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A Kleptoparasitic Cecidomyiid and Other Flies Associated With Spiders

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A Kleptoparasitic Cecidomyiid and Other Flies Associated With Spiders
  A KLEPTOPARASITIC CECIDOMYIID AND OTHER FLIES ASSOCIATED WITH SPIDERS BY JOHN SIVINSKI AND MARK STOWE Spiders and their webs are predictable sources of insect cadavers. A small number ofanimals regularly exploit this resource, eitheras kleptoparasites or commensals, depending on whether symbionts compete for the same prey (see Robinsonand Robinson, 1977, for more detailed terminology). Among the thievesare specialized spiders (citations in Vollrath1979a, 1979b), mature maleand juvenilespiders (Stowe 1978, citationsin Nyffeler and Benz 1980), Hemiptera(Davis and Russell 1969), a hummingbird (takes web- bing in addition to small insects, Young 1971), panorpid scorpion- flies (Thornhill 1975), Lepidoptera larvae (Robinson 1978), wasps (Jeanne 1972), damselflies (Vollrath 1977), and a handful of flies (reviews in Knab 1915; Bristowe 1931,1941; Lindner 1937; Richards 1953; Robinson and Robinson 1977). Only a few of thereports on Diptera kleptoparasites srcinate from North America (McCook 1889, Frost 1913, Downes and Smith 1969). With a single exception (Downes andSmith 1969), all of the previouslydescribed klepto- parasitic flies belong to the Brachycera and Cyclorrhapha. We reporthere on a surprisingly diverse kleptoparasitic Dipterafauna in north central Floridawith a cecidomyiid (Nematocera) as its dominantmember. METHODS Unless otherwisenoted, specimens were taken in Alachua County, Florida, during August and September, 1980. Observations were made principally at night, using red filteredlight. A trap was constructed to test whether flies were attracted to dead insectsin general or those partially digested by spiders in particular. Trans- parent plastic discs (10 cm. dia.) were covered on one side with Tacky Trap(R), a trapping compound. Three discs were strung between bamboo poles and placed near a web of Nephila clavipes (a Department of Entomology and Nematology, Universityof Florida,Gainesville, Fla. 32611 2Museum of Comparative Zoology, Harvard University, Cambridge, Mass. 02138 Manuscript received by the editor May 13, 1981. 337  338 Psyche [Vol. 87 large orb-web spider). On one disc was placed a cricket (Gryllus assimilis) that had been fed on by the spider for 30-60 minutes. Another carried an intact cricket, killed by freezing, then thawed, and the third was a blank control. Fourteen replicates were made. In addition, we periodically collected by aspiration flies hanging on webs and spider draglines independent of webs. RESULTS We propose various flies to be spider symbionts on thebasis of either direct or circumstantial evidence. The latter category consists of flies caught exclusively,or forthe most part, on trap discs baited with partially consumed spiderprey. Known Kleptoparasites Cecidomyiidae:Didactylomyia longimana (Felt), length 1.3 mm. This most abundant ofkleptoparasites was active at dusk and night. In certain locationsvirtually every Nephila clavipeswith prey would have from one to overa dozen midges perched on the semi-digested prey (Fig. 1). We also observed D. longimana in association withotheraraneids; Argiope aurantia, Mastophora bisaccata, and Eriophora ravilla. While individuals were sometimes found on swathed insects stored in the web, they were more commonly seen on fluid-covered preybeing consumed by the spider. Midges were observed with their heads applied to the surfaceof the insect and their abdomens expanded, leaving no doubt that feeding had occurred. Rarely, a fly was found on the dorsalsurfaceof the abdomen or the carapace of a spider. Examination of 3 photo-graphs of flies resting on spiders shows no evidenceof feeding on the spider. Spiders defended their catch from D. longimana by batting at approaching flies with their forelegs. One of us (Stowe) has seen Scoloderus cordatus (Araneidae) vigorously brushing nematocerous flies off its prey. McCook (1889) describes a similar behavior in Argiope aurantia. SinceNephila,Argiope, and Scoloderus are in separatesubfamilies, the behavior may predate theradiation of thefamily. (Nephila maculata behaves similarly toward kleptoparasitic spiders of the genusArgyrodes, Robinson and Robinson, 1973; however in Scoloderus this behavior must be adapted for klepto- parasitic flies alone since Argyrodes are never intheir webs.) Prey defense is indicative of a competitive relationship and substantiates  1980] Sivinski & Stowe Kleptoparasitic cecidomyiid 339 Figure 1. (left) A female Didactylomyia longimana perched on the partially consumed prey of Nephila clavipes; (right) D. longimana female on the cephalothorax of Argiope aurantia. A) line in Nephilaweb; B) anterior end of abdomen; C) leg (space bars mm).  340 Psyche [Vol. 87 our classification of the midge as a kleptoparasite rather than a commensal. True carnivory, the direct consumption of animal food, is unknown among adult cecidomyiids. The only previous recordof kleptoparasitism and protein consumption we are aware ofconcerns two African species that steal regurgitants being passed between ants (Farquharson 1922). A recordof cecidomyiids attached to the wings of Neuroptera is probably a misidentification of a cera- topogonid ectoparasite (described by Slosson 1896). Twenty flies were aspirated from spider prey; all were females. Traps baited with partially digested insects captured 7 females. No midges were taken on the trapwith a dead, intactinsect or on the control. The flies are probably attracted by volatile products of the spider’s external digestion. Flies always approached fromdown- wind and were oftenseen attempting to land on the spiders’ mouthparts just after a feeding bout. Milichiidae(acalypterate Cyclorrhapha): The Milichiidaecontain a number ofkleptoparasitic species, primarily in the genera Desmometopa, Phyllomyza, and Neophyllomyza. Hosts include asilid flies (Kertesz 1897; Mik 1898; Biro 1899; Peyerimhoff 1917), reduviid bugs (Biro 1899; Richards 1953; Robinson 1977), and crab, orb-web, and jumping spiders (Frost 1913; Richards 1953). The spider Misumena vatia strikes out at approaching milichiids and oscillatesto dislodge those already perched on prey(Biro 1899). Again, defense suggests competition, hence,kleptoparasitism. Paramyia nitens (Loew), length 1.9 mm. This small black fly was seen on two occasions: asingle individual was found on the prey of a Nephila clavipes and approximately 10 flies on a vespid wasp being consumed by an A. aurantia. Both observations were at night. The fly is agile and difficult to dislodge from prey. One individual managed to balance on the spider’s prey while the prey item was brisklyrotated beneath thechelicerae of its host (behavior and appeb.rance are similar to that of an unidentified fly watched by McCook 1889). All 5 specimenscaptured were females. The mouthparts of milichiids areoften elongated; thoseof Paramyia nitens are strikingly exaggerated, nearly as long as the body. The rostrum alone is 1.3 the height of the head. This extension may aid in reaching through wrapping silk or lapping at the particularly fluid, but dangerous, areas near the spider’s mouthparts. Such precarious feeding, apparently between the jaws of spiders, has been  1980] Sivinski & Stowe Kleptoparasitic cecidomyiid 341 noted in Didactylomyia longimana; unidentified fly (McCook 1889); and milichiids, (Champion-Jones 1937; Robinsonand Robin- son 1977). The mouthparts of D. longimana arealso somewhat pronounced for a cecidomyiid(R. J. Gagne, pers. comm.). Phylomyza sp. near securicornis, length 2.8 mm. A single female was found riding on a Nephila clavipes at the juncture of the abdomen and cephalothorax. This is the only species we en- countered that appeared to be phoretic, i.e., attached to ahost who is not fed upon. Phoresy is reported in a neotropical Phyllomyza sp. (Robinson and Robinson 1977). Our sighting was made at night. Neophyllomyza species A, length 1.5 mm. A diurnally active species captured in Marion Co., Fla., on the prey of a Nephila clavipes. The mouthparts are as elongated as those of Paramyia nitens; the rostrum is 1.3 the heightof the head. The single female specimen was of 5 flies on the prey (see below). Neophyllomyza species B, length 1.8 mm. A species taken from the same prey as species A. Mouthpart development is more conventional. The rostrum is 0.8 the heightof the head. Two females were captured. Suspected Kleptoparasites The following were captured most frequently in traps baited with spider prey. Flies may be kleptoparasites or participants in a number ofother symbioses, locating spiders, their eggs or webs through scents released by pre-oral digestion. Ceratopogonidae: Culicoides baurL length 1.0 mm. Seven females were taken from spider prey discs, three on intact insects but none on controls. The two previous feeding records of C. bauri were fromhumans, suggesting catholic tastes (see Blanton and Wirth 1979). A considerable number of Ceratopogonidae are carnivores, sapro- phrages or ectoparasites of insects (Downes 1978; Downes and Smith 1969; Wirth 1956, 1971). Downes and Smith (1969)mention an Atrichopogon sp. feeding on dead insectsin spiderwebs. Phoridae: Megaselia sp., length 2-3 mm. Seven female specimens of this genus were taken from spider prey-baited discs, none from intact insects or controls. Kleptoparasitism may not be the most 3In a more benign relationship probably derived from kleptoparasitism,Australian orb-web spiders spread their chelicerae to aid mutualistic milichiids cleaning their mouthparts (McMillan 1975).
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