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Conservative Benefits in an Ant-Hemipteran Association in the Brazilian Tropical Savanna by K. Del-Claro , J. Byk , G.M. Yugue1, & M.G. Morato1 1 2 ABSTRACT Terrestrial communities based on living plants involve at least three interacting trophic levels: plants, herbivores, and natural enemies of herbivores. Recent studies have showed that the outcomes of these relationships are essential for understanding not only insect-plant interactions but also whole communities. Here, we present results of manipulative experiments (ant-exclusion) in the field following an ant-plant-hemipteran interaction for eight years in the same Cerrado vegetation area. We showed that the interaction results in benefits to the hemipterans in terms of high survivorship and reproduction and to the host plant in leaf herbivory reduction. The benefits are dependent of ant presence and endure through time. The studied interaction shows that this ant-hemipteran interaction is conservative in terms of maintenance of the related species and outcomes in the same geographical area. Keywords: ant, hemipteran, plant, interaction. INTRODUCTION Most species are collections of genetically differentiated populations, making each population a small evolutionary experiment and each local interspecific interaction a potential coevolutionary experiment (Wade & Goodnight 1998, Thompson 2005). Additionally, interactions are held together over the long term partly because most species are phylogenetically conservative in their interaction with other species, and they probably interact with only a small group of species that have the potential to affect the fitness of the individuals (Thompson 2005). Ant-hemipteran relationship can represent an excellent opportunity to search for data corroborating or not to this discussion. Studies have demonstrated that hemipterans (mainly aphids and membracids) Universidade Federal de Uberlândia, Instituto de Biologia, L.E.C.I., CEP: 38400-902 Uberlândia, MG, Brazil. [email protected] 2 Universidade Federal de Juiz de Fora, ICB, Departamento de Zoologia, CEP: 36036010, Juiz de Fora, MG, Brazil. 1 Sociobiology Vol. 47, No. 2, 2006 are able to attract ants through the droplets of honeydew that they flick on the ground and leaves (Del-Claro & Oliveira 1996), and that ants feeding on this sugary secretion offer protection to the hemipterans against natural enemies (Way 1963, Buckley 1987, Del-Claro & Oliveira 2000). Recently, new studies showed that the outcomes of ant-membracid relationships can be positive also to the host plant, through reduction of leaf herbivory (Messina 1981, Moreira & Del-Claro 2005) and increase in fruit production (Oliveira & Del-Claro 2005). The membracid Enchenopa brasiliensis Strümpel is a common species feeding on apical meristems and inflorescences of Solanum lycocarpum (Solanaceae) in the Brazilian tropical savanna. Moreira & Del-Claro (2005) between 1996 and 1997 performed a series of manipulative experiments in the Cerrado (the Brazilian tropical savanna) showing that tending ants can significantly increase survivorship and reproduction of E. brasiliensis and reduction on the level of herbivory on host plant. Multitrophic interactions as between ants and hemipterans can present conditional outcomes (see Bronstein 1998a,b; Del-Claro 2004), that can vary between populations producing distinct selective patterns of coevolution in different localities (the “Geographic Mosaic Theory”, Thompson 1999), and perhaps time. Thus so, the aim of our study was to investigate the outcomes of an ant-hemipteran relationship through time in the same study site, performing the first step in an investigation making comparisons between localities. We mainly answered the questions: Does the interaction between ants and E. braziliensis show similar results throughout time in the same place? Are the same ant species present in the relationships a decade later? MATERIAL AND METHODS We reproduced after eight years the experiments performed between 1996 and 1997 by Moreira & Del-Claro (2005, see also Moreira 1999) with the association between ants, E. brasiliensis and shrubs of S. lycocarpum. The study site was the same area of open cerrado (a tropical savanna like vegetation with 75% of the grasses covering the landscape, with few trees and shrubs, see Oliveira & Marquis 2002), in the Gloria’s farm (an experimental farm belonging to the Federal University of Uberlândia), used by Moreira & Del-Claro (2005). In October of 2004, we tagged 22 individuals of S. lycocarpum with Del-Claro, K. et al. — Benefits in an Ant-Hemipteran Association similar phonological state (1-2m high, presenting inflorescences, young and mature leaves), all of them infested by E. brasiliensis being tended by ants. In each plant we tagged the two more similar branches, having approximately the same number of membracids (eggs, nymphs and adults) and by the flip of a coin each stem was designated as control or treatment. The control branches were maintained in natural state. The treatment ones had all ants manually removed and after that they received in their junction with the main trunk the application of a stick resin (Tanglefoot®) that is known to act as a physical barrier avoiding ant access to the membracids. The number of membracids (egg masses, nymphs and adults) was recorded to both groups of stems in the first (October) and last day of the experiment (December). Leaf herbivory was evaluated also in the first and last day of the study following Dirzo & Dominguez (1995). Voucher specimens of ants and membracids were collected in the field in non experimental plants and deposited in the Museu de Biodiversidade do Cerrado (MBC). We applied Mann-Whitney U-Test to verify differences between the median values obtained. RESULTS Eleven ant species were observed tending E. brasiliensis in the study area. The ant genera Camponotus (4 species) was the most common followed by Cephalotes (3 species), Crematogaster (1 species), Pheidole (1 species), Pseudomyrmex (1 species) and Ectatomma (1 species). Individuals of different ant species were seen taking care of membracids in the same host plant, impeding us to define an ant species as the main attendant of an aggregation. The most common ant in number of individuals were Camponotus crassus, Camponotus sericeiventris and an undetermined species of Pheidole. Generally, the most common ant in a particular plant had nest near (30 cm distant) the host plant and several times in the roots of the plant. Membracids in stems with free ant access presented significantly higher survivorship (Fig. 1A, B) and reproduction (Fig. 1D) than that in stems where we performed ant exclusion. So ants protect membracids and their egg masses against the attack of natural enemies. Additionally, stems visited by ants presented a significant reduction in leaf herbivory through time (Fig.1C). Sociobiology Vol. 47, No. 2, 2006 Fig. 1. Comparison between the average number (X ± 1 SD) of total of individuals of Enchenopa brasiliensis (A), only nymphs (B) and new egg masses (D) in stems of shrubs of Solanum lycocarpum between October and December of 2004 in a Cerrado field. The percentage of leave herbivory between groups with (white bars) and without ant attendance (black bars) in the same shrubs is also presented (C). The symbols indicate: *(p < 0.05); ***( p < 0.001) – Mann-Whitney U-Test. DISCUSSION Comparing our results with those from Moreira & Del-Claro (2005, see also Moreira 1999) we observed the occurrence of few variations in the final results of the interactions between ants - E. brasiliensis and S. lycocarpum through time in the same locality. After almost a decade, with an increase in the human disturbance in the field site and at Cerrado in general (see Oliveira and Marquis 2002 for a review) the same ant species continued attending the hemipterans in the same host plant offering similar quality of benefits. In fact, the E. brasiliensis- ants -S. lycocarpum system is apparently conditioned by a number of factors (e.g., time, habitat type, identity, abundance, and behavior of species partners, severity of herbivore damage) that may influence its final outcomes (Bronstein 1994; Del-Claro 2004; Moreira & Del-Claro, K. et al. — Benefits in an Ant-Hemipteran Association Del-Claro 2005). Small variations in biotic or abiotic factors can completely change the direction of a mutualistic relationship, from positive to negative and vice-versa (e.g. Oliveira & Del-Claro 2005). However, the conservative relationship between E. brasiliensis with the guild of tending-ant species in the study site is apparently the strong selective force maintaining the benefits of the interaction to the three main trophic levels related. As Thompson (2005) suggested at the local level, there is strong evidence that there are coevolutionary dynamics managing the interacting species in a way that the changes occurring through time are absorbed more quickly than we figured out, keeping populations viable. In ant-hemipteran relationships, the ants receive an energy-rich and predictable liquid resource (e.g. Tobin 1994, Davidson et al. 2003), and in turn increase treehopper survival and reduce herbivore damage to the host plant. The present study provides additional evidence that the relationship between ants, honeydew-producing hemipterans and their host plants can result in positive effects for all participants in the interaction (Messina 1981, Oliveira & Del-Claro 2005). Additionally, our results support the hypothesis that benefits can persist throughout years in the same locality. Almost all widespread species that have been studied in detail for their adaptation to other species show geographic differences in ecological outcomes or traits linked to interactions (e.g. Travis 1996; Brodie et al. 2002; Benkman 2003). The main question that still remains is if in the tropical savanna the same mutualistic interaction, common in several areas with distinct Cerrado physiognomies, also presents similar outcomes in distinct regions.- Acknowledgments K. Del-Claro thanks CNPq for a research grant. G.M. Yugue and M. Morato also thank CNPq for a Scientific Initiation fellowship. J. 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