Ground-Dwelling Spider Fauna (Araneae) of Two Vineyards ... - BioOne

COMMUNITY AND ECOSYSTEM ECOLOGY

Ground-Dwelling Spider Fauna (Araneae) of Two Vineyards in Southern Quebec ELISE BOLDUC,1 CHRISTOPHER M. BUDDLE,1, 2 NOUBAR J. BOSTANIAN,3 CHARLES VINCENT3

AND

Environ. Entomol. 34(3): 635Ð645 (2005)

ABSTRACT The spider fauna of vineyards in northern parts of North America are completely unknown, even though spiders represent important natural enemies to phytophagous insects occurring in vineyards. Weekly pitfall trapping in 1998 and 1999 in two vineyards in southern Quebec yielded over 4,600 spiders belonging to 97 species and 16 families. Spider assemblages (diversity and community composition) were similar between the two vineyards independent of environmental differences. However, some species-speciÞc patterns were noted when the two vineyards were compared. High landscape diversity, including fallow Þelds and adjacent apple orchards, is hypothesized to account for a higher abundance of certain agrobiont species in one of the vineyards. Phenological data shows the most abundant linyphiid species, Tennesseellum formicum (Emerton), exhibits high phenotypic variation, and its multivoltine life cycles may be of adaptive importance for vineyards that are frequently disturbed. We also note several other species exhibiting period of peak activity in the spring [e.g., the wolf spiders Pardosa moesta Banks and Trochosa ruricola (De Geer)] or autumn [e.g., the funnel-web spider Agelenopsis potteri (Blackwall)]. Species turnover was high between sample dates, and data on activity and species richness of two guilds (web-building spiders and hunting spiders) indicate that many species that differ in foraging mode are active during all months of the growing season. The diverse ground-dwelling spider fauna in vineyards is therefore well positioned to prey on phyotophagous pests, and their populations should be conserved in these agroecosystems. KEY WORDS agrobiont spiders, grapes, landscape diversity, natural enemies, phenology

VINEYARDS ARE A RELATIVELY NEW industry in the province of Quebec, Canada (Dubois and Dehaies 1997). Until recently, growers followed guidelines set for Ontario and New York state vineyards for the management of many arthropod pests (Bostanian et al. 2003). However, Bostanian et al. (2003) observed that phytophagous arthropods in Quebec vineyards differ qualitatively and quantitatively from those in Ontario and New York. They hypothesized that the lowest abundance of pests in Quebec vineyards was caused by a high pest mortality caused by colder winter temperatures and the agroeconomic activity of earthing up the vines in autumn (Bostanian et al. 2003). The “earth-up” of the vines consists in scraping earth between vineyard rows to cover the roots with 45 cm of soil to prevent them from freezing during the winter. This practice can kill the phytophagous insects overwintering in or on the soil by exposing them to cold, by mechanically destroying them, or by exposing them to predators (Bostanian et al. 2003). The differences in 1 Department of Natural Resource Sciences, McGill University, Macdonald Campus, 21,111 Lakeshore Rd., Ste Anne de Bellevue, Quebec H9X 3V9, Canada. 2 Corresponding author, e-mail: [email protected]. 3 Horticultural Research and Development Centre, Agriculture and Agri-Food Canada, 430 Gouin Blvd., Saint-Jean-sur-Richelieu, Quebec J3B 3E6, Canada.

phytophagous fauna between Quebec and neighboring vineyards show the need for the development of management techniques speciÞc to local climatic and agricultural conditions. To reach this goal, it is important to document the assemblages of both phytophagous insects and the native natural enemy complex occurring within Quebec vineyards. Spiders (Arachnida: Araneae) are important predators in almost every imaginable habitat. In vineyards, the spider community is comprised of both arboreal and ground dwelling species (Costello and Daane 1995, 2003). Here, we focus on the ground-dwelling spider fauna. Most spiders are generalist predators, although a few exceptions exist (Nentwig 1986). In their review of the role of generalist predators as biological control agents, Symondson et al. (2002) highlighted numerous examples of how generalist arthropod predators signiÞcantly decreased pest populations, and in many cases, increased yield as a result. Although individual spider species may not exhibit classic density-dependent control of pests (Riechert and Lockley 1984, Sunderland 1999), it has been shown that a diverse assemblage of spiders has the potential to regulate pest insect populations (e.g., Mansour and Whitecomb 1986, Oraze and Grigarick 1989, Riechert and Bishop 1990, Carter and Rypstra 1995, Nyffeller and Benz 1997). Therefore, maintain-

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ing a diverse spider fauna, with species complementing each other in terms of size, spatial-temporal distribution, foraging mode, and food preferences (Nyffeler and Sterling 1994, Marc and Canard 1997), represents an important component of control by native natural enemy assemblages in agroecosystems. Hence, the importance of spider conservation in Quebec vineyards cannot be understated, and spider diversity should be promoted. A Þrst step to reach this goal is to actually document the fauna present in vineyards. To our knowledge, the only extensive research on spiders in North American vineyards has occurred in California (e.g., Costello and Daane 1995, 1999, 2003). Management practices are likely to affect spider assemblages. Epstein et al. (2000), for example, noted higher spider catches after eliminating broad-spectrum insecticides from apple orchards. This effect may be linked to the toxicity of the compounds themselves and/or to a reduction in available prey after insecticide application. Similarly, Peka´r (1999) observed lower spider abundance under conventional spraying practices than under integrated pest management (IPM), and Brown et al. (2003) documented higher spider diversity when apple trees were left unsprayed. Cultural practices such as tillage, ground cover, and intercropping also inßuence spider diversity and abundance by modifying the availability of habitat and food (Rypstra and Carter 1999, Costello and Daane 2003). The main objective of this study was to characterize the ground-dwelling spider fauna occurring in vineyards of southern Quebec. Two vineyards were compared, across 2 sampling yrs, to assess whether faunal differences occur between vineyards, in terms of diversity and species composition. We also evaluated phenological patterns of the dominant species in the system and examined species turnover by sample period and patterns in activity and species richness of two foraging guilds: web-building spiders and hunting spiders. This is done to test whether different species may compliment each other during the growing season, and thus potentially exert consistent predation pressure on phytophagous insect pests in vineyards (i.e., effects of spider assemblages rather than speciÞc species; Riechert and Lawrence 1997). This work represents the Þrst survey of spiders occurring in vineyards in northeastern North America, and this baseline data will be critical when evaluating future management regimes for vineyards in northern climes. Materials and Methods Study Area and Sampling. Two vineyards were studied: vineyard I (lÕOrpailleur; 45⬚07⬘ N, 72⬚51⬘ W), located near Dunham, Quebec (Canada), consists of Seyval Blanc as the sole cultivar planted on sand and gravel loam. This study plot is bordered on its northern side by an apple orchard, a large fallow Þeld and a small bushy site with leaf litter on the western side, and vineyard on the southern and eastern sides. Vineyard II (Dietrich-Jooss; 45⬚16⬘ N, 73⬚11⬘ W), near

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Iberville, Quebec, contains the cultivars Cayuga white, De Chaunac, and Seyval blanc planted on a clay loam soil. A stream within an herbaceous fallow band ⬇15 m wide bordered the southern side of this study plot. Vineyards border the three other sides, although there is a corn Þeld near the eastern side. The two study plots have a light weed cover during spring and summer. In both vineyards, soil was managed in a similar fashion, with topsoil removed twice a year (spring and fall) to cover and uncovered young vines and protect them from cold temperature. For the data-collecting period, plots received no herbicides or insecticides but were treated with fungicides. Products used were captan (Captan 50 WP, Micro Flo Corp., Memphis, TN), metaxyl (Ridomil 72 WP, Syngenta Crop Protection, Toronto, ON, Canada), metiram (Polyram 80 WP, BASF Corp. Ag Products, Toronto, ON, Canada), and myclobutanil (Nova 40 WP, Dow Agro Science, Indianapolis, IN). See Bostanian et al. (2003) for additional details about the vineyards. Spiders were collected weekly from May to midSeptember 1998 Ð1999 in each of the vineyards. Pitfall traps were put in random locations determined directly in the Þeld. Thirteen pitfall traps were placed in lÕOrpailleur, and 24 pitfall traps were placed in Dietrich-Jooss. The traps were all placed randomly and were serviced about every 7 d. Pitfall traps were yellow vinyl trays (18.5 by 11.5 by 5.5 cm) positioned in a wooden frame 1.3 cm thick (outside dimensions, 19.5 by 26.5 cm; inside dimensions, 11.8 by 18.7 cm). The outer frame edges were cut at ⬇45⬚ to make the junction between the ground and frame more continuous. The inner side of the frame was routed to form a 1-cm-wide and 0.25-cm-deep groove on the upper surface. The vinyl container had a ßat 6- to 7-mm-wide rim on its edge for rigidity. This rim Þtted perfectly into the wood frame and was curved down into the container. Holes were dug in the ground within the rows, and traps were Þt in such a way that the top of the frame would be ßush to the ground. Each trap was Þlled with 30% ethylene glycol and 2 ml liquid soap. With the exception of immature spiders and damaged specimens, all spiders were keyed to species using Paquin and Dupe´ rre´ (2003) and other miscellaneous literature. Immatures were all identiÞed to family with the exception of spiderlings (i.e., spiders recently emerged from an egg sac). Voucher specimens will be deposited in the Canadian National Collection (Ottawa, Ontario, Canada). ClassiÞcation and nomenclature followed Paquin and Dupe´ re (2003). Data Analysis. To standardize catch rates between the two orchards (i.e., caused by the different number of traps occurring in each orchard), all relative abundance data were compared using a mean number of spiders collected on a per-trap basis. This approach included juvenile spiders, but not spiderlings. The overall means were used to assess whether spiders were caught in higher frequency in any particular vineyard or in 1 particular yr. Diversity comparisons were done using rareÞed estimates of species richness using Ecosim software (Gotelli and Entsminger 2001).

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BOLDUC ET AL.: GROUND-DWELLING SPIDER FAUNA OF VINEYARDS IN QUEBEC

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Table 1. Species richness and mean no. individual spiders (ⴞSE) per pitfall trapfrom collections made in two vineyards of southern Quebec (1998 and 1999) Species Total no. specimens Mean no. spiders per trap Tennesseellum formicum (Emerton) Trochosa ruricola (De Geer) Erigone atra Blackwall Halorates plumosus (Emerton) Erigone blaesa Crosby & Bishop Agyneta unimaculata (Banks) Agelenopsis potteri (Blackwall) Islandiana flaveola (Banks) Walckenaeria spiralis (Emerton) Pardosa moesta Banks Raw species richness RareÞed estimates of expected species richness

Vineyard I (lÕOrpailleur)

Vineyard II (Dietrich-Jooss)

Raw total

1998

1999

1998

1999

1998 Ð1999

1,448 111.4 ⫾ 16.5 54.6 ⫾ 10.6 6.9 ⫾ 1.4 11.4 ⫾ 2.4 9.9 ⫾ 2.0 1.7 ⫾ 0.6 2.2 ⫾ 0.6 0.2 ⫾ 0.1 0.1 ⫾ 0.1 1.4 ⫾ 0.4 0.1 ⫾ 0,1 43 38.2

1,035 79.6 ⫾ 11.1 38.3 ⫾ 10.0 2.8 ⫾ 0.4 7.4 ⫾ 1.3 3.2 ⫾ 1.7 0.3 ⫾ 0.2 1.6 ⫾ 0.5 0.5 ⫾ 0.2 0.0 0.4 ⫾ 0.2 0.4 ⫾ 0.2 50 38.0

1,125 46.9 ⫾ 3.8 14.0 ⫾ 2.3 9.7 ⫾ 1.1 1.5 ⫾ 0.4 1.3 ⫾ 0.4 1.3 ⫾ 0.3 2.0 ⫾ 0.3 0.9 ⫾ 0.2 1.3 ⫾ 0.3 0.3 ⫾ 0.1 0.4 ⫾ 0.1 44 40.5

1,002 41.8 ⫾ 3.3 13.1 ⫾ 1.7 4.3 ⫾ 0.5 1.1 ⫾ 0.3 1.7 ⫾ 0.4 3.9 ⫾ 1.3 0.9 ⫾ 0.2 1.7 ⫾ 2.3 0.3 ⫾ 0.1 0.1 ⫾ 0.1 0.2 ⫾ 0.1 48 48.9

4,610 Ñ 1,858 463 307 230 152 120 57 40 33 21 97 Ñ

Total collection and common species (those with ⬎10 individuals) are presented, as well as raw totals for both years combined. RareÞed estimates of expected species richness are based on 720 individuals.

This was done to standardize species richness to sampling effort (i.e., number of individuals or samples) (Gotelli and Colwell 2001). Input data were the individuals (separated by species) captured by year and/or vineyard (i.e., I or II). Expected number of species, E(s), were generated through resampling (using the rarefaction algorithm) for various sample sizes, up to the total number of collected individuals. Measures of variance (⫾SD) were calculated for each subsample size. Because these curves use both species richness and relative abundance data, they represent an index of diversity (Magurran 2004). To investigate variation in community composition, individual pitfall trap data were analyzed using detrended correspondence analysis (DCA). This ordination technique allows for assessing variation between samples using relative abundance data for the entire species complement (McCune and Grace 2002). For this analysis, rare species were downweighted, and the program PCOrd (version 4.0) was used (McCune and Mefford, 1999). Species turnover was evaluated by completing a matrix of shared species by sample period. Phenological patterns were determined by plotting catches of males and females of the most commonly collected species. We also separated the spider data into two foraging guilds (web-building species and hunting species) to evaluate whether species from these guilds compliment each other (species richness and relative abundance) over the growing season in the vineyards. Web-builders (e.g., families Agelenidae, Araneidae, Dictynidae, Linyphiidae, Tetragnathidae, Theridiidae) use silk to capture prey, whereas hunters (e.g., families Anyphaenidae, Clubionidae, Gnaphosidae, Lycosidae, Philodromidae, Salticidae, Thomisidae) do not rely on silk to capture prey. This approach allows us to compare the temporal distribution of two groups of spiders that have distinct foraging modes and food preferences (e.g., Bultman and Uetz 1982, Riechert and Lawrence 1997, Buddle et al. 2000).

Results A total of 1,258 trap-days yielded 4,610 individual spiders. They represented 97 species distributed in 16 families (Tables 1 and 2). Overall, more spiders were collected from vineyard I (Table 1), and this seems partially driven by an increased catch of spiders in vineyard I in 1998 (Table 1). The family Linyphiidae (dwarf and sheet-web weavers) was dominant in the samples, representing 32 of the 97 species and 78.6% of the total number of individuals collected (Table 2). Tennesseellum formicum (Emerton) accounted for 51% of all mature spiders collected and was more abundant in vineyard I than in vineyard II for both years (Table 1). The linyphiids Erigone atra Blackwall and Halorates plumosus (Emerton) were also most abundant in vineyard I (Table 1). The wolf spider (Lycosidae) Trochosa ruricola (De Geer) accounted for 12.7% of the adult spiders collected and were more frequently collected in 1998 than 1999 (Table 1). We also recorded Wulfila saltabundus (Hentz) (Family Anyphaenidae) for the Þrst time in Quebec (Table 2). Raw species richness varied from 43 to 50 by vineyard type and collection year (Table 1). Individualbased rarefaction curves reveal that enough sampling was done to make comparisons of spider diversity by vineyard and year (Fig. 1). RareÞed estimates at 720 individuals suggest few differences in diversity between year or vineyard, except higher expected species richness in vineyard II in 1999 (Table 1). Focusing on vineyard I, it is clear that spider diversity was the same for both sampling years, because the expected number of species did not differ signiÞcantly across all subsamples (Fig. 1A). In vineyard II, however, diversity was signiÞcantly lower in 1998 compared with 1999, with subsamples of ⬎400 individuals (Fig. 1B). There were no signiÞcant differences when both vineyards were compared (Fig. 1C). The DCA is not presented, because the ordination explained only 10.4% of the total variation in the spe-

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Table 2. Spider (Araneae) families and species (adults only, immature presented to family level only) collected in two vineyards of southern Quebec (1998 –1999) Vineyard I Agelenidae Agelenopsis potteri (Blackwall) Amaurobiidae Wadotes hybridus (Emerton) Anyphaenidae Wulfila saltabundus (Hentz) Araneidae Argiope trifasciata (Forskal) Araneus trifolium (Hentz) Araneus diadematus Clerck Clubionidae Clubiona abbotii L. Koch Clubiona canadensis Emerton Clubiona johnsoni Gertsch Corinnidae Castianeira descripta (Hentz) Castianeira longipalpa (Hentz) Dictynidae Argenna obesa Emerton Dictyna minuta Emerton Emblyna annulipes (Blackwall) Emblyna phylax (Gertsch and Ivie) Emblyna sublata (Hentz) Gnaphosidae Drassyllus depressus (Emerton) Drassyllus fallens Chamberlin Herpyllus ecclesiasticus Hentz Micaria publicaria (Sundevall) Sosticus insularis (Banks) Callilepsis pluto Banks Zelotes fratris Chamberlin Gnaphosa parvula Banks Linyphiidae (Linyphiinae) Agyneta fabra (Keyserling) Agyneta simplex (Emerton) Agyneta unimaculata (Banks) Bathyphantes brevis (Emerton) Bathyphantes concolor (Wider in Reuss) Bathyphantes pallidus (Banks) Centromerus sylvaticus (Blackwall) Microlinyphia mandibulata mandibulata (Emerton) Microlinyphia pusilla (Sundevall) Ostearius melanopygius (O. Pickard-Cambridge) Tennesseellum formicum (Emerton) Linyphiidae (Erigoninae) Aphileta misera (O. Pickard-Cambridge) Ceraticelus similes (Banks) Ceratinella buna Chamberlin Eperigone trilobata (Emerton) Eperigone undulata (Emerton) Erigone atra Blackwall Erigone autumnalis Emerton Erigone blaesa Crosby and Bishop Erigone dentigera O. Pickard-Cambridge Grammonota gentiles Banks Grammonota inornata Emerton Grammonota pallipes Banks Halorates plumosus (Emerton) Hypomma marxi (Keyserling) Islandiana flaveola (Banks) Islandiana longisetosa (Emerton) Oedothorax trilobatus (Banks) Scylaceus pallidus (Emerton) Walckenaeria atrotibialis O. Pickard-Cambridge Walckenaeria spiralis (Emerton) Walckenaeria tibialis (Emerton) Liocranidae Phurotimpus alarius (Hentz) Phurotimpus borealis (Emerton) Agroeca pratensis Emerton

Vineyard II

1998

1999

1998

1999

2

6

21

28

Ñ

2

Ñ

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2

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Ñ

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Ñ 7

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1 3 Ñ 1 1

5 5 1 Ñ Ñ

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1 Ñ Ñ 1 Ñ Ñ 1 Ñ

11 12 29 1 6 1 Ñ Ñ Ñ Ñ 710

4 3 21 Ñ 2 Ñ 2 Ñ 2 Ñ 498

1 1 49 Ñ 2 Ñ Ñ 4 1 1 336

3 3 21 1 1 Ñ Ñ Ñ 1 Ñ 314

Ñ 1 1 2 Ñ 148 1 22 9 3 1 Ñ 129 1 1 Ñ 1 1 1 18 Ñ

Ñ 2 Ñ 6 1 96 1 4 1 Ñ 1 Ñ 41 Ñ Ñ Ñ 1 Ñ Ñ 5 Ñ

1 Ñ Ñ 2 Ñ 37 6 32 Ñ 4 Ñ 1 32 Ñ 31 1 Ñ Ñ Ñ 8 Ñ

Ñ 1 Ñ 2 Ñ 26 1 94 Ñ 3 Ñ Ñ 28 Ñ 8 1 Ñ Ñ Ñ 2 1

1 2 Ñ

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(Continued on next page)

June 2005 Table 2.


639

(Continued) Vineyard I

Lycosidae Arctosa emertoni Gertsch Pardosa milvina (Hentz) Pardosa moesta Banks Pardosa xerampelina (Keyserling) Pirata aspirans Chamberlin Pirata minutus Emerton Pirata piraticus (Clerck) Schizocosa crassipalpata Roewer Trochosa ruricola De Geer Trochosa terricola Thorell Philodromidae Philodromus cespitum (Walckenaer) Philodromus rufus vibrans Dondale Tibellus maritimus (Menge) Tibellus oblongus (Walckenaer) Salticidae Habronattus decorus (Blackwall) Phidipus clarus Keyserling Talavera minuta (Banks) Tutelina similis (Banks) Tetragnathidae Pachygnatha autumnalis Marx in Keyserling Pachygnatha tristriata C. L. Koch Tetragnatha laborisa Hentz Theridiidae Achaearanea tabulata Levi Crustulina sticta (O. Pickard-Cambridge) Enoplognatha marmorata (Hentz) Neottiura bimaculata (Linnaeus) Steatoda americana (Emerton) Steatoda castanea (Clerck) Theridion differens Emerton Theridion murarium Emerton Thymoites unimaculatus (Emerton) Thomisidae Misumena vatia (Clerck) Ozyptila distans Dondale and Redner Xysticus Canadensis Gertsch Xysticus discursans Keyserling Xysticus ferox (Hentz) Xysticus luctans (C. L. Koch) Xysticus triguttatus Keyserling Immature Agelenidae Immature Araneidae Immature Clubionidae Immature Corinnidae Immature Dictynidae Immature Gnaphosidae Immature Linyphiidae Immature Lycosidae Immature Philodromidae Immature Salticidae Immature Tetragnatidae Immature Theridiidae Immature Thomisidae

Vineyard II

1998

1999

1998

1999

Ñ 8 1 1 Ñ Ñ Ñ 1 90 2

Ñ 8 5 1 Ñ 1 Ñ 4 37 Ñ

Ñ 1 10 2 Ñ 8 1 Ñ 232 Ñ

2 Ñ 5 4 1 5 2 Ñ 104 Ñ

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10 1 Ñ Ñ Ñ 2 Ñ 1 1

1 1 1 1 1 Ñ 1 2 Ñ Ñ Ñ 1 Ñ 50 137 Ñ 2 1 5 Ñ

Ñ Ñ Ñ 3 1 Ñ 1 9 1 Ñ 1 Ñ 1 7 203 Ñ Ñ Ñ Ñ 2

Ñ Ñ Ñ Ñ 4 Ñ Ñ 28 6 1 Ñ Ñ 1 83 104 8 1 2 33 2

Ñ Ñ Ñ Ñ 2 2 Ñ 41 4 1 2 Ñ Ñ 16 195 9 Ñ 2 6 1

Species are arranged alphabetically by family.

cies by sample matrix. This means the overall community composition is similar across years and between vineyards. Phenological patterns are depicted for the most commonly collected species (these account for 65.3% of the total number of spiders collected; Fig. 2). Males and females of T. formicum were collected in virtually every month of the study, with irregular peaks in male activity (Fig. 2A). T. ruricola was most frequently

found in pitfall traps in the spring and early summer (Fig. 2B), although some females continued to be collected into late summer. The linyphiid E. atra exhibited the same patterns of activity as shown for T. formicum, because males peaked in activity in various months, and patterns in activity were not consistent between years (Fig. 2C). H. plumosus, however, did show a consistent pattern between years, because this species had the highest captures of males in July

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For clarity and brevity, information on shared species and phenological patterns by foraging guild are presented for samples pooled over 2-wk periods (i.e., eight samples). In general, there were typically between 10 and 20 species collected in each 2-wk sample period for both vineyards (diagonal line; Table 3). The collection of spiders with the fewest species (six) occurred on 18 August 1999 in vineyard I (Table 3B), and the most species were collected in early June in 1999 (both vineyards; Table 3B, D) and early June in 1998 for vineyard II (Table 3C). In 1998, in vineyard I, 20 species were recorded on 1 and 15 July (Table 3A). When considering the total number of species collected in two sample dates (upper triangle, Table 3), the data were variable, ranging from a low of 12 species (vineyard I 1999, Table 3B) to a high of 35 species, collected in both 9 June and 1 September samples in vineyard I in 1999 (Table 3B). The percentage of species shared between sample periods was generally low, with only three cases of ⱖ50% of the species shared between sample dates, and in two of these cases, these were shared between adjacent sample periods (19 July to 12 August 1998; vineyard I; 8 Ð22 July 1999, vineyard II; Table 3A, D). In most cases, adjacent sample periods shared more species in common than did sample periods further away in time (Table 3), which indicated high species turnover in the vineyards. The most distant sample periods for all vineyards and years ranged from 28.6 to 31.8% in shared species. When separated by foraging guild (web-builders versus hunters), the data show that, during all sample periods, both hunting species and web-building species were present in the vineyards (Fig. 3). In all cases, more species of web-builders were collected than were hunting spiders, and hunting spider species richness always decreased toward the end of the season (Fig. 3). Web-building spiders were also numerically dominant, with the exception of three sample periods in 1998 (4 June to 2 July) in vineyard II (Fig. 3). Discussion

Fig. 1. Rarefaction curves for adult spiders collected in two vineyards in southern Quebec. The expected number of species, E(s), is plotted against subsamples (number of individuals); error bars are ⫾SD. (A) Vineyard I, by collection year (1998 and 1999). (B) Vineyard II by collection year. (C) Vineyards plotted separately, with collection years pooled.

for 1998 and 1999 (Fig. 2D). E. blaesa Crosby and Bishop was collected in similar frequency through much of 1998, but males and females peaked in activity in spring (MayÐJune) in 1999 (Fig. 2E). Of the remaining species collected, only Agelenopsis potteri (Blackwall) and Pardosa moesta Banks exhibited meaningful phenological patterns. A. potteri was never collected in pitfall traps until the Þrst week of August, whereas P. moesta was only present until mid-June.

A diverse assemblage of ground-dwelling spiders was collected in two vineyards from southern Quebec over 2 yr of collection. Because ⬇600 species of spiders are known from the province of Quebec (Paquin and Dupe´ rre´ 2003), these vineyards harbor ⬇16% of the spiders in Quebec, and this number is an underestimate because our sampling protocol did not focus on arboreal species. Even though our two vineyards differed from each other in some important ways (i.e., soil type, proximity to stream, differences in adjacent habitats), the spider fauna was largely unaffected by these factors because we detected few differences in overall community composition or diversity between the vineyards. This is in contrast to work by Costello and Daane (1995), because they detected a high degree of dissimilarity between vineyards in a study in San Joaquin Valley, CA. However, our results do support other Þndings from Quebec vineyards, because Goulet et al.(2004) found few

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641

Fig. 2. Total number of adult males and females spider collected by sample date. Collections are from pitfall trap data, placed in two vineyards (pooled). (A) T. formicum. (B) T. ruricola. (C) E. atra. (D) H. plumosus. (E) E. blaesa.

coarse differences in ground beetle diversity between the two vineyards. The similarity in the spider assemblages between vineyards may indicate these agroecosystems harbor a characteristic ground dwelling spider fauna independent of surrounding habitats and independent of variations in abiotic factors such as soil type.

The same conclusion cannot, however, be drawn from some species-speciÞc patterns, as was also the case with ground beetles (Goulet et al. 2004). In contrast to the aforementioned argument, these differences can probably be explained by the landscape context of the vineyards. For example, E. atra and T. formicum were found to be more commonly col-

642 Table 3.


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Shared species by sample period (end date of 2 wk of pooled pitfall trap data shown) separated by year and vineyard

20-May 03-Jun 17-Jun 01-Jul 15-Jul 29-Jul 12-Aug 26-Aug

20-May 16 25.0% 27.3% 24.1% 26.7% 24.0% 27.8% 31.6%

03-Jun 20 9 40.0% 20.8% 20.8% 20.0% 25.0% 28.6%

17-Jun 22 15 12 23.1% 23.1% 17.4% 21.1% 31.3%

(A) 1998 Vineyard I 01-Jul 29 24 26 20 37.9% 25.0% 19.2% 31.8%

15-Jul 30 24 26 29 20 40.0% 29.2% 38.1%

29-Jul 25 20 23 28 25 15 52.9% 33.3%

12-Aug 18 16 19 26 24 17 11 42.9%

26-Aug 19 14 16 22 21 18 14 9

26-May 09-Jun 21-Jun 07-Jul 21-Jul 04-Aug 18-Aug 01-Sep

26-May 11 23.3% 22.7% 25.0% 47.1% 25.0% 30.8% 28.6%

09-Jun 30 26 31.3% 20.7% 25.0% 16.7% 14.3% 20.0%

21-Jun 22 32 16 31.6% 30.4% 25.0% 15.8% 18.5%

(B) 1999 Vineyard I 07-Jul 16 29 19 9 35.3% 50.0% 25.0% 25.0%

21-Jul 17 32 23 17 14 46.7% 25.0% 42.9%

04-Aug 16 30 20 12 15 9 25.0% 31.6%

18-Aug 13 28 19 12 16 12 6 22.2%

01-Sep 21 35 27 20 21 19 18 16

21-May 04-Jun 18-Jun 02-Jul 16-Jul 30-Jul 13-Aug 27-Aug

21-May 13 36.4% 36.4% 33.3% 26.3% 38.9% 35.0% 31.8%

04-Jun 22 17 36.0% 33.3% 27.3% 26.1% 29.2% 32.0%

18-Jun 22 25 17 47.4% 27.3% 38.1% 29.2% 32.0%

(C) 1998 Vineyard II 02-Jul 18 24 19 11 29.4% 43.8% 38.9% 42.1%

16-Jul 19 22 22 17 11 35.3% 38.9% 22.7%

30-Jul 18 23 21 16 17 12 44.4% 47.4%

13-Aug 20 24 24 18 18 18 14 36.4%

27-Aug 22 25 25 19 22 19 22 16

27-May 10-Jun 22-Jun 08-Jul 22-Jul 05-Aug 19-Aug 02-Sep

27-May 18 22.2% 26.9% 28.6% 34.8% 17.4% 22.7% 29.2%

10-Jun 36 26 32.3% 29.6% 25.8% 25.9% 16.7% 25.8%

22-Jun 26 31 15 41.2% 33.3% 26.3% 20.0% 40.0%

(D) 1999 Vineyard II 08-Jul 21 27 17 9 57.1% 38.5% 28.6% 37.5%

22-Jul 23 31 21 14 13 29.4% 22.2% 36.8%

05-Aug 23 27 19 13 17 9 28.6% 29.4%

19-Aug 22 30 20 14 18 14 9 46.7%

02-Sep 24 31 20 16 19 17 15 13

Thirteen pitfalls traps were placed in vineyard I, and 24 pitfall traps were placed in vineyard II. Diagonal depicts species richness for each sample date; upper right triangle data are the total no. of species collected in both sample periods; lower left triangle data are the percentage of shared species by sample periods.

lected in vineyard I (Table 1). These species are both known from a variety of agroecosystems (e.g., Culin and Yeargan 1983, Bishop and Riechert 1990, Young and Edwards 1990, Lemke and Poehling 2002), and they can be considered “agrobiont” species (Samu and Szinenta´r 2002). Agrobiont spiders are known for their ability to rapidly colonize agroecosystems. E. atra, in fact, is known as an effective aerial disperser (Thomas et al. 1990). We can speculate that the proximity of a large fallow Þeld near vineyard I, and the proximity of an apple orchard, may provide a diverse array of suitable habitats for these agrobiont species, allowing larger populations compared with vineyard II. The adjacent apple orchard may be of additional signiÞcance for T. formicum, a species whose natural habitat is leaf litter (Kaston 1948). Apple orchards will provide a larger input of leaf litter than vineyards alone, and therefore, large populations of this agrobiont species may partially be explained by the adjacent orchard, and vineyard II, without as diverse an array of adjacent habitats, was unable to support as large pop-

ulations of T. formicum. Landscape heterogeneity may therefore play an important role for certain natural enemy species occurring in vineyards, a Þnding consistent with some biological control literature (e.g., Thies and Tscharntke 1999, Elliot et al. 2002). The only notable difference in spider diversity in our study system was the lower expected species richness in 1998 compared with 1999 in vineyard II (Fig. 2B). This difference is somewhat puzzling, especially given the lack of any general differences in the overall fauna between sites and years. Spider assemblages in vineyards are known to vary from year to year (Costello and Daane 1995), and larger climatic factors are likely driving the year-to-year difference in diversity. Additionally, species that require ⬎1 yr to complete development (e.g., Dondale 1977, Buddle 2000) will also be under- or over-represented in particular years, depending on the maturation of active adults that may be subsequently collected by pitfall traps.

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Fig. 3. Number of individuals (line graphs) and number of species (bar graphs) of web-building spiders and hunting spiders collected by pitfall traps placed in two vineyards over 2 collection yr. Date represents the end date for 2-wk (pooled) sample periods.

The wolf spider T. ruricola was common within our study vineyards of southern Quebec; this species was second only to T. formicum in its overall catch rate. T. ruricola had been introduced from the Palearctic and also occurs in Bermuda (Platnick 1991). It was found for the Þrst time in Canada in 1994 (Lalonge´ et al. 1997). Lalonge´ et al. (1997) found it to have displaced the native Trochosa terricola Thorell in cultivated cruciferous Þelds ⬍70 km away from the vineyards. Our study also indicates that T. ruricola is displacing T. terricola from vineyards, because the latter species was only collected twice over the 2 collection yr (Table 2). The phenology of T. ruricola was somewhat variable, but the species generally occurred most frequently from May to July, and because male and female activity corresponded during this time period, this is likely when mating occurs. Females were active for longer, a situation recorded for other wolf spiders (e.g., Dondale 1977, Workman 1978, Buddle 2000). Female wolf spiders survive longer than males and may continue to produce egg sacs throughout the summer months (Buddle 2000). The phenological patterns observed for many of the other more commonly collected linyphiid species

were highly variable. This variability is consistent with the observations of Draney and Crossley (1999). They show there is a link between linyphiid phenology and habitat disturbance. Highly disturbed areas such as agricultural Þelds seem to be characterized by a predominance of multivoltine species. This phenological ßexibility may allow the spiders to have mature individuals available for reproduction whenever conditions are suitable. The treatise of Samu and Szinenta´r (2002) on “agrobiont” spiders also supports this claim, because they depict many linyphiids in agroecosystems in Hungary as probably multivoltine. Selection for these life history traits in vineyards could have been achieved through disturbances such as earthingup, pesticides (insecticide use was stopped 1 yr before this experiment), and other agricultural activities such as grape picking and vine pruning. Samu and Szineta´r (2002) also suggest spider life cycles in agroecosystems are synchronized with the crop-growing season. Although vines are a perennial crop, they are cut down in the fall every year in Quebec, and so the arboreal spider fauna would have to recolonize the vines every year. The ground-dwelling spiders, however, may be less dependent on the crop growth, and so the best

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strategy for vineyard ground spiders is probably to have phenological plasticity to be available for reproduction and high activity period whenever the system is favorable. Among the less commonly collected species, we documented P. moesta to be most frequently collected in late May and early June. This species has previously been observed to peak in mid-May and early June in a deciduous forest in central Alberta (Buddle 2000), and Pickavance (2001) depicts a peak period of activity in July in Newfoundland. The delay in Newfoundland is likely caused by cooler climate conditions compared with continental Canada. In all three locations, the average daily temperature at the peak occurrence is between 10 to14⬚C. This temperature is reached in July in Newfoundland but May to June in Iberville (Quebec) and Edmonton (Alberta) (Environment Canada 2004). The other species showing a speciÞc phenological pattern is A. potteri. Males and females of this funnel-web spider were Þrst collected during the beginning of August, corresponding to the egg laying period (late summer and fall) (Kaston 1948). Assemblages of spiders are probably more important in limiting prey densities than are individual species (e.g., Riechert and Bishop 1990, Wise 1993, Riechert and Lawrence 1997), in part, because of an individual generalist predator speciesÕ inability to track pest outbreaks in a density dependent fashion (Riechert and Lockley 1984, Symondson et al. 2002). This means that multiple species must be present, and predatory species would need to compliment each other in terms of, for example, temporal segregation and foraging mode. The temporal segregation of spider species in our vineyards suggest high species turnover over the growing season (Table 3; Fig. 3). This is documented for both raw species richness (Table 3) and when considering the temporal patterns of catch rates and species richness of two distinct foraging guilds (i.e., web-builders and hunters; Fig. 3). In general, adjacent sample periods shared more species in common than sampling periods further away in time, and overall, shared species richness was almost always ⬍50%. This supports the claim that the spider assemblage present in the vineyards is constantly changing. Additionally, spiders with different foraging modes are always present in the vineyards, and potential prey items will be exposed to different types of predation from spiders throughout the season. Although we do not present data on phytophagous insects in the vineyards, we can hypothesize that the temporal segregation of spider species and the consistent presence of both hunters and web-building species will provide background control of pest species in the vineyards. In conclusion, our study shows that ground-dwelling spiders in vineyards of north-eastern North America are abundant and diverse and likely to form an important natural enemy assemblage to the diverse assemblage of pests occurring in this agroecosystem. Any pest management strategies in vineyards must therefore consider potential effects on spiders. Although we detected few gross differences in the fauna between the two vineyards, some species-speciÞc pat-

Vol. 34, no. 3

terns do suggest landscape diversity, and heterogeneity may play a role in maintaining high populations of certain species within the vineyards. Future research should be directed at better understanding the larger landscape context, so we can best preserve and maintain natural enemies within agroecosystems.

Acknowledgments The authors thank C.-H. de Coussergues, the late V. Dietrich, and C. Jooss, the proprietors of the two vineyards. We also thank J. Bellemare for servicing the numerous traps over the 2-yr period, J. Gill, L. Bartel, and C. Boudreault for sorting the samples, C. Dondale and M. Larrive´ e for conÞrming and assisting with species determinations, and McGillÕs insect ecology laboratory for discussions and insights. This project was Þnanced by Agriculture and AgriFood Canada MII Project 97-5735 and was partially Þnanced by the National Science and Engineering Research Council of Canada (Discovery Grant to CMB).

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