Exploitation of organisms by multiple parasite species is common in nature, but interactions among parasites have rarely been studied. Myrmica ants are rich in parasites. Among others, the ectoparasitic Rickia wasmannii fungus and the parasitic caterpillars of myrmecophilous Phengaris butterflies often infect the same Myrmica colonies. In this study, we examined the effects of R. wasmannii on the adoption, long-term development, and survival of P. alcon. In laboratory conditions, caterpillars introduced into nests of Myrmica scabrinodis uninfected with R. wasmannii survived significantly longer compared to caterpillars introduced into infected nests. In the field, joint infection was less common than expected if both parasites exploited M. scabrinodis colonies independently. Pre-pupal caterpillars of P. alcon were somewhat larger in nests infected with R. wasmannii than those found in uninfected nests. Based on these results it seems that R. wasmannii infection of M. scabrinodis affects the survival and development of P. alcon caterpillars, suggesting competition between these two ant parasites.

Bezerédi str 10 5462 Cibakháza Hungary

Centre for Social Evolution Department of Biology University of Copenhagen Universitetsparken 15 2100 Copenhagen Denmark

Department of Evolutionary Zoology and Human Biology University of Debrecen Egyetem tér 1 4032 Debrecen Hungary

Department of Forest Protection University of Sopron Forest Research Institute Hegyalja str 18 3232 Mátrafüred Hungary

Department of Zoology Hungarian Natural History Museum Baross str 13 1088 Budapest Hungary

Evolutionary Ecology Research Group Institute of Ecology and Botany Centre for Ecological Research Alkotmány út 2 4 Vácrátót Hungary 2163

Faculty of Science University of South Bohemia Branišovská 31 370 05 České Budějovice Czech Republic

Juhász Nagy Pál Doctoral School of Biology and Environmental Sciences University of Debrecen Egyetem tér 1 4032 Debrecen Hungary

Research Group Mycology Department of Biology Ghent University K L Ledeganckstraat 35 9000 Ghent Belgium

Zobrazit více v PubMed

Frank SA. Models of parasite virulence. Q. Rev. Biol. 1996 doi: 10.1086/419267. PubMed DOI

Dobson AP. The population dynamics of competition between parasites. Parasitology. 1985 doi: 10.1017/S0031182000057401. PubMed DOI

Haelewaters D, et al. Mortality of native and invasive ladybirds co-infected by ectoparasitic and entomopathogenic fungi. PeerJ. 2020 doi: 10.7717/peerj.10110. PubMed DOI PMC

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

Renkema JM, Cuthbertson AGS. Impact of multiple natural enemies on immature Drosophila suzukii in strawberries and blueberries. Biocontrol. 2018 doi: 10.1007/s10526-018-9874-8. DOI

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

Lafferty KD. Interacting parasites. Science. 2010 doi: 10.1126/science.1196915. PubMed DOI

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

Telfer S, et al. Species interactions in a parasite community drive infection risk in a wildlife population. Science. 2010 doi: 10.1126/science.1190333. PubMed DOI PMC

Carlson CJ, et al. A global parasite conservation plan. Biol. Conserv. 2020 doi: 10.1016/j.biocon.2020.108596. DOI

Colwell RK, Dunn RR, Harris NC. Coextinction and persistence of dependent species in a changing world. Annu. Rev. Ecol. Evol. Syst. 2012;43:183–203. doi: 10.1146/annurev-ecolsys-110411-160304. DOI

Gagne RB, et al. Parasites as conservation tools. Conserv. Biol. 2021 doi: 10.1111/cobi.13719. PubMed DOI

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

Csata E, et al. Lock-picks: fungal infection facilitates the intrusion of strangers into ant colonies. Sci. Rep. 2017 doi: 10.1038/srep46323. PubMed DOI PMC

Pearson B, Raybould AF. 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. 1998;31:77–90.

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

Donisthorpe JK. The Guests of British Ants—Their Habits and Life Histories. George Routledge And Sons, Limited; 1927.

Hölldobler BE, Wilson EO. The Ants. The Belknap Press of Harvard University Press; 1990.

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

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

Quevillon LE, Hughes DP. Pathogens, parasites, and parasitoids of ants: a synthesis of parasite biodiversity and epide-miological traits. BioRxiv. 2018 doi: 10.1101/384495. DOI

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

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

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

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

Wardlaw JC, Thomas JA, Elmes GW. Do Maculinea rebeli caterpillars provide vestigial mutualistic benefits to ants when living as social parasites inside Myrmica ant nests? Entomol. Exp. Appl. 2000 doi: 10.1046/j.1570-7458.2000.00646.x. DOI

Thomas JA, Wardlaw JC. The capacity of a Myrmica ant nest to support a predacious species of Maculinea butterfly. Oecologia. 1992 doi: 10.1007/BF00317247. PubMed DOI

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. 2018 doi: 10.1007/s00040-018-0628-5. DOI

Csősz S, Rádai Z, Tartally A, Ballai LE, Báthori F. Ectoparasitic fungi Rickia wasmannii infection is associated with smaller body size in Myrmica ants. Sci. Rep. 2021 doi: 10.1038/s41598-021-93583-0. PubMed DOI PMC

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. 2014 doi: 10.1007/s00040-014-0349-3. DOI

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. 2017 doi: 10.3897/jhr.58.13253. DOI

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

Tartally A. Myrmecophily of Maculinea Butterflies in the Carpathian Basin (Lepidoptera: Lycaenidae) Hungary: University of Debrecen; 2008.

Elmes GW, Wardlaw JC, Schönrogge K, Thomas JA, Clarke RT. 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. 2004 doi: 10.1111/j.0013-8703.2004.00121.x. DOI

Nash DR, Als TD, Boomsma JJ. Survival and growth of parasitic Maculinea alcon caterpillars (Lepidoptera, Lycaenidae) in laboratory nests of three Myrmica ant species. Insectes Soc. 2011 doi: 10.1007/s00040-011-0157-y. PubMed DOI PMC

Wilson K, Grenfell BT, Shaw DJ. Analysis of aggregated parasite distributions: a comparison of methods. Funct. Ecol. 1996 doi: 10.2307/2390169. DOI

Tartally A, Nash DR, Varga Z, Lengyel S. Changes in host ant communities of Alcon Blue butterflies in abandoned mountain hay meadows. Insect Conserv. Divers. 2019 doi: 10.1111/icad.12369. DOI

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. 2017 doi: 10.1016/j.jinsphys.2017.01.004. PubMed DOI

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

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).

Thomas JA, Elmes GW, Wardlaw JC. Contest competition among Maculinea rebeli butterfly larvae in ant nests. Ecol. Entomol. 1993 doi: 10.1111/j.1365-2311.1993.tb01082.x. DOI

Nash DR, Als TD, Maile R, Jones GR, Boomsma JJ. A mosaic of chemical coevolution in a large blue butterfly. Science. 2008 doi: 10.1126/science.1149180. PubMed DOI

Schlick-Steiner BC, et al. A butterfly’s chemical key to various ant forts: intersection-odour or aggregate-odour multi-host mimicry? Naturwissenschaften. 2004 doi: 10.1007/s00114-004-0518-8. PubMed DOI

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. 2004 doi: 10.1023/B:JOEC.0000013184.18176.a9. PubMed DOI

Als TD, Nash DR, Boomsma JJ. Geographical variation in host-ant specificity of the parasitic butterfly Maculinea alcon in Denmark. Ecol. Entomol. 2002 doi: 10.1046/j.1365-2311.2002.00427.x. DOI

Als TD, Nash DR, Boomsma JJ. Adoption of parasitic Maculinea alcon caterpillars (Lepidoptera: Lycaenidae) by three Myrmica ant species. Anim. Behav. 2001 doi: 10.1006/anbe.2001.1716. DOI

Tartally A, Somogyi AÁ, Révész T, Nash DR. Host ant change of a socially parasitic butterfly (Phengaris alcon) through host nest take-over. Insects. 2020 doi: 10.3390/insects11090556. PubMed DOI PMC

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).

Thomas JA, et al. Mimetic host shifts in an endangered social parasite of ants. Proc. Biol. Sci. 2013 doi: 10.1098/rspb.2012.2336. PubMed DOI PMC

Fürst MA, Durey M, Nash DR. Testing the adjustable threshold model for intruder recognition on Myrmica ants in the context of a social parasite. Proc. R. Soc. B Biol. Sci. 2012 doi: 10.1098/rspb.2011.0581. PubMed DOI PMC

Maák I, et al. Habitat features and colony characteristics influencing ant personality and its fitness consequences. Behav. Ecol. 2021 doi: 10.1093/beheco/araa112. PubMed DOI PMC

Chapman BB, Thain H, Coughlin J, Hughes WOH. Behavioural syndromes at multiple scales in Myrmica ants. Anim. Behav. 2011 doi: 10.1016/j.anbehav.2011.05.019. DOI

Martin SJ, Helanterä H, Drijfhout FP. Is parasite pressure a driver of chemical cue diversity in ants? Proc. R. Soc. B Biol. Sci. 2011 doi: 10.1098/rspb.2010.1047. PubMed DOI PMC

Nehring V, Evison SEF, Santorelli LA, D’Ettorre P, Hughes WOH. Kin-informative recognition cues in ants. Proc. R. Soc. B Biol. Sci. 2011 doi: 10.1098/rspb.2010.2295. PubMed DOI PMC

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

Nash DR, Andersen A. Maculinea-sommerfugle og stikmyrer på danske heder—coevolution i tid og rum. Flora og Fauna. 2015;121:133–141.

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. 2015 doi: 10.1163/15707563-00002472. DOI

Dallas TA, Laine A-L, Ovaskainen O. Detecting parasite associations within multi-species host and parasite communities. Proc. R. Soc. B Biol. Sci. 2019 doi: 10.1098/rspb.2019.1109. PubMed DOI PMC

Herczeg D, Ujszegi J, Kásler A, Holly D, Hettyey A. Host–multiparasite interactions in amphibians: a review. Parasit. Vectors. 2021 doi: 10.1186/s13071-021-04796-1. PubMed DOI PMC

Bronstein JL. Conditional outcomes in mutualistic interactions. Trends Ecol. Evol. 1994 doi: 10.1016/0169-5347(94)90246-1. PubMed DOI

Zhang Z, Yan C, Zhang H. Mutualism between antagonists: Its ecological and evolutionary implications. Integr. Zool. 2021 doi: 10.1111/1749-4877.12487. PubMed DOI

Rogalski MA, Stewart Merrill T, Gowler CD, Cáceres CE, Duffy MA. Context-dependent host-symbiont interactions: Shifts along the parasitism-mutualism continuum. Am. Nat. 2021 doi: 10.1086/716635. PubMed DOI

Pfliegler WP, Báthori F, Haelewaters D, Tartally A. Studies of Laboulbeniales on Myrmica ants (III): myrmecophilous arthropods as alternative hosts of Rickia wasmannii. Parasite. 2016 doi: 10.1051/parasite/2016060. PubMed DOI PMC

Chouvenc T, Efstathion CA, Elliott ML, Su N-Y. Resource competition between two fungal parasites in subterranean termites. Naturwissenschaften. 2012 doi: 10.1007/s00114-012-0977-2. PubMed DOI

Lawton JH, Hassell MP. Asymmetrical competition in insects. Nature. 1981 doi: 10.1038/289793a0. DOI

Price PW. Evolutionary Biology of Parasites. Princeton University Press; 1980.

Nash DR, Boomsma JJ. Communication between hosts and social parasites. In: D’Ettorre P, Hughes DP, editors. Sociobiology of Communication. Oxford University Press; 2008. pp. 55–80.

Tartally A, Szűcs B, Ebsen JR. 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) Myrmecological News. 2007;10:123.

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

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

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

Espadaler X, Santamaria S. Ecto- and endoparasitic fungi on ants from the Holarctic Region. Psyche. 2012;2012:168478. doi: 10.1155/2012/168478. DOI

Báthori F, Pfliegler WP, 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. 2017;61:85–94. doi: 10.3897/jhr.61.20255. DOI

Riddick EW. Ectoparasitic mite and fungus on an invasive lady beetle: parasite coexistence and influence on host survival. Bull. Insectol. 2010;63:13–20.

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. 10.1098/rspb.2014.197620141976 (2015). PubMed PMC

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

Haelewaters, D. The first record of Laboulbeniales (Fungi, Ascomycota) on Ants (Hymenoptera, Formicidae) in The Netherlands. Ascomycete.org4, 65-69 (2012).

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

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

Wallis de Vries M. Code rood voor het gentiaanblauwtje. Vlinders. 2017;4:5–8.

Barbero F, Thomas JA, Bonelli S, Balletto E, Schönrogge K. Queen ants make distinctive sounds that are mimicked by a butterfly social parasite. Science. 2009 doi: 10.1126/science.1163583. PubMed DOI

Thomas JA, Elmes GW, Wardlaw JC, Woyciechowski M. Host specificity among Maculinea butterflies in Myrmica ant nests. Oecologia. 1989 doi: 10.1007/BF00378660. PubMed DOI

Elmes GW, et al. The ecology of Myrmica ants in relation to the conservation of Maculinea butterflies. J. Insect Conserv. 1998 doi: 10.1023/A:1009696823965. DOI

Schindelin J, et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods. 2012 doi: 10.1038/nmeth.2019. PubMed DOI PMC

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

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