Abstract
Myrmecochory is a widespread mutualism in which plants benefit from seed dispersal services by ants. Ants might also be providing seeds with an additional byproduct benefit via reduced plant pathogen loads in the ant nest environment through their antimicrobial glandular secretions. We investigate this byproduct benefit by identifying fungal communities in ant nests and surrounding environments and quantifying fungal community change (1) through time, (2) between different nest substrates, and (3) as a function of average ant activity levels within nests (based on observed ant activity at nest entrances throughout the summer). We split fungal communities by functional guild to determine seed-dispersing ant-induced changes in the overall fungal community, the animal pathogen fungal community, the plant pathogen fungal community, and the myrmecochore pathogen fungal community. Nest substrate (soil or log) explained much of the variation in fungal community dissimilarity, while substrate occupation (ant nest or control sample) and time had no influence on fungal community composition. Average ant activity had no effect on the community turnover in fungal communities except for the myrmecochore pathogenic fungal community. In this community, higher ant activity throughout the summer resulted in more fluctuation in the pathogenic community in the ant nest. Our results are not consistent with a byproduct benefit framework in myrmecochory, but suggest that nest substrate drives dissimilarity in fungal communities. The influence of nest substrate on fungal communities has important implications for seeds taken into ant nests, as well as ant nest location choice by queens and during nest relocation.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdulina GA, Gazaliev AM, Baikenova GG, Fazylov SD, Kudaibergenova SZ (2002) A comparative study of the antibacterial and antifungal activity of anabasine hydrochloride and dialkythiophosphates. Pharm Chem J 36:119–120. https://doi.org/10.1023/A:1019670008920
Anthony WE, Palmer-Young EC, Leonard AS, Irwin RE, Adler LS (2015) Testing dose-dependent effects of the nectar alkaloid anabasine on trypanosome parasite loads in adult bumble bees. PLoS ONE 10:e0142496. https://doi.org/10.1371/journal.pone.0142496
Attygalle AB, Kern F, Huang Q, Meinwald J (1998) Trail pheromone of the myrmicine ant Aphaenogaster rudis (Hymenoptera: Formicidae). Naturwissenschaften 85:38–41. https://doi.org/10.1007/s001140050450
Beattie AJ (1985) The dispersal of seeds and fruits by ants. The evolutionary ecology of ant-plant mutualisms. Cambridge University Press, Cambridge, pp 73–95. https://doi.org/10.1017/CBO9780511721878.007
Beattie AJ, Culver DC (1981) The guild of myrmecochores in the herbaceous flora of West Virgina forests. Ecology 62:107–115. https://doi.org/10.2307/1936674
Beattie AJ, Culver DC (1982) Inhumation: how ants and other invertebrates help seeds. Nature 297:627. https://doi.org/10.1038/297627a0
Beattie AJ, Turnbull C, Hough T, Jobson S, Knox RB (1985) The vulnerability of pollen and fungal spores to ant secretions: evidence and some evolutionary implications. Am J Bot 72:606–614. https://doi.org/10.1002/j.1537-2197.1985.tb08315.x
Berg-Binder MC, Suarez AV (2012) Testing the directed dispersal hypothesis: are native ant mounds (Formica sp.) favorable microhabitats for an invasive plant? Oecologia 169:763–772. https://doi.org/10.1007/s00442-011-2243-2
Bot A, Ortius-Lechner D, Finster K, Maile R, Boomsma J (2002) Variable sensitivity of fungal and bacteria to compounds produced by the metapleural glands of leaf-cutting ants. Insectes Soc 49:363–370. https://doi.org/10.1007/PL00012660
Brough EJ (1983) The antimicrobial activity of the mandibular gland secretion of a formicine ant, Calomyrmex sp. (Hymenoptera: Formicidae). J Invertebr Pathol 42:306–311. https://doi.org/10.1016/0022-2011(83)90168-4
Brutsch T, Felden A, Reber A, Chapuisat M (2014) Ant queens (Hymenoptera: Formicidae) are attracted to fungal pathogens during the initial stage of colony founding. Myrmecol News 20:71–76
Cabrera A, Williams D, Hernandez JV, Caetano FH, Jaffe K (2004) Metapleural- and postpharyngeal-gland secretions from workers of the ants Solenopsis invicta and S. geminata. Chem Biodivers 1:303–311. https://doi.org/10.1002/cbdv.200490027
Canner JE, Dunn RR, Giladi I, Gross K (2012) Redispersal of seeds by a keystone ant augments the spread of common wildflowers. Acta Oecologica 40:31–39. https://doi.org/10.1016/j.actao.2012.02.004
Carrino-Kyker SR et al (2016) Mycorrhizal fungal communities respond to experimental elevation of soil pH and P availability in temperate hardwood forests. FEMS Microbiol Ecol. https://doi.org/10.1093/femsec/fiw024
Chao A, Gotelli NJ, Hsieh TC, Sander EL, Ma KH, Colwell RK, Ellison AM (2014) Rarefaction and extrapolation with hill numbers: a framework for sampling and estimation in species diversity studies. Ecol Monogr 84:45–67. https://doi.org/10.1890/13-0133.1
Charney N, Record S (2012) vegetarian: Jost Diversity Measures for Community Data. R package version 1.2. https://CRAN.Rproject.org/package=vegetarian
Cregger MA, Veach AM, Yang ZK, Crouch MJ, Vilgalys R, Tuskan GA, Schadt CW (2018) The Populus holobiont: dissecting the effects of plant niches and genotype on the microbiome. Microbiome 6:31. https://doi.org/10.1186/s40168-018-0413-8
Culver DC, Beattie AJ (1980) The fate of viola seeds dispersed by ants. Am J Bot 67:710–714. https://doi.org/10.1002/j.1537-2197.1980.tb07701.x
Davidson DW, Morton SR (1981) Myrmecochory in some plants (F. chenopodiaceae) of the Australian arid zone. Oecologia 50:357–366. https://doi.org/10.1007/BF00344976
Fernandez-Marin H, Zimmerman JK, Rehner SA, Wcislo WT (2006) Active use of the metapleural glands by ants in controlling fungal infection. Proc Royal Soc B 273:1689–1695. https://doi.org/10.1098/rspb.2006.3492
Fernandez-Marin H, Nash DR, Higginbotham S, Estrada C, van Zweden JS, d’Ettorre P, Wcislo WT, Boomsma JJ (2015) Functional role of phenylacetic acid from metapleural gland secretions in controlling fungal pathogens in evolutionarily derived leaf-cutting ants. Proc Royal Soc B 282:20150212. https://doi.org/10.1098/rspb.2015.0212
Fischer RC, Ölzant SM, Wanek W, Mayer V (2005) The fate of Corydalis cava elaiosomes within an ant colony of Myrmica rubra: elaiosomes are preferentially fed to larvae. Insectes Soc 52:55–62. https://doi.org/10.1007/s00040-004-0773-x
Fox J, Weisberg S (2019) An {R} Companion to Applied Regression, Third Edition. Thousand Oaks CA: Sage. https://socialsciences.mcmaster.ca/jfox/Books/Companion/
Giladi I (2006) Choosing benefits or partners: a review of the evidence for the evolution of myrmecochory. Oikos 112:481–492
Goldmann K, Schoning I, Buscot F, Wubet T (2015) Forest management type influences diversity and community composition of soil fungi across temperate forest ecosystems. Front Microbiol 6:1300. https://doi.org/10.3389/fmicb.2015.01300
Hill MO (1973) Diversity and evenness: a unifying notation and its consequences. Ecology 54:427–432. https://doi.org/10.2307/1934352
Horvitz CC, Schemske DW (1986) Ant-nest soil and seedling growth in a neotropical ant-dispersed herb. Oecologia 70:318–320. https://doi.org/10.1007/BF00379258
Jones TH, Brunner SR, Edwards AA, Davidson DW, Snelling RR (2005) 6-Alkylsalicylic acids and 6-akylresorcylic acids from ants in the genus Crematogaster from Brunei. J Chem Ecol 31:407–417. https://doi.org/10.1007/s10886-005-1349-6
Jost L (2006) Entropy and diversity. Oikos 113:363–375. https://doi.org/10.1111/j.2006.0030-1299.14714.x
Jost L (2007) Partitioning diversity into independent alpha and beta components. Ecology 88:2427–2439. https://doi.org/10.1890/06-1736.1
Khlifa R, Paquette A, Messier C, Reich PB, Munson AD (2017) Do temperate tree species diversity and identity influence soil microbial community function and composition? Ecol Evol 7:7965–7974. https://doi.org/10.1002/ece3.3313
Kogel KH, Franken P, Huckelhoven R (2006) Endophyte or parasite–what decides? Curr Opin Plant Biol 9:358–363. https://doi.org/10.1016/j.pbi.2006.05.001
Leclercq S, Charles S, Daloze D, Braekman J-C, Aron S, Pasteels JM (2001) Absolute configuration of anabasine from Messor and Aphaenogaster ants. J Chem Ecol 27:945–952. https://doi.org/10.1023/A:1010335003297
Legendre P, Legendre L (2012) Numerical Ecology 3rd, English edn. Elsevier, Amsterdam
Lengyel S, Gove AD, Latimer AM, Majer JD, Dunn RR (2010) Convergent evolution of seed dispersal by ants, and phylogeny and biogeography in flowering plants: a global survey. Perspect Plant Ecol Evol Syst 12:43–55. https://doi.org/10.1016/j.ppees.2009.08.001
Lenoir A, Benoist A, Hefetz A, Francke W, Cerdá X, Boulay R (2011) Trail-following behaviour in two Aphaenogaster ants. Chemoecology 21:83–88. https://doi.org/10.1007/s00049-011-0071-9
Lubertazzi D (2012) The biology and natural history of Aphaenogaster rudis. Psyche 2012:1–11. https://doi.org/10.1155/2012/752815
Marion ZH, Fordyce JA, Fitzpatrick BM (2017) Pairwise beta diversity resolves an underappreciated source of confusion in calculating species turnover. Ecology 98:933–939. https://doi.org/10.1002/ecy.1753
McGinley MA, Dhillion SS, Neumann JC (1994) Environmental heterogeneity and seedling establishment: ant-plant-microbe interactions. Funct Ecol 8:607–615. https://doi.org/10.2307/2389922
Meunier J (2015) Social immunity and the evolution of group living in insects. Proc Royal Soc B 370:20140102. https://doi.org/10.1098/rstb.2014.0102
Ness JH, Morin DF, Giladi I (2009) Uncommon specialization in a mutualism between a temperate herbaceous plant guild and an ant: are Aphaenogaster ants keystone mutualists? Oikos 118:1793–1804. https://doi.org/10.1111/j.1600-0706.2009.17430.x
Nguyen NH, Song Z, Bates ST, Branco S, Tedersoo L, Menke J, Schilling JS, Kennedy PG (2016) FUNGuild: an open annotation tool for parsing fungal community datasets by ecological guild. Fungal Ecol 20:241–248. https://doi.org/10.1016/j.funeco.2015.06.006
Nilsson R, Larsson KH, Taylor AFS, Bengtsson-Palme J, Jeppesen TS, Schigel D, Kennedy P, Picard K, Glöckner FO, Tedersoo L, Saar I, Kõljalg U, Abarenkov K (2018) The UNITE database for molecular identification of fungi: handling dark taxa and parallel taxonomic classifications. Nucleic Acids Res. https://doi.org/10.1093/nar/gky1022
Oksanen J, Guillaume Blanchet F, Friendly M, Kindt R, Legendre P, McGlinn D, Minchin PR, O'Hara RB, Simpson GL, Solymos P, Stevens MHH, Szoecs E, Wagner H (2019) Vegan: community ecology package. R package version 2.5-6. https://CRAN.R-project.org/package=vegan
Osburn ED, McBride SG, Aylward FO, Badgley BD, Strahm BD, Knoepp JD, Barrett JE (2019) Soil bacterial and fungal communities exhibit distinct long-term responses to disturbance in temperate forests. Front Microbiol 10:2872. https://doi.org/10.3389/fmicb.2019.02872
Rico-Gray V, Oliveira P (2007) Mutualism from antagonism: ants as primary seed dispersers. Ecology and evolution of ant-plant interactions. University of Chicago Press, Chicago, Il, pp 42–67. https://doi.org/10.7208/chicago/9780226713540.003.0003
Sachs JL, Mueller UG, Wilcox TP, Bull JJ (2004) The evolution of cooperation. Q Rev Biol 79:135–160. https://doi.org/10.1086/383541
Schultz MN (2014) Effects of myrmecochore species abundance, diversity, and fruiting phenology on Aphaenogaster (Hymenoptera: Formicidae) nesting and foraging in Southern Appalachian rich cove forests. Master thesis, Western Carolina University, Cullowhee, North Carolina, USA
Schulz B, Boyle C (2005) The endophytic continuum. Mycol Res 109:661–686. https://doi.org/10.1017/s095375620500273x
Smallwood J, Culver D (1997) Colony movements of some North American ants. J Anim Ecol 48:373–382. https://doi.org/10.2307/4167
Talbot M (1946) Daily fluctuations in aboveground activity of three species of ants. Ecology 27:65–70. https://doi.org/10.2307/1931019
Tarsa C, McMillan A, Warren RJ (2018) Plant pathogenic fungi decrease in soil inhabited by seed-dispersing ants. Insectes Soc 65:315–321. https://doi.org/10.1007/s00040-018-0618-7
Tragust S, Mitteregger B, Barone V, Konrad M, Ugelvig LV, Cremer S (2013) Ants disinfect fungus-exposed brood by oral uptake and spread of their poison. Curr Biol 23:76–82. https://doi.org/10.1016/j.cub.2012.11.034
Tranter C, Graystock P, Shaw C, Lopes JFS, Hughes WOH (2013) Sanitizing the fortress: protection of ant brood and nest material by worker antibiotics. Behav Ecol Sociobiol 68:499–507. https://doi.org/10.1007/s00265-013-1664-9
Umphrey GJ (1996) Morphometric discrimination among sibling species in the fulva -rudis –texana complex of the ant genus Aphaenogaster (Hymenoptera: Formicidae). Can J Zool 74:528–559. https://doi.org/10.1139/z96-060
Vander Meer R (2012) Ant interactions with soil organisms and associated semiochemicals. J Chem Ecol 38:728–745. https://doi.org/10.1007/s10886-012-0140-8
Vieira AS, Morgan ED, Drijfhout FP, Camargo-Mathias MI (2012) Chemical composition of metapleural gland secretions of fungus-growing and non-fungus-growing ants. J Chem Ecol 38:1289–1297. https://doi.org/10.1007/s10886-012-0185-8
Voriskova J, Brabcova V, Cajthaml T, Baldrian P (2014) Seasonal dynamics of fungal communities in a temperate oak forest soil. New Phytol 201:269–278. https://doi.org/10.1111/nph.12481
Warren RJ, Elliott KJ, Giladi I, King JR, Bradford MA (2019) Field experiments show contradictory short- and long-term myrmecochorous plant impacts on seed-dispersing ants. Ecol Entomol 44:30–39. https://doi.org/10.1111/een.12666
Wheeler JW, Olubajo O, Storm CB, Duffield RM (1981) Anabaseine: venom alkaloid of Aphaenogaster ants. Science 211:1051–1052. https://doi.org/10.1126/science.211.4486.1051
Yek SH, Mueller UG (2011) The metapleural gland of ants. Biol Rev 86:774–791. https://doi.org/10.1111/j.1469-185X.2010.00170.x
Yek SH, Nash DR, Jensen AB, Boomsma JJ (2012) Regulation and specificity of antifungal metapleural gland secretion in leaf-cutting ants. Proc Royal Soc B 279:4215–4222. https://doi.org/10.1098/rspb.2012.1458
Zettler JA, McInnis TM Jr, Allen CR, Spira TP (2002) Biodiversity of fungi in red imported fire ant (Hymenoptera: Formicidae) mounds. Ann Entomol Soc Am 95:487–491. https://doi.org/10.1603/0013-8746(2002)095[0487:BOFIRI]2.0.CO;2
Acknowledgements
CLL was funded by the Margaret Walton Scholarship from Mountain Lake Biological Station. Field work was funded by the Breedlove, Dennis Fund for Student Botanical Field Experiences from the TENN Herbarium and lab work was funded by a Student Faculty Research Award to CLL and CK from the University of Tennessee, Knoxville. JAF was supported by National Science Foundation grant DEB-1638922. Collections were done through permitting from The Nature Conservancy and the Virginia Department of Conservation and Recreation’s Natural Heritage Program. Thanks to Sam Truslow and Ryan Klopf for assistance with field site access. Austin Davis, Henry Davie, and Jamie Albert assisted with field collections. Thanks to Kimberly Gwinn, Kimberly Sheldon, Sam Borstein, Veronica Brown and two anonymous reviewers for suggestions on earlier versions of this manuscript.
Author information
Authors and Affiliations
Contributions
CLL and CK originally formulated the idea and developed methodology. CLL conducted all field and lab work. JAF generated the statistical framework and JAF and CLL conducted all statistical analyses. CLL wrote the first draft of the manuscript and CK and JAF commented on subsequent versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Human and animal rights
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Caroline Müller.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Lash, C.L., Fordyce, J.A. & Kwit, C. Nest substrate, more than ant activity, drives fungal pathogen community dissimilarity in seed-dispersing ant nests. Oecologia 194, 649–657 (2020). https://doi.org/10.1007/s00442-020-04796-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-020-04796-5