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Edge effects on epigeic ant assemblages in a grassland–forest mosaic in southern Brazil
Acta Oecologica 36 (2010) 365e371
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Original article
Edge effects on epigeic ant assemblages in a grasslandeforest mosaic in southern Brazil Esther R.S. Pinheiro*, Leandro da S. Duarte, Elena Diehl, Sandra M. Hartz Departamento de Ecologia, Universidade Federal do Rio Grande do Sul, A. Bento Gonçalves 9500, CP 15007, Porto Alegre RS 91501-970, Brazil
a r t i c l e i n f o
a b s t r a c t
Article history: Received 6 August 2009 Accepted 9 March 2010 Published online 1 April 2010
This study analyzed the influence of vegetation structure variation along a natural vegetation mosaic formed by Araucaria forest and Campos grassland in the southern Brazilian highlands, on the species richness and composition of epigeic ants. The study site consisted of two different grasslandeforest ecotones, where 76 pitfall traps were installed. We estimated the area covered by canopy vegetation by hemispherical photographs, and the structure of the understory vegetation by counting the number of vegetation touches, using a graduated stick. We collected 31 species or morphospecies of epigeic ants belonging to 17 genera and 6 subfamilies. Cluster analysis defined three habitat groups (grassland, edge, and forest) with different ant species composition as revealed by ordination analysis. The highest richness was observed at the forest edge, and decreased towards the grassland and the forest interior. Variation in the richness and composition of epigeic ant species was significantly explained by the factor of distance from the forest. The relationship between species richness and understory density was negative. On the other hand, species composition of epigeic ant assemblages was significantly explained by canopy cover. This finding indicates that the ecological responses of ant assemblages resulted predominantly from edge effects mediated by changes in vegetation structure. Ó 2010 Elsevier Masson SAS. All rights reserved.
Keywords: Habitat structure Ecotones Species diversity Araucaria forest Campos grasslands
1. Introduction Edge effects result from the interplay between two spatially contiguous ecosystems (Murcia, 1995). Edges usually exhibit features of both contiguous ecosystems, merged with particular microhabitat conditions generated by the contact between distinct environments (Risser, 1995). Edges often show increased biodiversity levels and complexity of vegetation structure (Murcia, 1995; Risser, 1995), which influences both vertebrate (Stevens and Husband, 1998) and invertebrate assemblage patterns (Majer et al., 1997). Insect assemblages are very important components of biodiversity, because they accumulate considerable biomass and show high species richness. Furthermore, insects play central roles in ecosystem functioning (Erwin, 1991; Folgarait, 1998). For these reasons, insects are valuable ecological indicators of edge effects in natural mosaic landscapes. Among insects, ants can be considered as terrestrial ecosystem engineers, because they are capable of modifying habitats and regulating resource distribution to other organisms (Jones et al., 1994). Many studies have used ants as
* Corresponding author. E-mail address: [email protected] (E.R.S. Pinheiro). 1146-609X/$ e see front matter Ó 2010 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2010.03.004
bioindicators of ecological processes (Culver and Beattie, 1983; Majer, 1983; Andersen and Sparling, 1997) in some cases, ant functional groups have been identified (Andersen, 1995; King et al., 1998; Hoffmann and Andersen, 2003; Stephens and Wagner, 2006), making possible comparisons among ant communities across biogeographical zones (Hoffmann and Andersen, 2003). Edges influence ant assemblage patterns, because variation in vegetation structure creates environmental gradients that affect ant activities such as nesting and foraging (Basu, 1997). For this reason, habitats with different degrees of complexity tend to show ant assemblages with distinct species compositions (Lassau and Hochuli, 2004). Nonetheless, Andersen (2008) has argued that habitat characteristics may not explain all the variation in richness and composition in ant assemblages. Other factors such as dispersal limitation could also be involved in the formation of ant assemblages across landscapes. Thus, analyses of speciesehabitat relationships should take into account between-site variation in species distribution, to avoid confounding effects of habitat on ant assemblages with spatial dispersal limitation. Although forests with Araucaria angustifolia (Araucariaceae) constitute the main forest type on the highland plateau in southern Brazil at altitudes above 500 m a.s.l. (Duarte and Dillenburg, 2000), data about the ant fauna of Brazilian Araucaria forests are scarce (but see Ketterl et al., 2003; Silva and Silvestre, 2004; Diehl et al., 2005).
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Araucaria forests in southern Brazil often form mosaics with Campos, which is a native grassland vegetation (Rambo, 1994; Duarte et al., 2002). Our main goal in this study was to analyze the influence of edge effects on species richness and composition of epigeic ant assemblages occurring in a natural vegetation mosaic formed by Araucaria forest and Campos grassland in southern Brazilian highlands. Then, we discuss the suitability of ants for the conservation of ecological processes in forestegrassland mosaics. 2. Materials and methods 2.1. Study site The study was conducted at 29 280 S and 50130 W, in the PróMata Research and Nature Conservation Center (CPCN Pró-Mata). The Center covers an area of 4500 ha and is located in São Francisco de Paula, state of Rio Grande do Sul, southern Brazil. The regional climate is classified according to Köppen’s system as Cfb (Moreno, 1961), which is subtropical (C) and rainy, with precipitation uniformly distributed throughout the year (f), and warm summers (b). The annual mean temperature is ca. 15.1 C (Hijmans et al., 2005), with freezing temperatures occurring from April to November (Backes, 1999). The annual mean rainfall is 2086 mm, equally distributed throughout the year (Hijmans et al., 2005). The study site consisted of ca. 78 ha Campos grassland surrounded by Araucaria forest, situated on a plateau at about 900 m a.s.l. Araucaria forest communities are characterized by the presence of woody species that are phytogeographically related to Austral-Antarctic and Andean floras (Rambo, 1951; Waechter, 2002). The most physiognomically important tree species is A. angustifolia. Some other typical species in these forests are Podocarpus lambertii, Drimys brasiliensis, Dicksonia sellowiana, and several species of Myrtaceae, Melastomataceae, and Lauraceae. Oliveira-Filho and Fontes (2000) recognized the Brazilian Araucaria forest as a particular type of Atlantic Forest. In the grassland, small forest nuclei, regionally called capões, are found, in different degrees of development (Duarte et al., 2006). Cattle grazing and burning practices were terminated in 1993, allowing increasing regeneration of the forest and more biomass accumulation and woody-plant establishment in the grassland (Oliveira and Pillar, 2004). These conditions generated a tall dense grassland matrix composed of caespitose grasses (Andropogon lateralis, up to 0.8 m high) and shrubs (Baccharis uncinella, Calea phyllolepis), which tend to suppress short grasses and other herbaceous species (Oliveira and Pillar, 2004).
identified by comparison with the specimens of Formicidae in the collection of the Laboratório de Insetos Sociais, UNISINOS, where all the collected specimens were deposited. 2.2.2. Ant attributes For each identified species, its foraging habit (carnivorous, granivorous, nectarivorous, omnivorous) and nesting site (epiphytes, hollow wood, litter, plant cavities, rocks, soil, trees) was categorized as nominal variables, according to information available in specialized literature (Takahashi-Del-Bianco et al., 1998; Holway et al., 2002; Rossi and Fowler, 2002; Kaufmann et al., 2003; Passos and Oliveira, 2003; Ramos et al., 2003; Schilman and Roces, 2003; Milesi and Casenave, 2004; Battirola et al., 2005; Harada, 2005; Longino, 2006; Marchioretto and Diehl, 2006; Weiser and Kaspari, 2006; Delabie et al., 2007; Longino and Fernández, 2007; Milks et al., 2007; Vieira et al., 2007; Brandt et al., 2009; Silva-Melo and Giannotti, 2010). For morphospecies we used available information encompassing the whole genus. 2.2.3. Habitat variables We evaluated the canopy vegetation cover by means of hemispherical photographs of the canopy (Frazer et al., 2001). Photographs were taken just above the soil traps, at ca. 1.5 m from the soil surface. The images were analyzed by using the software Gap Light Analyzer 2.0 (Frazer et al., 1999), and the proportion of sky area covered by vegetation (0e1) was obtained. At each sampling point, the structure of the understory vegetation was characterized by counting the number of vegetation touches at each 10-cm interval from the ground up to 1.5 m above the sampling trap, using a graduated stick (Bibby et al., 1992; Baldissera et al., 2008). By doing so, we estimated the density of the understory vegetation as the total number of vegetation touches along the stick (number of touches m1). Additionally, we calculated an index of understory homogeneity. For this, we generated a matrix describing the number of vegetation touches in each 10 cm interval (variables) at each sampling point. Whenever we found more than 10 vegetation touches per 10 cm interval, these were grouped in the same class. Thus, our data matrix contained ten variables (from 0 to 10 or more touches). We then computed a Shannon diversity index for each sampling point, which was taken as an index of understory height homogeneity. High Shannon index values indicated more vertically heterogeneous understories, while low values indicated more concentrated understories.
2.2. Sampling methods
2.3. Data analyses
2.2.1. Ant assemblages Sampling was carried out in January 2006, in two different grasslandeforest ecotone sites. In each site (at least 500 m distant from each other), two parallel, 180 m long transects were delimited, 20 m distant from each other. Transects were centralized in relation to the outermost forest tree/shrub with diameter at breast height >10 cm and whose crown was touching the continuous forest canopy. This point was assumed to represent the limit between grassland and forest (zero distance point). Nine sampling points were established at 10 m distance intervals starting from the edge, both in the direction of the grassland (negative distances), and in the direction of the forest (positive distances). Along each transect, one soil trap (300 mL) containing 70% ethanol mixed with detergent was installed at each sampling point (10 m distant from each other), totaling 76 sampling units. After 48 h of exposure, soil traps were collected (adapted from Agosti and Alonso, 2000). The collected material was identified at the genus level according to Palacio and Fernández (2003). All species and morphospecies were
We used ANOVA with permutation tests (Pillar and Orlóci, 1996) to evaluate the effects of the factors ‘site’ and ‘distance from forest edge’, as well as the interaction between these two factors, on the number of ant species found in each soil trap. Prior to the analysis, we performed a logarithmic transformation on the number of ant species. To control for spatial autocorrelation within transects, permutations among sampling units were nested within transects; after nesting, transects were permuted between sites as bundles (see Pillar, 2006). We used MANOVA with permutation tests (Pillar and Orlóci, 1996) to evaluate the effects of the factors ‘site’ and ‘distance from forest edge’, as well as the interaction between those two factors, on the composition of epigeic ant assemblages found in each soil trap, described as a presence/absence data matrix. Prior to the analysis, variables (ant species) were centralized to control for species commonness/rarity in the sample, and sampling units (traps) were normalized (Legendre and Legendre, 1998). For MANOVA we used the same permutation design as in the previous ANOVA. In both analyses, Euclidean distances were used as the
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dissimilarity index, and the sum of squares between groups (Qb statistics) was used as the test criterion. We used polynomial regression to analyze the association between the richness of epigeic ant species (dependent variable) and the distance from the forest edge (independent variable) (Sokal and Rohlf, 1981). To evaluate the association between the species composition of epigeic ants (dependent variable) and the distance from the forest edge (independent variable), we calculated the frequency of each taxon at each distance interval as the number of soil traps where the taxon was recorded (1e4) divided by the total number of soil traps per distance interval (4). From the matrix C containing each distance interval (sampling units) described by the frequency of ant taxa (variables), we computed a Euclidean distance matrix and performed a UPGMA cluster analysis. The number of sharp groups obtained was evaluated by bootstrapped auto-resampling (Pillar, 1999). Furthermore, we carried out a Principal Coordinates Analysis (PCoA) of sampling units in order to detect the principal axes of variation of habitat clusters obtained through UPGMA (sampling units) in relation to ant species (variables), based on Euclidean distances between sampling units (Legendre and Legendre, 1998). We explored the relationship between different habitat types and ant attributes (foraging habit and nesting site) through PCoA ordination, based on a chord distance matrix between sampling units. For this, we first expanded nominal attributes into dummy variables (Legendre and Legendre, 1998); accordingly, for a given
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attribute containing n states, n 1 binary variables were generated. This so-generated attribute matrix T contained ant taxa (sampling units) described by foraging and nesting binary attributes (variables). By matrix multiplication, T C generated a matrix CT containing each distance interval (sampling units) described by the frequency of ant attributes (variables). As distinct distance intervals showed highly variable numbers of ant species, the occurrence of particular foraging/nesting strategies were obviously dependent on how many species were present in each distance interval. For this reason, we standardized the frequency of occurrence of each attribute at each distance interval by the respective number of ant occurrences at the respective distance interval. This standardized matrix was then submitted to a PCoA ordination. We used a forward stepwise multiple regression to evaluate the association between the richness of epigeic ant species (dependent variable) and the three habitat variables (independent variables). To evaluate the association between the species composition of epigeic ants (dependent variable) and the three habitat variables (independent variables), we performed a stepwise canonical correspondence analysis (CCA, Ter Braak and Smilauer, 2002). P values for stepwise CCA were obtained through randomization of residuals, using a full model approach (see Legendre and Legendre, 1998). Regression analyses were carried out using the software STATISTICA 7 (StatSoft Inc., 2004). Analyses of variance, UPGMA, and PCoA were performed using the MULTIV 2.63 (Pillar, 2006)
Table 1 Assemblages of epigeic ants collected using soil traps distributed along a grasslandeforest gradient in southern Brazil. Species or morphospecies
Code
Foraging habit
Nest site
Mean frequency SEa
ECITONINAE Labidus coecus Latreille 1802
Laco
Carnivore
Soil
0.013 0.029
DOLICHODERINAE Linepithema sp.
Lisp
Nectarivore/omnivore
Soil
0.105 0.087
FORMICINAE Brachymyrmex heeri Forel 1874 Brachymyrmex sp. Camponotus sp. 1 Camponotus sp. 2 Camponotus rufipes Fabricius 1775 Myrmelachista sp. 1 Myrmelachista sp. 2 Paratrechina sp. 1 Paratrechina sp. 2
Brhe Brsp Cas1 Cas2 Caru Mys1 Mys2 Pas1 Pas2
Omnivore Omnivore Omnivore Omnivore Nectarivore Unknown Unknown Nectarivore Nectarivore
Under rocks/plant cavities Plant cavities/under epiphytes/litter Hollow wood Hollow wood Hollow wood Hollow wood/plant cavities Hollow wood/plant cavities Soil/under rocks/hollow wood Soil/under rocks/hollow wood
0.013 0.013 0.013 0.013 0.421 0.013 0.039 0.092 0.026
0.029 0.029 0.029 0.029 0.094 0.029 0.047 0.085 0.039
MYRMICINAE Crematogaster sp. Crematogaster quadriformis Roger 1863 Pheidole sp. 1 Pheidole sp. 2 Pheidole sp. 3 Pheidole sp. 4 Pheidole sp. 5 Pheidole fallax Mayr 1870 Solenopsis sp. 1 Solenopsis sp. 2 Solenopsis invicta Buren 1972 Strumigenys sp. Wasmannia sp.
Crsp Crqu Phs1 Phs2 Phs3 Phs4 Phs5 Phfa Sos1 Sos2 Soin Stsp Wasp
Omnivore Omnivore/nectarivore/seed Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore/seed Carnivore Omnivore/Carnivore
Arboreal/hollow wood/plant cavities Arboreal/hollow wood/plant cavities Soil Soil Soil Soil Soil Soil Soil Soil Soil Soil Hollow wood/litter/under rocks
0.092 0.013 0.013 0.355 0.092 0.026 0.013 0.092 0.171 0.026 0.105 0.053 0.132
0.085 0.029 0.029 0.105 0.085 0.039 0.029 0.085 0.118 0.057 0.076 0.052 0.087
PONERINAE Anochetus sp. Ectatomma sp. Hypoponera sp. Hypoponera trigona Mayr 1887 Pachycondyla striata Smith 1858
Ansp Ecsp Hisp Hytr Past
Carnivore Omnivore/Carnivore Carnivore Carnivore Omnivore/Carnivore/seed
Hollow wood/under epiphytes Soil Soil/hollow wood/under rocks Soil/hollow wood/under rocks Soil
0.066 0.053 0.092 0.026 0.447
0.057 0.052 0.085 0.039 0.164
PSEUDOMYRMECINAE Pseudomyrmex sp. Pseudomyrmex acanthobius Emery 1896
Pssp Psac
Omnivore Omnivore
Hollow wood Hollow wood
0.013 0.029 0.013 0.029
a
SE ¼ standard error.
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statistical software. CCA was performed using the software CANOCO 4.5 (Ter Braak and Smilauer, 2002).
3. Results We collected 31 species or morphospecies of epigeic ants belonging to 17 genera and 6 subfamilies (Table 1). Species showing the highest frequencies were Pachycondyla striata Smith 1858, Camponotus rufipes Fabricius 1775, Pheidole sp. 2, Solenopsis sp. 1, Wasmannia sp., Solenopsis invicta Buren 1972, and Linepithema sp. (Table 1). The variation in the richness of epigeic ant species was significantly explained by the factor ‘distance to forest edge’ (Table 2), while the factors ‘site’ or interaction between site and distance from forest edge had no significant effects on either species richness or composition. A third-order polynomial was the best regression model explaining the variation of species richness along the grasslandeforest ecotone (Fig. 1). The highest richness was observed at the forest edge, decreasing towards the grassland and the forest interior. UPGMA classification of the frequency of epigeic ants along the grasslandeforest ecotone indicated three sharp groups of sampling units (Fig. 2), representing the grassland, the forest, and the edge between the two landscape matrices, starting in the grassland, at 10 m from the limit between grassland and forest, and extending to 20 m in the forest interior. PCoA ordination showed the association between the UPGMA groups and taxa of epigeic ants (Fig. 3a). Pseudomyrmex acanthobius Emery 1896, Brachymyrmex sp., Myrmelachista sp. 2, Solenopsis sp. 2, and Strumigenys sp. were associated with grassland. Labidus coecus Latreille 1802, Camponotus sp. 2, Crematogaster sp., Myrmelachista sp. 1, Pheidole sp. 1, Pheidole sp. 5, Solenopsis sp. 1, and Wasmannia sp. were related to the forest interior. Brachymyrmex heeri Forel 1874, Crematogaster quadriformis Roger 1863, Pheidole fallax Mayr 1870, Camponotus sp. 1, Linepithema sp., and Pseudomyrmex sp. were the ant taxa associated with the edge habitat. Other ant taxa did not show any specific association with habitat groups. PCoA ordination detected association between different habitat types and ant attributes related to foraging habit and nesting sites (Fig. 3b). Nectarivorous ants were associated with grassland sites, while carnivorous, granivorous and omnivorous species were related to forested sites. Edge habitats did not show any close relationship with specific foraging habits. Furthermore, use of hollow wood as nesting sites was related to open areas, while nesting in soil, litter or under rocks was related to forest sites. Nesting inside plant cavities, on epiphytes or trees was associated with edge habitats.
Fig. 1. Third-order polynomial regression of species richness in epigeic ants in a grasslandeforest mosaic on the distance from forest edge. R2 ¼ 0.33, F3,72 ¼ 11.63, P < 0.001. Probabilities of variables showing normal distribution were obtained through KolmogoroveSmirnov normality testing (P ¼ 0.29). Probabilities of variables showing constant variance were obtained through Spearman correlation tests between the absolute values of the residuals and the observed value of the dependent variable (P ¼ 0.84).
The variation patterns of habitat variables along the grasslandeforest gradient are shown in Fig. 4. A steep increase in canopy vegetation cover was observed, starting at 20 m (from grassland to forest) until 10 m inside the forest (Fig. 4a). Understory vegetation cover decreased from grassland to forest (Fig. 4b). Grassland tended to show a higher variability in relation to understory vegetation density than did forest. Also, the transition zone between grassland and forest was less abrupt in relation to understory density than that observed for canopy vegetation cover. In contrast, forest locations had higher and more variable understory homogeneity indices than did grassland locations (Fig. 4c). The stepwise regression of species richness on habitat variables (canopy cover, understory density, and understory homogeneity) showed that the best fit was attained when only understory vegetation density was included as the independent variable (Table 3). The relationship between species richness and understory density was negative; that is, denser understories tended to show lower species richness.
Table 2 Analyses of variance of species richness and composition of epigeic ants in a grasslandeforest mosaic in southern Brazil. Source of variation
Richnessa Compositionb
Sum of squared distances (Q) Site (S)
Distance to edge (D)
SD
Residual
Total
0.394 ns 3.717 ns
2.008** 19.759*
0.642 ns 15.642 ns
3.044 36.123
4.313 75.241
**P 0.001; *P 0.03; ns P > 0.3. P values obtained through random permutations (10 000 iterations). a ANOVA on the log-transformed number of ant species by sampling unit. b MANOVA on presence/absence of ant species in each sampling unit. Data were submitted to centralization within variables and normalization within sampling units (Legendre and Legendre, 1998).
Fig. 2. UPGMA classification of sampling points described by assemblages of epigeic ants and distributed along a grasslandeforest gradient in southern Brazil. Bootstrap auto-resampling indicated three sharp groups of sampling units, representing open field, edge, and forest habitats (1000 iterations).
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Fig. 4. Mean abiotic characteristics of sampling points along a grasslandeforest gradient in southern Brazil. a) Mean canopy cover (%) estimated through hemispherical photographs taken at approximately 1.5 m above the ground. b) Mean understory density estimated as the number of vegetation touches m1. c) Mean understory homogeneity index, obtained through the computation of Shannon diversity index using the number of vegetation touches as variables. The higher the index, the more homogeneous is the understory vegetation. Bars crossing the means (black squares) are standard errors.
4. Discussion
Fig. 3. PCoA ordination of sampling units classified into three habitat types (grassland, edge, and forest) described by a) taxa of epigeic ants and b) foraging habit and nesting sites of ants in a grasslandeforest mosaic in southern Brazil. See species coding in Table 1.
On the other hand, stepwise CCA showed that the species composition of epigeic ant assemblages was significantly explained by canopy cover (Table 4), although predictor variables explained only a minor proportion of the variation in ant species composition.
The species richness and composition of epigeic ants varied significantly along the grasslandeforest gradient, indicating that variation in vegetation structure influenced distribution patterns of ant assemblages (Basu, 1997; Lassau and Hochuli, 2004; Ribas et al., 2003; Vasconcelos et al., 2008). Furthermore, ant species richness and composition varied only in relation to the distance from the forest edge, independently of the site factor. This finding indicates that ecological responses of ant assemblages resulted exclusively from edge effects mediated by changes in vegetation structure
Table 3 Stepwise linear regression of species richness of epigeic ants in a grasslandeforest mosaic in southern Brazil on microhabitat characteristics. Independent variable added at each step b
Understory density Understory homogeneity index Canopy cover a
Cumul. R2a
df
F to enter/remove
P
Normality (P)c
Constant variance (P)c
0.22 0.24 0.25
1.74 2.73 3.72
20.49 2.13 0.72
<0.01 0.15 0.40
0.43 0.29 0.22
0.55 0.49 0.71
Cumulative R2 as independent variables were added to the model. Regression equation: y ¼ 0.71 0.21x þ 3. c Probabilities of variables showing normal distribution were obtained through the KolmogoroveSmirnov normality testing. Probabilities of variables showing constant variance were obtained through Spearman correlation tests between the absolute values of the residuals and the observed value of the dependent variable. b
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Table 4 Stepwise canonical correspondence analysis of species composition of epigeic ant assemblages on habitat variables. Pseudo-F Pb Independent variable added Sum of all Proportion of at each modeling step eigenvalues total explained variationa Canopy cover Understory homogeneity index Understory density
0.35 0.53
0.035 0.053
2.53 1.26
0.0001 0.1772
0.69
0.069
1.12
0.3131
a
The sum of all eigenvalues of the correspondence analysis of species composition ¼ 10.012. b P values generated through randomization (9999 iterations).
along transects (canopy cover and understory vegetation density). Although dispersal limitation in ant assemblages can determine in some extent species composition in different sites (Andersen, 2008), our results suggested that habitat characteristics were much more important to predict species composition than dispersal limitation. Ordination analysis revealed distinct ant species compositions for the three habitat groups defined by cluster analysis (grassland, edge, and forest). Habitat separation is likely to have occurred as a consequence of the influence of the variation in vegetation structure on the environmental conditions and resource availability for ants. Interestingly, species richness and composition along the grasslandeforest gradient responded to different vegetation structure factors. Species richness was negatively associated with understory vegetation density, a finding that could be explained by the more energetically efficient ant movement in less-complex habitats, especially in terms of resource acquisition, chemical trail establishment, and nesting activities (Lassau and Hochuli, 2004). In contrast, the variation in species composition along the gradient was significantly explained by canopy cover, although the amount of variation explained was very low. A possible explanatory mechanism underlying the variation in the composition of epigeic ant assemblages along the grasslandeforest ecotone might involve the variability in habitat range of some species in relation to others. Because the variation in vegetation structure affects ant abundance, less-competitive ant species are prevented from sharing the habitat space with more-competitive species, which is likely to exert a significant effect on the composition of epigeic ant assemblages (Perfecto and Vandermeer, 1996; Punttila et al., 1996). For instance, the influence of canopy cover on ant species composition might occur as a consequence of variation in light incidence, soil humidity, and temperature across habitats (Ríos-Casanova et al., 2006); these environmental fluctuations are likely to benefit some ant groups to the detriment of others, because species sharing ecological similarities (functional groups) probably occur in environmentally similar habitats (Vasconcelos et al., 2008). For instance, Holec et al. (2006) have found association between nesting strategy and habitat type. In our study, we observed that ants occurring in open areas tend to build their nests within hollow wood. This association could be explained by the frequent occurrence of B. uncinella shrubs in open areas near forest edges (Oliveira and Pillar, 2004). As those woody shrubs die, they offer good nesting sites for ants living in grassland. Along the grasslandeforest mosaic where the study was performed, accelerated vegetation dynamic is currently observed, in which Araucaria forest is expanding over Campos grassland (Oliveira and Pillar, 2004). In this process, plant species characteristic of forest edges begin the forest expansion over grassland. Although available evidence suggests that birds are the major seed transporters from the forest at the study site (Duarte et al., 2007), some pioneer plants may benefit from associations with seeddisperser ants. Seed dispersal by ants is a very frequent process in
nature. For instance, Pizo (2008) showed the importance of Pheidole praeses as a seed disperser of small-seeded plants in a tropical rainforest site. Seeds can be removed from the neighborhood of the parent plant and dispersed by a myriad of very generalist ant species, with very low interaction specificity (Berg, 1975). In our study, species such as C. quadriformis and P. fallax, which show very generalist dietary habits (Battirola et al., 2005; Ramos et al., 2003) and occur in Araucaria forest edges, might be promoting the dispersal of forest-plant seeds over grassland. Nonetheless, our results seem to suggest that some forest development is necessary for ants to act as effective promoters of seed dispersal in our study area, as we did not find any close association between foraging habit and edge habitat; indeed, granivorous and omnivorous ants were more associated with forested sites than with edges. Conservation of Araucaria foresteCampos grassland mosaics relies crucially on the maintenance of edge dynamics. Furthermore, organisms inhabiting edges play major ecological roles in the maintenance of the ecosystem as a whole, and knowledge about different ecological agents depends, obviously, on their accurate taxonomic identification. Unfortunately, knowledge about ant species remains sparse in the ecosystem evaluated in this study. In this paper we confirmed the existence of edge effects on ant assemblages occurring in forestegrassland mosaics. A more complete portrait of the contribution of ants the conservation of vegetation mosaics should arise as a deeper understanding of their functional roles in forestegrassland dynamics can be achieved. Acknowledgements The authors thank Marcelo Saraiva for field assistance, and Aline Centa, Aline Moraes, and Camila Santos for laboratory assistance. This study had logistical support from CPCN Pró-Mata PUCRS, and was funded by an undergraduate fellowship from PIBIC-CNPq to Esther Pinheiro, and grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) to Sandra M. Hartz (304036/2007-2). References Agosti, D., Alonso, L.E., 2000. The ALL protocol: a standard protocol for the collection of ground-dwelling ants. In: Agosti, D., Majer, J.D., Alonso, L.E., Schultz, T.R. (Eds.), Ants: Standard Methods for Measuring and Monitoring Biodiversity. Smithsonian Institution Press, Washington, pp. 204e206. Andersen, A.N., 1995. Measuring more of biodiversity: genus richness as a surrogate for species richness in Australian ant fauna. Biol. Conserv. 73, 39e43. Andersen, A.N., 2008. Not enough niches: non-equilibrial processes promoting species coexistence in diverse ant communities. Aust. Ecol. 33, 211e220. Andersen, A.N., Sparling, G.P., 1997. Ants as indicators of restoration success: relationship with soil microbial biomass in the Australian seasonal tropics. Restor. Ecol. 7, 109e114. Backes, A., 1999. Condicionamento climático e distribuição geográfica de Araucaria angustifolia (Bertol.) Kuntze no Brasil e II. Pesqui. (Bot.) 49, 31e52. Baldissera, R., Ganade, G., Brescovit, A., Hartz, S.M., 2008. Landscape mosaic of Araucaria forest and forest monocultures influencing understorey spider assemblages in Southern Brazil. Aust. Ecol. 33, 45e54. Basu, P., 1997. Seasonal and spatial patterns in ground foraging ants in a rain forest in the Western Ghats, India. Biotropica 29, 489e500. Battirola, L.D., Marques, M.I., Adis, J., Delabie, J.H.C., 2005. Composição da comunidade de Formicidae (Insecta, Hymenoptera) em copas de Attalea phalerata Mart (Arecaceae), no Pantanal de Poconé, Mato Grosso, Brasil. Rev. Bras. Entomol. 49, 107e117. Berg, R.Y., 1975. Myrmecochorous plants in Australia and their dispersal by ants. Aust. J. Bot. 23, 475e508. Bibby, C.J., Burgess, N.D., Hill, D.A., 1992. Bird Census Techniques, first ed. Academic Press, London. Brandt, M., Wilgenburg, E., Sulc, R., Shea, K.J., Tsutsiu, N.D., 2009. The scent of supercolonies: the discovery, synthesis and behavioural verification of ant colony recognition cues. BMC Biol. 7, 1e9. Culver, C.D., Beattie, A.J., 1983. Effects of ant mounds on soil chemistry and vegetation patterns in a Colorado Montane Meadow. Ecology 64, 485e492. Delabie, J.H.C., Alves, H.S.R., França, V.C., Martins, P.T.A., Nascimento, I.C., 2007. Biogeografia das formigas predadoras do gênero Ectatomma (Hymenoptera:
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Original article
Edge effects on epigeic ant assemblages in a grasslandeforest mosaic in southern Brazil Esther R.S. Pinheiro*, Leandro da S. Duarte, Elena Diehl, Sandra M. Hartz Departamento de Ecologia, Universidade Federal do Rio Grande do Sul, A. Bento Gonçalves 9500, CP 15007, Porto Alegre RS 91501-970, Brazil
a r t i c l e i n f o
a b s t r a c t
Article history: Received 6 August 2009 Accepted 9 March 2010 Published online 1 April 2010
This study analyzed the influence of vegetation structure variation along a natural vegetation mosaic formed by Araucaria forest and Campos grassland in the southern Brazilian highlands, on the species richness and composition of epigeic ants. The study site consisted of two different grasslandeforest ecotones, where 76 pitfall traps were installed. We estimated the area covered by canopy vegetation by hemispherical photographs, and the structure of the understory vegetation by counting the number of vegetation touches, using a graduated stick. We collected 31 species or morphospecies of epigeic ants belonging to 17 genera and 6 subfamilies. Cluster analysis defined three habitat groups (grassland, edge, and forest) with different ant species composition as revealed by ordination analysis. The highest richness was observed at the forest edge, and decreased towards the grassland and the forest interior. Variation in the richness and composition of epigeic ant species was significantly explained by the factor of distance from the forest. The relationship between species richness and understory density was negative. On the other hand, species composition of epigeic ant assemblages was significantly explained by canopy cover. This finding indicates that the ecological responses of ant assemblages resulted predominantly from edge effects mediated by changes in vegetation structure. Ó 2010 Elsevier Masson SAS. All rights reserved.
Keywords: Habitat structure Ecotones Species diversity Araucaria forest Campos grasslands
1. Introduction Edge effects result from the interplay between two spatially contiguous ecosystems (Murcia, 1995). Edges usually exhibit features of both contiguous ecosystems, merged with particular microhabitat conditions generated by the contact between distinct environments (Risser, 1995). Edges often show increased biodiversity levels and complexity of vegetation structure (Murcia, 1995; Risser, 1995), which influences both vertebrate (Stevens and Husband, 1998) and invertebrate assemblage patterns (Majer et al., 1997). Insect assemblages are very important components of biodiversity, because they accumulate considerable biomass and show high species richness. Furthermore, insects play central roles in ecosystem functioning (Erwin, 1991; Folgarait, 1998). For these reasons, insects are valuable ecological indicators of edge effects in natural mosaic landscapes. Among insects, ants can be considered as terrestrial ecosystem engineers, because they are capable of modifying habitats and regulating resource distribution to other organisms (Jones et al., 1994). Many studies have used ants as
* Corresponding author. E-mail address: [email protected] (E.R.S. Pinheiro). 1146-609X/$ e see front matter Ó 2010 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.actao.2010.03.004
bioindicators of ecological processes (Culver and Beattie, 1983; Majer, 1983; Andersen and Sparling, 1997) in some cases, ant functional groups have been identified (Andersen, 1995; King et al., 1998; Hoffmann and Andersen, 2003; Stephens and Wagner, 2006), making possible comparisons among ant communities across biogeographical zones (Hoffmann and Andersen, 2003). Edges influence ant assemblage patterns, because variation in vegetation structure creates environmental gradients that affect ant activities such as nesting and foraging (Basu, 1997). For this reason, habitats with different degrees of complexity tend to show ant assemblages with distinct species compositions (Lassau and Hochuli, 2004). Nonetheless, Andersen (2008) has argued that habitat characteristics may not explain all the variation in richness and composition in ant assemblages. Other factors such as dispersal limitation could also be involved in the formation of ant assemblages across landscapes. Thus, analyses of speciesehabitat relationships should take into account between-site variation in species distribution, to avoid confounding effects of habitat on ant assemblages with spatial dispersal limitation. Although forests with Araucaria angustifolia (Araucariaceae) constitute the main forest type on the highland plateau in southern Brazil at altitudes above 500 m a.s.l. (Duarte and Dillenburg, 2000), data about the ant fauna of Brazilian Araucaria forests are scarce (but see Ketterl et al., 2003; Silva and Silvestre, 2004; Diehl et al., 2005).
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Araucaria forests in southern Brazil often form mosaics with Campos, which is a native grassland vegetation (Rambo, 1994; Duarte et al., 2002). Our main goal in this study was to analyze the influence of edge effects on species richness and composition of epigeic ant assemblages occurring in a natural vegetation mosaic formed by Araucaria forest and Campos grassland in southern Brazilian highlands. Then, we discuss the suitability of ants for the conservation of ecological processes in forestegrassland mosaics. 2. Materials and methods 2.1. Study site The study was conducted at 29 280 S and 50130 W, in the PróMata Research and Nature Conservation Center (CPCN Pró-Mata). The Center covers an area of 4500 ha and is located in São Francisco de Paula, state of Rio Grande do Sul, southern Brazil. The regional climate is classified according to Köppen’s system as Cfb (Moreno, 1961), which is subtropical (C) and rainy, with precipitation uniformly distributed throughout the year (f), and warm summers (b). The annual mean temperature is ca. 15.1 C (Hijmans et al., 2005), with freezing temperatures occurring from April to November (Backes, 1999). The annual mean rainfall is 2086 mm, equally distributed throughout the year (Hijmans et al., 2005). The study site consisted of ca. 78 ha Campos grassland surrounded by Araucaria forest, situated on a plateau at about 900 m a.s.l. Araucaria forest communities are characterized by the presence of woody species that are phytogeographically related to Austral-Antarctic and Andean floras (Rambo, 1951; Waechter, 2002). The most physiognomically important tree species is A. angustifolia. Some other typical species in these forests are Podocarpus lambertii, Drimys brasiliensis, Dicksonia sellowiana, and several species of Myrtaceae, Melastomataceae, and Lauraceae. Oliveira-Filho and Fontes (2000) recognized the Brazilian Araucaria forest as a particular type of Atlantic Forest. In the grassland, small forest nuclei, regionally called capões, are found, in different degrees of development (Duarte et al., 2006). Cattle grazing and burning practices were terminated in 1993, allowing increasing regeneration of the forest and more biomass accumulation and woody-plant establishment in the grassland (Oliveira and Pillar, 2004). These conditions generated a tall dense grassland matrix composed of caespitose grasses (Andropogon lateralis, up to 0.8 m high) and shrubs (Baccharis uncinella, Calea phyllolepis), which tend to suppress short grasses and other herbaceous species (Oliveira and Pillar, 2004).
identified by comparison with the specimens of Formicidae in the collection of the Laboratório de Insetos Sociais, UNISINOS, where all the collected specimens were deposited. 2.2.2. Ant attributes For each identified species, its foraging habit (carnivorous, granivorous, nectarivorous, omnivorous) and nesting site (epiphytes, hollow wood, litter, plant cavities, rocks, soil, trees) was categorized as nominal variables, according to information available in specialized literature (Takahashi-Del-Bianco et al., 1998; Holway et al., 2002; Rossi and Fowler, 2002; Kaufmann et al., 2003; Passos and Oliveira, 2003; Ramos et al., 2003; Schilman and Roces, 2003; Milesi and Casenave, 2004; Battirola et al., 2005; Harada, 2005; Longino, 2006; Marchioretto and Diehl, 2006; Weiser and Kaspari, 2006; Delabie et al., 2007; Longino and Fernández, 2007; Milks et al., 2007; Vieira et al., 2007; Brandt et al., 2009; Silva-Melo and Giannotti, 2010). For morphospecies we used available information encompassing the whole genus. 2.2.3. Habitat variables We evaluated the canopy vegetation cover by means of hemispherical photographs of the canopy (Frazer et al., 2001). Photographs were taken just above the soil traps, at ca. 1.5 m from the soil surface. The images were analyzed by using the software Gap Light Analyzer 2.0 (Frazer et al., 1999), and the proportion of sky area covered by vegetation (0e1) was obtained. At each sampling point, the structure of the understory vegetation was characterized by counting the number of vegetation touches at each 10-cm interval from the ground up to 1.5 m above the sampling trap, using a graduated stick (Bibby et al., 1992; Baldissera et al., 2008). By doing so, we estimated the density of the understory vegetation as the total number of vegetation touches along the stick (number of touches m1). Additionally, we calculated an index of understory homogeneity. For this, we generated a matrix describing the number of vegetation touches in each 10 cm interval (variables) at each sampling point. Whenever we found more than 10 vegetation touches per 10 cm interval, these were grouped in the same class. Thus, our data matrix contained ten variables (from 0 to 10 or more touches). We then computed a Shannon diversity index for each sampling point, which was taken as an index of understory height homogeneity. High Shannon index values indicated more vertically heterogeneous understories, while low values indicated more concentrated understories.
2.2. Sampling methods
2.3. Data analyses
2.2.1. Ant assemblages Sampling was carried out in January 2006, in two different grasslandeforest ecotone sites. In each site (at least 500 m distant from each other), two parallel, 180 m long transects were delimited, 20 m distant from each other. Transects were centralized in relation to the outermost forest tree/shrub with diameter at breast height >10 cm and whose crown was touching the continuous forest canopy. This point was assumed to represent the limit between grassland and forest (zero distance point). Nine sampling points were established at 10 m distance intervals starting from the edge, both in the direction of the grassland (negative distances), and in the direction of the forest (positive distances). Along each transect, one soil trap (300 mL) containing 70% ethanol mixed with detergent was installed at each sampling point (10 m distant from each other), totaling 76 sampling units. After 48 h of exposure, soil traps were collected (adapted from Agosti and Alonso, 2000). The collected material was identified at the genus level according to Palacio and Fernández (2003). All species and morphospecies were
We used ANOVA with permutation tests (Pillar and Orlóci, 1996) to evaluate the effects of the factors ‘site’ and ‘distance from forest edge’, as well as the interaction between these two factors, on the number of ant species found in each soil trap. Prior to the analysis, we performed a logarithmic transformation on the number of ant species. To control for spatial autocorrelation within transects, permutations among sampling units were nested within transects; after nesting, transects were permuted between sites as bundles (see Pillar, 2006). We used MANOVA with permutation tests (Pillar and Orlóci, 1996) to evaluate the effects of the factors ‘site’ and ‘distance from forest edge’, as well as the interaction between those two factors, on the composition of epigeic ant assemblages found in each soil trap, described as a presence/absence data matrix. Prior to the analysis, variables (ant species) were centralized to control for species commonness/rarity in the sample, and sampling units (traps) were normalized (Legendre and Legendre, 1998). For MANOVA we used the same permutation design as in the previous ANOVA. In both analyses, Euclidean distances were used as the
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dissimilarity index, and the sum of squares between groups (Qb statistics) was used as the test criterion. We used polynomial regression to analyze the association between the richness of epigeic ant species (dependent variable) and the distance from the forest edge (independent variable) (Sokal and Rohlf, 1981). To evaluate the association between the species composition of epigeic ants (dependent variable) and the distance from the forest edge (independent variable), we calculated the frequency of each taxon at each distance interval as the number of soil traps where the taxon was recorded (1e4) divided by the total number of soil traps per distance interval (4). From the matrix C containing each distance interval (sampling units) described by the frequency of ant taxa (variables), we computed a Euclidean distance matrix and performed a UPGMA cluster analysis. The number of sharp groups obtained was evaluated by bootstrapped auto-resampling (Pillar, 1999). Furthermore, we carried out a Principal Coordinates Analysis (PCoA) of sampling units in order to detect the principal axes of variation of habitat clusters obtained through UPGMA (sampling units) in relation to ant species (variables), based on Euclidean distances between sampling units (Legendre and Legendre, 1998). We explored the relationship between different habitat types and ant attributes (foraging habit and nesting site) through PCoA ordination, based on a chord distance matrix between sampling units. For this, we first expanded nominal attributes into dummy variables (Legendre and Legendre, 1998); accordingly, for a given
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attribute containing n states, n 1 binary variables were generated. This so-generated attribute matrix T contained ant taxa (sampling units) described by foraging and nesting binary attributes (variables). By matrix multiplication, T C generated a matrix CT containing each distance interval (sampling units) described by the frequency of ant attributes (variables). As distinct distance intervals showed highly variable numbers of ant species, the occurrence of particular foraging/nesting strategies were obviously dependent on how many species were present in each distance interval. For this reason, we standardized the frequency of occurrence of each attribute at each distance interval by the respective number of ant occurrences at the respective distance interval. This standardized matrix was then submitted to a PCoA ordination. We used a forward stepwise multiple regression to evaluate the association between the richness of epigeic ant species (dependent variable) and the three habitat variables (independent variables). To evaluate the association between the species composition of epigeic ants (dependent variable) and the three habitat variables (independent variables), we performed a stepwise canonical correspondence analysis (CCA, Ter Braak and Smilauer, 2002). P values for stepwise CCA were obtained through randomization of residuals, using a full model approach (see Legendre and Legendre, 1998). Regression analyses were carried out using the software STATISTICA 7 (StatSoft Inc., 2004). Analyses of variance, UPGMA, and PCoA were performed using the MULTIV 2.63 (Pillar, 2006)
Table 1 Assemblages of epigeic ants collected using soil traps distributed along a grasslandeforest gradient in southern Brazil. Species or morphospecies
Code
Foraging habit
Nest site
Mean frequency SEa
ECITONINAE Labidus coecus Latreille 1802
Laco
Carnivore
Soil
0.013 0.029
DOLICHODERINAE Linepithema sp.
Lisp
Nectarivore/omnivore
Soil
0.105 0.087
FORMICINAE Brachymyrmex heeri Forel 1874 Brachymyrmex sp. Camponotus sp. 1 Camponotus sp. 2 Camponotus rufipes Fabricius 1775 Myrmelachista sp. 1 Myrmelachista sp. 2 Paratrechina sp. 1 Paratrechina sp. 2
Brhe Brsp Cas1 Cas2 Caru Mys1 Mys2 Pas1 Pas2
Omnivore Omnivore Omnivore Omnivore Nectarivore Unknown Unknown Nectarivore Nectarivore
Under rocks/plant cavities Plant cavities/under epiphytes/litter Hollow wood Hollow wood Hollow wood Hollow wood/plant cavities Hollow wood/plant cavities Soil/under rocks/hollow wood Soil/under rocks/hollow wood
0.013 0.013 0.013 0.013 0.421 0.013 0.039 0.092 0.026
0.029 0.029 0.029 0.029 0.094 0.029 0.047 0.085 0.039
MYRMICINAE Crematogaster sp. Crematogaster quadriformis Roger 1863 Pheidole sp. 1 Pheidole sp. 2 Pheidole sp. 3 Pheidole sp. 4 Pheidole sp. 5 Pheidole fallax Mayr 1870 Solenopsis sp. 1 Solenopsis sp. 2 Solenopsis invicta Buren 1972 Strumigenys sp. Wasmannia sp.
Crsp Crqu Phs1 Phs2 Phs3 Phs4 Phs5 Phfa Sos1 Sos2 Soin Stsp Wasp
Omnivore Omnivore/nectarivore/seed Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore Omnivore/seed Carnivore Omnivore/Carnivore
Arboreal/hollow wood/plant cavities Arboreal/hollow wood/plant cavities Soil Soil Soil Soil Soil Soil Soil Soil Soil Soil Hollow wood/litter/under rocks
0.092 0.013 0.013 0.355 0.092 0.026 0.013 0.092 0.171 0.026 0.105 0.053 0.132
0.085 0.029 0.029 0.105 0.085 0.039 0.029 0.085 0.118 0.057 0.076 0.052 0.087
PONERINAE Anochetus sp. Ectatomma sp. Hypoponera sp. Hypoponera trigona Mayr 1887 Pachycondyla striata Smith 1858
Ansp Ecsp Hisp Hytr Past
Carnivore Omnivore/Carnivore Carnivore Carnivore Omnivore/Carnivore/seed
Hollow wood/under epiphytes Soil Soil/hollow wood/under rocks Soil/hollow wood/under rocks Soil
0.066 0.053 0.092 0.026 0.447
0.057 0.052 0.085 0.039 0.164
PSEUDOMYRMECINAE Pseudomyrmex sp. Pseudomyrmex acanthobius Emery 1896
Pssp Psac
Omnivore Omnivore
Hollow wood Hollow wood
0.013 0.029 0.013 0.029
a
SE ¼ standard error.
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statistical software. CCA was performed using the software CANOCO 4.5 (Ter Braak and Smilauer, 2002).
3. Results We collected 31 species or morphospecies of epigeic ants belonging to 17 genera and 6 subfamilies (Table 1). Species showing the highest frequencies were Pachycondyla striata Smith 1858, Camponotus rufipes Fabricius 1775, Pheidole sp. 2, Solenopsis sp. 1, Wasmannia sp., Solenopsis invicta Buren 1972, and Linepithema sp. (Table 1). The variation in the richness of epigeic ant species was significantly explained by the factor ‘distance to forest edge’ (Table 2), while the factors ‘site’ or interaction between site and distance from forest edge had no significant effects on either species richness or composition. A third-order polynomial was the best regression model explaining the variation of species richness along the grasslandeforest ecotone (Fig. 1). The highest richness was observed at the forest edge, decreasing towards the grassland and the forest interior. UPGMA classification of the frequency of epigeic ants along the grasslandeforest ecotone indicated three sharp groups of sampling units (Fig. 2), representing the grassland, the forest, and the edge between the two landscape matrices, starting in the grassland, at 10 m from the limit between grassland and forest, and extending to 20 m in the forest interior. PCoA ordination showed the association between the UPGMA groups and taxa of epigeic ants (Fig. 3a). Pseudomyrmex acanthobius Emery 1896, Brachymyrmex sp., Myrmelachista sp. 2, Solenopsis sp. 2, and Strumigenys sp. were associated with grassland. Labidus coecus Latreille 1802, Camponotus sp. 2, Crematogaster sp., Myrmelachista sp. 1, Pheidole sp. 1, Pheidole sp. 5, Solenopsis sp. 1, and Wasmannia sp. were related to the forest interior. Brachymyrmex heeri Forel 1874, Crematogaster quadriformis Roger 1863, Pheidole fallax Mayr 1870, Camponotus sp. 1, Linepithema sp., and Pseudomyrmex sp. were the ant taxa associated with the edge habitat. Other ant taxa did not show any specific association with habitat groups. PCoA ordination detected association between different habitat types and ant attributes related to foraging habit and nesting sites (Fig. 3b). Nectarivorous ants were associated with grassland sites, while carnivorous, granivorous and omnivorous species were related to forested sites. Edge habitats did not show any close relationship with specific foraging habits. Furthermore, use of hollow wood as nesting sites was related to open areas, while nesting in soil, litter or under rocks was related to forest sites. Nesting inside plant cavities, on epiphytes or trees was associated with edge habitats.
Fig. 1. Third-order polynomial regression of species richness in epigeic ants in a grasslandeforest mosaic on the distance from forest edge. R2 ¼ 0.33, F3,72 ¼ 11.63, P < 0.001. Probabilities of variables showing normal distribution were obtained through KolmogoroveSmirnov normality testing (P ¼ 0.29). Probabilities of variables showing constant variance were obtained through Spearman correlation tests between the absolute values of the residuals and the observed value of the dependent variable (P ¼ 0.84).
The variation patterns of habitat variables along the grasslandeforest gradient are shown in Fig. 4. A steep increase in canopy vegetation cover was observed, starting at 20 m (from grassland to forest) until 10 m inside the forest (Fig. 4a). Understory vegetation cover decreased from grassland to forest (Fig. 4b). Grassland tended to show a higher variability in relation to understory vegetation density than did forest. Also, the transition zone between grassland and forest was less abrupt in relation to understory density than that observed for canopy vegetation cover. In contrast, forest locations had higher and more variable understory homogeneity indices than did grassland locations (Fig. 4c). The stepwise regression of species richness on habitat variables (canopy cover, understory density, and understory homogeneity) showed that the best fit was attained when only understory vegetation density was included as the independent variable (Table 3). The relationship between species richness and understory density was negative; that is, denser understories tended to show lower species richness.
Table 2 Analyses of variance of species richness and composition of epigeic ants in a grasslandeforest mosaic in southern Brazil. Source of variation
Richnessa Compositionb
Sum of squared distances (Q) Site (S)
Distance to edge (D)
SD
Residual
Total
0.394 ns 3.717 ns
2.008** 19.759*
0.642 ns 15.642 ns
3.044 36.123
4.313 75.241
**P 0.001; *P 0.03; ns P > 0.3. P values obtained through random permutations (10 000 iterations). a ANOVA on the log-transformed number of ant species by sampling unit. b MANOVA on presence/absence of ant species in each sampling unit. Data were submitted to centralization within variables and normalization within sampling units (Legendre and Legendre, 1998).
Fig. 2. UPGMA classification of sampling points described by assemblages of epigeic ants and distributed along a grasslandeforest gradient in southern Brazil. Bootstrap auto-resampling indicated three sharp groups of sampling units, representing open field, edge, and forest habitats (1000 iterations).
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Fig. 4. Mean abiotic characteristics of sampling points along a grasslandeforest gradient in southern Brazil. a) Mean canopy cover (%) estimated through hemispherical photographs taken at approximately 1.5 m above the ground. b) Mean understory density estimated as the number of vegetation touches m1. c) Mean understory homogeneity index, obtained through the computation of Shannon diversity index using the number of vegetation touches as variables. The higher the index, the more homogeneous is the understory vegetation. Bars crossing the means (black squares) are standard errors.
4. Discussion
Fig. 3. PCoA ordination of sampling units classified into three habitat types (grassland, edge, and forest) described by a) taxa of epigeic ants and b) foraging habit and nesting sites of ants in a grasslandeforest mosaic in southern Brazil. See species coding in Table 1.
On the other hand, stepwise CCA showed that the species composition of epigeic ant assemblages was significantly explained by canopy cover (Table 4), although predictor variables explained only a minor proportion of the variation in ant species composition.
The species richness and composition of epigeic ants varied significantly along the grasslandeforest gradient, indicating that variation in vegetation structure influenced distribution patterns of ant assemblages (Basu, 1997; Lassau and Hochuli, 2004; Ribas et al., 2003; Vasconcelos et al., 2008). Furthermore, ant species richness and composition varied only in relation to the distance from the forest edge, independently of the site factor. This finding indicates that ecological responses of ant assemblages resulted exclusively from edge effects mediated by changes in vegetation structure
Table 3 Stepwise linear regression of species richness of epigeic ants in a grasslandeforest mosaic in southern Brazil on microhabitat characteristics. Independent variable added at each step b
Understory density Understory homogeneity index Canopy cover a
Cumul. R2a
df
F to enter/remove
P
Normality (P)c
Constant variance (P)c
0.22 0.24 0.25
1.74 2.73 3.72
20.49 2.13 0.72
<0.01 0.15 0.40
0.43 0.29 0.22
0.55 0.49 0.71
Cumulative R2 as independent variables were added to the model. Regression equation: y ¼ 0.71 0.21x þ 3. c Probabilities of variables showing normal distribution were obtained through the KolmogoroveSmirnov normality testing. Probabilities of variables showing constant variance were obtained through Spearman correlation tests between the absolute values of the residuals and the observed value of the dependent variable. b
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Table 4 Stepwise canonical correspondence analysis of species composition of epigeic ant assemblages on habitat variables. Pseudo-F Pb Independent variable added Sum of all Proportion of at each modeling step eigenvalues total explained variationa Canopy cover Understory homogeneity index Understory density
0.35 0.53
0.035 0.053
2.53 1.26
0.0001 0.1772
0.69
0.069
1.12
0.3131
a
The sum of all eigenvalues of the correspondence analysis of species composition ¼ 10.012. b P values generated through randomization (9999 iterations).
along transects (canopy cover and understory vegetation density). Although dispersal limitation in ant assemblages can determine in some extent species composition in different sites (Andersen, 2008), our results suggested that habitat characteristics were much more important to predict species composition than dispersal limitation. Ordination analysis revealed distinct ant species compositions for the three habitat groups defined by cluster analysis (grassland, edge, and forest). Habitat separation is likely to have occurred as a consequence of the influence of the variation in vegetation structure on the environmental conditions and resource availability for ants. Interestingly, species richness and composition along the grasslandeforest gradient responded to different vegetation structure factors. Species richness was negatively associated with understory vegetation density, a finding that could be explained by the more energetically efficient ant movement in less-complex habitats, especially in terms of resource acquisition, chemical trail establishment, and nesting activities (Lassau and Hochuli, 2004). In contrast, the variation in species composition along the gradient was significantly explained by canopy cover, although the amount of variation explained was very low. A possible explanatory mechanism underlying the variation in the composition of epigeic ant assemblages along the grasslandeforest ecotone might involve the variability in habitat range of some species in relation to others. Because the variation in vegetation structure affects ant abundance, less-competitive ant species are prevented from sharing the habitat space with more-competitive species, which is likely to exert a significant effect on the composition of epigeic ant assemblages (Perfecto and Vandermeer, 1996; Punttila et al., 1996). For instance, the influence of canopy cover on ant species composition might occur as a consequence of variation in light incidence, soil humidity, and temperature across habitats (Ríos-Casanova et al., 2006); these environmental fluctuations are likely to benefit some ant groups to the detriment of others, because species sharing ecological similarities (functional groups) probably occur in environmentally similar habitats (Vasconcelos et al., 2008). For instance, Holec et al. (2006) have found association between nesting strategy and habitat type. In our study, we observed that ants occurring in open areas tend to build their nests within hollow wood. This association could be explained by the frequent occurrence of B. uncinella shrubs in open areas near forest edges (Oliveira and Pillar, 2004). As those woody shrubs die, they offer good nesting sites for ants living in grassland. Along the grasslandeforest mosaic where the study was performed, accelerated vegetation dynamic is currently observed, in which Araucaria forest is expanding over Campos grassland (Oliveira and Pillar, 2004). In this process, plant species characteristic of forest edges begin the forest expansion over grassland. Although available evidence suggests that birds are the major seed transporters from the forest at the study site (Duarte et al., 2007), some pioneer plants may benefit from associations with seeddisperser ants. Seed dispersal by ants is a very frequent process in
nature. For instance, Pizo (2008) showed the importance of Pheidole praeses as a seed disperser of small-seeded plants in a tropical rainforest site. Seeds can be removed from the neighborhood of the parent plant and dispersed by a myriad of very generalist ant species, with very low interaction specificity (Berg, 1975). In our study, species such as C. quadriformis and P. fallax, which show very generalist dietary habits (Battirola et al., 2005; Ramos et al., 2003) and occur in Araucaria forest edges, might be promoting the dispersal of forest-plant seeds over grassland. Nonetheless, our results seem to suggest that some forest development is necessary for ants to act as effective promoters of seed dispersal in our study area, as we did not find any close association between foraging habit and edge habitat; indeed, granivorous and omnivorous ants were more associated with forested sites than with edges. Conservation of Araucaria foresteCampos grassland mosaics relies crucially on the maintenance of edge dynamics. Furthermore, organisms inhabiting edges play major ecological roles in the maintenance of the ecosystem as a whole, and knowledge about different ecological agents depends, obviously, on their accurate taxonomic identification. Unfortunately, knowledge about ant species remains sparse in the ecosystem evaluated in this study. In this paper we confirmed the existence of edge effects on ant assemblages occurring in forestegrassland mosaics. A more complete portrait of the contribution of ants the conservation of vegetation mosaics should arise as a deeper understanding of their functional roles in forestegrassland dynamics can be achieved. Acknowledgements The authors thank Marcelo Saraiva for field assistance, and Aline Centa, Aline Moraes, and Camila Santos for laboratory assistance. This study had logistical support from CPCN Pró-Mata PUCRS, and was funded by an undergraduate fellowship from PIBIC-CNPq to Esther Pinheiro, and grants from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) to Sandra M. Hartz (304036/2007-2). References Agosti, D., Alonso, L.E., 2000. The ALL protocol: a standard protocol for the collection of ground-dwelling ants. In: Agosti, D., Majer, J.D., Alonso, L.E., Schultz, T.R. (Eds.), Ants: Standard Methods for Measuring and Monitoring Biodiversity. Smithsonian Institution Press, Washington, pp. 204e206. Andersen, A.N., 1995. Measuring more of biodiversity: genus richness as a surrogate for species richness in Australian ant fauna. Biol. Conserv. 73, 39e43. Andersen, A.N., 2008. Not enough niches: non-equilibrial processes promoting species coexistence in diverse ant communities. Aust. Ecol. 33, 211e220. Andersen, A.N., Sparling, G.P., 1997. Ants as indicators of restoration success: relationship with soil microbial biomass in the Australian seasonal tropics. Restor. Ecol. 7, 109e114. Backes, A., 1999. Condicionamento climático e distribuição geográfica de Araucaria angustifolia (Bertol.) Kuntze no Brasil e II. Pesqui. (Bot.) 49, 31e52. Baldissera, R., Ganade, G., Brescovit, A., Hartz, S.M., 2008. Landscape mosaic of Araucaria forest and forest monocultures influencing understorey spider assemblages in Southern Brazil. Aust. Ecol. 33, 45e54. Basu, P., 1997. Seasonal and spatial patterns in ground foraging ants in a rain forest in the Western Ghats, India. Biotropica 29, 489e500. Battirola, L.D., Marques, M.I., Adis, J., Delabie, J.H.C., 2005. Composição da comunidade de Formicidae (Insecta, Hymenoptera) em copas de Attalea phalerata Mart (Arecaceae), no Pantanal de Poconé, Mato Grosso, Brasil. Rev. Bras. Entomol. 49, 107e117. Berg, R.Y., 1975. Myrmecochorous plants in Australia and their dispersal by ants. Aust. J. Bot. 23, 475e508. Bibby, C.J., Burgess, N.D., Hill, D.A., 1992. Bird Census Techniques, first ed. Academic Press, London. Brandt, M., Wilgenburg, E., Sulc, R., Shea, K.J., Tsutsiu, N.D., 2009. The scent of supercolonies: the discovery, synthesis and behavioural verification of ant colony recognition cues. BMC Biol. 7, 1e9. Culver, C.D., Beattie, A.J., 1983. Effects of ant mounds on soil chemistry and vegetation patterns in a Colorado Montane Meadow. Ecology 64, 485e492. Delabie, J.H.C., Alves, H.S.R., França, V.C., Martins, P.T.A., Nascimento, I.C., 2007. Biogeografia das formigas predadoras do gênero Ectatomma (Hymenoptera:
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