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Moniliformis moniliformis Increases Cryptic Behaviors in the Cockroach Supella longipalpa Author(s): Janice Moore and Nicholas J. Gotelli Source: The Journal of Parasitology, Vol. 78, No. 1 (Feb., 1992), pp. 49-53 Published by: The American Society of Parasitologists Stable URL: http://www.jstor.org/stable/3283684 . Accessed: 04/05/2013 10:57 Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at . http://www.jstor.org/page/info/about/policies/terms.jsp . JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected]. . The American Society of Parasitologists is collaborating with JSTOR to digitize, preserve and extend access to The Journal of Parasitology. http://www.jstor.org This content downloaded from 132.198.40.214 on Sat, 4 May 2013 10:57:24 AM All use subject to JSTOR Terms and Conditions J. Parasitol., 78(1), 1992, p. 49-53 ? American Society of Parasitologists 1992 MONILIFORMIS MONILIFORMIS INCREASESCRYPTICBEHAVIORS IN THECOCKROACH SUPELLALONGIPALPA Janice Moore and Nicholas J. Gotelli* FortCollins,Colorado80523 Departmentof Biology,ColoradoState University, We measuredthe behavioral responses of the domiciliary pest cockroachSupella longipalpa to infectionby the archiacanthocephalan Moniliformismoniliformis.In blackand whitebehavioralarenas,infected animals spent significantlyless time on white horizontalsurfacesthan did controls. Use of black horizontal, black vertical, and white vertical surfaceswas not affectedby parasitism,althoughuse of these surfaceswas affectedby white vs. red light. In a separateexperiment,there was no effectof parasitismon the percentageof time animalswere active, the total distancetraveled,or the averagevelocity duringtime of travel. Activity and distance traveledby both control and parasitizedanimals were reducedsharplyin white vs. red light. In responseto directed light (phototaxis),control and parasitizedanimals did not differ in the direction of movement. However, control animalswere more likely to move in responseto directionallight (photokinesis) than wereparasitizedanimals.Finally,whenoffereda choice of shadeor light (photophilia),therewas a tendency for parasitizedanimals to spend more time in shade than controls. IfS. longipalpais a naturalintermediatehost, these crypticbehaviorsareunlikelyto increasethe transmission of M. moniliformisthroughpredation.This is the first report of an acanthocephalaninfection that decreases host conspicuousnessto visual predators. ABSTRAcr: The propensity of acanthocephalans for altering intermediate host behavior is well documented (Moore, 1984). Among these hosts, the American cockroach, Periplaneta americana, has been shown to increase activity and positive response to light when infected with Moniliformis moniliformis (Moore, 1983; Wilson and Edwards, 1986; Edwards, 1987). We report here the behavioral responses of the domiciliary brownbanded cockroach, Supella longipalpa, to parasitism by M. moniliformis. Cochran (1982) reviewed the natural history of S. longipalpa, a small (10-14 mm) cockroach of African origin that is now cosmopolitan. In houses, it tends to be distributed more widely than some other domestic species, and it can use nutrients that are not limited simply to the kitchen (e.g., wallpaper paste). Although often considered a tropical or subtropical species, it colonizes dwellings readily; introduced in Florida early in the twentieth century, it had spread to 47 states by 1967. Moniiformis moniliformis has not been reported from naturally infected S. longipalpa, but this may merely reflect lack of parasite surveys of this cockroach species. Supella longipalpa habitat is similar to that of P. americana and Blattella germanica, and S. longipalpa may well be exposed to M. moniliformis eggs in the same way. In this study we compare the behavioral responses of infected and uninfected cockroaches. Our laboratory experiments tested for effects of parasitism on substrate orientation, color choices, open field activity, and photic responses. MATERIALS AND METHODS Infection and maintenance Moniliformismoniliformisexhibits a typical acanthocephalanlife cycle, involving a rat definitive host and a cockroachintermediatehost. Development to infective cystacanth in the cockroach takes 7-8 wk (Moore, 1946; Olsen, 1974). According to Schmidt (1964), Moniliformishas been reportedfrom naturally infectedP. americana.To our knowledge,wild S. longipalpa has not been surveyed for acanthocephalans. We were able to infect a rat with cystacanthsfrom S. longipalpaand recovermatureworms, includinggravid females, almost 10 wk later. This experimentconfirms that M. moniliformiscan successfullycomplete its life cycle with S. longipalpaas an intermediatehost. Supella stock was acquiredfrom D. Cochran,Virginia PolytechnicInstituteand State University, and was maintainedin the laboratory(22 C, 50%RH, 12: 12 LD photoperiod) in Plexiglas containers, provisioned with Agwayrat chow and cotton-stopperedwater vials. A total of 20-40 adult males was taken randomly from the stock cultureand provided with only waterfor 5 days. They then werecombined (disrupting any dominancehierarchiesthat might influenceaccess to food), randomlyassignedto parasitizedand control treatments,and given applesauce;in the case of the infectedtreatment,this containedM. moniliformiseggs. Roachesthen weremaintainedas beforefor 8 wk until infections matured. Received 21 March 1991; revised 16 July 1991; acBehavioral arenas cepted 28 August 1991. * Department of Zoology, University of Oklahoma, The polyurethanearenaswere 30.5 cm deep and 61 cm in diameter, with the top 2-3 cm lubricated to Norman, Oklahoma73019. 49 This content downloaded from 132.198.40.214 on Sat, 4 May 2013 10:57:24 AM All use subject to JSTOR Terms and Conditions 50 THEJOURNAL OFPARASITOLOGY, VOL.78, NO.1, FEBRUARY 1992 prevent escape. Observationswere performedon individual cockroachesbetween 1 and 3 hr after scotophase commencement;cockroachesare more active at this time (Roberts, 1960; Barth, 1964). No cockroach was tested more than once per day. Acclimation periods were 20 min (15 min for phototaxis).Sequential observationswere made every 15 sec for 15 min; each roach furnished60 observationsper test. Arenaswere cleaned with a spongeand 10%ethanol betweentests. Parasiteintensity was determinedby dissection upon completion of behavioraltests. Substrateand activity tests were conducted under red light (4 25-W red bulbs; 350 lux) and white light (4 GE CHROMALINEfull-spectrumbulbs; 700 lux). Arenas were positioned so that shadows did not fall on arena floors. The walls and floor of the substrate arenawere half blackand half white, and we recorded color (black/white)and orientation (horizontal/vertical). The fractionof time on each of the 4 surfaceswas the responsevariable. A grid of 5-cm squareswas drawn on the floor of the whiteactivityarena.A pairof cartesiancoordinates was associatedwith each squareand recordedfor each observation.In the caseof animalson verticalsurfaces, the coordinatesof the nearestgrid squarewere recorded. These coordinatedata were convertedto total distance moved (cm), mean velocity (cm/sec) for those observationsthat involved movement,and proportion of observationsthat recordeda shift in location. Photophiliatests (presencein light vs. shade) were performedin a blackarenaunderwhite light. One half of the arenawas coveredby a blackpolyurethanesheet 15.2 cm above the arena floor; this height provided shadebut did not confounda preferencefor shadewith positive thigmotaxis. Phototaxismeasurements(movementtowardslight) wereconductedin a whitearena.The animalwasplaced in the centerof the arenaunder an opaque, 5-cm (diameter) cup with lubricatedinside walls. The acclimatization period was under red light except for the last minute, when a white lightbulbon the upperedge of the arenawas lit. The cup was lifted rapidlyat the beginningof the test. Freezetime for each animal was the time in seconds betweenthe cup removaland animal locomotion. Direction of movement is reflected in a score for each animal rangingfrom 0 (movement directly toward the light) to 6 (movement 180*away from light). Animals that managedto climb the walls of the cup or to fall on their backswere tested another day. Statistical tests Our experimentswere designed to evaluate the simultaneouseffectsof lightandparasitismon cockroach behavior. For each behavioralresponse variable, the statistical design is a repeated measures analysis of variance because each animal was tested separately under red and white light. The within-subjectsfactor is light (red or white), and the between-subjectsfactor is parasitism(controlor parasitized).This designtakes into accountthe factthateach animalwas testedunder both red and white light. To test for the effectsof parasiteintensityon behavior, we calculatedthe correlationcoefficient(Pearson's r) between maturecystacanthnumberand behavioral scores of parasitizedanimals. We used a chi-square analysisto determinewhethermovement was affected by parasitismin the phototaxisexperiment. Percentageswere arc-sine square-roottransformed before analysis, and distance and velocity data were logarithmicallytransformedto normalizethe data. In the figureand tables, means and standarddeviations are presentedfor untransformeddata to ease the interpretation. RESULTS Responses to substrate Parasitized animals spent significantly less time on white horizontal surfaces than did controls (FI,48 = 11.31; P < 0.01, Fig. 1). However, there was no relationship between the intensity of the infection (number of cystacanths) and the use of white horizontal surfaces (r = 0.06, P > 0.50). Parasitism had no effect on the use of black vertical (F ,48 = 0.31; P > 0.10), white vertical (F,,48 = 1.17; P > 0.10), or black horizontal (FI,48 0.35; P > 0.10) surfaces. Under both red and white light, there was a tendency for parasitized animals to spend more time on vertical surfaces than controls did (Fig. 1). Control animals under red light spent the most Red Light 1.0 0.8--I 90 1 Control Parasitized 0.6 0.4 0.2 Z 0.0 D 1.0 White Light 0.8 0.6 0.4 0.2 0.0 BV WV BH WH FIGURE 1. The frequencyof substrateuse by control and parasitizedSupellalongipalpa.BV, blackvertical; WV, white vertical;BH, black horizontal;WH, white horizontal.Eachbar is an average,and the vertical line is 1 SD. Sample sizes are control = 26, parasitized = 24. Each animal was tested underred and white light on separatedays. This content downloaded from 132.198.40.214 on Sat, 4 May 2013 10:57:24 AM All use subject to JSTOR Terms and Conditions MOOREAND GOTELLI-ROACHBEHAVIORAND MONILIFORMIS INFECTION 51 TABLE I. Distance traveled,percentageof time active, DISCUSSION and average velocity for control and parasitizedSupella longipalpaunder red and white light. Standard Under simulated daylight conditions, S. londeviations are given in parentheses,and sample sizes gipalpa is a remarkably quiescent animal. For are given in brackets. instance, under white light, S. longipalpa is active less than 5% of the time (Table I). This inAverage % Time Distance velocity activity may have important consequences for active traveled (cm) (cm/sec) the extent to which S. longipalpa behavior may 27.75 1.33 337.26 Control, red light be modified by parasitism. (0.43) ([19] (30.72) [27] (381.11) [27] 435.10 1.35 36.94 In the case of response to light, for example, Parasitized, red light (30.93) [24] (361.42) [24] (0.53) ([17] freeze times exceeded 4 min for half of the con1.22 4.77 58.31 Control, white light trol animals and three quarters of infected ones. (0.62) ([5] (13.64) [27] (169.31) [27] 0.78 0.93 6.70 Parasitized, These freeze times are substantially longer than white light (0.09) [2] (3.16) [24] (27.8) [24] those of any species examined to date (Moore, 1983; Carmichael and Moore, 1991; Gotelli and time on white vertical surfaces. Under white light, Moore, 1992). In S. longipalpa, parasitism does not alter the average freeze time; it does decrease these animals spent the most time on black horthe probability that animals will move when exizontal surfaces and showed a significant shift posed to sudden light. This may not have ecoaway from white horizontal surfaces (F,,48 = 6.66; P < 0.05). The use of black vertical surfaces was logical significance, however, because the manot affected by light or parasitism. jority of animals that moved in both treatments were stationary for at least 30 sec. Under these Activity measurements circumstances, parasitism is unlikely to affect There was no significant effect of parasitism predator-prey interactions, one possible selective basis for altered behaviors (Moore and Goon the percentage of time an animal was active telli, 1990). In a similar fashion, parasite-in(F ,49 = 0.15; P > 0.10), the total distance travduced photophobia exhibited by S. longipalpa is eled (F,,49 = 0.02; P > 0.10), or the velocity unlikely to increase the conspicuousness of the during travel (F, s = 0.09; P > 0.10). Variances in these measures were large, and parasitism had cockroach to a visual predator. This shift toward cryptic behavior is seen also inconsistent effects on activity under red and in the response of parasitized S. longipalpa to white light (Table I). For uninfected animals, light had strong effects substrate color. Parasitized animals avoid white on the percentage of time active and the total horizontal surfaces. They also tend to use vertical distance traveled. These animals were signifi- surfaces more when parasitized. These behaviors cantly less active under red light than under white could present a 2-fold problem for potential light (Table I). Average velocities during time of predators: parasitized S. longipalpa may be more travel were somewhat lower under white light, difficult to see and (on vertical surfaces) more although sample sizes were limited because so difficult to catch. Of course, we do not know for certain that S. few animals were active under white light. longipalpa serves as a natural intermediate host Responses to light for M. moniliformis. This is likely, however, givFor animals that moved in response to a di- en its overlap in habitat with other natural inrected white light (phototaxis) there was no effect termediate hosts. We also do not know which of parasitism on the direction of movement (FI,19 rodent species acquire M. moniliformis in this = 0.31, P > 0.05). However, parasitism affected way. The altered behaviors would render S. lonthe probability of movement. More of the con- gipalpa less noticeable to almost any visual predtrol animals moved in response to light (14/27) ator, however, by decreasing contrast with substrate and decreasing time spent in lighted areas. than did the parasitized animals (6/26; x2 = 4.67, P < 0.05). These results stand in stark contrast to reThere was also a marginally nonsignificant ef- sponses of other cockroaches to Moniliformis infect of parasitism (FI,25 = 3.42; P = 0.07) on the fection. Comparisons with B. germanica are of response to shade vs. light (photophila). Control particular interest because the German cockanimals spent more time under light (2 = 34.0%) roach is similar to S. longipalpa in size and asthan did parasitized animals (f = 6.8%). sociation with human dwellings. Blattella ger- This content downloaded from 132.198.40.214 on Sat, 4 May 2013 10:57:24 AM All use subject to JSTOR Terms and Conditions 52 THEJOURNALOF PARASITOLOGY, VOL. 78, NO. 1, FEBRUARY1992 manica is 10-15 mm long, of African origin, and TABLEII. Effect of Moniliformismoniliformisparasitism on the behaviorof Supellalongipalpaand Blata successful colonist (Cochran, 1982). Uninfected B. germanica and S. longipalpa also exhibit tella germanica.Results from B. germanicaare summarizedfrom Gotelli and Moore (1992). similar substrate choices, especially in the time they spend on white horizontal surfaces (white S. longipalpa B. germanica light: 7% for each species; red light: approxiSubstrate Avoid white horiIncrease use of black and mately 10% and 20%, respectively). choice zontal white horizontal, decrease use of black vertiDespite these similarities, B. germanica recal sponse to M. moniliformis parasitism is comAvoid light, deNo effect Light pletely different from that of S. longipalpa (Gocrease probability responses of movement telli and Moore, 1992). Parasitized German No effect Decrease velocity, distances cockroaches increase use of white horizontal sur- Activity faces whereas parasitized brown-banded cockroaches avoid them, despite similar control re- portant as susceptibility in the potential of that sponses. Parasitism does not affect light responses species to transmit disease. Supella longipalpa is in German cockroaches whereas parasitized highly susceptible to M. moniliformis infection; brown-banded cockroaches become more cryp- 93% of exposed cockroaches developed mature tic. Finally, parasitism decreases velocity and cystacanths. Yet our results suggest that S. lontravel distance in B. germanica but has no effect gipalpa is unlikely to be important in Monilion S. longipalpa activity (Gotelli and Moore, formis transmission. Of course, this has yet to be tested in predation experiments, but given the 1992; Table II). In most cockroaches examined to date, Mo- nearly opposite responses of S. longipalpa and niliformis-induced behaviors increase visual B. germanica, they are probably not encounterconspicuousness. Activity may be altered (Moore, ing predators at the same rate. There are examples of parasitoids inducing 1983; Wilson and Edwards, 1986), and for 3 other species (Periplaneta brunnea, P. americana, cryptic host behavior (Brodeur and McNeil, and B. germanica), parasitized animals increase 1990), and these behaviors may promote paratheir use of white horizontal surfaces. sitoid survivorship. The host moves to a proAcanthocephalan infections commonly en- tected place where the parasitoid can develop hance host conspicuousness in a variety of host- and emerge. This is the first report of an acanparasite associations and often are associated with thocephalan infection that does not appear to demonstrably increased predation (Holmes and increase intermediate host conspicuousness to Bethel, 1972; Moore, 1984). Given the behav- predators and that induces crypticity instead. The ioral alterations we describe here, increased risk ecological implications of such alterations reof predation seems to be unlikely in S. longipalpa main to be investigated. infected with Moniiformis, even though S. longipalpa habitat easily could overlap with rat ACKNOWLEDGMENTS predators, as does the habitat of P. americana We thank Michael Freehling for assistance and and B. germanica. In fact, we do not know the this project. intermediate host that contributes most to M. thoughtful suggestions throughout Donald Cochran provided cockroaches, Douglas moniliformis transmission in nature. The ma- Ishii provided rats, and Terry Blasdel furnished jority of laboratory work has been done with P. M. stock. This work was supported moniliformis americana, in large part because it is easy to rear NSF BSR 8817495 to J.M. and N.J.G. and and manipulate. Other cockroaches that live near by contributions from the Monsanto Company, by Moniliformis egg sources also may be candidates. Whitehall Foundation, Exxon Education FounNonsignificant results must be interpreted caudation, and Burroughs Wellcome Fund. tiously because the large variance in the data (Table I) reduces the power of the statistical test LITERATURE CITED (Toft and Shea, 1983). Nevertheless, if consistent effects of parasitism cannot be demonstrated in BARTH, R. H., JR. 1964. The mating behavior of Byrsotriafumigata (Gubrin)(Blattidae,Blaberia controlled laboratory setting, they are unlikely nae). Behaviour23: 1-30. to be important in the field. BRODEUR, J., AND J. N. MCNEIL. 1990. Over-winVector biologists have acknowledged that the teringmicrohabitatselectionby an endoparasitoid behavioral attributes of a species may be as im(Hymenoptera;Aphidiidae):Inducedphototactic This content downloaded from 132.198.40.214 on Sat, 4 May 2013 10:57:24 AM All use subject to JSTOR Terms and Conditions INFECTION MOOREAND GOTELLI-ROACHBEHAVIORAND MONILIFORMIS and thigmotacticresponsesin dyinghosts. 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