Short-Term Response of Soil to Cover-Crop Removal in an Organic Olive Orchard in a Mediterranean Setting Author(s): Manuel Cárdenas, Juan Castro and Mercedes Campos Source: Journal of Insect Science, 12(61):1-18. 2012. Published By: Entomological Society of America DOI: http://dx.doi.org/10.1673/031.012.6101 URL: http://www.bioone.org/doi/full/10.1673/031.012.6101

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Short-term response of soil spiders to cover-crop removal in an organic olive orchard in a Mediterranean setting Manuel Cárdenas1a*, Juan Castro2b, and Mercedes Campos3c

1Department of Botany and Zoology, Masaryk University, Kotlářská 2, 61 137, Brno, Czech Republic 2Department of Environmental Protection, Estación Experimental del Zaidín (CSIC), Profesor Albareda nº 1, 18008, Granada, Spain 3IFAPA Centro Camino de Purchil, Junta de Andalucía, P.O. Box 2017, 18080, Granada, Spain Abstract This study shows that disturbance caused by cover-crop removal (CCR) in an organic olive orchard affects ground- populations. The effect of CCR on various organic olive-orchard plots was assessed by monitoring the abundance and diversity of ground-dwelling spiders. Covered plots in the organic olive orchard were compared with uncovered plots where the covers had been removed mechanically. CCR positively affected the most abundant spider species Zodarion styliferum (Simon) (Araneae: Zodariidae) as well as other species of running spiders belonging to the families Gnaphosidae and Lycosidae. Over time, the two types of plots did not significantly differ in diversity or dominance. Similarly, no differences were detected between the study plots in terms of the distribution of individuals when a cluster-similarity analysis was performed. This lack of difference in diversity might be due to the spatial scale used in the study or climatology. Because of their general effects, CCR profoundly changed the abundance of spiders in the olive orchard, but with no clear impact on spider diversity.

Keywords: Araneae, cover crops, disturbance, ground dwelling spiders, olive agroecosystem Abbreviations: CCR, cover-crop removal; CP, covered plot; UP, uncovered plot Correspondence: a [email protected], b [email protected], c [email protected], *Corresponding author Received: 1 March 2011, Accepted: 19 March 2012 Copyright : This is an open access paper. We use the Creative Commons Attribution 3.0 license that permits unrestricted use, provided that the paper is properly attributed. ISSN: 1536-2442 | Vol. 12, Number 61 Cite this paper as: Cárdenas M, Castro J, Campos M. 2012. Short-term response of soil spiders to cover-crop removal in an organic olive orchard in a Mediterranean setting. Journal of Insect Science 12:61 available online: insectscience.org/12.61

Journal of Insect Science | www.insectscience.org 1 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al.

Introduction The control of surface erosion from water in The olive-orchard agroecosystem represents olive orchards requires the constant presence one of the most important crops in southern of plant remains on the surface, mainly to Spain (Civantos 2004), and thus it is protect the ground from the direct impact of informative to study the impact that cover- raindrops (Castro 1993; De Luna 1994; crop removal (CCR), a supplementary land- Gómez et al. 2004). These complementary maintenance technique, exerts on the improvements in the soil’s physical, chemical, associated predator , particularly and biological properties favor biodiversity, spiders (Cárdenas et al. 2006; Cotes et al. by increasing the content of organic matter in 2009). CCR is vigorous farm work that the surface layers (thereby increasing subjects the ground and its inhabitants to a infiltration), reducing water loss through major disturbance, and is a prevailing cultural evaporation, and reducing lixiviation and practice in Spanish olive groves (Pastor 2004). nutrient leaching, thereby improving the water Farmers clear the ground for both fire balance in olive orchards. Consequently, if prevention and the positive aesthetic of clean olive orchards with crop covers are correctly olive fields. This cultural practice opposes the managed, good harvests and long-term recommendations of Cross-Compliance productivity are ensured (Castro et al. 2008). (Common Agricultural Policy, UE for erosion The tolerance of macroinvertebrate taxa to control: conditionality). Vegetal cover on the physicochemical stress has been widely used ground is known to protect against direct in the analysis and interpretation of field data scarring of raindrops and erosion. Aside from (Carlisle et al. 2005). Several spider studies this disadvantage, this study investigated demonstrate that disturbances such as fire whether CCR affects the spider fauna. (Urones and Majadas 2002), flooding (Bonn et al. 2002), agricultural management systems Land-maintenance systems in organic olive (Haskins and Shaddy 1986; Cattin et al. 2003; orchards are based on the use of cover crops, Pfiffner and Luka 2003), and the use of which are mechanically controlled with pesticides (Kennedy et al. 2001; Bell et al. mowers. The plant remains are either left on 2002) diminish spider abundance. the surface or buried, thereby eliminating the cover crop (Guzmán and Alonso 2004). Non- However, the effect that these disturbances organic olive orchards also practice CCR at may have on diversity will depend on the the end of spring, presumably because olive degree to which this disturbance affects the growers consider weeds to indicate neglect of particular ecosystem. Consequently, very orchard maintenance, and because they seek aggressive disturbances (i.e., fire) will to maintain an easily accessible and regular decrease the diversity of predators such as ground surface to pass with the tine harrow spiders, ants, and beetles—at least initially (Pastor 2004); that is, one of the types of (Oliver et al. 2000; Urones and Majadas harrows (secondary tillage for seedbed 2002). Other moderate disturbances can preparation or light surface cultivation) with augment species richness (Connell 1978), as an operating depth about 1-2 inches, and for example the temporary presence of operating speed from 4 to 7 miles per hour vegetation that could promote diversity, (NRCS 2005). according to the hypothesis that intermediate

Journal of Insect Science | www.insectscience.org 2 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. disturbances provide greater species diversity in an orchard called Peñaflor. The 25-ha than larger or smaller disturbances (Huston orchard consists of single-trunk cv. Picual 1979, 1994; Aronson and Precht 1995). In the olive trees Olea europa L. (Lamiales: case of spiders, an exception has been found Oleaceae) with crown diameters ranging from to this trend in areas with temporary 1.5 to 3 m, and annually increasing vegetation such as coastal dunes (Bonte et al. productivity currently between 20 and 30 2004), due to the narrow range of the kg/tree. The orchard was established in 1994 environmental variation studied. There are, with an 8 × 8 m planting pattern (156 olive however, examples of different taxa where trees/ha). The orchard has an underground this hypothesis of intermediate disturbance irrigation system and the olives are can be verified, such as in fouling mechanically harvested. Olive-orchard communities (Lenz et al. 2004). maintenance was conventional until 2002, and since 2005 the farm has been organically Spiders, an abundant and diverse group of certified. This organic farm was chosen in arthropods (Turnbull 1973), constitute a group order to eliminate the possible effects of of predators that can be classified into various pesticides on the fauna. groups according to their hunting strategy. For example, Uetz et al. (1999) distinguishes two Experimental design major guilds: active cursorial spiders and The land-maintenance technique used in the web-spinning spiders. These guilds, in turn, experiment was that of weed cover crops have other subgroups depending on their controlled by constant mowing. The mower ecological strategy. The short-term effects blade repeatedly strikes the ground, leveling (positive or negative) of the elimination of the soil and eliminating unevenness. The cover vegetation on the spider community in mowing frequency depended on the plant- an organic olive grove were investigated, as cover development, and normally the species well as how these effects developed completed their cycle and produced seeds. throughout the first months, since this is one Cover crops present in the plot were entirely of the most widely used techniques among dominated by native spontaneous grasses, non-tillage cultural practices in olive orchards. with clumps of Bromus sp., Hordeum sp., and In comparing disturbed and undisturbed olive Diplotaxis sp. All the species were annuals. groves, both the possible negative effects on During the study year, the cover was not abundance and diversity and the subsequent particularly well developed, and the cover immigration from adjacent areas could be species were Gramineae. documented. The aim of this study was to determine the impact of tine harrowing CCR, Pre-sample intervention (CCR) consisted of and thus the existence of bare ground, on land passing the tine harrow over the dry debris of arthropods, particularly ground-dwelling the plant cover cut by the mower. The tine spiders. harrow broke up the surface crust and broke apart the remains of the existing cover, mixing Materials and Methods them in the first few millimeters of the soil. The debris and seeds remained on the soil or Study site were partially buried. The harrow passed four The study was conducted in a large olive- times or until no debris remained on the soil growing area near Mancha Real, Jaén, Spain, surface. The areas under the tree crowns were

Journal of Insect Science | www.insectscience.org 3 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. subsequently cleared manually and all the four rows each with five trees were sampled, plant remains, fallen leaves, and fruit were for a total of 20 sampled trees per plot. removed with hand rakes. The weed characteristics under the crown were similar The sample season was selected according to to those between the rows of trees since the the phenology of the cover vegetation. Four crown diameter was small and gave negligible samplings were conducted in the year 2005: in canopy shade. the first sampling, the traps were collected 14 days after the disturbance during the last week Three experimental uncovered plots (UPs) of June; in the second sampling, 30 days after were chosen in which CCR was carried out as the disturbance, in the middle of July; in the described above during the first week of June third sampling, 70 days after the disturbance, 2005 (Figure 1A). In each plot, four rows each in the middle of September; and in the last with five trees were randomly sampled (20 sampling, 85 days after the disturbance, at the trees sampled in each plot), for a total of 11 × end of September. The first two samplings 11 olive trees in each frame plot sampled (121 were made to observe the short-term effects of trees; 0.77 ha). There was a minimum space CCR. The September samples provided data of 30 m between plots. In each plot, five trees on the time course of species abundance and were sampled, leaving one unsampled tree diversity. between analyzed trees. All the study plots were surrounded by olive A north-facing pitfall trap measuring 11 cm in orchards under organic management, diameter was placed and remained active for spontaneous grasses, and hedgerows with 48 hours. For the preservation of the spontaneous vegetation. individuals captured, the traps were filled with Scheerpeltz liquid (60% ethanol 97º, 38% Statistical analysis distilled water, 1% pure acetic acid, 1% Samples were transported to the laboratory glycerine). Pitfall traps, a relatively simple where the spiders were frozen and capture method for collecting active subsequently cleaned and identified to the arthropods on the soil surface, particularly lowest taxonomical level possible. The cryptic and nocturnal ones, constitute a individuals identified were adults and standard method for establishing the relative juveniles. After identification, statistical abundance of soil arthropods (Luff 1987). analysis was carried out using ANOVA non- However, this is not a good capture method parametric statistical tests (Kruskall-Wallis for web-building spiders in general. The fact test) for independent samples using the SPSS that a large majority of spiders recorded on program version 13.0. the olive-orchard soil were hunters was taken into account when the capture method was Species richness and diversity (closely chosen in order to reduce the error in correlated indices) were recorded because ecological studies of this type (Uetz and they were referred to as more representative Unzicker 1976). diversity measures for this group (Hill 1973).

This design was repeated in the same orchard in three control covered plots (CPs) where the cover was not cleared (Figure 1B). In these,

Journal of Insect Science | www.insectscience.org 4 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. Spider diversity (H ') was measured over the season using the Shannon-Wiener information index (Shannon 1948): where D is a measure of the dominance of the most abundant species in the community (range 0 to 1), Nm is the absolute abundance of the most common species in the community where H ' is the amount of observed diversity under consideration, and Ni is the overall in a community, S is the number of species density of all the species in that community. (species richness), and pi is the relative The higher the proportion of single species, abundance of the ith species. The greater the the more unevenly distributed is the species in number of species (S) and the more even their a community. abundance, the higher the diversity index H ' will be. The maximum possible diversity for a Menhincik’s richness index (Menhinick 1964) community can be calculated as follows: estimates the ratio of the number of taxa to the square root of the sample size:

Using the equitability index (Pielou 1966), the evenness of spider species representation in where D is the diversity, S is the number of the organic olive orchards was calculated as: species in whole distribution, a is a parameter by which the number of species is decreased with a reduced sample size, I is number of individuals in the whole distribution and b is a where H ' is the observed diversity as defined parameter expressing the reduction of sample in first equation, Hmax is the maximal possible size. diversity as defined in second equation, and E is the measurement of equitability. The Margalef’s richness index: equitability index ranges from 0 to 1, and the closer E is to 1, the more equally abundant are the species in the community under study. where S is the number of taxa and n is the Simpson’s Index (Simpson 1949) measures number of individuals. “evenness” of the community from 0 to 1. Dominance (1−Simpson index) ranges from 0 Equitability is Shannon diversity divided by (all taxa are equally present) to 1 (one taxon the logarithm of number of taxa. This dominates the community completely). measures the evenness with which individuals are divided among the taxa present.

Fisher’s alpha (Fisher et al. 1943) is a where ni is the number of individuals of taxon diversity index, defined by the formula i.

The Berger-Parker index was used to estimate dominance (Berger and Parker 1970):

Journal of Insect Science | www.insectscience.org 5 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. where S is number of taxa, n is number of abundant was Zodariidae, which represented individuals and α is the Fisher’s alpha. more than 82% of the individuals; For the diversity study, the diversity indices Gnaphosidae and Lycosidae represented 11.2 were calculated using the computer programs and 2.9% of the captures, respectively; and Ecosim 7.72 (Gotelli and Enstminger 2006), Sicariidae represented 1.1% (Table 1). For the divers 1.0 (Pérez-López and Sola-Fernández different species, the most abundant was the 1993), and PAST version 1.38 (Hammer et al. only species representative of the family 2006). Non-parametric statistical tests Zodariidae, Zodarion styliferum (Simon). The (Kruskall-Wallis test) were applied to these next species in order of abundance were two indices to verify the possible differences gnaphosids, Zelotes spp. and Zelotes tenuis (L. between handlings and dates. Koch) and one lycosid Lycosa ambigua (Barrientos), but in much lower abundance Cluster analysis allowed classified (Table 2). observations according to disturbance dates. The Jaccard index was used because it 70% of spiders were captured in UPs, while provided better information in terms of only 30% were captured in CPs. This pattern classification than other matching indices was the same among the most abundant (Finch 2005). families, such as Zodariidae, from which 70.4% of the individuals were collected from Results UPs. Something similar occurred with Gnaphosidae and Lycosidae, with 73.2% and Abundance 71.7% of individuals captured in UPs, A total of 2082 specimens were collected in respectively. However, in Sicariidae, the the pitfall traps placed in all the sampling greatest number of individuals was found in cycles, representing 15 families and 41 CPs (52.2%, Figure 2). This resulted in species. Of all the families captured, four significant differences in the total number of families (Zodariidae, Gnaphosidae, spiders between UPs and CPs (p < 0.01). For Lycosidae, and Sicariidae) represented almost the different families, Zodariidae, 98% of the collected specimens. The most Gnaphosidae, and Lycosidae presented

Table 1. Number of specimens collected in the different families over the sampling dates (in alphabetical order), (n) Number of species collected per family.

Journal of Insect Science | www.insectscience.org 6 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. Table 2. Total number of different species captured in the two treatments during the sampling cycles (species are grouped according to family).

significant differences with a greater significant differences were found between abundance in UPs in relation to CPs (all p < UPs and CPs for the total number of spiders 0.01). Sicariidae registered no significant and also for the families Zodariidae and differences in the number of individuals Gnaphosidae (all p < 0.01). After 70 days, collected between UPs and CPs (p > 0.05). significant differences were found only for the family Zodariidae, and also for the number of In each sampling, differences were noted for spiders collected (both p < 0.01). Finally, after the number of individuals collected and also 85 days, the previous case was repeated, with for the four main families between the significant differences for the family different plots (Figures 3A-E). At 14 days Zodariidae and for the total number of spiders after CCR, CPs and UPs did not significantly (both p < 0.01). differ (p > 0.05), whereas at 30 days,

Journal of Insect Science | www.insectscience.org 7 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. Throughout the sampling season, a The majority of the captured species belonged significantly greater number of spiders to the guild of cursorial spiders (families appeared in the first two samplings (end of Zodariidae, Gnaphosidae, Liocranidae, and June, mid-July) compared to the final two Lycosidae), followed by ambusher spiders samplings (mid-September and end of (families Oxyopidae, Philodromidae, September) (p < 0.01). In the UPs and CPs, Salticidae, Sicariidae, and Thomisidae), and differences were observed for the dates, with with little representation of web-building more individuals collected in the first two spiders, whether sheet-web builders samplings than in the last two samplings (both (Agelenidae and Filistatidae) or aerial-web p < 0.01, Figure 4). The most abundant family builders (Families Dictynidae, Linyphiidae, (Zodariidae) displayed significant differences Pholcidae, Theridiidae; Figure 5). Although between the first two and the last two there were no differences in the distribution of samplings (p < 0.01). This same trend was the captures between these groups of spiders, displayed in the Gnaphosidae and Lycosidae running spiders significantly differed between families with declining abundance, UPs and CPs (p < 0.01). No differences were respectively. In both cases, the differences in found for the other groups of spiders collected the number of captures between the first two (ambushers and sheet-web or aerial-web and last two samplings were significant (both builders, p > 0.05 in all cases). p < 0.01 respectively).

Table 3. Species abundance and diversity values calculated for the different plots studied, by date and cover handling (UP uncovered plots; CP covered plots).

Table 4. Family abundance and diversity values calculated for the different plots studied, by date and presence (C) or (U).

Journal of Insect Science | www.insectscience.org 8 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. Diversity in terms of the distribution between treatments The diversity results (Tables 3 and 4) gave a over time (Figure 8). total of 35 species belonging to 13 families in UPs and 27 species of 11 families in CPs. Discussion Significant differences appeared between CPs and UPs for species richness, this being Faunistic composition greater in UPs (p < 0.05). Throughout the In the present study, the taxonomical year, a greater number of species were composition of spiders for the most abundant observed in the first two samplings (those of taxa was limited to families of cursorial June and July) and a subsequent decrease in spiders: Zodariidae, Gnaphosidae, Lycosidae, the last two (Figure 6A). Similarly, the and Sicariidae. It also included other ground- number of families collected declined over the dwelling specialist spiders belonging to the sampling season (Figure 6B). families Theridiidae, such as Steatoda phralerata (Panzer) and Euryopis episinoides The diversity indices on the different (Walckenaer) (also ant-eaters, as zodariids), sampling dates did not show any significant and Thomisidae (Xysticus genus). differences for any of the indices calculated. Only in the case of Shannon’s diversity index In view of the sampling results, the were any significant differences recorded taxonomical composition of spiders was between the families collected in UPs and strongly influenced by at least two factors: those collected in CPs (p < 0.05) across all sample dates. (1) The small size of this year’s cover crop, due to the shortage of rain and high For all the families except Zodariidae, temperatures during samplings (Figure 9). significant differences were recorded for This presumably prevented greater differences Hulbert’s diversity index between UPs and from being recorded, and therefore families CPs (Chi-squared = 6.277; df = 1; p < 0.05). normally collected in olive orchards with low cover crops, as for example the family In terms of dominance, no significant Linyphiidae, were not collected here in large differences (p > 0.05) were detected between numbers due to the vegetation not having the plots on different sampling dates. However, sufficient size or structure necessary for the significant differences were found for placement of the laminar capture webs. dominance (which was greater in CPs) when Another example would be provided by the the family Zodariidae (p < 0.05) was excluded spiders of the genus Oxyopes (family from the analysis. Oxyopidae), which also inhabit this stratum of scant vegetation and are abundant in olive When a cluster analysis was performed, there orchards with crop cover (Cárdenas pers. were differences only for the time but not for obs.). the management (Figure 7). Additionally, there were no differences recorded in the (2) In addition, when the disturbance occurs distribution of families between UPs and CPs, (cover crop removal), this results in since the most abundant family (Zodariidae) colonizing species moving into this “empty” showed little similarity with the other families area from surrounding patches with crop cover, both from other covered plots and also

Journal of Insect Science | www.insectscience.org 9 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. from other bordering vegetation patches. (Heinze 1993). Ants modify their pattern of Therefore, in this experiment, species of exploitation of the area after the disturbance. Gnaphosidae (e.g., various species of the The same presumably occurred in our study as genus Zelotes) were captured in similar in other cases of disturbances (e.g., fire) in numbers in the two types of plots, since errant that abundance first increased, but then spiders colonize the free space. In the case of decreased progressively to reach values closer species of the family Lycosidae, such as to those of the undisturbed area (García et al. Hogna radiata (Latreille) and Lycosa 1995). Furthermore, Zodarion reportedly prey ambigua, one explanation could be the more easily on ant species of the subfamily territoriality exhibited by species of this Formicinae (such as Cataglyphis and family. Specimens without hunting territories Camponotus) than on species of the subfamily seek to increase prey availability (Moya- Myrmicinae (such as Messor or Tetramorium) Laraño et al. 2002) in these disturbed but as of (Pekár 2004). The ant-abundance results yet unoccupied plots. reveal greater abundance of individuals in the subfamily Formicinae (with more than 50% of Abundance the captures) in UPs than in CPs, where values The greater abundance found in plots where represented only 31% and Myrmicinae the crop cover was removed might be due to predominated, explaining the greater the greater capacity of species of cursorial abundance of these spiders in UPs (Campos et spider families (families Zodariidae, al. 2011). This appears to be due to the fact Lycosidae, and Gnaphosidae) to occupy the that ants of the subfamily Formicinae are space created after the disturbance by CCR. paralyzed more quickly by the venom of However, it should be emphasised that highly spiders of the genus Zodarion than that of the mobile species will be more frequently and subfamily Myrmicinae (Pekár 2005). abundantly collected in a pit-fall trap due to their behavior. Since Zodariidae frequently Few differences were found between CPs and construct silken retreats in ground debris UPs, perhaps because of the very sparse cover and/or below ground (Jocqué 1991; Ramirez in CPs, together with a low impact of the 1995), they found better shelter options in different agricultural practices. In summary, uncovered plots that offer a clear environment pitfall traps show insect activity that can be to place their shelter under stones as other higher under specific conditions (i.e. less Zodarion species (Pekár 2004). In fact, the structured vegetation). uncovered soil offers a lower resistance to spider dispersal compared to a covered soil, The families Lycosidae and Gnaphosidae causing an apparent increase in spider showed a trend similar to that of the family abundance. In the case of the family Zodariidae, with greater abundance in plots Zodariidae, these spiders—specialized ant- without a cover crop. Despite these eaters (Jocqué 1991)—could continue the differences, the time course of the captures in displacement criteria of their prey, some ant both plots proved similar (Figure 3). In both species, who take advantage of the space families, the disturbance (i.e., CCR) would created by the disturbance caused by cover cause a migration from areas with cover crop removal to colonize this free space and to crops, less prey, greater competition, other build their nests. Habitat structure is predators, and other spiders (with other fundamental for ant dispersal strategies hunting strategies), towards uncovered areas

Journal of Insect Science | www.insectscience.org 10 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. with more prey and less competition. Two taxonomic levels were used for the Furthermore, observation of the lycosids diversity results according to the two most revealed that they did not vary their widely used techniques: the taxonomic phenological cycle, registering a greater surrogacy for a rapid assessment of abundance in the months of June and July, and biodiversity in agroecosystems (Biaggini et al. declining in September. In the last sampling, 2007) and the trough species level (Bertrand no individuals of this family were collected in et al. 2006). any of the plots. When the dominant species in Z. styliferum Diversity was removed, the diversity results failed to Species richness significantly increased in reveal any significant differences except for uncovered plots because, like other organisms the diversity index of Hulbert’s PIE between (plants), disturbance temporarily elevated the CPs and UPs, with a greater diversity in UPs, importance of spontaneous/pioneer species, probably due to the taxonomical composition which were quickly replaced by other species of mainly spiders which actively move from better adapted over time (De Cauwer et al. one place to another. 2005; Cauwer et al. 2006). This affects herbivorous insect populations in different The results agreed with the fact that temporal ways (Pöyry et al. 2006) and thus affects variations in species abundance also affects predators (Hendrikx et al. 2007). the measure of diversity (Leponce et al. 2004). Time was found to be the most important The diversity results do not indicate any factor to explain spider species presence in differences except in the case of Shannon’s olive orchards. diversity index calculated for the families, which is one of the most appropriate diversity Finally, the results of the similarity cluster indices for litter-diversity measure in analysis revealed no clear grouping to indicate arthropods (Leponce et al. 2004). A greater a trend concerning the effects of an number of families in UPs would reflect the intermediate disturbance on species fact that, of these, the greatest number belongs distribution in the olive orchard (Figure 8). to spider families, the main characteristic of Additionally, the families did not show any which is a large dispersal capacity either pattern of distribution in accordance with the because of their hunting strategy as active degree of disturbance between UPs and CPs cursorial spiders (families such as Zodariidae, (Figure 7), although this might be due to the Gnaphosidae, Lycosidae, Sicariidae), or narrow time range studied. because of their high dispersal capacity (e.g., families Salticidae or Linyphiidae). Conclusions Differences in dispersal capabilities also occur with other arthropods, as in the case of These results indicate that a disturbance such coleopterans, in which the taxa with a higher as CCR in an olive orchard has a positive dispersal capacity (greater flying capacity) are effect on the abundance of certain spider the ones that first colonize rural and urban species, such as Z. styliferum and other areas that have been disturbed by humans running spiders of the families Gnaphosidae (Venn et al. 2003). and Lycosidae. Throughout the post- disturbance period, the differences found

Journal of Insect Science | www.insectscience.org 11 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al. between the CPs and the UPs were even more intermediate disturbance hypothesis. Journal pronounced in families such as Zodariidae of Experimental Marine Biology and Ecology than in other running spiders. 192: 1-14.

However, cover removal does not have a Bell JR, Haughton AJ, Boatman ND, Wilcox strongly significant effect on diversity. The A. 2002. Do incremental increases of the greater diversity found in the UPs might be herbicide glyphosate have indirect due to disturbance (i.e., CCR), which means consequences for spider communities? that taxa present in adjacent areas take Journal of Arachnology 30: 288-297. advantage of the newly created ecological niche to colonize it. Berger WH, Parker FL. 1970. Diversity of planktonic Foraminifera in deep-sea There is one finding that slightly complicates sediments. Science 168: 1345-1347. the conclusions and that could mask certain results—the large number of Z. styliferum Bertrand Y, Pleijel F, Rouse GW. 2006. individuals. In future samplings, it would be Taxonomic surrogacy in biodiversity useful to determine whether their high number assessments, and the meaning of Linnean responds to the direct effect of the disturbance ranks. Systematics and Biodiversity 4(2): 149- or is due to their normal population dynamics 159. in this region. Further studies are recommended at greater temporal and spatial Biaggini M, Consorti R, Dapporto L, scales in order to verify long-term effects of Dellacasa M, Paggetti E, Corti C. 2007. The an intermediate disturbance (e.g., CCR) on the taxonomic level order as a possible tool for abundance and diversity of soil spiders in rapid assesment of Arthropod diversity in olive orchards. agricultural landscapes. Agriculture, Ecosystems and Environment 122(2): 183- Acknowledgements 191.

We would like to thank the Soria-Herrera Bonn A, Hagen K, Wohlgemuth-von reiche D. family who owns the Cortijo Peñaflor for their 2002. The significance of flood regimes for facilities and interest in our study. Also, carabid beetle and spider communities in thanks to Carmen R. Rodriguez, María Luisa riparian habitats - A comparison of three Fernández, and IFAPA’s workers who helped major rivers in Germany. River Research in the collection and sample cleaning. We also Applications 18: 43-64. thank Harmut G. Göbel, Gustavo Hormiga, and Suresh Benjamin for their helpful Bonte D, Criel P, Vanhoutte L, Van comments on earlier drafts of this report. This Thournout I, Maelfait JP. 2004. The study was funded by the projects RTA 04- importance of habitat productivity, stability 083-C2-02 and AGL2005-00932. and heterogeneity for spider species richness in coastal grey dunes along the North Sea and References its implications for conservation. Biodiversity and Conservation 13: 2119-2134. Aronson MA, Precht WF. 1995. Landscape patterns on reef coral diversity: a test of the

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Figure 2. Mean number of individuals from the four main families collected in the covered and uncovered plots. High quality figures are available online.

Figure 3. Average number of individuals collected during Figure 1. (A) View of uncovered plots (UP) during season sampling (error bars represent ± SE). (A) Spiders (Araneae), (B) sampling. (B) View of covered plots (CP) during season sampling. Family Zodariidae, (C) Gnaphosidae, (D) Lycosidae, (E) Sicariidae. High quality figures are available online. High quality figures are available online.

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Figure 5. Mean number of captured spiders according to their hunting strategy. High quality figures are available online.

Figure 4. Time course of the mean number of captured spiders of the most abundant families in the study in the (A) uncovered plots and (B) covered plots. The left Y-axis represents the mean specimens of the Araneae order and Zodariidae family; right Y- axis represents the mean specimens of other families: Gnaphosidae, Lycosidae, and Sicariidae. The X-axis represents the time after CCR. High quality figures are available online.

Figure 6. Time course of diversity measured in terms of richness over the sampling season. (A) Species richness. (B) Time course of Figure 7. Dendrogram resulting from the multivariate analysis of diversity measured in terms of family richness over the sampling paired groups calculated for the Jaccard index. Correlation season. High quality figures are available online. coefficient 0.755. High quality figures are available online. Journal of Insect Science | www.insectscience.org 17 Journal of Insect Science: Vol. 12 | Article 61 Cárdenas et al.

Figure 8. Dendrogram resulting from the multivariate analysis of paired groups calculated for the Jaccard index. Correlation coefficient 0.9654. High quality figures are available online.

Figure 9. Temperature (ºC) and rainfall (mm) during sampling from Mancha Real meteorological station (Weather stations, Consejería de Agricultura y Pesca, Junta de Andalucía, 2006). High quality figures are available online.

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