Ant taxonomic and functional diversity show differential response to plantation age in two contrasting biomes

Forest Ecology and Management 437 (2019) 304–313

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Ant taxonomic and functional diversity show differential response to plantation age in two contrasting biomes

T

⁎

Santiago Santoandréa, , Julieta Filloya, Gustavo A. Zuritab, M. Isabel Bellocqa a Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires – IEGEBA (CONICET-UBA), Ciudad Universitaria, Pab 2, Piso 4, BAC1428EHA, Argentina b Instituto de Biología Subtropical – Facultad de Ciencias Forestales, Universidad Nacional de Misiones – CONICET, Bertoni 85, Pto Iguazú, 3770, Misiones, Argentina

A R T I C LE I N FO

A B S T R A C T

Keywords: Assemblage formation Environmental filtering Plantation chronosequences Richness Tree monoculture

The increasing global demand for lumber and pulp has led to the conversion of natural habitats into monocultures of fast-growing tree plantations. The environmental filtering model proposes that both environmental characteristics of anthropogenic habitats and biotic interactions act as a filter that can be passed through by some species of the regional pool, driving the formation of local assemblages. Therefore, environmental filtering promotes the selective loss of species and convergence of functional traits, resulting in assemblages of species that are functionally more similar than expected by chance. In Argentina, pine monocultures have expanded in both subtropical forest and grassland biomes. Typically, environmental similarity between plantations and natural habitat decreases in the grassland and increases in the subtropical forest with increasing plantation age (time since pine stands were planted). Then, we predict that changes in biological diversity with plantation age will be opposite when plantations develop in environmentally contrasting biomes. To test the prediction, we studied taxonomic (species richness) and functional (based in morphological functional traits) diversity of epigeal ant assemblages in pine plantations of different ages (from 1 to 12 years old), developing in contrasting biomes that determined different contexts of the main natural (i.e., native) habitat: subtropical forest and grassland. Temperature, humidity and vegetation cover were recorded, and ants were collected using pitfall traps. For plantations and natural habitats of both biomes, we estimated functional diversity in sets of randomized communities and compared them with the observed functional diversity throughout plantation age. As expected, results showed opposite environmental similarity gradients between natural habitats and plantation ages. In the subtropical forest, ant species richness remained similar but functional diversity increased with increasing plantation age, associated with the presence of predatory ants. In the grassland, species richness showed a maximum at intermediate ages, but functional diversity remained similar with increasing plantation age. Null model analyses showed lower functional diversity than expected by chance in young plantations developing in the subtropical forest and at all ages in grassland, indicating convergence of functional traits. Our findings support environmental filtering as the primary mechanism driving the formation of ant assemblages along pine plantation cycle. To our best knowledge, this is the first study analysing patterns of diversity along tree plantation cycles developing in contrasting biomes. Our results show that the biome effect should be taken into consideration to predict diversity responses to commercial forestry and to unify a theory of assemblage formation in monoculture plantations.

1. Introduction The conversion of natural into anthropogenic habitat driven by land use due to human activities is a global threat to the conservation of biodiversity (Flynn et al., 2009; Cadotte et al., 2011; Newbold et al., 2015). Therefore, the consequences and processes involved in habitat

anthropization have become a focus of attention in ecological studies. The growing global demand for lumber and pulp has led to the conversion of native (referred to as “natural” from here on) habitats into monoculture of fast-growing plantations (Cossalter and Pye-Smith, 2003). Environmental changes and disturbances associated with the transformation of natural habitats into monoculture plantations often

⁎ Corresponding author at: Intendente Güiraldes 2160, Ciudad Universitaria, Pabellón II, 4° piso, laboratorio 55, BAC1428EHA Ciudad Autónoma de Buenos Aires, Argentina. E-mail address: [email protected] (S. Santoandré).

https://doi.org/10.1016/j.foreco.2019.01.021 Received 13 November 2018; Received in revised form 14 January 2019; Accepted 17 January 2019 0378-1127/ © 2019 Elsevier B.V. All rights reserved.

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preserve, at least partially, microclimate conditions and the original vegetation structure and composition are more frequently used by native animal species than those land uses that imply drastic changes (Filloy et al., 2010). For example, land use types resulting in multistratified habitats, such as tree plantations for lumber and pulp production, support a greater diversity of native bird species in forest than in grassland biomes, whereas land use types resulting in single-stratum habitats, such as cropfields, maintain a greater native diversity in the grassland biomes (Filloy et al., 2010). In Argentina, monocultures of fast-growing Pinus sp. and Eucalyptus sp. plantations have expanded in both the subtropical forest biome (Atlantic Forest ecoregion) and the grassland biome (Campos ecoregion), promoted by government incentives (AFOA, 2017). However, tree plantations may have different effects on local biological communities, because the gradual increase of canopy cover during plantation growth causes changes in environmental conditions. Those changes associated with plantation development create an environmental gradient that has contrasting characteristics in the subtropical forest and the grassland biomes. For example, in the grassland biome, young plantations are structurally more similar to grasslands than mature tree plantations; in contrast, in the subtropical forests mature plantations are structurally more similar to the native forest than young plantations. In our literature search, we found no previous study addressing patterns of biological community attributes and functional traits across the tree plantation cycle in monocultures growing in contrasting biomes implying different landscape context. Ants have been widely used as indicators in biodiversity studies (Hoffmann and Andersen, 2003; Claver et al., 2014; Cuautle et al., 2016), because they usually exhibit high local diversity (Hölldobler and Wilson, 1990), account for more than 30% of the animal biomass in tropical systems (Fittkau and Klinge, 1973), and are relatively easy to capture and identify. Moreover, previous studies showed that habitat disturbances and transformation may have effects on both richness and composition of ant assemblages, as well as on functional diversity (Fotso Kuate et al., 2015; Mumme et al., 2015; Liu et al., 2016). Those effects may be either direct, especially if ants nest in the soil, or indirect, if they affect vegetation structure, resource availability or interactions among species (Andersen, 1995; Maeto and Sato, 2004; Corley et al., 2006; Calcaterra et al., 2014). The aim of this study was to explore the patterns and causes of taxonomic and functional diversity of epigeal ants in pine plantations developing in environmentally contrasting biomes (where landscape contexts are subtropical forest and grassland). We ask whether changes in ant taxonomic and functional diversity as a response of plantation age (from 1 to 12 years old) and the similarity with the landscape context results in opposite patterns in grassland and subtropical forest biomes. We hypothesize that: (1) pine plantations have a negative effect on taxonomic richness of epigeal ants; (2) taxonomic and functional diversity of ant assemblages within plantations increase with increasing environmental similarity between the native habitat and pine plantations of different age; and (3) environmental filtering is the main mechanism involved in the formation of ant assemblages across pine plantation cycle and in both biomes, and their effect decrease with increasing environmental similarity between the native habitat and pine plantations of different age. Then, we predict that: (1) ant taxonomic richness will be lower in plantations than in natural environments in both biomes; (2) ant taxonomic richness and functional diversity will increase with increasing age of the plantation in the subtropical forest biome and decrease in the grassland biome, because environmental similarity between plantations and the natural environment throughout the forest cycle is different between biomes; and (3) functional diversity will be lower in plantation assemblages than in random assemblages generated from the regional species pool, and that difference will decrease with increasing age of the plantation in the subtropical forest and increase in the grassland biome.

have a negative impact on biological diversity; species loss and change in species composition were widely reported (Pacheco et al., 2009; Robson et al., 2009; Mentone et al., 2011; Suguituru et al., 2011; Pryke and Samways, 2012a; Phifer et al., 2016; Groc et al., 2017). Tree monocultures may also result in the loss of functional trait diversity within plantations (Liu et al., 2016). Martello et al. (2018) found that the functional diversity loss between rain forest and Eucalyptus monocultures was due to the loss of ant species with predatory characteristics, possible due to change in microclimatic conditions and the consequent reduction on the availability of small invertebrates. Functional traits are characteristics of individuals that can potentially affect the performance or fitness of the species, and determine when and where they can exist and interact with other species (McGill et al., 2006; Cadotte et al., 2011). For example, eye diameter in ants is a functional trait related to activity time, habitat use, and trophic position; predatory ants tend to have smaller eyes than omnivorous ants (Weiser and Kaspari, 2006; Gibb and Parr, 2013). Although the deficit of functional diversity is usually related to species loss, taxonomic and functional diversity are not always correlated (Dı́az and Cabido, 2001; Petchey et al., 2007), therefore, it is relevant to consider both facets of diversity. Highly disturbed environments, such as anthropogenic habitats, undergo changes in the mechanisms shaping biological assemblages (Temperton et al., 2004). An approach to the study of those mechanisms involves the analysis of the relationship between taxonomic and functional diversity (Petchey et al., 2007), i.e., the relationship between the number of species (taxonomic alpha diversity) and the size of the functional space determined by the value of species functional traits (functional alpha diversity). For example, the neutral theory of assemblage formation postulates that persistence and coexistence of species is independent of their functional traits, because all species are functionally equivalent (Hubbell, 2001). If a local species assemblage is composed of a random set of the regional pool, functional traits of the species that compose the assemblage will tend to be randomly distributed (Petchey et al., 2007). On the other hand, in relatively undisturbed environments, biotic interactions produce displacement of functional traits generating niche differentiation (Hardin, 1960; Grime, 1973; Mayfield et al., 2010). In those environments, assemblages are composed of species whose functional traits are different from those expected by chance (divergence of functional traits) (Petchey et al., 2007). In contrast, in highly disturbed environments such as anthropogenic habitat, environmental filtering is the primary driver of assemblage formation (Keddy and Weiher, 1999; Temperton et al., 2004), resulting in assemblages composed by species with similar functional traits (i.e. convergence of functional traits). The environmental filtering model proposes that both environmental characteristics and biotic interactions act as a filter that can be passed through by some species of the regional pool; those species have certain functional traits that allow them to survive in the new environments (Zobel, 1997; Mouchet et al., 2010). Therefore, environmental filtering results in the selective loss of species and convergence of functional traits, and in assemblages composed of species that are functionally more similar between them than expected by chance (Petchey et al., 2007). The response of biological communities to anthropogenic changes depends on the characteristics of the land use and the biome where human activities are developed. Climate (temperature and precipitation) imposes a large-scale environmental filtering in the evolutionary process of species pool formation given by the consistency between environmental conditions and the species ecological niches (Dı́az and Cabido, 2001). Thus, climate determines the biomes, which are characterized by (but not restricted to) a given vegetation type that strongly influences animal communities. A single anthropogenic land use causes changes in environmental filters, which will differ among biomes, and the effect of those changes on biodiversity will depend on the capacity of species of each regional pool to go through those filters (i.e. tolerate the new environmental conditions). Overall, the land use types that 305

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Fig. 1. Location of study pine plantations in the subtropical forest of the Atlantic Forest (light grey) and in the grasslands of the Campos ecoregion (dark grey). Photographs illustrate the primary native vegetation type in both biomes.

2. Methods

activities but native extensions still remain due to land protection or low exploitation pressure. Today, the subtropical forest mean temperature is 20 °C and average annual rainfall is 2 000 mm, with a cold season between June and August and no dry season (Oliveira-Filho et al., 2000; Plací and Di Bitetti, 2012). The native vegetation is a subtropical semideciduous forest, with a complex vegetation structure of four to five strata. It is characterized by a canopy dominated by 20 to 30 m tall trees and a lower stratum. Canopy is predominated by Fabaceae, Lauraceae, Myrtaceae and Meliaceae. The understory is characterized by ferns, or bamboos of the genera Guadua, Chusquea, and Merostachys. Many moss,

2.1. Study area The study was conducted in two biomes: the subtropical forest represented by the Southern Atlantic Forest (between 25° 41′ 20″S, 54° 20′ 13″W and 25° 51′ 8″S, 54° 35′ 31″W) and grasslands represented by the Campos (Campos y Malezales) (between 28° 57′ 45″S, 56° 42′ 54″W and 29° 35′ 53″S, 57° 11′ 33″W) regions in Argentina (Fig. 1), hereafter referred to as the subtropical forest biome and the grassland biome. The original climax vegetation in both biomes was deeply altered by human 306

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400 1 200 11 No thinning 6 No pruning 600 No change 4 No thinning 4 No pruning 1 000 1 200 0–2 0–2 0–2 0–2

Density after first thinning (ind/ha) Age at first thinning (years) Age at first pruning (years) Plantation density (ind/ha) Age at herbicide application (years)

Lumber Pulp

At each site, an automatic sensor of temperature and relative humidity was placed 10 cm above the ground level, which gathered data at 5-minute intervals for two weeks. In each biome, average temperature and humidity were calculated for each plantation age. Thermal variability was estimated as the standard deviation of temperature. Ants

Grassland Subtropical forest

2.3. Environmental similarity estimation

Age at formicide application (years)

To describe alpha diversity patterns throughout pine plantation age and compare those patterns between environmental contrasting biomes, we sampled epigeal ants in pine plantations of different ages and in natural habitats in a grassland and a subtropical forest biome. In each biome, we selected Pinus taeda stands of eight ages (1, 2, 3, 4, 5, 6, 9 and 12 years after planting) to represent the environmental gradient of the forest cycle. Three stands (replicates) separated by at least 500 m were selected per age class. In addition, three sites with natural vegetation (relatively low human impact) were selected in each biome. Thus, the entire study design consisted of 54 sites (27 in each biome). The study was designed to perform regression analysis, the power are determined by the number of experimental units, but not the number of replicates per treatments, as with ANOVA analysis (Cottingham et al., 2005). At each site, ants were sampled and environmental variables were measured at least 100 m from the stand edge to minimize edge effect.

Purpose

2.2. Study design

Biome

Table 1 Silvicultural characteristics of commercial pine plantations developing in the grassland and the subtropical forest biomes.

Age at second pruning (years)

Age at commercial thinning (years)

Density at harvesting (ind/ ha)

Age at harvesting (clearcut) (years)

lianas and epiphytes are also present (Cabrera and Willink, 1973). Most of the native forests have been exploited for lumber in the past mainly through selective cutting; as a consequence, they are currently primary and secondary forests at different succession stages (Plací and Di Bitetti, 2012). The biome shows a mosaic composed of large remnants of native forests in protected areas and fragments of native forest and tree plantations of variable sizes and shapes in private lands. Primary land use is tree plantations for pulp production (especially pine and eucalypt), followed by livestock pastures, annual crops, and yerba mate plantations (Zurita and Bellocq, 2010). In South America, grasslands developed extensively without supporting large herds of vertebrate herbivores (except during the Tertiary with great extinct mammals during the latest Pleistocene-earliest Holocene) until the Spanish colonization. The development of the grasslands was governed by the principal environmental factors (i.e. climate, soils and topography) (Burkart, 1975). The study grassland has temperate climate with no dry season; average annual temperature and precipitation are 19 °C and 1 200 mm, respectively. The native vegetation is primarily composed of grasses such as Andropogon, Axonopus, Bromus, Paspalum, Piptochaetium and Stipa (Burkart, 1975; Matteucci, 2012). Small dicots grow in between grasses and are favoured by cattle grazing (Paruelo et al., 2007). Shrubs (Baccharis and Eupatorium) are poorly represented, but may become locally dominant probably due to anthropogenic disturbances (Paruelo et al., 2007). The biome has a landscape matrix of natural grasslands with extensive low managed cattle ranching, crossed by ravines and patches of tree plantations. Provincial incentives to forestry industry during the last two decades have resulted in the expansion of commercial pine and eucalypt plantations for lumber production (Baldi and Paruelo, 2008; Matteucci, 2012). In both biomes, pine plantations of different ages are widely distributed over the landscape surrounded by natural or seminatural habitat (AFOA, 2017). Silvicultural management showed some differences between biomes because of different commercial purposes of plantations. In the subtropical forest, the main commercial purpose for Pinus plantations is wood pulp. Therefore, the plantations are not pruned or thinned. On the other hand, in the grassland, the principal commercial purpose is knot-free lumber and veneer. Thus, pine plantations are pruned and thinned throughout the cycle (Table 1).

18–20 11–13

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services of ecosystems; that is, they represent the effect on the ecosystem. However, some functional traits can be interpreted as effect or response (Dı́az and Cabido, 2001). For example, the presence of trait characteristics of predatory ants has an effect on the ecosystem functioning. But also, it could be thought that the abiotic and biotic conditions of the ecosystem allow to be inhabited by predatory ants with characteristic traits. We measured traits in up to three individuals per species whenever possible (Gibb et al., 2015) using only minor workers (Bihn et al., 2010), and estimated the mean value for each trait and species, when the number of collected specimens allowed it. We measured functional trait width to 0.01 mm with an ocular micrometre mounted on a Carl-Zeiss Discovery V8 stereo-microscope.

are typically thermophilic, it has been reported that variations in temperature or humidity produce change in species richness and functional diversity (Castro Delgado et al., 2008; Bharti and Sharma, 2009; Werenkraut et al., 2015; Kwon, 2016). At each site we established two 5 × 5 m plots (subsamples) to visually estimate percent cover for each growth form of herbaceous plants (grasses, dicots and ferns). The loss of vegetation cover has also been associated with the ant richness decrease and the change en functional diversity (Mentone et al., 2011; Gibb and Parr, 2013). To estimate average canopy cover, a digital photograph was taken by pointing vertically to the sky from a height of 1.5 m within each plot (Vespa et al., 2014). Images were analysed using software ImageJ to estimate percentage canopy cover (Schneider et al., 2012). The change in the canopy cover caused an alteration in sunlight incidence, resulting in local microclimatic changes (i.e. in temperature and humidity), this can affect the ants diversity (Werenkraut et al., 2015; Queiroz and Ribas, 2016). Finally, to perform statistical analysis, averages of all variables were calculated for each plantation age and natural habitat. This was necessary due to the limited availability of temperature and humidity sensors to cover all the sites simultaneously.

2.6. Data analysis The effect of pine plantations on richness of epigeal ant was analysed by comparing rarefied species richness between the natural environment and forest plantation. The calculation of rarefied richness with a confidence interval of 95% was performed with EstimateS (Colwell, 2013). This analysis allows comparison of richness among treatments using different sampling efforts, in this case, three sites in the natural environment and 24 sites in forest plantations per biome. A Principal Component Analysis (PCA) was performed for each biome separately using the environmental variables average to describe environmental changes throughout the forest cycle and natural habitats (Legendre and Legendre, 2012). Then, ant taxonomic richness was calculated as the number of observed species per site and functional diversity was estimated using the FDis index (Laliberte and Legendre, 2010). Only species presence data were used. To obtain the functional trait matrix, Generalized Linear Models (GLMs) were performed between Weber’s length and all functional traits to obtain residuals that were independent of body size using the stats package in R (Gibb et al., 2015). That was allowed to standardize all morphometric traits to capture internal proportionality of the different structures. Then, a species by species Gower distance matrix was calculated from scaled and centred trait data, as input for FDis analysis, together with the matrix of species per site. Finally, we compared taxonomic and functional diversity patterns between biomes by performing GLMs for each biome with diversity estimators as response variables and plantation age as independent variable. To explore whether environmental filtering is the main mechanism involved in assemblage formation within plantations, we compared observed functional diversity with that expected according to the null model of assemblage formation. To obtain the null distribution of species, 999 assemblage were randomly generated per site, using the list of species collected from each biome (regional species pool) and the randomizeMatrix function of the picante package in R (Bryant et al., 2008; Swenson, 2014; RCoreTeam, 2017). Each randomly generated assemblage maintained the same number of species observed per site.

2.4. Ant sampling and identification Pitfall traps are widely used to sample epigeal ants and obtain representative samples of the community (Agosti et al., 2000). We sampled ants using three pitfall traps (subsamples) at each site, separated 40 m from each other (2 biomes × (8 ages + native forest) × 3 replicates × 3 pitfall traps = 162 pitfall traps). Each trap consisted of a 1 l plastic container of 10 cm in diameter, partially filled with a solution of 30% propylene glycol in water, and buried flush with the ground surface. A plastic cover was placed above each trap to avoid flooding by rain. In both biomes, traps operated continuously from late spring to early summer (end of November to mid-January of the following year); they were checked twice during the sampling period and the captured arthropods were collected. Captured specimens were identified to species whenever possible (using taxonomic keys, see Appendix A) or to morphospecies based on relevant characters of the different genera (Palacio and Fernández, 2003), from here on refer to both as species. 2.5. Selection of functional traits The functional response of ant assemblages to the environment conditions was estimated from seven continuous morphometric traits related to metabolism, resource acquisition, trophic position and habitat use (Table 2). Dı́az and Cabido (2001) have proposed the distinction between functional traits of response and effect. The response traits are those related to fitness, and reflect environmental filtering and the action of natural selection under certain environmental conditions (Keddy and Weiher, 1999). Effect traits can affect the properties and

Table 2 Morphological traits, measurements that were taken to ants and hypothesised responses. Trait

Trait measurement and environmental response

Weber’s length

Length of alitrunk (Brown, 1953). Estimator of ant size related to metabolic activity, microclimatic characteristics (Kaspari, 1993) and habitat complexity (Gibb and Parr, 2013). Related to habitat complexity; femur length decreases with increasing habitat complexity (Gibb and Parr, 2013), as well as with locomotion speed and load balancing (Feener et al., 1988). Related to habitat use and trophic position; predatory ants have smaller eyes than omnivorous ants (Weiser and Kaspari, 2006); also related to time of activity. Calculated as the maximum width of head at the level of eyes minus the distance between eyes, in full face view; related to habitat type, ants with more dorsally positioned eyes are usually more common in simple and open habitats; also related to the trophic position, eyes of predatory ants are more laterally positioned (Gibb et al., 2015). Related to the sensory capacity of ants, for example, to follow chemical cues or to detect resources (Weiser and Kaspari, 2006). Related to the trophic position; a greater mandible length indicates a predation specialization; ants with short mandibles have generalist diets (Hölldobler and Wilson, 1990). Related to the consumption of sweet liquids (Fowler, 1991).

Femur length Maximum eye diameter Eye position

Scape length Mandible length Clypeus length

308

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(a)

Functional diversity expected by chance was estimated using the Functional Dispersion index (FDis) (Laliberte and Legendre, 2010) for each randomization. To analyse the relationship between the observed FDis and that expected by chance for each site, the standardized effect sizes of FDis (SES FDis) were calculated (Swenson, 2014; Liu et al., 2016; Cadotte and Tucker, 2017). The SES FDis values are a measure of the deviation of the observed values from those expected by chance; negative SES FDis values lower than expected by chance indicate an environmental filtering effect. To analyse the influence of the biome on the SES FDis patterns throughout the plantation age, we performed GLMs of SES FDis as response variable and plantation age as independent variable.

9

temperature grassland

canopy.cover

4

thermal.var herb.cover

3

rhumidity 0

3. Results

(b)

We identified a total of 12 435 ants collected during samplings in both biomes; they belonged to 7 subfamilies and 36 genera. In the subtropical forest biome, we collected 5 997 individuals from 29 genera and the total number of species was 58, whereas is the grassland we captured 6 438 individuals representing 20 genera and 46 species (Appendix B). The influence of tree plantations on ant richness was different between biomes. Rarefied taxonomic richness was significantly higher in the subtropical forest (36 ± 5 species, 95% CI) than in plantations (20 ± 5 species, 95% CI) (Fig. 2), in which half of the epigeal ants richness estimated in the natural forest was observed in the pine plantations; in contrast, ant richness was similar between the grassland (22 ± 5 species, 95% CI) and pine plantations (25 ± 5 species, 95% CI) (Fig. 2). The PCA showed different environmental patterns between biomes throughout plantation age. In plantations developing in the subtropical forest, the first PCA component (PC 1) explained 77.4% of the variance (Fig. 3 a), and was positively associated with temperature and thermal variability and negatively associated with percentage canopy cover and moisture. Herbaceous cover was mainly correlated to the second component (PC 2), which accounted for 12.8% of the variance in plantation age dispersion. In pine plantations from the grassland biome, PC 1 explained 81.3% of the environmental variation with plantation age (Fig. 3 b), and was negatively correlated with temperature, thermal variability and percentage of herbaceous cover, and positively correlated with percentage canopy cover. PC 2 explained 16.1% of the

canopy.cover

subtropical forest herb.cover

Fig. 3. Environmental description of pine plantation developed in the subtropical forest (a) and the grassland (b) biomes throughout pine plantation age. Ordination diagram of first and second components of the Principal Component Analysis; the percentage of variation explained by each axis is into brackets. Black dots indicate the plantation age in years and the grassland. Arrows represent the environmental variables, canopy.cover = canopy cover percentage, herb.cover = herbaceous cover percentage, temperature = average temperature, thermal.var = average thermal variability, rhumidity = relative humidity.

variation and was negatively associated with moisture. Although plantation ages were arranged as a relatively well defined gradient in the biplots for both biomes, two groups could be distinguished. One of the groups corresponded to young (one to three years old) plantations with low canopy cover and high temperature and thermal variability. The other group corresponded to mid-age and mature plantations (four to twelve ages), where opposite values were observed, as high canopy cover and low temperature and thermal variability. However, the degree of definition of the groups differed between biomes. The comparison of the PCAs showed that natural environments of each biome are located on opposite sides of the plantation age chronosequence. Grassland was associated with high temperature and thermal variability, low canopy cover and high herbaceous cover; these environmental characteristics were similar to those observed in young pine plantations. The subtropical forest was associated with low temperature and thermal variability, high canopy cover and high relative humidity, being environmentally similar to mature pine plantations. Taxonomic and functional diversity of ants throughout plantation age showed different patterns within and between biomes. In plantations from the subtropical forest, ant taxonomic richness showed no trend through the forest cycle (F2,20 = 3.30; p > 0.05) (Fig. 4) whereas in plantations that developed in the grassland biome, a maximum taxonomic richness was observed at intermediate ages (F2,21 = 147.90 ; p < 0.05) (Fig. 4). In plantations growing in the subtropical forest, ant functional diversity (FDis) increased across the forest cycle (F1,21 = 34.30; p < 0.01) (Fig. 5). However, in the grassland biome functional diversity show no clear pattern across the cycle

Rarefied species number

20

10

0 Plantation in subtropical forest

9 0

30

Plantation in grassland

3 temperature thermal.var

40

Grassland

4

rhumidity

Subtropical forest

Land use Fig. 2. Summary results of rarefied ant species richness in pine plantations and natural habitat in the grassland and the subtropical forest biomes. The asterisk indicates significant differences. 309

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SES FDis

12 8 4

Species richness

16

Subtropical forest Grassland

0

Subtropical forest Grassland

4 0

1

2

3

4

5

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7

8

9

10 11 12 13

6

8

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Stand age (Years)

Stand age (Years)

Fig. 6. Standardized effect size of FDis index (SES FDis) relative to pine plantation age in the subtropical forest and the grassland biomes. The dotted line indicates the expected value if assemblages follow the null model (SES = 0); values above and below the straight line indicate sites with greater trait divergence and convergence than expected by chance, respectively. The straight line indicates the GLM for both plantations in the subtropical forest biome.

0.20

Fig. 4. Taxonomic richness in relation to pine plantation age. The straight line indicates the GLM for plantations in the grassland biome.

4. Discussion

0.10

Pine plantations had a negative effect on richness of epigeal ants in the subtropical forest biome, but not in the grassland. The environmental gradient imposed by the plantation age resulted in different patterns of taxonomic richness and functional diversity of epigeal ants, depending on the biome. Our results suggested that environmental filtering proved to be the main mechanism involved in the formation of ant assemblages through pine plantation cycle in the grassland biome and in young plantations developing in the subtropical forest. As expected, pine plantations caused a loss of ant species compared to the richness observed in the native forest. That result is consistent with previous studies of ant richness in different monocultures growing in the tropical forest, such as in agroforestry systems of the Amazon forest (plantations of rubber trees, acacia trees, pine trees and cocoa trees) (Groc et al., 2017; Muñoz Gutiérrez et al., 2017), in rubber tree plantations in the tropical region of south-eastern China (Liu et al., 2016), and in rubber and oil palm tree plantations in Sumatra (Mumme et al., 2015). A relevant consequence of environment structure simplification in the tropics is the loss of ant diversity, because most of ant species have very specialized niches (Brühl et al., 2003). Typically, environmental simplification reduces microchabitat diversity (Soares et al., 1998) and species richness (Lopes et al., 2010; Groc et al., 2017). On the other hand, our results indicated similar ant richness in both pine plantations and grassland. In contrast, other studies conducted in forest plantations in grassland biomes reported the loss of different native species of arthropods (including ants) (Pryke and Samways, 2012b) and birds (Phifer et al., 2016). Our study grassland sites were under extensive livestock production (Matteucci, 2012); then, the similarity in ant richness between land uses might be due to the loss of species in the grassland caused by disturbances associated with grazing (Folgarait, 1998). However, some previous studies reported a lack of variation in ant richness between grazed and ungrazed sites (Schmidt et al., 2012), or inconsistent responses (Hoffmann, 2010). For example,

0.05

FDis

0.15

plantation cycle (Fig. 6).

0.00

Subtropical forest Grassland

0

1

2

3

4

5

6

7

8

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10 11 12 13

Stand age (Years) Fig. 5. Functional diversity (FDis index) in relation to pine plantation age. The straight line indicates the GLM for plantations in the subtropical forest biome.

(F1,22 = 1.14; p > 0.05) (Fig. 5). The diversity comparison with null models showed differents results between biomes. In plantations that developed in the subtropical forest, SES FDis increased with plantation age from negative values in the earliest stages of the forest cycle to positive values in mature plantations (F1,21 = 33.29; p < 0.05) (Fig. 6). Therefore, functional diversity changed from less to more than expected by chance through the pine plantation cycle. In plantations developed in the grassland, SES FDis did not show a trend through the plantation cycle (F1,22 = 0.26; p > 0.05). However functional diversity was lower than that expected by chance (SES FDis lower than zero) (T24 = −5.97 ; p < 0.05) across the 310

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because it was observed a lower functional diversity than expected. Nevertheless, opposite to expected, the effects of environmental filtering did not increase with increasing environmental contrast with the grassland through the plantation cycle. Therefore, pine plantations developing in the grassland could be generate environmental filter for ants, and the intensity of that filter does not vary despite environmental changes induced by the development of plantations. Overall, pine monocultures developing in the subtropical forest caused a greater loss of epigeal ants than those in the grassland. Considering that in tropical regions half of ant species are present in the canopy decreasing to 12% in temperate areas (Floren et al., 2014), the loss of species due to the replacement of native trees with pine monocultures might be much greater than that estimated in our study, in which half of the epigeal ants richness estimated in the natural forest was observed in the pine plantations. Our results support environmental filtering as the primary mechanism in the formation of ant assemblages across the plantation cycle in the grassland biome. In the subtropical forest, environmental filtering in young plantations and niche differentiation in mature plantations would structure ant assemblages through the plantation cycle. Our study showed that anthropogenic land uses such as commercial tree plantations may have different effects on ant taxonomic and functional diversity depending on the biome where the activity is developed. Our approach and findings may help to improve land use planning at the regional scale to enhance biodiversity conservation in productive systems.

it has been observed that livestock grazing in the shrubby steppe did not drive changes in ant richness, but it did produce variations in functional diversity possibly due to structural differences in vegetation that also affect microclimatic conditions (Claver et al., 2014). The pattern of ant taxonomic and functional diversity found throughout plantation age depended on the biome; however, responses of both facets of diversity were decoupled within both biomes. In the subtropical forest, we expected an increase in taxonomic and functional diversity throughout plantation age, a pattern reported recently for ant assemblages in a secondary succession tropical forest (Rocha-Ortega et al., 2018). Functional diversity, unlike taxonomic richness, increased with plantation age. These results suggest a turnover of species with novel functional traits, that may produce an increase in the functional space in mature forest plantations. For example, the establishment of species with traits associated with being predator specialists (small eyes positioned on the side of the head or absents, and larger mandibles) was observed in different regions and continents (Weiser and Kaspari, 2006; Bishop et al., 2015; Gibb et al., 2015), such as in Odontomachus chelifer, or Labidus coecus; or large size associated with being able to capture larger prey (Traniello, 1987), i.e. Dinoponera australis and Pachycondyla striata. In the grassland, the highest richness was recorded in plantations of intermediate ages. The decrease of taxonomic richness towards both extremes of the plantation cycle might be due to different factors. We expected higher species richness in young plantations due to the low environmental contrast with the grassland. However, the low taxonomic richness observed in young plantations was possibly due to disturbances produced by site preparation, such as soil mechanical removal and application of herbicides and insecticides (Haeussler et al., 2002) that may cause the local loss of ant species. The time required for recolonization will depend on stochastic processes related to the dispersal capacity of the different species (Keddy and Weiher, 1999). Towards the end of the plantation cycle, a smaller number of ant species was observed probably because they are unable to tolerate the new environmental conditions generated by reduced environmental similarity between mature plantations and the grassland, such as the reduction in temperature and herb plant cover, or the accumulation of pine needles on the soil (Peichl and Arain, 2006). Those changes in soil cover and their characteristics might cause an increase in the effect of environmental filtering on ant assemblages. These soil characteristics might act directly by hindering ant movement on the substrate, or indirectly by limiting resource availability, such as the growth of herbs. However, in contrast to our predictions, no decrease on functional diversity was observed across the forest cycle. Other possible explanation of the greater species richness at intermediate ages is that the environmental conditions allow the coexistence of open habitat and forest species (Osorio-Perez et al., 2007). Possible effects of environmental filtering were observed on forest plantations in both biomes, but the pattern and intensity of those effects throughout the plantation age varied between biomes. In the subtropical forest biome, our study suggested that the main mechanism involved in ant assemblage formation changed throughout pine plantation cycle. A lower functional diversity than expected by chance was observed only in young plantations, indicating that environmental filtering would be the primary mechanism in assemblage formation. However, the opposite situation was observed in mature plantations, where a higher functional diversity than expected was found, suggesting that niche differentiation would prevail over environmental filtering as a mechanism structuring ant assemblage. In tropical forests, the rise in ant functional diversity with plantation age could be due to increased interspecific competition (Rocha-Ortega et al., 2018). In a recent study, Groc et al. (2017) found that the functional diversity of litter-dwelling ants in 40-year-old pine plantation was similar to the surrounding Amazonian forest. On the other hand, our results indicate that environmental filtering is the main mechanism structuring ant assemblage within pine plantations developing in the grassland biome,

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