A Tephritid Mimics the Territorial Displays of its Jumping Spider Predators

Erick Greene; Larry J. Orsak; Douglas W. Whitman

Science, New Series, Vol. 236, No. 4799. (Apr. 17, 1987), pp. 310-312.

Stable URL: http://links.jstor.org/sici?sici=0036-8075%2819870417%293%3A236%3A4799%3C310%3AATFMTT%3E2.0.CO%3B2-U

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http://www.jstor.org Wed Jan 16 17:10:06 2008 wings with a black felt-ti ped marker. were marking, nor was their ability to flee spiders ham- precise details of these stereotyped behavior- first immobiid by ch&g them at -10°C for pered. about 30 seconds. 13. This spdy was sup rted an NSERC Canada 2 displays vary intraspe~ifica"~,salticid ago- 12. To determine that pen markine' on the wing do not o ranng grant to f?D.R.%e thank L. Dill, R. nistic displays generally commence with leg- directl cause increased modty, we maintained 20 &berg, and R. Smith for reviewing the manu- flies, ib of which we marked, within a Plexiglas script. We also thank L. Dill and B. Lalonde for waving (6). cage. Mean age at death for each group did not Mer advlce and B. Lalonde for photographs. To test the effect of the wing pattern and Mann-Whimey U test). Further, 0bse~ationScon- 6,ed that flies did not behave diferently after 20 October 1986; accepted 11 Febv1987 the wing-waving display on the behavior of jumping spiders and other potential preda- tors, we transplanted wings between house flies (Mwca domestics) and Zmsmaflies (7). House fly wings are the same general A Tephritid Fly Mimics the Territorial Displays of Its size and shape as Zonaremata wings, but they lack pattern. After this operation, the flies Jumping Spider Predators retained complete movement of their wings, and could display and fly normally (Fig. 1B). Behavioral trials between jumping spiders The tephritid fly Zmmemuta vittigera (Cquillett) has a leg-like pattern on its wings and flies were conducted for 5 minutes in a and a wing-waving display that together mimic the agonistic territorial displays of glass-topped arena (8). Jumping spiders jumping spiders (Salticidae). Zmmemuta flies initiate this display when stalked by were collected on or around Zmsemata jumping spiders, causing the spiders to display back and retreat. Wing transplant host plant (silver leaf nightshade, Solanum experiments showed that both the wing pattern and wing-waving displays are elaegnifolium). Twenty jumping spiders necessary for effective mimicry: Zmsemuta flies with transplanted house fly wings and representing 11 species (9) were each pre- house flies with transplanted Zmsemuta wings were attacked by jumping spiders. sented with five treatments: normal Zonose- Similar experiments showed that this mimicry does not protect Zotwsemuta against mata, Zmsemata with other Zonusemata nonsalticid predators. This is a novel form of sign stimulus mimicry that may occur wings (sham operation), Zonusemata with more generally. house fly wings, house flies with wings, and normal house flies. Each spider OST FORMS OF MIMICRY, SUCH Many flies have dark wing markings and was presented with these treatments in a as cryptic coloration or Batesian wing-flicking displays, so Zunosemata might random order. All jumping spiders were M and Miillerian systems, confer fortuitously resemble jumping spiders, but hungry when tested: they were given water protection against a wide array of predators not gain protection from predators by these but no food for 2 days before the trial. (1). We describe a novel form of mimicry in features. If Zunosemata is in fact a jumping Individual spiders were never tested more which an organism mimics its major preda- spider mimic, it is not clear what types of than twice in one day. tor and thereby reduces the risk of being predators are deterred. Since salticids are The wing pattern had a profound effect eaten by it. A tephritid fly, by mimicking the quick and have a poisonous bite, it has been upon jumping spider behavior (Fig. 2). stereotyped aggressive behavior of one fam- suggested that a salticid mimic may be Normal Zonosemata and the sham-operated ily of spiders, can escape from spiders of this shunned by many vertebrate and control flies were attacked or killed less family but not from other predators. predators (3). fiequently than flies in the three remaining The fly Zmsemata vieera (Diptera: Another possibility, which had not been treatments (10). There was no smtisticallv ) is purported to mimic jumping suggested, is that Zmsemata displays may significant diffeknce in the jumping spider;' spiders (Araneae: Salticidae) (2, 3). Both specifically mimic salticid territorial displays, responses to the normal Zonosemata flies and sexes have dark wing bands, which resemble and be effective only against salticid preda- thi sham-operated control flies (homogene- spider legs, and false eyespots on the end of tors (4). Many salticids defend "privacy ity test, G = 3.28, P > 0.1), indicating that the abdomen. When disturbed, these flies spheresyyaround themselves. Wheri two the operation itself did not affect spider hold their wings perpendicular to the body meet they usually initially perform agonistic responses. Jumping spiders began stalking and wave them up and down (Fig. 1A); this displays (which may turn into courtship these flies within seconds after the trial resembles the agonistic leg-waving behavior displays depending upon sex and species) began. When the spider approached to with- typical of the jumping spiders. However, (5). These displays can be performed by in about 5 cm, Zonosma flies usually there have been no experimental demonstra- juveniles and adults of both sexes and occur began a vigorous wing-waving display. tions that Zmsemata is a spider mimic. within and between species. Although the response, the jumping spiders abruptly stopped stalking and waved their legs at the flies. The flies backed away in a zigzag fashion while waving their wings and flew off. Most jumping spiders made no further stalking attempts during the remaining 5 minutes. Jumping spiders were repelled from both the front and back of the flies. In

E. Gmne, De amnent of Biology, Princeton Universi- ty, Princeton, b08544. L. J. Orsak, Institute of Ecology, University of Georgia, Flg. 1. (A)A female Zmnnata vitt&cra beginning its wing-waving display toward a stalking jumping Athens, GA 30602. D. W. Whirman, Biol and Population Man- spider (Phidippw qacheanw). The jumping spider stopped stalking, waved its legs at the fly, and then agement Research LaboratoV~.s.Dqamnent of retreated. (B) A Zaosnnata a'tt&cra fly with transplanted house fly wings. Such flies can display "culture, Agricultural R-ch Service, P.O. Box 7%; normally and fly. Tifton, GA 31793.

SCIENCE, VOL. 236 A B C D E and normal house flics). Of particular intcr- Table 1.Capture times for three fly treatments by est, Zonosernata with house fly wings dis- potential predators of Zonosemata. The fly treat- ment symbols arc the same as for Fig. 2. For each played identically to normal Zonosenzata predator there is no statistically significant differ- flies, but this never elicited the leg-waving ence between treatment medians (painvise Mann- displays from spiders, and all but one were Whitney U tcsts, all Ps > 0.05). attacked or killed. House flies with Zonose- Median nzata wings held the wings flat over their Fly Range capture treat- ple (scc- bodies: the pattern was not visible to spi- time ment onds) ders, which never displayed toward these (n) (seconds) flies. To determine if these displays also pro- Nonsalticid spzder Oxyopes salt~cus A 10 80 16-207 tected Zonosernata flics against other potcn- 6: 10 77 32-149 tial prcdators, we performed similar expcri- E 10 56 32-292 mcnts using nonsalticid spiders (Oxyopes sal- ticus), mantids (Mantis rel&iosa), assassin Assassin bufi Pselliopus zebra bugs (Pselliopus zebra), and whiptail lizards A 8 234 39-632 C 8 309 52-889 (Cnernidophorous uniparens; Arizona Re- E 8 162 34-736 search Permit 089). All predators wcre caught on or around the host plant of Mantis Mantis rcligiosa Zonosernata. These predators were presented A 12 88 29-435 C 12 64 11-215 Fig. 2. Behavioral responses of jumping spidcrs to with three fly treatments (A, C, and E of E 12 94 41-341 fly presentations. The response is the highest level Fig. 2). The same testing protocol was used of aggression attained during 5 minutes of behav- except that the test chamber sizes were Wh$tail liza~dCnemidophorous uniparens ioral interaction in a test arena. The fly treatments varied to accommodate the different sizes of A 10 101 47-355 arc: A, normal Zonosemata; R, Zonosemata with these predators (11 ). C 10 81 24-370 %)nosenzatawings glued on (control for the opera- E 10 92 9-1 19 tion); C, Zonosemata with housc fly wings; D, The Zonosenzata display is not effective house fly with Zonosemata wings; and E, normal against these four types of prcdators (Table house fly. Sample sizes arc 20 for each fly treat- 1). None wcrc deterred by displaying flies, ment. The bars connect homogeneous groups (G tcsts, P's > 0.1). All other combinations are het- as occurred with jumping spiders. For each ior, since refinements of displays that de- erogeneous (all P's < 0.01 ). predator, there was 110 statistically signifi- terred jumping spider attacks could confer cant difference in capture times for the three large survivorship advantages. A cursory six trials the jumping spiders stalked from treatment groups (pairwise Mann-Whitney glance at a museum drawer of flics reveals behind, apparently ~o6servedby the fly. U tests, all P's > 0.05). many with leg-like wing patterns. Thus, The flies gave spontaneous wing-flicks In summary, Zonosemata is a specialized jumping spider mimicry may be a wide- (about one series in 10 seconds). The jump- mimic. Rather than conferring protection spread phenomenon among many species of ing spiders stopped stalking, waved thEir against many types of visual prcdators, this flies. Analogous defenses might be expected legs, and backed away. jumping spider mimicry is effective only in other that are also highly apparent However, not all Zonosemata flies with the against jumping spidcrs. The neurological to a specific class of prcdators. wing pattern were immune to jumping spi- mechanism of this mimicry is clear: jumping der attacks: of the 40 Zonosemata in treat- spidcrs possess feature detectors in the retina REFERENCES AND NOTES ments A and K, 2 wcre attacked, and 8 of their central anterior-median eyes which 1. M. Edmunds, 1)efenc~in : A Sun~cyoj'Anti- I'redntorlIefEnces (Longman, Essex, 1974). others were killed. This is partly a reflection arc excited by waving leg-like patterns (12). 2. T. Eisncr, Nat. Hist. 112, 103 (1984). It has bccn of the conservative bias used in classifying Model presentations to salticids have shown suggested that other tephritids in the Hhn~oletis pommella s ccies group reseniblc jumping spidcrs the behavioral responses: spiders were that leg-like patterns are potent releasers [A. C. Hofson, Ext. Polde~Minn. A~tic.Ext. SEW. scored on their highest level of aggression that cause jumping spidcrs to abruptly stop 122 (1944); L. G. Monteith, Can. Entomol. 104, 257 (1972); G. L. Rush, cited in T. Eisncr (3, p. during" the 5-minute ex~xriment.Of these what they are doing (usually stalking) and 1 n4)1 ten flics that were attacked, six probably display back (13). Thus, the Zonosemata would have escaped if unconfined since they display mimics a sign stimulus recognized observed that jumping spidcrs sce~nedto avoid thi repeatedly displayed and repelled attacks (a by salticids but not by other predators. This tephritid fly Rha&~tis pomonella, but he did not mean of 2.1 effective displays). Also, even propose a mechanisn~. accounts for the extreme specificity of the 5. R. R. Jackson, in Spider (:ommunicatwn: Mechanisms though they were eventually attacked, the protection: other examples of sign stimulus and Ecolu&al S&n$cance, P. N. Witt and J. S. flies displaying with patterned wings were mimicry arc cffcctive against a similarly nar- Rovner, Eds. (Princcton Univ. Press, Princeton, NJ, 1982), PI) 213-247. aEorded some ~rotection:the latencv to the row range of signal receivers (14). 6. L. Forster, in Spider Communication: Mechanisms first attack was longer for these six flies How could this mimicry syndrome have and Ecolo~ical S&nzficance, P. N. Witt and J. S. Rovner, Eds. (Princeton Univ. Press, Princcton, NJ, than for Zonosenzata flies with house fly evolved? Wing markings and wing-flicking 1982), PI) 161-212. wings (median latency was 44 seconds ver- displays arc common among acalyptrate 7. Zonosemata flics wcrc obtained by gently swcep- netting the host plant, silver leaf ni hnhade (Sola- sus ll seconds; Mann-Whitney U = 61, P flies, and are especially prominent in the num elaegn$dium). Flies were coltckd between < 0.005). The remaining four flies were courtship displays of tephritid flics (15). 15 June and 5 August 1986, along State Line Road near Rodeo, NM, and briefly maintained in a 2 by 1 attacked so quickly they had no chance to Salticids can occur at very high densities, by 1 nl terrarium that contiined potted nightshade display. and they can exert strong predation pres- and water, dq powdered milk, and a honey and watcr solution. Flies wcre cooled in a refrigerator In contrast, the spiders responded much sures on many insects, such as tephritid flies, until inactive, thal held immobile on an operating more aggressively &ward the three other that spend time on exposed vegetation (16). board with paper strips and insect pins. Their wings types of flies (Zonosemata with house fly were cut off distal to a line connecting the nicdial cell It is possible that the defensive display of and the intersection of veins KLtiand &, (Cmnl- wings, house flies with Zonosenzata wings, Zonosernata derived from courtship behav- stock terminology). Wings from donor flies wcre http://www.jstor.org

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You have printed the following article: A Tephritid Fly Mimics the Territorial Displays of its Jumping Spider Predators Erick Greene; Larry J. Orsak; Douglas W. Whitman Science, New Series, Vol. 236, No. 4799. (Apr. 17, 1987), pp. 310-312. Stable URL: http://links.jstor.org/sici?sici=0036-8075%2819870417%293%3A236%3A4799%3C310%3AATFMTT%3E2.0.CO%3B2-U

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14 Aggressive Mimicry in Photuris Fireflies: Signal Repertoires by Femmes Fatales James E. Lloyd Science, New Series, Vol. 187, No. 4175. (Feb. 7, 1975), pp. 452-453. Stable URL: http://links.jstor.org/sici?sici=0036-8075%2819750207%293%3A187%3A4175%3C452%3AAMIPFS%3E2.0.CO%3B2-T

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