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Effects of habitat complexity on ant assemblages

Scott A. Lassau and Dieter F. Hochuli

Lassau, S. A. and Hochuli, D. F. 2004. Effects of habitat complexity on ant assemblages. / Ecography 27: 157 /164. We investigated responses of ant communities to habitat complexity, with the aim of assessing complexity as a useful surrogate for ant species diversity. We used pitfall traps to sample ants at twenty-eight sites, fourteen each of low and high habitat complexity, spread over ca 12 km in Sydney sandstone ridge-top woodland in Australia. Ant species richness was higher in low complexity areas, and negatively associated with ground herb cover, tree canopy cover, soil moisture and leaf litter. Ant community composition was affected by habitat complexity, with morphospecies from the genera Monomorium, Rhytidoponera and Meranoplus being the most significant contributors to compositional differences. Functional group responses to anthropogenic disturbance may be facilitated by local changes in habitat complexity. Habitat complexity, measured as a function of differences in multiple strata in forests, may be of great worth as a surrogate for the diversity of a range of arthropod groups including ants. S. A. Lassau(slassau@bio.usyd.edu.au) and D. F. Hochuli, Inst. of Wildlife Research, School of Biological Sciences, Heydon-Laurence Bldg A08, The Univ. of Sydney, NSW 2006, Australia.

Patterns in nature which occur over a variety of spatiotemporal scales are sometimes referred to as general laws of ecology (Lawton 1999). Numerous ecological patterns exist, although many generalisations have been accepted without substantial evidence (Beck 1997). The general assumption that habitat complexity is positively associated with the diversity of its constituent fauna (McCoy and Bell 1991) may not be strongly supported across scale, taxa and systems being investigated (e.g. Kotze and Samways 1999). The majority of studies concerning the role of habitat structure and complexity on its associated biota in undisturbed areas is focussed on aquatic environments (reviewed by Turner et al. 1999). General patterns in terrestrially based work suggests that species richness of ants (Andersen 1986), a range of other arthropods (Uetz 1979, Gardner et al. 1995, Humphrey et al. 1999, Hansen 2000) and mammals (August 1983, Dueser and Porter 1986) is positively associated with habitat complexity. Habitat complexity may also affect the composition of arthropod assemblages (e.g. Gardner et al. 1995). In outlining these

patterns, we note that an inherent difficulty in describing a general response to complexity is the multitude of operational definitions adopted in the literature. Our operational definition is consistent with the predominant usage at the scale of our work, considering habitat complexity as the heterogeneity in the arrangement of physical structure in the habitat surveyed. Ants respond to a range of disturbances and have been used as bio-indicators in the wake of forest clearing (Majer et al. 1997, King et al. 1998, Gascon et al. 1999), fire (Andersen 1991, Vanderwoude et al. 1997), minesites (Majer 1984, Majer and Nichols 1998), road construction (Samways et al. 1997, Lassau and Hochuli 2003), agricultural practices (Burbidge et al. 1992, Perfecto and Snelling 1995) and general anthropogenic disturbances (Burbidge et al. 1992). Mechanisms by which anthropogenic disturbance affect the composition of ants include alterations in shade (King et al. 1998, Hoffman et al. 2000), vegetation structure (Greenslade and Greenslade 1977) and plant species richness (Hoffman et al. 2000). Ant genera have been assigned to functional

Accepted 30 September 2003 Copyright # ECOGRAPHY 2004 ISSN 0906-7590

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groups that are thought to respond predictably to disturbances (Andersen 1990, Andersen et al. 2002) and help indicate ecosystem health. Functional groups could thus be used in conservation planning and assessment, reducing the expenses associated with surveys for arthropod diversity. One of the likely causal mechanisms underpinning functional group composition is their response to environmental variation, such as changes in habitat structure, associated with disturbance (Andersen 1990). Our study aims to examine the responses of ants to the large physical variability that may occur naturally in undisturbed habitats. We test whether high complexity habitat supports a greater richness, and/or a different composition of ant species than low complexity habitat.

Statistical analyses
We performed single-factor Analysis of Variance (ANOVA) to examine differences in the species richness of ants at high versus low complexity habitats and to detect the differences for those species that were comparatively most abundant in either low or high complexity areas. We tested correlations between ant species richness and individual habitat variable scores using Spearman Rank Correlations (SRCs). We also tested correlations among habitat variables using SRCs. Using the statistical package PRIMER (Anon. 2001), we constructed a Bray-Curtis dissimilarity matrix of our ant species data using a fourth root transformation to allow a more equal contribution of rare species (Clarke 1993). Non-standardised data were used, since throughout the study all collection sites were treated with equal importance. We then plotted a two-dimensional ordination using nonmetric multi-dimensional scaling (MDS), and performed Analysis of Similarities (ANOSIM) with 999 permutations. We used these methods to detect any compositional differences in ant assemblages between areas of low and high habitat complexity. We calculated Similarity Percentages (SIMPER) to determine which species contributed most to differences between treatment types.

Methods
Survey design
We selected fourteen study areas in Sydney sandstone ridge-top woodland (using the classification of Benson and Howell 1994). Each study area was selected so that it contained a pair of high and low complexity sites situated within 50 m of one another. This resulted in twenty-eight sites in 14 areas and over three National Parks in northern Sydney; Marramarra National Park, Muogamarra Nature Reserve and Ku-Ring-Gai Chase National Park (Fig. 1). Each of the twenty-eight sites were characterised according to their habitat complexity, using scores between 0 and 3 for six habitat variables, which is a modified version of the technique (i.e. the addition of a score for leaf litter) used by Coops and Catling (1997) (Table 1). The sites were selected a priori, fourteen being categorised as low complexity, after scoring 8 or less from 18 (Fig. 2a) and fourteen as high complexity, scoring 11 or greater (Fig. 2b).

Results
Low habitat complexity sites supported a much greater species richness of ants (ANOVA, F(1,26) 0/9.23, pB/0.01) (Fig. 3). The richness of ants was negatively associated with the ground herb cover (Spearman Rho0/ (/0.52, n0/28, pB/0.005), tree canopy cover (Spearman Rho 0/ (/0.45, n0/28, pB/0.05), soil moisture (Spearman Rho 0/ (/0.44, n0/28, pB/0.05) and leaf litter (Spearman Rho0/ (/0.39, n0/28, pB/0.05) (Fig. 4). A surprisingly low number of correlations existed among habitat variables; soil moisture was positively associated with tree canopy cover (Spearman Rho0/0.59, n0/28, pB/0.001), shrub canopy cover (Spearman Rho0/0.40, n0/28, pB/0.05), ground herb cover (Spearman Rho0/0.47, n0/28, pB/0.05) and ground herb cover was positively associated with tree canopy cover (Spearman Rho 0/0.45, n0/28, pB/0.05). The species composition of ants differed between habitat complexity treatments (ANOSIM, Global R 0/0.193, pB/0.005), and high complexity sites were generally more similar to each other than to low complexity sites based on ant species composition (Fig. 5), although the ordination may not be an accurate representation of the data considering the stress is /0.2. This indicates the species contributing most to the differences between low and high complexity areas thrived in a different range of ecological conditions and/or were dependent of other species which have a niche in a particular habitat type.
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Sampling methods
We sampled ants using five pitfall traps in each of the twenty-eight sites during December 2000/January 2001. The traps were 9 cm in diameter and were left out for a period of 28 d, one-third filled with ethylene glycol for preservation of captured arthropods. We identified ants to genus and species or morphospecies, depending on the certainty of species-level classification information (Shattuck 1999). We refer to morphospecies as species for the duration of this paper for simplicity. We compared patterns in ant species richness and composition to address the aims of our study. 158

Fig. 1. a) Schematic representation of the sampling design. Within the three National Parks, each square represents paired H and L sites (high and low habitat complexity, respectively). b) Study area location.

Less than 6% of species trapped contributed to /16% of the dissimilarity in ant composition between low and high complexity areas. Inspection of the most contribut-

ing species and their functional groups revealed that Monomorium A (ANOVA, F(1,26) 0/7.89, pB/0.01) (Generalised myrmicine), Rhytidoponera metallica A

Table 1. Visual method for scoring habitat complexity (modied from Coops and Catling 1997). Structure Score 0 Tree canopy (% cover) Shrub canopy (% cover) Ground flora (height in m) Logs, rocks, debris etc. (% cover) Soil moisture Leaf litter (% cover) 0 0 Sparse* (and B/0.5) 0 Dry 0 1 B/30 B/30 Sparse* (and /0.5) B/30 Moist B/30 2 30 /70 30 /70 Dense** (and B/0.5) 30 /70 Permanent water adjacent 30 /70 3 /70 /70 Dense** (and /0.5) /70 Water-logged /70

* Sparse ground flora refers to grasses covering B/50% of a study site. ** Dense ground flora refers to grasses covering /50% of a study site.
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Fig. 2. a) Example of low habitat complexity (site 3 in Marramarra National Park). This site scored 6 from 18 (tree canopy cover0/1; shrub canopy cover0/1; ground herb cover0/1; leaf litter0/1; moisture0/ 0; amount of logs, sticks and debris 0/2). b) Example of high habitat complexity (site 6 in Marramarra National Park). This site scored 11 from 18 (tree canopy cover0/2; shrub canopy cover0/2; ground herb cover0/2; leaf litter0/2; moisture0/1; amount of logs, sticks and debris 0/2).

(ANOVA, F(1,26) 0/6.23, pB/0.02) (opportunist) and Meranoplus A (ANOVA, F(1,26) 0/6.59, pB/0.02) (hot climate specialist) had a significantly higher abundance in low complexity than high complexity areas. The abundance and species richness of total ants belonging to these functional groups was also greater in low complexity areas (Table 2).

Discussion
We found that habitat complexity was an important factor governing ant species richness and composition in 160

Sydney sandstone ridgetop woodland. The species richness of ants was greater in areas of low habitat complexity, contrary to many habitat complexity/fauna diversity studies suggesting general relationships. Although there are exceptions, it is commonly reported that species richness generally correlates with the complexity of physical structure (McCoy and Bell 1991). Our results suggest a combination of habitat characteristics govern the presence and preferences of ant assemblages. Of the six environmental structure variables assessed, ground herb cover, tree canopy cover, soil moisture and leaf litter were negatively correlated with ant species richness. Andersen (1986) concluded that higher species diversity
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Fig. 3. Mean species richness (9/SE) of ants trapped in low and high habitat complexity areas.

of ants in woodland than heath was probably because areas with a more complex habitat are likely to provide

more environmental niches and more foraging opportunities. Contrary to these comparisons among habitat types, our data suggest higher levels of complexity are not preferable environments to the majority of ant species within a woodland. Furthermore, differences in the complexity of habitat in our study did not appear to reflect a different successional state, but rather the patchy mosaic of eucalypt-dominated sandstone woodlands on nutrient-poor soils. One possible mechanism for the patterns observed is that ant movement may be more energy efficient in less complex areas, where the ground cover (including leaf litter, ground herb, logs, rocks, sticks and debris) is more negotiable at the scale of a foraging ant (e.g. Kaspari and Weiser 1999). The same may apply for following chemical cues excreted for trails by other individuals in a colony. Other advantages of low complexity areas may be simpler construction and guarding of nests or lower soil moisture and shadow levels, leading to greater

Fig. 4. Species richness of ants found in areas of varying comparative a) tree canopy cover b) shrub canopy cover c) ground herb cover d) leaf litter e) soil moisture and f) amount of logs, sticks and debris. A blank column indicates the habitat variable score was not found in the survey.

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Fig. 5. MDS ordination of sample sites, based on the species composition of ants in low and high complexity habitats.

light and heat intensities for energy requirements, since the vast majority of ant species are strongly thermophilic (Holldobler and Wilson 1990). Despite being one of the most commonly used methods to survey terrestrial arthropods in ecological

studies, a range of possible biases may accompany pitfall trapping as a comparative technique, such as digging-in affects (Greenslade 1973) or skewed trap results depending on the habitat being surveyed and the activity of ants (Romero and Jaffe 1989, Melbourne 1999, Bestelmeyer et al. 2000). The immediate surface around all pitfalls in our study were set identically flush with soil to minimise habitat dependent variation, and we consider that twenty-eight days is ample time to allow less active ants to be captured. Melbourne (1999) showed that habitat structure at very fine scales (manipulations within 80 cm) may bias ant catch in pitfall samples. This bias is unlikely to explain the patterns observed in our study, as we observed responses over far greater scales. We suggest that pitfall traps were ideal for our study, and for assessing responses to disturbances over landscape scales, justifying their widespread use (Andersen et al. 2002). However, responses detected from our study cannot necessarily be generalised across all ant fauna, and may be only applicable to ground foraging species. Open areas are reported to support a greater percentage of opportunistic ants (Andersen 1990, King

Table 2. Ant functional groups and genera abundance totals in low and high complexity areas. Data in brackets is species richness of each genus. Totals of each functional group are given in bold. Functional Group 1. Dominant Dolichoderinae 2. Associated subordinate Camponotinae 3a. Hot climate specialists Genus Froggattella Iridomyrmex Leptomyrmex Camponotus Polyrhachis Cerapachys Melophorus Meranoplus Dolichoderus Notoncus Prolasius Sphinctomyrmex Oligomyrmex Solenopsis Strumigenys Discothyrea Hypoponera Tapinoma Paratrechina Tetramorium Rhytidoponera Adlerzia froggatti Crematogaster Monomorium Pheidole Myrmecia Low Complexity Areas 70(1) 671(2) 13(1) 754(4) 160(10) 5(1) 165(11) 0 179(5) 166(1) 345(6) 122(4) 29(1) 13(1) 164(6) 1 1 36(1) 3(1) 1 1 43(6) 24(1) 24(1) 289(2) 22(1) 205(2) 516(5) 4(1) 313(4) 467(7) 1153(5) 1937(17) 3(2) 3(2) High Complexity Areas 54(1) 195(3) 7(2) 256(6) 54(7) 0 54(7) 2(1) 15(3) 18(1) 35(5) 25(3) 14(1) 21(2) 60(6) 0 0 18(1) 15(1) 1 0 34(3) 9(1) 9(1) 203(2) 11(1) 12(1) 226(4) 5(1) 201(4) 69(6) 440(5) 715(16) 8(3) 8(3)

3b. Cold climate specialists

4a. Cryptic species

4b. Sub-cryptic species 5. Opportunists

6. Generalised myrmicines

7. Large, solitary foragers

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et al. 1998), a generalisation supported by our study. We found that the generalised myrmicines and hot climate specialists followed the same pattern. The ant community patterns observed in our survey basically correspond to the functional group model formally proposed and tested (Andersen 1986, 1990, King et al. 1998), suggesting functional group generalisations may be applicable in Sydney sandstone woodlands. Although ants are often promoted as a good bioindicator for ecological disturbance (Andersen 1991, Majer et al. 1997, King et al. 1998, Gascon et al. 1999), the species richness of ants may be negatively associated with other arthropod taxa within a particular habitat, since the majority of studies have found a positive relationship between habitat complexity and arthropod species diversity (Uetz 1979, Gardner et al. 1995, Humphrey et al. 1999, Hansen 2000). Habitat complexity, measured as a function of differences in multiple strata in forests, may be of great worth as a surrogate for the diversity of a range of arthropod groups including ants.
Acknowledgements / This project was supported by the Australian Museum and the Australian Research Council. SAL is also grateful for support from the Australian Museum student grant scheme. For patient help with ant identications we thank Derek Smith and Elizabeth Jeffreys. For valued support, discussion and comments on the manuscript we especially thank Gerry Cassis, Lance Wilkie, Paul Flemons and Heloise Gibb.

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