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Behavioral Manipulation of the Spider Macrophyes Pacoti (Araneae: Anyphaenidae) by the Araneopathogenic Fungus Gibellula Sp

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Behavioral Manipulation of the Spider Macrophyes Pacoti (Araneae: Anyphaenidae) by the Araneopathogenic Fungus Gibellula Sp Canadian Journal of Zoology Behavioral manipulation of the spider Macrophyes pacoti (Araneae: Anyphaenidae) by the araneopathogenic fungus Gibellula sp. (Hypocreales: Cordycipitaceae) Journal: Canadian Journal of Zoology Manuscript ID cjz-2020-0232.R2 Manuscript Type: Article Date Submitted by the 14-Dec-2020 Author: Complete List of Authors: Arruda, Italo; Universidade Federal do Ceará, Centro de Ciências, Departamento de Biologia; Universidade da Integração Internacional da Lusofonia Afro-Brasileira, Laboratório de Ecologia e Evolução, Instituto de CiênciasDraft Exatas e da Natureza Villanueva-Bonilla, German; Universidade Estadual de Campinas Faustino, Marcio; Universidade da Integração Internacional da Lusofonia Afro-Brasileira, Instituto de Ciências Exatas e da Natureza Sobczak, Jullyana; Universidade Federal do Ceará, Centro de Ciências, Departamento de Biologia Sobczak, Jober; Universidade da Integração Internacional da Lusofonia Afro-Brasileira, Instituto de Ciências Exatas e da Natureza Is your manuscript invited for consideration in a Special Not applicable (regular submission) Issue?: Host Manipulation, Entomopathogenic fungi, Massif of Baturité, ghost Keyword: spider, Macrophyes pacoti, Gibellula © The Author(s) or their Institution(s) Page 1 of 30 Canadian Journal of Zoology Behavioral manipulation of the spider Macrophyes pacoti (Araneae: Anyphaenidae) by the araneopathogenic fungus Gibellula sp. (Hypocreales: Cordycipitaceae) I.D.P. Arruda Universidade Federal do Ceará, Centro de Ciências, Departamento de Biologia, Programa de Pós-Graduação em Ecologia e Recursos Naturais, Fortaleza, CE, Brazil. [email protected] G.A. Villanueva-Bonilla Programa de Pós-graduação em Biologia Animal, Instituto de Biologia, Universidade Estadual de Campinas, CP 6109, CEPDraft 13083-970, Campinas, SP, Brazil. [email protected] M.L. Faustino Universidade da Integração Internacional da Lusofonia Afro-Brasileira – UNILAB, Instituto de Ciências Exatas e da Natureza, Laboratório de Ecologia e Evolução, R. José Franco de Oliveira, s/n, Redenção, Ceará, 62790-972, Acarape, CE, Brazil. [email protected] J.C.M.S. Moura-Sobczak Universidade Federal do Ceará, Centro de Ciências, Departamento de Biologia, Programa de Pós-Graduação em Ecologia e Recursos Naturais, Fortaleza, CE, Brazil. [email protected] 1 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 2 of 30 J.F. Sobczak Laboratório de Ecologia e Evolução, Instituto de Ciências Exatas e da Natureza, Universidade da Integração Internacional da Lusofonia Afro Brasileira, Rodovia CE- 060, Km 51, s/n, 62785-000, Acarape, CE, Brazil. [email protected] Corresponding author: German Antonio Villanueva-Bonilla. Instituto de Biologia, Universidade Estadual de Campinas, CP 6109, CEP 13083-970, Campinas, SP, Brazil. Phone number: +55 (19) 981937682. E-mail: [email protected]. Draft 2 © The Author(s) or their Institution(s) Page 3 of 30 Canadian Journal of Zoology I.D.P. Arruda, G.A. Villanueva-Bonilla, M.L. Faustino, J.C.M.S. Moura-Sobczak, J.F. Sobczak Behavioral manipulation of the spider Macrophyes pacoti (Araneae: Anyphaenidae) by the araneopathogenic fungus Gibellula sp. (Hypocreales: Cordycipitaceae) Abstract Host manipulation has already been documented in several distinct host-parasite associations, covering all major phyla of living organisms. While in animals we know that several species have the ability to manipulate their hosts for the benefit of the parasite, in arthropopathogenic fungi there Draftis very little knowledge about possible behavioral manipulation. We report for the first time the interaction between the araneopathogenic fungus Gibellula sp. Cavara and the spider Macrophyes pacoti Brescovit, Oliveira, Sobczak & Sobczak, 2019 (Anyphaenidae) in addition to investigating the potential change in behavior of spiders infected by the parasitic fungus. We also investigated whether the rainfall regime influences the abundance of infected spiders and the parasitism rate by the araneopathogenic fungus. Our results corroborated our hypothesis that the fungus induces vertical segregation in the spider population, inducing infected spiders to be at higher heights than uninfected ones. Dead infected spiders were found in a stretched position that probably helps in fixing the carcass on the leaves by increasing the contact surface between the host and the substrate. Our results also confirm the positive relationship between the rainy season and the greater number of parasitic spiders and the parasitism rate. Keywords: Host Manipulation, Entomopathogenic fungi, Massif of Baturité. ghost spider, Macrophyes pacoti, Gibellula. 3 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 4 of 30 INTRODUCTION Parasites are of great importance for the functioning of communities and ecosystems, and can influence the population dynamics of their hosts, as well as act on the persistence of these species through their pathogenic effects (Lefèvre et al. 2009; Hatcher et al. 2012). Some species of parasites have the ability to manipulate the behavior of their hosts to survive, transmit, and complete their life cycle (Moore 1984; Poulin et al.1994). Host manipulation has already been documented in several distinct host-parasite associations, covering all major phyla of living organisms (Moore 2002). In animals, we know that some species have the evolutionary characteristic of an extended phenotype, which is the ability to manipulate their host in a way that benefits the parasite. For example, moth caterpillars Spodoptera exigua Hübner, 1808, normally live hidden in the soil, but when infectedDraft with baclovirus they rise in the treetops where they die, melt and release their virions that will infect new caterpillars (Van Houte et al. 2014). The fish Fundulus parvipinnis Girard, 1854, known as “killifish” infected by the trematode Euhaplorchis californiensis Martin, 1950 has its behavior altered where its movements become more conspicuous and makes it more visible. This altered behavior makes them more easily depredated upon, favoring the trophic transmission of the trematodes from the intermediate host, fish, to the definitive host, bird (Lafferty and Morris 1996). Entomopathogenic fungi also stand out as a group of parasites that manipulate the behavior of their hosts, with some examples already studied including flies (Elya et al. 2018), beetles (Steinkraus et al. 2017), and, mainly ants, which are popularly known as “zombie ants” (Andersen et al. 2009; Pontoppidan et al. 2009; Hughes et al. 2011; De Bekker 2019; Kurze et al. 2020). In the literature, two types of manipulative effects can be observed in the hosts, (1) induce the host to select a different habitat which will 4 © The Author(s) or their Institution(s) Page 5 of 30 Canadian Journal of Zoology benefit the spore dispersion (e.g. Maitland 1994) and (2) modify the final posture of the host to increase the surface of contact and adhesion to the substrate (Hughes et al. 2011). There are species of fungi that infect some arachnids such as mites (Trandem et al. 2015), harvestmen (Barbosa et al. 2015; Santamaria et al. 2017) and spiders, the latter being called araneopathogenic fungi (Evans and Samson 1987; Evans 2013; Hughes et al. 2016). Records of spiders being infected with fungi are abundant, but so far none of these studies have tested the possibility of behavioral manipulation of infected spiders (Evans and Samson, 1987; Evans 2013; Costa 2014; Hughes et al. 2016; Brescovit et al. 2019). Among the araneopathogenic fungi, some are considered specific to spiders, the best known being grouped in the genera Torrubiella Boud., which comprises the sexual teleomorphicDraft stage, and Gibellula Cavara, which represent the asexual anamorphic stage, both included in the Cordycipitaceae family (Johnson et al. 2009). Currently these genera of fungi comprise 23 and 80 species described respectively with worldwide distribution (Kobayasi and Shimizu 1982; Kirk 2020). Several of the host spider species are adult individuals from the Salticidae family (Evans and Samson 1987; Samson and Evans 1992), but in many records the material collected describes the host as an “unidentified spider” (Johnson et al. 2009) which limits the degree of knowledge about possible host specificity of the parasitic fungus. Recently, Brescovit et al. (2019) described a new species of spider in the family Anyphaenidae, and recorded the interaction between this species and the araneopathogenic fungus Gibellula sp. but without any details about the possible behavioral manipulation. The Anyphaenidae family is represented by small to medium wandering hunting spiders. The group is relatively uniform and well defined, morphologically and geographically (Ramírez 2003). Currently, this family is composed 5 © The Author(s) or their Institution(s) Canadian Journal of Zoology Page 6 of 30 of 56 genera and 572 species described (World Spider Catalog 2020). The greatest diversity of Anyphaenidae occurs in the New World, especially in South America, with 29 endemic genera (World Spider Catalog 2020). Interactions between Anyphaenidae and araneopathogenic fungi are scarce due to the difficulty of correctly identifying the host spider because sometimes it is completely covered by the parasitic fungus (Hughes et al. 2016). However, a few records reported that Anyphaenidae represents one of the most frequent spider families parasitized by Gibellula in the inventories, with the species Iguarima sensoria Keyserling,
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