Skip to main content Skip to main navigation menu Skip to site footer
Type: Article
Published: 2021-11-24
Page range: 403-414
Abstract views: 482
PDF downloaded: 22

First record of the interaction between the arthropod-pathogenic fungus Gibellula and a new species of harvestman Auranus (Stygnidae) narrowly endemic to the Brazilian rain forest

Programa de Pós-graduação em Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, CP 6109, CEP 13083-970, Campinas, SP, Brazil.
Programa de Pós-graduação em Zoologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, CEP 58051-900, Cidade Universitária, João Pessoa, PB, Brazil.
Departamento de Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, Brazil. Neto
Programa de Pós-Graduação em Ecologia e Recursos Naturais, Centro de Ciências, Departamento de Biologia, Universidade Federal do Ceará, Fortaleza, CE, Brazil.
Programa de Pós-Graduação em Ecologia e Recursos Naturais, Centro de Ciências, Departamento de Biologia, Universidade Federal do Ceará, Fortaleza, CE, Brazil.
Programa de Pós-Graduação em Ecologia e Recursos Naturais, Centro de Ciências, Departamento de Biologia, Universidade Federal do Ceará, Fortaleza, CE, Brazil.
Programa de Pós-Graduação em Ecologia e Recursos Naturais, Centro de Ciências, Departamento de Biologia, Universidade Federal do Ceará, Fortaleza, CE, Brazil. Laboratório de Ecologia e Evolução, Instituto de Ciências Exatas e da Natureza, Universidade da Integração Internacional da Lusofonia AfroBrasileira, Rodovia CE-060, Km 51, s/n, 62785-000, Acarape, CE, Brazil.
Programa de Pós-Graduação em Ecologia e Recursos Naturais, Centro de Ciências, Departamento de Biologia, Universidade Federal do Ceará, Fortaleza, CE, Brazil. 6Laboratório de Ecologia e Evolução, Instituto de Ciências Exatas e da Natureza, Universidade da Integração Internacional da Lusofonia AfroBrasileira, Rodovia CE-060, Km 51, s/n, 62785-000, Acarape, CE, Brazil.
Departamento de Sistemática e Ecologia, Centro de Ciências Exatas e da Natureza, Universidade Federal da Paraíba, CEP 58051-900, Cidade Universitária, João Pessoa, PB, Brazil.
Laboratório de Ecologia e Evolução, Instituto de Ciências Exatas e da Natureza, Universidade da Integração Internacional da Lusofonia AfroBrasileira, Rodovia CE-060, Km 51, s/n, 62785-000, Acarape, CE, Brazil.
Opiliones Akanthomyces Brejos Cearenses Laniatores biogeography

Abstract

Harvestmen are one of the largest groups of arachnids with more than 6,500 species distributed in 1,500 genera and 50 families. However, the interactions between harvestmen and arthropod-pathogenic fungi have rarely been studied. Certain previous studies report that fungal attack represents one of the most important factors for the mortality of harvestmen, but the fungus has rarely been identified, and most of the important information about the fungus-host interactions remains unrecorded. In the present study, we have described the new species Auranus quilombola sp. nov. and reported its interactions with the arthropod-pathogenic fungus Gibellula sp. Auranus quilombola sp. nov. belongs to the family Stygnidae, and it is endemic to the humid mountain forests of Ceará state, Brazil in an area of endemism known as Brejos Cearenses. The species is related to five other species of Auranus, all of which have been recorded from the Amazon rainforest. A taxonomic description of this new species and its biogeographic implications have also been discussed in this paper.

 

References

  1. Acosta, L.E. & Machado, G. (2007) Diet and foraging. In: Pinto-da-Rocha, R., Machado, G. & Giribet, G. (Eds.), Harvestmen: the biology of Opiliones. Harvard University Press, Cambridge, pp. 309–338.
    Andersen, S.B., Gerritsma, S., Yusah, K.M., Mayntz, D., Hywel-Jones, N.L., Billen, J., Boomsma J.J. & Hughes, D.P. (2009) The life of a dead ant: the expression of an adaptive extended phenotype. The American Naturalist, 174, 424–433. https://doi.org/10.1086/603640
    Arruda, I., Villanueva-Bonilla, G.A., Faustino, M.L., Sobczak, J.M.S.M. & Sobczak, J. (2021) Behavioral manipulation of the spider Macrophyes pacoti (Araneae: Anyphaenidae) by the araneopathogenic fungus Gibellula sp. (Hypocreales: Cordycipitaceae). Canadian Journal of Zoology, 99, 401–408. https://doi.org/10.1139/cjz-2020-0232
    Balazuc, J. (1990) The Laboulbeniales (Ascomycetes) parasitic on Acari. Description of a new species. Acarologia, 31, 103–112.
    Barbosa, B.C., Maciel, T.T., Abegg, A.D., Borges, L.M., Rosa, C.M. & Vargas-Peixoto, D. (2016) Arachnids Infected by arthropod-pathogenic Fungi in an urban fragment of Atlantic Forest in southern Brazil. Natureza on line, 14, 11–14.
    Batalha-Filho, H., Fjeldsa, J., Fabre, P.H. & Miyaki, C. (2013) Connections between the Atlantic and the Amazonian forest avifaunas represent distinct historical events. Journal of Ornithology, 154, 41–50. https://doi.org/10.1007/s10336-012-0866-7
    Brescovit, A.D., Villanueva-Bonilla, G.A., Sobczak, J.C.M., Nóbrega, F.A.D.S., Oliveira, L.F.M.D., Arruda, I.D.P. & Sobczak, J.F. (2019) Macrophyes pacoti n. sp. (Araneae: Anyphaenidae) from Brazilian Atlantic Forest, with notes on an araneopathogenic fungus. Zootaxa, 4629 (2), 294–300. https://doi.org/10.11646/zootaxa.4629.2.12
    Colmenares, P.A. Porto, W. & Tourinho, A.L. (2016) Taxonomic notes on the genus Auranus (Opiliones, Laniatores, Stygnidae), with description of two new species. Zootaxa, 4103, 117–129. http://doi.org/10.11646/zootaxa.4103.2.2
    Cokendolpher, J.C. (1993) Pathogens and parasites of Opiliones (Arthropoda: Arachnida). Journal of Arachnology, 21, 120–146.
    Curtis, D.J. & Machado, G. (2007) Ecology. In: Pinto-da-Rocha, R., Machado, G. & Giribet, G. (Eds.), Harvestmen: the biology of Opiliones. Harvard University Press, Cambridge, pp. 280–308.
    De Bekker, C., Quevillon, L.E., Smith, P.B., Fleming, K.R., Ghosh, D., Patterson, A.D. & Hughes, D.P. (2014) Species-specific ant brain manipulation by a specialized fungal parasite. BMC evolutionary biology, 14, 166. https://doi.org/10.1186/s12862-014-0166-3
    Delgado, P.A.M. & Murcia-Ordoñez, B. (2011) Hongos entomopatógenos como alternativa para el control biológico de plagas. Ambi-Agua, Taubaté, 6 (2), 77–90. https://doi.org/10.4136/1980-993X
    DaSilva, M.B., Pinto-da-Rocha, R. & DeSouza, A.M. (2016) História biogeográfica da Mata Atlântica: opiliões (Arachnida) como modelo para sua inferência. In: Carvalho, C.J.B. & Almeida, E.A.B. (Eds.), Biogeografia da América do Sul: Análise de Tempo, Espaço e Forma. Editora Roca, São Paulo, pp. 227–244.
    DeSouza, A.M., DaSilva, M.B. & Carvalho, L.S. (2017) Opiliões Laniatores do Semiárido: grandes achados taxonômicos com o pouco que se conhece. In: Bravo, F. (Eds.), Artrópodes do Semiárido II: biodiversidade e conservação. Métis Produção Editorial, São Paulo, pp. 7–27.
    d’Horta, F.M., Cabanne, G.S., Meyer, D. & Miyaki, C.Y. (2011) The genetic effects of Late Quaternary climatic changes over a tropical latitudinal gradient: diversification of an Atlantic Forest passerine. Molecular Ecology, 20, 1932–1935. https://doi.org/10.1111/j.1365-294X.2011.05063.x
    Evans, H.C. & Samson, R.A. (1987) Fungal pathogens of spiders. Mycologist, 1, 152–159. https://doi.org/10.1016/S0269-915X(87)80107-6
    Fernandes-Ferreira, H., Gurgel-Filho, N.M., Feijó, A., Mendonça, S.V., Alves, R.R. da N. & Langguth, A. (2015) Non-volant mammals from Baturité Ridge, Ceará state, Northeast Brazil. Check List, 11, 1630. https://doi.org/10.15560/11.3.1630
    Giribet, G. & Sharma, P.P. (2015) Evolutionary biology of harvestmen (Arachnida, Opiliones). Annual Review of Entomology, 60, 157–175. https://doi.org/10.1146/annurev-ento-010814-021028
    Hoogmoed, M.S., Borges, D.M. & Cascon, P. (1994) Three new species of the genus Adelophryne (Amphibia: Anura: Leptodactylidae) from northeastern Brazil, with remarks on the other species of the genus. Zoologische Mededelingen Leiden, 68, 271–300.
    Hughes, D.P., Andersen, S.B., Hywel-Jones, N.L., Himaman, W., Billen, J. & Boomsma, J.J. (2011) Behavioral mechanisms and morphological symptoms of zombie ants dying from fungal infection. BMC ecology, 11 (1), 1–10. https://doi.org/10.1186/1472-6785-11-13
    Hywel-Jones, N.L. (1993) Torrubiella luteorostrata: A pathogen of scale insects and its association with Paecilomyces cinnamomeus with a note on Torrubiella tenuis. Mycological Research, 97 (9), 1126–1130. https://doi.org/10.1016/S0953-7562(09)80514-5
    Johnson, D., Sung, G.H., Hywel-Jones, N.L., Luangsa-Ard, J.J., Bischoff, J.F., Kepler, R.M. & Spatafora, J.W. (2009) Systematics and evolution of the genus Torrubiella (Hypocreales, Ascomycota). Mycological Research, 113, 279–289. http://doi.org/10.1016/j.mycres.2008.09.008
    Kepler, R.M., Luangsa-ard, J.J., Hywel-Jones, N.L., Quandt, C.A., Sung, G.H., Rehner, S.A., Aime, M.C., Henkel, T.W., Sanjuan, T., Zare, R., Chen, M., Li, Z., Rossman, A.Y., Spatafora, J.W. & Shrestha, B. (2017) A phylogenetically-based nomenclature for Cordycipitaceae (Hypocreales). International Mycological Association Fungus, 8, 335–353. http://doi.org/10.5598/imafungus.2017.08.02.08
    Kirk, P.M. (2019) Species Fungorum (version Oct 2017). In: Roskov, Y., Ower, G., Orrell, T., Nicolson, D., Bailly, N., Kirk, P.M., Bourgoin, T., DeWalt, R.E., Decock, W., Nieukerken, E. van, Zarucchi, J. & Penev, L. (Eds.), Species 2000 & ITIS Catalogue of Life, 2019 Annual Checklist. Available from: http://www.catalogueoflife.org/annual-checklist/2019 (accessed 3 April 2021)
    Kobayasi, Y. & Shimizu, D. (1982) Monograph of the genus Torrubiella. Bulletin of the National Science Museum, Tokyo, 8, 43–78.
    Kury, A.B. (2003) Annotated catalogue of the Laniatores of the New World (Arachnida, Opiliones). Revista Ibérica de Aracnología, Volumen especial monográfico, 1, 1–337.
    Kury, A.B. & Medrano, M. (2016) Review of terminology for the outline of dorsal scutum in Laniatores (Arachnida, Opiliones). Zootaxa, 4097 (1), 130–134. http://doi.org/10.11646/zootaxa.4097.1.9
    Kury, A.B. & Villarreal, O. (2015) The prickly blade mapped: establishing homologies and chaetotaxy for macrosetae of penis ventral plate in Gonyleptoidea (Arachnida, Opiliones, Laniatores). Zoological Journal of the Linnean Society, 17, 1–46. https://doi.org/10.1111/zoj.12225
    Kury, A.B., Mendes, A.C., Cardoso. L., Kury, M.S., Granado, A.A., Yoder, M.J. & Kury, I.S. (2021) WCO-Lite version 1.1: an online nomenclatural catalog of harvestmen of the World (Arachnida, Opiliones) curated in TaxonWorks. Zootaxa, 4908 (3), 447–450. https://doi.org/10.11646/zootaxa.4908.3.10
    Machado, G. & Oliveira, P.S. (1998) Reproductive biology of the neotropical harvestman (Goniosoma longipes) (Arachnida, Opiliones: Gonyleptidae): mating and oviposition behaviour, brood mortality, and parental care. Journal of Zoology, 246, 359–367. https://doi.org/10.1111/j.1469-7998.1998.tb00166.x
    Machado, G. & Raimundo, R.L.G. (2001) Parental investment and the evolution of subsocial behaviour in harvestmen (Arachnida Opiliones). Ethology Ecology & Evolution, 13, 133–150. https://doi.org/10.1080/08927014.2001.9522780
    Mello-Leitão, C.F. (1941) Opiliões coligidos por Antenor Leitão de Carvalho no Tapirapés. Revista Brasileira de Biologia, 1, 435–442.
    Møller, A.P. (1993) A fungus infecting domestic flies manipulates sexual behaviour of its host. Behavioral ecology and sociobiology, 33, 403–407. https://doi.org/10.1007/BF00170255
    Mullens, B., Rodriguez, J. & Meyer, J. (1987) An epizootiological study of Entomophthora muscae in muscoid fly populations on southern California poultry facilities, with emphasis on Musca domestica. Hilgardia, 55, 1–41. https://doi.org/10.3733/hilg.v55n03p041
    Pinto-da-Rocha, R. (1995) Redescription of Stenostygnus pusio Simon and synonymy of Caribbiantinae with Stenostygninae (Opiliones: Laniatores, Biantidae). Journal of Arachnology, 23, 194–198.
    Pinto-da-Rocha, R. (1997) Systematic review of the Neotropical family Stygnidae (Opiliones, Laniatores, Gonyleptoidea). Arquivos de Zoologia, 33, 163–342. https://doi.org/10.11606/issn.2176-7793.v33i4p163-342
    Pinto-da-Rocha, R. & Tourinho, A.L. (2012) Two new genera, ten new species and new records of Amazonian Stygnidae Simon, 1879 (Opiliones: Laniatores). Zootaxa, 3340 (1), 1–28. https://doi.org/10.11646/zootaxa.3340.1.1
    Pinto-da-Rocha, R. & Villarreal-Manzanilla, O. (2009) Cladistic analysis of the Stygninae and description of a new species of Protimesius Roewer, 1913 (Opiliones: Stygnidae). Zootaxa, 2176, 48–56.
    Pontoppidan, M.B., Himaman, W., Hywel-Jones, N.L., Boomsma, J.J. & Hughes, D.P. (2009) Graveyards on the move: the spatio-temporal distribution of dead Ophiocordyceps-infected ants. PloS one, 4 (3), e4835. https://doi.org/10.1371/journal.pone.0004835
    Roy, H.E., Steinkraus, D.C., Eilenberg, J., Hajek, A.E. & Pell, J.K. (2006) Bizarre interactions and endgames: entomopathogenic fungi and their arthropod hosts. Annual Review of Entomology, 51, 331–357. https://doi.org/10.1146/annurev.ento.51.110104.150941
    Samson, R.A. & Evans, H.C. (1992) New species of Gibellula on spiders (Araneida) from South America. Mycologia, 84, 300–314.
    Santamaria, S., Enghoff, H. & Reboleira, A.S.P.S. (2016) Hidden biodiversity revealed by collections-based research—Laboulbeniales in millipedes: genus Rickia. Phytotaxa, 243, 101–127. https://doi.org/10.11646/phytotaxa.243.2.1
    Santamaria, S., Enghoff, H., Gruber, J. & Reboleira, A.S.P.S. (2017) First Laboulbeniales from harvestmen: the new genus Opilionomyces. Phytotaxa, 305 (4), 285–292. https://doi.org/10.11646/phytotaxa.305.4.4
    Santos, A.M.M., Cavalcanti1, D.R., Cardoso, J.M.S. & Tabarelli, M. (2007) Biogeographical relationships among tropical forests in north-eastern Brazil. Journal of Biogeography, 34, 437–446. https://doi.org/10.1111/j.1365-2699.2006.01604.x
    Silva-de-Miranda, P.L., Oliveira-Filho, A., Pennington, R.T., Neves, D.M., Baker, T.R. & Dexter, K.G. (2018) Using tree species inventories to map biomes and assess their climatic overlaps in lowland tropical South America. Global Ecology and Biogeography, 27, 899–912. https://doi.org/10.1111/geb.12749
    Silveira, M.H.B.; Mascarenhas, R., Cardoso, D. & Batalha-Filho, H. (2019) Pleistocene climatic instability drove the historical distribution of forest islands in the northeastern Brazilian Atlantic Forest. Palaeogeography, Palaeoclimatology, Palaeoecology, 527, 67–76. https://doi.org/10.1016/j.palaeo.2019.04.028.
    Tabarelli, M. & Santos, A.M. (2004) Uma breve descrição sobre a história natural dos Brejos Nordestinos. In: Porto, K.C., Cabral, J.J.P. & Tabarelli, M. (Eds.), Brejos de altitude em Pernambuco e Paraíba: história natural, ecologia e conservação. Ministério do Meio Ambiente, Serie Biodiversidade, Brasília, pp. 917–24.
    Vega, F.E., Meyling, N.V., Luangsa-ard, J.J. & Blackwell, M. (2012) Fungal entomopathogens. In: Vega, F.E. & Kaya, H.K. (Eds.), Insect pathology. Academic Press, London, pp. 171–220. https://doi.org/10.1016/B978-0-12-384984-7.00006-3
    Villarreal, O., Ázara, L.N. & Kury, AB. (2019) Revalidation of Obidosus Roewer, 1913 and description of two new cave-dwelling species of Protimesius Roewer, 1913 from Brazil (Opiliones: Stygnidae). Journal of Natural History, 53, 965–989. https://doi.org/10.1080/00222933.2019.1620893
    World Catalogue of Opiliones (2019) World Catalogue of Opiliones. Version 2.3.0. Available from: https://wcolite.com/ (accessed 1 July 2021)

  2.  

  3.