Florivorous Myrmecophilous Caterpillars Exploit an Ant–Plant

Austral Ecology (2018) , – Florivorous myrmecophilous caterpillars exploit an ant– plant mutualism and distract ants from extraﬂoral nectaries

ESTEVAO ALVES-SILVA,1,2* ALEXANDRA BACHTOLD€ 1,3 AND KLEBER DEL-CLARO2 1Universidade do Estado de Mato Grosso, Rua Prof. Dr. Renato Figueiro Varella, Caixa Postal 08, CEP: 78690-000, Nova Xavantina, Mato Grosso (Email: [email protected]); 2Instituto de Biologia, Universidade Federal de Uberlandia,^ Uberlandia,^ Minas Gerais; and 3Universidade de Sao~ Paulo, Ribeirao~ Preto, Sao~ Paulo, Brasil

Abstract Females of myrmecophilous butterflies tend to oviposit in plants visited by ant species that engage in stable associations with its larvae. In Banisteriopsis malifolia, caterpillars are attended by the same ants that feed on extrafloral nectaries. A conflict may arise when both the plant and caterpillars compete for ant attention, and ants are assumed to forage on the highest quality resource. By attending caterpillars, ants can be indirectly detrimental to plant fitness because florivorous larvae feed intensively until pupation. In this study, we specifically investigated (i) whether the occurrence of facultative myrmecophilous Synargis calyce (Riodinidae) caterpillars in B. malifolia was based on ant species (Camponotus blandus or Ectatomma tuberculatum) and abundance; (ii) the monopolization of ants by the butterfly larvae and (iii) the florivory rates incurred by the caterpillars on inflorescences. The abundance of S. calyce was six-fold greater in plants with C. blandus, compared to E. tuberculatum treatments. Caterpillars monopolized up to 50% of C. blandus on the plants, indicating that the resources offered by S. calyce were more attractive to ants than extrafloral nectaries. Florivory by riodinids incurred losses of almost 60% of flower buds. Myrmecophilous riodinids exploited an ant–plant mutualism by attracting aggressive ants that become larvae bodyguards. Thus, this ecological interaction is potentially detrimental to B. malifolia, since the ants, which can provide protection against herbivores, shift to provide defence for one of these herbivores.

Key words: Banisteriopsis malifolia, Brazilian savanna, Camponotus, Ectatomma, Synargis calyce.

INTRODUCTION (B€achtold et al. 2013; Torres & Pomerantz 2016). This timing seems to be important for the natural Many ant species are known for their mutualistic history of myrmecophilous butterflies because it interactions with extrafloral nectary (EFN) plants matches the period when potential specific ant-part- (Del-Claro et al. 2016). These ants, however, not ners occur on plants (Kaminski 2008). Depending only feed on plant-derived resources, but also on the on the ant species, caterpillars can be ignored, secretions of myrmecophilous insects, such as tended or preyed upon (Robbins & Aiello 1982; hemipterans and caterpillars (DeVries 1991; Sendoya DeVries et al. 1992). Therefore, adult females should et al. 2016). For instance, larval stages of Lycaenidae be able to evaluate host plants to maximize larval sur- and Riodinidae butterflies have so-called ant-organs vivorship (Ballmer 2003; Mota & Oliveira 2016) and (DeVries et al. 1992; Campbell & Pierce 2003), thus oviposit in plants with certain ant species to which release a nectar-like solution for ants that, in achieve this goal (Collier 2007; B€achtold et al. 2017). turn, faithfully attend the larvae (Kaminski & Car- A conflict arises when both the plant (with EFNs) valho-Filho 2012). In this mutualistic interaction, and myrmecophilous caterpillars compete for ant ants receive a valuable sugared food source (Cush- attention (DeVries & Baker 1989). Ants can shift man et al. 1994), while butterfly larvae are protected from foraging for plants to animal resources, depend- from natural enemies, especially parasitoids (Stadler ing on quality (Bluthgen€ & Fiedler 2004). Thus, a et al. 2003; Weeks 2003). shift from EFN to insect secretions can occur in In the tropics, florivorous myrmecophilous butter- some scenarios (Katayama et al. 2013). Indeed, it flies occur in a large array of EFN plants, and some- has been recently shown that myrmecophilous cater- times during specific periods of EFN activity pillars can chemically (through secretions from ant- organs) manipulate ant behaviour so that ants remain *Corresponding author. close to larvae (Hojo et al. 2014). In this context, Accepted for publication March 2018. caterpillars can monopolize ant attention (i.e. a high

© 2018 Ecological Society of Australia doi:10.1111/aec.12609 2E.ALVES-SILVAET AL. abundance of ants are attracted to caterpillars, in Blooming and EFN activity are markedly seasonal and take comparison to the number of ants that forage on the place from January/February to April. Flower buds are plant) to get them close and serve as bodyguards. 8 mm in diameter, pinkish and grow in inflorescences Most studies on the interaction between ants and located at the apex of stems (Alves-Silva & Del-Claro myrmecophilous larvae have been performed with 2016). This plant is visited by a wide range of arthropods, of which oil-gathering bees and EFN feeding ants have lycaenids (see Fiedler 1991, 2001; Eastwood & Fra- € been the most studied (Rocha-Filho et al. 2008; Vilela et al. ser 1999; Pierce et al. 2002; Bachtold et al. 2014) 2014). Camponotus blandus and E. tuberculatum (Fig. 1a,b) and little is known about ant associations within are frequently found in B. malifolia (B€achtold et al. 2016). myrmecophilous riodinid caterpillars, despite recent These ants are known as plant guards as they engage in efforts in the neotropics (Kaminski et al. 2013). Since mutualistic associations with EFN plants, thereby reducing many riodinid caterpillars have ant-organs, they also herbivory rates (Oliveira et al. 1987). engage in stable associations, either facultative or Banisteriopsis malifolia also supports a rich fauna of obligate, with ants (DeVries 1988; DeVries et al. myrmecophilous caterpillars (Lycaenidae – B€achtold et al. 2004; Kaminski 2008; Kaminski et al. 2013). More- 2016), some of which are specialized in the family over, myrmecophilous riodinids tend to occur in Malpighiaceae (Kaminski & Freitas 2010). Information on the interactions between ants and riodinids are scarce EFN plants, most likely because the same ants that (DeVries & Baker 1989; Kaminski et al. 2013), but in feed on EFNs may also tend the caterpillars (Robbins B. malifolia (and in other Malpighiaceae) it is known that & Aiello 1982; DeVries 1988; DeVries et al. 1992; myrmecophilous metalmarks co-exist with ants (B€achtold Torres & Pomerantz 2016). et al. 2016), what suggests that larvae can be attended by In this study, we investigated some aspects of the the same ants that attend lycaenids and visit EFNs. The interaction between a facultative myrmecophilous rio- myrmecophilous metalmark S. calyce (Riodinidae) spends dinid caterpillar (Synargis calyce (C. Felder and R. its whole immature stage feeding on flower buds of B. mali- Felder, 1862), Riodinidae) and tending ants (Cam- folia (Fig. 1c,d). ponotus blandus (Smith 1858) and Ectatomma tuberculatum (Olivier, 1792)) in the extrafloral nectaried shrub Banisteriopsis malifolia (Nees and Mart.) B. Sampling and conditions of study Gates (Malpighiaceae). We specifically analysed (i) whether riodinid occurrence was based on ant species A total of 60 B. malifolia individuals were tagged in the end fl (C. blandus or E. tuberculatum) and abundance, (ii) a of January, prior to the onset of the owering season. These shrubs (1.62 Æ 0.02 m tall, mean Æ SE) had the same phe- possible monopolization of ants by riodinid larvae nological conditions, such as presence of young foliage, fl fl and (iii) the orivory rates in in orescences with and absence of flower buds and presence of the target ants. without riodinids. We hypothesized (i) a higher Plants consistently supported either C. blandus or E. tuber- abundance of caterpillars in plants with C. blandus culatum throughout the whole study period (no ant species because ants in this genus are known to engage in overlap), and were tagged to account for two equal groups stable associations with myrmecophilous butterflies, of shrubs (n = 30 shrubs per group) with each ant species. that is, lycaenids (Kaminski et al. 2010), whereas In our study system, Camponotus and Ectatomma occur con- Ectatomma may prey on caterpillars (Robbins 1991); sistently in different individual plants, with no overlap of ii) that ants should be consistently concentrated in different ant species in the same individual plant, a natural € inflorescences with riodinids (ant-monopolization) trend noted in other Malpighiaceae (Bachtold et al. 2017). This permitted us to investigate if riodinids occurred more and (iii) that riodinids themselves should inflict high fl in plants with Camponotus or Ectatomma because no other orivory rates in plants (like their sister group Lycae- ant species were present on tagged plants. Neither ant pres- – nidae Badenes-Perez et al. 2010), compared to ence nor species were manipulated in B. malifolia. other herbivores. In the field, we examined the beha- Synargis calyce caterpillars occurred on the plants from viour of ants towards riodinids to see whether ants February to April. Whenever a larva was found, it was consistently attended caterpillars, what would be evi- monitored in the field until it reached approximately dence of stable ant–larvae relationships (i.e. myrme- 10 mm in length, when part of the study was performed cophily). (objectives ii, iii). This was done to standardize the data, especially on feeding damage (florivory rate). If more than one larva was found on the same individual plant, one was METHODS removed and taken to the laboratory, to maintain only one caterpillar per individual plant. During the study period, Study subjects plants were visited periodically once or twice per week to make sure that the study system persisted unaltered, with- Banisteriopsis malifolia is an EFN shrub that occurs in the out disturbance, and that ants remained on plants. After Brazilian savanna (Cerrado biome) including the city where the fieldwork was completed, caterpillars were collected the work was carried out (Uberlândia city, 18°59 S and reared in the laboratory to investigate parasitism. Adult 48°18 W, southeastern Brazil). A pair of round and convex butterflies obtained from larvae reared in the laboratory EFNs occur at the base of leaves, near the petiole. were used to confirm species identification and potential doi:10.1111/aec.12609 © 2018 Ecological Society of Australia RIODINIDS MONOPOLIZE ANT ATTENTION 3

Fig. 1. Interactions between ants and caterpillars in Banisteriopsis malifolia. (a) Five Camponotus blandus individuals attending a Synargis calyce larvae. (b) An Ectatomma tuberculatum close to a caterpillar. (c) Herbivory mark in a flower bud. (d) S. calyce adult butterfly. Scale bars: 5 mm. parasitism. Adult butterflies were eventually released in the ants on plants and the number that were associated with field at the study area. caterpillars or foraging in other stems or inflorescences. Here, we were interested in whether ants would spend more time attending larvae or visiting a plant’s active EFN. Caterpillar–ant interactions

To investigate potential variation in ant abundance that Florivory might affect the study (objective i), ant abundance was estimated for each plant once per week for 3 weeks in the To examine the florivory rates (objective iii), we estimated morning. It was done before plant flowering and the occur- both the number and proportion (number of buds con- rence of riodinid larvae were detected. Nonetheless, no sumed divided by the total number of buds produced) of significant temporal variation was noted for any ant species flower buds consumed by riodinid caterpillars. These larvae before riodinid occurrence (repeated measures analysis eat all the internal flower bud tissues and leave an empty of variance: F2,87 = 0.8133, d.f. = 2, P > 0.05 and bud shell (Fig. 1c). This type of herbivory is characteristic F2,87 = 0.1852, d.f. = 2, P > 0.05 for C. blandus and E. tu- of caterpillars only. Florivory was examined for a period of berculatum, respectively). Therefore, the abundance of ants 10 days and, during this time, all caterpillars foraged in at the beginning of the study, just after plants were tagged, only two inflorescences, presumably because each plant was chosen for statistical procedures (objective i) to ease produces tens of buds per inflorescence. Florivory (%) was the analyses. compared for inflorescences with and without caterpillars, at the plant level (n = 2inflorescences with and 2 without riodinids, per plant). Here, we intended to investigate Spatial segregation whether riodinids inflicted a loss in flower buds, compared to florivory by other herbivores of B. malifolia. To investigate the distribution and the spatial segregation of ants on different stems (objective ii), each plant with a riodinid larva was observed from 08:00 to 19:00 h. The Ant behaviour number of ants on inflorescences with riodinids and on other inflorescences within the plant was recorded hourly In the field, we conducted ad libitum observations of ants (Apple & Feener 2001). Thus, we noted the location of and caterpillars. These observations were made whenever

© 2018 Ecological Society of Australia doi:10.1111/aec.12609 4E.ALVES-SILVAET AL. we went to the field to accompany the development of lar- 0.60 Æ 0.15; and n = 3 larvae, 0.10 Æ 0.07 larvae vae and confer the plants, and accounted for approximately per plant, respectively) (U30, 30 = 243.5; P < 0.01). 40 hours. We were interested to see whether caterpillars Riodinids were observed on 16 (53%) B. malifolia were attended, attacked or ignored by ants (Kaminski & individuals with C. blandus and on only two (6.7%) Freitas 2010). We also recorded in video the interactions plants with E. tuberculatum (v²=10.889; d.f. = 1; between ants and caterpillars as it could show the eversion P < 0.01). The number of caterpillars on B. malifolia of tentacle organs, structures that evert and release sugar- like solution to ants (DeVries et al. 2004; Kaminski et al. ranged between 0 and 3 larvae, and most plants = 2013). where riodinids were found (n 12 plants) supported only one larva. Riodinids oviposited predominantly in plants where Statistical analyses C. blandus were more abundant. Data showed that the average initial abundance of C. blandus was Quantitative data are presented as the mean and standard 33.4% higher in plants where riodinids were later error whenever appropriate. The frequency of plants with found (t28 = 3.7710; P < 0.001) (Fig. 2). The abun- riodinids according to each ant species was compared using dance of E. tuberculatum was three and four ants on a goodness-of-fit chi-squared test (objective i); the abun- the two plants that supported riodinids; the other dance of caterpillars according to each ant species was plants hosted three to five E. tuberculatum ants. Due – compared with a Mann Whitney U (non-parametric data, to the low frequency/abundance of riodinids in plants objective i). We used a Student’s t test to compare the with E. tuberculatum, we were unable to run statistical number of ants on plants where riodinids were found and plants where they were absent throughout the study period tests. (objective i). A Student’s t test was also used to investigate In plants without riodinids, C. blandus ants were the spatial segregation of ants throughout the day (e.g. ants distributed evenly on up to four stems within plants attending riodinids and ants patrolling the plant on other (Fig. 3) (H3 = 0.8758; P > 0.05) and each stem was stems, objective ii). The distribution of ants within several visited by no more than three individual ants. In con- plant stems was compared using the Kruskal–Wallis tests trast, for plants with riodinids, ants were markedly (non-parametric data, objective ii). A Student’s t test was concentrated on inflorescences with caterpillars performed to compare the florivory (%) (objective iii) (H4 = 49.1379; P < 0.0001). Thus, a pattern of spa- incurred by riodinids and other arthropods. Statistical pro- tial segregation of ants was observed, as most ants fi cedures and gures were made in R and GraphPad Prism remained on inflorescences upon which riodinids statistical softwares, respectively. were feeding on, and attending caterpillars (Fig. 4) (t11 = 8.4801; P < 0.0001) throughout the whole day. Furthermore, a single riodinid larva could be RESULTS

A total of 21 S. calyce were found and caterpillars were six-fold more abundant on plants with C. blandus than on plants with E. tuberculatum (n = 18;

Fig. 2. Abundance (median, quartiles and range) of Cam- Fig. 3. Percentage of Camponotus blandus ants attending ponotus blandus in plants of Banisteriopsis malifolia where caterpillars and foraging on other stems or inflorescences caterpillars were found and where they were absent. The within plants. The symbols ‘***’ and ‘n.s.’ denote symbol ‘**’ denotes P < 0.001, according to a Students’ t P < 0.0001 and non-significant, respectively, according to test. Kruskal–Wallis tests. doi:10.1111/aec.12609 © 2018 Ecological Society of Australia RIODINIDS MONOPOLIZE ANT ATTENTION 5 attended by up to five C. blandus individuals simulta- of up to half the number of flower buds per inflores- neously, all of which walked over the caterpillar body cence. and took turns to attend larvae (Fig. 1a). Synargis calyce caterpillars were found predomi- Caterpillars everted the tentacle organs in the end nantly in shrubs visited by C. blandus and these ants of the abdomen very often in response to antennation attended the caterpillars very often and intensively. by C. blandus. Ectatomma tuberculatum ants also The association between Camponotus ants (i.e. crassus, attended riodinids, but these ants occasionally aban- blandus and rufipes) and myrmecophilous caterpillars doned the caterpillars and foraged on other plant (especially lycaenids) is very common in several plant parts. No more than two individuals of E. tubercula- species (Ross 1966; Fiedler 2001; Kaminski et al. tum attended a larva simultaneously in the field. No 2010). Species of Ectatomma also engage in stable larvae reared in the laboratory were parasitized. associations with riodinid larvae (DeVries 1988; Tor- Among inflorescences containing riodinids, res & Pomerantz 2016), but in our study, the abun- 57.55% (Æ 3.64%; range: 38–86%) of buds had her- dance and frequency of riodinids in plants with bivory signs and all of these (29.25 Æ 1.0 buds; E. tuberculatum was almost negligible. Similar results range: 22–37 buds) displayed the characteristic marks were also found for tropical myrmecophilous lycae- of riodinid feeding damage, such as consumption of nids, which presented a strong tendency to associate the internal flower bud parts (Fig. 1c). In contrast, with Camponotus than with Ectatomma (B€achtold inflorescences without riodinids showed only 4.29% et al. 2016). For myrmecophilous butterflies, associ- (Æ 0.51%; range: 1.4–8%; abundance = 2.21 Æ 0.24 ating with E. tuberculatum may be risky because these buds) of buds with herbivory marks (t14 = 16.1673; ants can either attend or prey on caterpillars (Ross P < 0.0001), such as necrosis and lacerations, none 1966; Robbins 1991), especially the first stages when of which was caused by caterpillars. larvae are small (B€achtold & Alves-Silva 2013). In contrast, Camponotus might either tend or ignore larvae (B€achtold & Alves-Silva 2013). Therefore, in this DISCUSSION case, the risk for caterpillars is lower and might be counterbalanced by the positive effect of ants in lur- All the hypotheses established for this work were cor- ing away natural enemies of the larvae (Kaminski roborated: (i) riodinids occurred mostly in associa- et al. 2010). tion with C. blandus, and were present in the plants Synargis calyce caterpillars monopolized ants that where these ants were more abundant; (ii) ant might otherwise patrol the plant and exert their role recruitment increased in response to riodinid occur- as plant guards. One of the early alleged functions of rence since most ants within plants engaged in inter- EFNs was to distract ants from myrmecophilous actions with caterpillars and a few foraged in other insects (Del-Claro et al. 2016), but in this study, we stems and (iii) florivory by riodinids incurred losses may assume that riodinids represented a better resource to ants than EFNs because caterpillars gath- ered several attending individuals of C. blandus that remained in close contact with larvae throughout the whole day. The quality of resources is important for the decisions of foraging ants (Bluthgen€ & Fiedler 2004), and secretion from riodinids may contain more amino acids than EFNs (DeVries 1988). Our results also suggest that riodinids are a better resource for ants, which potentially allowed the caterpillars to monopolize ant attention and gather up to 50% of ants from plants. Studies with lycaenids indi- cate that tended larvae are less parasitized (Weeks 2003). In our study, no immature was parasitized during the fieldwork. Florivory by S. calyce larvae incurred losses of up to 50% of flower buds of B. malifolia. In comparison, inflorescences without riodinids displayed low florivory rates. Caterpillars consumed flower buds that otherwise could turn into seeds or seedlings. There- fore, the presence of this myrmecophilous riodinid Fig. 4. Abundance (mean Æ standard error) of Campono- species was detrimental to B. malifolia because larvae tus blandus ants attending Synargis calyce caterpillars, and both monopolize patrolling ants and feed intensively ants foraging on inflorescences without riodinids. on plant reproductive structures. In similar studies © 2018 Ecological Society of Australia doi:10.1111/aec.12609 6E.ALVES-SILVAET AL. with riodinid–ant interactions, authors found losses CONCLUSION of 33% in seed production and up to 38% of foliage (Horvitz & Schemske 1984; DeVries & Baker 1989). The evidence presented here indicates that myrme- This asymmetric ant–plant mutualism, that is, the cophilous riodinid caterpillars exploit an ant–plant ants feed on EFNs, but fail to protect the plant mutualism to their own advantage, by attracting against herbivores, is quite common in facultative aggressive ants (C. blandus) that become larvae body- systems (Del-Claro et al. 2016). Nonetheless, the guards and by feeding on flower buds that would exploitation of ant–plant mutualisms by myrme- otherwise be defended by ants from herbivores. From cophilous insects, with consequent disadvantages for the plant’s perspective, the association between ants the host plant as shown in the present study, has and caterpillars results in losses of flower buds and scarcely been studied, but show severe decrements in reproductive output. Taken together, the evidence plant fitness when a myrmecophilous insect exploit suggests that caterpillars of S. calyce might be acting the ant–plant mutualism (Buckley 1983; Horvitz & as parasites of its host plant, by stealing a direct and Schemske 1984). For instance, Ferreira and Tore- important resource of plants – in this case, the EFN zan-Silingardi (2013) showed that florivory in B. mal- feeding ants (which are responsible for herbivore ifolia renders flowers less attractive to pollinating deterrence). Larvae of S. calyce then disrupt the ant– bees, which negatively affects the fruiting rate and plant mutualism. Given the pervasiveness of myrme- the reproductive success of plants. cophilous caterpillars (especially lycaenids) and ants Attendance to caterpillars appeared to boost the in EFN (tropical) plants, such outcomes may be aggressive behaviour of C. blandus because sudden common and largely detrimental to plants, as ants approaches near (~1 m) plants during observation attend the herbivores that they should be protecting triggered marked changes in ant behaviour: they the plants from. became very agitated near the caterpillar, turned their abdomens downward (Yamamoto & Del-Claro 2008) and also displayed co-specific aggressive behaviour. ACKNOWLEDGEMENTS Such behaviour was not noticed when ants were foraging on EFNs. This behaviour is characteristic of Lucas Kaminski for riodinid identification; six anony- the liberation of alarm pheromones that trigger a mous reviewers for their suggestions; Capes (Coor- fast-running behaviour of ants associated with enemy denacß~ao de Aperfeicßoamento de Pessoal de Nıvel hunting and recruitment (Ali & Morgan 1990; Fuji- Superior), CNPq (Conselho Nacional de Desenvolvi- wara-Tsujii et al. 2006). In addition, this ant beha- mento Cientıfico e Tecnologico) and Fapemat viour can be labelled as ‘enticement and binding’ (Fundacß~ao de Amparo a Pesquisa do Estado de Mato (DeVries 1988), whereby caterpillars affect ant beha- Grosso) for funding. viour so that ants remain close to larvae and display aggressive behaviour. This excitation can be attribu- ted to the discovery of a new potential food resource REFERENCES and result in the recruitment of conspecifics. Ali M. F. & Morgan E. D. 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