Abstract Introduction Methods

STUDIES ON THE ARTHROPOD FAUNA OF ALFALFA V. SPIDERS (ARANEIDA)' A. G. WHEELER,JR.~ Department of Entomology, Cornell University, Ithaca, New York

Abstract Can. Ent. 105: 425-432 (1973) The spider fauna of alfalfa was studied at Ithaca, N.Y., in three experimental plots and in nearby fields during 1966-69. As part of an overall study of the arthropod fauna of alfalfa, the spider populations in the study plots were recorded weekly during visual examination of the terminal 6 in. of five stems for 100 plants in each of the plots. Additional information was obtained from sweep-net and pitfall trap collections in the study plots and from sweeping several commercial plantings. The spider fauna of alfalfa was found to consist of 78 species, 10 of which were collected only from the ground layer. Tetragnatha 1abo:iosa Hentz and Dictyna volucripes Keyserling were the most abundant species found in the weekly samples. Notes on the seasonal occurrence, location on the plants, and feeding habits are given for the common species.

Introduction Although the spiders associated with various specialized habitats, e.g., cedar glades (Meyer 1937), xeric dunelands (Lowrie 1942), and maritime communities (Barnes 1953; Barnes and Barnes 1954), have been studied, it has been only recently that the spiders associated with crop plants have received the attention they deserve. Among the more detailed studies on crop plant spiders are those on cotton by Whitcomb et al. (1963) and Whitcomb and Bell (1964) and on grain sorghums by Bailey and Chada (1968). Several lists of spiders found in crop plants have been compiled. Spiders occurring in corn were reported by Everly (1938), those in cole crops by Pimentel (1961 ), those in sugar cane by Hensley et al. ( 1961) and those in soybeans by Blickenstaff and Huggans (1962). Alfalfa, Medicago sativa L., has been noted to harbor an extremely rich arthropod fauna (Folsom 1909) and an unusually large general population of spiders (Muniappan and Chada 1970). However, there had been no compre- hensive survey of the spider fauna of alfalfa until the recent survey of Virginia alfalfa fields by Howell and Pienkowski ( 1971 ) . Previous to their work, Fenton (1959) mentioned that 15 species of spiders were taken from alfalfa in Oklahoma; those species plus two additional ones were listed by Fenton (ms.). The primary purpose of this investigation, which is part of an overall study of the arthropod fauna of alfalfa, was to determine the species composition of the spider fauna occurring in alfalfa fields at Ithaca, N.Y. Additional aims were to determine the position of the various species on the plants, their feeding habits, and their relative abundance in the alfalfa community.

Methods The majority of the spider collections and observations were made at Cornell University's Savage Farm during visual examination of alfalfa foliage as part of the systematic sampling of the alfalfa-arthropod community. Sampling consisted of the weekly counting of all arthropods on the terminal 6 in. of five stems on 100 plants in three study plots 100' x 100'. Details of the sampling technique and plots can be found in Pimentel and Wheeler (in press). Additional collections of spiders were made by sweeping alfalfa in the study plots and in other alfalfa fields 'This research supported by grant GB-19239 from the National Science Foundation. =Present address: Bureau of Plant Industry, Pennsylvania Department of Agriculture, Harrisburg. 425 Downloaded from https://www.cambridge.org/core. Tufts Univ, on 24 Mar 2018 at 18:52:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.4039/Ent105425-3 426 THE CANADIAN ENTOMOLOGIST March 1973 Table I. The spider fauna of alfalfa fields at Ithaca, N.Y., giving the stages collected on the plants and in the ground layer and overwintering within the fields (A, adult; S, subadult; I, immature)

Stages Stages collected collected Overwinteringm Species on plant on ground stages

Theridiidae Argyrodes trigonum (Hentz) I Enoplognatha ovata (Clerck) A Theridion differens Emerton A, I T.frondeum Hentz A, I T. murarium Emerton I Thymoites unimaculata (Emerton) A, I Linyphiidae Bathyphantes concolor (Wider) A, I Centromerus cornupalpis (0. P. - Cambridge) Ceraticelus emertoni (0. P. - Cambridge) A C. similis (Banks) A Ceratinopsidis formosa (Banks) A Eridantes erigonoides (Emerton) A Erigone autumnalis Emerton I E. blaesa Crosby & Bishop A, I Hypselistes $orens (0.P. - Cambridge) A, I Grammonota inornata Emerton A G. pictilis (0. P. - Cambridge) A Linyphia mandibulata Emerton A, 1 L. waldea Chamberlin and Ivie Meioneta nigripes (Simon) M. sp. A M. sp. B Tennesseellum formicum (Emerton) Walckenaera vigilax (Blackwall) Araneidae Acanthepeira stellata (Walckenaer) Araneus marmoreus Clerck A. trijolium (Hentz) A. sp. (cavaticus type) Araniella displicata (Hentz) Argiope trifasciata (Forskal) Cyclosa sp. Eustala cepina (Walckenaer) Larinia sp. Mangora gibberosa (Hentz) Mimoguatha foxi (McCook) Nesoscona arabesca (Walckenaer) Pachv~nathatristriata C. L. Koch 5'ingaratensis Emerton Tetragnatha laboriosa Hentz Mimetidae Mimetus epeiroides Emerton I Agelenidae Agelenopsis sp. I Pisauridae Dapanus miris (Walckenaer) A Lycosidae ? Arctosa sp. Lycosa helluo Walckenaer Pardosa milvina (Hentz) P. nzodica (Blackwall) P. moesta Banks Pirata minutus Emerton

Table I. (Continued)

Stages Stages collected collected Overwintering Species on plant on ground stages

Clubionidae Anyphaena sp. Anyphaenella saltabunda (Hentz) Chiracanthium SD. Clubiona abbotii'l. Koch C. obesa Hentz I Trachelas tranquillus (Hentz) A Thomisidae Misumena calycina (Clerck) Misumenoides aleatorius (Hentz) Mzsumenops asperatus (Hentz) Philodromus placidus Banks P. rufus Walckenaer Synema sp. Tibellrts oblongrts (Walckenaer) Tn~nrlcsangulntits (Il'alckenaer) -yslicrrs disrrtrsnns Keyserling S.,funfsks Keywrling X.~uroslis Keyserling S,luclnns (C. L. 1Cot.h) Salticidae Hubronattus decorus (Blaclcc~all) I A Icizcr lanrfii (Emerton) I dIetapkidipp~rsgaktkca (Kalcke~laer) A, 1 AT. pralcrvur (if aIckenacr) I Phidipims ntidas (Hentz) S P. princcps (Peckham) I I Talrrz*ern n~inrlla (Banks) A Dictynidae Argenna? obesa Emerton I Dictyna foliacea (Hentz) A D. hentzi Kaston A, I D. manitoba Ivie A D. volucripes Keyserling A. I I

in the Ithaca, N.Y., area. The spider fauna of the ground layer was determined through pitfall trap collections taken in the study plots.

Results Of the 78 species collected in alfalfa, 45 (57.7% ) were web builders and 33 (42.3%) were hunters. Excluding the 10 species that were taken only from the ground layer, 40 species (58.8% ) were web builders and 28 species (41.2%) were hunters. Table I lists the 78 species and their stages, i.e., adults or immatures, taken on foliage and the ground layer, and the overwintering stages found within the fields. Notes on individual species, including location on the plants, feeding habits, and seasonal occurrence, are presented by family in the following discussion. Theridiidae. Members of the Theridiidae were never abundant on alfalfa. Theridion murarium, the most numerous of the theridiids, built a tangled web on terminal buds and was found on the plants from early May to late October. Eno- plognatha ovata also built a loose, tangled web on terminal stems and was also found occasionally in webs on stems near the soil surface. During July, females with egg sacs were found concealed among rolled leaflets near the top of the plants. A

Downloaded from https://www.cambridge.org/core. Tufts Univ, on 24 Mar 2018 at 18:52:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.4039/Ent105425-3 428 THE CANADIAN ENTOMOLOGIST March 1973 female of T. differens was also found in July with an egg sac concealed within four leaflets tied together with silk. Linyphiidae. In terms of the number of species this was the dominant family of spiders, but few of the species were abundant in alfalfa. Linyphia mandibulata, however, was one of the most common spiders found in the study. It built a dense, flat, platform web among stems, usually several inches below the top of the plant. During April, immatures were found in small webs at the base of the plants. L. mandibulata was observed to feed on large numbers of potato leafhoppers, Empoasca fabae (Harris), as well as on clover leafhoppers, Aceratagallia sanguinolenta (Provancher), and small Diptera. Tennesseellum formicum was commonly found in webs at the base of small plants. Collembola and pea aphids, Acyrthosiphon pisum (Harris), frequently were caught in the webs. Immatures of T. formicum were also found wandering over foliage, and adults and immatures were taken in pitfall traps. Bathyphantes concolor built a sheet web near the base of the plants. In late October 1969 it was collected in large numbers on the plants, along with Walckenaera vigilax, following heavy frost. The ballooning habit following the first frosts of autumn is well known among the Linyphiidae (Kaston 1948). Erigone blaesa built small irregular webs on stems near the ground; immatures were also taken on the soil surface. An egg sac of E. blaesa was found in a crevice in the soil in mid-July. Hypselistes florens built small irregular webs on stems near the ground; it also was observed to hunt over the foliage and on one occasion to capture a pea aphid. Araneidae. Several orb weavers were among the most abundant spiders in alfalfa. Tetragnatha laboriosa, the most abundant species found on the plants, was most numerous from June to October. It built symmetrical webs near the top of plants and was observed to feed on potato and clover leafhoppers, cowpea aphids, Aphis craccivora Koch, tarnished plant bugs, Lygus lineolaris (Beauvois), the anthocorid Orius insidiosus (Say), and small Diptera. Courtship behavior was observed during early to mid-August; egg sacs were found from July to September on alfaIfa leaflets both near ground Ievel and at the top of the plants. Araniella displicata was the second most common araneid on alfalfa and was found in small, symmetrical webs near the top of the plants where it fed on 0. insidiosus, the flower thrips, Frankliniella tritici (Fitch), the nitidulid beetle Brachypterolus pulicarius L., and the coccinellid Coleomegilla maculata (DeGeer) . This species was also found to hide by day within retreats of rolled alfalfa leaflets. Araneus trifolium, the third most common araneid, was found from June to late September in large orbs with foundation lines often running to several plants. A. trifolium was most often found above the webs within retreats made of alfalfa leaflets tied together and lined with silk. This species was observed to feed on redlegged grasshoppers, Melano- plus femurrubrum (DeGeer), C. maculata, northern corn rootworm, Diabrotica longicornis (Say), the mirid Plagiognathus politus Uhler, and a halictid bee. On one occasion an immature of Eustala cepina was found feeding on small insects caught in the periphery of a large orb of A. trifolium. Mimetidae. A single immature of Milnetus epeiroides was taken on alfalfa foliage in mid-October. Agelenidae. Immatures of Agelenopsis sp. were found occasionally in large funnel webs that surrounded entire plants. Pisauridae. A single specimen of Dapanus miris was found in late May sitting at night on the top of a plant.

Downloaded from https://www.cambridge.org/core. Tufts Univ, on 24 Mar 2018 at 18:52:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.4039/Ent105425-3 Volume 105 THE CANADIAN EXTOMOtMil!tT 429 Lycosidae. The wolf spiders were rarely collected on alfalfa although several species were common in the ground layer. Extensive nocturnal collecting resulted in the collection of only an occasional immature of Pardosa rnilvina and P. moesta on the foliage. Immatures of Pirata minutus were found by day on the plants during May and October. Clubionidae. Clubionids were found to be particularly active on the plants at night. The most common species, Clubiona abbotii, was found on the plants from April to October and was on one occasion observed at night to prey on an adult alfalfa weevil, Hypera postica (Gyllenhal). Anyphaenella saltabunda was also active at night, and like the other clubionids on alfalfa, was found to hide by day in tubular nests made of alfalfa leaflets. Thomisidae. The crab spiders were often common on terminal buds and within flowers. Misurnenops asperatus, common from June to October, was observed to capture alfalfa weevil larvae, adults, and nymphs of tarnished plant bugs and a nymph of the alfalfa plant bug, Adelphocoris lineolatus (Goeze). Misurnenoides formosipes was most numerous in August and was observed to capture an adult tarnished plant bug and an adult of the anthomyiid Hylemya sp. Tibellus oblongus was collected from late May to mid-October and was on several occasions taken on the plants at night. Salticidae. The jumping spiders were another common group of hunting spiders on alfalfa. Metaphidippus galathea, the most common of the salticids, was found on the plants from May to November. Their egg sacs were often found within nests made of alfalfa leaflets lined with silk. Subadults overwintered within hollow, dead alfalfa stems near the base of the plants. This species was twice observed to capture adults of the alfalfa seed chalcid, Bruchophagus roddi Gussakovsky. Immatures of Habronattus decorus were taken within silk nests at the top of the plants. Dictynidae. Of the five species of this family, only one species, Dictyna volucripes, was collected in considerable numbers. D. volucripes, the second most abundant spider collected in alfalfa, was common from June to October in small snares placed on terminal stems, especially on the dead stems of older plants. Large numbers of flower thrips, 0. insidiosus, and small flies and wasps were caught in the snares. Egg sacs were found in webs from early June to late August. D. hentzi was not common; it also built irregular webs on terminal stems. A single immature of Argenna obesa was collected in late May within a folded alfalfa leaflet lined with silk. Spider populations in alfalfa. Figure 1 gives the population trends of spiders taken in the weekly systematic sampling of 300 alfalfa plants during 1966 to 1969. Populations were generally low during May and June, gradually increased to a peak during late July to early September, and persisted in low numbers into October and November. In terms of the numbers of spiders collected during sampling in 1968, 76.7% of all spiders were web builders and 23.3% were hunters. In 1969, 83.2% of all spiders collected were web builders while only 16.8% ,were hunters.

Discussion The spider fauna of New York alfalfa fields had several species in common with the fauna reported from alfalfa in Virginia and Oklahoma. Thirty-one of the 110 named species reported from Virginia by Howell and Pienkowski (1971) and

I 21 1 6 20 I 3 17 31 1 15 28 1 12 26 113 JUNE JULY AUG SEPT OCT NOV

I 7 21 1 5 14 1 2 16 36 1 13 27 112 25 JUNE JULY AUG SEW OCT

50 -1 1968

1 1711 I? 28110 2517 2114 1915 2110 MAY JUNE JULY AUG SEPT OCT NOV

7 211 5 1914 171 7 14 76111 MAY JUNE JULY AUG SEPT FIG. 1. Number of spiders from the terminal 6 in. of five alfalfa stems on 300 plants/week during 196669.

five of the 16 named species reported by Fenton (ms.) from Oklahoma alfalfa were also found in the present study. Three species, Acanthepeira stellata, Tetragnatha laboriosa, and Phidippus audax, were found in all three studies. T. laboriosa, the most common spider in Virginia alfalfa fields (Howell and Pienkowski 1971), was also the most abundant spider found in alfalfa in the Ithaca area. If the method of prey capture of the different species is considered, a higher proportion of web builders to hunters was found than was reported from Virginia alfalfa (Howell and Pienkowski 1971) or from cotton (Whitcomb and Bell 1964). Although a direct comparison is not possible, it appears that if individual specimens

Downloaded from https://www.cambridge.org/core. Tufts Univ, on 24 Mar 2018 at 18:52:38, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.4039/Ent105425-3 Volume 105 THE CANADIAN ENTOMOLOGIST 43 1 are considered, a similarly high proportion of web builders to hunters was found in foliage samples from New York alfalfa. This apparent high proportion of web- building species might be a reflection of the sampling technique employed in which only the terminal 6 in. of stems were sampled. However, the contrast would appear to be due in part to the minor role of the Clubionidae, the nearly complete absence of the Lycosidae on the foliage, and absence of the Oxyopidae. The oxyopids, or lynx spiders, were found to be an important group of predators in Arkansas cotton (Whitcomb and Bell 1964), and Oxyopes salticus was reported as one of the most common spiders in Virginia alfalfa (Howell and Pienkowski 1971) . In contrast to the apparent minor role of the Dictynidae in Virginia alfalfa, five dictynids were collected in New York alfalfa, including Dictyna volucripes, the second most abundant species encountered. A discussion of the prey selection of spiders is still partly a matter of conjecture and beyond the scope of this paper. However, two rather obvious factors, the position of the various species on the plants and their method of prey capture, appeared to influence the frequency of encounters with potential prey species on alfalfa. For example, Collembola and other members of the ground fauna were likely to enter the small webs of Tennesseellum formicum and Bathyphantes concolor that were built at the bases of the plants, whereas leafhoppers and flower thrips entered the large platform webs of Linyphia mandibulata that were built near the tops of the plants. Among the hunters, Misumenops asperatus and Misumenoides formosipes, species that were largely restricted to lying in ambush within blossoms or on terminal buds, would more frequently encounter insect visitors to the blossoms or plant bugs that fed on the reproductive structures. Hunting species that ranged over the plants, e.g., Metaphidippus galathea, would perhaps come into contact with different prey species. It was not possible to assess the role of spiders in limiting populations of in- jurious insects on alfalfa. Some recent experimental field work has shown that herbivore populations may be limited by spiders (Kajak et al. 1968). Spiders were the first predators found in alfalfa in early spring and presumably began to exert some pressure on the herbivores present early in the season, e.g., pea aphids and plant bugs. Their early season activity and their persistence into November make them an important group of predators in alfalfa.

Acknowledgments I am grateful to the late Wilton Ivie and Dr. J. A. Beatty for their determina- tions of the spiders. References Bailey, C. L. and H. L. Chada. 1968. Spider populations in grain sorghums. Ann. ent. Soc. Am. 61: 567-571. Barnes, R. D. 1953. The ecological distribution of spiders in non-forest maritime communities at Beaufort, North Carolina. Ecol. Monogr. 23: 3 15-337. Barnes, B. M. and R. D. Barnes. 1954. The ecology of the spiders of maritime drift lines. Ecology 35: 25-35. Blickenstaff, C. C. and J. L. Huggans. 1962. Soybean insects and related arthropods in Missouri. Univ. Mo. agric. Exp. Sin Res. Bull. 803. 51 pp. Everly, R. T. 1938. Spiders and insects found associated with sweet corn with notes on the food and habits of some species. I. Arachnida and Coleoptera. Ohio I. Sci. 38: 136-140. Fenton, F. A. 1959. The effect of several insecticides on the total arthropod population in alfalfa. I. econ. Ent. 52: 428-432. - (unpub.) List of arthropods collected in alfalfa, Stillwater, Oklahoma, 1954-56.

Folsom, J. W. 1909. The insect pests of clover and alfalfa. Univ. Ill. agric. Exp. Stn Bull. 134. pp. 113-197. Hensley, S. D., W. H. Long, L. R. Roddy, W. J. McCormick, and E. J. Concienne. 1961. Effects of insecticides on the predaceous arthropod fauna of Louisiana sugarcane fields. J. econ. Ent. 54: 146-149. Howell, J. 0. and R. L. Pienkowski. 1971. Spider populations in alfalfa, with notes on spider prey and effect of harvest. J. econ. Ent. 64: 163-168. Kajak, A., L. Andrzejewska, and Z. Wojcik. 1968. The role of spiders in the decrease of damages caused by Acridoidea on meadows - experimental investigations. Ekol. pol. (A) 16: 755-764. Kaston, B. J. 1948. Spiders of Connecticut. Bull. Conn. St. geol. nut. Hist. Surv., No. 70. 874 pp. Lowrie, D. C. 1942. The ecology of the spiders of the xeric dunelands in the Chicago area. Bull. Chicago Acad. Sci. 6: 161-189. Meyer, A. M. 1937. An ecological study of cedar glade invertebrates near Nashville, Tennessee. Ecol. Monogr. 7: 403-443. Muniappan, R. and H. L. Chada. 1970. Biology of the crab spider, Misumenops celer. Ann. ent. Soc. Am. 63: 1718-1722. Pimentel, D. 1961. Competition and the species-per-genus structure of communities. Ann. ent. Soc. Am. 54: 323-333. Pimentel, D. and A. G. Wheeler, Jr. 1973. Influence of alfalfa resistance on a pea aphid population and its associated parasites, predators, and competitors. Environ. Ent. 2: 1-1 1. Whitcomb, W. H. and K. Bell. 1964. Predaceous insects, spiders, and mites of Arkansas cotton fields. Bull. Ark. agric. Exp. Stn, No. 690. 84 pp. Whitcomb, W. H., H. Exline, and R. C. Hunter. 1963. Spiders of the Arkansas cotton field. Ann. ent. Soc. Am. 56: 653-660. (Received 20 November 1972)