Ecological Entomology (2008), 33, 202–212 DOI: 10.1111/j.1365-2311.2007.00958.x

© 2008 The Authors202 Journal compilation © 2008 The Royal Entomological Society

Introduction

The composition of species assemblages in a particular habitat is shaped by the complexity of the landscape and also by proc-esses occurring at that scale ( Benton et al. , 2003; Kruess, 2003; Clough et al. , 2005; Bianchi et al. , 2006 ). For example, large-

scale landscape characteristics, such as the amount of forests and semi-natural grasslands around focal habitats, are important for butterfly assemblages in focal patches ( Bergman et al. , 2004 ). Bommarco and Ekbom (2000) reviewed the effects of landscape complexity and food limitation. They concluded that fecundity of predatory carabid beetles increased with landscape heterogeneity and with the proportion of perennial crop in the landscape due to higher arthropod abundance and diversity. Likewise, the composition of agricultural landscapes influenced the density of sheet-web spiders (Linyphiidae) in crops, i.e.

Correspondence: Efrat Gavish-Regev, Mitrani Department of Desert Ecology, Ben-Gurion University of the Negev, Sede-Boqer Campus, 84990 Midreshet Ben-Gurion, Israel. E-mail: efratg@bgu.ac.il

Migration patterns and functional groups of spiders in a desert agroecosystem

E F R AT G AV I S H - R E G E V 1 , 2 , YA E L L U B I N 2 and M O S H E C O L L 3

1 Department of Life Sciences, Ben-Gurion University, Beer-Sheva, Israel , 2 Mitrani Department of Desert Ecology, Blaustein

Institutes for Desert Research, Ben-Gurion University, Midreshet Ben-Gurion, Israel and 3 Department of Entomology,

The Hebrew University of Jerusalem, Rehovot, Israel

Abstract . 1. Arthropods living in annual crops suffer mortality caused by agricultural practices. Therefore, migration from surrounding habitats is crucial to maintain populations of natural enemies of insect pests in crops. In desert agroecosystems there is a pronounced contrast between managed and unmanaged habitats, where irrigated and fertilised crops are islands of productivity in an arid matrix. This contrast could either enhance or inhibit movement of natural enemies between the landscape components.

2. The importance of the surrounding arid habitats as a source for spiders in crops was examined in the Negev desert of Israel. Spiders were sampled in both arid natural habitat and adjacent wheat fields using pitfall traps and visual searching. In addition, spiders in wheat fields were sampled throughout the winter cropping season using emergence traps at increasing distances from the field edge. Stationary and movable emergence traps were used to distinguish between residents and migrant species.

3. The spider assemblage in the wheat was dominated by three families: Linyphiidae, Theridiidae, and Gnaphosidae. Spider sampling in both natural arid habitat and adjacent wheat fields enabled four functional groups to be recognised that differed in habitat preference, movement patterns, and population dynamics. Thirty-three per cent of collected individuals were classified as crop residents whereas more than 50% were classified as migrants from the surrounding habitats. These findings suggest that the surrounding habitats influence spider assemblage composition in the fields, in spite of the marked contrast in habitat structure and productivity.

4. Spider assemblages in the wheat fields were dominated by migrant species arriving from the surrounding arid habitats. Migrant spiders inhabited the crop throughout the cropping season. The combined contribution of resident and migrant functional groups may act to prevent insect pest outbreaks in this desert agroecosystem.

Key words . Araneae , arthropods , assemblage , generalist predators , habitat contrast , movement patterns , natural arid habitats , pest suppression , wheat .

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landscapes with higher non-crop habitat area promoted higher spider densities ( Schmidt & Tscharntke, 2005a ). Moreover, spi-der species richness was higher in more complex agricultural landscapes ( Schmidt et al. , 2005 ).

Agricultural landscapes are a matrix consisting of crop and non-crop elements (i.e. agricultural and natural or semi-natural habitats), each with its own distinctive species assemblage and abiotic characteristics. An overlap in species composition be-tween these two landscape components can occur when mobile species move between habitats ( Bishop & Riechert, 1990; Wissinger, 1997; Bommarco & Ekbom, 2000; Schmidt & Tscharntke, 2005b ). For arthropods living in annual crops, mi-gration can be important, especially because of the high mortal-ity of field-inhabiting species inflicted by agricultural practices. Hence, individuals either recolonise annual crop fields from the surrounding habitats ( Wissinger, 1997; Thorbek & Bilde, 2004 ), or survive in the fields between successive cropping cycles. Consequently, the proportion and types of the surrounding habi-tats, their proximity to crop fields, permeability of the boundary ( Duelli et al. , 1990 ) and the degree of contrast between the crop and non-crop landscape elements may all influence the species composition in crop fields ( Dennis et al. , 2000; Landis et al. , 2000; Sunderland & Samu, 2000; Collinge & Palmer, 2002; Dauber & Wolters, 2004; Tscharntke et al. , 2005 ).

These landscape-level factors should be more pronounced in desert agroecosystems than in temperate ones. The contrast be-tween crop and non-crop elements is high in arid agroecosystems. Crop fields are irrigated and fertilised as opposed to the non-crop areas that suffer from water deficiency and nutrient-poor soils. In addition, fields planted with annual crops are relatively simple and of uniform structure with a high percentage of green leaf area. The surrounding arid habitats, however, are covered with annuals only for a short period, during or after the rainy season, and con-sist mostly of dry thorny plants for the rest of the year. Furthermore, the boundary between the crop and the surrounding desert be-comes more pronounced as the crop grows taller. Thus, cursorial migration by arthropods may be favoured in the beginning of the season, when the boundary is less pronounced and the contrast between habitats is relatively low ( Collinge & Palmer, 2002 ).

Three main movement patterns can occur between neigh-bouring habitat types. The first pattern is a unidirectional move-ment, i.e. a source – sink relationship, in which individuals migrate from a habitat where their population growth rate is positive to a habitat where their growth rate is negative ( Pulliam, 1988 ). Such migration could occur in a desert agroecosystem due to seasonal preference for the crop field. The second pattern is a bidirectional movement, for example cyclic colonisation, in which individuals migrate from their permanent habitat to a sea-sonal habitat when this habitat is preferred, and then back to the permanent habitat when the seasonal habitat become hostile ( Wissinger, 1997 ). The third pattern is that of negligible move-ment of individuals between habitats. This could happen when one habitat is unsuitable, and as a result the species will have a metapopulation structure, with individuals moving between patches of habitat of one type and having to traverse patches of unsuitable habitat ( Hanski & Gilpin, 1991; Hanski, 1998 ). In the case of the arthropod communities in desert agroecosys-tems, where the habitat types are strongly contrasting, all of

these movement patterns could take place: specialist species will have a preference for one of the habitat types, while oppor-tunistic species may use both habitats to different degrees. Nevertheless, because of the large contrast between crop fields and matrix in this agroecosystem, it could be expected that the opportunistic-migrant component will be poorly developed.

Spiders (Araneae) are mobile generalist predators that are abundant in agroecosystems ( Riechert & Lockley, 1984 ), in part because of their ability to recolonise fields after disturbance ( Bishop & Riechert, 1990 ). It has been suggested that spiders could suppress insect pests in crops in mesic areas if they reach high abundance early in the season, before the pest outbreak ( Nyffeler & Sunderland, 2003 ). Spiders have two dispersal modes, cursorial and aerial. Cursorial migration usually serves spiders for short-distance dispersal of up to a few dozen metres. Aerial migration by ballooning is a random dispersal process and enables long-distance movement (hundreds of metres to several kilometres). Ballooning is usually performed by juve-niles, although adults of many small species also use this mode of dispersal ( Bell et al. , 2005 ).

The potential role of spiders as natural enemies of insect pests in agroecosystems can be viewed according to the functional group concept. This concept defines a group of species that uti-lise resources in a similar way and have a similar function in the ecosystem ( Simberloff & Dayan, 1991; Blondel, 2003 ). The definition of a functional group is based on one or more com-mon characters of a group of species, such as morphology, be-haviour or ecology ( Davic, 2003 ). Given that spiders share insects as a common food resource, spider functional groups were defined according to the spider’s potential spatial and tem-poral use of insects in the fields. Sampling in both arid natural habitats and adjacent wheat fields enabled us to determine a spe-cies’ habitat choice, namely the spatial component of resource use. Sampling in wheat throughout the cropping season and in three distances from the field edge enabled us to determine the between-habitat movement pattern (i.e. both spatial and tempo-ral components). Using these characters, four spider functional groups were defined. The concept of functional groups allowed us to simplify ( Simberloff & Dayan, 1991; Perner & Voigt, 2007 ) and better understand the processes that determine the spider assemblage composition in an arid agroecosystem.

The objective of this study was to assess the importance of the surrounding natural desert habitats as a source for generalist predatory spiders, and to investigate how the desert landscape influences the dynamics of spider populations in crop fields. The specific goals were to: (i) recognise the functional groups that comprise the spider assemblage in a desert agroecosystem; (ii) identify the taxa in each functional group; and (iii) describe their life history and population dynamics in the crop.

Materials and methods

Study area

The study site was situated in Sede Teiman in the northern Negev desert, Israel, about 7 km north-west of Be’er Sheba (31°18 � N, 34°41 � E). Spider sampling was carried out in an area

204 Efrat Gavish-Regev, Yael Lubin and Moshe Coll

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of 5 km that included three wheat fields (46, 94, and 108 ha in area) and their surrounding natural and semi-natural desert hab-itats. The fields were not treated with pesticides. Recently, sev-eral insect pests (leaf aphids, bugs, beetles, and others) have become abundant in the northern Negev wheat fields. After the wheat growing season (October to February/May), the fields were planted with sunflowers (March to August), maize (July to September), or cotton (July to September). The crops were grown under conventional cultivation practices and with irriga-tion. The surrounding habitats include loess plain, slopes, and wadis (dry river beds) with desert shrubs and geophytes ( Noaea mucronata , Prosopis farcta , Asphodelus aestivus , Carthamus sp., Aellenia hierochuntica and Atriplex spp.) and annual plants in spring. In 1994 – 1995, Eucalyptus spp. trees were planted in some wadis, and Tamarix spp. and Acacia spp. in the surround-ing loessial habitats. Precipitation occurs in winter (November to February, mean annual rainfall 170 mm) in the form of spo-radic and unpredictable rainfall events.

Spider sampling in wheat and adjacent natural habitat

Spiders were sampled using two complementary methods in order to avoid skewed data caused by non-representative sam-pling ( Lang, 2000 ). Ground-level pitfall traps were used in or-der to catch the ground-dwelling and cursorial dispersing spiders, and a visual search on plants was carried out in order to catch the plant-dwelling spiders. In addition, emergence traps were used to detect changes in spider presence and hatching of egg sacs over time.

Spiders were surveyed in February 2003, in both the arid natu-ral habitat and adjacent wheat fields using pitfall traps and visual search. This sampling helped to identify the spider’s habitat choice and therefore was used to identify the functional group members.

A total of 240 pitfall traps were placed in three wheat fields and adjacent natural habitats. The pitfall traps were set at 10 randomly selected rows in each of the fields and natural habi-tats. Each field contained 30 traps, with three traps per row, po-sitioned at 5, 50, and 150 m from the edge of the field. Each adjacent natural habitat contained 150 traps, with five traps per row, positioned at 5, 25, 50, 100, and 150 m from the edge of the field. Each pitfall trap was made of two plastic cups (one inside the other; 12 × 10 cm, height × Ø), buried in the ground such that the rim was level with the ground surface.

In addition, a total of 18 visual search samples were con-ducted in the crop and natural habitats. The samplings were ran-domly assigned into one of the pitfall rows at one of the distances. This resulted in three plots (plot size: 1 × 1 m, width × length) in each of the fields and natural habitats. The sampling followed the same procedure, which included hand collection for 15 min of all spiders from the ground and vegetation, in the plot.

Emergence traps in wheat

Spiders were sampled in the wheat fields throughout the win-ter growing season of 2002 – 2003. Emergence traps were used to find which spiders migrate to the fields from the natural habitats

and which are residents of the crops, as well as to obtain quanti-tative data on the abundance of the spiders in the fields. Both stationary and movable emergence traps were used. Stationary emergence traps were placed in the field at the beginning of the crop season and remained at the same location throughout the growing season. The spiders caught in these traps had either sur-vived in the soil between cropping cycles, or were young that emerged from egg sacs deposited either by surviving spiders or by spiders in the previous season, or they could be migrants that had arrived early in the season before the traps were established. Movable emergence traps were relocated after each sampling. Thus, movable traps were expected to catch all of the above groups (surviving residents and their offspring) as well as spi-ders that immigrated into the field later in the season.

Each emergence trap was made of a metal cylinder (50 × 20 cm, Ø × height), buried approximately 7 cm in the ground, and sealed on top with a weighted plastic cover. Ventilation was provided by an opening (Ø 15 cm) in the centre of the cover that was covered with spider-proof mesh fabric. Two pitfall traps were placed in each emergence trap. Each pit-fall trap was made of two plastic cups (one inside the other; 12 × 10 cm, height × Ø), buried in the ground such that the rim was level with ground surface, and containing 100 mm ethylene glycol (antifreeze) diluted with water (1:1 by volume).

A total of 72 traps were used and were sampled on seven trap-ping events throughout the cropping season. The emergence traps were set in eight randomly selected rows in each of the three fields immediately after the wheat was sown. In each row, three emergence traps were positioned at 5, 50, and 150 m from the edge of the field. In each field, the emergence traps in four of the rows were stationary traps, whereas the remaining four rows were movable traps. These traps were moved every 2 weeks to four new randomly selected rows. The distance from the border of the field was kept constant for each trap throughout the grow-ing season. On each sampling date all the spiders found within each emergence trap and in the pitfall traps were collected. The procedure was repeated every 2 weeks from wheat sowing to harvest (18 October 2002 to 11 February 2003 respectively).

Spider identifi cation

Spiders were kept in 70% ethanol prior to sorting and identi-fication. All specimens were identified to species or morpho-species, except for juveniles that were identified to the genus or family level. Spiders were identified using the national arachnid collection (Department of Evolution, Systematics and Ecology, The Hebrew University of Jerusalem, Israel) and taxonomic lit-erature ( Levy, 1985, 1998; Roberts, 1995; Dippenaar-Schoeman & Jocque, 1997; Nentwig et al. , 2003; Proszynski, 2003 ). Owing to the large number of juveniles that were trapped, the analyses in the study were conducted at the family level.

Functional group identifi cation

Functional group members were assigned according to their habitat choice (wheat field vs arid natural habitat) and

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between-habitat movement (migration type and pattern), re-sulting in four functional groups. The response curves method was used (explained in detail in the Statistical analysis sec-tion) to confirm this grouping.

Statistical analysis

Ordination methods were used to identify spider habitat choice and to examine the patterns of spider colonisation of the crop fields over time. Redundancy analysis (RDA) was per-formed testing habitat (field, natural habitat) and trapping method. Partial RDA ( canoco for windows 4.5; ter Braak & Smilauer, 2002 ) was performed testing time (a continuous vari-able), trap type (movable or stationary), and distance from the edge (a continuous variable) as separate main effects while the other effects served as co-variables. Monte Carlo permutation (4999 permutations, main effects: design-based permutation; interactions: model-based permutation) was used to test the sig-nificance of the ordination axes ( ter Braak & Smilauer, 2002; Leps & Smilauer, 2003 ).

The response curves method ( Leps & Smilauer, 2003 ) was used to confirm the functional groups to which different fami-lies were assigned, under the assumption that functional groups respond differently in abundance to the environmental gradi-ents. The environmental gradients in this analysis are the first-order interactions, i.e. the pairwise interactions between time, trap type, and distance. The response to these interactions demonstrates differences in movement patterns of spiders, i.e. early or late migrants versus permanent inhabitants (residents). Response curves were fitted using, for the y -axis, the scores of the first axis obtained in the partial RDA plotted against each interaction. The response variable is thus a measure of the abundance of the families that were affected significantly by the first-order interactions. The curves were fitted using GAM (Generalised Additive Model: smooth term complexity with 3 d.f.). A Poisson distribution was assumed for the response variable, and Log was used as the link function. Curve selec-tion was based on the Akaike information criterion (AIC) ( Leps & Smilauer, 2003 ). For all ordinations the row data for

Table 1. Ordination results showing the effect of habitat and trapping method on the spider family composition in a desert agroecosystem: Monte Carlo permutation tests (4999 runs) of redundancy analysis (RDA) testing habitat [three arid natural habitats (NH) and three adja-cent fi elds] and trapping method (pitfall trap, visual search).

Predictor Variance explained F P

Habitat (natural, crop) 0.46 8.61 0.003 Trapping method (pitfall, visual search)

0.08 0.85 0.401

Interaction Habitat (arid) × trapping method

0.12 2.50 0.089

Habitat (crop) × trapping method

0.04 0.85 0.417

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Fig. 1. Spider family composition of a desert agroecosystem from two habitats and two trapping methods (pitfall traps and visual search): an ordination diagram from a redundancy analysis (RDA) of 12 samples from three wheat fi elds and three adjacent arid natural habitats (NH). The families are labelled by the fi rst three letters of the family name for this fi gure and for subsequent fi gures: LIN, Linyphiidae; GNA, Gna-phosidae; THE, Theridiidae; PHI, Philodromidae; LYC, Lycosidae; ZOD, Zodariidae; SPA, Sparassidae; ZOR, Zoropsidae; SALT, Saltici-dae; THO, Thomisidae; and CLU, Clubionidae; LIO, Liocranidae; OXY, Oxyopidae.

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Fig. 2. Rank abundance of spider families collected in wheat fi elds based on season-long captures in emergence traps during winter 2002 – 2003 ( n = 1622). The families are arranged along the x -axis from the most abundant, on the left, to the rarest family on the right. Individuals ( n = 107) whose family affi liation is yet to be determined were ex-cluded from the analysis.

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Fig. 3. Spider family composition based on seven sampling dates, at three distances from fi eld edge, and from two trap types. Ordination diagrams from a redundancy analysis (RDA) of 126 samples from three wheat fi elds: (a) biplot (family – environment) ordination diagram of the fi rst and second axes, (b) biplot (family – environment) ordination diagram of the fi rst and third axes. The arrow type of each fam-ily differs according to the functional group as fol-lows: residents – fi lled arrow with solid line; mi-grants – fi lled arrow with dashed line; arid – empty arrow with dotted line; rare families – small empty arrow with dotted line. The quantitative environ-mental variables are distance from fi eld edge (Dist) and time in the season (Time); the qualitative vari-able is trap type, represented by two categories (Movable, Stationary). See Fig. 1 legend for family abbreviations.

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each trap type in each field were grouped due to a low number of captures and high variances between individual traps.

In addition, a general linear model analysis ( SAS, 2001 ) was per-formed for each of the three most abundant spider families to test

differences in their abundance between trap types (stationary and movable) and distance from the field edge over the season. Time in the season, field, distance, trap type, the interactions between time and distance, and time and trap type were used as predictors.

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Results

Spider assemblages, family composition and habitat choice in a desert agroecosystem

A total of 194 individual spiders were collected in pitfall traps and using visual search in both crop and natural habitat. The family composition differed significantly between habitat types (crop vs natural), and in the natural habitat there was a trend for a difference between trapping methods ( Table 1 ). Linyphiids mainly, but also sparassids and zoropsids were abundant in the crop (negative values on axis 1, Fig. 1 ), whereas all other families had higher abundance in the natural habitat (positive values on axis 1, Fig. 1 ). In addition gna-phosids, thomisids, lycosids, salticids, and liocranids were more abundant in the pitfall traps in the natural habitat (posi-tive values on axis 2, Fig. 1 ), as opposed to theridiids, zodari-ids, oxyopids, and philodromids, which were more abundant in the visual search in the natural habitat (negative values on axis 2, Fig. 1 ).

Family composition of the spider assemblage in wheat

A total of 1729 individual spiders were collected from the emergence traps, belonging to 11 families. The spider assem-blage in the wheat fields was dominated numerically by three families: Linyphiidae, Gnaphosidae, and Theridiidae. These three families represented only 27% of the families, but 84.5% of the collected individuals: Linyphiidae with 33% of the total individuals, Gnaphosidae with 31.8%, and Theridiidae with 19.6% of the total individuals ( Fig. 2 ).

Figure 3 shows the family composition in the different trap types at three distances from the field edge and throughout the season. The family composition is distinct over time between the trap types and by distance from the edge (see also Table 2 ). Linyphiids, theridiids, gnaphosids, and lycosids increased in abundance with time (positive values on axis 1, Fig. 3a,b ), whereas salticids, philodromids, and clubionids decreased in abundance with time (negative values on axis 1, Fig. 3a,b ).

Theridiids, lycosids, gnaphosids, philodromids, clubionids, thom-isids, and salticids were more abundant in the movable traps (posi-tive values on axis 2, Fig. 3a ). Only linyphiids were more abundant in the stationary traps (negative value on axis 2, Fig. 3a ) and there-fore this family characterises the stationary traps. Thomisids and zodariids were found exclusively closer to the field edge [negative values on axis 1 ( Fig. 3a ) and axis 3 ( Fig. 3b )].

Functional groups of the spider assemblage

The spider assemblage as determined by the emergence traps was composed of four functional groups that differed in their habitat choice (field vs natural habitat, Fig. 1 ) and in abundance in the trap types, distances, and time in the season, correspond-ing to their different migration patterns. The resident functional group was represented solely by linyphiid species that were present in the fields from the beginning of the cropping season. These spiders were caught almost exclusively in the crop ( Fig. 1 ), where they were numerically dominant in stationary traps, and increased in abundance with time and distance from the field edge ( Fig. 4a – c ). The second and third groups are the migrant functional groups, found in both habitats ( Fig. 1 ), and consisting of species that migrate into crops from the surround-ing natural habitats. The early migrants are cursorial dispersers (caught in pitfall traps in the natural habitats) and were repre-sented mainly by gnaphosid species that showed similar abun-dances in both emergence trap types early in the season and close to the edge, but had lower abundances both in the station-ary emergence traps distant from the edge and in the movable emergence traps late in the season ( Fig. 4a,c ). The late migrants are aerial dispersers that were caught in visual searches in the natural habitats, but not in pitfall traps. This group is repre-sented mainly by theridiid species that show higher abundances in movable emergence traps late in the season, without a dis-tinct pattern of distance from the edge ( Fig. 4a ). The fourth group consists of typical arid habitat species ( Fig. 1 ) and in-cludes spiders with low abundances in the crop both over time and with distance from the edge (Philodromidae, Zodariidae, Fig. 4b ).

Table 2. Ordination results showing the effect of time, trap type, and distance from the edge on the spider family composition in wheat: Monte Carlo permutation tests (4999 runs, main effects: design-based permutation; interactions: model-based permutation) of the partial RDA (redundancy analy-sis), testing time (a continuous variable), trap type (movable or stationary), and distance from fi eld edge (a continuous variable) as separate main effects while the other effects serve as covariables.

Predictor Trace F P

Main effects Time (seven dates, continuous) 0.133 23.70 0.002 Trap type (two categories): movable, stationary 0.057 10.07 0.002 Distance (three, continuous): 5, 50, and 150 m 0.028 4.91 0.004

First-order interactions (Block defi ned model-based permutations) Crop, distance Time × trap type 0.041 7.71 0.002 Crop, trap type Time × distance 0.022 3.96 0.012 Crop, time Trap type × distance 0.014 2.57 0.040 Second-order interactions (Model-based permutations)

Time × distance × trap type 0.013 1.30 0.260

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Population dynamics and life history

Sequential sampling in the fields over the cropping season and at different distances from the field edge allowed us to de-termine the pattern of population dynamics and life history of the three dominant families in the wheat: Gnaphosidae, Theridiidae, and Linyphiidae. Time in the season had signifi-cant effects on all three families, and distance from the field edge and trap type had significant effects on at least on one of the three families ( Table 3 ). Gnaphosids were found in signifi-cantly higher numbers in distant traps at the end of the season than in distant traps at the beginning of the season. They oc-curred in significantly lower numbers in the movable traps to-ward the end of the season (interactions between time × trap type and time × distance). Theridiids were found in signifi-cantly higher numbers late in the season and especially in the movable traps toward the end of the season (interaction be-tween time × trap type). There was no significant difference in the numbers of theridiids at different distances from the field edge, nor in the interaction between time × distance. There was no significant difference in the numbers of linyphiids in the time × distance or time × trap type interactions, nor in distance from the field edge. Linyphiids were found in signifi-cantly higher numbers in the stationary traps than in the movable traps.

Figure 5 shows the abundance of juveniles, sub-adults, and adults plotted against time in the season. Linyphiidae were found in all developmental stages (juveniles, sub-adults, and adults of both sexes) throughout the crop season. The number of females increased continuously during the season ( Fig. 5a ). Male abun-dance peaked toward the middle of the season, and juveniles were found in higher numbers from the middle of the season and onward ( Fig. 5a ). Gnaphosid juveniles were abundant in the fields from early in the season while sub-adults increased in numbers toward the end of season ( Fig. 5b ). Contrary to the linyphiid pattern, only a few adult male gnaphosids were found and only one adult female was collected at the end of the season ( Fig. 5b ). Theridiid juveniles appeared only toward the second third of the season with peak density in the middle of the season. Although the density of sub-adult males of this family also in-creased at that time, no adult females were found during the cropping season ( Fig. 5c ).

Discussion

Spider assemblages in the sampled wheat fields in the north-ern Negev desert were composed of four functional groups, each with a unique combination of migration pattern, habitat preference, and population dynamics. The resident spiders (Linyphiidae) were found in higher abundances in the station-ary traps. Only spiders from this group had mature females and males during the cropping season, and new hatchlings appeared in the stationary traps throughout the season.

Early migrants (Gnaphosidae) were found in large numbers early in the season and were equally abundant in both trap types. The trapping pattern suggests that cursorial migration takes place from the edge toward the field centre: the abundance of

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Fig. 4. Response curves of the most abundant spider families to the fi rst-order interactions. See Fig. 1 legend for family abbreviations. Only sig-nifi cant curves are presented and fi tted using generalised additive models (GAM): (a) response curve for Time × Trap type; (b) response curve for Time × Distance; (c) response curve for Distance × Trap type.

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Table 3. The effect of time, trap type, and distance from the edge on the three dominant families: Linyphiidae ( n = 563); Gnaphosidae ( n = 550); and Theridiidae ( n = 293) in wheat (general linear model of the average number of spiders per trap in wheat, signifi cant parameters are given in bold).

Parameter (levels) d.f.

Theridiidae Linyphiidae Gnaphosidae

F P F P F P

Time in season (7) 6 20.87 <0.0001 6.31 <0.0001 4.52 0.0004 Field (3) 2 4.29 0.0164 15.66 <0.0001 2.00 0.1398 Distance (3) 2 0.14 0.8674 2.57 0.0815 6.65 0.0020 Trap type (2) 1 50.26 <0.0001 9.18 0.0031 1.73 0.1910 Time × distance 12 0.59 0.8373 0.95 0.4946 1.83 0.0532 Time × trap type 6 5.75 <0.0001 1.49 0.1897 3.21 0.0065

gnaphosids was greater close to the field edge early in the sea-son, and later on the numbers increased in the distant traps ( Table 3, Fig. 4b ). These cursorial migrants started their disper-sal as juveniles before the wheat was sown and continued to en-ter the fields throughout the season. Their movement was slower toward the end of season, perhaps because of the increase in vegetation density. This group differs from the residents because individuals did not appear to reproduce during the cropping sea-son. Most gnaphosids are relatively large spiders; as such they are likely to be exposed to injury by tilling and plowing and therefore are unlikely to survive in the field from one season to the next.

Late migrants (Theridiidae) were caught in large numbers in the movable traps, but only from the end of the first third of the season [positive correlation with the interaction between mova-ble traps and time ( Table 3, Fig. 4a )]. Their equal distribution across distance suggests aerial migration from the surrounding habitats. These late season migrants were probably unable to re-produce during the cropping season, because no adult females were found in the fields during the season.

The fourth group constituted the arid habitat species . These spiders were found at the edge of the field early in the season but did not penetrate the fields. The same spider species were col-lected from the surrounding habitats ( Fig. 1 ).

This study provides the first data on patterns of migration of predatory arthropods between natural and managed habitats in a semi-arid agroecosystem. Temporal sampling with two types of emergence traps – stationary and movable – provided a detailed picture of the colonisation of these fields by resident and migrant functional groups of spiders. Owing to this strong temporal component, as well as the large area of the crop fields, sampling more than three fields was unfeasible. Thus, at present, generalisation beyond the spatial scale of the study is not possible. Nevertheless, there were no significant differ-ences between the three fields in any of the observed patterns, which suggests that these patterns are accurate at a larger scale.

Linyphiid spiders in desert agroecosystems: residents or aerial migrants?

Linyphiid species are generally abundant in temperate agro-ecosystems ( Nyffeler & Sunderland, 2003 ) and potentially are

important natural enemies of insect crop pests ( Harwood et al. , 2001, 2003, 2004 ). Linyphiidae was the numerically dominant family in crop fields in this desert agroecosystem as well. This family is usually found in humid habitats and was rare in the natural arid habitats in the present study. Indeed, most of the linyphiid species trapped in the crop fields did not occur in the surrounding natural arid areas (E. Gavish-Regev, Y. Lubin and M. Coll, unpublished data). Therefore it is important to under-stand the dynamics, dispersal pattern, and survival of these spi-ders in such a hostile environment. In the crop fields, linyphiids were found in the stationary traps throughout the season and were represented by all developmental stages. This pattern is consistent with a resident status in the crop. The short life cycle of these small spiders, the negligible captures of these species in the surrounding habitats, and their abundance in temperate agro-ecosystems support the view that linyphiids are indeed resi-dents of wheat fields in this desert agroecosystem. They are able to reproduce in the fields and likely remain in the soil between cropping season. Nevertheless, two other scenarios cannot be excluded. The first involves metapopulation dynamics, whereby individuals might exhibit bidirectional movement between dif-ferent crop fields, or between crop fields and some more suita-ble semi-natural habitats, such as other planted vegetation. In the extensive sampling in this ecosystem carried out in the present study, no evidence was found for massive ballooning or cursorial dispersal of linyphiid species into or out of crop fields. However, the planted vegetation was not sampled extensively and trees such as Eucalyptus spp., Tamarix spp., and Acacia spp. might serve as summer shelter sites for these spiders.

The second possible scenario involves long-distance aerial dispersal by ballooning. In this case, the linyphiids might have a source – sink relationship, with more mesic Mediterranean agroecosystems to the north as source habitats. Such habitats could be found for example in the NW Negev, the southern coastal plain and the Judean foothills (20 – 60 km away). Spiders inhabiting such areas could possibly arrive in the northern Negev through aerial dispersal. Schmidt and Tscharntke (2005a, b) found that linyphiid spiders ballooned to crop fields from the surrounding habitats, but also from more distant locations in the landscape. Although massive bal-looning was not detected in Israel, a small number of migrants could be sufficient to start a population in the crops. To resolve these issues, further investigation of ballooning and large-scale sampling is required.

210 Efrat Gavish-Regev, Yael Lubin and Moshe Coll

© 2008 The AuthorsJournal compilation © 2008 The Royal Entomological Society, Ecological Entomology, 33, 202–212

Spider assemblage in wheat fi elds and the infl uence of non-crop elements on the desert agroecosystem

More than 50% of the individuals collected in the emergence traps belonged to migrant functional groups. These findings suggest that the crop fields in desert agroecosystems resemble temperate agroecosystems in the way they interact with the sur-rounding natural habitats ( Schmidt & Tscharntke, 2005b ). Even though the natural and semi-natural desert habitats and the irri-gated crops in the desert agroecosystem differ markedly, some desert species can utilise both habitats. Some of these species are early season and others are late season migrants into the crops. Thus, the surrounding desert habitats have the potential to serve as a source of generalist predators that may act as natu-ral enemies of insect pests in the crops ( Dennis & Fry, 1992; Pfiffner & Luka, 2000 ).

This study is a first stage in the authors’ efforts to understand the factors that determine spider assemblages in desert agroeco-systems, where irrigated crop fields are islands in an arid ma-trix. The different non-crop elements in desert agroecosystems may play an important role in promoting a diverse generalist predator assemblage, which may provide biological suppression of insect pest populations ( Marc & Canard, 1997; Altieri, 1999; Marc et al. , 1999 ). Understanding the role of each of the four functional groups (residents, early season migrants, late season migrants, and desert species) in pest suppression is needed, as each group has unique population dynamics in the crop fields and probably also different predatory abilities. The early mi-grants may be of great importance in pest suppression because they reach high densities early in the season, while the com-bined effects of early migrants, residents, and late migrants may act to prevent insect pest outbreaks in desert agroecosystems. Therefore, there is a need to conserve natural habitats in order to conserve spiders not only numerically but also in terms of spe-cies diversity so as to optimise levels of biological pest suppression.

Acknowledgements

Thanks to G. Levy (The Hebrew University of Jerusalem, Israel) for assistance in spider identification; L. Baert (Royal Belgian Institute of Natural Sciences, Brussels, Belgium) and R. Bosmans (Gent University, Belgium) for taxonomic assist-ance with Linyphiidae and Lycosidae; and I. Peretz and espe-cially S. Eliasim (‘Moshavei HaNegev’, Development Association Ltd) for the use of their fields. Thanks to numer-ous people for help with field work and for useful discussions and comments, but especially M. Segoli, I. Musli, and E. Elimelch. M . Schmidt and K. Birkhofer and two anonymous referees provided valuable comments on the manuscript. The study was supported in part by FPVI of The European Commission; a Taxonomic Facility Consortia access grant (SYNTHESYS) from the Royal Institute of Natural Sciences, Brussels, Belgium; and the Professor Yanai and Jean Tab Fund, Arad Municipality, Israel (To E.G.-R.). This is publication no. 580 of the Mitrani Department of Desert Ecology, Ben-Gurion University, Israel.

100 Juvenile

Linyphiidae

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Gnaphosidae100 Juvenile

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Fig. 5. Population dynamics of (a) Linyphiidae, (b) Gnaphosidae, and (c) Theridiidae spiders, the three numerically most abundant families in wheat, based on season-long captures in emergence traps during winter 2002 – 2003 ( n = 1622).

Spider assemblages in a desert agroecosystem 211

© 2008 The AuthorsJournal compilation © 2008 The Royal Entomological Society, Ecological Entomology, 33, 202–212

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Accepted 31 August 2007First published online 1 February 2008