in

Ectoparasitic fungi of Myrmica ants alter the success of parasitic butterflies

  • 1.

    Frank, S. A. Models of parasite virulence. Q. Rev. Biol.  https://doi.org/10.1086/419267 (1996).

    Article 
    PubMed 

    Google Scholar 

  • 2.

    Dobson, A. P. The population dynamics of competition between parasites. Parasitology https://doi.org/10.1017/S0031182000057401 (1985).

    Article 
    PubMed 

    Google Scholar 

  • 3.

    Haelewaters, D. et al. Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi. PeerJ https://doi.org/10.7717/peerj.10110 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 4.

    Shapiro-Ilan, D. I., Bruck, D. J. & Lacey, L. A. Principles of Epizootiology and Microbial Control. In Insect Pathology 29–72 (Elsevier, 2012). https://doi.org/10.1016/B978-0-12-384984-7.00003-8.

  • 5.

    Renkema, J. M. & Cuthbertson, A. G. S. Impact of multiple natural enemies on immature Drosophila suzukii in strawberries and blueberries. Biocontrol https://doi.org/10.1007/s10526-018-9874-8 (2018).

    Article 

    Google Scholar 

  • 6.

    Furlong, M. & Pell, J. Interactions between entomopathogenic fungi and other arthropods natural enemies. In Insect-Fungal Associations, Ecology and Evolution (eds Vega, F. & Blackwell, M.) 51–73 (Oxford University Press, 2005).

    Google Scholar 

  • 7.

    Lafferty, K. D. Interacting parasites. Science https://doi.org/10.1126/science.1196915 (2010).

    Article 
    PubMed 

    Google Scholar 

  • 8.

    Price, S. L. et al. Recent findings in fungus-growing ants: evolution, ecology, and behavior of a complex microbial symbiosis. In Genes, Behaviors and Evolution of Social Insects (eds Azuma, N. & Higashi, S.) 255–280 (Hokkaido University Press, 2003).

    Google Scholar 

  • 9.

    Telfer, S. et al. Species interactions in a parasite community drive infection risk in a wildlife population. Science https://doi.org/10.1126/science.1190333 (2010).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 10.

    Carlson, C. J. et al. A global parasite conservation plan. Biol. Conserv. https://doi.org/10.1016/j.biocon.2020.108596 (2020).

    Article 

    Google Scholar 

  • 11.

    Colwell, R. K., Dunn, R. R. & Harris, N. C. Coextinction and persistence of dependent species in a changing world. Annu. Rev. Ecol. Evol. Syst. https://doi.org/10.1146/annurev-ecolsys-110411-160304 (2012).

    Article 

    Google Scholar 

  • 12.

    Gagne, R. B. et al. Parasites as conservation tools. Conserv. Biol. https://doi.org/10.1111/cobi.13719 (2021).

    Article 
    PubMed 

    Google Scholar 

  • 13.

    Csősz, S. & Majoros, G. Ontogenetic origin of mermithogenic Myrmica phenotypes (Hymenoptera, Formicidae). Insectes Soc.  https://doi.org/10.1007/s00040-008-1040-3 (2009).

    Article 

    Google Scholar 

  • 14.

    Csata, E. et al. Lock-picks: fungal infection facilitates the intrusion of strangers into ant colonies. Sci. Rep. https://doi.org/10.1038/srep46323 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 15.

    Pearson, B. & Raybould, A. F. The effects of antibiotics on the development of larvae and the possible role of bacterial load in caste determination and diapause in Myrmica rubra (Hymenoptera: Formicidae). Sociobiology 31, 77–90 (1998).

    Google Scholar 

  • 16.

    Schmid Hempel, P. Evolutionary Parasitology—The Integrated Study of Infections, Immunology, Ecology, and Genetics (Oxford University Press, 2011).

    Google Scholar 

  • 17.

    Donisthorpe, J. K. The Guests of British Ants—Their Habits and Life Histories (George Routledge And Sons, Limited, 1927).

    Google Scholar 

  • 18.

    Hölldobler, B. E. & Wilson, E. O. The Ants (The Belknap Press of Harvard University Press, 1990).

    Book 

    Google Scholar 

  • 19.

    Buschinger, A. Social parasitism among ants: A review (Hymenoptera: Formicidae). Myrmecol. News 12, 219–235 (2009).

    Google Scholar 

  • 20.

    Quevillon, L. E. The Ecology, Epidemiology, and Evolution of Parasites Infecting Ants (Hymenoptera: Formicidae) (Pennsylvania State University, 2018).

    Google Scholar 

  • 21.

    Quevillon, L. E. & Hughes, D. P. Pathogens, parasites, and parasitoids of ants: a synthesis of parasite biodiversity and epide-miological traits. BioRxiv https://doi.org/10.1101/384495 (2018).

    Article 

    Google Scholar 

  • 22.

    Di Salvo, M. et al. The microbiome of the Maculinea-Myrmica host-parasite interaction. Sci. Rep. https://doi.org/10.1038/s41598-019-44514-7 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 23.

    Witek, M., Barbero, F. & Markó, B. Myrmica ants host highly diverse parasitic communities: from social parasites to microbes. Insectes Soc. https://doi.org/10.1007/s00040-014-0362-6 (2014).

    Article 

    Google Scholar 

  • 24.

    Witek, M. et al. Interspecific relationships in co-occurring populations of social parasites and their host ants. Biol. J. Linn. Soc. https://doi.org/10.1111/bij.12074 (2013).

    Article 

    Google Scholar 

  • 25.

    Tartally, A. et al. Patterns of host use by brood parasitic Maculinea butterflies across Europe. Philos. Trans. R Soc. B Biol. Sci. https://doi.org/10.1098/rstb.2018.0202 (2019).

    Article 

    Google Scholar 

  • 26.

    Wardlaw, J. C., Thomas, J. A. & Elmes, G. W. Do Maculinea rebeli caterpillars provide vestigial mutualistic benefits to ants when living as social parasites inside Myrmica ant nests? Entomol. Exp. Appl. https://doi.org/10.1046/j.1570-7458.2000.00646.x (2000).

    Article 

    Google Scholar 

  • 27.

    Thomas, J. A. & Wardlaw, J. C. The capacity of a Myrmica ant nest to support a predacious species of Maculinea butterfly. Oecologia https://doi.org/10.1007/BF00317247 (1992).

    Article 
    PubMed 

    Google Scholar 

  • 28.

    Csata, E., Billen, J., Bernadou, A., Heinze, J. & Markó, B. Infection-related variation in cuticle thickness in the ant Myrmica scabrinodis (Hymenoptera: Formicidae). Insectes Soc. https://doi.org/10.1007/s00040-018-0628-5 (2018).

    Article 

    Google Scholar 

  • 29.

    Csősz, S., Rádai, Z., Tartally, A., Ballai, L. E. & Báthori, F. Ectoparasitic fungi Rickia wasmannii infection is associated with smaller body size in Myrmica ants. Sci. Rep. https://doi.org/10.1038/s41598-021-93583-0 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 30.

    Csata, E., Erős, K. & Markó, B. Effects of the ectoparasitic fungus Rickia wasmannii on its ant host Myrmica scabrinodis: Changes in host mortality and behavior. Insectes Soc. https://doi.org/10.1007/s00040-014-0349-3 (2014).

    Article 

    Google Scholar 

  • 31.

    Báthori, F., Rádai, Z. & Tartally, A. The effect of Rickia wasmannii (Ascomycota, Laboulbeniales) on the aggression and boldness of Myrmica scabrinodis (Hymenoptera, Formicidae). J. Hymenopt. Res. https://doi.org/10.3897/jhr.58.13253 (2017).

    Article 

    Google Scholar 

  • 32.

    Báthori, F., Csata, E. & Tartally, A. Rickia wasmannii increases the need for water in Myrmica scabrinodis (Ascomycota: Laboulbeniales; Hymenoptera: Formicidae). J. Invertebr. Pathol. https://doi.org/10.1016/j.jip.2015.01.005 (2015).

    Article 
    PubMed 

    Google Scholar 

  • 33.

    Tartally, A. Myrmecophily of Maculinea Butterflies in the Carpathian Basin (Lepidoptera: Lycaenidae), PhD thesis, https://dea.lib.unideb.hu/dea/handle/2437/78921 (University of Debrecen, Hungary, 2008)

    Google Scholar 

  • 34.

    Elmes, G. W., Wardlaw, J. C., Schönrogge, K., Thomas, J. A. & Clarke, R. T. Food stress causes differential survival of socially parasitic caterpillars of Maculinea rebeli integrated in colonies of host and non-host Myrmica ant species. Entomol. Exp. Appl. https://doi.org/10.1111/j.0013-8703.2004.00121.x (2004).

    Article 

    Google Scholar 

  • 35.

    Nash, D. R., Als, T. D. & Boomsma, J. J. Survival and growth of parasitic Maculinea alcon caterpillars (Lepidoptera, Lycaenidae) in laboratory nests of three Myrmica ant species. Insectes Soc. https://doi.org/10.1007/s00040-011-0157-y (2011).

    Article 

    Google Scholar 

  • 36.

    Wilson, K., Grenfell, B. T. & Shaw, D. J. Analysis of aggregated parasite distributions: a comparison of methods. Funct. Ecol. https://doi.org/10.2307/2390169 (1996).

    Article 

    Google Scholar 

  • 37.

    Tartally, A., Nash, D. R., Varga, Z. & Lengyel, S. Changes in host ant communities of Alcon Blue butterflies in abandoned mountain hay meadows. Insect Conserv. Divers. https://doi.org/10.1111/icad.12369 (2019).

    Article 

    Google Scholar 

  • 38.

    Csata, E., Bernadou, A., Rákosy-Tican, E., Heinze, J. & Markó, B. The effects of fungal infection and physiological condition on the locomotory behaviour of the ant Myrmica scabrinodis. J. Insect Physiol. https://doi.org/10.1016/j.jinsphys.2017.01.004 (2017).

    Article 
    PubMed 

    Google Scholar 

  • 39.

    Baylis, M. & Pierce, N. E. Lack of compensation by final instar larvae of the myrmecophilous lycaenid butterfly, Jalmenus evagoras, for the loss of nutrients to ants. Physiol. Entomol. https://doi.org/10.1111/j.1365-3032.1992.tb01186.x (1992).

    Article 

    Google Scholar 

  • 40.

    Elgar, M. A. & Pierce, N. E. Mating success and fecundity in an ant-tended lycaenid butterfly. In Reproductive Success: Studies of Individual Variation in Contrasting Breeding Systems 59–75 (Chicago University Press, 1988).

  • 41.

    Thomas, J. A., Elmes, G. W. & Wardlaw, J. C. Contest competition among Maculinea rebeli butterfly larvae in ant nests. Ecol. Entomol. https://doi.org/10.1111/j.1365-2311.1993.tb01082.x (1993).

    Article 

    Google Scholar 

  • 42.

    Nash, D. R., Als, T. D., Maile, R., Jones, G. R. & Boomsma, J. J. A mosaic of chemical coevolution in a large blue butterfly. Science https://doi.org/10.1126/science.1149180 (2008).

    Article 
    PubMed 

    Google Scholar 

  • 43.

    Schlick-Steiner, B. C. et al. A butterfly’s chemical key to various ant forts: intersection-odour or aggregate-odour multi-host mimicry? Naturwissenschaften https://doi.org/10.1007/s00114-004-0518-8 (2004).

    Article 
    PubMed 

    Google Scholar 

  • 44.

    Schönrogge, K. et al. Changes in chemical signature and host specificity from larval retrieval to full social integration in the myrmecophilous butterfly Maculinea rebeli. J. Chem. Ecol.  https://doi.org/10.1023/B:JOEC.0000013184.18176.a9 (2004).

    Article 
    PubMed 

    Google Scholar 

  • 45.

    Als, T. D., Nash, D. R. & Boomsma, J. J. Geographical variation in host-ant specificity of the parasitic butterfly Maculinea alcon in Denmark. Ecol. Entomol. https://doi.org/10.1046/j.1365-2311.2002.00427.x (2002).

    Article 

    Google Scholar 

  • 46.

    Als, T. D., Nash, D. R. & Boomsma, J. J. Adoption of parasitic Maculinea alcon caterpillars (Lepidoptera: Lycaenidae) by three Myrmica ant species. Anim. Behav. https://doi.org/10.1006/anbe.2001.1716 (2001).

    Article 

    Google Scholar 

  • 47.

    Tartally, A., Somogyi, A. Á., Révész, T. & Nash, D. R. Host ant change of a socially parasitic butterfly (Phengaris alcon) through host nest take-over. Insects https://doi.org/10.3390/insects11090556 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 48.

    Thomas, J. A., Elmes, G. W., Schönrogge, K., Simcox, D. J. & Settele, J. Primary hosts, secondary hosts and ‘non-hosts’: common confusions in the interpretation of host specificity in Maculinea butterflies and other social parasites of ants. In Studies on the Ecology and Conservation of Butterflies in Europe (eds. Settele, J., Kühn, E. & Thomas, J. A.) vol. 2 99–104 (Pensoft, 2005).

  • 49.

    Thomas, J. A. et al. Mimetic host shifts in an endangered social parasite of ants. Proc. Biol. Sci. https://doi.org/10.1098/rspb.2012.2336 (2013).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 50.

    Fürst, M. A., Durey, M. & Nash, D. R. Testing the adjustable threshold model for intruder recognition on Myrmica ants in the context of a social parasite. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2011.0581 (2012).

    Article 

    Google Scholar 

  • 51.

    Maák, I. et al. Habitat features and colony characteristics influencing ant personality and its fitness consequences. Behav. Ecol. https://doi.org/10.1093/beheco/araa112 (2021).

    Article 
    PubMed 

    Google Scholar 

  • 52.

    Chapman, B. B., Thain, H., Coughlin, J. & Hughes, W. O. H. Behavioural syndromes at multiple scales in Myrmica ants. Anim. Behav. https://doi.org/10.1016/j.anbehav.2011.05.019 (2011).

    Article 

    Google Scholar 

  • 53.

    Martin, S. J., Helanterä, H. & Drijfhout, F. P. Is parasite pressure a driver of chemical cue diversity in ants? Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2010.1047 (2011).

    Article 

    Google Scholar 

  • 54.

    Nehring, V., Evison, S. E. F., Santorelli, L. A., D’Ettorre, P. & Hughes, W. O. H. Kin-informative recognition cues in ants. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2010.2295 (2011).

    Article 

    Google Scholar 

  • 55.

    Van Zweden, J. S. et al. Blending of heritable recognition cues among ant nestmates creates distinct colony gestalt odours but prevents within-colony nepotism. J. Evol. Biol. https://doi.org/10.1111/j.1420-9101.2010.02020.x (2010).

    Article 
    PubMed 

    Google Scholar 

  • 56.

    Nash, D. R. & Andersen, A. Maculinea-sommerfugle og stikmyrer på danske heder—coevolution i tid og rum. Flora og Fauna 121, 133–141 (2015).

    Google Scholar 

  • 57.

    Haelewaters, D., Boer, P., Gort, G. & Noordijk, J. Studies of Laboulbeniales (Fungi, Ascomycota) on Myrmica ants (II): variation of infection by Rickia wasmannii over habitats and time. Anim. Biol. https://doi.org/10.1163/15707563-00002472 (2015).

    Article 

    Google Scholar 

  • 58.

    Dallas, T. A., Laine, A.-L. & Ovaskainen, O. Detecting parasite associations within multi-species host and parasite communities. Proc. R. Soc. B Biol. Sci. https://doi.org/10.1098/rspb.2019.1109 (2019).

    Article 

    Google Scholar 

  • 59.

    Herczeg, D., Ujszegi, J., Kásler, A., Holly, D. & Hettyey, A. Host–multiparasite interactions in amphibians: a review. Parasit. Vectors https://doi.org/10.1186/s13071-021-04796-1 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 60.

    Bronstein, J. L. Conditional outcomes in mutualistic interactions. Trends Ecol. Evol. https://doi.org/10.1016/0169-5347(94)90246-1 (1994).

    Article 
    PubMed 

    Google Scholar 

  • 61.

    Zhang, Z., Yan, C. & Zhang, H. Mutualism between antagonists: Its ecological and evolutionary implications. Integr. Zool. https://doi.org/10.1111/1749-4877.12487 (2021).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 62.

    Rogalski, M. A., Stewart Merrill, T., Gowler, C. D., Cáceres, C. E. & Duffy, M. A. Context-dependent host-symbiont interactions: Shifts along the parasitism-mutualism continuum. Am. Nat. https://doi.org/10.1086/716635 (2021).

    Article 
    PubMed 

    Google Scholar 

  • 63.

    Pfliegler, W. P., Báthori, F., Haelewaters, D. & Tartally, A. Studies of Laboulbeniales on Myrmica ants (III): myrmecophilous arthropods as alternative hosts of Rickia wasmannii. Parasite https://doi.org/10.1051/parasite/2016060 (2016).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 64.

    Chouvenc, T., Efstathion, C. A., Elliott, M. L. & Su, N.-Y. Resource competition between two fungal parasites in subterranean termites. Naturwissenschaften https://doi.org/10.1007/s00114-012-0977-2 (2012).

    Article 
    PubMed 

    Google Scholar 

  • 65.

    Lawton, J. H. & Hassell, M. P. Asymmetrical competition in insects. Nature https://doi.org/10.1038/289793a0 (1981).

    Article 

    Google Scholar 

  • 66.

    Price, P. W. Evolutionary Biology of Parasites (Princeton University Press, 1980).

    Google Scholar 

  • 67.

    Nash, D. R. & Boomsma, J. J. Communication between hosts and social parasites. In Sociobiology of Communication (eds D’Ettorre, P. & Hughes, D. P.) 55–80 (Oxford University Press, 2008).

    Chapter 

    Google Scholar 

  • 68.

    Tartally, A., Szűcs, B. & Ebsen, J. R. The first records of Rickia wasmannii Cavara, 1899, a myrmecophilous fungus, and its Myrmica Latreille, 1804 host ants in Hungary and Romania (Ascomycetes: Laboulbeniales; Hymenoptera: Formicidae). Myrmecol. News 10, 123 (2007).

    Google Scholar 

  • 69.

    Radchenko, A. G. & Elmes, G. W. Myrmica (Hymenoptera: Formicidae) ants of the Old World. vol. 6 (Fauna Mundi 3, 2010).

  • 70.

    Tragust, S., Tartally, A., Espadaler, X. & Billen, J. Histopathology of Laboulbeniales (Ascomycota: Laboulbeniales): ectoparasitic fungi on ants (Hymenoptera: Formicidae). Myrmecol. News 23, 81–89 (2016).

    Google Scholar 

  • 71.

    Haelewaters, D., Boer, P. & Noordijk, J. Studies of Laboulbeniales (Fungi, Ascomycota) on Myrmica ants: Rickia wasmannii in the Netherlands. J. Hymenopt. Res. https://doi.org/10.3897/JHR.44.4951 (2015).

    Article 

    Google Scholar 

  • 72.

    Espadaler, X. & Santamaria, S. Ecto- and endoparasitic fungi on ants from the Holarctic Region. Psyche, 2012, 168478. https://doi.org/10.1155/2012/168478 (2012).

    Article 

    Google Scholar 

  • 73.

    Báthori, F., Pfliegler, W. P., Zimmerman, C.-U. & Tartally, A. Online image databases as multi-purpose resources: discovery of a new host ant of Rickia wasmannii Cavara (Ascomycota, Laboulbeniales) by screening AntWeb.org. J. Hymenopt. Res, 61, 85-94. https://doi.org/10.3897/jhr.61.20255 (2017).

    Article 

    Google Scholar 

  • 74.

    Riddick, E. W. Ectoparasitic mite and fungus on an invasive lady beetle: parasite coexistence and influence on host survival. Bull. Insectol. 63, 13–20 (2010).

    Google Scholar 

  • 75.

    Konrad, M., Grasse, A. V, Tragust, S. & Cremer, S. Anti-pathogen protection versus survival costs mediated by an ectosymbiont in an ant host. Proc. Biol. Sci. https://doi.org/10.1098/rspb.2014.197620141976 (2015).

  • 76.

    De Kesel, A., Haelewaters, D. & Dekoninck, W. Myrmecophilous Laboulbeniales Ascomycota in Belgium. Sterbeeckia 34, 3–6 (2016).

    Google Scholar 

  • 77.

    Haelewaters, D. The first record of Laboulbeniales (Fungi, Ascomycota) on Ants (Hymenoptera, Formicidae) in The Netherlands. Ascomycete.org 4, 65-69 (2012).

  • 78.

    van Swaay, C. et al. European Red List of Butterflies (Publications Office of the European Union, 2010).

    Google Scholar 

  • 79.

    Gergely, P. & Hudák, T. Revision of threatened butterfly species in Hungary (Lepidoptera: Rhopalocera). Lepidopterol. Hungarica https://doi.org/10.24386/lephung.2021.17.1.27 (2021).

    Article 

    Google Scholar 

  • 80.

    Wallis de Vries, M. Code rood voor het gentiaanblauwtje. Vlinders 4, 5–8 (2017).

    Google Scholar 

  • 81.

    Barbero, F., Thomas, J. A., Bonelli, S., Balletto, E. & Schönrogge, K. Queen ants make distinctive sounds that are mimicked by a butterfly social parasite. Science https://doi.org/10.1126/science.1163583 (2009).

    Article 
    PubMed 

    Google Scholar 

  • 82.

    Thomas, J. A., Elmes, G. W., Wardlaw, J. C. & Woyciechowski, M. Host specificity among Maculinea butterflies in Myrmica ant nests. Oecologia https://doi.org/10.1007/BF00378660 (1989).

    Article 
    PubMed 

    Google Scholar 

  • 83.

    Elmes, G. W. et al. The ecology of Myrmica ants in relation to the conservation of Maculinea butterflies. J. Insect Conserv. https://doi.org/10.1023/A:1009696823965 (1998).

    Article 

    Google Scholar 

  • 84.

    Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods https://doi.org/10.1038/nmeth.2019 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 85.

    Cammaerts-Tricot, M.-C. Ontogenesis of the defence reactions in the workers of Myrmica rubra L. (Hymenoptera: Formicidae). Anim. Behav. https://doi.org/10.1016/0003-3472(75)90058-5 (1975).

    Article 

    Google Scholar 

  • 86.

    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. https://doi.org/10.18637/jss.v067.i01 (2015).


  • Source: Ecology - nature.com

    Strategic Forest Reserves can protect biodiversity in the western United States and mitigate climate change

    New visions for better transportation