, it is also possible that the genus Mycetosoritis consists actually of only a single species, M. hartmanni, ranging from the USA to Costa Rica. The little that is known about the biology of M. hartmanni derives entirely from the original species and genus description by William Morton Wheeler [15]; hartmanni is the type species of the genus Mycetosoritis). During Wheeler’s last few months as faculty at the University of Texas at Austin, and before he then became curator at the American Museum of Natural History in New York, Wheeler discovered on 09. May 1903 a large population of M. hartmanni in sandy, rural habitat just east of the City of Austin, Texas: “There were hundreds of their nests, often within a few decimeters of one another, in the fields or in clearings among the oaks and whenever the sand was fully exposed to sun” (page 761 in [15]). Wheeler (...truncated)