What's in Your Head, Zombie? Camponotus renggeri Ants Parasitized by the Entomopathogenic Fungus Ophiocordyceps camponoti-renggeri in a Relic of Atlantic Forest in Caatinga Biome, Brazil
DOI:
https://doi.org/10.37002/biodiversidadebrasileira.v12i4.2081Keywords:
Biodiversity, formicidae, negative interaction, parasitism, pathogenAbstract
Entomopathogenic fungi are widely known to parasitize and manipulate the behavior of various orders of arthropods. In this study, we recorded parasitism involving the entomopathogenic fungus Ophiocordyceps camponoti-renggeri and host ants of the species Camponotus renggeri in a relic of Atlantic Forest in Caatinga biome, in addition to characterizing the environmental and ecological aspects of the interaction. We found 210 infected ant workers, fixed predominantly on the margins of the abaxial face of leaves of the local vegetation. Most ants used simple phyllotaxis leaves for fixation and death, whose size varied widely. The parasitized ants died about 1.5 m above the ground. These results suggest that Ophiocordyceps camponoti-renggeri has high virulence and that the behavioral changes induced in its hosts favor their fitness
References
Alves SB. 1988. Fungos entomopatogênicos. In: Alves, SB (Eds.), Controle microbiano de insetos (pp. 308-310). 2.ed. Piracicaba: FEALQ.
Andersen SB, Ferrari M, Evans HC, Elliot SL, Boomsma JJ, Hughes DP. Disease dynamics in a specialized parasite of ant societies. PloS ONE 7: e36352, 2012. doi: 10.1371/journal.pone.0036352
Andersen SB, et al. The life of a dead ant: the expression of an adaptive extended phenotype. The American Naturalist 174: 424-433, 2009. doi: 10.1086/603640
Andrade CFS. Epizootia natural causada por Cordyceps unilateralis (Hypocreales, Euascomycetes) em adultos de Camponutus sp. (Hymenoptera, Formicidae) na região de Manaus, Amazonas, Brasil. Acta Amazonica 10: 671-677, 1980. doi: 10.1590/1809-43921980103671
Andriolli FS, Ishikawa NK, Vargas-Isla R, Cabral TS, Bekker C, Baccaro FB. Do zombie ant fungi turn their hosts into light seekers? Behavioral Ecology 30: 609-616, 2019. doi: 10.1093/beheco/ary198
Araújo JPM, Evans HC, Geiser DM, Mackay WP, Hughes DP. Unravelling the diversity behind the Ophiocordyceps unilateralis (Ophiocordycipitaceae) complex: Three new species of zombie-ant fungi from the Brazilian Amazon. Phytotaxa 220: 224-238, 2015. doi: 10.11646/phytotaxa.220.3.2
Araújo JPM, Evans HC, Kepler R, Hughes DP. Zombie-ant fungi across continents: 15 new species and new combinations within Ophiocordyceps. I. Myrmecophilous hirsutelloid species. Studies in Mycology 90: 119-160, 2018. doi: 10.1016/j.simyco.2017.12.002
Araújo JPM, Hughes, DP. 2016. Diversity of Entomopathogenic Fungi: Which groups conquered the insect body? In: Lovett B, Leger RS. Genetics and molecular biology of entomopathogenic fungi. Academic Press.
Basset Y, et al. Arthropod diversity in a tropical forest. Science 338: 1481-1484, 2012. doi: 10.1126/science.1226727
Brandão CRF. Adendos ao catálogo abreviado das formigas da região Neotropical (Hymenoptera: Formicidae). Revista Brasileira de Entomologia 35: 319-412, 1991. doi: http://doi.org/10.5281/zenodo.24565
Cooke RC, Whipps JM. The evolution of modes of nutrition in fungi parasitic on terrestrial plants. Biological Reviews 55: 341-362, 1980. doi: 10.1111/j.1469-185X.1980.tb00697.x
Dáttilo W., et al. (2020). Mexico ants: incidence and abundance along the Nearctic-Neotropical interface. Ecology 101: e02944. doi: 10.1002/ecy.2944
Dawkins R. The extended phenotypes: The gene as the unit of selection. Oxford: Oxford University Press, 307p, 1982.
Delgado PAM, Murcia OP. Hongos entomopatógenos: uma alternativa para la obtención de Biopesticidas. Ambi-Agua 6: 77-90, 2011. doi: 10.4136/ambi-agua.187
Evans HC. Natural control of arthropods, with special reference to ants (Formicidae), by fungi in the tropical high forest of Ghana. Journal of Applied Ecology 11: 37-49, 1974. doi: 10.2307/2402003
Hawksworth DL. The magnitude of fungal diversity: the 1.5 million species estimate revisited. Mycological research 105: 1422-1432, 2001. doi: 10.1017/S0953756201004725
Hawksworth DL, Lücking R. Fungal diversity revisited: 2.2 to 3.8 million species. The fungal kingdom 79-95, 2017. doi: 10.1128/microbiolspec.FUNK-0052-2016
Hughes DP. Pathways to understanding the extended phenotype of parasites in their hosts. Journal of Experimental Biology 216(1): 142-147, 2013. doi: 10.1242/jeb.077461
Hughes DP, Libersat F. Parasite manipulation of host behavior. Current Biology 29: 45-47, 2019. doi: 10.1016/j.cub.2018.12.001
Hughes DP, Andersen SB, Hywel-Jones NL, Himaman W, Billen J, Boomsma JJ. Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC ecology 11(1): 13, 2011. doi: 10.1186/1472-6785-11-13
Janicki J, Narula N, Ziegler M, Guénard B, Economo EP. Visualizing and interacting with large-volume biodiversity data using client-server web-mapping applications: The design and implementation of antmaps.org. Ecological Informatics 32: 185-193, 2016. doi: 10.1016/j.ecoinf.2016.02.006
Khachatourians GG, Qazi SS. Entomopathogenic fungi: biochemistry and molecular biology. 2008. In: Brakhage AA, Zipfel PF (Eds.). Human and animal relationships. Springer, Berlin, Heidelberg, 296p.
Loreto RG, Elliot SL, Freitas ML, Pereira TM, Hughes DP. Long-term disease dynamics for a specialized parasite of ant societies: a field study. PloS ONE 9: e103516, 2014. doi: 10.1371/journal.pone.0103516
Maccheroni W, Araújo WL, Lima AOS. 2004. Fungos: uma introdução à biologia, bioquímica e biotecnologia. Caxias do Sul: EDUCS, 490p.
Mora MAS, Castilho AMC, Fraga ME. Classification and infection mechanism of entomopathogenic fungi. Arquivos do Instituto Biológico 84: 1-10, 2017. doi: 10.1590/1808-1657000552015
Moro MF, Macedo MB, Moura-Fé MMD, Castro ASF, Costa RCD. Vegetação, unidades fitoecológicas e diversidade paisagística do estado do Ceará. Rodriguésia 66: 717-743, 2015. doi: 10.1590/2175-7860201566305
Morozov AY, Robin C, Franc A. A simple model for the dynamics of a host-parasite-hyperparasite interaction. Journal of theoretical biology 249: 246-253, 2007. doi: 10.1016/j.jtbi.2007.05.041
Nascimento FR, Souza MJN. Diagnóstico Socioeconômico da Área de Proteção Ambiental da Serra de Baturité - Ceará. Raega - O Espaço Geográfico em Análise 20: 19-33, 2010. doi: 10.5380/raega.v20i0.20602
PDITS. 2014. Plano de Desenvolvimento Integrado do Turismo Sustentável. Fortaleza - CE, 129p.
Prado LP, Feitosa RM, Triana SP, Gutiérrez JAM, Rousseau GX, Silva RA, et al. An overview of the ant fauna (Hymenoptera: Formicidae) of the state of Maranhão, Brazil. Papéis Avulsos de Zoologia 59: e20195938, 2019. doi: 10.15560/12.4.1922
Rebouças NC, Sila Aivy AF, Sousa LM. Vascular epiphytes (Spermatophytes) of the Baturité Massif, Ceará, Northeast Brazil. Revista Brasileira de Geografia Física, 14(03), 1748-1766, 2021.
Santos-Silva L, Vicente RE, Feitosa RM. Ant species (Hymenoptera, Formicidae) of forest fragments and urban areas in a Meridional Amazonian landscape. Check List 12: 1885, 2016. doi: 10.15560/12.3.1885
Schultz TR. In search of ant ancestors. Proceedings of the National Academy of Sciences 97: 14028-14029, 2000. doi: 10.1073/pnas.011513798
Shrestha B, Tanaka E, Hyun MW, Han JG, Kim CS, Jo JW, et al. Coleopteran and lepidopteran hosts of the entomopathogenic genus Cordyceps sensu lato. The Journal of Mycology 2016: 1-16, 2016. doi: 10.1155/2016/7648219
Silvaâ€Viana CB, Vicente RE, Kaminski LA, Izzo TJ. Beyond the gardens: The extended mutualism from antâ€garden ants to nectaryâ€bearing plants growing in Amazon treeâ€fall gaps. Biotropica, 53(2), 433-441, 2021.
Sobczak JF, Arruda IDP, Pádua DG, Villanueva-Bonilla GA. Parasitism in Theridion sp. (Araneae: Theridiidae) by Zatypota riverai Gauld, 1991 (Hymenoptera: Ichneumonidae: Pimplinae). The Journal of Arachnology 47: 266-270, 2019. doi: 10.1636/JoA-S-18-103
Sobczak JF, Arruda IDP, Fonseca EO, Rabelo PJQ, Julião P, Nóbrega S, et al. Manipulation of Wasp (Hymenoptera: Vespidae) Behavior by the Entomopathogenic Fungus Ophiocordyceps humbertii in the Atlantic Forest in Ceará, Brazi1. Entomological News 129(1): 98-104, 2020. doi: 10.3157/021.129.0115
Sobczak JF, Costa LFA, Carvalho JLVR, Salgado-Neto G, Moura-Sobczak JCMS, Messas YF. The zombie ants parasitized by the fungi Ophiocordyceps camponoti-atricipis (Hypocreales: Ophiocordycipitaceae): new occurrence and natural history. Mycosphere 8: 1261-1266, 2017. doi: 10.5943/mycosphere/8/9/1
Sobczak JF, Pádua DG, Costa LF, Carvalho JL, Ferreira JPS, Sobczak J, et al. The parasitoid wasp Eruga unilabiana Pádua & Sobczak, sp. nov. (Hymenoptera: Ichneumonidae) induces behavioral modification in its spider host. Entomological Science 21: 59-65, 2017. doi: 10.1111/ens.12278
Vicente RE, Izzo TJ. Effect of dominant parabiotic Antâ€Garden ants on the understory and groundâ€dwelling ant assemblage in the Amazon rainforest. Insect Conservation and Diversity 14, 95-106, 2021. doi: 10.1111/icad.12449
Vicente RE, Ferreira AC, Santos RCLD, Prado LPD. Ants (Hymenoptera: Formicidae) from an Amazonian fragmented landscape, Juara, Mato Grosso, Brazil, with new records of ant species. Papéis Avulsos de Zoologia 58: e20185840, 2018. doi: 10.11606/1807-0205/2018.58.40
Vicente RE, Ferreira-Silva D, Guerreiro LM. New records of three Neotropical arboreal ant species of Camponotus, subgenus Dendromyrmex (Hymenoptera: Formicidae) for the southern Amazon, including biological information. Acta Amazonica 49(1): 36-40, 2019. doi: 10.1590/1809-4392201801951
Vicente RE, Prado LP, Izzo TJ. Amazon rainforest Ant-Fauna of Parque Estadual do Cristalino: understory and ground-dwelling Ants. Sociobiology 63: 894-908, 2016. doi: 10.13102/sociobiology.v63i3.1043
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