Spider Mimicry in Fruit Flies (Diptera: Tephritidae): Further Experiments

Spider Mimicry in Fruit Flies (Diptera: Tephritidae): Further Experiments on the Deterrence of Jumping Spiders (Araneae: Salticidae) by Zonosemata vittigera (Coquillett)

DOUGLAS W. WHITMAN,1 LARRY ORSAK,2 AND ERICK GREENE3 Department of Entomology, University of Georgia, Athens, Georgia 30602

Ann. Entomol. Soc. Am. 81(3): 532-536 (1988) Downloaded from https://academic.oup.com/aesa/article/81/3/532/60805 by guest on 29 September 2021 ABSTRACT Zonosemata vittigera (Coquillett) possesses dark transverse wing bands and abdominal eye spots, which cause it to resemble a salticid spider. Jerky motion, wing flicking behavior, and sudden short flights to nearby foliage enhance this resemblance. Here we provide observations on the behavioral interactions between jumping spiders and Z. vittigera. In the laboratory, sympatric jumping spiders (Salticidae) attacked and captured more house flies (Musca domestica L.) or wing-painted Z. vittigera (wing markings disguised by green paint) than unpainted Z. vittigera. Furthermore, salticids backed away from, or gave threat or courtship displays to, normal Z. vittigera but not to house flies or wing-painted Z. vittigera. These results provide further evidence that Z. vittigera mimic jumping spiders and that this resemblance reduces jumping spider predation.

KEY WORDS Insecta, Araneae, mimicry, predation

3 NUMEROUS SPIDERS mimic insects such as ants search station. Flies were kept in a 2-m cage and (Reiskind 1970, 1977, Englehardt 1971, Edmunds provided with water, sugar water, honey, dry pow- 1978, Foelix 1982, Jackson 1982a). However, Hin- dered milk, sliced fruit, and potted S. elaeagni- ton (1976) noted that virtually no insect seemed to folium plants. Salticid spiders were collected from mimic spiders; the few postulated cases were with- the desert flats and foothills near Portal on S. out empirical evidence. Flies of the family Te- elaeagnifolium or adjacent vegetation. Zonose- phritidae offer a fascinating exception. Monteith mata vittigera also occurred in this area. The spi- (1972) noted the uncanny resemblance of apple ders were maintained in 6-ml vials and starved 1- maggot, Rhagoletis pomonella (Walsh) adults, to 6 d prior to testing. sympatric jumping spiders (Salticidae), as did Eis- Experiment 1: Salticid Spider Response to ner (1984) with the southwestern tephritid Zono- House Flies Versus Fruit Flies. On 14 July, 19 semata vittigera (Coquillett). Although these mim- spiders were isolated in 1-liter glass jars containing icry patterns were very apparent, the significance two dry sticks and a S. elaeagnifolium stem (13 of this phenomenon remained untested until Greene cm long). After a 30-min acclimation period, each et al. (1987) and Mather & Roitberg (1987) pro- of 10 jars received a specimen of M. domestica; vided evidence that spider mimicry in the Te- the other nine were given one of Z. vittigera. Fol- phritidae serves to reduce predation by salticid spi- lowing fly introduction, spider-fly interactions were ders. Here we present additional confirmation of monitored for 50 min or until the spider caught this hypothesis derived from wing-painting exper- the fly.Capture d flies were immediately taken from iments and speculate on the conditions that led to the spider and removed from the jar to prevent the evolution of this mimicry. spider feeding. A second 30-min acclimation period was followed by the introduction of the alternate fly species and a second 50-min observation Materials and Methods period. The S. elaeagnifolium was periodically re- Experiments were conducted at the Southwest- placed with fresh material. Ambient temperatures ern Research Station (Portal, Cochise County, Ariz.) during tests ranged from 27 to 29°C. during July 1986. Zonosemata vittigera were ob- Experiment 2: Salticid Spider Response to Nor- served in the field and collected from their food mal and Disguised Fruit Flies. On 15 July, the plant, Solanum elaeagnifolium Cavanilles, in and same 19 spiders were tested as in Experiment 1, near Rodeo, N. Mex. Wild house flies (Musca do- except that they received either normal Z. vittigera mestica L.) were collected near refuse at the re- or flies that had been painted on the upper and lower wing surfaces with a green felt-tip marker. 1 Department of Entomology, University of Georgia, Athens, This painting completely obscured the dark wing Ga. 30602. markings, destroying the spider-leg image. Spider- 2 Institute of Ecology, University of Georgia, Athens, Ga. 30602. 3 Department of Biology, Princeton University, Princeton, N.J. fly interactions were observed for 10 min followed 08544. by a 30-min fly-free acclimation period, and then

Table 1. Response of sympatric jumping spiders when presented with house flies (M. domestica) or tephritid flies (Z. vittigera) for 50 min

Capture latency (min) Spider Species M. domestica Z. vittigera 1 Sassacus papenhoei Peck ham 2 Phidippus sp. A — — 3" Metaphidippus arizo- 3.9 — nensis (Peckham) 4 Habronattus sp. 1.0 10.9 5 Phidippus apacheanus 13.8 — Fig. 1. Posterior aspect of Zonosemata vittigera. Note Chamberlin & Downloaded from https://academic.oup.com/aesa/article/81/3/532/60805 by guest on 29 September 2021 leglike patterns on wings, and abdominal eyespots ar- Gertsch 6 Metaphidippus sp. A — — ranged in a spiderlike pattern. 7 Phidippus sp. A 1.2 7.0 8 Thiodina sp. 4.3 — 9* Habronattus sp. 4.5 44.4 a final 10-min period with the alternate fly species. 10 Eris sp. 0.5 21.0 Temperatures during tests ranged from 20 to 23°C. 11 Phidippus apacheanus 5.9 — The resulting data were analyzed using the Mann- Chamberlin & Whitney U test and a binomial test for changes Gertsch 12 Eris sp. (prob. aurantia — — with small expected frequencies (Siegel 1956). (Lucas)) 13 Thiodina sp. — — 14 Metaphidippus sp. A — — Results 15 Phidippus apacheanus 0.3 8.6 Chamberlin & Appearance and Behavior of Z. vittigera. Eis- Gertsch ner's (1984) observations were quickly confirmed. 16" Phidippus sp. B — _ In nature, Z. vittigera resembled jumping spiders. 17 Phidippus sp. B 2.3 — 18C Phidippus apacheanus 0.2 19.0 The wings possessed dark lines (Fig. 1), which, Chamberlin & because of the translucence of the rest of the wing, Gertsch appeared as legs. This salticid image was further 19 Phidippus sp. B 23.8 15.3 enhanced by dark abdominal spots (arranged in a x ± SD 5.14 ± 7.00 18.03 ± 12.74

pattern resembling spider eyes), and a proclivity a to rotate the wings outward and upward. This ro- Spider backed away from wing-rotating Z. vittigera. b Spider responded to Z. vittigera with a threat display then tation caused the dark wing lines to move up and backed away. down in a manner resembling the foreleg threat c Spider responded to Z. vittigera by repeatedly signaling with or courtship displays common to salticids (Foelix first one leg then the other. 1982, Jackson 1982b,c,d, Witt & Rovner 1982). The flies were in nearly constant motion on both to Z. vittigera wing flicks, some spiders performed the upper and lower S. elaeagnifolium vegetation behaviors similar to salticid sexual or aggressive surfaces, exhibiting short, jerky locomotory move- displays (Tables 1 and 2); the front legs were jerked ments reminiscent of the stereotypic movements upward, or moved in a repetitious manner, and of jumping spiders. They generally remained with- the whole prosoma was lifted up, exposing the che- in the S. elaeagnifolium vegetation, making sud- licerae. Such displays were never elicited by house den short flights from adjacent leaves or stems and flies or wing-painted Z. vittigera. Courting of spi- occasionally to adjacent plants. ders by male fruit flies did not result in predation. In the laboratory both sexes, but particularly In the two cases when male flies landed on spiders, males, increased wing flicking in response to the the spiders became highly agitated and attempted presence of other small objects such as other te- to escape. phritids, house flies, or spiders. During the exper- Experiment 1: House Flies Versus Normal Fruit iments, male Z. vittigera sometimes "courted" Flies. During the 50-min observation period, 12 jumping spiders by facing them and moving back out of 19 M. domestica were captured, whereas and forth sidewise while rotating their wings. Twice, significantly fewer (7 out of 19; binomial test for male flies actually flew onto the backs of spiders changes, P = 0.031) Z. vittigera were taken (Table but immediately decamped and flew away. 1). In addition, the salticids required a significantly Salticid Behavior in the Laboratory. During longer time (18.0 ± 12.7 min versus 5.1 ± 7.0 min; successful prey capture, salticids oriented toward Mann-Whitney U = 10, P < 0.01) to make the Z. and stalked flies, then at a distance of 1-6 cm, made vittigera captures, indicating a reluctance to at- a short leap that ended in prey capture. This se- tack. Half the M. domestica captures took place quence was typical of house fly encounters. How- in less than 2.5 min, whereas none of the Z. vittigera ever, most salticids failed to attack normal Z. vit- captures occurred before 7 min had elapsed. In tigera, and instead backed up or rotated and faced, response to Z. vittigera, two spiders displayed and but did not advance toward, the prey. In response three backed away (Table 1). 534 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 81, no. 3

Table 2. Jumping spider response to unpainted (nor- and that this mimicry reduces attack from this mal) and wing-painted Z. vittigera during 10-min trials predacious group. Capture latency (min) We feel that spiders mistook the tephritid flies for other jumping spiders. Salticid spiders are well Spider Species Normal Wing-painted known to use vision in both hunting and courtship Z. vittigera Z. vittigera (Land 1969, Forster 1979,1982,1985, Foelix 1982). 1 Sassacus papenhoei — Some can distinguish prey or conspecific spiders Peckham 2 Phidippus sp. A — — from 20 cm away (Jackson & Blest 1982). Jumping 3° Metaphidippus arizo- — — spiders generally do not attack other salticids (Crane nensis (Peckham) 1949, Foelix 1982). Such behavior could be mal- 4 Habronattus sp. — 7.8 adaptive, because attackers risk becoming prey. 5 Phidippus apacheanus — — Instead, jumping spiders often signal one another Chamberlin & Downloaded from https://academic.oup.com/aesa/article/81/3/532/60805 by guest on 29 September 2021 Gertsch during both interspecific and intraspecific con- 6 Metaphidippus sp. A — — frontations (Crane 1949, Drees 1952, Jackson 7 Phidippus sp. A — 3.6 1982b,c,d, Krafft 1982, Witt & Rovner 1982). A 8 Thiodina sp. — — major feature of conspecific recognition in salticid 9 Habronattus sp. — — 10°b Eris sp. — — spiders is leg shape and movement (Drees 1952). 11 Phidippus apacheanus — — In fact, jumping spiders possess retinal feature de- Chamberlin & tectors, highly adapted for the resolution of leglike Gertsch 12 Eris sp. (prob. aurantia — — images (Barth 1985). (Lucas)) It is not surprising, then, that the spiders re- 13" Thiodina sp. — — sponded to the tephritid flies as if they were other 14 Metaphidippus sp. A — — spiders. As we have shown, the appearance and 15 Phidippus apacheanus — 2.7 behavior of Z. vittigera mimics that of jumping Chamberlin & Gertsch spiders. They are similar in size, possess false eye 16° Phidippus sp. B — 1.3 spots on the abdomen, move in a jerky fashion, and 17 Phidippus sp. B — — make short flights that resemble spider jumps to 18 Phidippus apacheanus 3.1 0.0 nearby vegetation. Most important are the dark leg Chamberlin & Gertsch images on the wings and the proclivity for wing 19° Phidippus sp. B — 9.0 flicking which causes the leg images to move in a f ± SD 3.1 4.07 ± 3.59 manner similar to that of a displaying salticid.

0 How could such a mimicry phenomenon evolve? Spider backed or moved away from wing-rotating Z. vittigera. One possible route is through sexual selection for b In response to an unpainted Z. vittigera, spider gave an aggressive display. wing markings. Males in some families related to tephritids (such as Drosophilidae) court females by walking near them while vibrating their wings Experiment 2: Normal Versus Painted Fruit (Manning 1960, Spieth 1974, Cobb et al. 1986, Flies. During these 10-min trials, significantly few- Crossley 1986). Species in other related families er normal Z. vittigera were taken (1 out of 19) such as the Diopsidae, Otitidae, Platystomatidae, versus painted Z. vittigera (12 out of 19) (binomial Sepsidae, and Sciomyzidae use their colored wings test for changes, P = 0.031) (Table 2). Mean capture in visual courtship, lekking, and territorial displays time for the painted flies was 4.1 ± 3.6 min, where- (Burk 1981, Thornhill & Alcock 1983, Yoon et al. as the one normal Z. vittigera was taken in 3.1 min. 1983, Kuba & Koyama 1985, Pont 1987). During Spider 10 performed a threat display in response courtship encounters, tephritids produce both to a wing flicking Z. vittigera, and five spiders acoustic and visual wing signals (Prokopy & Bush moved away from advancing Z. vittigera (Table 1973, Zwolfer 1974, Burk 1981, Smith & Prokopy 2). Spider 19 stalked a Z. vittigera as if to attack. 1982, Robacker & Hart 1985, Sivinski & Webb After closing to within 1 cm, the fly flicked its wings 1985, 1986, Dodson 1987). It it thus possible that and the spider immediately backed away. visual wing markings in these flies arose to serve an intraspecific communicatory function (Zwolfer 1974). Indeed, in certain drosophilids, males pos- Discussion sessing dark apical wing patches enjoy a greater Our results show that spiders captured fewer Z. mating success (Singh & Chatterjee 1987). vittigera than house flies. Moreover, they took lon- Because salticids are common (sometimes dom- ger to catch Z. vittigera than house flies and backed inant), predators in trees and herbaceous foliage away or gave threat or courtship displays to Z. (Reichert & Lockley 1984), they undoubtedly rep- vittigera but never to Musca domestica or painted resent a strong selective force, possibly driving the Z. vittigera. Although spiders avoided attacking evolution of spider mimicry in tephritids. Thus, normal Z. vittigera, they did attack wing-painted dark wing lines in tephritids probably evolved to Z. vittigera, demonstrating that a spider-deterrent serve an intraspecific function and later came to factor resides in the wings. These results strongly serve an exaptative defensive role. suggest that Z. vittigera mimics jumping spiders, This mimicry system is viable because of the May 1988 WHITMAN ET AL.: SPIDER MIMICRY IN FRUIT FLIES 535 high activity rate of Z. vittigera. Spiders have only Cobb, M., B. Burnet & K. Connolly. 1986. The struc- a few seconds to decide to attack before the fly ture of courtship in the Drosophila melanogaster moves away. Thus, the mimicry needs to be effec- species sub-group. Behaviour 97: 182-212. tive for only a short period of time at any one Crane, J. 1949. Comparative biology of salticid spiders at Rancho Grande, Venezuela. IV. An analysis location. Furthermore, jumping spiders are suc- of display. Zoologica 34: 159-214. cessful predators because they are usually unde- Crossley, S. A. 1986. Courtship sounds and behaviour tected by their prey. With Z. vittigera, however, in the four species of the Drosophila bipectinata com- predator detection is of little importance; flies spon- plex. Anim. Behav. 34: 1146-1159. taneously rotate their wings, and spiders are de- Dodson, C. 1987. The significance of sexual dimor- terred whether or not the fly is aware of their phism in the mating system of two species of tephritid presence. This is not to say that Z. vittigera never flies (Aciurina trixa and Valentibulla dodsoni) (Dip- respond to spiders. Like many tephritids (Prokopy tera: Tephritidae). Can. J. Zool. 65: 194-198. & Bush 1973, Greene et al. 1987), Z. vittigera wing Drees, O. 1952. Untersuchungen iiber die angebor- Downloaded from https://academic.oup.com/aesa/article/81/3/532/60805 by guest on 29 September 2021 flicking increases in the presence of small objects. enen Verhaltensweisen bei Springspinnen (Saltici- dae). Z. Tierpsychol. 9: 169-209. During the experiments, it was noted that some Edmunds, M. 1978. On the association between Myr- male Z. vittigera appeared to "court" spiders. marachne spp. (Salticidae) and ants. Bull. Br. Arachn. However, the courted spiders never attacked. Even Soc. 4: 149-160. in the two cases when male flies landed upon spi- Eisner, T. 1984. A flytha t mimics jumping spiders. ders' backs, the action was so quick that the spiders Psyche 92: 103-104. had little time to react. Moreover, these encounters Englehardt, W. 1971. Gestalt und Lebensweise der elicited spider escape reactions rather than pred- "Ameisenpinne" Synageles venator (Lucas). Zug- atory behavior. leich ein beitrag ziir Ameisenmimikryforschung. Zool. Anz. 185: 318-334. Mimicry of predators by their prey in order to Foelix, R. F. 1982. Biology of spiders. Harvard Uni- deter predation is essentially unknown in the ani- versity, Cambridge, Mass. mal world. Many inquilines inhabiting ant nests Forster, L. M. 1979. Visual mechanisms of hunting resemble their hosts (Wilson 1971, Kistner 1982), behaviour in Trite planiceps, a jumping spider (Ara- but this mimicry has generally not been shown to neae: Salticidae). N.Z. J. Zool. 6: 79-93. reduce ant predation. Because the inquilines usu- 1982. Visual communication in jumping spiders, pp. ally feed at the expense of the colonies, such re- 161-212. In P. Witt & J. Rovner [eds.], Spider com- lationships are often classified as aggressive mim- munication: mechanisms and ecological significance. icry. The only related example comes from plants— Princeton University, Princeton, N.J. Passiflora spp. vines produce structures that mimic 1985. Target discrimination in jumping spiders (Ara- neae: Salticidae), pp. 249-274. In F. Barth [ed.], Neu- Heliconius spp. eggs, deterring the female butter- robiology of arachnids. Springer-Verlag, Berlin. flies from ovipositing (Williams & Gilbert 1981). Greene, E., L. Orsak & D. Whitman. 1987. A te- In conclusion, these experiments further support phritid fly mimics its jumping spider predators. Sci- the hypothesis that Zonosemata vittigera adults ence 236: 310-312. mimic salticid spiders. Although dark wing pat- Hinton, H. E. 1976. Possible significance of the red terns perhaps arose as a tephritid sexual feature, in patches of the female crab spider, Misumena vatia. Z. vittigera they also serve a defense function. As J. Zool. (Lond.) 180: 35-39. far as we know this type of mimicry—resemblance Jackson, R. R. 1982a. The biology of ant-like jumping spiders: intraspecific interactions of Myrmarachne lu- of a predator resulting in reduced predation by the pata (Araneae, Salticidae). Zool. J. Linn. Soc. 76: 293- same predator—is unknown in the animal world 319. and represents a new form of mimicry. 1982b. The courtship behavior of Phidippus femor- atus (Araneae, Salticidae). Southwest. Nat. 27: 187- 195. Acknowledgment 1982c. The biology of Portia fimbriata, a web-build- ing jumping spider (Araneae, Salticidae) from We are grateful to Willis Gertsch, David Richman, Queensland: intraspecific interactions. J. Zool. (Lond.) and Vincent Roth for spider identification, and to Murray 196: 295-305. Blum, Jim Cane, Thomas Eisner, Ann Greene, Robert 1982d. The behavior of communicating in jumping Jackson, Ronald Prokopy, John Sivinski, Kathy Smith, spiders (Salticidae), pp. 213-247. In P. Witt & J. and Lenny Vincent for advice, assistance, and manu- Rovner [eds.], Spider communication: mechanisms and script review. We thank the American Museum of Nat- ecological significance. Princeton University, Prince- ural History (New York) for use of the facilities at the ton, N.J. Southwestern Research Station (Portal, Ariz.), and the Jackson, R. R. & A. D. Blest. 1982. The distances at Theodore Roosevelt Fund for financial assistance to L.J.O. which a primitive jumping spider, Portia fimbriata, makes visual discriminations. J. Exp. Biol. 97: 441- 445. References Cited Kistner, D. 1982. The social insects' bestiary, pp. 1- 244. In H. R. Hermann [ed.], Social insects, vol. III. Barth, F. C. [ed.]. 1985. Neurobiology of arachnids. Academic, New York. Springer-Verlag, Berlin. Krafft, B. 1982. The significance and complexity of Burk, T. 1981. Signaling and sex in acalyptrate flies. communication in spiders, pp. 15-66. In P. Witt & Fla. Entomol. 64: 30-43. J. Rovner [eds.], Spider communication: mechanisms 536 ANNALS OF THE ENTOMOLOGICAL SOCIETY OF AMERICA Vol. 81, no. 3

and ecological significance. Princeton University, Singh, B. N. & S. Chatterjee. 1987. Greater mating Princeton, N.J. success of Drosophila biarmipes males possessing an Kuba, H. & J. Koyama. 1985. Mating behavior of apical dark black wing patch. Ethology 75: 81-83. wild melon flies, Dacus cucurbitae Coquillett (Dip- Sivinski, J. & J. C.Webb. 1985. The form and func- tera: Tephritidae) in a field cage: courtship behavior. tion of acoustic courtship signals of the papaya fruit Appl. Entomol. Zool. 20: 365-372. fly, Toxotrypana curvicauda (Tephritidae). Fla. Land, M. F. 1969. Movements of the retinae of jump- Entomol. 68: 634-641. ing spiders (Salticidae: Dendryphantinae) in response 1986. Changes in a Caribbean fruit fly acoustic signal to visual stimuli. J. Exp. Biol. 51: 471-493. with social situation (Diptera: Tephritidae). Ann. Manning, A. 1960. The sexual behaviour of two sibling Entomol. Soc. Am. 79: 146-149. Drosophila species. Behaviour 15: 123-145. Smith, D. C. & R. J. Prokopy. 1982. Mating behavior Mather, M. H. & B. D. Roitberg. 1987. A sheep in of Rhagoletis mendax (Diptera: Tephritidae) flies in wolf's clothing: tephritid flies mimic spider predators. nature. Ann. Entomol. Soc. Am. 75: 388-392. Science 236: 308-310. Spieth, H. T. 1974. Courtship behavior in Drosophila. Downloaded from https://academic.oup.com/aesa/article/81/3/532/60805 by guest on 29 September 2021 Monteith, L. G. 1972. Status of predators of the adult Annu. Rev. Entomol. 19: 385-405. apple maggot, Rhagoletis pomonella (Diptera: Te- Thornhill, R. & J. Alcock. 1983. The evolution of phritidae), in Ontario. Can. Entomol. 104: 257-262. insect mating systems. Harvard University, Cam- Pont, A. C. 1987. The mysterious swarms of sepsid bridge, Mass. flies: an enigma solved? J. Nat. Hist. 21: 305-317. Williams, K. S. & L. E. Gilbert. 1981. Insects as Prokopy, R. J. & G. L. Bush. 1973. Mating behavior selective agents on plant vegetative morphology: egg of Rhagoletis pomonella (Diptera: Tephritidae) IV. mimicry reduces egg laying by butterflies. Science Courtship. Can. Entomol. 105: 873-891. 212: 467-469. Reiskind, J. 1970. Multiple mimetic forms in an ant- Wilson, E. O. 1971. The insect societies. Harvard mimicking clubionid spider. Science 169: 587-588. University, Cambridge, Mass. 1977. Ant-mimicry in Panamanian clubionid and sal- Witt, P. N. & J. S. Rovner [eds.]. 1982. Spider com- ticid spiders (Araneae: Clubionidae, Salticidae). Bio- munication: mechanisms and ecological significance. tropica 9: 1-8. Princeton University, Princeton, N.J. Riechert, S. & T. Lockley. 1984. Spiders as biological Yoon, J. S., M. T. Mathew & R. E. Holman. 1983. control agents. Annu. Rev. Entomol. 29: 299-320. Biology of Euxesta quaternaria Loew (Diptera: Otiti- Robacker, D. C. & W. G. Hart. 1985. Courtship and dae). Entomol. News 94: 122-126. territoriality of laboratory-reared Mexican fruit flies, Zwolfer, H. 1974. Innerartliche Kommunikationssys- Anastrepha ludens (Diptera: Tephritidae), in cages teme bei Bohrfliegen. Biol. Unserer Zeit 4: 147-153. containing host and nonhost trees. Ann. Entomol. Soc. Am. 78: 488-494. Received for publication 1 July 1987; accepted 23 Siegel, S. 1956. Nonparametric statistics for the be- November 1987. havioral sciences. McGraw-Hill, New York.