Studies on Neotropical Fauna and Environment

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Ants, plant characteristics and habitat conservation status affect the occurrence of myrmecophilous on an extrafloral nectaried Malpighiaceae

Alexandra Bächtold, Estevao Alves Silva & Kleber Del-Claro

To cite this article: Alexandra Bächtold, Estevao Alves Silva & Kleber Del-Claro (2016): Ants, plant characteristics and habitat conservation status affect the occurrence of myrmecophilous butterflies on an extrafloral nectaried Malpighiaceae, Studies on Neotropical Fauna and Environment, DOI: 10.1080/01650521.2016.1198192

To link to this article: http://dx.doi.org/10.1080/01650521.2016.1198192

Published online: 19 Jun 2016.

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Download by: [CAPES], [Mr Kleber Del-Claro] Date: 20 June 2016, At: 07:01 STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT, 2016 http://dx.doi.org/10.1080/01650521.2016.1198192

Ants, plant characteristics and habitat conservation status affect the occurrence of myrmecophilous butterflies on an extrafloral nectaried Malpighiaceae Alexandra Bächtolda,b, Estevao Alves Silvab and Kleber Del-Clarob aUniversidade de São Paulo, Department of Entomology Ribeirão Preto, São Paulo, Brazil; bUniversidade Federal de Uberlândia, Uberlândia, Minas Gerais, Brazil

ABSTRACT ARTICLE HISTORY We investigated the occurrence of myrmecophilous florivorous lycaenid larvae in Banisteriopsis Received 8 May 2015 malifolia (Malpighiaceae) according to habitat conservation status (disturbed and preserved Accepted 8 June 2016 savanna), plant phenology, height and the presence of tending ants. The abundance and richness KEYWORDS of lycaenids were sixfold and fivefold greater, respectively, in the disturbed area than in the Banisteriopsis; Brazilian protected savanna. Lycaenids occurred mostly on plants visited by Camponotus blandus,a savanna; Camponotus; mutualistic partner of larvae. Habitat type was the main factor influencing lycaenid occurrence, Ectatomma; as plants in open areas offered more food resources and tending ants. Banisteriopsis malifolia was polibetes considered useful as a host for lycaenids in disturbed sites.

Introduction in order to provide appropriate approaches for the conservation of species, which usually involves the The occurrence of organisms is constrained by biotic knowledge of their interspecific interactions (Thomas and abiotic factors that not only influence their distri- 1983; Schmitt & Seitz 2002; Maes et al. 2004). In Brazil, bution but also affect interspecific interactions only recently have lycaenids been studied in detail, with (Folgarait 1998; Tanaka et al. 2007). A main issue for descriptions of their host plants and interactions with conservation ecology is to understand the conditions ants (Kaminski et al. 2010; Schmid et al. 2010; Silva for the persistence of organisms in nature (Samways et al. 2011), but even so our knowledge is undoubtedly 2007). It is only with knowledge of organisms’ habitat underestimated, in comparison to temperate areas. ranges and ecological interactions that we can support Ant–lycaenid interactions seem to be particularly their preservation in natural areas (see Thomas 1991; interesting for the understanding of lycaenid natural Gibbs & Stanton 2001). Butterflies are interesting and history, as some species show a strong tendency to conspicuous organisms whose ecological interactions occur in the presence of tending ants (Fiedler 1991; with plants and other may be key to under- Bächtold et al. 2014). In these mutualistic interactions, standing several coevolved systems in natural commu- ants feed on honey-like solutions provided by larvae nities (Thompson 2005, 2013). and in turn protect them from natural enemies (Weeks

Downloaded by [CAPES], [Mr Kleber Del-Claro] at 07:01 20 June 2016 Among , lycaenid butterflies deserve 2003). Therefore, from a conservation point of view, attention, as some species are now at risk of extinction the maintenance of specific plants species that sustain (Maes et al. 2004; Kaminski et al. 2010; Freitas & tending ants can be a first goal to preserve lycaenids at Marini-Filho 2011; Garvie et al. 2014) and some a local scale (Terblanche & Hamburg 2004; Kaminski aspects of their biology, ecology and occurrence are & Freitas 2010). At least in Brazil, extrafloral nectaried still poorly known in the tropics, in comparison to Malpighiaceae stands out as an important family that temperate areas, inhibiting conservation initiatives can sustain both lycaenids and their ant partners (see Heath 1998; Rabasa et al. 2005; Bais 2015; (Monteiro 2000; Alves-Silva et al. 2013; Bächtold et al. Haaland 2015). For instance, there are quite a number 2013, 2014), thus being ideal as a model to study of studies calling attention to the decline of lycaenid lycaenid habitat requirements. populations in non-tropical areas (Thomas 1985; In the Brazilian savanna, some Malpighiaceae spe- Fischer et al. 1999). Initiatives have been taken aiming cies (e.g. Banisteriopsis, Peixotoa, Heteropterys)which at the detailed understanding of lycaenid life histories

CONTACT Alexandra Bächtold [email protected] Universidade Federal de Uberlândia, Rua Ceará, s/n. Bloco 2D-Campus Umuarama, CEP 38400902 Uberlândia, Minas Gerais, Brazil © 2016 Informa UK Limited, trading as Taylor & Francis Group 2 A. BÄCHTOLD ET AL. Downloaded by [CAPES], [Mr Kleber Del-Claro] at 07:01 20 June 2016

Figure 1. a, Flower and clusters of flower buds of Banisteriopsis malifolia (Malpighiaceae), the host plant for lycaenid larvae. b, Larva of Parrhasius polibetes feeding on a flower bud (arrow). c, A common visiting ant, Ectatomma tuberculatum. Scales: a = 15 mm; b, c = 10 mm.

are hosts for lycaenids also tend to occur on disturbed Del-Claro 2014). Thus we might assume that these sites like clearings and zones recovering from fire or plants in early successional stages may be more attrac- mowing (Bächtold et al. 2014). In disturbed sites these tive to lycaenids, because ovipositing females might be plants usually present increased performance and pro- guided by both the presence of ant-partners and the duce more resources to herbivores (flowers, soft and quality of floral resources that larvae feed on (Wagner tender leaves) and mutualistic ants (increased extra- &Kurina1997;Kaminskietal.2010;Rodriguesetal. floral concentration) (e.g. Banisteriopsis;Alves-Silva& 2010). STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 3

The larval stages of many lycaenids are polyphagous were not used in statistical tests, but rather as a poten- and feed on the reproductive parts of plants, especially tial factor that might influence lycaenid occurrence in a on buds and flowers, but also on fruits (Chew & given site. We also expected to find differences in Robbins 1984; Fiedler 1991; Schmid et al. 2010). lycaenid abundance according to different ant species, Adult females should be able to recognize specific as larvae, even myrmecophilous, can either be attended characteristics of the host plants that may increase or preyed upon depending on the ant species (Robbins survival of larvae (Singer 2008). Besides plant quality, & Aiello 1982; Robbins 1991). food characteristics (Rodrigues et al. 2010) and the presence of ants is especially important for lycaenid species, as adult females use ants as cues for oviposition Materials and methods (Pierce & Elgar 1985; Wagner & Kurina 1997; Study species Kaminski et al. 2010; Bächtold et al. 2014). In addition, the conspicuousness of the host plant is supposed to The study plant B. malifolia was examined during its play a role in lycaenid oviposition choices (Jorge et al. flowering period from February to May 2011. 1988; Meyer-Hozak 2000). Plant height is related to the Lycaenids are found on the plants only during this structural complexity as taller plants may support more specific period, as larvae feed on flower buds and vegetative and reproductive organs, relative to short flowers (Alves-Silva et al. 2013)(Figure 1a, b). The plants; and consequently these showy plants may sus- plants were studied in a Brazilian savanna area in ′ ′ tain more (Lawton 1983), including butter- Uberlândia city (18°97 S, 48°29 W), where they grow flies. For instance, Nowicki et al. (2005) found that mainly in disturbed/open sites, but are also found in lycaenids were negatively related to plants surrounded undisturbed areas. Banisteriopsis malifolia is a much- by vegetation, presumably because these plants are branched shrub (<2 m tall). Flower buds grow along hard to find for adult ovipositing females. This is also inflorescences, close to young leaves with active extra- noted in other lepidopteran groups, but is far from floral nectaries. Buds are round (c.6 mm in diameter) being a pattern (Bergman 2001; Trager et al. 2009). and pinkish; leaves are up to 15 cm in length and In this study, we used a natural experiment to 10 cm in width, and have small hairs on both sides. investigate the abundance and diversity of myrmeco- A pair of extrafloral nectaries is located at each side of philous florivorous lycaenid butterflies in relation to the midrib and is visited by many patrolling ant spe- habitat conservation status (disturbed and protected cies, especially Camponotus spp. and Ectatomma spp. areas), plant characteristics (phenology and height) (Alves-Silva 2011; Vilela et al. 2014; Figure 1c). Species and the presence of different species of tending ants. within these two genera were observed in association Fieldwork was conducted in a disturbed (open) area with several myrmecophilous lycaenids (Robbins & and in a preserved reserve of tropical savanna, and our Aiello 1982; Kaminski et al. 2010). study plant was the extrafloral nectaried Malpighiaceae Banisteriopsis malifolia (Nees & Mart.) B. Gates, which Study sites sustains florivorous lycaenids and their ant partners, such as Camponotus (Alves-Silva et al. 2013). These The “open area” is a private site characterized by

Downloaded by [CAPES], [Mr Kleber Del-Claro] at 07:01 20 June 2016 ants are important partners of tropical lycaenids roughly 10 ha of short and secondary vegetation, with (Kaminski et al. 2010; Bächtold et al. 2014). One inter- a predominance of shrubs (<2 m tall), especially esting aspect of B. malifolia is that it occurs in both Bignoniaceae, Malpighiaceae and Fabaceae, and a mod- open and preserved sites (see Alves-Silva 2011), which erate cover of grasses. A dirt road about 3 m wide permits the evaluation of the associated lycaenid fauna crosses the area and soil erosion is common. The and their interactions in different microhabitats. flow of people, vehicles and animals on this road is As discussed above, given the tendency of constant, imposing injuries and sometimes killing seed- Banisteriopsis to present increased performance lings and small shrubs. In addition, fires and mowing (growth, phenology) in disturbed sites, we hypothe- by bulldozers destroy the vegetation every two to three sized that lycaenids would be more abundant and years. In this area, B. malifolia receives both vertical rich in plants located at the non-protected area, in and lateral sunlight all day. Shrubs are not in contact comparison to conspecific plants at the protected with plant species other than grasses. reserve. Plant height was expected to relate positively The “reserve” is a fenced protected natural site (cer- with lycaenid abundance, as they might stand out in rado sensu stricto) measuring about 230 ha with dense the vegetation and be easier to find. Phenological dif- vegetation containing Ochnaceae, Caryocaraceae, ferences in plants from both sites were investigated, but Vochysiaceae and Myrtaceae, among other plant 4 A. BÄCHTOLD ET AL.

families. This area is also crossed by a narrow dirt road average values were used in analysis. Plant size (in m) (<2 m) and the flow of people and vehicles is limited was estimated once at the start of the study. and requires permission. The site chosen for the study Measurements were made from the plant foot to the (approximately 10 ha within the protected area) had apex of the highest branch. not been burned for the previous 10 years and mowing does not occur at all at this location. The distance between the protected and disturbed sites is approxi- Statistical analyses mately 1.7 km. Banisteriopsis malifolia grows mostly at the borders of the area and individuals are sometimes Quantitative data are presented as mean ± standard shaded by the canopy of large trees, thus receiving low deviation whenever appropriate, and the use of para- direct and lateral light. Shrubs are also in constant metric or non-parametric statistical procedures was contact with other plant species. based on normality tests. We performed a logistic regression to examine the odds of finding lycaenids in a given habitat type. Areas were designated as “0” or Fieldwork and sampling design “1” and lycaenid presence/absence was employed as the In early February 2011, we tagged 40 B. malifolia intercept. The frequency of plants supporting lycaenids ’ shrubs in the open area and the reserve (total of 80 in each area was examined with Fisher s exact test. A ’ plants). However, in the course of the study some Student s t-test was used to test for differences in plant plants died due to unknown causes or did not bloom size between areas. An analysis of covariance test was at all. Therefore, the final sample sizes were standar- used to investigate whether lycaenid abundance was dized to n =29B. malifolia individuals in each area. related to area and plant height (covariate). Ants occur on the plants only during the period of The G test was used to investigate the frequency of extrafloral nectary activity, which coincides with the B. malifolia supporting each ant species in both areas. ’ reproductive season (Alves-Silva et al. 2013). Since Fisher s exact tests were used to analyze the relation plants were tagged in February, i.e. before the repro- between lycaenids and plants with each ant species. A ductive season and ant colonization, we had no control logistic regression analysis was used to test whether of the species of ants that might later occur on them. lycaenids were related to different ant species, but in The frequency (number of plants on which they this last test we did not consider the effect of area, that occurred) of ants was estimated once (February) in is, all data were pooled. Statistical procedures were both areas as their presence on the plants was consis- performed in R statistical software version 3.2.4 tent throughout the study. Ant abundance was not (R Core Team 2016). used as a variable in this study, as we did not know the exact number of ants on a given shrub when lycaenid oviposition occurred. Results Plants were visited weekly for lycaenid sampling, Lycaenids and plant characteristics totaling 14 sampling occasions. On each occasion, flower buds and inflorescences were carefully exam- Twenty-five lycaenid larvae (0.86 ± 0.99 per plant) were

Downloaded by [CAPES], [Mr Kleber Del-Claro] at 07:01 20 June 2016 ined. Larvae were captured, kept individually in trans- found on B. malifolia in the open area (n = 29 plants parent plastic pots (200 ml) and maintained in the examined) whereas only four larvae were found at the laboratory (12 h L:12 h D, ±25°C). Larvae were fed reserve (0.14 ± 0.35 per plant, n = 29 plants examined) whenever necessary with B. malifolia flower buds until (Table 1). These differences were statistically significant pupation (following Bächtold et al. 2013). Adults were in a logistic regression, showing that the odds of finding identified to species soon after emergence and released lycaenids in the open area were six times greater than in in the field whenever possible. During field sampling, the reserve (odds-ratio = 6.6964, intercept = −1.8326, the interactions between lycaenid larvae and ants were slope = 1.9016, p < 0.01). Furthermore, significantly observed to investigate whether larvae were tended by more individual plants supported lycaenids in the open ants or not. area (n = 15; 51.7%) than in the reserve (n = 4; 13.8%) Banisteriopsis malifolia phenology was recorded for (Fisher’sexacttestp <0.05). all tagged individuals at both sites. Observations were Plant height was significantly different between made every two weeks, from March to May. The inten- areas, averaging 1.55 ± 0.29 m in the open area and sity of flowering phenophase was scored from 0 to 4: 1.06 m ± 0.24 m in the reserve (U = 76.0, p < 0.0001; 1=1–25%; 2 = 26–50%; 3 = 51–75%; 4 = 76–100% of n = 29 plants per area). The analysis of covariance plants with flowers (Vilela et al. 2014), and the monthly showed that lycaenids were significantly related to STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 5

Table 1. Larvae of lycaenid species found together with the ant species Camponotus blandus and Ectatomma tuberculatum on Banisteriopsis malifolia at two Brazilian savanna areas with distinct characteristics. Number of larvae with ants Open area Reserve species Camponotus blandus Ectatomma tuberculatum Camponotus blandus Ectatomma tuberculatum Allosmaitia strophius 31 –– Parrhasius polibetes 54 4 – stagira 1 ––– Rekoa marius 42 –– Tmolus venustus 1 ––– Unidentified species 4 ––– Total abundance 18 7 4 0 Total species richness 5 3 1 0

Table 2. Occurrence of lycaenid larvae according to plant (Banisteriopsis malifolia) height and areas (disturbed and reserve). Effects Df Sum of squares Mean of squares F-value Main effects Area 1 0.4259 0.4259 18.4248*** Plant height 1 0.1429 0.1429 6.1847* Interaction effects Area* + plant height 1 0.3321 0.3321 14.3674 *** Residuals 54 1.2481 0.0231 Both the main and the interaction effects were statistically significant. Df = degrees of freedom; superscript asterisks indicate statistical significant differences, *** = p < 0.0001 and * = p < 0.05.

both plant height and the interaction effect between reserve, the scenario was opposite, as E. tuberculatum plant height + area (Table 2). was more frequently associated with B. malifolia plants In the reserve, all four larvae were of Parrhasius than C. blandus (G = 9.9702, df =1,p < 0.01) polibetes. In the open area P. polibetes was also abun- (Figure 3a). There was no overlap between ant species dant (n = 9 larvae, 36% of individuals), but four other on any individual plants throughout the study period. lycaenid species were also found: Rekoa marius (24%; Most lycaenids in the open area were found in associa- n = 6); Allosmaitia strophius (16%; n = 4); Rekoa stagira tion with C. blandus (Fisher’s exact test, p > 0.05) (4%; n = 1); and Tmolus venustus (4%; n = 1). Four (Figure 3b). In the reserve lycaenids were found only larvae (16%) collected in the open area died in the on plants with C. blandus (Fisher’s exact test, p < 0.05) laboratory from unknown causes and their identifica- (Figure 3b). tion was not possible. At the lycaenid species level, there was a slight Plants bloomed in the same period in both areas, difference concerning larvae found together with C. from March to May, but the intensity of flowering blandus and E. tuberculatum (Table 1). Eighteen lycae- was markedly greater in the open area (Figure 2). nids were found in association with C. blandus and The greatest abundance of lycaenids at this site seven with E. tuberculatum at the disturbed site. Downloaded by [CAPES], [Mr Kleber Del-Claro] at 07:01 20 June 2016 occurred in April, when 96% of larvae were col- Plants with C. blandus had significantly more larvae lected. This period overlapped with the maximum than plants with E. tuberculatum (Fisher’s exact test, intensity of flowering. In the reserve, lycaenids were p > 0.05). In addition, the logistic regression showed only found in March and May (n = 2 larvae in each that the odds of finding lycaenids on plants with C. month), when flowering intensity was low blandus were greater (odds-ratio = 3.5625, inter- (Figure 2). cept = −1.5581, slope = 1.2705, p < 0.05). In the open area, both Rekoa species were attended by C. blandus. This ant species also attended P. polibetes in both study Lycaenids and ants areas. Individuals of E. tuberculatum were not observed Only two ant species were frequently found in associa- tending any larvae that co-occurred with them on the tion with the plants, Camponotus blandus (Formicinae) same individual plant. Other than lycaenids, two larvae and Ectatomma tuberculatum (Ectatomminae). In the of the myrmecophilous species Synargis calyce open area most plants supported C. blandus while E. (Felder & Felder 1862) (Riodinidae) were also found in tuberculatum was not found as frequently B. malifolia and were tended by C. blandus, but we did (G = 58.6098, df =1,p < 0.0001) (Figure 3a). In the not include these riodinids in the analyses above. 6 A. BÄCHTOLD ET AL.

Figure 2. Banisteriopsis malifolia flowering phenology, showing the percentage of individual plants flowering in each month. Flowering was more intense in the open area. Numbers inside the circles indicate the percentage of flowering plants.

Figure 3. a, Frequency of Banisteriopsis malifolia individuals supporting Camponotus blandus and Ectatomma tuberculatum. Numbers inside bars indicate the number of plants with each ant species. b, Frequency of lycaenids found in association with each ant species in each study area. Numbers inside bars indicate the abundance of lycaenids. Downloaded by [CAPES], [Mr Kleber Del-Claro] at 07:01 20 June 2016

Discussion In our study, most lycaenids were found in associa- tion with C. blandus, and in fact, this is common in Our results showed that ants (notably C. blandus), lycaenid–ant interactions. In general, lycaenid abun- together with plant phenology, size and habitat affected dance was up to threefold higher on plants with C. the occurrence of larval lycaenids on B. malifolia. The blandus than on plants with E. tuberculatum. These lycaenid species found in this study also occur on other results comply with the literature of ant–lycaenid inter- plant species, especially on Malpighiaceae (Silva et al. actions, where authors state that Ectatomma ants may 2011; Bächtold et al. 2013, 2014). Camponotus species sometimes kill the larvae (Robbins 1991; Bächtold & have been observed tending P. polibetes and Rekoa Alves-Silva 2013). On the other hand, Camponotus ants spp., but not A. strophius (Monteiro 2000; Kaminski play an important role in lycaenid life history, as adult & Freitas 2010). The biology and ecology of T. venustus females of butterflies use these ants as cues for oviposi- larvae is unknown (but see Silva et al. 2014), since tion, and ants also tend the lycaenid larval stages records are based on adult individuals (Pinheiro & (Kaminski et al. 2010; Alves-Silva et al. 2013; Emery 2006). Bächtold et al. 2014). This mutualistic interaction is STUDIES ON NEOTROPICAL FAUNA AND ENVIRONMENT 7

mediated by the sugared liquids produced by caterpil- the ecological factors responsible for the occurrence, lars (see Schmid et al. 2010), and in our study all of the maintenance and stability of the lycaenid fauna at a lycaenid species sampled have ant-organs which are local scale (Brown 1993). Any information on lycaenid responsible for the association with ants to some extent host range and interspecific interactions contributes to (but see Kaminski & Freitas 2010). the understanding of these butterflies in natural areas, In lycaenids, habitat selection is determined by the especially in the neotropics where deforestation imposes conditions required by the immature stages (Ellis 2003) a serious risk for butterflies and their host plants and plants that offer more resources (e.g. food and (Oliveira & Marquis 2002; Freitas & Marini-Filho 2011). mutualistic ant) may sustain a more abundant lycaenid fauna (see Rodrigues et al. 2010). In this context, B. Acknowledgments malifolia is advantageous for the development and survivorship of larvae since it offers plenty of food The authors thank the staff of Clube de Caça e Pesca Itororó (hundreds of flowers) and ant guards (Alves-Silva de Uberlândia, where the study was carried out; Lucas et al. 2013) which can provide enemy-free space for Kaminski for the identification of lycaenid species and two myrmecophilous larvae (Kaminski et al. 2010). In this reviewers for their comments on the manuscript. study, most larvae were found in the open area where plants bloomed intensively. In general, florivorous Disclosure statement lycaenids are well adapted to exploit the cycle of flow- ering seasons (New 1993), and the polyphagous habit No potential conflict of interest was reported by the authors. of many species allows for their maintenance in time and space on different plants (Robbins & Aiello 1982; Funding Kaminski & Freitas 2010; Silva et al. 2011). In this study, habitat conservation status was an We thank Coordenação de Aperfeiçoamento de Pessoal de important factor influencing lycaenid occurrence. Nível Superior (Capes grant number 1142XPOS026); Conselho Nacional de Pesquisa e Desenvolvimento Some studies demonstrate that several lycaenid species Tecnológico (CNPq grant numbers 301605/2013-0 and are common in disturbed areas and stressed environ- 473055/2012-0) and Fundação de Amparo à Pesquisa do ments with open vegetation (New 1993; Ellis 2003). Estado de São Paulo (Fapesp grant number 2010/52231-8) This is because larvae of some species can develop for the financial support. better in hosts adapted to disturbed and/or early suc- cessional habitats (Thomas 1985; Dover et al. 2009). References Banisteriopsis malifolia has characteristics of pioneer/ early successional species (Swaine & Whitmore 1988; Alves-Silva E. 2011. Post fire resprouting of Ban malifolia Válio & Scarpa 2001), such as rapid growth, ability to (Malpighiaceae) and the role of extrafloral nectaries on the associated ant fauna in a Brazilian Savanna. Sociobiology. resprout after disturbance and production of hundreds 58(2):327–340. of fruits dispersed by wind (Alves-Silva & Del-Claro Alves-Silva E, Bächtold A, Barônio GJ, Del-Claro K. 2013. 2016). Because of its rapid growth, this plant stands out Influence of Camponotus blandus (Formicinae) and flower in open areas. This factor may account for the greater buds on the occurrence of Parrhasius polibetes (Lepidoptera: Lycaenidae) in Banisteriopsis malifolia

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