Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions

Carabid beetles as useful model organisms, indicators, or both? 287 Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions Matti J. Koivula Finnish Forest Research Institute, Vantaa Research Unit, P.O. Box 18, FI-01301 Vantaa, Finland Corresponding author: Matti J. Koivula ([email protected]) Academic editor: D.J. Kotze |Received 27 Novenber 2009|Accepted 7 July 2010|Published 20 May2011 Citation: Koivula MJ (2011) Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions. In: Kotze DJ, Assmann T, Noordijk J, Turin H, Vermeulen R (Eds) Carabid Beetles as Bioindicators: Biogeographical, Ecological and Environmental Studies. ZooKeys 100: 287–317. doi: 10.3897/ zookeys.100.1533 Abstract Classic studies have successfully linked single-species abundances, life-history traits, assemblage structures and biomass of carabid beetles to past and present, human-caused environmental impacts and variation in ‘natural’ conditions. This evidence has led many to suggest carabids to function as ‘indicators’ − a term that bears multiple meanings. Here, a conservation-oriented definition for an indicator is used, carabid indicator potential from seven views is evaluated, and ways to proceed in indicator research are discussed. (1) Carabid species richness poorly indicates the richness and abundance of other taxa, which underlines the importance of using multiple taxa in environmental assessments. The ability of assemblage indices and specialist or functional-group abundances to reflect rare species and habitats should be examined in detail. (2) Experimental evidence suggests that carabids may potentially serve as keystone indicators. (3) Carabids are sensitive to human-altered abiotic conditions, such as pesticide use in agro-ecosystems and heavy metal contamination of soils. Carabids might thus reflect ecological sustainability and ‘ecosystem health’. (4) Carabid assemblages host abundant species characteristic of particular habitat types or successional stages, which makes them promising dominance indicators. (5) Carabids reflect variation in ‘natural’ conditions, but vegetation and structural features are more commonly adopted as condition indicators. Carabids nevertheless provide yet another, equally accurate, view on the structure of the environment. (6) Carabids may function as early-warning signalers, as suggested by recent studies linking climate and carabid distributions. (7) Carabids reflect natural and human-caused disturbances and management, but the usefulness of these responses for conservation purposes requires further research. In summary, European carabids appear useful model organisms and possibly indicators because they are diverse, taxonomically and ecologically well-known, efficiently reflect biotic and abiotic conditions, are relevant at multiple spatial scales, and are easy to collect in sufficiently large numbers to allow statistical analyses. The assumption ZooKeys 100: 287–317 (2011) doi: 10.3897/zookeys.100.1533 www.zookeys.org Copyright M.J. Koivula. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. ReseARCh ARtiCle Launched to accelerate biodiversity research A peer-reviewed open-access journal Matti J. Koivula / ZooKeys 100: 287–317 (2011) 288 that carabid responses would reflect rare environmental conditions or the responses of rare and threatened species ‒ crucial information for conservationists and managers ‒ has not yet been critically evaluated. Even if it holds, the usefulness will be context dependent: species and their populations vary, conditions vary, questions put forward vary, and assessment goals vary. Keywords abiotic, assessment, bioindicator, biotic, change, conservation, disturbance, dominance, early warning, human impact, keystone, management, richness introduction Indicators, in the most general sense, can refer to anything that have been shown to reflect something apart from their individualistic response. For example, different species reflect habitat types through their associations with particular biotic and abiotic conditions, and a common assumption is that the magnitude and direction of this reflection are not unique to the studied species. For conservationists and environmental managers, i.e., the potential end users of indicators, such general patterns will not suffice. For them, an indicator should permit conclusions regarding particular conditions or biodiversity, which could not otherwise be concluded either without using the indicator or through using easier, cheaper and/or quicker assessment tools. Indeed, Landres et al. (1988) described an indicator as being a taxon or a structure ”…whose characteristics (e.g., presence or absence, population density, dispersion, reproductive success) are used as an index of attributes too difficult, inconvenient, or expensive to measure for other species or environmental conditions of interest“. Here I use the term ‘indicator’ following this strict definition unless stated otherwise. In ecological impact studies carabid beetles are frequently cited as indicators in the vague sense described above, but according to the strict sense they should more often be cited as model or study organisms. A model organism is a (group of) species that is used to examine a particular study question (a hypothesis) under a research programme (sensu Underwood 1997; see also den Boer 2002). For example, the researcher’s general question might be ”Does fungicide spraying affect soil-dwelling animals?” which is then studied using carabids to model a biological response. If you type the words ’carab*‘ and ’indicator*‘ into Scopus you get 172 results, and similarly ISI Web of Science produces 186 results (26 May 2010). Many if not most of these studies have little to do with carabids indicating anything else but themselves, i.e., their individualistic response to treatments of interest, except perhaps trivial issues such as the sampled habitat type. Such ‘watering down’ of terms may lead to misunderstandings among scientists, practitioners and amateurs, including the media, and to an impoverishment of the scientific language. Here I evaluate the indicator potential of carabid beetles for seven common applications of indicators (Lindenmayer et al. 2000): (1) indicating richness and abundance of taxa other than carabids; (2) functioning as keystone organisms; (3) indicating hu- Carabid beetles as useful model organisms, indicators, or both? 289 man-altered abiotic conditions, here pollution; (4) indicating particular environmental conditions through numerical or biomass dominance; (5) reflecting variation in ‘natural’ conditions; (6) acting as early-warning signalers; and (7) indicating disturbances and management. Generally speaking, the basic requirements for the use of indicators are fulfilled by most European carabids: good knowledge exists on (i) conditions to which these species are adapted to; (ii) distributions of the species in a given set of patches; (iii) the species’ responses to environmental variation/alteration; and (iv) variation in the species’ population dynamics (Andersen 1999; Lindenmayer et al. 2000; see "Carabids as model organisms" below). In this review I ask three questions with a combined European and North American focus. Which features characterize carabids as potential indicators? In "Carabids as model organisms" I briefly review the current state of ecological knowledge, information gaps, and methods used in carabid research. What kinds of indicators might be found among carabids, considering the seven indicator categories above? In other words, what is the evidence for and against using carabids as indicators? In "Evaluation of carabids as indicators" my aim is to summarize key evidence for carabid indicator potential. This Section is intentionally critical, as the use of indicators in conservation should be on an exceptionally solid basis: threatened species or habitats are at stake. Where, and how, should carabidologists proceed in their search for indicators? In "Identifying and using carabid indicators" I discuss (a) ways to incorporate carabids into routine environmental assessments, (b) issues about carrying out research searching for indicators, and (c) where to find new areas in the ongoing indicator hunt. Carabids as model organisms Prerequisites for being good model organisms and also potential indicators include vast knowledge on carabid taxonomy and ecology, as well as ease of collecting, but these hold mostly only for north-temperate regions (e.g., New 1998). Carabids are taxonomically well known, with relatively stable systematics, and their ecology has been widely studied (Lövei and Sunderland 1996). Variation in carabid morphology, life-history strategies and abiotic and biotic requirements are also extensively documented. We know, for example, many species that are specialized to certain moisture, temperature and shadiness conditions (Rainio and Niemelä 2003; Niemelä et al. 2007). Carabids are also widely distributed, from the arctic and alpine tundra to seashores, deserts and tropical rainforests, and they can be common in these environments (Lövei and Sunderland 1996). However, knowledge about basic life-history parameters appears limited to a few well-studied species. These parameters include birth and death rates, population age structure and growth rate, resource allocation between reproduction and growth, and the causes and magnitude of variation in Matti J. Koivula / ZooKeys 100: 287–317 (2011) 290 these. Such parameters are not only interesting but may appear crucial for indicator use (see "Identifying and using carabid indicators"). The reasons for particular distributions, local abundances or behavioral responses of carabids are generally well understood. Carabids are influenced by temperature, moisture and shade (Thiele 1977), food quality and abundance (Lenski 1984; Van Dijk 1994; Bilde and Toft 1998; Bilde et al. 2000; Bohan et al. 2001), habitat structure as reflected by the vegetation (Rykken et al. 1997; Siemann et al. 1998; Brose 2003; Koivula et al. 1999; 2003; Taboada et al. 2008), and substrate salts, sugars and acidity (Merivee et al. 2001, 2004, 2006; Milius et al. 2006). Moreover, seasonal and life-history fluctuations strongly affect observed abundances and distributions (Thiele 1977; Lindroth 1985, 1986; Lövei and Sunderland 1996). Of largely unknown − though often suggested − importance are intraand interspecific interactions, of which competition has usually had minor effects (Loreau 1990; Niemelä and Spence 1991; Niemelä 1993a; Currie et al. 1996; Zetto Brandmayr et al. 2004). In ecological research, both landscape and smaller scales appear relevant for carabids, although the former usually requires extensive sampling. Carabids are not always considered relevant at spatial scales larger than a few hectares (e.g., Pearce and Venier 2006). This view relies on the idea of local populations or ‘home ranges’ of carabids (e.g., den Boer 1990a; Gaston and Blackburn 1996; Charrier et al. 1997). However, carabids predictably respond to landscape- (here, areas larger than 50 ha) and even continent-level phenomena (e.g., Hengeveld 1987; Kotze and O’Hara 2003; Kotze et al. 2003). For example, carabids reflected isolation in southern Finnish farmlands (Kinnunen et al. 1996), and responded to patch size and matrix type in an urban landscape in Belgium (Gaublomme et al. 2008). The structural heterogeneity of landscapes had variable impacts on different trophic groups of carabids in Germany (Purtauf et al. 2005). Moreover, carabid assemblages gradually changed across a forest/farmland gradient in Scotland (Vanbergen et al. 2005), and in Canadian post-fire forests, logging variably affected carabids at the stand level but strongly and predictably at the landscape scale (Koivula and Spence 2006). Most field studies on carabids have used pitfall traps, which is an easy and cheap method to collect sufficiently large samples to allow statistical analysis, by acknowledging that the catch indicates species-specific ‘activity density’ rather than true relative abundance (Greenslade 1964). The dominance of one method over others introduces a knowledge bias. New insights would be achieved by more often applying other collecting methods, such as capture-mark-recapture techniques, trapping and measuring live beetles, window trapping, tree-canopy pesticide spraying, hand collecting, and soil sampling to collect larvae (Sutherland 1996). The carabid beetle literature reflects a wide spectrum of approaches to study ecological questions. Papers on single species, total abundance and species richness are common. If the numbers of collected individuals are small, or if generalizations are required, carabids are often divided into functional groups to test the hypotheses put forward. These groups include seasonal abundance peak, reproduction period, diurnal activity, body size, wing morphology (e.g., brachypterous/wing-dimorphic/long-winged/ Carabid beetles as useful model organisms, indicators, or both? 291 flying), food preferences (e.g., predator/omnivore/plant-eater/specialist), associations with habitat openness (e.g., closed tree canopy or extensive vegetation cover/generalist/ open phase) and moisture preferences (e.g., dry/moist/wet). Clearly, species divisions into these groups involve subjectivity, because many categories were originally continuous variables, and may be poorly known even in regions with a long research tradition. Flight capability in carabids in Northern and Central Europe is a good example of such knowledge gaps (Niemelä et al. 2007). Morphospecies or higher-than-species level approaches are rarely applied by carabidologists, because different species within a genus are ecologically different and may consequently respond differently to the environment (Koivula et al. 2006; Langor and Spence 2006). Various diversity indices have been used on the carabid catch. These include, for example, rarefaction (Sanders 1968) and the Shannon-Wiener and Simpson indices (Magurran 2003; Tóthmérész and Magura 2005a). However, diversity indices may perform inconsistently (O’Hara 2005) and therefore should not be used as a sole justification of indicator functioning. Another obstacle is that diversity measures based on pitfall-trap data are problematic because the samples are biased toward actively moving, large-sized species (e.g., Morrill et al. 1990; Lang 2000). As such, these samples may have little to do with true assemblage composition and structure. The relationship between trap samples and true assemblages is poorly understood due to the difficulty in reliably determining the latter. Recent approaches to describe carabid assemblage structure include Mean Individual Biomass (Szyszko et al. 2000; see "Dominance indicators"), affinity indices (Allegro and Sciaky 2003; Tóthmérész and Magura 2005b) and indicator value calculations (IndVal; Dufrêne and Legendre 1997). Affinity indices aim at removing the effect of differences in species abundances among compared habitat types while simultaneously accounting for the species’ habitat specificity (Magura et al. 2006a). The IndVal approach uses data collected from habitat types of interest, and identifies species characteristic of particular habitat types based on their abundances and presences/absences among all samples (Dufrêne and Legendre 1997). evaluation of carabids as indicators Taxon indicators The presence of a taxon indicator reflects the presence of a set of other species, and its absence indicates the absence of the entire set of species (Slobodkin et al. 1980; Lindenmayer et al. 2000). The underlying assumption thus is that the presence of a limited subset of all species would indicate the presence of the complete set. As everything cannot be measured this approach may sound appealing, but evidence of carabids as taxon indicators is poor. Weak richness correlations with carabids have been demonstrated for spiders (Rushton et al. 1989; Niemelä et al. 1996) and some other invertebrate taxa (Duelli and Obrist 1998; Niemelä and Baur 1998). Barbaro et Matti J. Koivula / ZooKeys 100: 287–317 (2011) 292 al. (2005) found that the same structural features of forests predicted bird, spider and carabid richness in France. The utility of richness indicators becomes even more challenging at larger spatial scales, where richness correlations appear to be a biogeographic rule. Species richness of different taxa often correlate because of the general tendency of richness to increase toward the equator (Begon et al. 1996); for a national-scale invertebrate example, see Väisänen and Heliövaara (1994). The taxon indicator potential of carabid beetles has not yet been subject to a severe test (sensu Mayo 1997), but such tests do exist for other taxa. Jonsson and Jonsell (1999) showed that stand structure and the richness of taxa bearing high conservation relevance (lichens, plants, wood-rotting fungi and bryophytes) appeared to be poor a priori indicators of each other in Swedish boreal forests. Likewise, Similä et al. (2006) found that structural characteristics and plant richness somewhat reflected the richness of some invertebrate groups, but beetles very poorly reflected the richness of other taxa in Finnish boreal forests. Moreover, Sætersdal et al. (2005) showed that the degree of overlap in richness among six ecological groups, consisting of polypores, bryophytes and lichens, varied considerably from site to site in Norwegian coniferous forests. While discouraging, these results highlight the importance of using multiple taxa in environmental assessments (cf. Taylor and Doran 2001; Duelli and Obrist 2003; Paillet et al. 2009) and the absurdity of the idea of the existence of a single ‘biodiversity indicator’. Conservationists and managers generally agree in that protecting species diversity is a priority at global and national scales. At smaller spatial scales, however, richness may appear a misleading conservation measure without considering species identities. For example, Koivula and Spence (2006) showed that, in recently burned Canadian forests, logging increased the total richness of carabids due to the colonization of generalist open-area associated species. But simultaneously most closed-forest species decreased in abundance, the most drastic case being the over tenfold decrease of Calosoma frigidum, a tree-canopy caterpillar hunter (Larochelle and Larivière 2003). So, at the operational scale of individual forest stands, should the forest manager adopt the message obtained from total richness or that from species requiring closed forests? Keystone indicators A keystone indicator is a species, a group of species, or a structure that affects its environment and therefore other species disproportionately strongly relative to its abundance (Mills et al. 1993). The lack of a keystone indicator would thus lead to major changes in some other species’ occurrence, abundance and/or distribution. A classic example from forested environments is the woodpecker fauna (Virkkala 2006). These birds produce nesting sites for secondary cavity-nesters, are important vectors for wood-rotting fungi, and may even regulate bark beetle infestations, thus bearing economic importance (Fayt et al. 2004). Carabids have intrinsic biodiversity value and unknown future potential, and they can also be considered invaluable on an ethical basis, but can they serve as keystone indicators? Carabid beetles as useful model organisms, indicators, or both? 293 Evidence on the importance of carabids comes from agro-ecosystems, greenhouses and laboratories. Under laboratory conditions carabids forage efficiently on slugs and eggs, pupae, larvae and adults of pest insects (Kromp 1999). In the field, carabids indeed prey on pest invertebrates, such as slugs, aphids and mites (e.g., Allen 1979; Edwards et al. 1979; Hengeveld 1980a, 1980b; Luff 1987; Sopp et al. 1992; Bohan et al. 2001). Menalled et al. (1999) manipulated onion fly (Delia antiqua) pupae using exclosures in corn fields and found a positive relationship between carabid abundance and pupal death rates. But can the rates of foraging in the field be ecologically and/or economically important? Hance (1987) used 1 m2 enclosures with sugar beet and natural densities of aphids feeding on these plants, and released 0–30 individuals of Anchomenus dorsale and Asaphidion flavipes into these enclosures. Such densities (up to 30 ind.m-2) are common in the field (Lövei and Sunderland 1996). In enclosures without carabids, the density of aphids increased exponentially. At intermediate carabid densities, the aphid increase was delayed, and at high carabid densities the aphids often did not increase at all. It is easy to argue that this is ecologically and economically important, contrary to some ‘statistically significant’ 20–30% abundance changes. While this experiment can be criticized for using unrealistic, closed miniature systems, it shows that carabids have the potential for being economically important. Carabids thus have the potential, but lack field-based evidence, for truly functioning as keystone indicators. Are carabids necessary for ecosystem functioning, and even if they are, could other taxa replace them if they are removed from an ecosystem? Currently there are no answers to these questions, but in many ecosystems carabids are accompanied by other abundant generalist invertebrates, such as ants, staphylinid beetles and spiders (Turnbull 1973; Bohac 1999). Carabids are, on average, larger than these three, which suggests a higher trophic level and per capita effect on, for example, crop-pest invertebrates. On the other hand, carabids are often vastly outnumbered or even excluded by Formica wood ants in Fennoscandian boreal forests (e.g., Koivula et al. 1999). Pollution indicators Pollution indicators reflect human-altered abiotic conditions in the soil, water and the air (Spellerberg 1994). Urban ecological studies might be considered in this category, with the combined role of e.g. pollutants, soil compaction and the ‘heat island’ effect (Forman 2008; Marzluff et al. 2008). Pollution affects humans directly, and as such has been studied widely for several decades using several taxa, of which lichens may be the most famous (Lindenmayer et al. 2000). Other pollution indicators, too, have been proposed but not without problems. For example, the mollusc Velesunio ambiguus was long considered an excellent indicator of heavy metals in aquatic systems until it appeared that this species’ uptake of metals did not reflect the extent of pollution (Lindenmayer et al. 2000). Matti J. Koivula / ZooKeys 100: 287–317 (2011) 294 Carabids have been commonly studied to evaluate the ecological effects of industry emissions and agriculture chemicals. The below examples demonstrate the potential for carabids to also act as indicators of ecologically sustainable farming, environmental recovery and ‘ecosystem health’. The utility of carabids as indicators in these cases relies on the inadequately tested assumption that other, often more severely threatened, taxa similarly respond to these pollutants and chemicals. This issue concerns the other indicator categories as well. Several case studies all suggest that heavy metals in the soil significantly and negatively affect carabids (e.g., Ermakov 2004; Gongalsky et al. 2004; Belskaya and Zinoviev 2007). Moreover, cadmium and zink affect the growth and body caloric value of Poecilus cupreus individuals (Maryański et al. 2002). Carabids have also been used to assess the recovery of ecosystems after pollution events (e.g., Schwerk et al. 2006; Cárdenas and Hidalgo 2007). In agro-ecosystems, pesticide and fertilizer impacts on carabids have been studied (e.g., Dritschilo and Erwin 1982; Basedow 1990; Kromp 1990; Larsen et al. 1996; Bourassa et al. 2008). Carabids respond negatively to dimethoate (commonly-used pesticide) sprayings but their numbers may recover within a few weeks (Huusela-Veistola 1996). Fertilizer and herbicide impacts have often been minor, but may affect carabids indirectly through changes in the vegetation (Kromp 1999). Also cumulative impacts may appear common. For example, the intensity of carabid response to pollutants and chemicals depends on additional stressors, such as food scarcity and chemicals. Stone et al. (2001) studied adults of Pterostichus oblongopunctatus at a chronically polluted mining area in Poland. They collected individuals at sites with different levels of soil metals and subjected these beetles to food shortages and an insecticide (dimethoate) in the laboratory. Carabid death rates, caused by these stressors, were higher the more severely the collecting site had been contaminated by metals. To determine whether these responses were genetically based or resulted directly from soil contamination, Lagisz and Laskowski (2007) collected additional individuals at Stone et al.‘s (2001) sites, and reared a second generation in the laboratory. These laboratory specimens were subjected to food shortages and the same insecticide, and results showed that the collecting site of the parent individuals had no effect on death rates of the second generation. Thus, the interaction was not genetically based in this case. Recent advances in agro-ecosystems concern gene-manipulated (GM) or transgenic plants that can be considered ‘genetic pollutants’, as evidenced by the hybridization of native and GM corn in Mexico (Quist and Chapela 2000). GM techniques have been rapidly adopted into agriculture to increase the crop plants’ pest and disease tolerance, yield and/or nutritional value, but manipulating the genetic material of these plants is suspected to lead to unwanted consequences (e.g., Dunwell 1999). For example, the use of GM plants might directly or indirectly affect non-target organisms, including carabids. Non-target invertebrates were generally little affected by GM corn and cotton, as compared with non-transgenic versions of these plants, but were more affected by the use of pesticides (Marvier et al. 2007). Similarly, GM crops had a minor effect on adult carabids locally (Lopez et al. 2005; Szekeres et al. 2006; Floate et Carabid beetles as useful model organisms, indicators, or both? 295 al. 2007). However, Waltz (2009) summarized the effects of GM crops on insects and reported drastic effects on, e.g., butterfly larval death rates. Hence, experiments on the larval development of seed-eating carabids in GM and conventional crop fields would significantly contribute to this area of research. Dominance indicators Dominance indicators make up much of the total biomass or the number of individuals in an area of interest (Lindenmayer et al. 2000) and predict particular ecosystems or assemblages. For example, certain tree species form much of the biomass and broadly reflect habitat type in forests. Similarly, carabid dominance indicators should reflect particular habitat types, degrees of disturbance and ecosystem recovery, hot-spots of rare species or particular habitat types of conservation interest. The use of carabids in this sense has faced certain difficulties that might be overcome. Invertebrates are seldom used in environmental assessments because of the high expertise required (Andersen 1999; but see Andersen and Majer 2004). While strongly advocated here (see "Carabids as model organisms"), species-level approaches usually require considerable investments of expertise, time and money into education, sampling and analysis (Langor and Spence 2006). Hence, in rapid biodiversity assessments (e.g., Ward and Larivière 2004), numerical or biomass dominance might be alternative options. Niemelä (1993b) showed that boreal-forest carabid assemblages consist of a few abundant (easily identifiable) and several scarce (often more difficult to identify) species. In these forests, early successional phases can be numerically dominated by Pterostichus niger, while closed phases are often dominated by Calathus micropterus (e.g., Koivula et al. 2002). However, as these species are generalists of forest succession (Niemelä et al. 2007) and occur in many forest types (Lindroth 1985, 1986), their presence may not indicate aspects useful for conservation or management. Carabid body size has been linked to certain ecological processes, such as urbanization and succession (e.g., Magura et al. 2006b). The Mean Individual Biomass (MIB) approach requires only sampling, counting, weighing and using a simple equation developed by Szyszko et al. (2000). MIB is predicted to increase along gradual successional changes in vegetation that subsequently alters the carabid fauna, from smaller open-habitat (Amara, Bembidion, etc.) to larger closed-forest (Carabus, Cychrus, etc.) species (Szyszko et al. 2000). An increase in MIB should thus indicate conditions approaching late successional stages. MIB is advocated as an easy tool for policy makers to assess the state of the environment. The method assumes a linear relationship between MIB and time since disturbance, which seems to hold through early successional phases, during which the carabid fauna changes rapidly (Szyszko et al. 2000; Koivula et al. 2002). However, at least in boreal spruce forests the carabid assemblage structure − and consequently MIB − changes little between 30 and 100 years following clear-cutting (Koivula et al. 2002; M. Koivula unpubl.), suggesting a plateau in the trend. For forests older than Matti J. Koivula / ZooKeys 100: 287–317 (2011) 302 Assume you are interested in the impact of a fertilizer on meadow biodiversity, and you would like to study if carabids respond to the added fertilizer as an early warning indicator, i.e., before it can be detected by inventorying plants. You might have a reason for expecting some carabid species to be able to do so (see Merivee et al. 2006). You decide to explore slight differences in assemblage composition using pitfall traps. The study can be done by sampling, for example, (i) several treated (fertilizer added) and untreated (no fertilizer added; control), randomly-assigned sub-plots within one or a few meadows. Such a protocol would be suitable for detecting small-scale phenomena, such as variation within meadows; (ii) several (say >10) meadows treated with different levels of the fertilizer. This protocol might be fine for assessing threshold conditions by using non-linear regression modeling to evaluate, e.g., if the threshold of abundance change occurs earlier for carabids than for plants; (iii) multiple meadow pairs of which one is treated and the other is not; or (iv) separate, treated and untreated meadows (see, e.g., Underwood 1997). Assume that you end up using the last-mentioned option. A convincing demonstration of your case would require at least the following. a. Select meadows that are initially as similar as possible but still distinctive. b. Establish at least 3–4 treated and 3–4 untreated meadows to be able to calculate means and variances for both. The more meadows the better, as more natural variation will be covered and the more precise the estimate of mean. If possible, sample before and after the addition of the fertilizer to better account for initial variation (Underwood 1992). Concerning your study question, these meadows (not traps in them, irrespective of how they are placed) are your replicates: you are interested in a phenomenon that scales to variation between meadows. c. Spatially distribute your replicates evenly. They should not form treatment-specific clusters. d. The replicates should be separate, i.e., unlikely to affect each other ecologically. Sections of different habitat types between your study meadows help convince your colleagues that the meadows are indeed ecologically independent from each other. e. Synchronize the sampling, i.e., sample at every meadow over the same period. f. Collect multiple samples from each meadow (see point 5 above). g. Sample over a period long enough to representatively collect carabids, and also to see if the plant assemblage responds to the treatment. If the plants, or any other taxa other than carabids, do not respond to the treatment, you have failed to find an early warning indicator, whatever your result for carabids. The follow-up may easily take several years to produce useful information. A lack of proper replication is surprisingly common in ecology, considering the amount of literature on this issue. In the above example, you might have selected only one treated and one untreated meadow and set 10 traps in each, perhaps 15–20 m apart for sample independence (Digweed et al. 1995). But you would then have no replication Carabid beetles as useful model organisms, indicators, or both? 303 for the factor of interest, viz. the addition of fertilizer, which operated at the meadow scale. As a solution you might treat each trap as a replicate in your analysis, but you would then introduce pseudo-replication because samples from a given meadow are inter-dependent through ecological interactions between the plots with traps (Hurlbert 1984). Likewise, in a laboratory experiment with two cages (control and treatment), you might consider each individual in a cage a replicate, but you would have difficulty to convince others that it was not some characteristic of the cage that produced the result. Another example is to use spatially clumped treatments: here, clusters of meadows with similar treatment. Now, underlying environmental gradients or local conditions could drive the result, not necessarily the fertilizer addition. Similarly, you should not compare moist Dutch meadows with dry Belgian meadows if your aim is to study the effect of moisture on carabids. The only exceptions for not properly replicating treatments concern studies on exceptionally rare (or dangerous) taxa, habitat types or phenomena. Suggestions for further research Carabidologists have much to contribute to indicator studies. First of all, the researcher must adopt the conservationists’ view on what is an indicator. Second, the research must be properly carried out (see "Indicator hunt: common sense revisited"). Third, if the results suggest that carabids reliably reflect variation of high conservation relevance, the researcher should describe (i) the variables of the assemblage that best reflect this variation, (ii) the study conditions (context), (iii) the precision and accuracy of carabids in reflecting this variation based on, e.g., percent overlap, peak difference and confidence intervals, and (iv) the species or conditions that could not be easily observed without using carabids. Fourth, as the carabid ecological literature is vast (see "Carabids as model organisms"), and to increase the power of analyses, carabidologists should move on from twotailed null hypothesis testing toward routinely formulating explicit, directional hypotheses − not just in indicator research but in modeling biological phenomena in general. The various indicator categories ("Evaluation of carabids as indicators") provide potential for developing powerful management and conservation tools. Taxon, pollution, environmental and management indicators might be found by moving on from applying total richness toward using single-species abundances or their morphological/ genetic variation, groups of specialists, functional groups, or structural characteristics of assemblages (as reflected by, e.g., affinity indices; Magura et al. 2006a; Déri et al. 2010). A different way to approach the indicator issue might be to study if the presence of certain species would indicate the lack of conservation values at a given site (‘negative indicators’). Keystone indicators, on the other hand, might be found through experiments with multiple trophic levels and manipulated abundances of potential competitors. Early warning indicators are trendy because of their potential in assessing largescale environmental alterations, but the concept could also be examined through ecological interactions and at smaller spatial scales. For example, responses of carabids to Matti J. Koivula / ZooKeys 100: 287–317 (2011) 304 changes in combinations of temperature, soil chemistry and/or expansion of urban areas may be fruitful (see Knowlton and Graham 2010). The micro scale appears equally promising: carabids are physiologically extremely sensitive to sugars, salts, amino acids, pH and temperature (Merivee et al. 2004, 2005, 2008; Must et al. 2006). Thus, physiological alterations due to changes in these factors might function as early warning signals of currently minor environmental variation, such that cannot be observed by visual inspection of the environment. Some of these aspects could also be explored using affinity indices. Conclusions No two species can precisely reflect each other, and one must be prepared for uncertainty and error when using an indicator. The competitive exclusion principle (Hardin 1960) postulates that members of a guild must be ecologically at least slightly different from one another to co-occur in terms of e.g. population dynamics, habitat and foraging requirements, aspects of reproduction and environmental grain size. Defining acceptable imprecision is a political question, but research can only determine confidence limits. Indicators are assessment tools intended to be used in situations when habitats and species are lost, or conditions altered. Because humans will continue to utilizing the environment, some decrease in habitat area and, at some locations, quality is inevitable: biology competes with economics and social issues in policy. Detecting areas or sites of high conservation value assists in defining conservation priorities. Still, the conservationist may have to ask whether her/his statistically significant result is biologically or economically important, or whether a non-significant result is irrelevant. For example, if threatened or rare species are involved, the precautionary principle should apply (e.g., Haag and Kaupenjohann 2001): if a particular environmental impact is under evaluation, statistical non-significance should not be considered equal to no effect or zero difference (McGarvey 2007), and an indicator should be allowed to provide occasional ‘false positives’. The latter is important in protecting metapopulations, with both occupied and presently unoccupied habitat patches being necessary for the long-term persistence of an organism (Hanski 1999). Likewise, within a given area, local populations of carabids may differ in their reproductive capacity and other qualities, and consequently fluctuate partly independently (e.g., den Boer 2002). To be useful in conservation, an indicator must have high and consistent predictive power that relates to particular conditions and/or rare species. We still lack the first clear-cut case showing carabids to reliably predict entities of high conservation and management interest. To fill this gap, (a) knowledge on the relationship between carabids and other taxa must be greatly increased, and (b) strict tests must be applied to evaluate indicator functioning as outlined above. We should soon be able to define a ‘niche’ for carabids in environmental assessments. 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