1995. The Journal of Arachnology 23 :212–21 4

CHEMICAL ATTRACTION OF MALE CRAB (ARANEAE, ) AND KLEPTOPARASITIC FLIES (DIPTERA, MILICHIIDAE AND CHLOROPIDAE )

After the first day of a study testing the at- ticus females were caught, and one in- traction of scavenging flies (Diptera, Milichiidae dividual was caught in a control trap . Xysticus and Chloropidae) to defensive chemicals of true spp . from Field 2 were grouped because we coul d bugs (Heteroptera), it was apparent that males not reliably separate the species ; however, 15 out of one type of crab (Thomisidae) were also of the 25 specimens determined were X. aucti- attracted to the chemical treatments . Therefore, ficus. Again, the attraction to (E)-2-octenal was the original goal of the study was abandoned in greater, but not significantly so, than to (E)-2- 1993 in favor of a full-time investigation of spi- decenal (Table 1, P = 0 .35). der attraction . In order to determine if other compounds were Traps were constructed of transparent cylin- involved in spider attraction or if the know n drical containers (20.2 x 19.7 cm; Tri-State attractants acted synergistically, additional set s Molded Plastic, Dixson, Kentucky) by cutting of traps were deployed in Field 2 baited in a two 9-cm diameter holes in opposite sides, and similar manner with (E)-2-octenoic acid, octan- covering each hole with an inwardly projecting oic acid, 1-octanol, (E)-2-octenal/(E)-2-decena l screen funnel (Aldrich et al . 1984). On 8 June (1 :1 blend), (E)-2-nonenal, (E)-2-decenal ace - 1993, nine traps were hung from stakes in a 0 .9 tate, and (E)-2-hexenal butyrate (Aldrich Chem - ha fallow field 10 m apart in contact with foliage ical Co ., Milwaukee, Wisconsin; or Bedoukian (mixed grasses, goldenrod, and bush-clover), al- Research, Inc.). Standards of octenal and decena l ternating the following three treatments: (E)-2- contained impurities of the corresponding acids octenal, (E)-2-decenal, and unbaited controls . (1 .48% (E)-2-octenoic acid; 1 .58% (E)-2-decen - Chemicals were dispensed from cotton swabs (Q- oic acid; analyzed by standard methods, e . g., Tips©, Chesebrough Pond's Co., Greenwich, Aldrich et al . 1984), and the acids predominated Connecticut) dipped in neat standards (ca. 200 in extracts of Q-Tips after 24 h field exposure in µl; Bedoukian Research, Inc ., Danbury, Con- hot, sunny weather (88% and 65% (E)-2-octenoi c necticut). Traps were inspected every 1-2 days, acid and (E)-2-decenoic acid, respectively) . Nev- and rebaited every 2-3 days . ertheless, there was no indication that (E)-2-oc - From 9-18 June, 200 males of Xysticus ferox tenoic acid or octanoic acid are attractive to Xys- (Hentz) (Thomisidae) were caught in traps baited ticus species. Octanol was a common minor im - with alkenals; none were captured in controls purity (< 1%) in both octenal and decenal stan - (Table 1, Field 1) . Capture of X. ferox males was dards, but it seemed inactive. Similarly, there variable for both (E)-2-octenal-baited traps (to- was no indication of synergism between octena l tals of 28, 33, 59 males/trap) and (E)-2-decenal- and decenal, no evidence that (E)-2-nonenal is baited traps (7, 28, and 45 males/trap) such that attractive, and common esters of stink bugs, (E) - attraction to (E)-2-octenal was not significantly 2-decenyl acetate, and plant bugs (Miridae), (E) - greater than to (E)-2-decenal (P = 0 .33). 2-hexenyl butyrate, appeared inactive . From 18-20 June 1993, captures of Xysticus In 1994, traps were deployed earlier in Fiel d males dropped to almost zero in Field 1 ; there- 1 (14 May-30 June), and an additional set o f fore, on 21 June the traps were redeployed in traps was baited with another alkenal commonl y another field (0 .5 ha) that had been lightly sown produced by heteropterans, (E)-2-hexenal (Be - with a mixed ground cover including red clover doukian Research, Inc .) (Aldrich 1988) . Xysticus and vetch (Table 1, Field 2). Vegetation in Field individuals were caught from the first day of th e 2 was sparse, so traps were placed directly on the experiment in numbers greater than the previou s ground. From 22 June-15 July, a total of 74 year (Table 1) . The results for Xysticus (identified males of four Xysticus spp. was caught in traps to genus only) corroborated previous results fo r baited with (E)-2-octenal or (E)-2-decenal : X. male-specific attraction to (E)-2-octenal and (E)- ferox, X. discursans Keyserling, X. triguttatus 2-decenal, but (E)-2-hexenal was not attractive . Keyserling, and X. auctificus Keyserling. No Xys- In 1994 we also decided to collect the trapped

212

RESEARCH NOTES 213

Table 1 .—Total numbers of Xysticus species males and females caught in traps in 1993 and 1994 . Within a column, sums followed by the same letter are not significantly different at the 5% level (three traps/treatment ; one-way ANOVA of rank transformed sums/trap/trapping period, fit separately for each field) .

1993 1994 Field 1 Field 2 Field 1 Treatment Male Female Male Female Male Female (E)-2-Hexenal — — — — la 3a (E)-2-Octenal 120a Oa 52a Oa 224b Oa (E)-2-Decenal 80a Oa 22a Oa 115b la Control Ob Oa lb Oa Oa Oa

milichiid and chloropid flies, several of which ically baited traps, compared to 615 adult Xys- are ideptoparasitic on true bugs caught in spide r ticus males. webs (Eisner et al. 1991; Landau & Gaylor 1987) . Behavioral studies have shown that both web- Exclusively females of one milichiid, Milichiella building and hunting spiders communicate wit h arcuata (Loew), were significantly attracted t o pheromones (Barth 1993; Pollard et al. 1987; (E)-2-hexenal-baited traps, but not to the othe r Rovner 1991 ; Suter & Hirscheimer 1986; Tietjen alkenal-baited or control traps (Table 2) . Fifteen 1979). To date, there has been only one spider chloropid species were caught, totalling 2269 in- sex pheromone chemically identified : unmated dividuals (predominantly females), but Ocella females of the sheet-web weaving spider, Liny- trigramma (Loew) accounted for over 95% of th e phia triangularis (Clerck) (Linyphiidae), deposit total, with O. cinerea (Loew) and O. parva (Ad- the dimer of (R)-3-hydroxybutyric acid on thei r ams) comprising about 1% . Chloropids were at- webs which, after breaking down to the more tracted to all three alkenals compared to contro l volatile monomer, elicits the web reduction be- traps; however, (E)-2-octenal was most attrac- havior of males leading to copulation (Schulz & tive, followed by (E)-2-decenal, and (E)-2-hex- Toft 1993). Discovery of an acidic pheromone enal was the least attractive (Table 2). These data for a spider suggested that acidic impurities i n suggest that scavenging milichiid and chloropid alkenal standards might be responsible for at - flies use allomones from dying bugs in spider traction of Xysticus males. Nonetheless, trap s webs (and probably elsewhere), not just to fin d baited with high and low (10 Al) doses of (E)-2 - food, but also to discriminate between heterop- octenoic acid were unattractive in the field. teran species (see also Sugawara & Muto 1974) . In summary, the exact role of (E)-2-decenal The surprising discovery that male Xysticus and (E)-2-octenal in attraction of Xysticus males species are attracted to (E)-2-octenal and (E)-2 - is not yet clear, but our results suggest that th e decenal is difficult to explain . Xysticus species alkenals, or impurities in the synthetic standards , chemically attracted to alkenals are brown , are related or identical to sex pheromone com- ground-dwelling spiders that probably seize mos t ponents of these spiders . This is apparently the of their prey after laying-in-wait in the litter zon e (Morse 1983). A variety of heteropterans are among the natural prey of litter-inhabiting cra b Table 2.—Milichiid and chloropid flies caught in spiders (Nyffeler & Breene 1990; Nentwig 1986; traps in 1994. Within a column, sums followed by the Araya & Haws 1988); therefore, it is possible that same letter are not significantly different at the 5% level Xysticus use alkenals as host-finding kairomone s (three traps/treatment ; one-way ANOVA of rank trans- as do scavenging flies. This seems unlikely, formed sums/trap/trapping period) . though, because Heteroptera constitute only a Treatment small portion of the prey taken by ground-dwell- Milichiidae Chloropidae ing Xysticus species (Nyffeler & Breene 1990 ; (E)-2-Hexenal 136a 33a Nentwig 1986), and esters of Heteroptera were (E)-2-Octenal lb 2069b unattractive. Most importantly, only four fe- (E)-2-Decenal 7b 167c males and no immatures were caught in chem - Control Ob Od

214 THE JOURNAL OF ARACHNOLOGY

first report of spiders being attracted into trap s and Misumena vatia (Clerck) (Araneae : Thomisi- baited with synthetic chemicals . dae) on flowers . J. Arachnol., 11:87-94. Nentwig, W. 1986. Non-webbuilding spiders : Prey ACKNOWLEDGMENT S specialists or generalists? Oecologia, 69 :571-576. Nyffeler, M . R. G. Breene. 1990 . Spiders associated We thank Mr. Gustavo Hormiga of the Mary- with selected European hay meadows, and the ef- land Center for Systematic Entomology (Uni- fects of habitat disturbance, with the predation ecol - versity of Maryland and Smithsonian Institu- ogy of the crab spiders, Xysticus spp. (Araneae, tion) for identifying the spiders and reviewin g Thomisidae) . J. Appl . Entomol ., 110:149-159 . the manuscript, and Dr. C. W. Sabrosky (USDA- Pollard, S . D., A. M. MacNab R. R. Jackson. 1987. ARS, Systematic Entomology Laboratory) for Communication with chemicals : Pheromones and determinations of Diptera . We are also grateful spiders, Pp. 133-141, In Ecophysiology of Spiders to Dr. Douglass H . Morse, Division of Biology (W. Nentwig, ed.). Springer, New York . and Medicine, Brown University, for a helpfu l Rovner, J. S. 1991. Turning behaviour during pher- discussion of thomisid biology and for reviewing omone-stimulated courtship in wolf spiders . Anim. Behay., 42 an early draft of the manuscript. Mention of a :1015-1016. Schulz, S . S. Toft. 1993. Identification of a sex company name does not imply endorsement b y pheromone from a spider . Science, 260 :1635-1637 . the U. S. Department of Agriculture. Sugawara, R. T. Muto. 1974. Attraction of several LITERATURE CITED dipterous insects to aliphatic esters (Diptera : chiidae, Chloropidae and Ceratopogonidae). Appl . Aldrich, J. R. 1988. Chemical ecology of the Het - Entomol. Zool., 9:11-18 . eroptera. Ann. Rev. Entomol., 33:211-238. Suter, R. G. A. J. Hirscheimer. 1986. Multiple Aldrich, J. R., J. P. Kochansky C . B. Abrams. 1984. web-borne pheromones in a spider Frontinella pyr- Attractant for a beneficial insect and its parasitoids : amitela (Araneae : Linyphiidae).Anim. Behay ., 34: Pheromone of the predatory spined soldier bug, 748-753. Podisus maculiventris (Hemiptera: Pentatomidae) . Tietjen, W . J. 1979. Tests for olfactory communi- Environ . Entomol ., 13:1031-1036 . cation in four species of wolf spiders (Araneae, Ly- . B. A. Haws. 1988. pre- Araya, J. E cosidae). J. Arachnol., 6 :197-206 . dation of black grass bugs (Hemiptera : Miridae) in Utah ranges . J. Range Management, 41 :100-103 . Jeffrey R . Aldrich: Barth, F. G. 1993 . Sensory guidance in spider pre- Insect Chemical Ecology copulatory behaviour. Comp. Biochem. Physiol., Laboratory, USDA-ARS, Bldg 007, Agricul- 104A :717-733 . tural Research Center-West, Beltsville, Mary - Eisner, T., M. Eisner M. Deyrup. 1991. Chemical land 20705 USA attraction of kleptoparasitic flies to heteropteran in - sects caught by orb-weaving spiders . Proc. Natl. Tev M. Barros: Department of Entomology , Acad. Sci., 88:8194-8197. University of Maryland, College Park, Mary - Landau, G. D. M. J. Gaylor . 1987. Observations land 20742 USA. on commensal Diptera (Milichiidae and Chloropi- dae) associated with spiders in Alabama . J. Arach- Manuscript received 13 February 1995, revised 21 July nol., 15 :270-272. 1995. Morse, D. H. 1983. Foraging patterns and time bud - gets of the crab spiders Xysticus emertoni Keyserling