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Biological Journal of !he Linnean Sociep ( 199I ) , 43: 179- 195 Mutualism between Thisbe irenea butterflies and ants, and the role of ant ecology in the evolution of larval-ant associations P. J. DEVRIES Department of <oology, Uniuersily of Texas, Austin, Texas 787812 and Smithsonian Tropical Research Inst., Box 2072, Balboa, Panama A facultative mutualism between the riodinid butterfly Thisbe ircnca and the ponerine ant Ectafomma ruidurn is described from Panama. Ants protect larvae against attacks of predatory wasps, but not against tachinid parasitoids. Several potential sources of ecological variation affecting the larval survival of Thisbe irenea are noted. A preliminary means of testing the ability of larvae to appease ants is described that may be applied to all butterfly-ant systems. Observations and literature records indicate that ant taxa which tend butterfly larvae are the same taxa that tend extrafloral nectaries and Homoptera. A general hypothesis for the evolution of myrmecophily among butterflies suggests that ant taxa which utilize secretions in their diet are major selective agents for the evolution of the larval ant-organs, and hence, ant-larval mutualisms. This idea is extended to suggest how appeasement of predaceous ant taxa through the use of larval ant-organs can influence an ant-larval relationship, eventually leading to mutualism. KEY WORDS:-Butterflies - rnyrmecophily - Riodinidae - Lycaenidae - mutualisms - Vespidae predation - ants - extrafloral nectaries - Homoptera - evolution - larval ant-organs. CONTENTS Introduction . . . . . Natural history of Thisbe irenea . Materials and methods. . . Results . . . . . . Discussion . . . . . . Acknowledgements . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 179 181 182 184 190 193 193 INTRODUCTION The facultative habit of insects associating with ants (termed myrmecophily) is well established among the insect orders Homoptera and Lepidoptera (Way, 1963; Cottrell, 1984). Although facultative myrmecophiles can complete their life cycles without ants, benefits can be gained from associating with ants, including: protection against predators and parasitoids; faster growth rates; higher reproductive success; and safer aestivation sites (Bartlett, 1961; Banks & Nixon, 1958; Cottrell, 1984; DeVries, 1987; Pierce el al., 1987; Thomas et al., 1989; Wheeler, 1910; Way, 1963; Wilson, 1971). All myrmecophilous insects are distinguished from their non-myrmecophilous relatives by morphological and 0024-4066/9I/070179 + I 7 S03.00/0 I79 0 1991 The Linnean Society of London 180 P.J. DEVRIES behavioural adaptations for living among ants, one common adaptation being the possession of specialized secretory organs which either produce food that is imbibed by the ants or chemicals that modify ant behaviour (see Wheeler, 1910; Way, 1963; Wilson, 1971; Maschwitz, Wurst & Schurian, 1975; Cottrell, 1984; DeVries, 1987, 1988, 1990, 1991; Fiedler & Maschwitz, 1987, 1988, and references therein). Among butterflies only larvae of the monophyletic lycaenoids (the Lycaenidae plus Riodinidae) are known to possess specialized secretory organs for associating with ants. The widespread taxonomic occurrence of these organs on larval lycaenids (see Downey, 1961; Cottrell, 1984; DeVries, Harvey & Kitching, 1986), suggest that myrmecophily was an integral part of the evolutionary history of the lycaenoids (Hinton, 1951; Vane-Wright, 1978; Pierce et al., 1987), and probably played a n important role in promoting wide larval hostplant breadth and high species diversity (Pierce, 1984, 1987; Pierce & Elgar, 1985). Although riodinids and the lycaenids share a close relationship (Ehrlich, 1958; Kristensen, 1976; Harvey, 1987), it is likely that myrmecophily evolved independently in the two groups (DeVries, 1990, 1991). All riodinid and lycaenid larvae (myrmecophilous and non-myrmecophilous) have epidermal pits called pore cupolas that are considered important indicators of ancestral myrmecophily in lycaenoids (see Downey, 1961; Malicky, 1970; Cottrell, 1984; Pierce, 1987). However, the possession of pore cupolas by larvae of the completely non-myrmecophilous family Hesperiidae (Franzl, Locke & Huie, 1984) suggests that they may be inappropriate characters for assessing the evolution of myrmecophily in butterflies (DeVries, 1991). Nonetheless, only myrmecophilous larvae of many lycaenids and riodinids possess derived organs (hereafter termed ant-organs) that have clearly evolved in response to selection by ants. These specialized ant-organs provide ant food and chemicals that modify ant behaviour (see Ross, 1966; Malicky, 1970; Maschwitz el al., 1975; Henning, 1983; Pierce, 1984; Fiedler & Maschwitz, 1988, 1989; DeVries, 1988; DeVries & Baker, 1989), as well as sounds that function to attract ants (DeVries, 1988, 1990b). Two ideas have been advanced to explain the evolution of specialized antorgans and the nature of myrmecophily in butterflies. The ‘mutualism’ hypothesis (Thomann, 1901) holds that ants protect larvae from predators and parasitoids in exchange for secretions provided by the larval ant-organs. The ‘appeasement’ hypothesis (Lenz, 1917) maintains that, because ants are generally marauding predators and abundant in many habitats (e.g. Smiley, 1985; Koptur, 1984; Jones, 1987), larvae offer appeasement rewards to them via the ant-organs to avoid being killed. Support for the mutualism hypothesis comes from experimental studies on several lycaenid species (Atsatt, 1981a; Pierce & Mead, 1981; Pierce et al., 1987; Fiedler & Maschwitz, 1988; Thomas et al., 1989) and two riodinids (Ross, 1966; DeVries, 1987). These studies showed that ants protect larvae against enemies. In contrast, the observations of Malicky (1969, 1970) on a large sample of European lycaenid taxa support the appeasement hypothesis. He found that lycaenid larvae have a thick cuticle (as armour against ant attacks), that parasitoids were undeterred by ants, and argued that since many ants are predators on small arthropods, the secretions produced by larval ant-organs are used as ‘bribery’ to avoid being attacked or killed by ants. THISBE IRENEA AND THE EVOLUTION OF BUTTERFLY-ANT MUTUALISMS 181 Various authors have discussed theoretically the contributions of both mutualism and appeasement to the evolution of larval ant-organs and butterfly myrmecophily (Malicky, 1969, 1970; Pierce & Mead, 1981; Pierce, 1987; Fiedler & Maschwitz, 1988), and Cottrell (1984) pointed out that the two ideas may be difficult to separate. However, no published studies have attempted to evaluate both of them experimentally. In general, studies on larval-ant associations have not considered the feeding biology of ants. I suggest that important ecological relationships common to facultative myrmecophiles have been overlooked by previous studies considering the evolution of ant-organs and butterfly myrmecophily. Although there is overlap among taxa with respect to food items taken, the foraging biology of ants can be broken down into four general categories: (1) taxa that are primarily predators; (2) taxa that are herbivores and seed eaters; (3) taxa that are scavengers; and (4) taxa that primarily harvest secretions (Wheeler, 1910; Wilson, 1971 ; Carroll & Janzen, 1973). The specialized feeding biology within the Formicidae implies that classifying all ant species as mutualists or predators of butterfly larvae is too simplistic. Specializations in ant feeding biology suggests that the two hypotheses for explaining the evolution of ant-organs must be tested in different ways. By using simple pair-wise ant exclusion experiments one can test directly whether a particular larval-ant association is mutualistic: either there is a measurable benefit or there is not (e.g. Pierce & Mead, 1981; Pierce et al., 1987). Appeasement of ants by larvae, however, must be tested by measuring the outcome of the interactions between larvae and the different ant species composing an ant community, a test for which there are no available data. The purpose of this paper is to illustrate that broad patterns of butterfly-ant associations and the evolution of ant-organs may be better understood by examining them from the point of view of the ants, rather than of the butterflies (as has been traditionally done). This argument is developed in four stages. First, the facultative association between the riodinid butterfly Thisbe irenea and its attending ants is examined experimentally. Secondly, the interactions between T. irenea larvae and a subset of a local ant fauna are used to develop the idea that not all ants tend or kill larvae, and suggest that three outcomes may arise from ant-larval encounters, which are determined by the feeding biology of the ants. Thirdly, the general pattern of what types of ants tend T. irenea larvae is shown to occur in other local but terfly-ant associations. Finally, from observations and literature records it is argued that out of the total recognized ant diversity, only those small number of any genera that harvest secretions have selected for specialized ant-organs, and thereby promote the evolution of butterfly-ant mutualisms. Natural history of Thisbe irenea The study organism, Thisbe irenea (Stoll, 1780), is a widespread Neotropical riodinid butterfly that ranges from Mexico through Central America to Colombia, Venezuela and Ecuador. The present study was conducted in Panama on Barro Colorado Island, and surrounding mainland habitats (see Croat, 1978; Leigh, Rand & Windsor, 1982 for description of the area) from September 1985 to August 1986, and intermittently from October 1987 to 182 P. J. DEVRIES August 1988. At the study site 1.irenea lavae are monophagous on sapling plants of Croton billbergianus (Euphorbiaceae), a secondary forest tree that is common in lightgaps and along forest trails (Robbins & Aiello, 1982; personal observations). Each hostplant leaf bears a pair of extrafloral nectaries that produce secretions attractive to ants and to 1.irenea larvae. The primary ant species tending both larvae of T. irenea and C. billbergianus nectaries was Ectatomma ruidum (Ponerinae),one of the most abundant ant species at the study site (D. Feener & E. Schupp, unpublished). However, depending on the local distributions of ant colonies, some larvae and plants were tended by E. tuberculatum, or species in the genera Camponotus, Wasmannia, Pheidole or Tapinoma. O n many occasions wasps, beetles, flies and other insects were observed foraging on the leaves and/or extrafloral nectaries of C. billbergianus (and other plant' species) and being repelled by ants (personal observations), suggesting a facultative plant-ant mutualism similar to those found in many other plants (see review in Beattie, 1985). Of the five total larval instars of 1.irenea, only the third to fifth bear three distinct sets of ant-organs-vibratory papillae, tentacle nectary organs and anterior tentacle organs-that are used to attract and maintain ant associations (DeVries, 1988). Larvae remain in physical contact with a n individual hostplant throughout their lives, and duration of larval stages ranges from two days as first instars to as long as eight days in the fifth instar. All larval instars gain a measurable growth benefit from drinking the extrafloral nectar produced by the hostplant nectaries, in addition to consuming leaf tissue (DeVries & Baker, 1989). Since T. irenea larvae can be raised to adulthood without ants, their association with ants is facultative. From rearing numerous field-collected larvae, I established that the major parasitoids attacking 1.irenea at Barro Colorado Island and adjacent areas were three or more undetermined species of tachinid flies, all of which emerge from fifth instar larvae. Observations showed repeatedly that several species of vespid wasps commonly search C . billbergianus foliage and kill T. irenea larvae when they are found. MATERIALS AND METHODS To test whether the presence of ants influence larval abundance on hostplants, 102 C. billbergianus saplings (all approximately 1.5-2.0 m in height) were marked in three separate populations. All larvae (eggs could not be found reliably) and ants were removed from each plant, and the stem of each lant was then ringed 12 cm from the base with a viscous barrier of TanglefootTR to exclude crawling arthropods (i.e. ants, beetles, spiders, Hemiptera). From the ground upwards all surrounding vegetation that might serve as a bridge to insects was cut back at least 12 cm from each plant. Half of each population received a wooden stick bridge attached to the main stem above the Tanglefoot barrier and reaching to the ground, allowing ants to move on and off the plants. Experimental plants did not receive the bridge and therefore ants were denied access to these plants. Larvae subsequently found on plants were assumed to originate from eggs deposited by T, irenea females. All plants were censused once per week and the numbers of first through fourth instar larvae found on each plant were recorded. During each census the Tanglefoot barrier was inspected and all potential THISBE IRENEA AND THE EVOLUTION OF BUTTERFLY-ANT MUTUALISMS 183 vegetation bridges were pruned back. In each population the abundance of larval instars on plants with and without ants, treatment effects and the attrition of larval instars were compared using replicated goodness-of-fit tests (Sokal & Rohlf, 1981). Congruence of the three populations was compared with a 3-way contingency test (Bishop, Fienberg & Holland, 1975). To test if ant association reduced parasitoid attacks in T. irenea, all late fourth instar larvae were removed from plants in the three experimental populations over the course of 26, 31 and 42 weeks, depending on the population. These larvae were placed in individual petri dishes in an ambient temperature laboratory, and reared to adulthood or until parasitoids emerged. The differences in parasitoid and adult emergence between larvae originating from experimental and control plants were compared using a contingency test (Sokal & Rohlf, 1981). To test if the presence of ants reduced attacks on T. irenea larvae by predatory wasps the following experiments were performed. Two potted C. billbergianus saplings of approximately the same size, condition and number of leaves were ringed 12 cm from their bases with Tanglefoot, and placed in an area patrolled heavily by foraging vespine wasps ( = the Clearing Site). One plant received a stick bridge attached above the Tanglefoot barrier and leading to the ground near an E. ruidum colony, allowing the ants access to the plant; the other plant did not. Two additional pairs of potted plants (treated in the same manner) were placed in two areas within 30 m of the Clearing site but that appeared to be less patrolled heavily by wasps ( = the Edge Sites). Paired larvae of the same instar were placed simultaneously on each of the plants and then censused at various intervals. In some cases a stationary observer recorded all interactions between larvae, ants and wasps. A total of 33 pairs of larvae were tested at the Clearing site and 19 pairs were tested at the Edge sites. In all potted plant experiments, those larvae not found after a careful inspection of the plants between censuses were assumed to have been killed. In many instances this was confirmed by direct observation of wasps killing larvae, or by haemolymph stains on the plant (a characteristic effect of wasps killing larvae). For the Clearing site and pooled Edge Sites, the differences in time larvae remained on the plant pairs were compared against a binomial probability using a sign test (Siegel, 1956). Site effect was examined by comparing the pooled Edge sites to the Clearing site using a contingency test (Sokal & Rohlf, 1981). In an attempt to assess the ability of larvae to appease ants, 26 a n t species (see Table 4 for taxa) that occur commonly on Barro Colorado Island were allowed to encounter T . irenea larvae passively and the outcomes noted. Single larvae kept in containers without ants for at least 1 day (to avoid contamination by ant odours) were placed on potted plants and carried to areas where different ant species occurred. A bridge was then placed from the potted plant to where worker ants of the test species would encounter it, include the plant into their foraging territory, and eventually find the larva. Over 70 larvae were tested, and those used for more than one trial were always kept isolated from ants at least 1 day before retesting. Tests were done intermittently between 900 and 1600 hours except Camponotus sp. 1 which was active nocturnally. The number of colonies used varied with the species of ant: 1 colony Atta, Paraponera clavata, Pheidole, Crematogaster, Labidus; 2 colonies Aphaenogaster, Ccmponotus, Eciton hamatum; 3 colonies Wasmannia, Tapinoma; 4 colonies Monacis, Azteca, Zacryptocerus; I84 P. J. DEVRIES > 5 colonies Pseudomyrmex, Ectatomma tuberculatum; and > 12 colonies Ectatomma ruidum. Each colony was tested with at least two larvae. Variation in colony responses to larvae was not investigated. T o illustrate a pattern that is apparent on a local scale, the ant taxa found associating with T. irenea larvae were compared with ant taxa found associating with other species of butterfly larvae, Homoptera and plant EFNs. This pattern was then developed further by compiling literature records from other geographic areas in which ant taxa that visit butterfly larvae and secretion producing organisms were reported. RESULTS Larval abundance Table 1 presents the summed totals of weekly larval censuses. Because weekly censuses are summed, a single larva could have been recorded on subsequent occasions, but never twice as the same instar (the longest duration of any instar censused ranged 5-6 days). Lack of larval movement and census interval ensured that each larva was counted only once during each instar. In all three populations most plants accrued larvae, some individual plants (both experimental and controls) accrued higher cumulative larval densities than others, while some individuals were never occupied by larvae during the censuses (10% population 1, 30% population 2, and 12% population 3). However, the most parsimonious 3-way contingency model (larval instar, treatment, population: G = 18.82, d.f. = 14, 0.1 < P < 0.5) showed a significant relationship between larvae and treatment (G = 30.53, d.f. = 3, P < 0.001), that is independent of population. Significantly more larvae of all instars were found on ant occupied plants than on plants with ants excluded, and all populations showed a decline in proportions of later instars on plants without ants (Table 1). Four events might account for the higher numbers of larvae on plants with ants and the declining number of larvae on those plants without ants: (1) female 1.irenea may oviposit more frequently in the presence of ants, generating a pattern of more larvae on ant-tended plants; (2) larvae may crawl or drop off plants without ants; (3) attack by tachinid parasitoids may cause larvae to drop or crawl off the plant; (4) flying predators may remove larvae from plants without ant associates, especially larger larvae. Ant-mediated oviposition Ant-mediated oviposition as shown for some lycaenid species (Atsatt, 1981b; Pierce & Elgar, 1985) is unlikely for 1.irenea. Within the experimental populations, individual females of T. irenea laid single eggs quickly and indiscriminately on leaves, stems, and dead branches of C. billbergianus plants, often alternating between plants with and those without ants. Females also laid on detritus accumulated on plants, or on non-host plants near individual C. billbergianus (personal observations). Therefore, the disparity of larvae between plants with and without ants is most likely caused by egg and/or larval loss rates, and not adult choice of oviposition sites. However, the number of plants in all three experimental populations ( 10-3070) that did not accrue larvae suggests a potential effect of female oviposition undetected by this study. THISBE IRENEA AND T H E EVOLUTION OF BUTTERFLY-ANT MUTUALISMS 185 TABLE I . Attrition of older instars and larval abundance on plants with and without ants. All plants were censused once per week. Population 1 was censused for 31 weeks, population 2 for 26 weeks and population 3 for 42 weeks Instar With ants ((yo) Without ants (T,) Population I (N=30) I st 2nd 3rd 4th Total 54 80 41 22 197 (27) (41) (21) (11) 27 29 15 1 72 (29) (34) (23) (14) 25 (25) 12 (12) 6 (14) 1 (2) 44 (24) (40) (26) (10) 36 36 15 4 91 (38) (40) (21) (1) Population 2 ( N = 30) 1st 2nd 3rd 4th Total 56 65 43 27 191 Population 3 ( N = 42) 1st 2nd 3rd 4th Total 58 99 64 24 245 Larval attrition Larval abundance d.f. c P 3 15 18 170.72452 42.94902 213.67354 <0.001 <0.001 <0.001 Total Population d.f. G P 1 Ants I No ants 3 3 3 3 3 3 37.07103 38.30632 18.144I3 3 1.06788 49.39645 39.68773 213.67354 <0.001 'rest Pooled Hetero. Total 2 Ants 2 No ants 3 Ants 3 No ants Total (40) (40) (16) (4) 18 <0.001 <0.001 <0.001 <0.001 <0.001 d.f. G P Pooled 1 2 3 226.41322 6.40771 232.82093 <o.oo 1 Hetero. d.f. G P 1 I 2 3 Total 1 1 60.38065 99.15112 73.28916 232.82093 <0.001 <0.001 <0.001 Test Population 3 <0.05 <0.001 Larvae dropping of plants The larvae of at least one lycaenid species are known to drop off plants when they are not tended by ants. Although tarpaulins were not placed under plants (cf. Pierce & Easteal, 1986), it is unlikely that larvae dropping off the plants accounted for the disparity in abundance between experimental and control plants. Even when not tended by ants, T. irenea larvae do not drop off their hostplant when attacked by predators in the field or laboratory, nor can they be induced to drop off the plant by prodding them (they grip the substrate tighter). P.J. DEVRIES I86 TABLE2. Comparison of the number of butterflies and tachinid parasitoids arising from larvae reared on experimental plants with ants and without ants over the course of the study With ants Butterflies Tac hinids Total 50 23 73 Origin of larvae Without ants 5 1 6 Total 55 24 79 d.E= I , G=0.641, P=0.423. Furthermore, larvae grown on potted plants in a laboratory never crawled off plants ringed with Tanglefoot ( N > 400, personal observations). Parasihm Fourth instars reared from the experimental populations of C. billbergianus showed that E. ruidum did not protect T. irenea larvae against the attack of tachinid flies. Although larvae (both parasitized and unparasitized) were more abundant on plants with ants, there was no significant difference between rates of parasitoid attack on larvae from plants with or without ants (Table 2). Some tachinids that oviposited directly on T. irenea larvae were ignored by ants, and one species of tachinid circumvented ants by depositing minute eggs on leaf surfaces that were then apparently ingested by larvae (personal observations). This suggests that parasitoid attack did not account for differences in larval abundance between treatments in the experimental populations. However, removing fifth instars may have biased the results if some tachinids only attack this stage. Predators Potted C. billbergianus plants at experimental sites were patrolled by individuals of at least seven species of vespid wasps (Polistes canadensis, Polybia rejecta, Polybia aff. similliana, Stelopolybia areata, Parachartergus fraternus and Brachygastru sp.), all which were observed investigating the stems and leaves carefully, and killing and removing 7.irenea larvae whenever possible. When a wasp encountered a larva without attending ants it immediately stung the larva, eviscerated it, cut the carcass into pieces, and carried it off, leaving the gut contents behind. Small wasp species (e.g. Polybia rejecta) would make several return trips to completely remove the larval carcass, whereas a large species (e.g. Polistes canadensis) could, after manipulation, carry away the entire carcass. No other flying insect predators were observed killing T.irenea larvae. Therefore, it seems most likely that the differences in abundance between experimental and control plant populations was due to the effects of predatory wasps. Protection of larvae by ants In both Clearing and Edges sites, larvae tended by ants stayed on plants significantly longer than did larvae without attending ants (Table 3). All direct THISEE IRENEA AND THE EVOLUTION OF BUTTERFLY-ANT MUTUALISMS 187 TABLE 3. Ant protection from wasp predation on paired larvae on potted plants at two separate sites. ‘The occupancy times of larvae attended by ants were longer than larvae where ants were excluded Larval occupancy longer Clearing sites ( N = 33 pairs) Edge sites ( N = 19 pairs) SitK KffKCt With ants Without ants Equal P (I-tailed) 25 I1 0 1 8 7 <0.001 <0.005 d.f.=2, x2=2.96, P = 0 . 2 3 observations of wasp-larval encounters indicated that once a foraging wasp found a larva unprotected by ants, the larva had no chance of survival. In contrast, wasps of all body sizes encountering larvae with even a single ant in attendance were consistently repelled by the attending ants. Why older instars declined on plants through time is unknown, but it is likely that larger larvae are more readily found by visually hunting wasps. Two parallel observations argue that predation rates increase with larval instar: larval ant-organs which are important to ant association become functional at third instar, and late fourth and all fifth instar T. irenea feed almost entirely at night (DeVries, 1988). The discovery rates of different instar T. irenea by wasps is currently under investigation. Ant responses to larvae Table 4 shows the rsponses of 26 ant taxa tested. Although the responses of some ants were equivocal (e.g. Camponotus sp.-2, Monacis bispinosa), three general outcomes were apparent from encounters between different ant species and T. irenea larvae: ( 1 ) An ant species may ignore larvae (actively or passively), being neither mutualist not predator. Fourteen of the 26 ant taxa showed this response. (2) An ant species may attack larvae, injuring or killing them, thereby being a predator. Four ant taxa responded in this manner. (3) An ant species may investigate larvae and accept rewards from the antorgans. If the ant species continues to accept these rewards and attends the larvae, it thereby becomes a mutualist potentially capable of defending its resources against intruders. Six ant taxa responded in this way. Ants that ignored larvae were either specialist predators (i.e. Eciton) or general scavengers from all subfamilies, those that killed larvae were carnivores in the Ponerinae or secretion foragers in the Dolichoderinae, and those ants that tended larvae were all secretion foragers from the ponerine, formicine, myrmicine and dolichoderine subfamilies. A pattern became evident when 31 common Barro Colorado Island ant taxa were considered with respect to whether or not they were observed tending any species of riodinid or lycaenid butterfly larvae, extrafloral nectaries (EFNs) or homopterans under natural conditions. Ants that tended butterfly larvae were the same taxa that tended EFNs and homopterans (Table 4), and not surprisingly, all are well known to forage on secretions (D. Feener and E. Schupp, personal communication; personal observations). In contrast, it P. J. DEVRIES 188 TABLE 4. Thirty-one common Barro Colorado Island ant species and their reactions to 1.ireneu (=Ti) larvae, and their observed responses to other species of riodinid and lycaenid larvae, + extrafloral nectaries or homopterans. Symbols: = positive response; - =negative response; =response variable; + - =infrequently tended; ?=unknown; * =ant taxa tested with 1.ireneu larvae Ant taxon Ponerinae Ectatomma ruidum* E. tuberculatum* Pachycondyla harpax P . uilosa* P. sp. Paraponera clauata* Odontomachus bauri* Forrnicinae Camponotus sericeiuentris* c . sp. - I * c . sp. -2* Parathrechina sp.* Myrrnicinae Pheidole sp. - I * Monomorium sp. Solenopsis sp. Crematogaster sp. - I * c. sp. -2* Wasmannia auropunctata* Cephalotes atratus* Zacryptocerus sp. - 1* .5. sp. -2' Aphaenogaster araneoides* Atta cephalotes. Tend Ti Kill Ti Ignore Ti - ? + ? - + +- Other larvae EFNs and Hornoptera + +- -+ + + + +- - + f ? ? + ++ + + + + + + + + + +++- - Dolichoderinae Monacis bispinosa* Azteca sp. - 1 * A . SP. -2* Tapinoma sp.* - - + + + Pseudornyrrnecinae Pseudomymex sp. - I * P . sp. -2* + + - + - - - Ecitoninae Eciton hamalum* E . birchelli Labidus praedator: f ? t - would have been surprising indeed to find leaf-cutting ants (Atta) or army ants (Labidus, Eciton) tending any secretion producing organisms. Although not accounting for possible variation ant colonies, or potentially specific larval-ant associations (see below), two conclusions are suggested by these preliminary observations. One is that on Barro Colorado Island there are several possible outcomes in the encounters between ants and 7.irenea larvae (ant taxa ignore larvae, kill larvae or tend larvae). Secondly, of the ants that exhibited tending behaviour toward butterfly larvae, both riodinids and lycaenids, all were species that typically harvest the secretions of both insects and plants. THISBE IRENEA AND THE EVOLUTION O F BUTTERFLY-ANT MUTUALISMS 189 TABLE 5. Out of 266 ant genera recognized by Brown (1973), only these 24 are reported consistently to tend facultatively extrafloral nectaries, Homoptera and butterfly larvae, or combinations thereof. See text for orgins of the records. =Interactions + Taxon Ponerinae Ectatomma M yrmicinae Myrmica Pheidole Tetramorium Monomorium Solenopsis Cremalogaster Wasmannia Dolichoderinae Dolichoderus Monacis Iridomyrmex Azteca Tapinoma Formicinae Oecophylla Brachymyrmex Anoplolepis Acantholepis Prenolepis Paratrechina Lasius Myrmecocystus Formica Camponolus Polyrhachis Number of interactions EFNs Hornoptera Larvae + + + + + + + + ? + + + + + + + + + + + + + + + + + + + + + + ? + + + + + + + + + + + + + + + + + + + + + + + + + + + ? + + + 22 23 23 + + + + + + + + ? Ecological traits of tending ants A robust relationship emerges when records of ants tending EFNs, Homoptera and butterfly larvae from temperate and tropical sites throughout the world are summarized and compared. Of the 266 ant genera recognized by Brown (1973), only 24 are consistently reported as foraging on secretions of both insects and plants (these are listed in Table 5). Virtually all ant genera reported to associate regularly with lycaenid and riodinid larvae (see records and references in Lamborn, 1915; Farquarson, 1922; Jackson, 1937; Hinton, 1951; Clark & Dickson, 1971; Atsatt, 1981a; Cottrell, 1984; Pierce & Elgar, 1985; Maschwitz et al., 1985; Callaghan, 1977, 1986; Fiedler & Maschwitz, 1988, 1989; Horvitz et al., 1987; DeVries, 1987, 1988), also regularly tend homopterans (see records and references in Wheeler, 1910; Lamborn, 1915; Farquarson, 1922; Way, 1963; Malicky, 1969, 1970; Bristow, 1984; personal observations) and EFNs (see records and references in Bentley, 1977; Beckman & Stucky, 1981; Schemske, 1982; Buckley, 1983; Koptur, 1979, 1984; Koptur & Lawton, 1987; Horvitz & Schemske, 1984; Longino, 1984; Smiley, 1985; Beattie, 1985; Whalen & MacKay, 1988; Oliviera & Brandao, 1991; D. Feener & G . Schupp, unpublished data; personal observations). I90 P. J. DEVRIES Although it is not known how specific the foraging biology of all species in the largest ant genera may be (e.g. Camtonotus, Crematogaster, Pheidole, Aeteca, Zridomyrmex), or how complete these literature records are, the overall pattern presented in Table 5 indicates that only a fraction of the world’s generic diversity of ants (in this case less than 10%) tend secretion producing organisms. Thus insects and plants that typically produce secretions are unlikely to have strong interactions with the majority of ant species. DISCUSSION Ecological variation The facultative association between T. irenea and attending ants is mutualistic, and may be an important factor in determining larval population densities on hostplants. When a predatory wasp attempts to attack a larva tended by even a single E. ruidum it is likely that the ant will repel the wasp. In contrast, larvae without attending ants are virtually certain to be killed during a wasp attack. The larvae of T. irenea ‘pay’ for this production against predators by producing a concentrated amino acid secretion that is constantly solicited and imbibed by attending ants (DeVries, 1988; DeVries & Baker, 1989). The protection provided by ants explains part of the higher larval abundance on plants patrolled by ants shown in Table 1. Several factors not examined by this study may also affect larval abundance. Adult vespid wasps hunt for arthropods to supply their growing larvae with food (Spradbury, 1973; Evans & Eberhard, 1970; J. Carpenter, personal communication). If colony size and reproductive state influences wasp foraging behaviour, predator pressure on butterfly larvae is likely to vary in space and time. Thus, the local species composition and reproductive state of individual wasp colonies are factors likely to affect larval population densities of T. irenea. Insect parasitoids are considered strong selective agents for the maintenance of ant association in one North American lycaenid butterfly (Pierce & Mead, 1981; Pierce & Easteal, 1986). Finding that E. ruidum ants provided T. irenea larvae no protection against attack by tachinid flies (Table 2) is consistent with the observations of Malicky (1969, 1970), who observed that ants attending European lycaenids were too slow to protect larvae against parasitoids, and Pierce et al. (1987) who showed that ants were ineffective against a braconid wasp affecting an Australian lycaenid species. Together, these observations indicate that the strength of selection due to parasitoids may, in general, vary by site, the species of butterfly, and the species of parasitoids involved. The quality of protection conferred to myrmecophilous insects by ants can vary with ant species (Bristow, 1984). For T. irenea, smaller ants may be better at protecting larvae against parasitoids than the medium-sized E. ruidum, which is effective against wasp predators. Since the local distribution of ant colonies influences what ant species associate with T. irenea and other riodinid species (personal observations), rates of parasitism and predation may vary with the identity of the ant species tending larvae. Mutualism The present study supports the idea that mutualisms were important in the evolution of myrmecophily in butterflies: larvae gain survival benefits from THISBE IRENEA AND THE EVOLUTION OF BUTTERFLY-ANT MUTUALISMS 191 associating with ants. However, had this study occurred under conditions of negligible vespid predator attack (as tachinid parasitoid attacks were not ant dependent), or had a different ant fauna been tending the plants and larvae, this study might have lent support to the idea that appeasement is a driving force in the evolution of butterfly myrmecophily. The specialized ant-organs of riodinid and lycaenid larvae provide secretions and stimuli critical for obtaining the benefits of ant attendance (Pierce et al., 1987; DeVries, 1988, 1990; Fiedler & Maschwitz, 1988, 1989; DeVries & Baker, 1989). The pattern presented here (Tables 4, 5) suggests that butterfly larvae are attended only by ant taxa that frequently harvest the secretions produced by plants and insects. Thus, specialized larval ant-organs and butterfly-ant associations appear to have been selected for and maintained through facultative mutualisms with a restricted subset of the total ant species-secretion-foraging ants. If only secretion-foraging ants enter into mutualisms with larvae, it is likely that ant taxa with other feeding behaviours (predators, or taxa that ignore larvae) may have played a minor role in the evolution of ant-organs and associated characters. This study suggests that wherever myrmecophilous larvae occur they will be found associating only with ant species that typically use secretions as a major portion of their diet, and that the ant taxa found associating with butterfly larvae will also tend local Homoptera and EFNs. If the patterns found with T. irenea are general, many of the ant taxa in any community, especially tropical ones, should not be larval predators (cf. Malicky, 1970), but should ignore butterfly larvae, homopterans and EFNs. Facultative associations in which several different ant taxa may tend a species of butterfly larva appear to be common among riodinids and lycaenids in the neotropics (personal observations), and among lycaenids elsewhere in the world (Pierce, 1987;J. Thomas, personal communication). Ant taxa that kill ‘I.irenea (i.e. Azteca, M Q ~ Ubut C ~tend S ) other species of butterfly larvae (Table 4)indicate that secretion harvesting alone does not necessarily mean that an ant species will tend a butterfly larva-specialized associations do occur. Among neotropical riodinids there seems to be two broad categories of larval-ant association: facultative generalists that may associate with ants from the subfamilies Ponerinae, Formicinae and Myrmicinae, and specialists that apparently associate only with ants in the Dolichoderinae (DeVries, 1987, unpublished data). Although obligate or highly specific ant associations (involving a single ant species or genus) are uncommon in lycaenids (Pierce, 1987; Thomas el al., 1989) and riodinids (personal observations), it is reassuring to note that even these specialized associations all involve taxa of secretion harvesting ants. Appeasement The influence of appeasement on butterfly-ant interactions has been discussed with respect to how larvae may avoid ant aggression. Thus, ant-organs are thought to ‘detoxify’ ants by secreting adoption substances, appeasement substances or food rewards (e.g. Malicky, 1970; Henning, 1983; Pierce, 1987; Fiedler & Maschwitz, 1989). However, although it has been given thoughtful discussion, the role appeasement plays in the evolution of butterfly ant-organs needs to be broadly assessed experimentally in the future. I suggest that experimental assessment of the ability of larvae to appease ants can be done 192 P.J. DEVRIES through elaboration of the preliminary tests done with I: irenea described above. Future tests should also include a comparison of ant responses to lycaenoid larvae with ant responses to larvae from other groups of Lepidoptera that do not bear ant-organs (e.g. Papilionidae, Pieridae, Nymphalidae, Noctuidae, etc.) . By offering many species of larvae to many species of generally predaceous ants, and scoring what proportion of ant species kill or ignore larvae, one could estimate the importance of appeasement in ecological time. If larval ant-organs have evolved to appease predaceous ants, we would expect to see significant numbers of larvae with ant-organs surviving encounters with ants. If, however, all larvae are killed by ants, this would suggest that larval ant-organs can only ‘appease’ potentially mutualist ant taxa. The contribution of ‘appeased’ ant species to mutualistic associations with larvae can then be evaluated by performing ant exclusion experiments. Using the three outcomes of interactions between T. irenea larvae and ants as a model (ignore, kill, tend), ‘appeasement’, then, is the evolution of ant response from predation to ignoring larvae, and mutualism is the evolution from predation or ignoring larvae to tending them. Appeasement and mutualism There may be sufficient variation in diet among some predaceous ant taxa for appeasement to function in some cases. The subfamily Ponerinae is composed of predaceous ant species, all with well-developed stings used to immobilize arthropod prey (Wheeler, 1910; Brown, 1973, 1976, 1978; Carroll & Janzen, 1973). The genus Ectatomma is unusual among ponerines in that all species spend large fractions of their life harvesting secretions from EFNs (Bentley, 1977; Wheeler, 1986; personal observations), Homoptera (Wood, 1983; personal observations), and myrmecophilous butterfly larvae (personal observations). This suggests that within at least one ant subfamily there has been evolution from a predominantly predaceous diet to one where secretions are important. Although they are not known to tend larvae, the occasional utilization of some secretions in other ponerine genera (e.g. Odontomachus, Brown, 1976; Paraponera, Carrol & Janzen, 1983) may eventually permit larval secretory organs to function in appeasement, eventually leading to mutualism (e.g. as in Ectatomma). Most of the major groups of ants were present by the Oligocene, and the morphology of fossil ants suggests that many life-history patterns, including secretion foraging, were present at this time (Wilson, 1971; Brown, 1973). Assuming that the patterns of ant-larval associations described here reflect evolutionary history, it is plausible that, regardless of which associations evolved first-EFNs, homopterans or myrmecophilous butterfly larvae-once ants began foraging on and protecting secretion producing resources, other groups of plants or animals with secretory capabilities were effectively preadapted to form mutualisms with the same ant taxa. Although providing predaceous ants with appeasement rewards may have been an initial step in the evolution of larval ant-organs for butterflies, once larvae developed the capability to secrete substances, it is likely that the evolutionary refinement of ant-organs and their spread through the lycaenid and riodinid butterfly lineages was utlimately dependent upon mutualisms formed with ants that use secretions. Although this historical scenario cannot be tested, simple experimental manipulations with larvae and ant species can test whether the results of evolution on ant-organs contribute to mutualisms, to what extent THISBE IRENEA AND T H E EVOLUTION O F BUTTERFLY-ANT MUTUALISMS 193 ant-organs function in appeasement, and which ant taxa are likely candidates for exerting selection on ant-organs and other secretion producing organisms. ACLNOWLEDGEMENTS This paper benefited from comments and discussion provided by M. Aide, B. Bolton, L. Gilbert, N. Greig, D. Feener, D. Grimaldi, J. 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