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Ant-Related Oviposition Is Not Associated to Low Parasitism of the Myrmecophilous Butterfly Allosmaitia Strophius in an Extrafloral Nectaried Shrub

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Ant-Related Oviposition Is Not Associated to Low Parasitism of the Myrmecophilous Butterfly Allosmaitia Strophius in an Extrafloral Nectaried Shrub Acta Oecologica 83 (2017) 15e21 Contents lists available at ScienceDirect Acta Oecologica journal homepage: www.elsevier.com/locate/actoec Ant-related oviposition is not associated to low parasitism of the myrmecophilous butterfly Allosmaitia strophius in an extrafloral nectaried shrub * Alexandra Bachtold€ , 1, Estevao~ Alves-Silva 2, Kleber Del-Claro Instituto de Biologia, Universidade Federal de Uberlandia,^ Rua Ceara, s/n. Bloco 2D-Campus Umuarama, Cep 38400902, Uberlandia,^ Minas Gerais, Brazil article info abstract Article history: In Lycaenidae-ant mutualisms, ovipositing females select plants based on the presence and/or species of Received 23 August 2016 ants in order to maximize survival rates of immatures. The ants are supposed to protect the immatures Received in revised form from parasitoids, but there is large variation in the protection provided. Here, we experimentally 13 June 2017 investigated whether the occurrence of the facultative myrmecophilous Allosmaitia strophius (the Accepted 13 June 2017 dominant species in our study system) was ant-related. The parasitism rates of immatures collected in the field and reared in the laboratory were also investigated. Stems of the extrafloral nectaried shrub Peixotoa tomentosa were designated as either ant-present (control) or absent (treated). The occurrence of Keywords: fi Allosmaitia A. strophius on ant-present stems was ve times greater than on treated stems. Most eggs and larvae Butterfly were associated with Camponotus blandus and Ectatomma tuberculatum, two aggressive ant species in the Cerrado Brazilian savanna. Egg parasitism rate was 9%, and all the parasitized eggs were on ant-present stems. Conura Pupal parasitism on ant-present and ant-absent stems was 25.6% and 7%, respectively. The higher Eumaeini parasitism rate in the presence of ants might also have been density-dependent, because caterpillars Peixotoa were more abundant in ant-present stems. Tropical lycaenids are frequently found in association with patrolling ants. Nevertheless, there is growing evidence that parasitism is higher in the presence of ants, owing to caterpillar's density-dependent effects in plants with ants, and/or to the weak lycaenid-ant associations. This indicates that the offspring of myrmecophilous lycaenids may not benefit, at least in terms of lower parasitism, by living with ants. © 2017 Elsevier Masson SAS. All rights reserved. 1. Introduction 1991; Pierce and Elgar, 1985; Pierce et al., 2002). Myrmecophily in lycaenids ranges from obligate (including parasitic) to facultative Females of myrmecophilous insects oviposit preferentially in (Heath and Claassens, 2003), meaning respectively that larvae can plants that improve offspring survivorship (Forister, 2004; only develop in the presence of tending ants and that ants are not Kaminski et al., 2010; Rodrigues et al., 2010). For lycaenid butter- vital to caterpillars (Fiedler and Maschwitz, 1989; Pierce et al., flies, a remarkable group in which up to 50% of the caterpillars are 2002). Ant-related oviposition not only occurs in obligate, but myrmecophilous (Ballmer and Pratt, 1991; Dyck et al., 2000; also in facultative ant interactions (Bachtold€ et al., 2014; Rodrigues Eastwood and Fraser, 1999), there is evidence that female oviposi- et al., 2010), revealing that ants can play a role in the life history of tion choice is related to the presence of ants (reviewed by Fiedler, these lycaenid species and shape female oviposition choices. As demonstrated by Kaminski et al. (2010), in the presence of ants, caterpillars experience increased survivorship and less predation by natural enemies (protection hypothesis e Atsatt, 1981; see also * Corresponding author. Baylis and Pierce, 1991; Wagner and Kurina, 1997). The stability of E-mail addresses: [email protected] (A. Bachtold),€ [email protected] (E. Alves-Silva), [email protected] (K. Del-Claro). the interaction between ants and lycaenids is maintained by the 1 Previously at the Universidade de Sao~ Paulo, Avenida Bandeirantes 3900, Cep honey-like secretion caterpillars offer to ants (Albanese et al., 2007; 14040901, Ribeirao~ Preto, Sao~ Paulo, Brazil. Axen, 2000; Malicky, 1970); in turn, the ants patrol the caterpillars, 2 Currently at the Universidade do Estado de Mato Grosso, Rua Prof. Dr. Renato walking above and frequently antennating the larva's body (Alves- Figueiro Varella, Caixa Postal 08, CEP: 78690-000, Nova Xavantina, Mato Grosso, Brazil. Silva et al., 2013). Ants also incur in better performance in the http://dx.doi.org/10.1016/j.actao.2017.06.007 1146-609X/© 2017 Elsevier Masson SAS. All rights reserved. 16 A. Bachtold€ et al. / Acta Oecologica 83 (2017) 15e21 presence of myrmecophilous caterpillars, as the honey-like solu- 2. Materials and methods tion is a nutritious food source (Fiedler and Saam, 1995). In the tropics, females from several facultative myrmecophilous 2.1. Study area butterflies lay eggs preferentially on plants with ants, of which Camponotus (Formicinae) stands out as a marked lycaenid partner Fieldwork was carried out at the specific flowering period of the (Alves-Silva et al., 2013; Bachtold€ et al., 2014; Kaminski et al., 2010; study plant, P. tomentosa, from May to August 2012, in an area of Monteiro, 2000; Trager et al., 2013). Some species of this genus (e.g. Brazilian savanna (230 ha, 18590Se48180W, 830 m a.s.l.) located C. crassus, C. blandus, C. rufipes) engage in mutualistic associations within the vicinity of Uberlandia^ city, Brazil. The vegetation at the with lycaenid caterpillars (Fiedler, 2001; Kaminski and Rodrigues, study site (five ha within the Cerrado reserve, on a private property, 2011), and also ward-off potential natural enemies from the gen- described in Bachtold€ et al., 2016) is characterized by a predomi- eral vicinity (Kaminski et al., 2010). In addition, Camponotus are nance of shrubs and grasses; Malpighiaceae, Myrtaceae, and pervasive on many extrafloral nectaried plants in the Neotropics Fabaceae are the most common families at the site. Trees are absent (Malpighiaceae e Alves-Silva and Del-Claro, 2016; Ochnaceae e and, consequently, the shrubs are not shaded. The area is mowed Bachtold€ et al., 2012; Vochysiaceae e Calixto et al., 2015; Bigno- every two to three years to avoid the spread of fires, which are niaceae e Nogueira et al., 2012; legumes e Baker-Meio and common in the dry season (see Alves-Silva and Del-Claro, 2014). Marquis, 2012), enhancing the chances of ovipositing lycaenids to The climate in the region shows two well-defined periods. The hot- find a suitable host plant (Eastwood and Fraser, 1999). rainy season occurs from October to April and provides more than The potential role of other Neotropical ant species (e.g. Ecta- 90% of the annual rainfall (1500 mm per year); the average tem- tomma, Crematogaster, Cephalotes) as lycaenid partners has rarely perature can reach 25 C in February. The dry season, which runs been examined (but see Oliveira and Del-Claro, 2005; Robbins, from May to September, is characterized by low temperatures and 1991), owing to the low frequency of some tending ant species in humidity, with June being the coldest month (average of 20 C). the vegetation (Bachtold€ et al., 2014; Lange et al., 2013; Robbins and Aiello, 1982). This can be partly solved by studying extrafloral nectaried (EFN) plants. The relationship between EFN plants and 2.2. Study organisms lycaenids is still poorly understood, and initially, the relationship between the two appeared inconsistent (Fiedler, 1995). However, Peixotoa tomentosa is an extrafloral nectaried shrub (~1.5 m tall) more recent studies from the tropics indicate that lycaenids are that occurs mostly in open areas, edges, or sites subjected to regular common on EFN plants (Alves-Silva et al., 2013; Bachtold€ et al., deforestation (e.g. fire and mowing). Its phenology is markedly 2013, 2014; Kaminski and Freitas, 2010; Monteiro, 2000; Silva seasonal, with leaf flushing concentrated in the wet season, while et al., 2011), most likely because these plants are a reliable indi- reproductive events occur at the peak of the dry season (JuneeJuly, cator of the presence of ants and may sustain a rich community of see Vilela et al., 2014). Mature leaves can reach a length of up to tending ants (Fiedler, 2001; Lange and Del-Claro, 2014; Oliveira and 20 cm and a width of 15 cm. They tend to be ovate to obtuse, Freitas, 2004). For instance, Kaminski and Freitas (2010) showed coriaceous, dark green, with intact margins and small trichomes that the lycaenid Allosmatia strophius (Godart, 1824) occurs pref- erentially on extrafloral nectaried Malpighiaceae (oligophagy). Later, it was shown that female oviposition in this species is based on the presence of ants (Bachtold€ et al., 2014). Malpighiaceae are important not only to A. strophius; this plant family can support up to 15 lycaenid species (Bachtold€ et al., 2013; Fiedler, 1995; Monteiro, 1991; Silva et al., 2011). Thus, EFN plants seem to be a good model for the study of ant-lycaenid relationships (Seufert and Fiedler, 1996). The effective role of ants as lycaenid body-guards has been shown in a number of studies (Fraser et al., 2001; Pierce and Mead, 1981; Pierce and Easteal, 1986; Seufert and Fiedler, 1996; Weeks, 2003). However, this is not universal, and in some circumstances, ants either have no influence on immature parasitism (Atsatt, 1981) or parasitism can be higher in the presence of ants (Bachtold€ et al., 2014; Scholl et al., 2014; Turner and Hawkeswood, 1992). Overall, there is still little empirical data on ant-related oviposition in lycaenids (Trager et al., 2013), which could shed light on the effect of the presence of ants on lycaenid parasitism. In our study, we initially investigated whether oviposition of lycaenid butterflies on the extrafloral nectaried shrub Peixotoa tomentosa A. Juss. (Malpighiaceae) was related to the presence/ absence of ants and more particularly to which ant species. Then, we collected both lycaenid eggs and larvae to examine parasitism rate relative to the presence/absence of ants and to the ant species.
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