Influences of Species Interactions with Aggressive Ants and Habitat Filtering on Nest Colonization and Community Composition of Arboreal Twig-Nesting Ants

Environmental Entomology, XX(X), 2018, 1–9 doi: 10.1093/ee/nvy015 Community and Ecosystem Ecology Research

Influences of Species Interactions With Aggressive Ants and Habitat Filtering on Nest Colonization and Community Composition of Arboreal Twig-Nesting Ants

Stacy M. Philpott,1,2 Zachary Serber,3 and Aldo De la Mora4,5

1Environmental Studies Department, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, 2Corresponding author: E-mail: [email protected], 3Ecology and Evolutionary Biology Department, University of California, Santa Cruz, 1156 High Street, Santa Cruz, CA 95064, 4ECOSUR, Departamento de Entomología Tropical, Carretera Antiguo Aeropuerto Km 2.5 Tapachula, Chiapas, Mexico, and 5Current affiliation: Department of Plant and Soil Sciences, University of Vermont, Burlington, VT 05405

Subject Editor: Paul Ode

Received 1 August 2017; Editorial decision 15 January 2018

Abstract Ant community assembly is driven by many factors including species interactions (e.g., competition, predation, parasitism), habitat filtering (e.g., vegetation differences, microclimate, food and nesting resources), and dispersal. Canopy ant communities, including dominant and twig-nesting ants, are structured by all these different factors, but we know less about the impacts of species interactions and habitat filters acting at the colonization or recruitment stage. We examined occupation of artificial twig nests placed in shade trees in coffee agroecosystems. We asked whether species interactions—aggression from the dominant canopy ant, Azteca sericeasur Longino (Hymenoptera: Formicidae)—or habitat filtering—species of tree where nests were placed or surrounding vegetation—influence colonization, species richness, and community composition of twig-nesting ants. We found 20 species of ants occupying artificial nests. Nest occupation was lower on trees with A. sericeasur, but did not differ depending on tree species or surrounding vegetation. Yet, there were species-specific differences in occupation depending onA. sericeasur presence and tree species. Ant species richness did not vary with A. sericeasur presence or tree species. Community composition varied with A. sericeasur presence and surrounding vegetation. Our results suggest that species interactions with dominant ants are important determinants of colonization and community composition of twig-nesting ants. Habitat filtering at the level of tree species did not have strong effects on twig-nesting ants, but changes in coffee management may contribute to differences in community composition with important implications for ant conservation in agricultural landscapes, as well as biological control of coffee pests.

Key words: agroforestry, artificial nest, Chiapas – Mexico, habitat filtering, nest-site limitation

Ants (Hymenoptera: Formicidae) are a useful taxon for examining 2013, Adams et al. 2016), especially between ant species with similar patterns of community assembly and species co-existence in eco- traits (e.g., Fayle et al. 2015). Dominant ants, when patchily dis- logical systems. In the tropics, ants are diverse and abundant and tributed, create gaps into which subordinate species may colonize represent a large fraction of the animal biomass (Hölldobler and (Andersen 2008). Dominant ants may take over food and nesting Wilson 1990). Ant communities are structured by species inter- resources influencing the spatial or temporal patterns of colonization actions, habitat filtering, and dispersal (e.g., Palmer et al. 2003, or survival for subordinate ant species (Sanders and Gordon 2000, Sanders et al. 2003, McGlynn 2006, Dunn et al. 2007, Andersen Dietrich and Wehner 2003, Sanders et al. 2003), thereby affecting 2008, Stuble et al. 2013, Fayle et al. 2015). Ants are often cate- ant communities more broadly (Sanders et al. 2007). Habitat filters gorized as dominance-controlled communities, and competition acting at very local or broader spatial scales may also influence ant is a ‘hallmark of ant community ecology’ (Hölldobler and Wilson communities. Ant communities respond to preferred temperatures 1990, Parr and Gibb 2010). Interspecific competition from native or moisture conditions (Nestel and Dickschen 1990, Perfecto and or invasive ants can affect ant diversity (Leston 1978, Savolainen Vandermeer 1996, Cerdá et al. 1997, Kaspari and Weiser 2000), pre- and Vepsäläinen 1988, Holway et al. 2002, Parr and Gibb 2010). ferred prey sizes (McGlynn and Kirksey 2000), as well food resource Further, ant communities are often structured by competitive inter- availability or distribution (Albrecht and Gotelli 2001, Kaspari et al. actions (Yanoviak and Kaspari 2000, Perfecto and Vandermeer 2001, Blüthgen et al. 2004). Further, broader habitat shifts affecting © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: [email protected]. 1

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vegetation complexity may influence types and sizes of nests avail- in the canopy (but see Powell et al. 2011, Camarota et al. 2015, able to ants or enhance nest-site limitation (Byrne 1994, Torres and Jiménez-Soto and Philpott 2015). Snelling 1997, Armbrecht et al. 2004, Philpott and Foster 2005, Areas of ant community ecology that have received relatively lit- Powell et al. 2011). tle attention, in natural or agricultural habitats, include 1) processes Both species interactions and habitat filtering also influence can- acting at the recruitment stage and 2) the influence of patchily dis- opy ants. Dominant, aggressive canopy ants often form ‘ant mosaics’ tributed dominant ants on other ant species and diversity (Andersen defined as a patchy distributions of ant species with non-overlap- 2008). Here, we examined nest colonization by arboreal, twig-nest- ping foraging ranges resulting from territory defense and aggressive ing ants in shade trees within coffee agroecosystems. We examined behavior (Adams 1994). Ant mosaic formation is often attributed two potential factors that influence the colonization, species rich- to competition for patchily distributed canopy resources, includ- ness, and community composition of twig-nesting ants—species ing hemipterans and extrafloral nectar (Leston 1973, Majer et al. interactions and habitat filtering. First, we examined the influence 1994, Blüthgen and Stork 2007, Dejean et al. 2007), but reasons for of species interactions between the dominant ant, A. sericeasur, existence of these patchy distributions of dominant ants are con- and twig-nesting ants. Second, we examined whether habitat filters tentious (e.g., Ribas and Schoereder 2002, Camarota et al. 2016). driven by tree species differences or surrounding vegetation influ- Canopy ants may be affected by habitat filters both on the trees in enced twig-nesting ants. We specifically asked: 1) Do Azteca pres- which they live and in the surrounding habitat. Habitat filters that ence, tree species identity, surrounding vegetation, and time of year may influence ants include canopy resources (e.g. extrafloral nectar, affect nest colonization? 2) Do Azteca presence, tree species identity, hemipteran resources, fruits, arthropods), nest size or availability, and time of year influence species richness of colonizing ants? and as well as tree size (Kaspari and Weiser 2000, Albrecht and Gotelli 3) Do Azteca presence, tree species identity, and surrounding vegeta- 2001, Ribas et al. 2003, Philpott and Foster 2005, Powell et al. 2011, tion affect composition of colonizing ant species? Klimes et al. 2012, Grasso et al. 2015, Jiménez-Soto and Philpott 2015, Yusah and Foster 2016). In some cases, species composition of ant communities can strongly vary with the tree species on which Materials and Methods ants are found (Yanoviak and Kaspari 2000, Dejean et al. 2008, We conducted this study in Finca Irlanda, a 300-ha shaded, 2015) and strong habitat filters driven by tree species differences organic coffee farm located between 950 and 1,100 m eleva- may yield distinct ant communities. For example, extra floral nec- tion in the Soconusco region of Chiapas, Mexico. Beginning in taries (EFNs) may vary in their morphology or nectar quantity or July 2007, we located a total of 61 shade trees in a coffee agro- quality which may make certain tree species more attractive to cer- ecosystem belonging to three tree species: Inga micheliana Harms tain ant species (Aguirre et al. 2013). Yet, at least one arboreal ant (Fabales: Fabaceae) (n = 20), Trema micrantha L. (Urticales: community failed to respond to addition of artificial nectar, seasonal Ulmaceae) (n = 20), and Alchornea latifolia Swartz (Euphorbiales: differences in EFN nectar production, and presence or absence of Euphorbiaceae) (n = 21). Trees in this agroecosystem are regularly EFNs on trees (Camarota et al. 2015), indicating that ant responses pruned (i.e., annually or bi-annually) which can result in small tree to tree resources may be context dependent. canopies with only three to four major branches. Thus, tree crowns One tropical habitat where both the influences of species inter- in this agroecosystem are likely smaller and provide fewer resources actions and habitat filtering on canopy ant communities can be to twig-nesting ants than the same tree species in natural habitats. examined is traditional, shaded coffee systems. Shaded coffee agro- Each tree was separated by a minimum of 30 m. All trees selected ecosystems support high levels of biodiversity due to a diverse and for this study were located in areas of the farm between 970 and dense shade canopy that shades the coffee shrubs (Perfecto et al. 1,050 m elevation. Half (n = 10, except n = 11 for A. latifolia) of the 1996, Philpott et al. 2008). Coffee systems support two types trees of each species contained nests of the aggressive canopy ant, of canopy ants: 1) dominant ants, including Azteca sericeasur A. sericeasur (hereafter Azteca). We chose these three tree species (Hymenoptera: Formicadae, hereafter Azteca) that build carton because they are among the most abundant trees on the farm (repre- nests in shade trees and forage on shade trees and coffee plants, and senting 38.7, 10.3, and 4.9% of all trees in the study area), because 2) twig-nesting ants (e.g. Pseudomyrmex spp. Lund (Hymentopera: all three species can host twig-nesting ants (Carroll 1979, Livingston Formicidae), Camponotus spp. Mayr (Hymenoptera: Formicidae), et al. 2013), and also because they likely differ in the resources that Procryptocerus spp. Emery (Hymenoptera: Formicidae)) that inhabit they provide to ants. Inga spp. and A. latifolia trees have extra- hollow twigs in both the shade trees and coffee plants. Both domi- floral nectaries that differ in shape and size and may also differ in nant and twig-nesting ants are of interest in coffee agroecosystems terms of the quality and quantity of nectar provided (Aguirre et al. because they provide important ecosystem services (e.g. pest control) 2013). I. micheliana and A. latifolia also support high populations that benefit coffee farmers (Gonthier et al. 2013, Morris et al. 2015). of hemipteran insects (e.g., scales) that provide honeydew to tending Colonization, species richness, and community composition of ants, yet the population densities of hemipterans may vary greatly twig-nesting ants on coffee plants is affected by Azteca ants (Philpott on different tree species in the farm (Livingston et al. 2008, Gonthier 2010) and even by aggressive ground-nesting ants that forage on 2014). coffee plants (Ennis and Philpott 2017). Additional factors that may We placed 16 artificial nests (bamboo sticks, 10–20 cm long, influence colonization and communities of twig-nesting ants may 3–8 mm openings) in each tree by attaching nests to the main trunk include presence of canopy resources (e.g., hemipterans, extrafloral and primary branches of trees with plastic string. All nests were nectar, hollow twigs of different sizes), presence of dominant ants, placed on 23–24 July 2007. We harvested four nests every 3 months presence of other twig-nesting ant species, habitat characteristics, after placement (e.g., in October 2007, February 2008, May 2008, and habitat disturbance (Philpott and Foster 2005, Philpott 2010, and July 2008). After harvest, we opened all bamboo nests, recorded Philpott et al. 2010, Powell et al. 2011, Jiménez-Soto and Philpott whether the twig was occupied or not, and identified all ants to 2015). Yet influences of both species interactions and habitat filters species or morphospecies. If a twig contained any ant individuals, remain relatively unexplored because few studies have used manipu- it was considered occupied. Placing nests in the outer braches of lative experiments to examine nest colonization of twig-nesting ants the trees may have allowed a closer examination of certain canopy

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twig-nesting species, but we attached nests to the trunk and large chose to use proportion, rather than raw numbers of occupied nests branches for three reasons. First, we expected that placing nests on due to unequal numbers of nests collected because of loss of experi- the trunk and main branches would highlight any interactions with mental bamboos. Azteca, given that Azteca ants mainly forage on the main trunks of We compared the species richness of ants occupying artificial shade trees (Philpott 2005). Second, coffee farmers regularly prune nests on trees with and without Azteca ants, on the three tree spe- canopy tree branches, and putting nests on smaller branches would cies, and by harvest month. We calculated individual-based rarefied have increased the chances of nest loss. Third, logistical difficulties species richness with PAST (Hammer et al. 2001) and graphed 95% presented by steep terrain, tall trees, and heavy pruning made it diffi- confidence bands to compare richness on plants with and without cult and dangerous to reach outer branches with ladders or by climb- Azteca and on A. latifolia, I. micheliana, and T. micrantha trees, and ing trees. Further, we chose to use a design without replacement (e.g., collected after 3, 6, 9, or 12 months. Because some nests were lost putting all nests at the start of the experiment and harvesting them during the experiment (due to farm management), sample sizes of gradually over time) due to logistical constraints and danger associ- artificial nests were unequal on experimental trees. We thus chose ated with climbing trees that are often pruned. However, based on not to use mean species richness as a dependent variable in any ana- our previous work in the system, we estimate that there are between lysis examining the role of tree species richness on ant species rich- 200 and 400 nests within 10 m of each tree on to which nests were ness. Although canopy ant richness may often be correlated with tree added (in both coffee plants and shade trees) and thus nest availabil- richness (e.g., Ribas et al. 2003), at least one study has demonstrated ity of 16, 8, 12, or 4 nests would not largely bias our nest occupation that a loss of tree richness is not a major driver of changes in ant results. species richness in canopy trees (Klimes et al. 2012). Because vegetation and management characteristics vary greatly We compared species composition of twig-nesting ants colonizing in coffee farms and also affect twig-nesting ant communities and nests on trees with and without Azteca, on A. latifolia, I. micheliana, nest colonization (e.g., Armbrecht et al. 2004, Philpott and Foster and T. micrantha trees, and harvested after 3, 6, 9, and 12 months 2005), we measured vegetation characteristics within 12.5 m of trees after placement with three methods. We also included tree circumfer- where nests were added. In addition, because presence of Azteca was ence and height, as well as characteristics of the surrounding vegeta- not directly manipulated, we wanted to ensure that any observed dif- tion to examine whether differences in these features influenced ant ferences in colonization in areas with and without Azteca were not composition. To examine differences in composition of ants coloniz- due to vegetation differences in the surrounding areas. We counted ing artificial nests, we used a permutational multivariate analysis of and identified all trees and calculated the proportion of trees in variance (PERMANOVA) using the ‘adonis’ function in the ‘vegan’ the genus Inga. A high proportion of Inga spp. trees is indicative package in R (Oksanen et al. 2016). We included all ant species for of intensive coffee management whereas a low proportion of Inga which more than one occupied nest was collected (for a total of 10 spp. trees is indicative of more diverse, less intensive shade man- species included, Table 1). We used Bray–Curtis distances to assess agement. We compared the mean number of trees within 12.5 m of dissimilarity among communities and conducted 999 permutations. trees with and without Azteca and for each of the three tree species We included eight factors in the PERMANOVA including Azteca with general linear models in SPSS. We ran Pearson’s correlations to presence, tree species identity, month of harvest, tree circumference, determine if any of the three vegetation variables were correlated. tree height, and number of tree species within 12.5 m of trees where We used the number of tree species (correlated with tree abundance nests were placed. In addition, trees used in this study were tagged, [Pearson’s coefficient = 0.657, P < 0.001] and percent of Inga spp. and we included the x and y coordinates within a mapped 45-ha trees [Pearson’s coefficient = −0.457, P < 0.001]) in other analyses. plot to determine if any aspect of the spatial distribution of the trees Although we did not measure canopy cover in this study, canopy influenced colonization by twig-nesting ants. To visualize results, cover is frequently correlated with tree abundance, tree richness, we created nonmetric multidimensional scaling (NMDS) plots with and percent of trees with Inga in data from the study site (Philpott, the ‘ordiplot’ function and superimposed significant explanatory unpublished data). We also measured the circumference and height of each tree on which nests were placed to see if those features differed for trees with and without Azteca or for the three different tree species as these factors may impact nest colonization by ants. We examined whether nest occupation of twigs depended on Azteca presence, tree species identity, tree species richness, and month of harvest with generalized linear mixed models in R (R Core Team 2017). We used the cbind function to create a matrix of number of occupied and unoccupied nests used as the dependent variable, and then included Azteca presence, tree species identity, harvest month, and tree species richness within 12.5 m as fixed factors and tree individual as a random factor. We used the binomial (logit) fam- ily. We ran all possible models (with and without interaction terms, and with all single and combinations of fixed factors) and compared the AIC (Akaike information criterion) scores to choose the best model. We also ran the same models with number of occupied nests (instead of using the cbind function), and results were qualitatively identical. We do use proportion of occupied nests to visually repre- Fig. 1. Mean (±SE) proportion of artificial nests occupied by twig-nesting ants sent the results (Fig. 1). We calculated proportions with number of on three species of canopy shade trees with and without Azteca sericeasur in a coffee agroecosystem in Chiapas, Mexico. Nests placed in July and occupied nests as the numerator (range no occupied nests to four harvested after 3, 6, 9, or 12 months. Letters show significant differences occupied nests) and number of nests collected from one tree during between colonization in different months; all Azteca versus no Azteca one harvest month (range one to four nests) in the denominator. We treatments were significantly different P( < 0.05).

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variables with the ‘envfit’ function in the ‘vegan’ package. We only 55; P = 0.997), or proportion of Inga trees (F = 1.272; df = 2, 55; include significant factors in the final plots presented. P = 0.288) depending on tree species identity (Table 2). Features of To examine influences of Azteca and tree species identity on indi- the trees on which nests were placed also strongly varied ranging vidual ant species, we examined the number of occupied nests of from 65 to 340 cm circumference and 6 to 14 m height (Table 2). each species on trees with and without Azteca and on different tree Tree circumference differed with Azteca presence (F = 5.58; df = 1, species with chi-square tests. We also examined the mean number of 55; P = 0.022) and with tree species (F = 33.52; df = 2, 55; P < 0.001), nests (natural log transformed) occupied on individual trees (with and there was also a significant interaction between Azteca presence and without Azteca and of different tree species) with general linear and tree species (F = 3.60; df = 2, 55; P = 0.034), where A. latifolia models where each tree was considered a replicate. and T. micrantha trees with Azteca were larger, but I. micheliana trees with Azteca were smaller. Tree height differed by tree species (F = 6.57; df = 2, 55; P = 0.003), but did not differ on trees with and Results without Azteca (F = 1.49; df = 1, 55; P = 0.227). The vegetation characteristics varied in the study area with number We recovered 796 of the 976 nests placed. Of those, 202 nests of trees within 12.5 m radius circles varying from 3 to 33 individu- (25.4%) were occupied by one of 20 species of ants. The most com- als, the number of tree species varying from 2 to 11, and the propor- mon ant species encountered in artificial nests were Solenopsis picea tion of Inga spp. trees varying from 0 to 1. However, there were no Emery (Hymenoptera: Formicadae) (17.7% of occupied nests), differences in the tree abundance (F = 0.641; df = 1, 55; P = 0.427), Procryptocerus scabriusculus Forel (Hymenoptera: Formicadae) tree richness (F = 0.481; df = 1, 55; P = 0.491) or proportion of Inga (17.2%), Pseudomyrmex elongatus Mayr (Hymenoptera: trees (F = 1.777; df = 1, 55; P = 0.188) depending on Azteca pres- Formicadae) (13.3%), Dolichoderus lutosus Smith (Hymenoptera: ence (Table 2). Likewise, there were no differences in tree abundance Formicadae) (12.8%), and Crematogaster crinosa (F = 1.544; df = 2, 55; P = 0.223), tree richness (F = 0.003; df = 2, Mayr (Hymenoptera: Formicadae) (9.4%) (Table 1). As expected we

Table 1. Numbers of colonies of all ant species that colonized artificial nests placed on three species of shade trees with and without colonies of Azteca sericeasur ants in coffee farms in Chiapas, Mexico

Ant species Code Total Ant presence Tree species

No. colonies No Azteca Azteca P Alchornea latifolia Inga micheliana Trema micrantha P

Azteca sp. 1 AZSP 1 1 0 0.317 0 0 1 0.368 Camponotus abditus CAAB 1 1 0 1.000 0 0 1 0.368 Camponotus sp. 1 CASP 1 1 0 0.317 0 0 1 0.368 Camponotus striatus CAST 8 2 6 0.317 1 2 5 0.368 Colobopsis sp. 1 COSP 4 2 2 0.157 0 2 2 0.197 Crematogaster carinata CRCA 9 8 1 0.020 2 6 1 0.097 Crematogaster crinosa CRCR 19 16 3 0.003 1 10 8 0.029 Crematogaster nigropilosa CRNI 1 1 0 0.317 1 0 0 0.368 Crematogaster sumichrasti CRSU 1 1 0 0.317 0 0 1 0.368 Dolichoderus lutosus DOLU 26 19 7 0.019 1 15 10 0.003 Monomorium sp. 1 MOSP 1 0 1 0.317 1 0 0 0.368 Neoponera crenata NECR 1 1 0 0.317 1 0 0 0.368 Nesomyrmex echinatinodis NEEC 9 5 4 0.739 0 4 5 0.097 Platythyrea punctata PLPU 1 1 0 0.317 0 1 0 0.368 Procryptocerus PRSC 35 26 9 0.004 6 14 15 0.124 scabriusculus Pseudomyrmex ejectus PSEJ 1 1 0 0.317 0 1 0 0.368 Pseudomyrmex elongatus PSEL 27 14 13 0.847 10 6 11 0.459 Pseudomyrmex filiformis PSFI 6 1 5 0.102 1 0 5 0.030 Pseudomyrmex gracilis PSGR 14 5 9 0.285 2 3 9 0.046 Solenopsis picea SOPI 36 36 0 <0.001 17 18 1 0.001

Table 2. Mean (±SE) characteristics of shade trees (circumference and height) and vegetation variables (tree abundance, richness, and proportion of one tree species) within 12.5 m of trees on which artificial nests were placed in coffee farms in Chiapas, Mexico

Tree circumference Tree height (m)¶ No. trees No. tree species Proportion of Inga spp. trees (cm)§

Azteca 148.35 ± 11.41 (a) 10.48 ± 0.39 15.65 ± 1.17 6.52 ± 0.41 0.59 ± 0.04 No Azteca 123.63 ± 8.61 (b) 9.87 ± 0.39 17.17 ± 1.44 6.13 ± 0.36 0.65 ± 0.03 Alchornea latifolia 189.04 ± 12.05 (a) 10.14 ± 0.39 16.05 ± 1.49 6.33 ± 0.4 0.61 ± 0.04 (a,b) Inga micheliana 94.05 ± 5.25 (c) 9.08 ± 0.46 (b) 18.55 ± 1.76 6.30 ± 0.56 0.67 ± 0.05 Trema micrantha 122.85 ± 8.24 (b) 11.33 ± 0.46 (a) 16.39 ± 0.92 6.33 ± 0.27 0.62 ± 0.02

§Small letters show significant differences in tree circumference measurements between Azteca and No Azteca trees and between the three species. ¶Small letters show significant differences in tree height between the three tree species.

did not find A. sericeasur, a species that primarily inhabits carton nests, in the artificial nests. The proportion of occupied nests was significantly influenced by Azteca presence and by harvest month, however, nest occupation did not differ with the tree species in which nests were placed or with tree species richness in the surrounding area. The model that best predicted nest occupation included Azteca presence, tree species identity, and month (and tree individual as a random factor) but did not include tree species richness within 12.5 m or any interaction terms (Supp Table S1 [online only]). Occupation on trees without Azteca was two to three and a half times greater than on trees with Azteca (F = 15.349; df = 1, 60; P < 0.001, Fig. 1). Likewise, occupation was roughly twice as high in nests harvested after 9 (in May) and 12 months (in July) compared with those harvested after 3 (in October) or 6 months (in February) (F = 6.256; df = 3, 180; P < 0.001, Fig. 2). However, tree species identity was not a significant predictor of nest occupation (F = 2.7028; df = 2, 120; P = 0.071). Species richness in artificial nests was not significantly altered by the presence of Azteca, by tree species identity, or by sample month. Although the number of ant species colonizing trees without Azteca was about twice as high, when scaled to the same number of colonies collected, richness did not differ (Fig. 2a). Likewise, richness in nests collected from A. latifolia, I. micheliana, and T. micrantha (Fig. 2b) or 3, 6, 9, or 12 months after placement (Fig. 2c) did not differ significantly according to 95% confidence ellipses. Composition of ants colonizing artificial nests was significantly influenced by presence ofAzteca , tree height, the number of tree species surrounding the tree where nests were placed, as well as location of the tree (x and y coordinates) relative to other trees, an additional indicator of habitat filtering. The NMDS plot shows a clear separation between species composition of ants colonizing nests on trees with and without Azteca (Fig. 3). The PERMANOVA shows that the composition of ants was influenced by Azteca presence (P = 0.001), number of tree species (P = 0.008), tree height (P = 0.018), x coordinate (P = 0.001), and y coordinate (P = 0.002) within the 45-ha plot, but did not vary with differences in tree species identity (P = 0.078), harvest month (P = 0.425), or with differences in tree circumference (P = 0.173). Several ant species were more frequently encountered in nests on trees without Azteca or in one or two species of trees compared with others. Five species were significantly more likely to occur in nests on trees without Azteca, but no species were more common on trees with Azteca (Table 1). Four species were more likely to occur in T. micrantha trees; two of those were also more likely to occupy nests in I. micheliana trees. Only one ant species was more likely to occupy A. latifolia or I. micheliana trees and not T. micrantha (Table 1). No other ant species differed with Azteca presence or tree identity. Some ant species occupied more or fewer nests per tree on trees with or without Azteca. Most species that were more likely to occur on trees without Azteca also occupied more nests per tree on trees without Fig. 2. Rarefaction curves showing species accumulation of twig-nesting ants colonizing artificial nests in canopy trees with and withoutAzteca sericeasur Azteca; however, due to low numbers of nests overall collected and (a), in three different shade tree species (b), and collected in different sample high variation, only S. picea (F = 5.281; df = 1, 44; P = 0.026) occu- months (c) in a coffee agroecosystem in Chiapas, Mexico. Lines show pied significantly more nests per tree on trees without Azteca (Fig. 4). rarefaction curves, and ellipses show 95% confidence bands around the Most ant species for which occurrence did not differ on trees with and richness estimates. Curves with overlapping confidence bands do not differ without Azteca occupied more nests per tree on trees with Azteca; in rarefied richness. however, only Pseudomyrmex gracilis Fabricius (Hymenoptera: Formicadae) occupied significantly more nests (F = 6.679; df = 1, Discussion 44; P = 0.013), and Camponotus striatus Smith (Hymenoptera: We found strong effects of species interactions with Azteca and Formicadae) occupied marginally significantly more nests (F = 3.035; harvest month, but not habitat filters related to shade tree species df = 1, 44; P = 0.088) on trees with Azteca. No other species occupied identity or tree species richness in the surrounding area on colon- more or fewer nests on trees with or without Azteca or on different ization of artificial nests by twig-nesting ants on areas of the canopy species of trees (P > 0.05). trees where Azteca are active. A negative influence of Azteca on the

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colonization of twig nests is consistent with Azteca effects on nest of the rainy season, even for nests placed for a shorter time period colonization within the coffee plant layer (Philpott 2010) and also (Philpott 2010, Jiménez-Soto and Philpott 2015, Ennis and Philpott consistent with the impacts of other aggressive, ground-nesting ants 2017). Second, many of the species collected from artificial nests are in limiting twig-nest colonization on coffee plants (Ennis and Philpott polydomous, or inhabit several nests for a single colony (e.g., Ward 2017). We also saw higher occupation of twig nests harvested in May 1985). Nests that were in the canopy for a longer time period may and July, 9 and 12 months after placement. This higher occupation have experienced higher rates of colony expansion or budding from could be due to three factors. First, more ant species go on nuptial these polydomous ant species colonizing from neighboring artificial flights and colonize nests shortly after the start of the rainy season or natural tree twig nests on the same tree. Third, it is possible that (e.g. May in the study region) (Kaspari et al. 2001), and all studies an increase in nest occupation later in the experiment could be an examining artificial nest colonization by arboreal twig-nesting ants artifact of lowered nest availability (16 nests at the start versus 4 in the same study sites have found higher colonization at the start nests during the last 3 months). However, we estimate based on previous research that twig-nesting ants have between 190 and 390 nests available to them within a 12.5 m radius of the focal trees, making the difference between 16 and 4 nests relatively small. Contrary to our predictions, neither habitat filtering at the level of tree species nor surrounding vegetation were important determinants of colonization by twig-nesting ants. We did not measure specific canopy resources available to twig-nesting ants; however, previous studies document differences in the characteristics of the three species. In the study sites, I. micheliana and A. latifolia trees have high scale insect populations and EFNs, and scale abundance differs with species (Livingston et al. 2008), as may the quantity and quality of nectar provided in the EFNs of different tree species (Koptur 2005, Blüthgen and Feldhaar 2010). However, these two tree species are also frequently and heav- ily pruned, likely removing many of the dead twigs and branches and limiting the nesting resources available to twig-nesting ants. On the other hand, T. micrantha is among species in neotropical forests described as having straight stems with a well-developed pith canal that make them appropriate for twig-nesting ant species colonies (Carroll 1979). T. micrantha trees used for this study are taller than the I. micheliana or A. latifolia trees (S. Philpott, personal obser- Fig. 3. NMDS plots showing differences in species composition between vation); they have straight stems, few low branches, and are infre- twig-nesting ants colonizing artificial nests on canopy shade trees with and quently pruned, leading us to expect higher occupation on those trees without Azteca sericeasur in a coffee agroecosystem in Chiapas, Mexico. due to colony budding. We expected that differences in tree species Each dot represents a separate shade tree; filled in dots are trees withAzteca , would result in differences in colonization, but perhaps the relatively and open dots are trees without Azteca nests. The arrows show additional high nest-site limitation in this managed system is a stronger driver of significant predictors of species composition (tree, height, no. of tree species within 12.5 m of focal trees and spatial distribution of trees within a 45 colonization than species differences in food resources or nest quality. hectare plot). Similarity was calculated with the Bray–Curtis index. A lack of difference with tree species could also be due to the fact that

Fig. 4. Mean (±SE) number of nests occupied by twig-nesting ant species on individual trees with and without Azteca sericeasur in coffee agroecosystem in Chiapas, Mexico. Asterisks show species with significant P( < 0.05) or marginally significant (P < 0.08, asterisks in parentheses) differences in number of nests occupied depending on Azteca presence. Species abbreviations are the same as in Table 1.

we placed ant nests on the main trunk and branches, whereas most 2010). Finally, colonization of one species (Nesomyrmex echinatino- canopy resources differ in the outer crown of the tree. dis Forel [Hymenoptera: Formicadae]) did not differ on trees with and We did not find significant influences of either species interac- without Azteca, even though the frequency with which this species tions with Azteca or habitat filtering related to differences in tree colonized coffee plants with and without Azteca differs (Livingston species on ant species richness. The lack of effect of Azteca on spe- and Philpott 2010, Philpott 2010). This species may be concentrating cies richness is consistent with previous studies on twig-nesting ant its nesting efforts in the coffee layer (Livingston et al. 2013), or may colonization in the coffee layer (Philpott 2010). One reason that we be inhabiting canopy twigs in the crown, and not near the main trunk may not have documented differences in species richness of coloniz- or branches of the tree. ing ants on trees with and without Azteca is that we were using a Ant community composition was also strongly influenced by single species of nesting resource (bamboo) and a single size of nest habitat filters related to tree height and differences in the surround- entrance. In coffee agroecosystems, variation in nest size availabil- ing vegetation (tree species richness) as well as the spatial location ity influences canopy twig-nesting ants (Jiménez-Soto and Philpott of trees within the farm. The observed differences in ant compos- 2015) and variation in species richness of nesting resources influ- ition with tree size are consistent with other studies documenting ences richness of twig-nesting ants on the ground (Armbrecht et al. differences in ant abundance (Yusah and Foster 2016), ant richness 2004). A second explanation could be that Azteca ants base their (Klimes et al. 2012), and ant composition (Dejean et al. 2008) on diets primarily on honeydew from scale insects and not on EFN (a larger and smaller trees, even of the same species. Tree species rich- highly available resource in this system), a resource used by several ness was positively correlated with tree abundance and negatively twig-nesting ant species. Thus, Azteca may monopolize one impor- correlated with the percent of Inga spp. shade trees, all of which tant food resource used by the subordinate, twig-nesting ants, that might have contributed to observed differences and increases in can thus exploit them. We also did not see differences in species rich- the number of recruiting species. Further, canopy cover positively ness of colonizing nests in different months, despite finding a higher correlates with tree richness and abundance, so any one of those proportion occupied nests later in May or July. This may be either factors, or a combination, may affect the ant composition. Philpott because all ant species are present and expanding into new nests year (2010) found that tree richness influences the composition of ants round, or due to priority effects where ant species that colonized colonizing artificial nests on coffee plants. An area with more tree nests at the start of the experiment tended to hold on to these nests species may harbor different species that are recruiting to new for the duration of the time (Livingston and Philpott 2010). nests. Characteristics of more vegetatively complex coffee habitats We found that Azteca presence influenced twig-nesting ant com- including both diversity of nesting resources (Armbrecht et al. 2004, munity composition and colonization by individual ant species, in Powell et al. 2011, Jiménez-Soto and Philpott 2015) and connectiv- areas of the canopy where Azteca are active. This result is in contrast ity between canopy trees (Powell et al. 2011, Yusah and Foster 2016) to a lack of effect of Azteca presence on composition of twig-nesting may support higher diversity or abundance of ants and thus higher ants colonizing coffee twigs (Philpott 2010). This difference in Azteca recruitment (Philpott and Foster 2005). Additionally, spatial location influence in the coffee and shade trees may be because Azteca forag- of trees within the sampled area also correlated with differences in ing trails are stronger on the main trunk and branches in trees com- species composition. One reason for this spatial clustering, it might pared with coffee plants (Philpott 2005, Gonthier 2014). We did find appear from examining the placement of the x and y coordinate vec- differences in tree circumference on trees with and without Azteca, tors in relation to Azteca and No Azteca trees (Fig. 3) could be that perhaps contributing to this finding. However, trees with Azteca selected Azteca trees were clustered in one area of the farm (due to were larger, which should be associated with more food or other underlying vegetation differences or elevation changes in the coffee resources, and higher occupation, not lower occupation, as viewed farm). Azteca trees are indeed clustered in the farm, but this cluster- here. Species-specific effects of Azteca presence may be related to the ing is unlikely due to vegetation differences or preferences for certain ecology of different ant species. Five species (Crematogaster carinata trees (Vandermeer et al. 2008). Further, trees with Azteca, generally, Mayr [Hymenoptera: Formicadae], C. crinosa, D. lutosus, P. scabri- as with trees with Azteca selected for this study are not spatially clus- usculus, and S. picea) more often occupied nests on trees without tered along the x- or y-axes of the 45-ha plot in which we have sam- Azteca and one (S. picea) occupied more nests per tree on trees with- pled (Vandermeer et al. 2008). The elevation differences at locations out Azteca. All of these species are nesting generalists that inhabit of trees used in this study was less than 100 m, and thus unlikely to twig-nests in multiple vegetation strata in coffee farms (Livingston drive major changes in twig-nesting ant composition, even though et al. 2013, Ennis and Philpott 2017). Further, C. carinata, C. crinosa, composition of twig-nesting ants composition in coffee twigs does and S. picea frequently occupy multiple colonies on the same plant vary along much greater elevation ranges (Gillette et al. 2015). But, in colonies with hundreds of individuals (Philpott, unpublished data). other differences in environmental features that were not sampled These nest generalists, with large colonies, likely also forage on the along the spatial gradients (e.g., connectivity, distance between trees main trunk and branches of canopy trees, increasing their chance of or tree canopies) may result in differences in ant composition due to interacting with Azteca and leading to higher occupation on trees environmental requirements or foraging capabilities of different ant without the dominant ant. But at least one other study failed to find species (Klimes et al. 2015). Finally, spatial differences in compos- a negative interaction between S. picea and Azteca spp. (Adams et al. ition may indicate dispersal limitation in colonizing twig-nesting ant 2016). However, this study was conducted in a tropical rainforest queens, or a lack of source habitats or colonies nearby. where there are many more nesting resources in trees, lianas, or epi- Ant composition in tropical canopy ant communities often dif- phytes. In contrast, two species (P. gracilis and C. striatus) that more fers significantly by tree species (Yanoviak and Kaspari 2000, Dejean frequently nest in shade tree nests (Livingston et al. 2013) were more et al. 2008) but other studies attribute only a small fraction of varia- often found in more nests per tree on trees with Azteca. These ants tion in ant composition to differences associated with tree taxonomy may be nesting primarily in the crown, or may possibly benefit from (Klimes et al. 2012). Instead, other features or differences in individ- Azteca protection. If certain ants colonize early or by chance, they uals of different tree species such as crown or trunk size, presence of may gain access to resources or nest takeovers could be hindered by epiphytes, or number of available nests in canopies may account for a Azteca aggression towards the other species (Livingston and Philpott more of the variation observed (Klimes et al. 2012, Yusah and Foster

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2016). We did not document differences in overall ant community Núñez provided logistical support. We thank the Peters Foundation and Don composition based on habitat filtering related to tree species in which Walter Peters for allowing us to do research on their farm. Financial support nests were placed; however, we did see changes in composition with for this work came from DEB-0349388 to I. Perfecto and J. Vandermeer and tree height, which in our study also differed between two of the tree DEB-1262086 to S.M.P. species (T. micrantha were taller than I. micheliana). Nonetheless, the proportion of nests occupied by some individual species did vary Supplementary Data with tree species identity. Other canopy ant studies have found differences in species composition depending on tree size and tree con- Supplementary data are available at Environmental Entomology nectivity (Camarota et al. 2015), and have found strong separation online. in ant composition of ants visiting EFNs on Inga spp. and A. latifolia (Aguirre et al. 2013). Of course, there may not be an entire overlap References Cited between EFN-visiting ants and twig-nesting ants in these habitats, and despite differences with tree species, Camarota et al. (2015) did Adams, E. S. 1994. Territory defense by the ant Azteca trigona: maintenance not find differences in composition depending on presence of EFNs of an arboreal ant mosaic. Oecologia 97: 203–208. on tree species. We did, however, find differences in the proportion Adams, B. J., S. A. Schnitzer, and S. P. Yanoviak. 2016. 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