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Biodiversity of ground beetles (Coleoptera: Carabidae) in different habitats of the Italian Po lowland
Agriculture, Ecosystems and Environment 127 (2008) 273–276
Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee
Biodiversity of ground beetles (Coleoptera: Carabidae) in different habitats of the Italian Po lowland Mauro Gobbi a,*, Diego Fontaneto b a b
Sezione di Zoologia degli Invertebrati, Museo Tridentino di Scienze Naturali, Via Calepina 14, I-38100 Trento, Italy Imperial College London, Silwood Park Campus, Ascot Berkshire, SL5 7PY, United Kingdom
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 December 2007 Received in revised form 16 April 2008 Accepted 18 April 2008 Available online 2 June 2008
In this paper a meta-analysis of published and new data on ground beetle species assemblages in the agroecosystems of the Italian Po lowland was performed as a study case to describe the effect of habitat type with different human disturbance on species richness, taxonomic diversity and biological traits. Spatially explicit analyses gave species richness as positively related to human impact, while the proportions of short winged, large and predatory species were negatively related to human impact. The results highlight how species richness may be a completely misleading parameter for the interpretation of human impacts. Therefore, ecological traits for each species need to be standardized and included in the evaluation and monitoring of the effect of human activities on the environment. For ground beetles the use of morpho-ecological traits as wing morphology, diet and body size is recommended, and not species richness per se. ß 2008 Elsevier B.V. All rights reserved.
Keywords: Arable landscape Carabid beetles Spatially explicit model Species richness Biological functions Taxonomic diversity
1. Introduction In this paper the relationship between two of the main traits belonging to animal communities, i.e. species richness (the total number of species) and species traits (the morpho-ecological adaptations), was analysed using species assemblages of ground beetles (Coleoptera: Carabidae) in different habitats in Northern Italy. Ground beetles are one of the most common and species-rich families of ground-dwelling arthropods in agricultural ecosystems and their role as bioindicators of land-use and human impact is well known (e.g., Thiele, 1977; Lo¨vei and Sunderland, 1996; Holland, 2002; Rainio and Niemela¨, 2003). They are also widely distributed and biologically better known than other taxa of soil fauna, making them an excellent test case to describe and analyse how communities react to anthropogenic activities. Based on previous empirical works and reviews, it can be predicted that for ground beetles, absence of metathoracic wings, larger body size and strictly predatory diet are biological features negatively related to habitat disturbance (e.g. Kotze and O’Hara, 2003; Brandmayr et al., 2005; Purtauf et al., 2005; Lo¨vei and Magura, 2006). Brachypterous species can only colonise new areas by walking. As a result these animals are poorly represented in fragmented and degraded landscapes, where they only survive in patches large
* Corresponding author. Tel.: +39 03496356319. E-mail address: [email protected] (M. Gobbi). 0167-8809/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2008.04.011
enough and which suitability has been constant for long periods (Brandmayr, 1983; Lo¨vei and Sunderland, 1996; Kotze and O’Hara, 2003). Therefore, the expectation for a habitat with a high degree of disturbance is to have a lower proportion of brachypterous species, as they will be sensitive to unstable and variable conditions. Larger animals usually have larval stages which last longer; having to survive across more seasons, larvae are more prone to be negatively influenced by anthropogenic disturbance than adults (Blake et al., 1994; Kotze and O’Hara, 2003; Lo¨vei and Magura, 2006). Therefore, the expectation for disturbed habitats is to have a higher proportion of small species, as their larvae will not be so negatively affected as those of large species. Predators are more sensitive to landscape simplification than phytophages and omnivores; therefore, the expectation for habitats with high human disturbance is to have a lower proportion of strictly predatory species (Toft and Bilde, 2002; Purtauf et al., 2005). Habitat type and structure are known to drive local species richness and quality (With and Crist, 1995; Tews et al., 2004), and the Po plain in Northern Italy is a mosaic of different habitats within the same biogeographic area. The aim of this paper was to find out whether species assemblages in habitats of the Po plain in Northern Italy under various human disturbances had consistently different species richness, taxonomic diversity, and ecological traits of each species, in order to obtain reliable proxies to describe diversity for environmental assessments.
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2. Methods In order to obtain comparable data, only results from studies fulfilling the following conditions were included in the analysis: (1) pitfall trapping in clearly identifiable habitat categories (woodlands, poplar stands, meadows and crops), (2) overall sampling periods longer than one year, (3) at least five traps per habitat, and (4) explicit geographic location. A total of 18 studies (Boano et al., 1993; Chemini and Perini, 1982; Chemini and Werth, 1982; I.P.L.A, 1986; Pescarolo, 1990,1993; Pilon et al., 1991; Chemini and Pizzolotto, 1992; Casale et al., 1993; Casale and Giachino, 1994; Pilon, 1995; Bonavita and Chemini, 1996; Allegro, 2001; Fontaneto and Guidali, 2001; Allegro et al., 2002; Gobbi et al., 2005a,b, 2007) was retained, and unpublished data for another woodland area were added. Overall, a presence/absence matrix for 202 ground beetle species in 57 species assemblages, which covered almost all the Po plain was obtained. Distances between sampling sites ranged from less than 1 to more than 300 km. The four habitat categories were ranked by their anthropogenic disturbance: crops are the most affected habitat by human disturbance, due to complete removal of plant material. Woodlands are perennial and the least affected habitat by removal of plant material; poplar stands and meadows can be considered intermediate between crops and woodland. Meadows may be less disturbed by tillage than poplar stands, but in the latter habitat the vegetation cover is permanent, and less frequently cut as in the former habitat. Ground beetle species were divided in categories according to their biological features. As for wing morphology, all species were divided in two groups: brachypterous and macropterous. According to Cole et al. (2002), the species that are equal or longer than 15 mm were considered as large. As for diet, strict predators were distinguished from all other beetles, the species that are occasional predators being included in the latter group. To check for sign and strength of potential association between the three biological correlates (flying ability, body length, and diet) among different species, the phi correlation coefficients for all three pairwise comparisons were calculated. The phi was defined as the product moment applied to dichotomous data and was also a function of the chi-square of a four-fold table; it ranged between 1.00 and +1.00, with 1 indicating a perfect prediction, 0 a random prediction, and values below 0 a worse than random prediction (Conover, 1980). A chi-square test for the significance of the association was provided, and p-values calculated with Yate’s corrections. The phylogenetic distances between species were approximated using the branching topology of a taxonomic tree (Warwick and Clarke, 2001; Ricotta, 2004). All pairwise species distances within each assemblage were computed using their topological distances (number of segments separating two species in the taxonomic dendrogram, with nodes identified by the taxonomic categories from species to family), with taxonomic data from Fauna Europaea web project (Vigna Taglianti, 2007). The overall taxonomic diversity for each assemblage was then computed as the mean of all pairwise species distances. The other analysed parameters were the biological features related to species quality, expressed as the proportion of (1) brachypterous, (2) large and (3) predator species. First of all, the significance of the correlations between the three biological features for each assemblage was checked. Data for species assemblages were spatially correlated, inflating the number of degree of freedom in correlation tests; therefore, we applied Dutilleul (1993) method for estimating number of degrees of freedom, as implemented in spatial analysis in macroecology (SAM: Rangel et al., 2006). We then reduced the number of
variables to be analysed by applying a principal component analysis (PCA) on the biological variables that resulted highly correlated. Overall, five biodiversity estimates were analysed: the first parameter, species richness, was related to the number of species; the other parameters were related to which species were present and not to the number of species only. To avoid problems of spatial autocorrelation, residuals from a trend surface analysis (TSA: Wren, 1973) as implemented in SAM, were extracted to be used as response variables in Linear Model (LM) tests, with habitat type as explanatory variable. Residuals from TSA had errors normally distributed for species richness and predators, while data were log-transformed for taxonomic diversity and the 1st PC axis explaining large and brachypterous species, to have normally distributed errors in the test. Tukey’s Honestly Significant Differences (HSD) post hoc tests were used to disentangle differences between habitats. To detail the distribution of species in the habitats, and to qualitatively describe the taxonomic differences in species assemblages between habitats, LM and Tukey’s HSD tests were performed with the habitat as explanatory variable, and the proportion of each of the 19 subfamilies in each assemblage (using residuals from a TSA) as response variables. Also in this case, residuals from TSA had normally distributed errors for the most common subfamilies. Excel, SPSS, R and SAM were used to perform the analyses. 3. Results Biological traits of ground beetles were not associated with each other, as all phi values were below 0.5 (predators and large: phi = 0.23, chi-square = 9.07, p = 0.0026; brachypterous and predators: phi = 0.26, chi-square = 12.19, p < 0.001; brachypterous and large: phi = 0.41, chi-square = 31.69, p < 0.001). At the level of species assemblages, biological traits were associated with each other: the proportion of brachypterous and large species were highly significantly correlated (Pearson’s r = 0.899, corrected d.f. = 24.067, p < 0.0001); the proportion of brachypterous and predatory species (Pearson’s r = 0.462, corrected d.f. = 36.362, p = 0.003) and the proportion of large and predatory species (Pearson’s r = 0.518, corrected d.f. = 26.627, p = 0.004) were correlated, although with less strength than the proportion of brachypterous and large species. Therefore, the information for the proportion of brachypterous and large species was merged in a single variable, applying PCA. The first axis explained 95% of the variance and was positively related to both the proportion of brachypterous and large species. Habitat type significantly influenced the analysed variables (Table 1; Fig. 1). Species richness was significantly lower in woodlands than in crops, while the opposite pattern was evidenced for the biological traits of ground beetle species assemblages, with proportions of predatory, large and brachypterous species lower in crops than in woodlands. Woodlands and crops always had opposite patterns; meadows and poplar stands had intermediate levels, with poplar stands more similar to woodlands, and meadows more similar to crops. No significant effect of habitat type was detected on taxonomic diversity. Regarding the taxonomic association with particular habitats, LM tests seemed to provide evidence of a bias for some subfamilies. Cicindelinae and Harpalinae were negatively associated to woodlands; Brachininae, Broscinae and Chlaeniinae were positively associated to meadows. On the other hand, some subfamilies, as Carabinae, Platyninae and Pterostichinae, were slightly associated to woodlands. All other 11 subfamilies did not reveal any particular tendency towards any habitats.
M. Gobbi, D. Fontaneto / Agriculture, Ecosystems and Environment 127 (2008) 273–276 Table 1 Results of the LM tests with habitat type (woodlands, poplar stands, meadows and crops) as explanatory variable Dependent variable
F3,53
p
Richness Predators Brachypterous + large Taxonomic diversity
7.469 12.113 10.56 1.028
0.0003 <0.0001 <0.0001 0.387
Response variables are the residuals from a Trend Surface Analysis to exclude spatial autocorrelation of values, log-transformed when necessary.
4. Discussion Habitat type affected the biodiversity parameters analysed for species assemblages of ground beetles; species richness showed opposite patterns than the biological traits. No effect of habitat typology was observed on the taxonomic diversity. Moreover, few subfamilies were significantly associated to particular habitats. Taxonomic diversity was not linked to habitat type, while there was a taxonomic association to particular habitats. For example, Harpalinae were linked to highly disturbed crops, confirming that this subfamily is characterised by steppe or steppe-like elements coming from Eastern Europe, which may find a suitable habitat in the anthropogenic agricultural habitats of Central and Southern Europe (Andersen, 2000). Carabinae, Platyninae and Pterostichinae, associated to woodlands are mostly characterised by brachypterous,
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large, and predatory species while in Brachininae, Broscinae, and Chlaeninae, associated to open formations with permanent cover as meadows, macropterous and small species predominate (Hu˚rka, 1996). Nevertheless, within each subfamily there was variability in terms of wing morphology, diet and body length. This variability, coupled with the presence of other subfamilies not associated to any habitat, might explain the lack of influence of habitat type on taxonomic diversity. Confirming predictions, biological correlates of species assemblages were strongly related to habitat type. Dispersal capacity (expressed as metathoracic wing morphology), diet and body size may be used as informative biological parameters in relation to human disturbance on landscape management. Woodlands hosted few, but highly specialized species in terms of adaptive parameters. In habitats as poplar stands, meadows and crops, more impacted by human activities, brachypterous, large and predator species were less present. These results suggested that the analyses of ground beetle species assemblages commonly performed in applied studies and monitoring of landscape ecology, may be potentially misleading: species richness is a too much reductive parameter for the interpretation of habitat type, sensibility to human disturbance, and the role of species in the ecosystem. Therefore, ecological traits for each species need to be standardized and included in the evaluation of the effect of human activities on landscapes. For ground beetles the use of morpho-ecological traits, such as wing
Fig. 1. Box-plot of the distribution of (A) species richness, (B) taxonomic diversity, (C) proportion of predators, and (D) proportion of brachypterous and large species. The proportions of brachypterous and large species are reduced by the first axis of a PCA. The values for each variable are the residuals after a Trend Surface Analysis. Horizontal graphs represent homogeneous subgroups from a Tukey’s HSD Post Hoc test.
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morphology, diet and body size are recommended to evaluate the human interference in the landscape. This study introduces a nontaxonomic method to classify habitats with different levels of stability on the basis of ground beetle ecology. Functional groups are a better index of the impact of human activities on the landscape than species richness or taxonomic diversity. During the last century, brachypterous, large and specialist ground beetles declined in Europe, particularly in lowlands (Kotze and O’Hara, 2003). The present work analysed the responses of ground beetles to human management of rural patches and showed that specialist species living in patches of woodlands scattered in the Po plain are most prone to extinction; this could determine changes on the ecosystem (Duffy et al., 2007). For example the loss of predatory species in the simplified agricultural Po landscape may significantly affect the biological control of pests like aphids, caterpillars and slugs (Lo¨vei and Sunderland, 1996; Kromp, 1999; Holland, 2002). Moreover, patches with bigger species may favour the presence of small mammals, birds, reptiles and amphibians which prefer to eat higher biomass specimens (Hernandez et al., 1991; Holland, 2002). Acknowledgments We acknowledge the numerous discussion over years with carabidologist colleagues as Maurizio Pavesi (Museo Civico di Storia Naturale di Milano), Pietro Brandmayr (Universita` della Calabria), Roberto Fabbri (Museo Civico di Storia Naturale di Ferrara), Franca Guidali (Universita` degli Studi di Milano) and Riccardo Groppali (Universita` degli Studi di Pavia) who share our love for the ecology of carabid beetles. We wish to thank two anonymous reviewers for improving the manuscript. No specific fundings were received for this research, but DF was partially supported by a EU-FP6 Marie Curie Intra-European Fellowship. References Allegro, G., 2001. La carabidofauna dell’oasi WWF ‘‘Il Verneto’’ di Rocchetta Tanaro (Asti, Piemonte) (Coleoptera, Carabidae). Riv. Piem. St. Nat. 22, 165–182. Allegro, G., Cersosimo, M., Palestrini, C., 2002. I Carabidi dell’Oasi WWF ‘‘Bosco del Lago’’ di Castello di Annone (Asti, Piemonte) (Coleoptera Carabidae). Riv. Piem. St. Nat. 23, 175–194. Andersen, J., 2000. What is the origin of the carabid beetle fauna of dry, anthropogenic habitats in Western Europe? J. Biogeogr. 27, 795–806. Blake, S., Foster, G.N., Eyre, M.D., Luff, M.L., 1994. Effects of habitat type and grassland management practice on the body size distribution of carabid beetles. Pedobiologia 28, 502–512. Boano, G., Curletti, G., Del Mastro, G., Giachino, P.M., Sciaky, R., 1993. Carabidofauna del Bosco del Merlino (Caramagna, CN). In: Casale A., et al. (Ed.), Comunita` di Coleotteri Carabidi (Coleoptera) in pioppeti del Piemonte meridionale. Riv. Piem. St. Nat. 14, 149–170. Bonavita, P., Chemini, C., 1996. Structures and indicator role of Carabid assemblages from wet areas of the province of Trento, Italian Alps (Coleoptera, Carabidae). Quad. Staz. Ecol. Civ. Mus. St. Nat. Ferrara 10, 107–123. Brandmayr, P., 1983. The main axes of the coenoclinal continuum from macroptery to brachyptery in carabid communities of the temperate zone. Report 4th Symposium. European Carabidologists, Haus Rothenberge, Westphalia, Sept. 2426/1981, Pubbl. Agric. Univ. Wageningen, Brandmayr, P. Zetto, T., Pizzolotto, R., 2005. I Coleotteri Carabidi per la valutazione ambientale e la conservazione della biodiversita`. Manuale operativo. APAT Agenzia nazionale per la protezione dell’ambiente e per i servizi tecnici, Roma. Manuali e linee guida, 34. Casale, A., Giachino, P., 1994. Coleotteri Carabidi di Ambienti lacustri e lacustro torbosi dell’anfiteatro morenico di Ivrea (Coleoptera, Carabidae). Quad. Staz. Ecol. Civ. Mus. St. Nat. Ferrara 6, 225–274. Casale, A., Giachino, P.M., Allegro, G., Della Beffa, G., Picco, F., 1993. Comunita` di Coleotteri Carabidi (Coleoptera) in pioppeti del Piemonte meridionale. Riv. Piem. St. Nat. 14, 149–170.
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Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee
Biodiversity of ground beetles (Coleoptera: Carabidae) in different habitats of the Italian Po lowland Mauro Gobbi a,*, Diego Fontaneto b a b
Sezione di Zoologia degli Invertebrati, Museo Tridentino di Scienze Naturali, Via Calepina 14, I-38100 Trento, Italy Imperial College London, Silwood Park Campus, Ascot Berkshire, SL5 7PY, United Kingdom
A R T I C L E I N F O
A B S T R A C T
Article history: Received 14 December 2007 Received in revised form 16 April 2008 Accepted 18 April 2008 Available online 2 June 2008
In this paper a meta-analysis of published and new data on ground beetle species assemblages in the agroecosystems of the Italian Po lowland was performed as a study case to describe the effect of habitat type with different human disturbance on species richness, taxonomic diversity and biological traits. Spatially explicit analyses gave species richness as positively related to human impact, while the proportions of short winged, large and predatory species were negatively related to human impact. The results highlight how species richness may be a completely misleading parameter for the interpretation of human impacts. Therefore, ecological traits for each species need to be standardized and included in the evaluation and monitoring of the effect of human activities on the environment. For ground beetles the use of morpho-ecological traits as wing morphology, diet and body size is recommended, and not species richness per se. ß 2008 Elsevier B.V. All rights reserved.
Keywords: Arable landscape Carabid beetles Spatially explicit model Species richness Biological functions Taxonomic diversity
1. Introduction In this paper the relationship between two of the main traits belonging to animal communities, i.e. species richness (the total number of species) and species traits (the morpho-ecological adaptations), was analysed using species assemblages of ground beetles (Coleoptera: Carabidae) in different habitats in Northern Italy. Ground beetles are one of the most common and species-rich families of ground-dwelling arthropods in agricultural ecosystems and their role as bioindicators of land-use and human impact is well known (e.g., Thiele, 1977; Lo¨vei and Sunderland, 1996; Holland, 2002; Rainio and Niemela¨, 2003). They are also widely distributed and biologically better known than other taxa of soil fauna, making them an excellent test case to describe and analyse how communities react to anthropogenic activities. Based on previous empirical works and reviews, it can be predicted that for ground beetles, absence of metathoracic wings, larger body size and strictly predatory diet are biological features negatively related to habitat disturbance (e.g. Kotze and O’Hara, 2003; Brandmayr et al., 2005; Purtauf et al., 2005; Lo¨vei and Magura, 2006). Brachypterous species can only colonise new areas by walking. As a result these animals are poorly represented in fragmented and degraded landscapes, where they only survive in patches large
* Corresponding author. Tel.: +39 03496356319. E-mail address: [email protected] (M. Gobbi). 0167-8809/$ – see front matter ß 2008 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2008.04.011
enough and which suitability has been constant for long periods (Brandmayr, 1983; Lo¨vei and Sunderland, 1996; Kotze and O’Hara, 2003). Therefore, the expectation for a habitat with a high degree of disturbance is to have a lower proportion of brachypterous species, as they will be sensitive to unstable and variable conditions. Larger animals usually have larval stages which last longer; having to survive across more seasons, larvae are more prone to be negatively influenced by anthropogenic disturbance than adults (Blake et al., 1994; Kotze and O’Hara, 2003; Lo¨vei and Magura, 2006). Therefore, the expectation for disturbed habitats is to have a higher proportion of small species, as their larvae will not be so negatively affected as those of large species. Predators are more sensitive to landscape simplification than phytophages and omnivores; therefore, the expectation for habitats with high human disturbance is to have a lower proportion of strictly predatory species (Toft and Bilde, 2002; Purtauf et al., 2005). Habitat type and structure are known to drive local species richness and quality (With and Crist, 1995; Tews et al., 2004), and the Po plain in Northern Italy is a mosaic of different habitats within the same biogeographic area. The aim of this paper was to find out whether species assemblages in habitats of the Po plain in Northern Italy under various human disturbances had consistently different species richness, taxonomic diversity, and ecological traits of each species, in order to obtain reliable proxies to describe diversity for environmental assessments.
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2. Methods In order to obtain comparable data, only results from studies fulfilling the following conditions were included in the analysis: (1) pitfall trapping in clearly identifiable habitat categories (woodlands, poplar stands, meadows and crops), (2) overall sampling periods longer than one year, (3) at least five traps per habitat, and (4) explicit geographic location. A total of 18 studies (Boano et al., 1993; Chemini and Perini, 1982; Chemini and Werth, 1982; I.P.L.A, 1986; Pescarolo, 1990,1993; Pilon et al., 1991; Chemini and Pizzolotto, 1992; Casale et al., 1993; Casale and Giachino, 1994; Pilon, 1995; Bonavita and Chemini, 1996; Allegro, 2001; Fontaneto and Guidali, 2001; Allegro et al., 2002; Gobbi et al., 2005a,b, 2007) was retained, and unpublished data for another woodland area were added. Overall, a presence/absence matrix for 202 ground beetle species in 57 species assemblages, which covered almost all the Po plain was obtained. Distances between sampling sites ranged from less than 1 to more than 300 km. The four habitat categories were ranked by their anthropogenic disturbance: crops are the most affected habitat by human disturbance, due to complete removal of plant material. Woodlands are perennial and the least affected habitat by removal of plant material; poplar stands and meadows can be considered intermediate between crops and woodland. Meadows may be less disturbed by tillage than poplar stands, but in the latter habitat the vegetation cover is permanent, and less frequently cut as in the former habitat. Ground beetle species were divided in categories according to their biological features. As for wing morphology, all species were divided in two groups: brachypterous and macropterous. According to Cole et al. (2002), the species that are equal or longer than 15 mm were considered as large. As for diet, strict predators were distinguished from all other beetles, the species that are occasional predators being included in the latter group. To check for sign and strength of potential association between the three biological correlates (flying ability, body length, and diet) among different species, the phi correlation coefficients for all three pairwise comparisons were calculated. The phi was defined as the product moment applied to dichotomous data and was also a function of the chi-square of a four-fold table; it ranged between 1.00 and +1.00, with 1 indicating a perfect prediction, 0 a random prediction, and values below 0 a worse than random prediction (Conover, 1980). A chi-square test for the significance of the association was provided, and p-values calculated with Yate’s corrections. The phylogenetic distances between species were approximated using the branching topology of a taxonomic tree (Warwick and Clarke, 2001; Ricotta, 2004). All pairwise species distances within each assemblage were computed using their topological distances (number of segments separating two species in the taxonomic dendrogram, with nodes identified by the taxonomic categories from species to family), with taxonomic data from Fauna Europaea web project (Vigna Taglianti, 2007). The overall taxonomic diversity for each assemblage was then computed as the mean of all pairwise species distances. The other analysed parameters were the biological features related to species quality, expressed as the proportion of (1) brachypterous, (2) large and (3) predator species. First of all, the significance of the correlations between the three biological features for each assemblage was checked. Data for species assemblages were spatially correlated, inflating the number of degree of freedom in correlation tests; therefore, we applied Dutilleul (1993) method for estimating number of degrees of freedom, as implemented in spatial analysis in macroecology (SAM: Rangel et al., 2006). We then reduced the number of
variables to be analysed by applying a principal component analysis (PCA) on the biological variables that resulted highly correlated. Overall, five biodiversity estimates were analysed: the first parameter, species richness, was related to the number of species; the other parameters were related to which species were present and not to the number of species only. To avoid problems of spatial autocorrelation, residuals from a trend surface analysis (TSA: Wren, 1973) as implemented in SAM, were extracted to be used as response variables in Linear Model (LM) tests, with habitat type as explanatory variable. Residuals from TSA had errors normally distributed for species richness and predators, while data were log-transformed for taxonomic diversity and the 1st PC axis explaining large and brachypterous species, to have normally distributed errors in the test. Tukey’s Honestly Significant Differences (HSD) post hoc tests were used to disentangle differences between habitats. To detail the distribution of species in the habitats, and to qualitatively describe the taxonomic differences in species assemblages between habitats, LM and Tukey’s HSD tests were performed with the habitat as explanatory variable, and the proportion of each of the 19 subfamilies in each assemblage (using residuals from a TSA) as response variables. Also in this case, residuals from TSA had normally distributed errors for the most common subfamilies. Excel, SPSS, R and SAM were used to perform the analyses. 3. Results Biological traits of ground beetles were not associated with each other, as all phi values were below 0.5 (predators and large: phi = 0.23, chi-square = 9.07, p = 0.0026; brachypterous and predators: phi = 0.26, chi-square = 12.19, p < 0.001; brachypterous and large: phi = 0.41, chi-square = 31.69, p < 0.001). At the level of species assemblages, biological traits were associated with each other: the proportion of brachypterous and large species were highly significantly correlated (Pearson’s r = 0.899, corrected d.f. = 24.067, p < 0.0001); the proportion of brachypterous and predatory species (Pearson’s r = 0.462, corrected d.f. = 36.362, p = 0.003) and the proportion of large and predatory species (Pearson’s r = 0.518, corrected d.f. = 26.627, p = 0.004) were correlated, although with less strength than the proportion of brachypterous and large species. Therefore, the information for the proportion of brachypterous and large species was merged in a single variable, applying PCA. The first axis explained 95% of the variance and was positively related to both the proportion of brachypterous and large species. Habitat type significantly influenced the analysed variables (Table 1; Fig. 1). Species richness was significantly lower in woodlands than in crops, while the opposite pattern was evidenced for the biological traits of ground beetle species assemblages, with proportions of predatory, large and brachypterous species lower in crops than in woodlands. Woodlands and crops always had opposite patterns; meadows and poplar stands had intermediate levels, with poplar stands more similar to woodlands, and meadows more similar to crops. No significant effect of habitat type was detected on taxonomic diversity. Regarding the taxonomic association with particular habitats, LM tests seemed to provide evidence of a bias for some subfamilies. Cicindelinae and Harpalinae were negatively associated to woodlands; Brachininae, Broscinae and Chlaeniinae were positively associated to meadows. On the other hand, some subfamilies, as Carabinae, Platyninae and Pterostichinae, were slightly associated to woodlands. All other 11 subfamilies did not reveal any particular tendency towards any habitats.
M. Gobbi, D. Fontaneto / Agriculture, Ecosystems and Environment 127 (2008) 273–276 Table 1 Results of the LM tests with habitat type (woodlands, poplar stands, meadows and crops) as explanatory variable Dependent variable
F3,53
p
Richness Predators Brachypterous + large Taxonomic diversity
7.469 12.113 10.56 1.028
0.0003 <0.0001 <0.0001 0.387
Response variables are the residuals from a Trend Surface Analysis to exclude spatial autocorrelation of values, log-transformed when necessary.
4. Discussion Habitat type affected the biodiversity parameters analysed for species assemblages of ground beetles; species richness showed opposite patterns than the biological traits. No effect of habitat typology was observed on the taxonomic diversity. Moreover, few subfamilies were significantly associated to particular habitats. Taxonomic diversity was not linked to habitat type, while there was a taxonomic association to particular habitats. For example, Harpalinae were linked to highly disturbed crops, confirming that this subfamily is characterised by steppe or steppe-like elements coming from Eastern Europe, which may find a suitable habitat in the anthropogenic agricultural habitats of Central and Southern Europe (Andersen, 2000). Carabinae, Platyninae and Pterostichinae, associated to woodlands are mostly characterised by brachypterous,
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large, and predatory species while in Brachininae, Broscinae, and Chlaeninae, associated to open formations with permanent cover as meadows, macropterous and small species predominate (Hu˚rka, 1996). Nevertheless, within each subfamily there was variability in terms of wing morphology, diet and body length. This variability, coupled with the presence of other subfamilies not associated to any habitat, might explain the lack of influence of habitat type on taxonomic diversity. Confirming predictions, biological correlates of species assemblages were strongly related to habitat type. Dispersal capacity (expressed as metathoracic wing morphology), diet and body size may be used as informative biological parameters in relation to human disturbance on landscape management. Woodlands hosted few, but highly specialized species in terms of adaptive parameters. In habitats as poplar stands, meadows and crops, more impacted by human activities, brachypterous, large and predator species were less present. These results suggested that the analyses of ground beetle species assemblages commonly performed in applied studies and monitoring of landscape ecology, may be potentially misleading: species richness is a too much reductive parameter for the interpretation of habitat type, sensibility to human disturbance, and the role of species in the ecosystem. Therefore, ecological traits for each species need to be standardized and included in the evaluation of the effect of human activities on landscapes. For ground beetles the use of morpho-ecological traits, such as wing
Fig. 1. Box-plot of the distribution of (A) species richness, (B) taxonomic diversity, (C) proportion of predators, and (D) proportion of brachypterous and large species. The proportions of brachypterous and large species are reduced by the first axis of a PCA. The values for each variable are the residuals after a Trend Surface Analysis. Horizontal graphs represent homogeneous subgroups from a Tukey’s HSD Post Hoc test.
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morphology, diet and body size are recommended to evaluate the human interference in the landscape. This study introduces a nontaxonomic method to classify habitats with different levels of stability on the basis of ground beetle ecology. Functional groups are a better index of the impact of human activities on the landscape than species richness or taxonomic diversity. During the last century, brachypterous, large and specialist ground beetles declined in Europe, particularly in lowlands (Kotze and O’Hara, 2003). The present work analysed the responses of ground beetles to human management of rural patches and showed that specialist species living in patches of woodlands scattered in the Po plain are most prone to extinction; this could determine changes on the ecosystem (Duffy et al., 2007). For example the loss of predatory species in the simplified agricultural Po landscape may significantly affect the biological control of pests like aphids, caterpillars and slugs (Lo¨vei and Sunderland, 1996; Kromp, 1999; Holland, 2002). Moreover, patches with bigger species may favour the presence of small mammals, birds, reptiles and amphibians which prefer to eat higher biomass specimens (Hernandez et al., 1991; Holland, 2002). Acknowledgments We acknowledge the numerous discussion over years with carabidologist colleagues as Maurizio Pavesi (Museo Civico di Storia Naturale di Milano), Pietro Brandmayr (Universita` della Calabria), Roberto Fabbri (Museo Civico di Storia Naturale di Ferrara), Franca Guidali (Universita` degli Studi di Milano) and Riccardo Groppali (Universita` degli Studi di Pavia) who share our love for the ecology of carabid beetles. We wish to thank two anonymous reviewers for improving the manuscript. No specific fundings were received for this research, but DF was partially supported by a EU-FP6 Marie Curie Intra-European Fellowship. References Allegro, G., 2001. La carabidofauna dell’oasi WWF ‘‘Il Verneto’’ di Rocchetta Tanaro (Asti, Piemonte) (Coleoptera, Carabidae). Riv. Piem. St. Nat. 22, 165–182. Allegro, G., Cersosimo, M., Palestrini, C., 2002. I Carabidi dell’Oasi WWF ‘‘Bosco del Lago’’ di Castello di Annone (Asti, Piemonte) (Coleoptera Carabidae). Riv. Piem. St. Nat. 23, 175–194. Andersen, J., 2000. What is the origin of the carabid beetle fauna of dry, anthropogenic habitats in Western Europe? J. Biogeogr. 27, 795–806. Blake, S., Foster, G.N., Eyre, M.D., Luff, M.L., 1994. Effects of habitat type and grassland management practice on the body size distribution of carabid beetles. Pedobiologia 28, 502–512. Boano, G., Curletti, G., Del Mastro, G., Giachino, P.M., Sciaky, R., 1993. Carabidofauna del Bosco del Merlino (Caramagna, CN). In: Casale A., et al. (Ed.), Comunita` di Coleotteri Carabidi (Coleoptera) in pioppeti del Piemonte meridionale. Riv. Piem. St. Nat. 14, 149–170. Bonavita, P., Chemini, C., 1996. Structures and indicator role of Carabid assemblages from wet areas of the province of Trento, Italian Alps (Coleoptera, Carabidae). Quad. Staz. Ecol. Civ. Mus. St. Nat. Ferrara 10, 107–123. Brandmayr, P., 1983. The main axes of the coenoclinal continuum from macroptery to brachyptery in carabid communities of the temperate zone. Report 4th Symposium. European Carabidologists, Haus Rothenberge, Westphalia, Sept. 2426/1981, Pubbl. Agric. Univ. Wageningen, Brandmayr, P. Zetto, T., Pizzolotto, R., 2005. I Coleotteri Carabidi per la valutazione ambientale e la conservazione della biodiversita`. Manuale operativo. APAT Agenzia nazionale per la protezione dell’ambiente e per i servizi tecnici, Roma. Manuali e linee guida, 34. Casale, A., Giachino, P., 1994. Coleotteri Carabidi di Ambienti lacustri e lacustro torbosi dell’anfiteatro morenico di Ivrea (Coleoptera, Carabidae). Quad. Staz. Ecol. Civ. Mus. St. Nat. Ferrara 6, 225–274. Casale, A., Giachino, P.M., Allegro, G., Della Beffa, G., Picco, F., 1993. Comunita` di Coleotteri Carabidi (Coleoptera) in pioppeti del Piemonte meridionale. Riv. Piem. St. Nat. 14, 149–170.
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