Using ants as bioindicators in land management: simplifying assessment of ant community responses

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The indicator qualities of terrestrial invertebrates are widely recognized in the context of detecting ecological change associated with human land-use. However, the use of terrestrial invertebrates as bioindicators remains...

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Using ants as bioindicators in land management: Journal of Applied Ecology 2002 simplifying assessment of ant community responses 39, 8 – 17 ALA N N. A NDERSEN *, B EN JAMI N D. H OFFMANN *, WA RRE N J. M Ü LLER † AND A N THO N Y D. G RIFFITHS *‡ *Tropical Savannas Cooperative Research Centre, Division of Sustainable Ecosystems, CSIRO Tropical Ecosystems Research Centre, PMB 44 Winnellie, NT 0822, Australia; and †CSIRO Mathematical and Information Sciences, GPO Box 664, Canberra, ACT 2601, Australia Summary 1. The indicator qualities of terrestrial invertebrates are widely recognized in the context of detecting ecological change associated with human land-use. However, the use of terrestrial invertebrates as bioindicators remains more a topic of scientific discourse than a part of land-management practice, largely because their inordinate numbers, taxonomic challenges and general unfamiliarity make invertebrates too intimidating for most land-management agencies. Terrestrial invertebrates will not be widely adopted as bioindicators in land management until simple and efficient protocols have been developed that meet the needs of land managers. 2. In Australia, ants are one group of terrestrial insects that has been commonly adopted as bioindicators in land management, and this study examined the reliability of a simplified ant assessment protocol designed to be within the capacity of a wide range of land managers. 3. Ants had previously been surveyed intensively as part of a comprehensive assessment of biodiversity responses to SO2 emissions from a large copper and lead smelter at Mt Isa in the Australian semi-arid tropics. This intensive ant survey yielded 174 species from 24 genera, and revealed seven key patterns of ant community structure and composition in relation to habitat and SO2 levels. 4. We tested the extent to which a greatly simplifie d ant assessment was able to reproduce these results. Our simplified assessment was based on ant ‘bycatch’ from bucket-sized (20-litre) pitfall traps used to sample vertebrates as part of the broader biodiversity survey. We also greatly simplified the sorting of ant morphospecies by considering only large (using a threshold of 4 mm) species, and we reduced sorting time by considering only the presence or absence of species at each site. In this manner, the inclusion of ants in the assessment process required less than 10% of the effort demanded by the intensive ant survey. 5. Our simplified protocol reproduced virtually all the key findings of the intensive survey. This puts effective ant monitoring within the capacity of a wide range of land managers. Key-words: environmenta l assessment , land-use impacts, monitoring , sampling protocols, SO2 Journal of Applied Ecology (2002) 39, 8 – 17 Introduction Correspondence: Alan Andersen, Tropical Savannas Cooper- ative Research Centre, Division of Sustainable Ecosystems, The indicator qualities of terrestrial invertebrates are CSIRO Tropical Ecosystems Research Centre, PMB 44 Win- widely recognized in the context of detecting ecological nellie, NT 0822, Australia (e-mail Alan.Andersen@csiro.au). change associ ated with human land use (Rosenberg, ‡Present address: Key Centre for Tropical Wildlife Manage- Danks & Lehmkuhl 1986). This contrasts with the use © 2002 British ment, Northern Territory University, Darwin, NT 0909, of particular invertebrate groups as indicators of Ecological Society Australia. general
9 diversity patterns (Pearson & Cassola 1992; Kremen 1994), which has been widely disputed (Lawton et al. Simplified ant 1998; Kotze & Samways 1999). Invertebrates make assessment good indic- ators of ecological condition because they are highly diverse and functional ly important , can integrate a variety of ecol ogical processes, are sensitive to environ- mental change, and are easily sampled (Greenslad e & Greenslad e 1984 ; Brown 1997 ; McGeoch 1998). Despite these qualities, however, the use of terrestrial invertebrates as bioindicators remains more a topic of scientific discourse than a part of land- management practice. With few exceptions, invertebrates are rou- tinely ignored in land monitoring and assessment pro- grammes, largely because their inordinate numbers, taxonomic challenges and general unfamiliarity are too intimidating for most land-management agencies (New 1996). This contrasts with the situation in aquatic systems, where relatively simple protocols for assessing mac roinvertebrates have been widely applied in studies of river health (Hellawell 1978; Norris & Norris 1995). Terrestrial insects and other inverte- brates will not be widely adopted as bioindicators in land management until simple and efficient protocols have been developed that meet the needs of land man- agers (Andersen 1999). In Australia, ants are one group of terrestrial insects that has been common ly adopted as bioindic ators in land management (Majer 1983; Andersen 1997a). In particular, ants have frequent ly been used by the min- ing industry as indicators of restoration success (Majer 1984; Andersen 1997b). Ant species richness and com- position show predictable colonization patterns at mine sites undergoing rehabilitation (Andersen 1993; Majer & Nichols 1998; Bisevac & Majer 1999), with these patterns reflecting those of other invertebrate group s (Majer 1983 ; Andersen 1997b) and key eco- system processes (Andersen & Sparling 1997). More recently, ants have been used as indicators of off-site mining impacts (Read 1996; Hoffmann, Griffiths & Andersen 2000) and for other land uses such as forestry (York 1994; Vander woude, Andersen & House 1997) and pastoralism (Landsberg, Morton & James 1999; Hoffmann 2000; Read & Andersen 2000). However, in virtually all these cases ant surveys have involved spe- cialist entomologists, and comp rehensive ant surveys remain largely beyond the capacity of most environ- mental practitioner s. In any sampling programme there will inevitably be a trade-off between simplicity on one hand, and reli- ability on the other. When ende avouring to make insect surveys more accessible to land managers, there is no poin t i n d ev elopin g s implifie d s amplin g p rotocols if reliability is serious ly compromised. This © 2002 British Ecological Society, study examined the reliability of a simplified ant Journal of Applied assessment protocol designed to be within the capacity Ecology, 39, of a wide range of land managers. 8– 17 The study was conducted as part of a comprehensive assessment of biodiversity responses to SO2 emissions from a large copper and lead smelter at Mt Isa in the
to biogeographical affinity, with the overall Table 1. Key abundance of Eyrean findings of a (arid-adapted) taxa increasing in relation to SO2, comprehensive ant Torresian (tropical) taxa decreasing, and widespread sampling taxa showing no change. programme conducted as part of an assessment of the biodiversity Australian semi-arid tropics. Vegetation had been impacts of SO2 dra- matically affected immedi ately downwind from emissions from Mt the smelter, and the influence of the smelter could be Isa mine (Hoffmann, detected for at least 15 km (Griffiths 1998). A key Griffiths & ques- tion was whether or not faunal biodiversity Andersen 2000) was sim- ilarly affected. Routine vertebrate sampling indicated that bird and reptile assemblages were 1. The two significantly influ- enced by high SO2 levels (up to 5 regionally dominant km from the smelter), with mammals providing too landforms few records for statistical treatment (Griffiths 1998) . (rocky ridges A survey of ants, on the other hand, revealed an and alluvial effect of the smelter for up to 35 km (Hoffmann, plains) supported Griffiths & Andersen 2000). Ants were therefore a distinct ant far more sensitive indicator of the effects of the faunas. smelter on faunal integrity than vertebrates. 2. Ant The ant survey was based on catches in abundance small (4·5 cm) pitfall traps that were partly filled declined with increasing levels with pre- servative, which is the most widely used of SO2. technique for obtaining quantit ative assessments of 3. Species ant communities in open habitats (Andersen 1991; richness declined with increasing Bestelmeyer & Wiens levels of SO2. 1996; Fisher 1999). The survey yielded 174 species 4. from Speci 24 genera, and revealed seven key patterns of ant es com- munity structure and composition in relation comp to habi- tat and SO2 (Table 1). Our simplified ositio n protocol used the ant ‘bycatch’ from the bucket-sized varie pitfall traps used to capture vertebrates, which are d routinely used in wildlife surveys. We tested the syste extent to which our simplified ant assessment was matic ally sufficient to reproduce the seven key results of the with intensive ant sampling programme. incre asing levels Metho of ds SO2. 5. Several     common species Mt Isa is located in north-western Queensland showed (29°43′ S clear abundance 139°27′ E), Australia, with its 400-mm average patterns in annual rainfall being heavily concentrated within a relation to summer wet season. Temperatures are high year- SO2, with round, with mean monthly maxima ranging from some decreasing about 25 °C (July) to 38 °C (November), and and others minima 10 °C to increasing. 6. Ant functional group composition (sensu Andersen 1995) showed relatively little change in relation to SO2. 7. Ant responses varied according
the mayri and purpureus groups of Iridomyrmex, and 24 °C (Bureau of Meteorology, Mt Isa). The major 10 the bagoti and aeneovirens groups of Melophorus A.N. Andersen landforms in the region are erosional Tertiary surfaces et al. with skeletal soils, rock (sandstone, shale and quart- zite) outcrops and alluvial plains. The predominant vegetation is low open woodland dominated by species of Eucalyptus, Acacia and Atalaya, with the ground- layer dominated by hummock grass (Triodia spp.) on skeletal soils and tussock grasses (species of Aristida and Cenchrus) on alluvial loams.        Biodiversity sampling at Mt Isa was stratified accord- ing to four SO2 zones arranged along the direction of p revailin g winds : backg roun d (soi l s ulph ate levels 1– 5 p.p.m., 15 – 30 km upwind from the smelter), low (10 – 30 p.p.m., 30 – 35 km downwind), medium (30 – 70 p.p.m., 7 –15 km downwind) and high (70 –120 p.p.m., 3 – 5 km downwind) (Griffiths 1998). The intensive ant survey was conducted at 40 sites, comprising four rocky ridge and four alluvial plain sites at each of the low, medium and high SO2 zones, and eight sites from each habitat in the background zone (Hoffmann, Griffiths & Andersen 2000). Ants were sampled using 4·5-cm diameter pitfall traps partly filled with ethylene glycol as a preservative. A 5 × 3 grid of traps with 10-m spac- ing was established at each site, and operated for 48 h. All ants falling into traps were sorted to species, iden- tified and enumerated. Vertebrate pitfall traps (20-litre buckets, 28-cm diameter) were installed at 14, 14, 21 and 16 sites, respect ively, within the background, low, medium and high SO2 zones, distributed amongst the three major habitat types as follows: rocky ridges, 23 sites; rocky plains, 20 sites; alluvial plains, 22 sites (Table 2). These sites included all those used in the intensive ant survey, except for eight from the background zone. At each site, four pitfall traps (28-cm diameter plastic buckets), each with 10 m of drift fencing (height 30 cm), were randomly located within a 100 × 100-m plot. Our sim- plified protocol therefore considered ants from 220 (large) traps distributed across 65 sites, compared with 600 (small) traps from 40 sites for the intensive ant survey. Ants were collected from vertebrate traps early in the morning and late in the afternoon during 5 consecut ive days between late October and early December 1997. This was done within 2 weeks of the intensive ant survey. In addition to simplified sampling (i.e. using the ant bycatch from routine vertebrate traps), we also greatly simplified the sorting of specimens in the laboratory by considering only large species. A 4-mm total length threshold was used to © 2002 British designate genera and species groups to be Ecological Society, considered. The taxa we considered were Anochetus, Journal of Applied Bothroponera, Leptogenys, Odontomachus, Ecology, 39, Rhytidoponera, Calomyrmex, Camponotus, Opisthopsis 8– 17 and Polyrhachis (i.e. all specie s withi n these genera), as well as the diversus species group of Meranoplus,
species by site presence/absence matrix from our (nomenclature simplified protocol. Each species had a binary follows response at eac h site, producin g a numbe r of Andersen 2000). occupie d sites out of a total possible number of The use of sites for each zone × habitat combination. Our higher-level taxa analytical strategy was to fit generalized linear rather than a models (GLM) with bino- mial error and logit link strict size (Dobson 1990). These ana- lyses give rise to analysis criterion avoided of deviance tables. When the residual deviance is potential greater than one, extra-binomial variation may be confusion caused present and the deviance ratios are approximate F- by polymorphic ratios and can be tested for significance in a manner or otherwise similar to F-ratios in . When the residual variably sized deviance is less than or equal to one, binomial species in which variation is assumed and testing for significance some speci- mens is based on the deviance for each term being fall below but approxim- ately distributed as a chi-squared variate. others are above The outputs of such analyses are lists of factors with the threshold. their deviances or deviance ratios, and their level of Sorting time was significance. For significant terms we provided further reduced adjusted means and standard errors where by considering appropriate. The means were the average only the presence proportions of sites occupied by individual species or absence of for all species in the model. species at each Three sets of analyses were performed, fitting site, rather than indi- vidual species, functional groups (Andersen their abundanc e. 1995) and groups based on biogeographical We did not affinities (Andersen quantify it, but 2000) as factors, respectively. Five functional groups esti- mated that were commo n enoug h for analysis: Dominant our simplified Dolichoderinae (species of Iridomyrmex), protocol required Subordinate Camponotini (primari ly species of less than Camponotu s and Polyrhachis), Hot Climate 10% of the Specialists (species of Melophoru s and laboratory time. Meranoplus), Opportunists (primarily species of This was despite Rhyti- doponera) and Specialist Predators (primarily the sim- plified species of Bothroponera and Leptogenys). Similarly, protocol three bio- geographical groups, Eyrean, Torresian and covering more widespread, were common enough for analysis. sites. Analyses were also conducted on the eight individual species that were recorded from at least  15 sites.  Patterns of species composition in relation to  habitat and SO2 were explored by mult ivari ate  analysis, as was the case for results from the  intensive survey (Hoffmann, Griffiths & Andersen  2000) . Site species data were combined within  habitat types, and a similarity   was used to analyse abundance data in the inten- sive ant study (Hoffmann, Griffiths & Andersen 2000), but an alternative analytical strategy was needed for the
8 – 17 Ecology, 39, Journal of Applied Ecological Society, © 2002 British assessment Simplified ant 11 Table 2. Records of ant species across SO2 zones and habitat type (RR, rocky ridge; RP, rocky plain; AP, alluvial plain). Data are numbers of sites at which species were recorded. Species codes follow Hoffmann, Griffiths & Andersen (2000) (those not recorded by Hoffmann, Griffiths & Andersen 2000 are indicated by an asterisk). The functional group (FG; DD, Dominant Dolichoderinae; HCS, Hot Climate Specialist; OPP, Opportunist; SC, Subordinate Camponotini; SP, Specialist Predator) and biogeographical affinity (BIOG; E, Eyrean; T, Torresian; W, widespread) of each species is also given SO2 zone High Medium Low Background Total RR RP AP RR RP AP RR RP AP RR RP AP RR RP AP Habitat 7 3 6 6 8 7 5 5 4 5 4 5 23 20 22 No. sites FG BIOG Anochetus sp. C (armstrongi gp)* SP T 1 1 Bothroponera sp. B (excavata gp) SP T 2 2 4 Leptogenys adlerzi SP T 1 1 1 1 2 2 Odontomachus sp. A (ruficeps gp) OPP T 1 1 2 1 1 1 4 2 1 Rhytidoponera ?metallica* OPP W 1 1 Rhytidoponera sp. nr. reticulata OPP T 1 1 1 3 2 2 4 2 Rhytidoponera sp. nr. cornuta OPP T 1 1 3 1 4 2 2 1 2 4 9 Rhytidoponera sp. nr. rufithorax OPP E 7 1 4 3 5 4 4 2 2 4 5 16 12 13 Rhytidoponera sp. C (convexa gp) OPP E 3 3 6 Meranoplus sp. C (diversus gp) HCS E 1 1 Meranoplus sp. H (diversus gp) HCS E 1 1 Iridomyrmex sp. nr. mayri DD E 2 1 3 3 2 3 2 2 10 4 Iridomyrmex sanguineus DD E 2 1 1 1 1 1 1 3 2 3 Calomyrmex ?cyanea SC T 1 1 1 1 1 1 Camponotus dromas SC E 1 1 Camponotus sp. A (denticulatus gp) SC E 3 1 4 2 4 4 1 1 6 5 9 Camponotus fieldae SC T 2 1 1 4 5 3 4 4 1 2 1 12 11 5 Camponotus sp. C (discors gp) SC W 1 2 2 1 2 2 6 Camponotus sp. D (novaehollandiae gp) SC T 5 1 1 3 4 1 11 4 Camponotus sp. E (claripes gp) SC W 1 1 1 1 Camponotus sp. F (subnitidus gp) SC E 2 2 3 1 2 1 1 1 1 1 4 5 6 Camponotus sp. H (sponsorum gp) SC E 1 1 2 2 2 Camponotus sp. K (novaehollandiae gp)* SC T 1 1 1 1 Camponotus sp. L (rubiginosus gp)* SC W 1 1 2 Camponotus sp. M (rubiginosus gp)* SC W 1 1 Camponotus sp. O (claripes gp)* SC W 1 1 1 1 Camponotus sp. P (rubiginosus gp)* SC W 1 1 Camponotus sp. Q (discors gp)* SC W 5 1 4 3 3 1 1 2 1 1 1 3 10 7 9 Melophorus bagoti HCS E 1 3 2 2 2 6 Melophorus sp. AK (aeneovirens gp) HCS E 1 1 Opisthopsis haddoni SC T 1 1 1 3 1 5 Opisthopsis ?rufoniger SC T 1 1 Opisthopsis rufithorax SC T 1 1 1 1 1 1
12 matrix of habitat type /SO2 zone combinations was AP 3 3 22 A.N. Andersen con- structed using the Jaccard index, based on 4·5 1 99 28 et al. presence / absence data for all species. Habitat type /SO2 zone combinations were then ordinated RP 3 20 4·8 using semi-strong hybrid multidimensional scaling 2 4 1 3 96 28 (SSH option of the PATN software pack age; Belbin Total 1994). RR 23 4·6 3 4 4 1 3 3 23 105 Results AP 5 6·0          2 2 1 30 17 A total of 41 species from 12 genera was recorded by Background 5·5 RP 2 1 15 22 our simplified protocol, with Camponotus (14 species) 4 and Polyrhachis (eight) collectively contributing half of all species (Table 2). Twelve (29%) species were not 5·2 RR 2 1 3 1 1 15 26 5 among the 174 species recorded during the intensive ant survey of Hoffmann, Griffiths & Andersen (2000). 5·8 This high proportion can be explained by the greater AP 1 1 16 23 4 efficiency of drift fences in capturing uncommon species. We did not consider abundance per se, 6·0 RP 1 1 2 2 17 30 because we considered only presence/absence data. 5 However, the occurrence of species across sites can be used as an abundance surrogate. Considering all Low 4·2 RR 2 1 11 21 5 species, mean occur rence decreased significantly (deviance = 9·63, d.f. = 3, P = 0·02) with increasing 3·6 levels of SO2, and mean site species richness showed AP 12 25 7 a similar pattern, although this was not quite statistically significant (P = 0·07, one-way ; Fig. 1). 4·3 RP Individual species exhibited a wide range of responses 2 1 17 34 8 Medium in relation to SO2 (Fig. 2). Three of the eight most common species showed statistically significant 4·3 RR 1 1 2 2 14 26 responses (Table 3), with the most marked being 6 shown by Camponotus sp. A (denticulatus group), 3·5 which occurred primari ly at higher SO2 zones (Fig. AP 10 21 6 2d). Four of these eight species showed significant habitat effects (Table 3). The most marked was for 3·3 RP Camponotus sp. D (novaehollandiae group), which 1 8 10 SO2 zone 3 occurred primarily at rocky ridge sites and was not recorded at all in alluvial plain habitat (Table 2). High 4·6 RR 1 11 32 The functional group –zone interaction was not sig- 7 nificant (deviance ratio = 1·51, d.f. = 12,396, P > 0·05), indicating that functional group composition was rel- FG BIOG atively uniform across SO2 zones. There was a T T T E T T T T tendency for specialist predators to favour low levels of SO2 (the nine records occur red exclusively in the SC SC SC SC SC SC SC SC low or back- ground zones; Table 2), but their numbers were too low to influence the overall analysis. In cont rast, the bio- geographical group–zone inte raction was highly sig- nificant (deviance ratio = 4·57, d.f. = 6,418, P < 0·001). The mean occurrence of Polyrhachis sp. A (schwiedlandi gp) widespread species was relat- ively constant, but the Polyrhachis sp. J (ammon gp)* Polyrhachis sp. I (ammon gp)* occurrence of Torresian species declined Polyrhachis sp. B (gravis gp) Polyrhachis sp. K (gab gp)* Table 2. continued. systematically in relation to SO2, and Eyrean taxa Polyrhachis prometheus* Polyrhachis inconspicua showed a curvilinear response (Fig. 3). © 2002 British Polyrhachis senilis Total no. species Total no. records Ecological Society, Mean no. species No. sites Journal of Applied Habitat     Ecology, 39, 8– 17 Multivari ate ordination showed strong separation of habitats according to species composition, with rocky ridge and alluvial plain habitats at the two extremes,
13 Occurrence Richness 0·25 8 Simplified ant assessment 0·2 6 Occurrence Richness 0·15 4 0·1 2 0·05 0 0 H M L B SO2 zone Fig. 1. Mean (+ SE) site occurrence and species richness of species at high (H), medium (M), low (L) and background (B) SO 2 zones. A mean occurrence of 0·1 means that on average each species occupied 10% of sites. Only those species occurring at > 2 sites (n = 26) were considered for occurrence. (a) Rhy tidopone ra sp. nr. cornuta (b) Rhy tidopone ra sp. nr. rufithorax 0·4 0·8 0·3 0·6 0·2 0·4 0·2 0·1 0 0 H M L B H M L B (d) Campono tus sp. A (denticula tus gp) (c) Iridomyrmex sp. nr. mayri 0·5 0·4 0·4 0·3 0·3 0·2 0·2 0·1 0·1 0 0 H M L B H M L B Occurrence (e) Camponotu s fieldae (f) Camponotu s sp. D (novaehollandia e gp) 0·8 0·4 0·6 0·3 0·4 0·2 0·2 0·1 0 0 H M L B H M L B (g) Campono tus sp. Q (discors gp) (f) Camponotu s sp. F (subnitidu s gp) 0·8 0·5 0·4 0·6 0·3 0·4 0·2 0·2 0·1 0 0 H M L B H M L B SO2 zone Fig. 2. Occurrence (proportion of sites occupied) of common species at high (H), medium (M), low (L) and background (B) SO2 zones. Table 3. Results of GLM tests of the effects of habitat type and SO2 zone on the occurrence of the eight most common species (those recorded from at least 15 sites). Data are P-values, with significant values indicated in bold Habitat type SO2 zone Rhytidoponera sp. nr. cornuta 0·02 0·08 Rhytidoponera sp. nr rufithorax 0·74 0·16 Iridomyrmex sp. nr. mayri 0·01 0·63 Camponotus sp. A (denticulatus gp) 0·41 0·001 Camponotus fieldae 0·05 0·02 Camponotus sp. D (novaehollandiae gp) 0·000 0·05 Camponotus sp. F (subnitidus gp) 0·56 0·15 Camponotus sp. Q (discors gp) 0·97 0·23 Journal of Applied Ecology, 39, and rocky plains intermediate (Fig. 4). This was sup- 8– 17 ported by a highly significant species–habitat inter- action in GLM (deviance = 174·84, d.f. = 80, P < 0·001). © 2002 British Simila rly, S O2 zone s were als o clea rly eviden t i n Ecological Society, ordination space (Fig. 4), and this was supported by a
highly significant Discussi species–zone on inte raction in GLM (deviance =          222·18, d.f. = 120, The intensive ant survey at Mt Isa, yielding 174 P < 0·001). species, documented seven clear responses of ant communities to variation in habitat and SO2 (Table 1). Our simplified
14 Eyrean Torresian 0·25 A.N. Andersen et al. 0·2 Occurrence 0·15 0·1 0·05 0 H M L B SO2 zone Fig. 3. Mean (+ SE) occurrence (proportion of sites occupied) of eyrean and torresian biogeographical groups at high (H), medium (M), low (L) and background (B) SO2 zones. 1·5 Axis 2 Species composition varied with SO2 1 Mult ivari ate ana lysi s o f ou r result s s howe d clear 0·5 position, including distinguishin g bet ween low and background zones. Axis 1 0 –1·5 –1 – 0·5 0 0·5 1 1·5 – 0·5 Several common species showed clear abundance –1 Th e species common ly recorded by our simplified stress = 0·2 – 1·5 protocol showed a wide range of responses to SO2. 8– 17 Fig. 4. Multivariate ordination based on occurrence of ant species from rocky ridge (triangles), rocky plain (circles) and alluvial plain (squares) habitats, located in background (open symbols), low (lightly shaded), medium (heavily shaded) and high (closed) SO2 zones. ant assessment protocol utilized the ant bycatch from routine vertebrate pitfall traps, with analysis restricted to the occurrence of larger species. It recorded 41 species, and required less than 10% of the effort demanded by the intensive ant sampling programme. How well did it reproduce the seven results of the intensive ant survey? Rocky ridge and alluvial plain habitats supported distinct ant faunas This was demonstrated by multivariate analysis of the results of our simplified protocol, where the two habi- tats were clearly separated in ordination space based on ant species composition. In addition, our simplified protocol indicated that a third habitat, rocky ridges, had intermediate species composition. Ant abundance declined with increasing SO2 Ou r s implifie d protoco l on ly conside re d s pecies presence/ absence, so we used mean occur rence as a s ur rog at e o f abundanc e. M ea n occur renc e sh owe d a significant decline with increasing SO2. © 2002 British Species richness declined with increasing SO2 Ecological Society, Journal of Applied Our simplified protocol reproduced this pattern, but Ecology, 39,
the variation was Only one species, Camponotus sp. A (denticulatus not quite gp), was common ly recorded in our study as well as statistically in the intensive survey, and in both cases abundance significant. clearly increased wit h increasing SO2. Non e of ou r other commo n species was recorded frequent ly enoug h in the intensive survey to detect their responses to SO2. Ant functional group composition showed relatively little change in relation to SO2 From the result s of ou r simplified protocol , the lack of a significan t functiona l group–zon e interaction indicated that functional group profiles were relatively uniform across SO2 zones. Ant responses varied according to biogeographical affinity As in the intensive survey, our results revealed that Eyrean and Torresian taxa showed systematic overall variation in relation to SO2, but that widespread taxa did not. In both cases there were marked declines in Torresian taxa with increasing SO2. The intensive survey showed marked increases in Eyrean taxa with inc reas- ing SO2, but this was only weakly evident in our data. In summar y, ou r simplifie d protoco l reproduced vir- tually all the key findings of the intensive survey. This was despite some differences in sampling design. Mo reover, the protoco l not on ly detecte d rather obvious environmental variation, such as between major habitat types, and emission impacts in the imme- diate vicinity of the smelter, but was sensitive to the effects of low SO2 levels up to 35 km away. Such effects
laboratory time required 15 on f aun a were un able to b e detecte d by intens ive vertebrate survey. Simplified ant assessment Our simplified ant assessment protocol was highly effective at Mt Isa, but how widely applicable are our results to other regions? The reliability of our protocol elsewhere depends on the suitability of the environ- ment for pitfall trapping, and the abundance and diver- sity of the resident ant fauna. Pitfall trapping is effective for sampling ants in relatively open environ- ments (Andersen 1991; 1997c) but becomes less effect- ive as the compl exity of the ground layer increases, and is relatively ineffective in habitats with dense leaf litter (Agosti et al. 2000). Our protocol also relies on a diverse and abundant ant fauna. As such it is ideally suited for Australia, where open habitats predominate and the ant fauna is exceptional ly diverse. We and our colleagues have used the protocol successfully to sample ant s throughou t inlan d Aust rali a (Woinarsk i et al. 2002). It is likely to be similarly effective in arid lands and the seasonal tropics throughout the world. On the other hand, it would be less effective in cool– tempe rate zones, where ant diversity is relatively low and most of the abundant and speciose genera are relatively small sized (e.g. Formica, Lasius and Leptothorax through- out the Holarctic; Creighton 1950; Bolton 1995). In these regions, the body size threshold of 4 mm would have to be reduced in order to cover sufficient numbers of species.          Many authors have discussed the ideal attributes of an indicator group for assessing ecol ogical change, and ants routinely perform well against these criteria (Majer 1983; Greenslade & Greenslade 1984; Brown 1997). Many of the attributes directly address a taxon’s ability to reflect general ecol ogical change, and relate to their abundanc e, diversity, functional importance and sens- itivity to disturbanc e. Ants clearly meet these criteria, especial ly in Aust rali a (Anderse n 1990) . Howev er, it is also recognized that cost s and logistic const raints are important variables in the design of monitoring programmes (Spellerberg 1991). Ants also perform rel- atively well in this cont ext. For exampl e, Brown (1997) scored 21 potential insect indicator taxa in the neo- tropic s according to a variet y of attributes relating primarily to their practicality of use, and ants rated equal highest, scoring 19 out of a possible 20 points. Nevertheless, ants still pos e formidable challenges for workers who are inexperienced with insect surveys. The simplified ant assessment protocol we have tested here overcomes many of these challenges. First, it is readily incorporated into routine wildlife surveys, © 2002 British such that ants can be reliably assessed without speci- Ecological Society, fically sampling for them. Alternatively, if Journal of Applied Ecology, 39, vertebrate trapping is not being conducted, it is 8– 17 simple to install pitfall traps specifically for ants, as this takes only a few minutes per trap. Secondly, by considering only a sub- set of species it greatly reduces
Our sampling protocol has parallels with the for the processing con- cept of ‘taxonomic sufficiency’ (Ellis 1985), and sorting of which addresses the level of taxonomic resolution specimens. Most at which samples are most efficiently sorted and ant species are analysed. Both approaches focus on the resolution relatively small required to satisfy the object ives of the monitoring (< 4 mm), so or assessment pro- gramme, as opposed to what is most species required for a compre- hensive description of the were ignored by taxa under investigation. Given that they comprise our protocol. a single taxonomic fami ly, the question of Thirdly, large taxonomic sufficiency for ants is one of genus-level species are far analysis. Analysis of ant community data at genus easier to sort level can often reproduce species-level patterns into (Andersen 1997b; Pik, Oliver & Beattie 1999), but morphospecies the reliability of genus as a surrogate for species in than are small ants can vary widely between regions (Andersen species. 1997a). Our protocol has the advantages of species- Throughout the level precision, and achieves efficiency through world, small- ‘sampling sufficiency’. sized taxa (such as the myrmicine  genera Pheidole, Crematogaster, For 20 years scientists have been promoting the use Monomorium, of terrestrial invertebrates as bioindic ators, but such Leptothorax and use still largely remains a topic discussed by Strumigenys) are scientists rather than a practice embraced by land typic- ally the managers. In the scientific arena, attention has most demanding focused on identifying the mos t reli able indic ator ants taxon . Howev er, the actual use of invertebrates taxonomical ly, by land man agers is not limited by scientific and require uncertainty over which taxon might give the most considerable precise results. Rather, it is limited by gen- eral experience for unfamiliarity and inexperience with dealing with them to be insects. The truth is that a number of reliably sorted to functional ly important invertebrate groups can species level. provide valuable information on ecol ogical change Most large associ ated with land use. We suggest that research species can be directed at making these groups accessible to land suc- cessfully man agers deserves higher priority than does sorted with only further assessment of the relative merits of limited different candidate taxa. Once invertebrate experience, such bioindicators become engrained in land- that a focus on management culture, then it would be appropriate to large species focus attention on what might be the ‘best’ indicator makes ants taxon. accessible to a The main finding of our study does not really con- wide range of cern the details of our simplified sampling users. Finally, protocol. these efficiencies mean that a greater number of sites can be surveyed. Despite taking only about 10% of the effort, in this study our protocol was able to sample 65 sites compa red with 40 for the intensive survey.
16 Rather, it is the fact that comprehensive sampling was not required to reveal compl ex ant A.N. Andersen community responses to land use. Our study has et al. shown that a rel- atively few taxonomically tractable ants can say a lot about the environment in which they occur, and con- siderably more than could traditional wildlife (verte- brate) surveys. This is not to decry the need for detailed studie s of ant s or othe r invert ebrate group s as part of research into ecol ogical response s to land use. However, the requirements of such research should not be confused with those of routine monitoring pro- gramme s, where the focus is not on the target groups per se, but on using them to provide information on the broader environment. The main issue in environmental monitoring is not whether or not samples are compre- hensive, but whether they are reliable, and we have shown that simplified ant sampling can provide reliable results. Acknowledgements We thank Brandon Bestelmeyer, Jonathan Majer, John Woinarski and Rochelle Lawson for their helpful com- ments on the draft manuscript. This is CSIRO’s Trop- ical Ecosystems Research Centre publication number 1170. References Agosti, D., Majer, J.D., Alonso, L.E. & Schultz, T.R. (2000) Ants: Standard Methods for Measuring and Monitoring Biodiversity. Smithsonian Institution Press, Washington, DC. Andersen , A .N. ( 1990) The us e of a nt c ommunities t o evaluate change in Australian terrestrial ecosystems: a review and a recipe. Proceedings of the Ecological Society of Australia, 16, 347– 357. Andersen, A.N. (1991) Sampling communities of ground- foraging ants: pitfall catches compared with quadrat counts in an Australian tropical savanna. Australian Journal of Ecology, 16, 273 –279. Andersen, A.N. (1993) Ants as indicators of restoration success at a uranium mine in tropical Australia. Restoration Ecology, 1, 156 –167. Andersen, A.N. (1995) A classification of Australian ant com- munities, based on functional groups which parallel plant life-forms in relation to stress and disturbance. Journal of Biogeography, 22, 15 – 29. Andersen, A.N. (1997a) Using ants as bioindicators: multiscale issues in ant community ecology. Conservation Ecology [Online], 1, 8. Andersen, A.N. (1997b) Ants as indicators of ecosystem restoration following mining: a functional group approach. Conservation Outside Nature Reserves (eds P. Hale & D. Lamb), pp. 319 – 325. Centre For Conservation Biology, The Uni- versity of Queensland, Brisbane, Australia. Andersen, A.N. (1997c) Functional groups and patterns of organization in North American ant communities: a comparison with Australia. Journal of Biogeography, 24, © 2002 British 433 – 460. Ecological Society, Andersen, A.N. (1999) My bioindicator or yours? Making the Journal of Applied selection. Journal of Insect Conservation, 3, 1– 4. Ecology, 39, Andersen, A.N. (2000) The Ants of Northern Australia: A Guide 8– 17 to the Monsoonal Fauna. CSIRO Publishing, Collingwood, Australia. Andersen, A.N. & Sparling, G.P. (1997) Ants as indicators
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