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The role of dispersal from natural habitat in determining spider abundance and diversity in California vineyards
Agriculture, Ecosystems and Environment 135 (2010) 260–267
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Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee
The role of dispersal from natural habitat in determining spider abundance and diversity in California vineyards Brian N. Hogg *, Kent M. Daane Department of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720-3114, United States
A R T I C L E I N F O
A B S T R A C T
Article history: Received 4 March 2009 Received in revised form 7 October 2009 Accepted 13 October 2009 Available online 17 November 2009
Many generalist predators do not persist in crops year-round, and must colonize crops on a seasonal basis from natural vegetation. We monitored the spider community in the air, on the ground, and in the foliage of California vineyards and neighboring oak-woodlands, to assess whether dispersal from natural habitats influences the abundance and species diversity of spiders in agroecosystems. Early in the growing-season, low spider numbers in vineyard foliage indicated that few spiders overwintered in the vineyard. Aerial dispersal did not, however, occur primarily in the spring when generalist predators are likely to be important in pest suppression, but in mid-summer, while dispersal activity on the ground did not change over time. Aerial collection traps showed greater similarity to spider composition in vineyard foliage than ground collection traps, indicating that spiders in vineyards disperse more by air than over ground. Dwarf spiders (Linyphiidae) dominated spider composition on aerial traps but were not abundant on the vine, while other spider species showed an opposing pattern, suggesting that while spiders may have entered vineyards by air, other factors may have also contributed to spider composition in vineyards. These results are discussed with respect to control of vineyard pests and the establishment of spiders in vineyard agroecosystems. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Araneae Linyphiidae Ballooning Dispersal Habitat fragmentation Habitat preferences
1. Introduction Generalist arthropod predators can play a key role in the suppression of herbivores. Their ability to utilize a range of prey often allows them to persist in crop systems when pest numbers are low (Settle et al., 1996; Symondson et al., 2002). In this way, generalist predators may prevent pest outbreaks early in the season before specialist natural enemies arrive (Landis and van der Werf, 1997; Wissinger, 1997). The impacts of generalist predators on pest populations are therefore contingent on their year-round presence in crop systems, or the timing of their arrival from other habitats. Generalist predators that are not resident in the crop yearround must colonize crops on a seasonal basis, most likely from natural vegetation (Bedford and Usher, 1994; Wissinger, 1997; Duelli and Obrist, 2003; Oberg and Ekbom, 2006). If distance from natural habitats is minimal, predator species may persist that would otherwise be absent from an agricultural monoculture. Immigration can stabilize predator guild structure and allow the persistence of less competitive species through mass or rescue
* Corresponding author at: c/o Daane Lab, 137 Mulford Hall, University of California, Berkeley, CA 94720-3114, United States. Tel.: +1 510 643 4019; fax: +1 559 646 6593. E-mail address: [email protected] (B.N. Hogg). 0167-8809/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2009.10.004
effects (Leibold et al., 2004; Bonte et al., 2006). In addition, the dispersal capacities of predator species will influence whether or not they reach crop fields from natural habitats (Sunderland and Samu, 2000; Tscharntke et al., 2005). Species with high dispersal capacities often dominate species composition in crop systems (Burel and Baudry, 1995). As the landscape is opened through agricultural intensification, highly mobile species may be favored (de la Pena et al., 2003). Resulting changes to predator diversity may in turn influence herbivore suppression (Snyder et al., 2006). As a ubiquitous and taxonomically diverse group of generalist predators, spiders can be effective natural enemies of herbivore pests in crop systems (Riechert and Lockley, 1984; Nyffeler and Sunderland, 2003). Their dispersal capacities may further increase their importance, as spiders are known to disperse aerially over long distances by ballooning on threads of silk (Greenstone et al., 1987; Weyman et al., 2002). Ballooning spiders are often pioneers of newly opened habitat, and are commonly one of the first predators to arrive in crop fields (Weyman et al., 1995; Suter, 1999). Aerial dispersal may contribute more to spider composition in crop systems than terrestrial movement from neighboring natural habitat (Bishop and Riechert, 1990). The roles of ground versus aerial dispersal are still ambiguous, however (Sunderland and Samu, 2000; Schmidt and Tscharntke, 2005). Past research has indicated that ground dispersal can contribute to spider composition in crop systems, particularly in close proximity to non-crop source habitats (Oberg and Ekbom, 2006; Oberg et al., 2007).
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We monitored aerial and ground movement of spiders in California vineyards, where spiders can comprise up to 95% of the arthropod predators (Costello and Daane, 1995, 1999). The most abundant insect pests in the studied vineyards were leafhoppers, Erythroneura spp., which are closely tied to vine phenology and condition (Daane and Williams, 2003) and are a likely prey source for spiders (Costello and Daane, 2003). Here, we examine whether spider dispersal in vineyards occurred (1) mainly in the spring season, when spiders are likely to play a critical role in pest suppression, (2) from within the vineyard or from the surrounding natural habitat, and (3) by air or over ground. 2. Materials and methods 2.1. Study sites Sample sites were three commercial vineyards in Napa County, California that abutted natural oak woodland/chaparral habitats. All vineyards were Cabernet cv., planted between 1998 and 2000, wire-trellised to a vertical system, on drip irrigation and with similar soil conditions. Large expanses of vineyard monoculture (500 m 500 m) that were adjacent to oak woodland but contained no additional trees or small clumps of natural vegetation were required as sites for this study, and vineyards in only one district of the Napa Valley met these criteria. Although the vineyards, hereafter referred to as the West, North, and South sites, were necessarily in close proximity to each other, each bordered a different patch of natural habitat. The West site was 930 m and 1040 m from the North and South sites, respectively. The North and South sites were 250 m apart. A road 10 m wide separated each vineyard and natural habitat. 2.2. Sampling methods Sticky traps were used to collect ballooning spiders, using a system adapted from Greenstone et al. (1985). Sticky traps consisted of hardware cloth coated with Stikem (Seabright Enterprises, Emeryville, CA). The cloth was 6.3 mm gauge and traps were 30 cm 50 cm. Traps were attached to stakes with two binder clips, which were affixed to stakes with cable ties. In vineyards, sticky traps were attached to 1 m wooden stakes, which were then secured to the vineyards’ metal trellis stakes using cable ties. Once in place, traps were above grape vine foliage, with their base 2 m above the ground. All foliage around traps was cut back to prevent foliage from becoming entangled on the trap. Sticky traps in oak woodland were placed on metal stakes hammered into the ground. As in the vineyards, the base of each trap was 2 m above the ground. For all sticky traps, a 2 cm wide band of Stikem was applied to the support stakes to prevent spiders from walking onto traps from below. Pitfall traps were used to monitor walking spiders and consisted of 11 cm 14 cm plastic cups buried in the ground up to the rim. A second rimless cup, filled with 2.5 cm of 25% solution of propylene glycol, was inserted inside the outer cup. Wood squares, supported by 2 cm wooden dowels, were placed over the mouth of pitfall traps to prevent debris from falling into traps. Spiders were removed from pitfall traps by pouring the liquid through a sieve. Pitfall traps were placed underneath each sticky trap. Sticky traps and pitfall taps were located along three transects at each site. Each transect was five rows (10 m) apart and ran 250 m into the vineyard and 50 m into the natural habitat. Trap distances were at 10, 50, 100, 150, 200 and 250 m into the vineyard, and were at 0 (woodland edge with the dirt road), 25 and 50 m into the natural habitat. Sticky traps and pitfall samples were collected at 13–15-day intervals, from 4 May through 4 October, 2006. The start date corresponded with pest development and vine
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phenology; in the Napa Valley, leafhoppers overwinter as adults and typically start laying eggs during late April or early May, when mature foliage begins to appear on vines (Daane and Costello, 2000). Sticky traps were removed and immediately replaced with fresh traps; spiders were removed from pitfall traps in the field and later stored at 4 8C before placing them in 70% alcohol. For sticky traps, spiders had to be removed in the laboratory. Sticky traps were stored at 4 8C for 24–48 h and then visually searched for spiders using a circular fluorescent light equipped with a magnifying glass. All spiders found were removed and placed in paint thinner for 7 days, to dissolve Stikem, and then placed in 70% alcohol. Spiders were sorted to species, genus, or morphospecies. Additionally, to monitor the composition of the spider community in vineyards and woodland, beat samples were taken on 27 April, 13–14 June, 5 September (West and South sites only) and 16 September (North site only), and 24–25 October. Three beat samples were collected at each transect distance from approximately 1 m3 of foliage. In vineyards, foliage between two vines was shaken and beaten for 30 s to dislodge spiders into a 1 m2 cloth funnel equipped at the bottom with a removable plastic bag (after Costello and Daane, 1997). In woodland, coast live oak (Quercus agrifolia) foliage was shaken (but not beaten) for 30 s, using the cloth funnel procedure. Coast live oak is the dominant tree species in Napa County, and in preliminary sampling contained higher numbers of spiders per sample than other common tree species or low-lying vegetation (i.e., grasses and bushes). All samples were transported to the laboratory in a cooler to retard predation, stored at 4 8C, and then placed in 70% alcohol and sorted to species, genus, or morphospecies. 2.3. Data analysis 2.3.1. Timing of spider dispersal and arrival in vineyards To assess the timing of spider dispersal and arrival in vineyards, seasonal spider abundance data from sticky traps, pitfall traps and beat samples were analyzed using MANOVA, with habitat, site and sample date as independent variables and spider number in each type of sample as the dependent variables. For sticky trap data, we conducted separate analyses of total spider numbers and spider numbers excluding dwarf spiders, Erigone spp. (Linyphiidae). Dwarf spiders dominated sticky traps, but were uncommon in vineyard foliage, and we wanted to examine the timing of dispersal for those spiders that are likely to play a role in the vineyard spider community. Data were log(x + 1) transformed prior to analyses. 2.3.2. Natural habitat as a source for spiders To assess whether spillover of ballooning spiders occurred from woodland into vineyards, Kruskal–Wallis tests and nonparametric multiple comparison tests, using the kruskalmc function in R version 2.7.0 (R Development Core Team, 2008), were used to compare number of spiders per sticky trap and number of species per sticky trap between transect distances. Parametric tests could not be used for sticky trap data, since variables did not conform to the assumption of equal variances, even after transformation. Numbers of spiders and spider species per pitfall trap were compared between transect distances using analysis of variance (ANOVA); spider numbers were log(x + 1) transformed prior to analysis. For these analyses, spider numbers were summed through the season for each transect distance at each site (after Bedford and Usher, 1994) and divided by the number of samples, resulting in 9 replicates for each transect distance (3 from each site). To further examine spillover of spiders from woodland into vineyards, spider composition of sticky and pitfall traps was compared between vineyard and woodland transect distances. For this analysis, data for each transect distance were averaged across
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the season and across all sites, resulting in one averaged sample for each transect distance. Spider composition was compared between each vineyard distance and each of the three woodland distances using the Sorensen index of similarity. The Sorensen index is a measure of proportional similarity, and ranges from 0 (no similarity) to 1 (identical). Overall numbers of ballooning spiders were low, making the Sorensen index the most appropriate choice for this analysis, since it uses incidence of species to compare samples, and is insensitive to changes in species abundances. 2.3.3. Dispersal mode The relative contributions of the two modes of dispersal (aerial versus ground) to spider composition in vineyards were assessed by comparing the spider composition in vineyard sticky traps and pitfall samples with beat samples from vineyards, using the Sorensen index of similarity and proportion of species collected in beat samples that were also present in both types of traps. Sites were analyzed separately. Data for traps and beat samples were summed through the season for each site and divided by the number of samples. Sites were also analyzed together by summing spider numbers across all three sites and through the season. In addition, total frequencies of those species that represented >1% of the spider composition in beat samples were compared between sticky and pitfall traps using 2 2 contingency tables and Fisher’s exact test, or in the case of dwarf spiders (Erigone spp.), a chi-square test (numbers were low for all species except Erigone spp., making the chi-square test inappropriate, while numbers of Erigone spp. were too high for Fisher’s exact test). The standard Bonferroni correction was used to compensate for Type I error. 3. Results 3.1. Spider composition in sticky traps A total of 1102 spiders (678 juveniles) representing 39 species and 16 families were collected on sticky traps in vineyards (Table 1). The most abundant spider family was Linyphiidae (58.4%), and dwarf spiders (Erigone spp.) accounted for the majority (94.9%) of the linyphiids. Besides Linyphiidae, the most common spider families on sticky traps in vineyards were: Gnaphosidae (6.2%), Tetragnathidae (4.8%), Araneidae (4.2%), Salticidae (4.2%), Philodromidae (4.1%), Theridiidae (3.2%), Thomisidae (3.1%), Lycosidae (2.7%), and Oxyopidae (2.2%). In woodland sites, a total of 1093 spiders (844 juveniles) were collected on sticky traps, representing 41 species and 16 families (Table 1). As in vineyards, the most numerous spider family on sticky traps was Linyphiidae (17.6%), with dwarf spiders constituting 73.6% of this group. The most numerous spider families on sticky traps in woodland were: Linyphiidae, Tetragnathidae (14.3%), Salticidae (13.3%), Theridiidae (10.9%), Philodromidae (7.0%), Araneidae (6.5%), Dictynidae (4.6%), Anyphaenidae (4.4%), Thomisidae (4.2%), and Miturgidae (3.9%). 3.2. Spider composition in pitfall traps A total of 2209 spiders representing 28 species and 14 families were collected in vineyard pitfall traps (Table 1). Pitfall samples were dominated by ground spiders of the family Gnaphosidae (53.2%), followed by the predominantly ground-dwelling Lycosidae (14.5%). Only four other families comprised more than 1% of the familial composition in vineyard pitfall traps: Oecobiidae (11.8%), Salticidae (9.6%, primarily an unidentified Metaphidippus sp. that was found only in pitfall samples), Corinnidae (8.3%, almost entirely Meriola californica Banks, which was unique to pitfall samples), and Linyphiidae (4.2%).
In woodland pitfall traps, a total of 1079 spiders from 24 species and 15 families were collected (Table 1). The family Lycosidae (35.9%) dominated these samples, followed by Gnaphosidae (29.1%), Corinnidae (10.5%), Salticidae (7.1%), and Liocranidae (5.4%). 3.3. Spider composition in beat samples In vineyard beat samples, a total of 219 spiders representing 23 species and 14 families were collected (Table 1). Spider composition was dominated by the families Miturgidae (30.7%), with Cheiracanthium mildei L. Koch alone constituting 24.7%, and Salticidae (28.6%), primarily comprised of Metaphidippus manni Peckham & Peckham, which represented 21.5% of spiders overall. Also represented were: Theridiidae (11.9%), comprised only of Theridion melanurum Hahn, Anyphaenidae (5.1%), Corinnidae (4.1%), represented solely by Trachelas pacificus Chamberlin, Gnaphosidae (3.2%), Mimetidae (3.2%), comprised only of Mimetus hesperus Chamberlin; and Oxyopidae (3.2%). A total of 660 spiders from 37 species and 16 families were collected in woodland beat samples (Table 1). Salticidae was the most abundant family (18.4%), followed by Theridiidae (16.4%). Other well-represented families included: Tetragnathidae (10.8%), Anyphaenidae (9.0%), Linyphiidae (7.5%), Dictynidae (6.9%), Miturgidae (5.5%), and Araneidae (4.9%). 3.4. Timing of spider dispersal and arrival in vineyards Sample date had a significant effect on total numbers of ballooning spiders (MANOVA analysis: F = 35.09; P < 0.001). There was also a sample date habitat interaction (F = 10.87, P < 0.001), showing that habitat had an effect on spider numbers that changed across the season. The lack of a sample date site interaction (Pillai’s trace = 1.40, P = 0.14) indicates that seasonal changes in spider abundance were not affected by study site. When dwarf spiders were excluded from analysis, numbers of ballooning spiders were affected by sample date (F = 25.82, P < 0.001), and the sample date habitat interaction (F = 8.82, P < 0.001), but not the sample date site interaction (Pillai’s trace = 1.08, P = 0.38). In vineyards, total numbers of ballooning spiders gradually declined during the sampling period, from May to October, while numbers of ballooning spiders in woodland were highest in late July (Fig. 1A). The vast majority of early-season ballooners in vineyards were dwarf spiders, however. For the rest of aerially dispersing spider community excluding dwarf spiders, numbers on vineyard sticky traps were low early in the season and reached a peak in mid-August (Fig. 1B). Numbers of spiders per pitfall trap were also influenced by sample date in MANOVA analysis (F = 2.748; P < 0.01), and habitat affected spider numbers over time (sample date habitat interaction, F = 6.64; P < 0.001). Changes over time in numbers of spiders per pitfall trap did not differ between study sites (sample date site interaction, Pillai’s trace = 1.37; P = 0.16). Numbers in woodland pitfall traps declined across the season, but numbers in vineyard pitfall traps did not follow a consistent pattern across the season (Fig. 1C). Differences between habitats were also inconsistent over time. In MANOVA analysis, numbers of spiders in foliage were affected by sample date (F = 14.29; P < 0.001). Habitat also influenced spider numbers across the season (sample date habitat interaction, F = 41.47; P < 0.001). There was no sample date site interaction (Pillai’s trace = 1.05; P = 0.40), which indicates that changes in spider numbers through time were similar across study sites. Numbers of spiders in vineyards gradually increased across the season (Fig. 1D). There were very few spiders in beat samples on either of the first two sampling
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Table 1 Percentages of spiders collected in sticky traps, pitfall traps, and beat samples. Spider family
Spider species
Sticky traps
Woodland
Vineyard
Amourobiidae
Unknown amaurobiid sp.
1.4
0.1
0.9
1.8
0.0
0.2
Anyphaenidae
Anyphaena pacifica Hibana incursa
0.5 0.5
0.5 3.9
0.1 0.0
0.0 0.0
4.6 0.5
2.3 6.7
Araneidae
Araneus sp. Cyclosa turbinata Araneid sp. 1 Araneid sp. 2 Araneid sp. 3 Unknown araneids
0.0 1.6 0.5 0.6 0.4 1.0
1.2 2.0 1.0 1.6 0.0 0.7
0.0 0.0 0.0 0.1 0.0 0.0
0.0 0.0 0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0 0.0 0.0
0.2 0.3 0.3 3.0 0.3 0.8
Clubionidae
Clubiona sp.
0.0
0.6
0.0
0.0
0.0
0.8
Corinnidae
Castianeira sp. Meriola californica Trachelas pacificus
0.0 0.0 1.8
0.0 0.0 5.9
0.0 8.1 0.1
9.9 0.6 0.0
0.0 0.0 4.1
0.0 0.0 7.3
Dictynidae
Dictyna sp. 1 Dictyna sp. 2 Mallos sp. Unknown dictynids
0.2 0.1 0.5 0.5
0.2 0.1 3.3 1.0
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.7
0.0 1.8 0.0 0.0
0.0 0.5 5.9 0.5
Gnaphosidae
Micaria sp. Zelotes sp. 1 Zelotes sp. 2 Unknown gnaphosids
0.0 0.0 0.0 6.2
0.0 0.0 0.0 1.6
7.2 28.6 16.5 0.9
1.0 13.4 12.8 1.9
0.0 0.5 0.9 2.7
0.0 0.0 0.0 1.7
Linyphiidae
Erigone spp. Other Erigoninae Pityohyphantes sp. Linyphiid sp. 1 Linyphiid sp. 2 Unknown linyphiids
55.4 0.0 0.0 1.9 0.5 0.6
11.2 0.0 0.1 2.3 3.4 0.6
2.8 0.0 0.0 0.2 0.3 0.1
0.0 2.0 0.0 0.0 0.0 0.2
1.4 0.0 0.0 0.0 0.0 0.0
3.6 0.0 0.2 0.2 3.5 0.0
Vineyard
Pitfall traps Woodland
Vineyard
Beat samples Woodland
Liocranidae
Unknown liocranid sp.
0.0
0.0
0.0
5.4
0.0
0.0
Lycosidae
Hogna sp. Pirata sp. Lycosid sp. 1 Unknown lycosids
0.0 0.0 0.0 2.7
0.0 0.0 0.0 1.3
9.5 0.0 5.0 0.0
14.6 0.7 20.6 0.0
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
Mimetidae
Mimetus hesperus
0.1
0.5
0.0
0.0
3.2
2.0
Miturgidae
Cheiracanthium inclusum Cheiracanthium mildei C. mildei or C. inclusum
0.6 0.7 0.5
1.3 1.0 1.6
0.1 0.0 0.0
0.0 0.2 0.0
5.5 24.7 0.5
1.5 3.9 0.0
Nemesiidae
Calisoga sp.
0.0
0.0
0.2
0.2
0.0
0.0
Oecobiidae
Oecobius navus
0.0
0.0
11.8
1.3
0.0
0.0
Oxyopidae
Oxyopes salticus Oxyopes scalaris Unknown oxyopids
1.5 0.5 0.2
1.5 1.7 0.0
0.0 0.0 0.0
0.0 0.0 0.0
2.7 0.5 0.0
2.0 0.0 0.0
Philodromidae
Ebo sp. Philodromus sp. 1 Philodromus sp. 2 Philodromus sp. 3 Unknown philodromids
0.2 2.9 0.5 0.5 0.0
0.2 4.8 0.7 1.3 0.0
0.0 0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0 0.2
0.0 0.5 0.5 0.5 0.0
0.3 2.4 0.5 1.5 0.0
Salticidae
Habronattus sp. Metaphidippus manni Metaphidippus sp. Phidippus sp. Salticus scenicus Salticus sp. Sassacus vitis Thiodiona hespera Unknown salticids
0.3 2.9 0.0 0.1 0.1 0.0 0.1 0.4 0.3
0.4 11.7 0.0 0.1 0.0 0.0 0.0 0.7 0.4
0.2 0.0 5.2 0.0 0.1 0.0 0.0 0.0 0.2
0.0 0.0 7.1 0.0 0.0 0.0 0.0 0.0 0.2
0.0 21.5 0.0 1.8 4.1 0.0 0.0 0.9 0.0
0.0 10.8 0.0 0.2 0.2 0.9 0.0 5.8 0.5
Tengellidae
Titiotus californicus
0.0
0.0
0.1
3.4
0.0
0.0
Tetragnathidae
Tetragnatha laboriosa Tetragnatha versicolor
4.8 0.0
14.3 0.0
0.0 0.0
0.0 0.0
2.7 0.0
10.3 0.5
Theridiidae
Euryopis sp. Theridion melanurum Theridion dilutum Theridion spp.
0.0 0.5 1.4 0.9
0.2 4.8 2.4 2.6
0.0 0.0 0.0 0.4
0.3 0.0 0.0 0.0
0.0 11.9 0.0 0.0
0.0 3.9 11.1 0.2
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Table 1 (Continued ) Spider family
Spider species
Sticky traps Vineyard
Thomisidae
Pitfall traps Woodland
Vineyard
Unknown theridiids
0.4
0.9
0.4
0.0
0.0
1.2
Coriarachne sp. Diaea sp. Misumenops sp. Tmarus sp. Xysticus sp.
0.0 0.0 1.5 0.2 0.8
0.0 0.8 0.7 0.6 1.3
0.0 0.0 0.0 0.0 0.5
0.0 0.1 0.0 0.0 1.9
0.0 0.0 0.9 0.0 0.9
0.0 0.2 1.4 0.2 0.0
0.6
0.8
0.0
0.6
0.5
1.1
Unknown
Woodland
Vineyard
Beat samples Woodland
Total spiders
1102
1093
2209
1079
219
660
Number spp.
39
41
28
24
23
37
dates. Numbers of spiders in woodland beat samples increased early in the season, before sharply declining late in the summer. For most of the season, numbers of spiders were higher in woodland than vineyard (Fig. 1D). 3.5. Natural habitat as a source for spiders Total number of spiders per sticky trap changed across transects (Fig. 2A), and were significantly different among transect distances (Kruskal–Wallis test, H = 46.86, P < 0.001). Within vineyards, numbers were significantly higher at the vineyard edge than at the furthest distance from woodland. Numbers of spiders per trap were higher 25 m into woodland than 50 m, 100 m, 150 m and 250 m from the woodland edge in the vineyard, while numbers at woodland distances 0 and 50 m were significantly higher than 50 and 250 m into the vineyard (nonparametric multiple comparison test, P < 0.05). Number of spider species per sticky trap also showed significant differences among transect distances (Kruskal–Wallis test, H = 60.05, P < 0.001; Fig. 2A). The number of species per trap was significantly higher at the vineyard edge than at the vineyard distance furthest from woodland (nonparametric multiple com-
parison test, P < 0.05). At all woodland distances there were significantly more species per trap than at all vineyard distances except at the vineyard edge and at the 200 m vineyard distance (nonparametric multiple comparison test, P < 0.05). Numbers of spiders per pitfall trap did not change across transects (ANOVA, F = 1.15, P = 0.34), although there was a nonsignificant decrease at the vineyard edge (Fig. 2B). Numbers of spider species per pitfall trap were similarly unaffected by transect distance (F = 0.55, P = 0.81). For sticky traps, spider species composition at the vineyard edge tended to be more similar to woodland than the other vineyard distances (Table 2). In comparisons of spider species composition in pitfall traps, by contrast, the vineyard distance furthest from woodland was the most similar to the woodland (Table 2). 3.6. Dispersal mode Sorensen index values and percentages of species found in vineyard beat samples that were also present in sticky and pitfall traps were consistently higher in comparisons between sticky traps and beat samples than between pitfall and beat samples (Table 3). Proportional representation for many of the dominant
Fig. 1. Mean numbers (SE) of spiders per sticky trap, including all spiders (A), per sticky trap, excluding dwarf spiders (B), per pitfall trap (C) and per beat sample (D) through the season in vineyard and woodland habitats.
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Table 3 Comparisons of sticky and pitfall traps with vineyard beat samples, using the Sorensen index of similarity, percentage of species collected in beat samples that were also present in traps, and number of species shared between beat samples and traps. Trap type
Study site
Sorensen index
Beat species shared (%)
Species shared
Sticky
West North South Overall
0.55 0.51 0.61 0.70
68.75 73.33 93.33 87.75
11 11 14 21
Pitfall
West North South Overall
0.17 0.17 0.39 0.46
18.75 20.00 46.67 50.00
3 3 7 12
Fig. 3. Comparison of proportional spider composition in pitfall traps, sticky traps and vineyard beat samples. Only a few individuals of some families were collected in pitfall traps, and are not visible in this figure.
Fig. 2. Mean numbers (SE) of spiders and spider species per sticky trap (A) and per pitfall trap (B) along transects, averaged across the season, with 9 replicates for each transect distance (3 from each site). Different lower- and uppercase letters indicate significantly different mean values for total number of spiders and number of spider species, respectively (nonparametric multiple comparison tests, P < 0.05).
families in beat samples was also higher on sticky traps than pitfall traps (Fig. 3). The only families that occurred in high proportions in both beat and pitfall samples were Gnaphosidae, Salticidae and Corinnidae, and of these, Salticidae and Corinnidae were represented almost entirely in pitfall traps by an unidentified Metaphidippus sp. and a Meriola sp., respectively, species that were unique to pitfall traps. Sticky traps and beat samples differed widely in relative abundance of families, however. Although linyphiid spiders made up the majority of spiders in vineyard sticky traps, they were rarely recovered in beat samples. On the other hand, Miturgidae and Salticidae dominated beat samples, but comprised only a small proportion of the familial composition of sticky traps.
Of the 13 species that represented >1% of the spider composition in beat samples, seven occurred in significantly higher numbers in sticky traps than pitfall traps. C. mildei, Cheiracanthium inclusum Hentz (Miturgidae), M. manni, T. pacificus, Erigone spp., Oxyopes salticus Hentz (Oxyopidae), and Tetragnatha laboriosa Hentz (Tetragnathidae) occurred more frequently on sticky traps than expected by chance alone (Fisher’s exact tests, P < 0.001; chi-square test, P < 0.001, for Erigone spp.). Six species showed no significant difference between trap types: Anyphaena pacifica Banks (Anyphaenidae); Dictyna sp. 2 (Dictynidae); M. hesperus; Salticus scenicus Clerck (Salticidae); Phidippus sp. 1 (Salticidae); and T. melanurum (Fisher’s exact tests, P > 0.001). No species were higher in number in pitfall traps. 4. Discussion In this study, numbers of dispersing spiders were not higher in the spring, with the exception of the linyphiid dwarf spiders, which ballooned in high numbers during May and June. These results are
Table 2 Comparisons of spider composition between vineyard and woodland transect distances for sticky and pitfall traps, using the Sorensen index of similarity. Trap type
Distance into woodland
Distance into vineyard 10
50
100
150
200
250
Sticky
0 25 50
0.80 0.81 0.83
0.78 0.73 0.81
0.77 0.72 0.81
0.74 0.72 0.74
0.81 0.78 0.81
0.70 0.64 0.74
Pitfall
0 25 50
0.65 0.67 0.65
0.65 0.67 0.70
0.63 0.59 0.63
0.65 0.67 0.65
0.65 0.61 0.65
0.75 0.71 0.74
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in accordance with Oberg and Ekbom (2006), who presented evidence that linyphiid spiders disperse early in the season. For the spider community excluding dwarf spiders, numbers of ballooning spiders were highest in vineyards and woodland during August and July, respectively. In addition, dispersal activity over ground did not occur mainly in the spring; spider numbers in vineyard pitfall traps showed no consistent pattern across the season. Oberg and Ekbom (2006) also found no change in numbers of grounddispersing spiders in crop fields over time. Early-season spider abundance on vines appeared to reflect the lack of increased dispersal activity during this time. Numbers on vines were low at least until mid-June, indicating that spiders neither overwintered in vineyards nor arrived early in the spring. We suggest that any impacts of spiders on pests in vine foliage are likely to be limited to late summer or early fall. Numbers of woodland spiders on aerial traps and in the foliage were consistently higher than in vineyards for most of the season, indicating that oak woodland was a source for spiders in vineyards. The density of source populations is often highly correlated with the total number of aerially dispersing spiders (Weyman et al., 1995). In this study, we did not directly examine movement between habitats or the role of reproduction in the increase of spiders across the season. However, the low numbers of spiders in vineyards observed early in the season, combined with the drastic difference between habitats in spider abundance, strongly indicates that spiders arrived in vineyards from nearby oak woodland. The increase in spider numbers and spider species richness on sticky traps at the vineyard edge, where spider species composition also tended to be more similar to woodland than at other vineyard distances, supplies additional indirect evidence that spillover of ballooning spiders from woodland contributed to vineyard spider composition. Similarly, Sackett et al. (2009) found that spider abundance and species composition in apple orchards were affected by distance from natural source habitat, and that this shift occurred over a distance of only 40 m. Results from the present study suggest that many spider species in the vineyard ecosystem balloon only short distances. Along transects, gradual transitions between habitats are often associated with species that have limited dispersal abilities (Duelli et al., 1990). Many spider species may have wafted short distances into vineyards from surrounding trees. Traps that are placed only a few meters from the ground, as they were in this study, may collect spider species that have merely drifted towards the ground from a higher take-off point (Greenstone et al., 1987). Other studies have shown that many spiders disperse only short distances by ballooning, in some instances traveling only a few meters (Riechert and Gillespie, 1986; Morse, 1993; Samu et al., 1999). Ground spiders were unaffected by transect distance, and numbers were not consistently higher in oak woodland. Oberg and Ekbom (2006) obtained similar results, and suggested that spiders may be able to rapidly recolonize fields from non-crop habitats by walking. In the present study, transects may not have been long enough to observe an effect on ground spiders. Alternatively, ground spiders may be unaffected by seasonal changes in vineyards, and may not recolonize vineyards from natural habitats. Ground dispersal appeared to contribute relatively little to the spider community on vines. Spider composition on vines reflected sticky traps far more than pitfall traps, and the majority of the wellrepresented vineyard species were more numerous on sticky traps. Most importantly, three of the four dominant vineyard species—C. mildei, C. inclusum and M. manni—occurred more frequently on sticky traps. These results suggest that spiders in vineyards disperse more by air than over ground. Bishop and Riechert (1990) also found that spider composition differed widely between sticky and pitfall traps, and concluded that many spiders arrived in crop
fields via ballooning. In this study, the vast majority of spiders collected in pitfall traps were from three predominantly grounddwelling families (Gnaphosidae, Lycosidae, Oecobiidae) that were not present in significant numbers on vines. Costello and Daane (2003) similarly report that spider species composition on the ground was different from that on the vines above. Although spiders may colonize vineyards by air, most likely from natural source habitats, other factors may also contribute to their establishment in vineyards. The four dominant species in vineyard beat samples—C. mildei, C. inclusum, M. manni and T. melanurum—appeared on sticky traps, but not in high numbers. These spiders, particularly C. mildei, are likely to be highly adapted to disturbed agricultural settings, and typically dominate vineyard spider composition in the Napa Valley region (Hogg and Daane, unpubl.). While only low numbers of C. mildei may disperse into vineyards, their competitive abilities may allow them to dominate the spider community. It is also possible that spiders such as C. mildei are year-round residents of vineyards, giving them an advantage over species that arrive from natural habitat in summer. This possibility does not seem likely, however, since vineyards are unlikely to provide a suitable habitat for spiders until vines sprout foliage in late spring, later than most spiders in this system emerge from hibernation and reproduce (B. Hogg, pers. obs.). Dwarf spiders showed high aerial dispersal rates, on the other hand, but were never well-represented on vines and may be unsuited to vineyard conditions. Habitat quality can be an important factor in determining whether spiders choose to stay, or balloon to another habitat (Morse, 1993; Samu et al., 1999), and traps such as those used in this study can collect spiders that would have immediately taken off again (Weyman et al., 2002). If many spider species are ballooning short distances from natural habitat into vineyards, close proximity to natural habitat may elevate spider diversity, which could have implications for pest suppression. Elevated predator diversity can increase impacts on herbivores (Snyder et al., 2006). Or, the few predator species that flourish in agroecosystems may drive impacts on pest populations. Further investigation of predator interactions is needed to understand the relative importance of local and landscape factors in shaping the impacts of predators on pest populations in agroecosystems. Acknowledgements This work was supported with grants from the National Science Foundation Dissertation Improvement Grant DEB 0710434, the van den Bosch Memorial Scholarship, and the California Table Grape Commission and American Vineyard Foundation. We thank vineyard managers for use of their farms Tian Hu for help in the field and laboratory, and three anonymous reviewers for their helpful comments and suggestions. References Bedford, S.E., Usher, M.B., 1994. Distribution of arthropod species across the margins of farm woodlands. Agric. Ecosyst. Environ. 48, 295–305. Bishop, L., Riechert, S.E., 1990. Spider colonization of agroecosystems: mode and source. Environ. Entomol. 19, 1738–1745. Bonte, D., Lens, L., Maelfait, J.P., 2006. Sand dynamics in coastal dune landscapes constrain diversity and life-history characteristics of spiders. J. Appl. Ecol. 43, 735–747. Burel, F., Baudry, J., 1995. Species biodiversity in changing landscapes: a case study in the Pays d’Auge, France. Agric. Ecosyst. Environ. 55, 193–200. Costello, M.J., Daane, K.M., 1995. Spider (Aranaeae) species composition and seasonal abundance in San Joaquin Valley grape vineyards. Environ. Entomol. 24, 823–831. Costello, M.J., Daane, K.M., 1997. Comparison of sampling methods used to estimate spider (Araneae) species abundance and composition in grape vineyards. Environ. Entomol. 26, 142–149. Costello, M.J., Daane, K.M., 1999. Abundance of spiders and insect predators on grapes in central California. J. Arachnol. 27, 531–538.
B.N. Hogg, K.M. Daane / Agriculture, Ecosystems and Environment 135 (2010) 260–267 Costello, M.J., Daane, K.M., 2003. Spider and leafhopper (Erythroneura spp.) response to vineyard ground cover. Environ. Entomol. 32, 1085–1098. Daane, K.M., Costello, M.J., 2000. Variegated and western grape leafhoppers. In: Christensen, P. (Ed.), Raisin Production Manual. Univ. Calif. Agricul. Natr. Resrc., Oakland, CA, pp. 173–181. Daane, K.M., Williams, L.E., 2003. Manipulating vineyard irrigation amounts to reduce insect pest damage. Ecol. Appl. 13, 1650–1666. de la Pena, N.M., Butet, A., Delettre, Y., Morant, P., Burel, F., 2003. Landscape context and carabid beetles (Coleoptera: Carabidae) communities of hedgerows in western France. Agric. Ecosyst. Environ. 94, 59–72. Duelli, P., Obrist, M.K., 2003. Regional biodiversity in an agricultural landscape: the contribution of seminatural habitat islands. Basic Appl. Ecol. 4, 129–138. Duelli, P., Studer, M., Marchand, I., Jacob, S., 1990. Population movements of arthropods between natural and cultivated areas. Biol. Conserv. 54, 193–207. Greenstone, M.H., Morgan, C.E., Hultsch, A.L., 1985. Spider ballooning: development and evaluation of field trapping methods (Araneae). J. Arachnol. 13, 337–345. Greenstone, M.H., Morgan, C.E., Hultsch, A.L., 1987. Ballooning spiders in Missouri, U.S.A., and New South Wales, Australia: family and mass distributions. J. Arachnol. 15, 163–170. Landis, D.A., van der Werf, D., 1997. Early-season predation impacts the establishment of aphids and spread of beet yellows virus in sugar beet. Entomophaga 42, 499–516. Leibold, M.A., Holyoak, M., Mouquet, N., Amarasekare, P., Chase, J.M., Hoopes, M.F., Holt, R.D., Shurin, J.B., Law, R., Tilman, D., Loreau, M., Gonzalez, A., 2004. The metacommunity concept: a framework for multi-scale community ecology. Ecol. Lett. 7, 601–613. Morse, D.H., 1993. Some determinants of dispersal by crab spiderlings. Ecology 74, 427–432. Nyffeler, M., Sunderland, K.D., 2003. Composition, abundance and pest control potential of spider communities in agroecosystems: a comparison of European and US studies. Agric. Ecosyst. Environ. 95, 579–612. Oberg, S., Ekbom, B., 2006. Recolonization and distribution of spiders and carabids in cereal fields after spring sowing. Ann. Appl. Biol. 149, 203–211. Oberg, S., Ekbom, B., Bommarco, R., 2007. Influence of habitat type and surrounding landscape on spider diversity in Swedish agroecosystems. Agric. Ecosyst. Environ. 122, 211–219. R Development Core Team, 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna.
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Riechert, S.E., Gillespie, R.G., 1986. Habitat choice and utilization in web-building spiders. In: Shear, W.A. (Ed.), Spiders: Webs Behavior and Evolution. Stanford University Press, Stanford, pp. 23–48. Riechert, S.E., Lockley, T., 1984. Spiders as biological control agents. Ann. Rev. Entomol. 29, 299–320. Sackett, T.E., Buddle, C.M., Vincent, C., 2009. Dynamics of spider colonization of apple orchards from adjacent deciduous forest. Agric. Ecosyst. Environ. 129, 144–148. Samu, F., Sunderland, K.D., Szinetar, C., 1999. Scale-dependent dispersal and distribution patterns of spiders in agricultural systems: a review. J. Arachnol. 27, 325–332. Schmidt, M.H., Tscharntke, T., 2005. Landscape context of sheetweb spider (Araneae: Linyphiidae) abundance in cereal fields. J. Biogeogr. 32, 467–473. Settle, W.S., Ariawan, H., Astuti, E.T., Cahyana, W., Hakim, A.L., Hindayana, D., Lestari, A.S., Pajarningsih, Sartanto, 1996. Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77, 1975–1988. Snyder, W.E., Snyder, G.B., Finke, D.L., Straub, C.S., 2006. Predator biodiversity strengthens herbivore suppression. Ecol. Lett. 9, 789–796. Sunderland, K., Samu, F., 2000. Effects of agricultural diversification on the abundance, distribution, and pest control potential of spiders: a review. Entomol. Exp. Appl. 95, 1–13. Suter, R.B., 1999. An aerial lottery: the physics of ballooning in a chaotic atmosphere. J. Arachnol. 27, 281–293. Symondson, W.O.C., Sunderland, K.D., Greenstone, M.H., 2002. Can generalist predators be effective biocontrol agents? Annu. Rev. Entomol. 47, 561–594. Tscharntke, T., Klein, A.M., Kruess, A., Steffan-Dewenter, I., Thies, C., 2005. Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol. Lett. 8, 857–874. Weyman, G.S., Jepson, P.C., Sunderland, K.D., 1995. Do seasonal changes in numbers of aerially dispersing spiders reflect population density on the ground or variation in ballooning motivation? Oecologia 101, 487–493. Weyman, G.S., Sunderland, K.D., Jepson, P.C., 2002. A review of the evolution and mechanisms of ballooning by spiders inhabiting arable farmland. Ethol. Ecol. Evol. 4, 307–326. Wissinger, S.A., 1997. Cyclic colonization in predictably ephemeral habitats: a template for biological control in annual crop systems. Biol. Control 10, 4–15.
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Agriculture, Ecosystems and Environment journal homepage: www.elsevier.com/locate/agee
The role of dispersal from natural habitat in determining spider abundance and diversity in California vineyards Brian N. Hogg *, Kent M. Daane Department of Environmental Science, Policy and Management, University of California, Berkeley, CA 94720-3114, United States
A R T I C L E I N F O
A B S T R A C T
Article history: Received 4 March 2009 Received in revised form 7 October 2009 Accepted 13 October 2009 Available online 17 November 2009
Many generalist predators do not persist in crops year-round, and must colonize crops on a seasonal basis from natural vegetation. We monitored the spider community in the air, on the ground, and in the foliage of California vineyards and neighboring oak-woodlands, to assess whether dispersal from natural habitats influences the abundance and species diversity of spiders in agroecosystems. Early in the growing-season, low spider numbers in vineyard foliage indicated that few spiders overwintered in the vineyard. Aerial dispersal did not, however, occur primarily in the spring when generalist predators are likely to be important in pest suppression, but in mid-summer, while dispersal activity on the ground did not change over time. Aerial collection traps showed greater similarity to spider composition in vineyard foliage than ground collection traps, indicating that spiders in vineyards disperse more by air than over ground. Dwarf spiders (Linyphiidae) dominated spider composition on aerial traps but were not abundant on the vine, while other spider species showed an opposing pattern, suggesting that while spiders may have entered vineyards by air, other factors may have also contributed to spider composition in vineyards. These results are discussed with respect to control of vineyard pests and the establishment of spiders in vineyard agroecosystems. ß 2009 Elsevier B.V. All rights reserved.
Keywords: Araneae Linyphiidae Ballooning Dispersal Habitat fragmentation Habitat preferences
1. Introduction Generalist arthropod predators can play a key role in the suppression of herbivores. Their ability to utilize a range of prey often allows them to persist in crop systems when pest numbers are low (Settle et al., 1996; Symondson et al., 2002). In this way, generalist predators may prevent pest outbreaks early in the season before specialist natural enemies arrive (Landis and van der Werf, 1997; Wissinger, 1997). The impacts of generalist predators on pest populations are therefore contingent on their year-round presence in crop systems, or the timing of their arrival from other habitats. Generalist predators that are not resident in the crop yearround must colonize crops on a seasonal basis, most likely from natural vegetation (Bedford and Usher, 1994; Wissinger, 1997; Duelli and Obrist, 2003; Oberg and Ekbom, 2006). If distance from natural habitats is minimal, predator species may persist that would otherwise be absent from an agricultural monoculture. Immigration can stabilize predator guild structure and allow the persistence of less competitive species through mass or rescue
* Corresponding author at: c/o Daane Lab, 137 Mulford Hall, University of California, Berkeley, CA 94720-3114, United States. Tel.: +1 510 643 4019; fax: +1 559 646 6593. E-mail address: [email protected] (B.N. Hogg). 0167-8809/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.agee.2009.10.004
effects (Leibold et al., 2004; Bonte et al., 2006). In addition, the dispersal capacities of predator species will influence whether or not they reach crop fields from natural habitats (Sunderland and Samu, 2000; Tscharntke et al., 2005). Species with high dispersal capacities often dominate species composition in crop systems (Burel and Baudry, 1995). As the landscape is opened through agricultural intensification, highly mobile species may be favored (de la Pena et al., 2003). Resulting changes to predator diversity may in turn influence herbivore suppression (Snyder et al., 2006). As a ubiquitous and taxonomically diverse group of generalist predators, spiders can be effective natural enemies of herbivore pests in crop systems (Riechert and Lockley, 1984; Nyffeler and Sunderland, 2003). Their dispersal capacities may further increase their importance, as spiders are known to disperse aerially over long distances by ballooning on threads of silk (Greenstone et al., 1987; Weyman et al., 2002). Ballooning spiders are often pioneers of newly opened habitat, and are commonly one of the first predators to arrive in crop fields (Weyman et al., 1995; Suter, 1999). Aerial dispersal may contribute more to spider composition in crop systems than terrestrial movement from neighboring natural habitat (Bishop and Riechert, 1990). The roles of ground versus aerial dispersal are still ambiguous, however (Sunderland and Samu, 2000; Schmidt and Tscharntke, 2005). Past research has indicated that ground dispersal can contribute to spider composition in crop systems, particularly in close proximity to non-crop source habitats (Oberg and Ekbom, 2006; Oberg et al., 2007).
B.N. Hogg, K.M. Daane / Agriculture, Ecosystems and Environment 135 (2010) 260–267
We monitored aerial and ground movement of spiders in California vineyards, where spiders can comprise up to 95% of the arthropod predators (Costello and Daane, 1995, 1999). The most abundant insect pests in the studied vineyards were leafhoppers, Erythroneura spp., which are closely tied to vine phenology and condition (Daane and Williams, 2003) and are a likely prey source for spiders (Costello and Daane, 2003). Here, we examine whether spider dispersal in vineyards occurred (1) mainly in the spring season, when spiders are likely to play a critical role in pest suppression, (2) from within the vineyard or from the surrounding natural habitat, and (3) by air or over ground. 2. Materials and methods 2.1. Study sites Sample sites were three commercial vineyards in Napa County, California that abutted natural oak woodland/chaparral habitats. All vineyards were Cabernet cv., planted between 1998 and 2000, wire-trellised to a vertical system, on drip irrigation and with similar soil conditions. Large expanses of vineyard monoculture (500 m 500 m) that were adjacent to oak woodland but contained no additional trees or small clumps of natural vegetation were required as sites for this study, and vineyards in only one district of the Napa Valley met these criteria. Although the vineyards, hereafter referred to as the West, North, and South sites, were necessarily in close proximity to each other, each bordered a different patch of natural habitat. The West site was 930 m and 1040 m from the North and South sites, respectively. The North and South sites were 250 m apart. A road 10 m wide separated each vineyard and natural habitat. 2.2. Sampling methods Sticky traps were used to collect ballooning spiders, using a system adapted from Greenstone et al. (1985). Sticky traps consisted of hardware cloth coated with Stikem (Seabright Enterprises, Emeryville, CA). The cloth was 6.3 mm gauge and traps were 30 cm 50 cm. Traps were attached to stakes with two binder clips, which were affixed to stakes with cable ties. In vineyards, sticky traps were attached to 1 m wooden stakes, which were then secured to the vineyards’ metal trellis stakes using cable ties. Once in place, traps were above grape vine foliage, with their base 2 m above the ground. All foliage around traps was cut back to prevent foliage from becoming entangled on the trap. Sticky traps in oak woodland were placed on metal stakes hammered into the ground. As in the vineyards, the base of each trap was 2 m above the ground. For all sticky traps, a 2 cm wide band of Stikem was applied to the support stakes to prevent spiders from walking onto traps from below. Pitfall traps were used to monitor walking spiders and consisted of 11 cm 14 cm plastic cups buried in the ground up to the rim. A second rimless cup, filled with 2.5 cm of 25% solution of propylene glycol, was inserted inside the outer cup. Wood squares, supported by 2 cm wooden dowels, were placed over the mouth of pitfall traps to prevent debris from falling into traps. Spiders were removed from pitfall traps by pouring the liquid through a sieve. Pitfall traps were placed underneath each sticky trap. Sticky traps and pitfall taps were located along three transects at each site. Each transect was five rows (10 m) apart and ran 250 m into the vineyard and 50 m into the natural habitat. Trap distances were at 10, 50, 100, 150, 200 and 250 m into the vineyard, and were at 0 (woodland edge with the dirt road), 25 and 50 m into the natural habitat. Sticky traps and pitfall samples were collected at 13–15-day intervals, from 4 May through 4 October, 2006. The start date corresponded with pest development and vine
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phenology; in the Napa Valley, leafhoppers overwinter as adults and typically start laying eggs during late April or early May, when mature foliage begins to appear on vines (Daane and Costello, 2000). Sticky traps were removed and immediately replaced with fresh traps; spiders were removed from pitfall traps in the field and later stored at 4 8C before placing them in 70% alcohol. For sticky traps, spiders had to be removed in the laboratory. Sticky traps were stored at 4 8C for 24–48 h and then visually searched for spiders using a circular fluorescent light equipped with a magnifying glass. All spiders found were removed and placed in paint thinner for 7 days, to dissolve Stikem, and then placed in 70% alcohol. Spiders were sorted to species, genus, or morphospecies. Additionally, to monitor the composition of the spider community in vineyards and woodland, beat samples were taken on 27 April, 13–14 June, 5 September (West and South sites only) and 16 September (North site only), and 24–25 October. Three beat samples were collected at each transect distance from approximately 1 m3 of foliage. In vineyards, foliage between two vines was shaken and beaten for 30 s to dislodge spiders into a 1 m2 cloth funnel equipped at the bottom with a removable plastic bag (after Costello and Daane, 1997). In woodland, coast live oak (Quercus agrifolia) foliage was shaken (but not beaten) for 30 s, using the cloth funnel procedure. Coast live oak is the dominant tree species in Napa County, and in preliminary sampling contained higher numbers of spiders per sample than other common tree species or low-lying vegetation (i.e., grasses and bushes). All samples were transported to the laboratory in a cooler to retard predation, stored at 4 8C, and then placed in 70% alcohol and sorted to species, genus, or morphospecies. 2.3. Data analysis 2.3.1. Timing of spider dispersal and arrival in vineyards To assess the timing of spider dispersal and arrival in vineyards, seasonal spider abundance data from sticky traps, pitfall traps and beat samples were analyzed using MANOVA, with habitat, site and sample date as independent variables and spider number in each type of sample as the dependent variables. For sticky trap data, we conducted separate analyses of total spider numbers and spider numbers excluding dwarf spiders, Erigone spp. (Linyphiidae). Dwarf spiders dominated sticky traps, but were uncommon in vineyard foliage, and we wanted to examine the timing of dispersal for those spiders that are likely to play a role in the vineyard spider community. Data were log(x + 1) transformed prior to analyses. 2.3.2. Natural habitat as a source for spiders To assess whether spillover of ballooning spiders occurred from woodland into vineyards, Kruskal–Wallis tests and nonparametric multiple comparison tests, using the kruskalmc function in R version 2.7.0 (R Development Core Team, 2008), were used to compare number of spiders per sticky trap and number of species per sticky trap between transect distances. Parametric tests could not be used for sticky trap data, since variables did not conform to the assumption of equal variances, even after transformation. Numbers of spiders and spider species per pitfall trap were compared between transect distances using analysis of variance (ANOVA); spider numbers were log(x + 1) transformed prior to analysis. For these analyses, spider numbers were summed through the season for each transect distance at each site (after Bedford and Usher, 1994) and divided by the number of samples, resulting in 9 replicates for each transect distance (3 from each site). To further examine spillover of spiders from woodland into vineyards, spider composition of sticky and pitfall traps was compared between vineyard and woodland transect distances. For this analysis, data for each transect distance were averaged across
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the season and across all sites, resulting in one averaged sample for each transect distance. Spider composition was compared between each vineyard distance and each of the three woodland distances using the Sorensen index of similarity. The Sorensen index is a measure of proportional similarity, and ranges from 0 (no similarity) to 1 (identical). Overall numbers of ballooning spiders were low, making the Sorensen index the most appropriate choice for this analysis, since it uses incidence of species to compare samples, and is insensitive to changes in species abundances. 2.3.3. Dispersal mode The relative contributions of the two modes of dispersal (aerial versus ground) to spider composition in vineyards were assessed by comparing the spider composition in vineyard sticky traps and pitfall samples with beat samples from vineyards, using the Sorensen index of similarity and proportion of species collected in beat samples that were also present in both types of traps. Sites were analyzed separately. Data for traps and beat samples were summed through the season for each site and divided by the number of samples. Sites were also analyzed together by summing spider numbers across all three sites and through the season. In addition, total frequencies of those species that represented >1% of the spider composition in beat samples were compared between sticky and pitfall traps using 2 2 contingency tables and Fisher’s exact test, or in the case of dwarf spiders (Erigone spp.), a chi-square test (numbers were low for all species except Erigone spp., making the chi-square test inappropriate, while numbers of Erigone spp. were too high for Fisher’s exact test). The standard Bonferroni correction was used to compensate for Type I error. 3. Results 3.1. Spider composition in sticky traps A total of 1102 spiders (678 juveniles) representing 39 species and 16 families were collected on sticky traps in vineyards (Table 1). The most abundant spider family was Linyphiidae (58.4%), and dwarf spiders (Erigone spp.) accounted for the majority (94.9%) of the linyphiids. Besides Linyphiidae, the most common spider families on sticky traps in vineyards were: Gnaphosidae (6.2%), Tetragnathidae (4.8%), Araneidae (4.2%), Salticidae (4.2%), Philodromidae (4.1%), Theridiidae (3.2%), Thomisidae (3.1%), Lycosidae (2.7%), and Oxyopidae (2.2%). In woodland sites, a total of 1093 spiders (844 juveniles) were collected on sticky traps, representing 41 species and 16 families (Table 1). As in vineyards, the most numerous spider family on sticky traps was Linyphiidae (17.6%), with dwarf spiders constituting 73.6% of this group. The most numerous spider families on sticky traps in woodland were: Linyphiidae, Tetragnathidae (14.3%), Salticidae (13.3%), Theridiidae (10.9%), Philodromidae (7.0%), Araneidae (6.5%), Dictynidae (4.6%), Anyphaenidae (4.4%), Thomisidae (4.2%), and Miturgidae (3.9%). 3.2. Spider composition in pitfall traps A total of 2209 spiders representing 28 species and 14 families were collected in vineyard pitfall traps (Table 1). Pitfall samples were dominated by ground spiders of the family Gnaphosidae (53.2%), followed by the predominantly ground-dwelling Lycosidae (14.5%). Only four other families comprised more than 1% of the familial composition in vineyard pitfall traps: Oecobiidae (11.8%), Salticidae (9.6%, primarily an unidentified Metaphidippus sp. that was found only in pitfall samples), Corinnidae (8.3%, almost entirely Meriola californica Banks, which was unique to pitfall samples), and Linyphiidae (4.2%).
In woodland pitfall traps, a total of 1079 spiders from 24 species and 15 families were collected (Table 1). The family Lycosidae (35.9%) dominated these samples, followed by Gnaphosidae (29.1%), Corinnidae (10.5%), Salticidae (7.1%), and Liocranidae (5.4%). 3.3. Spider composition in beat samples In vineyard beat samples, a total of 219 spiders representing 23 species and 14 families were collected (Table 1). Spider composition was dominated by the families Miturgidae (30.7%), with Cheiracanthium mildei L. Koch alone constituting 24.7%, and Salticidae (28.6%), primarily comprised of Metaphidippus manni Peckham & Peckham, which represented 21.5% of spiders overall. Also represented were: Theridiidae (11.9%), comprised only of Theridion melanurum Hahn, Anyphaenidae (5.1%), Corinnidae (4.1%), represented solely by Trachelas pacificus Chamberlin, Gnaphosidae (3.2%), Mimetidae (3.2%), comprised only of Mimetus hesperus Chamberlin; and Oxyopidae (3.2%). A total of 660 spiders from 37 species and 16 families were collected in woodland beat samples (Table 1). Salticidae was the most abundant family (18.4%), followed by Theridiidae (16.4%). Other well-represented families included: Tetragnathidae (10.8%), Anyphaenidae (9.0%), Linyphiidae (7.5%), Dictynidae (6.9%), Miturgidae (5.5%), and Araneidae (4.9%). 3.4. Timing of spider dispersal and arrival in vineyards Sample date had a significant effect on total numbers of ballooning spiders (MANOVA analysis: F = 35.09; P < 0.001). There was also a sample date habitat interaction (F = 10.87, P < 0.001), showing that habitat had an effect on spider numbers that changed across the season. The lack of a sample date site interaction (Pillai’s trace = 1.40, P = 0.14) indicates that seasonal changes in spider abundance were not affected by study site. When dwarf spiders were excluded from analysis, numbers of ballooning spiders were affected by sample date (F = 25.82, P < 0.001), and the sample date habitat interaction (F = 8.82, P < 0.001), but not the sample date site interaction (Pillai’s trace = 1.08, P = 0.38). In vineyards, total numbers of ballooning spiders gradually declined during the sampling period, from May to October, while numbers of ballooning spiders in woodland were highest in late July (Fig. 1A). The vast majority of early-season ballooners in vineyards were dwarf spiders, however. For the rest of aerially dispersing spider community excluding dwarf spiders, numbers on vineyard sticky traps were low early in the season and reached a peak in mid-August (Fig. 1B). Numbers of spiders per pitfall trap were also influenced by sample date in MANOVA analysis (F = 2.748; P < 0.01), and habitat affected spider numbers over time (sample date habitat interaction, F = 6.64; P < 0.001). Changes over time in numbers of spiders per pitfall trap did not differ between study sites (sample date site interaction, Pillai’s trace = 1.37; P = 0.16). Numbers in woodland pitfall traps declined across the season, but numbers in vineyard pitfall traps did not follow a consistent pattern across the season (Fig. 1C). Differences between habitats were also inconsistent over time. In MANOVA analysis, numbers of spiders in foliage were affected by sample date (F = 14.29; P < 0.001). Habitat also influenced spider numbers across the season (sample date habitat interaction, F = 41.47; P < 0.001). There was no sample date site interaction (Pillai’s trace = 1.05; P = 0.40), which indicates that changes in spider numbers through time were similar across study sites. Numbers of spiders in vineyards gradually increased across the season (Fig. 1D). There were very few spiders in beat samples on either of the first two sampling
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263
Table 1 Percentages of spiders collected in sticky traps, pitfall traps, and beat samples. Spider family
Spider species
Sticky traps
Woodland
Vineyard
Amourobiidae
Unknown amaurobiid sp.
1.4
0.1
0.9
1.8
0.0
0.2
Anyphaenidae
Anyphaena pacifica Hibana incursa
0.5 0.5
0.5 3.9
0.1 0.0
0.0 0.0
4.6 0.5
2.3 6.7
Araneidae
Araneus sp. Cyclosa turbinata Araneid sp. 1 Araneid sp. 2 Araneid sp. 3 Unknown araneids
0.0 1.6 0.5 0.6 0.4 1.0
1.2 2.0 1.0 1.6 0.0 0.7
0.0 0.0 0.0 0.1 0.0 0.0
0.0 0.0 0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0 0.0 0.0
0.2 0.3 0.3 3.0 0.3 0.8
Clubionidae
Clubiona sp.
0.0
0.6
0.0
0.0
0.0
0.8
Corinnidae
Castianeira sp. Meriola californica Trachelas pacificus
0.0 0.0 1.8
0.0 0.0 5.9
0.0 8.1 0.1
9.9 0.6 0.0
0.0 0.0 4.1
0.0 0.0 7.3
Dictynidae
Dictyna sp. 1 Dictyna sp. 2 Mallos sp. Unknown dictynids
0.2 0.1 0.5 0.5
0.2 0.1 3.3 1.0
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.7
0.0 1.8 0.0 0.0
0.0 0.5 5.9 0.5
Gnaphosidae
Micaria sp. Zelotes sp. 1 Zelotes sp. 2 Unknown gnaphosids
0.0 0.0 0.0 6.2
0.0 0.0 0.0 1.6
7.2 28.6 16.5 0.9
1.0 13.4 12.8 1.9
0.0 0.5 0.9 2.7
0.0 0.0 0.0 1.7
Linyphiidae
Erigone spp. Other Erigoninae Pityohyphantes sp. Linyphiid sp. 1 Linyphiid sp. 2 Unknown linyphiids
55.4 0.0 0.0 1.9 0.5 0.6
11.2 0.0 0.1 2.3 3.4 0.6
2.8 0.0 0.0 0.2 0.3 0.1
0.0 2.0 0.0 0.0 0.0 0.2
1.4 0.0 0.0 0.0 0.0 0.0
3.6 0.0 0.2 0.2 3.5 0.0
Vineyard
Pitfall traps Woodland
Vineyard
Beat samples Woodland
Liocranidae
Unknown liocranid sp.
0.0
0.0
0.0
5.4
0.0
0.0
Lycosidae
Hogna sp. Pirata sp. Lycosid sp. 1 Unknown lycosids
0.0 0.0 0.0 2.7
0.0 0.0 0.0 1.3
9.5 0.0 5.0 0.0
14.6 0.7 20.6 0.0
0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0
Mimetidae
Mimetus hesperus
0.1
0.5
0.0
0.0
3.2
2.0
Miturgidae
Cheiracanthium inclusum Cheiracanthium mildei C. mildei or C. inclusum
0.6 0.7 0.5
1.3 1.0 1.6
0.1 0.0 0.0
0.0 0.2 0.0
5.5 24.7 0.5
1.5 3.9 0.0
Nemesiidae
Calisoga sp.
0.0
0.0
0.2
0.2
0.0
0.0
Oecobiidae
Oecobius navus
0.0
0.0
11.8
1.3
0.0
0.0
Oxyopidae
Oxyopes salticus Oxyopes scalaris Unknown oxyopids
1.5 0.5 0.2
1.5 1.7 0.0
0.0 0.0 0.0
0.0 0.0 0.0
2.7 0.5 0.0
2.0 0.0 0.0
Philodromidae
Ebo sp. Philodromus sp. 1 Philodromus sp. 2 Philodromus sp. 3 Unknown philodromids
0.2 2.9 0.5 0.5 0.0
0.2 4.8 0.7 1.3 0.0
0.0 0.0 0.0 0.0 0.0
0.0 0.0 0.0 0.0 0.2
0.0 0.5 0.5 0.5 0.0
0.3 2.4 0.5 1.5 0.0
Salticidae
Habronattus sp. Metaphidippus manni Metaphidippus sp. Phidippus sp. Salticus scenicus Salticus sp. Sassacus vitis Thiodiona hespera Unknown salticids
0.3 2.9 0.0 0.1 0.1 0.0 0.1 0.4 0.3
0.4 11.7 0.0 0.1 0.0 0.0 0.0 0.7 0.4
0.2 0.0 5.2 0.0 0.1 0.0 0.0 0.0 0.2
0.0 0.0 7.1 0.0 0.0 0.0 0.0 0.0 0.2
0.0 21.5 0.0 1.8 4.1 0.0 0.0 0.9 0.0
0.0 10.8 0.0 0.2 0.2 0.9 0.0 5.8 0.5
Tengellidae
Titiotus californicus
0.0
0.0
0.1
3.4
0.0
0.0
Tetragnathidae
Tetragnatha laboriosa Tetragnatha versicolor
4.8 0.0
14.3 0.0
0.0 0.0
0.0 0.0
2.7 0.0
10.3 0.5
Theridiidae
Euryopis sp. Theridion melanurum Theridion dilutum Theridion spp.
0.0 0.5 1.4 0.9
0.2 4.8 2.4 2.6
0.0 0.0 0.0 0.4
0.3 0.0 0.0 0.0
0.0 11.9 0.0 0.0
0.0 3.9 11.1 0.2
264
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Table 1 (Continued ) Spider family
Spider species
Sticky traps Vineyard
Thomisidae
Pitfall traps Woodland
Vineyard
Unknown theridiids
0.4
0.9
0.4
0.0
0.0
1.2
Coriarachne sp. Diaea sp. Misumenops sp. Tmarus sp. Xysticus sp.
0.0 0.0 1.5 0.2 0.8
0.0 0.8 0.7 0.6 1.3
0.0 0.0 0.0 0.0 0.5
0.0 0.1 0.0 0.0 1.9
0.0 0.0 0.9 0.0 0.9
0.0 0.2 1.4 0.2 0.0
0.6
0.8
0.0
0.6
0.5
1.1
Unknown
Woodland
Vineyard
Beat samples Woodland
Total spiders
1102
1093
2209
1079
219
660
Number spp.
39
41
28
24
23
37
dates. Numbers of spiders in woodland beat samples increased early in the season, before sharply declining late in the summer. For most of the season, numbers of spiders were higher in woodland than vineyard (Fig. 1D). 3.5. Natural habitat as a source for spiders Total number of spiders per sticky trap changed across transects (Fig. 2A), and were significantly different among transect distances (Kruskal–Wallis test, H = 46.86, P < 0.001). Within vineyards, numbers were significantly higher at the vineyard edge than at the furthest distance from woodland. Numbers of spiders per trap were higher 25 m into woodland than 50 m, 100 m, 150 m and 250 m from the woodland edge in the vineyard, while numbers at woodland distances 0 and 50 m were significantly higher than 50 and 250 m into the vineyard (nonparametric multiple comparison test, P < 0.05). Number of spider species per sticky trap also showed significant differences among transect distances (Kruskal–Wallis test, H = 60.05, P < 0.001; Fig. 2A). The number of species per trap was significantly higher at the vineyard edge than at the vineyard distance furthest from woodland (nonparametric multiple com-
parison test, P < 0.05). At all woodland distances there were significantly more species per trap than at all vineyard distances except at the vineyard edge and at the 200 m vineyard distance (nonparametric multiple comparison test, P < 0.05). Numbers of spiders per pitfall trap did not change across transects (ANOVA, F = 1.15, P = 0.34), although there was a nonsignificant decrease at the vineyard edge (Fig. 2B). Numbers of spider species per pitfall trap were similarly unaffected by transect distance (F = 0.55, P = 0.81). For sticky traps, spider species composition at the vineyard edge tended to be more similar to woodland than the other vineyard distances (Table 2). In comparisons of spider species composition in pitfall traps, by contrast, the vineyard distance furthest from woodland was the most similar to the woodland (Table 2). 3.6. Dispersal mode Sorensen index values and percentages of species found in vineyard beat samples that were also present in sticky and pitfall traps were consistently higher in comparisons between sticky traps and beat samples than between pitfall and beat samples (Table 3). Proportional representation for many of the dominant
Fig. 1. Mean numbers (SE) of spiders per sticky trap, including all spiders (A), per sticky trap, excluding dwarf spiders (B), per pitfall trap (C) and per beat sample (D) through the season in vineyard and woodland habitats.
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265
Table 3 Comparisons of sticky and pitfall traps with vineyard beat samples, using the Sorensen index of similarity, percentage of species collected in beat samples that were also present in traps, and number of species shared between beat samples and traps. Trap type
Study site
Sorensen index
Beat species shared (%)
Species shared
Sticky
West North South Overall
0.55 0.51 0.61 0.70
68.75 73.33 93.33 87.75
11 11 14 21
Pitfall
West North South Overall
0.17 0.17 0.39 0.46
18.75 20.00 46.67 50.00
3 3 7 12
Fig. 3. Comparison of proportional spider composition in pitfall traps, sticky traps and vineyard beat samples. Only a few individuals of some families were collected in pitfall traps, and are not visible in this figure.
Fig. 2. Mean numbers (SE) of spiders and spider species per sticky trap (A) and per pitfall trap (B) along transects, averaged across the season, with 9 replicates for each transect distance (3 from each site). Different lower- and uppercase letters indicate significantly different mean values for total number of spiders and number of spider species, respectively (nonparametric multiple comparison tests, P < 0.05).
families in beat samples was also higher on sticky traps than pitfall traps (Fig. 3). The only families that occurred in high proportions in both beat and pitfall samples were Gnaphosidae, Salticidae and Corinnidae, and of these, Salticidae and Corinnidae were represented almost entirely in pitfall traps by an unidentified Metaphidippus sp. and a Meriola sp., respectively, species that were unique to pitfall traps. Sticky traps and beat samples differed widely in relative abundance of families, however. Although linyphiid spiders made up the majority of spiders in vineyard sticky traps, they were rarely recovered in beat samples. On the other hand, Miturgidae and Salticidae dominated beat samples, but comprised only a small proportion of the familial composition of sticky traps.
Of the 13 species that represented >1% of the spider composition in beat samples, seven occurred in significantly higher numbers in sticky traps than pitfall traps. C. mildei, Cheiracanthium inclusum Hentz (Miturgidae), M. manni, T. pacificus, Erigone spp., Oxyopes salticus Hentz (Oxyopidae), and Tetragnatha laboriosa Hentz (Tetragnathidae) occurred more frequently on sticky traps than expected by chance alone (Fisher’s exact tests, P < 0.001; chi-square test, P < 0.001, for Erigone spp.). Six species showed no significant difference between trap types: Anyphaena pacifica Banks (Anyphaenidae); Dictyna sp. 2 (Dictynidae); M. hesperus; Salticus scenicus Clerck (Salticidae); Phidippus sp. 1 (Salticidae); and T. melanurum (Fisher’s exact tests, P > 0.001). No species were higher in number in pitfall traps. 4. Discussion In this study, numbers of dispersing spiders were not higher in the spring, with the exception of the linyphiid dwarf spiders, which ballooned in high numbers during May and June. These results are
Table 2 Comparisons of spider composition between vineyard and woodland transect distances for sticky and pitfall traps, using the Sorensen index of similarity. Trap type
Distance into woodland
Distance into vineyard 10
50
100
150
200
250
Sticky
0 25 50
0.80 0.81 0.83
0.78 0.73 0.81
0.77 0.72 0.81
0.74 0.72 0.74
0.81 0.78 0.81
0.70 0.64 0.74
Pitfall
0 25 50
0.65 0.67 0.65
0.65 0.67 0.70
0.63 0.59 0.63
0.65 0.67 0.65
0.65 0.61 0.65
0.75 0.71 0.74
266
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in accordance with Oberg and Ekbom (2006), who presented evidence that linyphiid spiders disperse early in the season. For the spider community excluding dwarf spiders, numbers of ballooning spiders were highest in vineyards and woodland during August and July, respectively. In addition, dispersal activity over ground did not occur mainly in the spring; spider numbers in vineyard pitfall traps showed no consistent pattern across the season. Oberg and Ekbom (2006) also found no change in numbers of grounddispersing spiders in crop fields over time. Early-season spider abundance on vines appeared to reflect the lack of increased dispersal activity during this time. Numbers on vines were low at least until mid-June, indicating that spiders neither overwintered in vineyards nor arrived early in the spring. We suggest that any impacts of spiders on pests in vine foliage are likely to be limited to late summer or early fall. Numbers of woodland spiders on aerial traps and in the foliage were consistently higher than in vineyards for most of the season, indicating that oak woodland was a source for spiders in vineyards. The density of source populations is often highly correlated with the total number of aerially dispersing spiders (Weyman et al., 1995). In this study, we did not directly examine movement between habitats or the role of reproduction in the increase of spiders across the season. However, the low numbers of spiders in vineyards observed early in the season, combined with the drastic difference between habitats in spider abundance, strongly indicates that spiders arrived in vineyards from nearby oak woodland. The increase in spider numbers and spider species richness on sticky traps at the vineyard edge, where spider species composition also tended to be more similar to woodland than at other vineyard distances, supplies additional indirect evidence that spillover of ballooning spiders from woodland contributed to vineyard spider composition. Similarly, Sackett et al. (2009) found that spider abundance and species composition in apple orchards were affected by distance from natural source habitat, and that this shift occurred over a distance of only 40 m. Results from the present study suggest that many spider species in the vineyard ecosystem balloon only short distances. Along transects, gradual transitions between habitats are often associated with species that have limited dispersal abilities (Duelli et al., 1990). Many spider species may have wafted short distances into vineyards from surrounding trees. Traps that are placed only a few meters from the ground, as they were in this study, may collect spider species that have merely drifted towards the ground from a higher take-off point (Greenstone et al., 1987). Other studies have shown that many spiders disperse only short distances by ballooning, in some instances traveling only a few meters (Riechert and Gillespie, 1986; Morse, 1993; Samu et al., 1999). Ground spiders were unaffected by transect distance, and numbers were not consistently higher in oak woodland. Oberg and Ekbom (2006) obtained similar results, and suggested that spiders may be able to rapidly recolonize fields from non-crop habitats by walking. In the present study, transects may not have been long enough to observe an effect on ground spiders. Alternatively, ground spiders may be unaffected by seasonal changes in vineyards, and may not recolonize vineyards from natural habitats. Ground dispersal appeared to contribute relatively little to the spider community on vines. Spider composition on vines reflected sticky traps far more than pitfall traps, and the majority of the wellrepresented vineyard species were more numerous on sticky traps. Most importantly, three of the four dominant vineyard species—C. mildei, C. inclusum and M. manni—occurred more frequently on sticky traps. These results suggest that spiders in vineyards disperse more by air than over ground. Bishop and Riechert (1990) also found that spider composition differed widely between sticky and pitfall traps, and concluded that many spiders arrived in crop
fields via ballooning. In this study, the vast majority of spiders collected in pitfall traps were from three predominantly grounddwelling families (Gnaphosidae, Lycosidae, Oecobiidae) that were not present in significant numbers on vines. Costello and Daane (2003) similarly report that spider species composition on the ground was different from that on the vines above. Although spiders may colonize vineyards by air, most likely from natural source habitats, other factors may also contribute to their establishment in vineyards. The four dominant species in vineyard beat samples—C. mildei, C. inclusum, M. manni and T. melanurum—appeared on sticky traps, but not in high numbers. These spiders, particularly C. mildei, are likely to be highly adapted to disturbed agricultural settings, and typically dominate vineyard spider composition in the Napa Valley region (Hogg and Daane, unpubl.). While only low numbers of C. mildei may disperse into vineyards, their competitive abilities may allow them to dominate the spider community. It is also possible that spiders such as C. mildei are year-round residents of vineyards, giving them an advantage over species that arrive from natural habitat in summer. This possibility does not seem likely, however, since vineyards are unlikely to provide a suitable habitat for spiders until vines sprout foliage in late spring, later than most spiders in this system emerge from hibernation and reproduce (B. Hogg, pers. obs.). Dwarf spiders showed high aerial dispersal rates, on the other hand, but were never well-represented on vines and may be unsuited to vineyard conditions. Habitat quality can be an important factor in determining whether spiders choose to stay, or balloon to another habitat (Morse, 1993; Samu et al., 1999), and traps such as those used in this study can collect spiders that would have immediately taken off again (Weyman et al., 2002). If many spider species are ballooning short distances from natural habitat into vineyards, close proximity to natural habitat may elevate spider diversity, which could have implications for pest suppression. Elevated predator diversity can increase impacts on herbivores (Snyder et al., 2006). Or, the few predator species that flourish in agroecosystems may drive impacts on pest populations. Further investigation of predator interactions is needed to understand the relative importance of local and landscape factors in shaping the impacts of predators on pest populations in agroecosystems. Acknowledgements This work was supported with grants from the National Science Foundation Dissertation Improvement Grant DEB 0710434, the van den Bosch Memorial Scholarship, and the California Table Grape Commission and American Vineyard Foundation. We thank vineyard managers for use of their farms Tian Hu for help in the field and laboratory, and three anonymous reviewers for their helpful comments and suggestions. References Bedford, S.E., Usher, M.B., 1994. Distribution of arthropod species across the margins of farm woodlands. Agric. Ecosyst. Environ. 48, 295–305. Bishop, L., Riechert, S.E., 1990. Spider colonization of agroecosystems: mode and source. Environ. Entomol. 19, 1738–1745. Bonte, D., Lens, L., Maelfait, J.P., 2006. Sand dynamics in coastal dune landscapes constrain diversity and life-history characteristics of spiders. J. Appl. Ecol. 43, 735–747. Burel, F., Baudry, J., 1995. Species biodiversity in changing landscapes: a case study in the Pays d’Auge, France. Agric. Ecosyst. Environ. 55, 193–200. Costello, M.J., Daane, K.M., 1995. Spider (Aranaeae) species composition and seasonal abundance in San Joaquin Valley grape vineyards. Environ. Entomol. 24, 823–831. Costello, M.J., Daane, K.M., 1997. Comparison of sampling methods used to estimate spider (Araneae) species abundance and composition in grape vineyards. Environ. Entomol. 26, 142–149. Costello, M.J., Daane, K.M., 1999. Abundance of spiders and insect predators on grapes in central California. J. Arachnol. 27, 531–538.
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