Trade-Ovs Underlying Polyphagy in a Facultative Ant-Tended Xorivorous Butterxy: the Role of Host Plant Quality and Enemy-Free Space
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Oecologia (2010) 163:719–728 DOI 10.1007/s00442-010-1626-0 PLANT-ANIMAL INTERACTIONS - ORIGINAL PAPER Trade-oVs underlying polyphagy in a facultative ant-tended Xorivorous butterXy: the role of host plant quality and enemy-free space Daniela Rodrigues · Lucas A. Kaminski · André V. L. Freitas · Paulo S. Oliveira Received: 23 July 2009 / Accepted: 17 March 2010 / Published online: 10 April 2010 © Springer-Verlag 2010 Abstract The underlying mechanisms mediating the use reared either on ScheZera or Pyrostegia presented no of multiple host plants were investigated in Parrhasius signiWcant damage. Additionally, we suggest that co-occur- polibetes (Lycaenidae), a Xorivorous and facultative rence with ant–treehopper associations on a plant provides myrmecophilous butterXy. Plant traits such as presence of parasitoid-free space for P. polibetes larvae. Our results ant–treehopper associations as a source of enemy-free support the hypothesis that ecological trade-oVs among space, Xower bud dimensions, toughness, thickness, tric- host plants (i.e., food quality and enemy-free space) pro- homes, and the corresponding performance and wear of mote polyphagy in natural populations of P. polibetes. P. polibetes mandibles were examined for three natural hosts: Host morphological traits seem to play a relevant role in ScheZera vinosa (Araliaceae), Pyrostegia venusta (Bignon- P. polibetes performance. To our knowledge, this is the Wrst iaceae) and Luehea grandiXora (Malvaceae). Parasitism report showing the costs of polyphagy in a myrmecophilous levels of larvae found on the three hosts were also deter- butterXy. mined. Almost all Luehea had ant–treehopper associations, and all larvae found on this host were non-parasitized. Keywords Insect performance · Mandibular wearing · Parasitism was low in larvae found on ScheZera, half of Enemy-free space · Myrmecophilous lycaenid · which hosted ant–treehopper associations. No ant–treehopper Parrhasius polibetes association was found on Pyrostegia, where parasitism was signiWcantly higher compared to other hosts. In the labora- tory, P. polibetes performed well on ScheZera, followed Introduction by Pyrostegia. No larvae survived when fed with Luehea. Flower buds of Luehea were thicker and tougher than those Although equally important for understanding community of ScheZera and Pyrostegia. Indeed, mandibles of larvae structure and dynamics, polyphagy in herbivorous insects reared on Luehea showed substantial wear, whereas those has historically received less attention in ecological and evolutionary studies than oligophagy (see Janz and Nylin 2008; Singer 2008, and references therein). From a bi-trophic perspective (i.e. host plants and the herbivore), it is Communicated by Roland Brandl. expected that the use of multiple hosts in nature entails D. Rodrigues (&) · L. A. Kaminski · A. V. L. Freitas · trade-oVs between components of herbivore performance P. S. Oliveira on diVerent hosts. That is, while a certain host can provide Departamento de Biologia Animal, Instituto de Biologia, an herbivore the best outcome regarding a given perfor- Universidade Estadual de Campinas, PO Box 6109, Campinas, SP 13083-970, Brazil mance component (e.g., survivorship), the same may not be e-mail: [email protected] true for some other parameters (e.g., growth rate) (Janz et al. 1994; Agosta 2008). In addition, performance out- L. A. Kaminski comes on plants that are both phylogenetically and structur- Programa de Pós-Graduação em Ecologia, V Instituto de Biologia, Universidade Estadual de Campinas, ally (i.e. physically and/or chemically) di erent can be Campinas, Brazil quite distinct (e.g., Janz and Nylin 2009). In such cases, the 123 720 Oecologia (2010) 163:719–728 underlying factors that determine such diVerences are information on whether host plant morphological and eco- poorly known. logical attributes can inXuence larval and adult life-history Singer (2008) pointed out some hypotheses to explain in polyphagous butterXies that are facultatively tended by how polyphagy could arise and be maintained in nature. ants. Several of these hypotheses involve diVerences in enemy- This study investigates how characteristics of diVerent free space among diVerent host plants (see Singer 2008, and host plants inXuence the performance of Parrhasius polibe- references therein). For example, a herbivore might experi- tes (Stoll) (mentioned as Panthiades polibetes in Oliveira ence trade-oVs between food quality and enemy-free space and Del-Claro 2005), a Xorivorous lycaenid facultatively among hosts (Singer et al. 2004). According to this hypoth- associated with ants (Fig. 1a). Through experimental esis, some hosts support superior performance due to favor- manipulations of ant–treehopper associations, P. polibetes able chemical or physical characteristics, whereas others has been shown to infest preferentially ScheZera vinosa may confer protection against natural enemies despite poor (Cham. and Schltdl.) (Araliaceae) (hereafter ScheZera) food quality. Although this hypothesis has been tested with plants hosting ant-tended treehoppers compared to plants several diVerent study systems in temperate regions, it has without such associations (Oliveira and Del-Claro 2005). rarely been tested in the tropics, where insect and plant More recently, presence of ant–treehopper associations on diversity are greatest. ScheZera plants has been shown to mediate P. polibetes The myrmecophily (symbiotic association with ants) oviposition, positively aVecting larval survival (L.A. present in some lycaenid and riodinid butterXies oVers an Kaminski, A.V.L. Freitas and P.S. Oliveira, submitted data). unusual opportunity to examine how enemy-free space The enemy-free space provided by ant–hemipteran asso- inXuences the evolution of host plant use (Atsatt 1981a). ciations, together with the quantiWcation of the quality of Several studies have shown that ant-tended lycaenid cater- diVerent hosts that may harbor such associations, can help pillars gain an advantage in enemy-free space over distinguish between the two hypotheses for polyphagy in untended caterpillars (e.g., Pierce and Easteal 1986; Weeks facultative myrmecophilous butterXies described above. 2003). This observation suggests that the quality of enemy- Although monophagous at the individual level, P. polibetes free space conferred by ants could be as important as host larvae have been found on over 20 plant species from sev- plant characteristics for the performance of myrmecophi- eral families (Beccaloni et al. 2008; Kaminski 2010). We lous caterpillars (Pierce and Elgar 1985; Oliveira and examine some ecological and morphological traits of three Del-Claro 2005). It has been proposed that obligate myrme- common host plants that vary in enemy-free space and/or cophily may be associated with the rise and maintenance of host suitability. More speciWcally, because host plants diVer polyphagy (e.g., Pierce and Elgar 1985; Fiedler 1994; remarkably in morphology and size (Fig. 1), we investigate DeVries et al. 1994; Kaminski 2008), where the presence how plant traits can aVect P. polibetes performance, man- of ants is one of the main factors leading to the use of a dibular wear, and thus life-history traits and associated given host plant. The known cases of association between trade-oVs. polyphagy and myrmecophily in riodinid and lycaenid larvae (e.g., Pierce and Elgar 1985; Kaminski 2008) suggest two testable hypotheses. First, myrmecophilous butterXies Materials and methods might use a set of host plants on which ants are present, regardless of host plant quality. Alternatively, there might Study sites, insects, and host plants be a trade-oV between enemy-free space and food quality among diVerent host plants, with each of these factors Parrhasius polibetes eggs, larvae and host plants were col- contributing to host plant use. lected in the cerrado area of the Laboratório Síncrotron in The presence of ants on host plants as a source of Campinas (22°48ЈS, 47°03ЈW) and in the Reserva Biológica enemy-free space for myrmecophilous caterpillars could e Estação Experimental de Mogi Guaçu (22°18ЈS, 47°13ЈW), result from host plant characteristics, such as extraXoral both in the State of São Paulo (southeastern Brazil), nectar, or from ants drawn to plants by sap-feeding insects during May–June 2008, which corresponds to the dry season (Carroll and Janzen 1973; Atsatt 1981a). Indeed, ants tend- (fall–winter). The vegetation in both areas consisted of a ing trophobiont insects such as honeydew-producing tree- cerrado sensu stricto, the typical Wre-prone savanna grow- hoppers (Del-Claro and Oliveira 2000) can extend their ing on sandy nutrient-poor soils covered by a grass layer, protective services to nearby myrmecophilous lycaenids small palms, bushes, and trees (Oliveira-Filho and Ratter (Oliveira and Del-Claro 2005). Moreover, although ant 2002). A survey for P. polibetes eggs on the three host plant presence and plant quality can mediate both oviposition and species was carried out at the Síncrotron site on 27 May 2008: larval survival in obligate ant-tended oligophagous lycae- 63, 96, and 150 eggs were recorded on ScheZera, Pyrostegia nids (Atsatt 1981b; Baylis and Pierce 1991), there is no venusta (Ker-Gawler) Miers (Bignoniaceae) (hereafter 123 Oecologia (2010) 163:719–728 721 Fig. 1 Flower buds of a ScheZera, b Pyrostegia, c Luehea and d P. polibetes eggs near ant–treehopper associations on Luehea stems. Arrows indicate the oviposition site selected by P. polibetes on ScheZera (a) as