Download Moniliformis moniliformis Increases Cryptic Behaviors in the Cockroach Supella longipalpa

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 .
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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
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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.
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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-
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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
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