Seasonal and Diurnal Dynamics of Spiders (Araneae) in ... - BioOne

COMMUNITY AND ECOSYSTEM ECOLOGY

Seasonal and Diurnal Dynamics of Spiders (Araneae) in West Virginia Orchards and the Effect of Orchard Management on Spider Communities M. W. BROWN,1 J. J. SCHMITT,2

AND

BARBARA J. ABRAHAM3

USDAÐARS, Appalachian Fruit Research Station, 45 Wiltshire Road, Kearneysville, WV 25430

Environ. Entomol. 32(4): 830Ð839 (2003)

ABSTRACT Four West Virginia apple orchards under different management (unmanaged; horticultural management only; horticultural management with apple, peach, and cherry trees interplanted; and standard commercial management) were sampled for spider abundance. Sampling was done with limb jarring at four times during the season; samples were taken hourly over a 24-h period. A total of 1,926 spiders from 15 families was collected, and 44% of all spiders were Salticidae. More spiders were collected in August (37%) than earlier months, but the highest diversity of spider families was in July. Older, unsprayed apple trees had the greatest diversity of spiders. The family Oxyopidae was most abundant in the commercially managed orchard. Spiders in the families Anyphaenidae, Philodromidae, and Thomisidae were signiÞcantly more abundant during night samples than during the day. Philodromids were also signiÞcantly more abundant on peach and cherry trees than on apple, possibly being attracted to extraßoral nectaries. Comparisons with other published data sets found that regional differences were more important determinants of spider community structure in apple than insecticide use. Northwest European, sprayed Quebec, and sprayed Washington apple orchards were found to be dominated by web-building spiders; the other North American and Israeli orchards were dominated by hunting spiders. Abundance and diversity of the spider community in orchards suggests that spiders could be major contributors to biological control of many insect pests. KEY WORDS biological control, Araneae, Salticidae, Oxyopes salticus, insecticide effects

SPIDERS ARE A MAJOR COMPONENT of the predatory arthropod trophic level in many ecosystems, but there has been little documentation of their impact on herbivore populations or of their general ecology (Wise 1993). Many studies have documented the composition of the spider community on apples in North America (Dondale 1956, Specht and Dondale 1960, Legner and Oatman 1964, Dondale et al. 1979, McCaffrey and Horsburgh 1980, Bostanian et al. 1984, Wisniewska and Prokopy 1997), Europe (Chant 1956, Olszak et al. 1992, Marc and Canard 1997, Bogya et al. 1999), Middle East (Mansour et al. 1980a), Japan (Hukusima 1961), and Australia (Dondale 1966). Recent research has investigated the overwintering ecology of spiders in orchards (Peka´r 1999a, Horton et al. 2001). A number of studies have compared the effect of insecticides on spider communities in apple orchards (Dondale et al. 1979, Mansour et al. 1981, Wisniewska and Prokopy 1997, Peka´r 1999b, Epstein et al. 2000) and also the effects of other levels of management such as differing intensities of integrated E-mail: [email protected]. USDAÐARS, 5601 Sunnyside Ave., Beltsville, MD 20705Ð5102. Department of Biological Sciences, Hampton University, Hampton, VA 23668. 1 2 3

pest management (IPM) (Wisniewska and Prokopy 1997, Bogya and Marko´ 1999, Miliczky et al. 2000) and the use of ßowering plants (Wyss et al. 1995, Samu et al. 1997, Peka´r 1999a). These studies showed that the spider communities were negatively affected by increased levels of management and positively affected by increased habitat diversity. Spiders have been shown to be able to reduce pest populations and damage in garden plots (Riechert and Bishop 1990) and on individual apple trees (Mansour et al. 1980b). Bogya and Mols (1996) analyzed the role of spiders in the complex food webs of orchards through a literature review of recent studies on spider behavior. The spiders found in orchards are capable of feeding on just about any arthropod prey, but particularly Homoptera and Lepidoptera (Hukusima and Kondo 1962, Bogya and Mols 1996, Marc and Canard 1997). Spiders have also been shown to be predators of spider mites (Tetranychidae) in orchards, potentially making valuable contributions to their control (Putman 1967). Ecosystems with a high diversity of herbivores, such as apple orchards (Brown and Schmitt 2001), require a diverse community of spiders to provide effective community regulation (Nyffeler et al. 1994, Provencher and Riechert 1994, Bogya and Mols 1996).

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BROWN ET AL.: SEASONAL AND DIURNAL DYNAMICS OF SPIDERS

This study was conducted to document the composition of the spider community in orchards under a range of management intensity from neglected to commercially managed. Data on the temporal dynamics and the effects of management intensity on insects and mites from this data set have been published (Brown and Schmitt 2001). Another objective of the study was to examine the seasonal and diurnal dynamics of spiders in the orchard to provide information for development of appropriate sampling methodology for the different groups of spiders found in orchards. Also, an examination of published data sets on the composition of spider communities in apple orchards was done to compare regional versus management inßuences as determinants of community composition. This study will help to provide some of the information needed on spider ecology with which to develop programs to increase biological control by spiders in orchards.

Materials and Methods Four orchards at the Appalachian Fruit Research Station, Kearneysville, WV, were sampled four times during 1991. Orchard A, 0.32 ha, was 8 yr old and had been completely unmanaged for 6 yr. This orchard received no pesticides and had not been mowed since 1985. It had high plant diversity, with numerous wild trees, vines, and herbaceous plants intermixed with the apple trees. Orchard C, 0.13 ha, was also 8 yr old but was regularly mowed, pruned, and had the herbicide paraquat applied in the tree rows as the only pesticide. Within orchards A and C, there were equal numbers of the apple cultivars “Delicious,” “Golden Delicious,” “Empire,” “York Imperial,” and “Stayman.” Orchard D, 0.22 ha, was 3 yr old and had the same horticultural management and herbicide use as orchard C. Orchard D had the apple cultivars “Prima” (29 trees) and “Liberty” (27 trees), peach cultivars “Summerglo” (29 trees) and “Harmony” (27 trees), and sour cherry cultivar “Montmorency” (14 trees). Apple and peach (or cherry) were planted alternately within and between rows. The only insect pest management activity used in orchard D was mating disruption for lesser peachtree borer, Synanthedon pictipes (Grote and Robinson) (Lepidoptera: Sessiidae), with one pheromone dispenser applied per tree on 1 June. Orchard M, 0.45 ha, was 13 yr old and was managed with conventional orchard production practices. This orchard was planted with the apple cultivar “Granny Smith.” Insecticide applications consisted of dormant oil on 25 March; chlorpyriphos on 6 April, 5 June, and 8 August; methomyl with azinphosmethyl on 8 May; formetanate hydrochloride on 20 June; methyl parathion on 10 July; and methyl parathion with propargite on 24 July; all were applied at recommended rates (Virginia, West Virginia, and Maryland Cooperative Extension Services 1991). Except for Orchard A, all orchards had a herbicide strip under the trees maintained with paraquat as needed throughout the season.

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Sampling was done at hourly intervals over a 24-h period, four times during the year. Sampling was within 5 d of a full moon when the forecast was for clear skies (to reduce the need for artiÞcial light during nocturnal sampling). Sample periods for orchards A, C, and D were 29 Ð30 May, 25Ð26 June, 31 JulyÐ1 August, and 26 Ð27 August. Sampling began at 0900 hours and continued to 0800 hours EDT the following day. Every hour, two apple trees in orchard A, two apple trees in orchard C, and two apple and two peach trees in orchard D were sampled. Every other hour, one cherry tree was also sampled from orchard D. In the May sample, 2 h of sampling (2400 and 0300 hours) were missed because of the length of time required to obtain samples during the night (the cherry tree selected for sampling at 0300 hours was sampled on time). An additional apple tree was not sampled in orchard D at 2200 in the May sample. Trees were randomly selected before beginning the sample period, and no tree was sampled twice during one sample period. Because of time limitations and distance between orchards, sampling in orchard M was done on 31 MayÐ1 June, 24 Ð25 June, 27Ð28 July, and 24 Ð25 August. Sample intensity was also less in orchard M, with 10 trees sampled at 1300 and 2000 hours on the Þrst day and at 0100 hours the following day. As with the other orchards, trees were randomly selected before going to the Þeld, and no tree was sampled twice during the same sample period. Sampling was by limb jarring, with three branches per tree struck three times with a rubber hose over a collection funnel. The funnel was made of clear plastic and had a 1-m2 collection opening. The funnel was held with a handle from a sweep net that allowed one person to hold the funnel while striking the branch. A 200-ml jar containing 50 Ð100 ml 70% alcohol was attached to the bottom of the funnel. The sample with all specimens from the three branches per tree was carried to a central location where the jar was unscrewed from the funnel, covered, labeled, and replaced with a new sample jar. Before the jar was removed from the funnel, all arthropods on the inside surface of the funnel were dislodged into the collecting jar. Leaves and fruit that fell into the funnel were removed after rinsing arthropods that were on the plant material into the jar. Samples were taken to the laboratory and stored in 70% ethyl alcohol for identiÞcation. IdentiÞcations were made conservatively, especially with regard to immatures, if there was any doubt as to an individual belonging to another species, it was not listed as a separate species. Representative specimens from identiÞed species are in the arthropod collection at the Appalachian Fruit Research Station, Kearneysville, WV. Diversity was estimated with ShannonÕs index of diversity using the formulae of Hutcheson (1970), which also provided an estimate of the variance of the diversity estimate for statistical comparison using 95% conÞdence intervals. Community evenness was calculated with the evenness formulation: (Number of species ⫺ 1)/natural log(number of individuals) (Margalef 1958). Differences in evenness were not

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ENVIRONMENTAL ENTOMOLOGY

statistically tested because of a lack of an unbiased estimate of variation. Diel periodicity was tested for the four most abundant families with the Rayleigh test (Batschelet 1981), a circular statistic to test for randomness in the distribution of angular data with a potential distribution of 360⬚. In this case, hour (0 Ð 2400 hours) was transformed into radians for the analysis. Data from orchard M was not included in the diel analysis because only three time intervals were sampled. ␹2 analyses were used to test for orchard and month effects on the abundance of spiders by taxonomic family. A literature survey was done to examine regional trends in spider community structure in apple orchards and to test for a generalized effect of insecticide use. Data sets were used for comparison only if they had family level identiÞcations for most spiders collected and if spider sampling was done with limb jarring. For comparison with these published data sets, we omitted all records of spiders from peach and cherry trees from the current study. Renkonen similarity (Wolda 1981) was calculated between sprayed and unsprayed orchards [for the purposes of this comparison, the organic orchards in Miliczky et al. (2000) were considered unsprayed] from the same study, and between all pairwise comparisons among unsprayed orchards in Europe, sprayed orchards in Europe, unsprayed orchards in North America, and sprayed orchards in North America. Principal component analysis (SAS Institute 1996) was also done on all 19 data sets using abundances of each spider family as the independent variables to compare spider communities. Results Species Composition. A total of 1,926 spiders, belonging to 15 families, was collected with limb jarring sampling of fruit trees (Table 1). Eighty-Þve species were identiÞed to at least the genus level. The vast majority of spiders were hunting spiders (86%) compared with web-building spiders (14%) (Table 2). The most abundant families collected were Salticidae (44%), Anyphaenidae (15%), and Philodromidae (10%), with Theridiidae (7%) being the most abundant web-building family (Table 2). The most abundant spiders were Eris militaris (Hentz) (Salticidae) (12% of all spiders), Anyphaena sp. (Anyphaenidae) (11%), and Philodromus sp. (Philodromidae) (5%) (Table 1). The majority of spiders collected were immatures (89%). The mean number of spiders collected per tree (Table 1) was similar (1.97Ð2.57) across all orchards, except for the commercially managed orchard (0.68 spiders per tree). Spider diversity at the family level ranged from 1.60 to 1.84 (ShannonÕs index) among the four orchards and three fruit tree species sampled (Table 1). Family diversity was signiÞcantly higher (P ⬍ 0.05, 95% conÞdence intervals) in the two older, unsprayed apple orchards, A and C, and on cherry than the younger and commercially managed apple orchards and on peach. Differences in evenness of

Vol. 32, no. 4

family abundance among orchards followed the same pattern as for diversity (Table 1). The distribution of oxyopid abundance was signiÞcantly different from that of all other families (P ⬍ 0.001, ␹2 test) with over 25% of the oxyopids found in the commercially managed orchard, whereas for no other family were there ⬎7.8% of the individuals in this orchard. Further ␹2 comparisons were made excluding oxyopids because of their large difference from the general pattern of distribution. Salticids, anyphaenids, philodromids, and thomisids were also distributed signiÞcantly differently from the other families of spiders (P ⬍ 0.01, ␹2 test; Table 2). Salticids were less abundant than expected in the commercially managed orchard. Anyphaenids were more abundant than expected in the two older, unsprayed apple orchards. Philodromids were more abundant than expected on the peach and cherry trees. Thomisids were more abundant on the younger apple trees in orchard D than expected. Diversity of the spider community was signiÞcantly greater during July than any other month (P ⬍ 0.05, 95% conÞdence interval) even though spiders were generally more abundant during August (Table 3). Evenness of distribution of family abundance was greatest in May and decreased through the year (Table 3). Abundance of most families followed the same trend as the overall spider abundance, increasing abundance from May to August. Theridiids had a signiÞcantly different seasonal abundance pattern with decreasing abundance from May to August (P ⬍ 0.01, ␹2 test). Araneids had a signiÞcantly higher seasonal abundance in June, and oxyopids had signiÞcantly higher abundance in July, with none being collected in May and June (P ⬍ 0.01, ␹2 test; Table 3). Only three spider families had a signiÞcantly nonrandom pattern of abundance during the day (P ⬍ 0.05, Rayleigh test). Anyphaenid abundance peaked at 0100 ⫾ 3 h (mean ⫾ SE). Philodromid abundance peaked at 2300 ⫾ 5 h. Thomisid abundance peaked at 2400 ⫾ 6 h. Comparisons with Published Data Sets. Ten data sets from sprayed apple orchards and 11 data sets from unsprayed apple orchards were found to be comparable with the current study (Table 4). Of these data sets, nine had data from both sprayed and unsprayed orchards. Among the sprayed orchards, the two data sets from Europe, the two from Quebec, Canada, and the one from Washington were dominated by webbuilding spiders, and the other data sets from North America and Israel were dominated by hunting spiders (Table 4). Among unsprayed orchards, only the four data sets from Europe were dominated by webbuilding spiders, and all orchards from North America and Israel were dominated by hunting spiders (Table 4). Similarity in spider family abundances between orchards was signiÞcantly higher between sprayed and unsprayed orchards from the same study than between orchards from other studies (Table 5). Between orchard similarity within Europe or North America for unsprayed orchards averaged from 0.57 to 0.60, with no signiÞcant differences (Table 5). The lowest sim-

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Table 1. Spider species collected over all four sample periods by orchard and tree species in West Virginia research orchards, 1991, including family level diversity and evenness Orcharda

Salticidae Maevia inclemens (Walckenaer) Maevia sp. Tutelina elegans (Hentz) Hentzia mitrata (Hentz) Hentzia sp. Thiodina sylvana (Hentz) Thiodina sp. 1 Thiodina sp. 2 Phidippus audax (Hentz) Phidippus putnami (Peckham and Peckham) Phidippus princeps (Peckham and Peckham) Phidippus clarus Keyserling Phidippus sp. 1 Phidippus sp. 2 Phidippus sp. 3 Phidippus sp. 4 Phidippus sp. 5 Eris militaris (Hentz) Eris aurantia (Lucas) Eris sp. 1 Eris sp. 2 Pelegrina galathea (Walckenaer) Pelegrina proterva (Walckenaer) Metaphidippus sp. 1 Metaphidippus sp. 2 UnidentiÞed spp. Total Salticidae Anyphaenidae Anyphaena pectorosa L. Koch Anyphaena spp. Wulfila saltabundus (Hentz) Wulfila sp. Hibana gracilis (Hentz) Total Anyphaenidae Philodromidae Philodromus keyserlingi Marx Philodromus vulgaris (Hentz) Philodromus minutus Banks Philodromus placidus Banks Philodromus marxi Keyserling Philodromus sp. 1 Philodromus spp. UnidentiÞed Philodromidae Total Philodromidae Thomisidae Xysticus ferox (Hentz) Xysticus funestus Keyserling Xysticus sp. 1 Xysticus sp. 2 Xysticus sp. 3 Xysticus spp. Misumenops asperatus (Hentz) Misumenops oblongus (Keyserling) Misumenops sp. Misumena vatia (Clerck) Tmarus angulatus (Walckenaer) Misumenoides formosipes (Walckenaer) Misumenoides sp. Synema parvulum (Hentz) Synema sp. UnidentiÞed Thomisidae Total Thomisidae Theridiidae Theridion albidum Banks Theridion frondeum Hentz Theridion glaucescens Becker Theridion ciiematos Gertsch and Archer Theridion spp.

A

C

0 1 15 7 20 1 2 0 1 0 0 1 0 1 6 18 11 58 16 0 0 18 1 6 1 37 221

D

M

Apple

Peach

Cherry

0 0 14 2 11 0 1 0 0 1 0 1 1 0 10 22 8 51 15 1 1 1 0 4 0 28 172

0 0 8 1 5 0 0 1 2 3 2 0 7 1 7 23 6 54 11 2 1 10 0 14 1 28 187

1 2 8 9 14 1 1 2 1 2 0 0 6 5 8 25 3 51 41 0 0 7 0 3 0 23 213

0 0 3 0 1 0 0 0 1 0 0 1 1 0 2 7 2 9 3 1 0 1 0 2 0 9 43

0 0 0 1 2 0 0 1 1 0 0 0 0 0 2 1 0 2 0 0 1 1 0 0 0 4 16

6 48 14 16 0 84

14 70 0 1 0 85

4 36 1 9 0 50

11 33 0 4 1 49

1 16 1 0 0 18

0 1 0 1 0 2

0 1 1 1 3 15 8 1 30

3 2 2 0 5 29 4 0 45

1 0 0 0 5 13 7 0 26

2 1 3 2 7 30 16 0 61

0 1 1 0 4 9 6 0 21

0 0 0 0 1 1 4 0 6

2 3 0 0 3 5 9 0 6 2 3 1 1 0 0 0 35

1 0 0 0 6 7 17 1 4 0 1 2 2 0 1 0 42

0 5 1 0 1 5 17 0 14 1 0 0 3 0 0 0 47

2 2 0 1 6 5 9 3 5 1 1 0 1 0 0 2 38

0 2 0 0 1 2 6 0 2 0 1 0 0 1 0 0 15

1 0 0 1 1 2 4 0 2 0 0 1 3 0 0 0 15

11 0 1 0 13

4 0 1 0 14

3 0 1 0 8

6 0 2 0 10

4 0 1 0 1

1 1 0 1 4

834 Table 1.


Vol. 32, no. 4

Continued Orcharda A

Thymoites unimaculatus (Emerton) Euryopis funebris (Hentz) Theridula spp. Dipoena nigra (Emerton) Dipoena buccalis Keyserling Dipoena sp. Achaearanea tepidariorum (C. L. Koch) UnidentiÞed Theridiidae Total Theridiidae Araneidae Acacesia hamata (Hentz) Araniella displicata (Hentz) Neoscona arabesca (Walckenaer) Verrucosa arenata (Walckenaer) Gea heptagon (Hentz) Cyclosa turbinate (Walckenaer) Cyclosa conica (Pallas) Metepeira labyrinthea (Hentz) Larinia directa (Hentz) Eustala sp. UnidentiÞed Araneidae Total Araneidae Oxyopidae Oxyopes salticus Hentz Oxyopes aglossus Chamberlin Oxyopes sp. Total Oxyopidae Uloboridae Octonoba sinensis (Simon) Dictynidae Dictyna foliacea (Hentz) Dictyna sp. Total Dictynidae Linyphiidae Frontinella communis (Hentz) Neriene radiata (Walckenaer) UnidentiÞed Linyphiidae Total Linyphiidae Pisauridae Pisaurina sp. Agelenidae UnidentiÞed Mimetidae Mimetus puritanus Chamberlin Micryphantidaeb Pelecopsis bishopi Kaston UnidentiÞed Micryphantidae Total Micryphantidae Clubionidae UnidentiÞed Clubionidae Diversity (ShannonÕs Index) Evenness Mean number of spiders per tree

D

C

Apple

Peach

Cherry

M

0 4 0 0 1 0 0 3 33

1 6 4 0 1 1 0 5 37

0 2 0 0 0 0 0 2 16

0 8 1 2 0 1 1 1 32

0 1 0 0 0 0 0 0 7

2 0 0 0 0 0 0 1 10

8 4 4 2 0 2 0 1 0 0 5 26

3 3 1 1 0 2 0 0 1 0 5 16

5 5 1 0 1 3 1 0 0 0 1 17

3 2 5 0 0 3 1 0 0 0 3 17

0 1 1 0 0 0 0 0 0 0 1 3

0 1 0 0 0 1 0 0 0 1 0 3

5 24 1 30

5 20 0 25

3 14 0 17

6 1 0 7

1 3 0 4

18 10 0 28

0

0

0

2

0

0

13 1 14

4 1 5

5 1 6

6 1 7

0 1 1

0 0 0

0 0 1 1

1 1 1 3

0 0 1 1

0 0 1 1

0 0 1 1

1 0 0 1

1

0

0

0

0

0

0

1

0

0

0

0

0

2

0

0

0

0

1 3 4

0 0 0

0 0 0

0 0 0

0 0 0

0 0 0

2 1.60b 1.69 1.97

8 1.63b 1.65 2.31

1 1.74a 2.11 2.40

0 1.67b 1.59 0.68

5 1.75a 1.94 2.57

10 1.84a 1.97 2.36

a Orchard abbreviations : A, unmanaged 8-year-old orchard; C, mowed, herbicide-treated and pruned 8-year old orchard; D, apple, peach, and cherry interplanted 3-year old orchard with same management as in C; and M, commercially managed 13-year-old orchard. b Considered subfamily Micryphantinae (Erigonidae) in the family Linyphiidae (Platnick 2002).

ilarity was among sprayed orchards in North America with only 0.42 average similarity. Geographical closeness did not seem to correspond with closer similarities between spider community compositions. The highest similarity between orchards from different studies was 0.73 between the sprayed orchards in Quebec (Dondale et al. 1979, Bostanian et al. 1984). The current study and the northern Virginia site (McCaffrey and Horsburgh 1980), located ⬇40 km apart,

were the next closest sites in proximity but had a similarity of only 0.59. The spider community in Washington (Miliczky et al. 2000) was more similar to the current study (0.70 for unsprayed orchards) than to Israel (Mansour et al. 1980a) (0.24 for unsprayed and 0.12 for sprayed) the only other data set from an arid environment. The position of each orchard in the two-dimensional space deÞned by the Þrst two principal com-

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Table 2. Percentage of total spiders collected by family, including only families with more than 20 individuals, by orchard, West Virginia, 1991 Percentage occurrence by orchard

Family (number of individuals)

A

C

Salticidae (852)a Anyphaenidae (288)a Philodromidae (189)a Thomisidae (192)a Theridiidae (135) Araneidae (82) Oxyopidae (111)a Dictynidae (33) Clubionidae (26) All others (18) Total (1926)

25.9 29.2 15.9 18.2 24.4 31.7 27.1 42.4 19.2 30.4 25.1

20.2 29.5 23.8 21.9 27.4 19.5 22.5 15.2 38.5 30.4 23.0

D Apple

Peach

Cherry

22.0 17.4 13.7 24.5 11.9 20.7 15.3 18.2 7.7 13.0 19.2

25.0 17.0 32.3 19.8 23.7 20.7 6.3 21.2 30.8 13.1 22.5

5.0 6.2 11.1 7.8 5.2 3.7 3.6 3.0 3.8 8.7 6.0

M 1.9 0.7 3.2 7.8 7.4 3.7 25.2 0.0 0.0 4.3 4.2

a Families that had a signiÞcantly different distribution among orchards and tree species than the mean distribution for all other spiders combined (␹2, P ⬍ 0.01).

ponents is shown in Fig. 1. The Þrst two principal components account for 44% of the total variation in spider family abundances. The Þrst principal component is deÞned by the difference in abundance between hunting and web-building spiders, with hunting spider abundance in the positive direction and webbuilding spiders in the negative direction. The second principal component is deÞned largely by differences among hunting spider family abundances. Greater abundance of thomisids, clubionids, and oxyopids are in the positive direction, and abundance of philodromids, anyphaenids, and salticids in the negative direction. The third principal component (data not shown) separated the Washington sprayed orchard (Miliczky et al. 2000) from the other data sets based on the dominance by linyphiids (79%), pooled with other web spiders in Table 4. All of the European orchards examined, the two sprayed Quebec orchards, and the sprayed Washington orchard were all clustered very closely together along the Þrst principal component axis, indicating the dominance of web-building spiders in those orchards. The effect of insecticide applications on spider communities from each study can be seen by comparing the capital (unsprayed) with the Table 3. Percent of individual spiders of each family (families with >10 individuals) by sample month, West Virginia, 1991 Family Salticidaea Anyphaenidaea Philodromidaea Thomisidae Theridiidaea Araneidaea Oxyopidaea Dictynidae Clubionidae All others Diversity Evenness Total no. spiders

May

June

July

August

12.7 13.6 1.7 11.3 40 15 0.0 2.9 3.9 36.4 1.56b 2.01 239

26.4 16.1 9.9 31.1 24 49 0.0 25.7 42.3 40.9 1.64b 1.81 434

21.4 26.9 38.7 27.7 20 19 66.3 25.7 19.2 9.1 1.81a 1.62 541

39.5 43.4 49.7 29.9 16 17 33.7 45.7 34.6 13.6 1.59b 1.54 712

a Families that had a signiÞcantly different distribution among months than the mean distribution for all other spiders combined (␹2, P ⬍ 0.01).

lowercase (sprayed) letters in Fig. 1. In each case, there was a shift in the position of the orchard in Fig. 1 because of insecticide use, but there was no consistent pattern in the direction of the shift. Most of the sprayed orchards exhibited a shift toward less dominance by hunting spiders, more negative on the Þrst principal component axis, as a result of spraying. The Israeli, Polish, and Massachusetts orchards, however, showed an opposite trend with more hunting spiders in the sprayed orchards. Discussion There is a large and diverse community of spiders in fruit orchards of West Virginia (Tables 1Ð3). Previous surveys have also shown a large, diverse community of spiders in fruit trees (Table 4). Although limb jarring sampling does not include the bark-dwelling, herbdwelling, or ground-dwelling spiders, it has been shown to be an effective sampling method for obtaining a representative sample of spiders in the apple canopy (McCaffrey et al. 1984). The abundance and diversity of the spider community in orchards should be expected to correspond with a high potential for controlling many pest species (Wise 1993, Nyffeler et al. 1994, Marc and Canard 1997). The hunting spiders that dominate the orchard ecosystem have been shown to prefer Lepidoptera and Homoptera food sources (Bogya and Mols 1996) but would probably accept any prey that are slightly smaller than the spider (Nyffeler et al. 1994). In peaches (Putman 1967), spiders have been shown to provide control of European red mites [Panonychus ulmi (Koch)] (Acari: Tetranychidae). Mansour et al. (1980b) demonstrated that an association of at least eight spider species, especially Cheiracanthium mildei Koch (Araneae: Clubionidae), reduced damage by Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae) on apple. Wyss et al. (1995) showed a signiÞcant reduction in rosy apple aphids, Dysaphis plantaginea (Passerini) (Homoptera: Aphididae), by Araniella sp. (Araneae: Araneidae) because of predation of fall migrants returning to apple.

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Table 4. Family composition (percentage) of spider communities from canopy of apple trees from North America, Europe, and the Middle East as collected by limb jarring Location (codea) Sprayed orchards WV, USA (a) VA, USA (b) MA, USA (c) WI, USA (d) Quebec, CA (e) WA, USA (f) Poland (g) England (h) Israel (i) Quebec, CA (j) Unsprayed orchards WV, USA (A) VA, USA (B) MA, USA (C) WI, USA (D) Quebec, CA (E) WA, USA (F) Poland (G) England (H) Israel (I) Switzerland (K) France (L)

Huntersb

Web-feedersb

Referencec

Salt

Anyph

Thom

Phil

Oxyop

Club

Pisa

Lyco

Ther

Aran

Dict

Other

0.20 0.26 0.41 0.10 0.13 0.04 0.01 0 0.10 0.05

0.02 0.05 0.10 0 0 0.01 0.01 0 0 0

0.19 0.16 0.03 0.03 0.07 0.05 0.07 0.03 0.16 0.03

0.07 0.17 0.25 0.55 0.13 0.02 0 0 0 0.21

0.35 0.05 0.01 0 0 0.03 0 0 0.04 0

0 0.03 0 0 0.01 0.01 0.04 0.05 0.57 0

0 0 0 0 0 0 0 0 0 0

0 0 0 0 0.01 0.01 0 0 0 0

0.12 0.06 0.11 0 0.14 0.03 0.26 0.66 0.01 0.18

0.04 0.02 0.05 0.19 0.29 0 0.29 0.14 0.12 0.36

0 0.15 0.01 0 0.03 0.01 0.08 0 0.01 0.01

0.01 0.05 0.04 0.13 0.22 0.79 0.25 0.12 0 0.17

This study McCaffrey et al. (1980) Wisniewska et al. (1997) Legner et al. (1964) Bostanian et al. (1984) Miliczky et al. (2000) Olszak et al. (1992) Chant (1956) Mansour et al. (1980a) Dondale et al. (1979)

0.45 0.27 0.21 0.32 0.42 0.46 0 0 0.12 0.01 0

0.17 0.07 0.13 0 0 0.01 0.01 0 0 0 0

0.10 0.11 0.02 0.01 0.06 0.06 0.06 0.03 0.17 0.02 0.01

0.08 0.24 0.31 0.45 0.10 0.05 0 0 0 0.10 0.17

0.06 0.02 0.01 0 0 0.09 0 0 0 0 0

0.01 0.03 0 0 0.01 0.02 0.04 0.05 0.40 0.01 0.04

0.01 0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0.01 0 0.01 0 0

0.07 0.15 0.22 0 0.19 0.07 0.41 0.61 0.02 0.30 0.19

0.05 0.03 0.06 0.20 0.16 0.01 0.23 0.08 0.28 0.54 0.37

0.02 0.07 0.03 0 0.01 0.01 0.09 0 0.01 0 0.13

0.04 0.02 0.02 0.02 0.05 0.22 0.16 0.23 0 0.04 0.09

This study McCaffrey et al. (1980) Wisniewska et al. (1997) Legner et al. (1964) Bostanian et al. (1984) Miliczky et al. (2000) Olszak et al. (1992) Chant (1956) Mansour et al. (1980a) Wyss et al. (1995) Marc et al. (1997)

a

Code refers to the letter symbol used in Fig. 1 to designate location of each orchard along the Þrst two principal components. Spider families: Salt, Salticidae; Anyph, Anyphaenidae; Thom, Thomisidae; Phil, Philodromidae; Oxyop, Oxyopidae; Club, Clubionidae; Pisa, Pisauridae; Lyco, Lycosidae; Ther, Theridiidae; Aran, Arancidae; Dict, Dictynidae; Other, all other families of web-feeding spiders. c All references listed only by senior author because of space constraints. b

Among the various studies published on composition of the spider community in North American orchards, a number of species were found in common with in this study (Table 1), and therefore, may be key species to be considered for biological control. A. displicata (Araneidae) has been the most geographically widespread species, being found from Virginia to Wisconsin and Quebec to Nova Scotia (Specht and Dondale 1960, Legner and Oatman 1964, Hagley 1974, Dondale et al. 1979, McCaffrey and Horsburgh 1980, Bostanian et al. 1984, Wisniewska and Prokopy 1997). Within the Salticidae, the most abundant family in North American orchards, Phidippus audax, has also been recorded in Massachusetts and Virginia (McCaffrey and Horsburgh 1980, Wisniewska and Prokopy 1997). The most abundant salticid in our data set, E. militaris, was also found, but only infrequently, in Table 5. Similarities among spider communities on apple by management type and geographic region using published data sets (see Table 4 for data set references) Comparison

N

Meana

Range

Sprayed vs. unsprayed, within studyb Unsprayed orchards, Europe Unsprayed orchards, North America Sprayed orchards, Europe Sprayed orchards, North America

10

0.74a

0.42Ð0.89

6 15 1 20

0.57b 0.60b 0.59 0.42c

0.38Ð0.71 0.40Ð0.78 0.19Ð0.73

a Means followed by the same letter within the column are not signiÞcantly different based on 95% conÞdence intervals. b Similarities between spider communities on sprayed and unsprayed apple orchards from the same study.

Washington (Miliczky et al. 2000). Oxyopes salticus, which we found to be especially abundant in the sprayed orchard (Table 1), has also been found in Massachusetts and Virginia (McCaffrey and Horsburgh 1980, Wisniewska and Prokopy 1997). Other species recorded from our orchards and other locations in North America, and which may be important species for biological control, are Misumenops asperatus (Thomisidae) (Specht and Dondale 1960, McCaffrey and Horsburgh 1980, Wisniewska and Prokopy 1997), Theridion albidum (Theridiidae) (Dondale 1956, McCaffrey and Horsburgh 1980), Wulfila saltabundus (Anyphaenidae) (Dondale 1956, McCaffrey and Horsburgh 1980), and Dictyna foliacea (Dictynidae) (Dondale 1956, McCaffrey and Horsburgh 1980). Three families of spiders were found to be more abundant during the night than during the day. Philodromids, thomisids, and anyphaenids are known to be nocturnal hunting spiders (Comstock 1912) and were all signiÞcantly more abundant during the night than the day. McCaffrey et al. (1984) also found that clubionids were more abundant at night in Virginia, but this family was uncommon in our sampling (Table 1). These results, with our previous work (Brown and Schmitt 2001), document the importance of sampling at all times during the day to collect data on the complete community of predatory arthropods and their ecosystem associations. One family of spiders, philodromids, was signiÞcantly more abundant on peach and cherry trees than on apple. A major difference between apple and the Prunus spp. is the presence of extraßoral nectaries on

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837

Fig. 1. Location of the spider community data sets from apples in the space deÞned by the Þrst two principal components (PC) using percentage of individuals in the spider community belonging to each family as the independent variables. Capital letters refer to unsprayed orchards and lowercase letters to sprayed orchards; letters refer to orchards listed in Table 4.

the leaves of the latter. These nectaries are attractive to a large number of beneÞcial and pest insects (Putman 1963, Bentley 1977). Some spiders have been found to feed on nectar secretions (Taylor and Foster 1996). Taylor and Foster (1996) noted that hunting spiders that are active at night, such as the philodromids in this study, were the types of species most often observed feeding on extraßoral nectar. Philodromids may have been responding to the presence of extraßoral nectar on peach and cherry trees, in which case they may contribute to the control of pests on these trees more than on trees without extraßoral nectar. Oxyopes aglossus was the most abundant oxyopid in this study but O.salticus was the most abundant oxyopid in the sprayed orchard. Oxyopes salticus has been shown to be resistant to insecticides in other systems (Young and Lockley 1985) and is an important predator of cotton ßeahopper, Pseudatomoscelis seriatus (Reuter) (Hemiptera: Miridae) in Texas (Nyffeler et al. 1992). Mansour et al. (1980a) found oxyopids only in his sprayed orchard in Israel, but Bogya et al. (2000) found no differences in abundance of Oxyopes heterophthalmus Latreille (Oxyopidae) between sprayed and unsprayed orchards in Hungary. Although oxyopid abundance did not differ with respect to insecticide use for the other data sets that compared sprayed and unsprayed orchards (Table 4), there does seem to be the potential for developing spiders resistant to insecticides for increasing biological control. O. salticus was observed feeding on European red mites in the laboratory (Brown and Schmitt, unpublished data), which also were more abundant in the sprayed orchard (Brown and Schmitt 2001), and may be able to contribute to mite biological control. There does not seem to be a generalized pattern of response by the spider community to the application of insecticides based on the principal component analysis (Fig. 1). This study and others (Legner and Oatman 1964, Bostanian et al. 1984, Peka´r 1999a, Miliczky et al. 2000) showed a reduction in the proportion of hunting spiders as a result of insecticide use, but this is not a universal pattern in the published data sets (Fig. 1). Two studies concluded that there was an

increase in the abundance of hunting spiders as a result of insecticide use (Mansour et al. 1980a, Wisniewska and Prokopy 1997). Bogya et al. (1999) found no disproportionate effect of insecticides on the relative abundance of hunting spiders compared with web-building spiders in Hungary. Two studies showed the major effect of spraying was an increase in the abundance of thomisids, clubionids, or oxyopids in West Virginia and Virginia (this study, McCaffrey and Horsburgh 1980). However, these same studies (this study, McCaffrey and Horsburgh 1980) were also the only two that included night sampling, when thomisids and clubionids were more abundant. A Polish study (Olszak et al. 1992) found an increase in the abundance of philodromids and anyphaenids relative to thomisids and clubionids as a result of spraying (Fig. 1). Geographic factors seem to be more important than insecticide use in determining the composition of the spider community in apple orchards (Table 5; Fig. 1). A more prevalent pattern in these data sets is the dominance of web-building spiders in European, sprayed Quebec, and sprayed Washington orchards compared with the other North American and Israeli orchards, in which hunting spiders were dominant (Table 4). In particular, salticids comprised a dominant portion of the spider community in most North American orchards but were rare in European orchards (Table 4). Bogya et al. (1999) found salticids abundant in Hungarian orchards and noted a distinct trend of increasing abundance of salticids in Southern and Central Europe as compared with Western Europe. A possible reason for the absence of salticids in Western Europe is the relative absence of cicadellids (Homoptera). Cicadellids are not mentioned as a pest of concern in several Western European reports of pest management (Solomon 1987, Blommers 1994), whereas in North America, three species of cicadellids [Typhlocyba pomaria McAtee, Edwardsiana rosae, L., and Empoasca fabae (Harris)], are pests often requiring control in North American orchards (Hogmire 1995). More than 19 species of cicadellids are found in eastern North American apple orchards (Brown et al.

838


1988), and several were the dominant plant feeding arthropods in sprayed and unsprayed apple orchards in eastern North America (Brown and Adler 1989). In laboratory feeding studies, we observed that cicadellids were a preferred food source of several species of salticids found in West Virginia orchards (Brown and Schmitt, unpublished data). More information on the biology and ecology of spiders in orchards has been collected recently. Overwintering behavior (Peka´r 1999a, Horton et al. 2001), response to insecticides (Specht and Dondale 1960, Legner and Oatman 1964, Mansour et al. 1980a, McCaffrey and Horsburgh 1980, Bostanian et al. 1984, Epstein et al. 2000, Miliczky et al. 2000), and response to ecosystem manipulation (Wyss et al. 1995, Samu et al. 1997, Wisniewska and Prokopy 1997, Bogya et al. 2000) are areas recently investigated. Feeding behavior has also been examined for spiders commonly found in orchards (Bogya and Mols 1996). However, actual impact of spiders on pest populations has remained largely unexamined. Other than the work by Mansour et al. (1980b), manipulating spider and prey populations on a few individual apple trees, most of the reports of control by spiders are anecdotal (e.g., Putman 1967). Orchards have a large diversity of pest species (Brown and Adler 1989, Hogmire 1995). The spider community is also large and diverse, conditions generally assumed to be requisite for making a significant contribution to biological control (Wise 1993, Provencher and Riechert 1994). Investigations that manipulate spider communities in orchards and laboratory tests on feeding preferences and feeding rates are needed to adequately document the effects of spiders on pest populations in orchard ecosystems. Acknowledgments We thank C. R. Mathews, D. C. Weber, and N. Bostanian for comments on an earlier version of this paper.

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