Acta Oecologica 26 (2004) 219226 www.elsevier.

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Original article

Correlational patterns between invertebrate species composition and the presence of an invasive plant
Miquel Palmer a,*, Marta Linde a, Guillem X. Pons b
a

IMEDEA (CSIC-UIB), Instituto Mediterrneo de Estudios Avanzados, Miquel Marqus 21, 07190 Esporles (Mallorca), Spain b Department of Earth Sciences, University Illes Balears, Cta Valldemossa km 7.5, 07071 Palma de Mallorca, Spain Received 17 January 2003; accepted 14 May 2004 Available online 20 August 2004

Abstract It is widely assumed that the presence of invasive exotic plants causes a negative impact on native biotas. Here, we analyse the correlational patterns between the presence of one of these invasive plants, the South African Hottentot g, Carpobrotus acinaciformis (L.) L. Bolus (Aizoaceae), and the terrestrial invertebrate species composition of a Mediterranean rocky shore. Variations in invertebrate community were estimated by determining the presenceabsence of 94 species in 30 plots along a 2.5 km shoreline. Canonical correspondence analyses revealed that three environmental variables showed signicant correlation with the invertebrate presenceabsence matrix. Namely, distance to the nearest urban area, soil type, and vegetation type. Presenceabsence of the invasive plant was correlated with these environmental variables, but no additional effect on the invertebrate community specically attributable to the presence of the invasive plant was detected. These facts exemplify the uncertainties in linking the presence of an invasive species with its putative outcomes because they are consistent with the hypothesis that a general gradient of anthropic inuence affects the invertebrate species composition, and that the supposed effects of C. acinaciformis on the invertebrate species composition are correlated with (and therefore, indiscernible from) those derived from the existence of such general gradient of anthropic inuence. 2004 Elsevier SAS. All rights reserved.
Keywords: Biogeography; Invasive plants; Islands; Invertebrates (Coleoptera, Arachnida, Gastropoda, Isopoda); Endemism; Canonical correspondence analysis

1. Introduction Carpobrotus acinaciformis (L.) L. Bolus is a creeping succulent herb native to the Cape region (South Africa) and naturalised in the Western Mediterranean littoral. This species forms extensive stands that exclude almost any other plant species, and alters the soil properties (http://www.ceh.ac.uk/EPIDEMIE/). Accordingly, the invasion of the rocky shores of the Balearic Islands by C. edulis and C. acinaciformis has been recognized as an environmental problem. For example, there are specic eradication programs running in the Cabrera National Park, and in Menorca (LIFE project 2000NAT/E/7355). However, doubts remain on the balance between economic cost and potential benets of these programs because few data on the whole-system effects of C. acinaciformis are available. Therefore, our main
* Corresponding author. E-mail address: ieampv@uib.es (M. Palmer). 1146-609X/$ - see front matter 2004 Elsevier SAS. All rights reserved. doi:10.1016/j.actao.2004.05.005

goal was to describe and analyse the overall patterns of ecosystem response to the presence of C. acinaciformis. Ecological indicators may be useful to assess the condition of the environment, or to diagnose the cause of a specic environmental problem (Dale and Beyeler, 2001). The adequacy of arthropods and other macroinvertebrates as bioindicators relies on their large number and their high species turnover along environmental gradients, while most vertebrates are insensitive to ne-scale habitat heterogeneity (Mattoni et al., 2000). For example, species turnover is estimated to be twice larger in beetles than in birds (Lawton et al., 1998). Bioindicator species covering different functional or taxonomic groups are used when emphasis is made on their capability to reect the expected outcomes related with the invasion of an exotic species, rather than in species-specic chains of cause-and-effect. These chains are often diffuse or unknown. Rarefaction or local extinction of some native plants after colonization by an alien plant implies negative

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effects on their species-specic invertebrate herbivores. However, changes in the vegetation structure surpass these naive effects, and they may affect many species belonging to diverse functional groups. For example, the species composition of spiders and other non-herbivorous macroinvertebrates changed after the invasion of a marsh by Phragmites australis (Talley and Levin, 2001). Changes in invertebrate composition can be related to unexpected indirect effects through the food web (e.g., increased abundance of native chironomids in response to high density populations of an alien aquatic snail, Potamopyrgus antipodarum; Schreiber et al., 2002), or even more diffuse effects (e.g., decreased abundance of the pollinator Bombus dahlbombii, Hymenoptera, in presence of cattle, Vzquez, 2002). Therefore, we analysed 94 species covering a broad taxonomic range (snails, spiders, beetles and isopods) as system-level indicators of the ecosystem response to the presence of C. acinaciformis. In the Balearic Islands, C. acinaciformis occupies preferably disturbed sites. It was introduced as ornamental plant, and is spanning to other habitat types out of the limits of urban areas. Therefore, the abundance of C. acinaciformis is expected to be correlated with a general gradient of anthropic inuence. This type of colonization pattern is probably common among invasive species, and our second goal was to discern the specic changes in species composition correlated with the presence of C. acinaciformis from those related with a general gradient of anthropic inuence or with other environmental variables.

Fig. 1. Location of the studied area. Sampling sites (30) denoted by dots. Axes are UTM coordinates (in m).

2. Methods 2.1. Sampling The study area (Pedreres de la Seu, South Mallorca, Balearic Islands) is a coastal slope 150250 m wide located between two urban areas placed 3 km apart (Fig. 1). The slope rises from the sea shore to a at plateau (6590 m a.s.l.) and is made up of a poorly cemented sandy substrate. The plateau corresponds to a hard, Upper Miocene coral reefderived limestone (Pomar et al., 1996), with interspersed patches of thin red soil (terra rossa). This soil type contrasts with the sandy soil found on the slope (derived from Quaternary dunes). The sampling grid consisted of 10 lines about 250 m apart, each containing three sampling sites (Fig. 1). The three sites on each line were located, respectively, at the lower vegetated strip of the slope, midway slope, and on top. Their positions were GPS-determined. Three pitfall traps (10 cm wide; 2 m left between traps; detergent and salt used as preservative) were installed at every site. The traps were installed on March 15th, and revised on April 15th, and again on May 15th 2002. The sampling schedule was complemented with 1 h of direct search (e.g., under stones) at each site on a 100 m2 plot around the pitfall traps. We analysed presenceabsence data because between species differences in detectability and catchability were noticeable. Data from

the three pitfalls and from direct search were pooled as a single sample per site. We focused on four groups of invertebrates, namely Coleoptera, Arachnida, Isopoda and Gastropoda. As regard Gastropoda, a species was considered to be present also when empty shells were found only. The material was sorted and preserved in ethanol 70%. The number of fully classied taxa (i.e., at species level) was 71 (76% of the total). Some of the species not readily determinable were identied as morphospecies (Oliver and Beattie, 1996) when further identication required detailed study. Morphospecies were classied at genus (three cases) or family level (20 cases), and all them belonged to groups without endemic species. Estimates of plant abundance (on a 100 m2 plot around the pitfall traps) were made using a 06 scale replacing a simplied BraunBlanquet scale (absence, +, 15). A similar replacement has been used elsewhere in similar quantitative multivariate analyses (ter Braak, 1987). Graminaceae and Limonium spp. were excluded from the analysis due to taxonomic constraints. Note that the target community of the present study were the invertebrates (i.e., ecological indicators) and that vegetation was considered only as a putative explanatory variable. 2.2. Statistical analysis The environmental variables correlated with the presenceabsence of C. acinaciformis were identied using a generalized linear model with a logit link and a binomial distribution. Concerning multivariate data, Partial Canonical Correspondence Analysis (pCCA, Legendre and Legendre, 1998) were used to estimate how much variation on the species composition (response variables) can be attributed exclu-

M. Palmer et al. / Acta Oecologica 26 (2004) 219226 Table 1 Putative explanatory variables considered in the CCA analyses Variable DistSea CarPre CarAbun Veg1 to Veg2 LnDistUrb Soil Description Distance to the sea (m) Presenceabsence of C. acinaciformis within a circle 20 m wide Square root and arcsin transformation of abundance (% cover within a circle 20 m wide) Scores on the rst two axes from a CA on plant species abundance Distance (ln-transformed) to the nearest urban area (m) Soil type (sandy versus red soil)

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using an iterative permutation test (by random permutation of rows and columns of one of the two considered matrices). Indeed, statistical testing of a correlogram implies multiple testing, since one test is performed on each of the considered lags. To take this into consideration, and in accordance to the aim of the overall procedure, we applied a progressive Bonferroni correction (Legendre and Legendre, 1998). 2.3. Mapping the fractions of variation on species composition Geostatistics was used to visualize the spatial variation of the variables measured and the sample scores resulting from the different CA and CCA runs. Values of variables measured at sites placed close to each other tended to be more similar than those measured at sites located far apart. Contouring maps were obtained by kriging (Englund and Sparks, 1988). Kriging parameters dene the extent of autocorrelation, and were assessed by visual inspection of semivariograms. Semivariance is a measure of similarity between the values of any variable recorded at pairs of points separated by a specic distance interval (i.e., lag distance). The semivariogram is the plot of the semivariances reached at successive multiples of the lag distance (Legendre and Legendre, 1998, Roa and Tapia, 2000, Rossi and Costantini, 2000). Semivariograms and contour maps were performed using Surfer 7 (Golden Software Inc.). 2.4. Describing biodiversity patterns Two biodiversity indices were used. First, the variation in taxonomic distinctness was determined because it provides unbiased diversity estimates based on species lists only (Clarke and Warwick, 2001). A species list with several orders represented by a single species only gives a high taxonomic distinctness compared to a list where all species belong to the same order. The second estimator used were the endemism richness, measured as the number of endemic species in a sample.

sively to one variable, once the effect of other variables has been taken into account. Five sets of putative explanatory variables were considered because we presumed a priori that they could affect invertebrate species composition (acronyms in Table 1). Namely, (1) abundance (cover percentage) of C. acinaciformis within a circle 20 m wide; presenceabsence was considered also because there was evidence that C. acinaciformis had been partially removed from several sites; (2) distance to the nearest urban area (as a measure of a general gradient of anthropic inuence; the two urban areas were located at the two extremes of the sampling area; Fig. 1); (3) the gradient of marine effect (estimated as distance to the sea); (4) the soil type (two categories considered: sandy soil and red soil); and nally (5) the rst two axes of a detrended correspondence analysis (DCA) of a matrix of plant species abundance as descriptors of the vegetation type. Correspondence analyses (DCA and CA; performed for descriptive purposes), CCAs and pCCAs were performed using CANOCO. Accordingly with the spatially structured sampling sites (see below), the F-ratio signicance of the canonical analyses was assessed by 1999 permutations of the 10 lines while the sampling sites within lines were not permuted (ter Braak and Smilauer, 2002). This permutation method was used to circumvent the lack of independence between samples due to autocorrelation. Spatial autocorrelation emerges when the plots cannot be considered as independent because they are close to each other, and the statistical consequence of this is that the number of effective degrees of freedom is smaller than that inferred from the number of plots only. The spatial patterns of the invertebrate assemblage were analysed using a multivariate Mantel correlogram (Legendre and Legendre, 1998) completed with a MATLAB routine available on request. The rationale of the multivariate Mantel correlogram implies calculating a measure of relatedness between two matrices (the Mantel z). In this case the two matrices were the pair-wise geographical distance matrix (X) and the pair-wise faunistic (dis) similarity matrix (Y). Among the plethora of possible faunistic (dis) similarity measures, we used the BrayCurtis distance (Legendre and Legendre, 1998). The Mantel correlogram is made up by plotting a number of Mantel z, one for each of the distance classes considered. We considered the rst 500 m only, and this distance was divided into six distance classes (lags). Testing the signicance of each of the zi was done

3. Results The presenceabsence of C. acinaciformis was signicantly related with LnDistUrb (Logit model: P = 0.003), and unrelated (partial analyses) with the other explanatory variables listed in Table 1. The probability of nding C. acinaciformis in relation to LnDistUrb is shown in Fig. 2. Considering now the vegetation type (considered here as an explanatory variable that can affect invertebrate species composition), the two first DCA axes explained 26.3% (rst axis, 20.0; second axis 6.3%) of the variability of the matrix of (plant) species abundance. Only 39 plants were included in this analysis, whereas other 17 rare species (present in one or two sites only) were excluded. The trends accounted for the rst two DCA axes were mapped to allow the visual

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of the studied area were more similar to each other than expected (irrespective of their vertical position on the slope). This could be related to an ancient (centuries ago) use of this area as a quarry. The site scores on the two rst axes of this correspondence analysis were used (see below) as vegetation descriptors (Veg1 and Veg2). As regard the spatial pattern displayed by invertebrates (94 species of Coleoptera, Arachnida, Isopoda and Gastropoda), the rst index used (taxonomic distinctness) showed an unexpected pattern (Fig. 4a), with lower values at seemingly undisturbed sites (i.e., toward the centre of the studied area). Note, however, that the variability experienced by this index was low. Endemism richness (measured as number of endemic species per plot) followed a complex pattern, with minima reached not only near the two urban areas but also at seemingly undisturbed sites (Fig. 4b). Prior to statistical analyses, the presenceabsence invertebrate data matrix was submitted to several preliminary steps. First, 25 species found only in one or two sites were excluded from subsequent analyses. Second, the extent of spatial autocorrelation was tested using a multivariate Mantel autocorrelogram (Fig. 5). The two rst lags considered showed signicant autocorrelation. Positive autocorrelation at the rst lag indicated that consecutive samples within the same line tend to be more similar than expected. Negative autocorrelation at the second lag indicated that the upper and the lower sample within the same line tend to be more dissimilar than expected. No signicant autocorrelation at the other lags pointed to spatial autocorrelation was limited to the samples within lines, and that samples between-lines could be consid-

Fig. 2. Probability (estimated using a logit model) of presence of C. acinaciformis in relation to the distance to the nearest urban area (LnDistUrb, m).

display of the main spatial vegetation trends (Fig. 3). The rst axis appeared to be linked to a gradient related to the (vertical) position of the sites on the slope. Species showing higher abundances near the sea were Chenopodium murale L. and Lycium intricatum Boiss. Contrasting, Pinus halepensis Miller and Ruta chalepensis L. preferred sites placed near the top of the slope. The second axis appeared related to a gradient of anthropic inuence (i.e., sites placed near urban areas tended to be more similar to each other). Chenopodium murale L. and Reseda alba L. tended to be more abundant near the urban areas, while Convolvulus cf cambrica L. and Evax pigmaea L. were more abundant on the middle of the studied area. Some sites placed near the south-eastern corner

Fig. 3. Maps corresponding to the rst (panel A) and second (panel B) axes derived from a correspondence analysis of the abundance of 39 plant species. Surfaces with similar plant species composition are denoted by similar grey intensity. The rst axis (20.0% variance explained) appears related to the gradient of vertical position along the slope. Accordingly, interpolation in panel A was forced to converge toward the same value along all the coastline. The second axis (6.3%) appears to represent a gradient of anthropic inuence.

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Fig. 4. Diversity measured as Taxonomic distinctness (panel A) and as number of endemic species (Panel B). Darkness in the grey scale denotes higher diversity. Note the existence of unexpected minima at apparently undisturbed sites.

Fig. 5. Multivariate Mantel correlogram for presenceabsence of 69 invertebrate species along 500 m and six distance intervals. Positive Mantel z indicates more similarity than expected by chance. Numbers of pairs indicated at each distance interval. The two rst intervals showed signicant spatial structure (lled circles), suggesting that points placed farther than 166 m should be considered as fully independent.

ered as fully independent. This justied the permutation method adopted in the statistical analyses. A correspondence analysis allowed mapping the main patterns of faunistic variability. The rst axis (Fig. 6a) discriminated the two sites placed at the north-west corner of the studied area. These sites were characterized by their soil type (terra rossa). The second axis (Fig. 6b) appeared related to a gradient of anthropic inuence. As a second analytical step, a canonical correspondence analysis was performed to nd the best subset of variables (using forward stepwise selection) to explain the variability in invertebrate presenceabsence data. The best subset explained up to 25.6% of this variability. Note that this relatively low amount of explained variance is usual in analyses of variability of presenceabsence data (ter Braak and Smilauer, 2002). This subset was composed of

SoilType, LnDistUrb and Veg1 to Veg2. Ination indexes (as a measure of collinearity) were all <2.0, suggesting that the predictors were not severely correlated. Decomposition of the variability explained by each of these explanatory variables is detailed in Table 2. Looking at the ordination biplot (Fig. 7), it is noticeable that there were no differences between the number of endemic and non-endemic species along the axes. Among endemics, Alphasida depressa Solier, Asida planipennis Schaufuss, Phylan semicostatus (Mulsant and Rey), Percus plicatus Dejean, and Orthomus balearicus (Piochard) (all them beetles; the rst three are detritophagous generalist species whereas the other two are predators) preferred the less disturbed sites. Surprisingly, in the studied area it was most likely to nd some endemic species near the urban sites. Namely: Euscorpius balearicus Capporiaco (Scorpionida; predator), Timarcha balearica Gory (Coleoptera; host-specic herbivore; the host plant, Rubia peregrina, is not restricted to disturbed sites), Pimelia criba Solier (Coleoptera; detritophagous generalist), Nemesia brauni Koch (Arachnida; predator) and Oxychilus lentiformis Kobelt (Gastropoda; herbivore generalist). Other endemics did not show a denite pattern of preferences. The main pattern of residual variability was estimated by the scores on the rst axis of an additional pCCA after taking all the variables as covariables. The map of these scores did not reveal any spatial pattern (results not shown). It is noticeable also that the effects of the presence absence of Carpobrotus acinaciformis (CarPre) were signicant (P = 0.017) when it was considered to be the unique explanatory variable (or even in combination with some but not all the variables included in the best model). Then it explained 6.8% of the presenceabsence variability of the invertebrate species composition. However, an additional

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Fig. 6. Maps corresponding to the rst (panel A) and second (panel B) axes derived from a correspondence analysis of the presenceabsence of 69 invertebrate species. These two axes explain 18.4% of the variability (10.7 and 7.7). Surfaces with similar invertebrate species composition are denoted by similar grey intensity.

partial CCA showed that the specic (partial) effects of C. acinaciformis were not signicant (P = 0.09 in the case of CarPre and P = 0.23 in the case of CarAbun) when distance to urban areas, soil type and vegetation type were all considered as covariables. This apparent contradiction is related to the fact that, in the studied area, the presence of C. acinaciformis is probably dependent of (or at least, correlated with) the distance to the urban sites and the vertical position on the slope (the latter was correlated also with soil type and vegetation type). Therefore, after controlling for the effects of distance to urban areas, soil type and vegetation type, the residual variability remained uncorrelated with any variable measuring the abundance of C. acinaciformis.

4. Discussion Biological invasions by non-native or exotic plants and animals are widely recognised as a signicant component of human-mediated global environmental change. They often

result in a signicant loss of economic value, biological diversity and function of the invaded ecosystems (Mooney and Hobbs, 2000; Mack et al., 2000; Pimentel et al., 2001). However, these negative outcomes are typically exerted by a small number of non-indigenous species (e.g., 91% of 139 non-indigenous species present on the Great Lakes region of N America have no relevant effects on the Great Lakes ecosystems; Mills et al., 1993). C. acinaciformis certainly is capable of forming extensive stands that excludes almost all other plant species. The congeneric species C. edulis successfully competes for water with some native plants, alters soil proprieties (ph), and promotes changes in canopy area and root structure in some native shrubs (DAntonio and Mahall, 1991). It is plausible that C. acinaciformis exhibits similar capabilities. However, in Mallorca, as well as in most Mediterranean islands, the presence of C. acinaciformis is always linked to urban areas (the only exception seems to be some islands of Port Cross National Park, France). The plant is capable to fruit, and seeds are mainly dispersed by rabbits (Oryctolagus

Table 2 Variance decomposition of the effects of SoilType, DistUrb and Veg1 to Veg2 on the presenceabsence data of 69 invertebrate species. The residual fraction was determined using a full model (i.e., including all three sets of explanatory variables). The other entries were determined using partial models. Note that the sum of the percentages of the variance explained by the three rst rows is not 100% of the variance explained by all three subsets taken together because of the between-factor shared variance LnDistUrb Veg1 to Veg 2 SoilType All three subsets Unexplained Trace 0.096 0.178 0.220 0.699 2.254 % 4.3 7.9 9.8 25.6 74.4 F-value 1.428 1.325 3.28 P 0.013 0.036 <0.0005

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Fig. 7. Biplot corresponding to a CCA on the presenceabsence of 69 invertebrate species. Endemic species denoted as lled dots and non-endemic species as open dots. Quantitative explanatory variables (LnDistUrb, and Veg1 to Veg2) indicated by arrows, and categorical explanatory variables (Soil type) by triangles. Scaling focuses on preserving (chi-squared) distances between species, and angle between arrows denotes correlation degree. Approximate ranking of species along a variable axis is given by the projection of species points on the arrow. The rst axis mainly discriminates the species that characterize the sites with red soil. The second axis appears to correspond to a gradient of anthropic inuence (larger effect toward the top).

cuniculus L.; Moragues and Traveset, personal communication). Rabbits seem to be poor dispersers because, in the case of C. edulis, depositions with viable seeds were only found at less than 10 m apart from a plant (DAntonio, 1990). Moreover, germination success in rocky coastal zones seems to be rather low (Moragues and Traveset, personal communication; C. edulis also shows noticeable differences in germination success and growth rate between habitats; DAntonio, 1993). Vegetative multiplication is easy, but it necessarily implies limited dispersal. Therefore, gardening is probably the only way to establish new populations of C. acinaciformis on Mallorcan shores. The distribution pattern of C. acinaciformis, limited to the vicinity of urban areas, supports this because the few populations found in pristine areas always suggest an human-mediated dispersal (e.g., around lighthouses in sa Dragonera islet, SW and SE coast of Mallorca and Cap de Cavalleria, Menorca; Pons, 1999). The foregoing paragraph recalls on the difculties for causal modelling in cases such as here presented because the general anthropic gradient and the probability of presence of C. acinaciformis overlap. More precisely, lithology, geomorphology, soil properties, vegetation and anthropic effects conform in the studied area two major gradients of environmental variation (i.e., vertical position on the slope and distance to urban areas). The sites with C. acinaciformis certainly are occupied by a different invertebrate assemblage than sites that are free of this invasive plant. However, and contrasting with what could be intuitively expected, the spe-

cic (i.e., partial as dened above) effects related with the presence of C. acinaciformis were non-signicant. The data presented here (based on correlational observations only) are consistent with the hypothesis that there is a general gradient of anthropic inuence affecting the invertebrate species composition, and that the supposed effects of C. acinaciformis on the species composition are correlated with (and, therefore, indiscernible from) those associated with this general anthropic inuence. One of the main environmental values of the studied area is that 19 (20%) of the invertebrates surveyed were endemic to the Balearic Islands. Insular endemisms should be among the priorities of environmental management (Gillespie and Roderick, 2002) and it is assumed that invasive species have negative effects on endemic species (for example, in the Balearics Islands, Rattus rattus L. produces the depression of the diversity of endemic invertebrates in the littoral rocky shores; Palmer and Pons, 1996). Surprisingly, the number of endemic species per site does not seem to be related to the presence of C. acinaciformis or to the general gradient of anthropic inuence. The number of endemic species followed a complex pattern at the studied site, with minima reached not only near the two urban areas but also at seemingly undisturbed sites (Fig. 4). Some endemic species seems even prone to be present at disturbed sites. Similarly, other biodiversity estimators showed that undisturbed sites could be even less diverse than other sites closer to urban areas. Obviously, more data are needed to extrapolate these species-specic patterns to a broader spatial scale, but some groups of species are insensitive to extreme habitat modication (Lawton et al., 1998). Maximum richness is not always reached at undisturbed habitats, and each group display a specic pattern (Lawton et al., 1998). Therefore, biodiversity can experience little changes with disturbance. Contrasting, invertebrate species composition (especially if a broad taxonomical approach is used; Mattoni et al., 2000) is revealed as an appropriate alternative to analyse spatial gradients linked to anthropic effects.

Acknowledgments The authors thank Anna Traveset and Eva Moragues for the invaluable data supplied on dispersal capability and grow rate of C. acinaciformis, and the comments and suggestions of Lluis Gomez and two referees. This is a contribution to EC EVK2-CT-2000-00074 (EPIDEMIE).

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