Behavioral Ecology Vol. 10 No. 4: 351-357
© 1999 International Society for Behavioral Ecology
Evidence that the parasitic nematode Skrjabinoclava manipulates host Corophium behavior to increase transmission to the sandpiper, Calidris pusilla
a Department of Biology, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario KIS 5B6, Canada b Acadia Centre for Conservation and Wildlife Biology, Acadia University and Nova Scotia Department of Natural Resources (Wildlife Division), 136 Exhibition Street, Kentville, Nova Scotia B4N 4E5, Canada
Address correspondence to D. G. McCurdy. E-mail: dmccurdy{at}ccs.carleton.ca
Received 12 March 1998; revised 22 September 1998; accepted 10 October 1998.
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ABSTRACT |
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We found evidence that a nematode (Skrjabinoclava morrisoni) adaptively manipulates the behavior of its intermediate host (the amphipod Corophium volutator) to increase its likelihood of transmission to its final host (the semipalmated sandpiper, Calidris pusilla). We found that male and female amphipods parasitized by nematodes increased their surface activity in the field during daytime, but not during nighttime hours. Increased surface activity is known to increase susceptibility of amphipods to predation by sandpipers during the day, but not at night, when sandpipers do not feed visually. Also, as predicted by the manipulation hypothesis, only late-stage (infective) larvae of nematodes were associated with behavioral changes of amphipods. We found no evidence that parasites were associated with other amphipod behaviors in the laboratory, such as trail complexity, distance traveled, or burrow-probing activity of crawling males as would be expected if parasitized hosts altered their own behavior. Survivorship of amphipods was also unaffected by parasitism, which may favor parasite transmission. Thus, behavioral changes of parasitized hosts were simple, and their expression was context-dependent and related to likelihood of predation. We argue that maturation times of nematodes in relation to migration schedules of sandpipers provide a narrow window of opportunity and may explain why nematodes manipulate amphipod behavior.
Key words: amphipod, Bay of Fundy, Calidris pusilla, Corophium volutator, host behavior, nematodes, parasite manipulation, sandpipers, Skrjabinoclava morrisoni.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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In recent years, ecologists and evolutionary biologists have unraveled the complex interplay between some parasites and their hosts. For example, some parasites appear to alter the behavior of intermediate hosts in ways to increase their likelihood of transmission to final hosts (Holmes and Bethel, 1972
;
Moore, 1995). However, there
can be costs to manipulating host behavior (e.g., production of chemicals that
interfere with normal host behavior;
Helluy and Holmes, 1990).
Consequently, natural selection should optimize (not maximize) the timing and
amount of manipulative effort of parasites (the manipulation hypothesis).
Energy not used to manipulate host behavior could be saved or channeled into
other fitness traits, such as parasite growth or fecundity
(Poulin, 1994a).
Researchers have detailed predictions concerning timing of manipulation of
host behavior (Combes, 1991;
Poulin, 1994a;
Poulin et al., 1994).
Parasites should begin to manipulate their hosts only once they have developed
sufficiently to be transmitted successfully to the final host, as being
ingested before development of the infective stage of the parasite would
result in the parasite's death. Manipulative effort also should be likely when
parasites, prey, and predators have limited temporal overlap (e.g., migrant
birds visiting staging areas for a few to several weeks).
A major difficulty in testing for adaptive manipulation of host behavior is
in determining whether any behavioral changes in hosts are due to the
parasite, the host, or both parasite and host
(Milinski, 1990;
Poulin et al., 1994). Using
meta-analysis, Poulin (1994b)
showed that parasites, including acanthocephalans and nematodes, appeared to
alter behavior of their hosts. However, he found that manipulation occurred
less often than expected (i.e, when it otherwise would have been adaptive for
the parasite). Poulin's work suggests that many changes in behavior may be due
to phylogenetic constraints. This problem is compounded by the fact that there
are few tests of the manipulation hypotheses in natural systems in which the
ecologies of intermediate and final hosts are well understood. Factors such as
the timing of changes in (antipredator) behavior must be known in relation to
development of parasites in order to adequately test for constraints or
adaptations of parasites.
Our general objective was to test predictions of the manipulation hypothesis. In particular, we tested whether an acuaroid nematode [Skrjabinoclava morrisoni (Wong and Anderson)] could increase its likelihood of transmission to its final host (a sandpiper, Calidris pusilla L.) by altering the behavior of its intermediate host, the amphipod Corophium volutator (Pallas). To this end, we observed behavior of infected and uninfected amphipods in both the field and laboratory. We also determined if infected C. volutator show different behavioral responses in daylight versus darkness (e.g., increased versus decreased frequency of crawling, respectively). We hypothesized that nematodes should interfere with normal antipredator responses. However, these responses may be context dependent. Nematodes that, for instance, increase crawling activity of amphipods when predators are unable to use visual cues (at night) would not increase the intermediate host's probability of being ingested.
Rationale of study
For several reasons, the amphipod-nematode-sandpiper system we studied is
ideal for investigating possible manipulation of host behavior by parasites.
First, C. volutator averages 86% of the diet of sandpipers as they
stage in the Bay of Fundy (Hicklin and
Smith, 1979). Each bird may consume 20,000 or more amphipods per
day (Boates, 1980). Second,
sandpipers prefer to feed on crawling amphipods during daylight hours (usually
mate-searching males; Boates and Smith,
1989), leading to the prediction that parasites should increase
crawling activity of male C. volutator at that time to increase their
likelihood of being ingested by a final host. Although the ecology of S.
morrisoni is relatively unknown, laboratory studies and our work have
shown that C. volutator is an intermediate host for this nematode
(Wong and Anderson, 1988).
S. morrisoni completes its life-cycle in semipalmated sandpipers; the
larvae migrate to the proventriculus where they mature, mate, and release eggs
(Wong and Anderson, 1987).
Presumably, nematodes are ingested by sandpipers during their fall migration
through the Bay of Fundy (Wong and
Anderson, 1990): this supposition can be tested indirectly by
examining when natural infections of nematodes appear. In doing this study, we
provide the first description of the distribution of S. morrisoni in
a natural population of C. volutator. This is needed to address the
extent of temporal overlap among nematodes, Corophium, and
sandpipers.
Specific predictions
If behavioral alteration increases the likelihood of a nematode being
ingested by a sandpiper, then late-stage larvae of nematodes that are capable
of infecting final hosts should be found disproportionately in crawling
amphipods. If male amphipods infected with early-stage larvae show more
crawling than uninfected males, then this is unlikely to be a parasite
adaptation, but may be a host adaptation (e.g., to optimize mate-searching
effort if parasites affect future survival;
(Forbes, 1993), or it may be a
nonadaptive side effect of paratism.
We also compared crawling activity of parasitized and unparasitized
amphipods in daylight and in darkness. Little is known about the ecology of
C. volutator at night. However, sandpipers appear to switch from
visual to tactile cues to locate their prey at night (i.e., pecking versus
probing; Mouritsen, 1994;
Robert and McNeil, 1989) and
may actually feed less at night than during the day
(Boates, 1980;
Manseau and Ferron, 1991; but
see McCurdy et al., 1997). As
mentioned above, if crawling activity is greater at night in infected
amphipods, then parasites may not increase their transmission rates at that
time.
We also addressed whether nematodes affect other amphipod behaviors or
amphipod survival in the laboratory. These other behaviors were unrelated or
tangentially related to the probability of ingestion by final hosts. We
expected that parasitized males, compared with uninfected controls, might
travel a shorter distance per unit time and/or attempt to enter fewer
(artificial) burrows of potential mates. We also examined trail complexity of
male amphipods. Trail complexity can decrease if an organism is under stress
(Alados et al., 1996), thus
simpler (linear) trails may be a side effect of parasitism, although
sandpipers may follow linear trails better than complex trails. Finally, we
predicted that parasitized amphipods should be positively phototactic while
crawling, but not while swimming, as this could make them susceptible to
predation by fish (Imrie and Daborn,
1981), which are inappropriate hosts.
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METHODS |
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Field studies
We collected C. volutator from the mudflat at Starrs Point, Nova Scotia, Canada (45°08' N; 64°22' W). This 4-km wide mudflat is located within the Hemispheric Shorebird Reserve in the Southern Bight of the Minas Basin and is exposed twice daily to tides ranging from 7.5 m to 15 m (Canadian Hydrographic Service, 1980
). We chose to sample at Starrs Point because it supports
large populations of C. volutator
(Boates, 1980). In addition,
large flocks of migratory sandpipers arrive in mid-summer to forage at this
site (Boates et al., 1995;
Matthews et al., 1992). This
allowed us to compare crawling activity of amphipods and prevalence of their
nematode parasites before versus after the arrival of the sandpipers, and also
when predation by sandpipers on crawling amphipods was high versus negligible
(daytime versus nighttime hours, respectively). We made frequent trips to
Starrs Point and to nearby roosting sites throughout the month of July to
determine when migrating sandpipers arrived in 1996, 1997, and 1998. Over the
last 20 years, sandpipers have arrived from mid- to late July (Boates JS,
personal observations).
We also made 23 visits to Starrs Point (May-August) over 3 years to compare
prevalence of nematodes in crawling versus noncrawling hosts, both during the
day (1110-1450 h Atlantic Standard Time) and at night (2205-0235 h). All trips
were made on neap tides, when the mudflat is exposed for extensive periods at
night (Boates, 1980). We
sampled within eight 10x10 m plots marked with stakes and colored tape.
Each plot contained a large subpopulation of C. volutator in previous
studies (Boates et al., 1995;
McCurdy et al., 1997). Plots
were placed in four pairs (members of pairs were 15-30 m apart) along tidal
channels at 500-m intervals. This spacing allowed us sufficient time to reach
each plot before it was uncovered by the tide.
We sampled for infected amphipods primarily within the four plots located
lowest in the intertidal zone (where shorebird feeding densities were highest;
McCurdy et al., 1997).
Sandpipers did not forage in plots while plots were being sampled. We
collected both crawling males and females only in areas that had been
uncovered by the tide within 15 min. Each adult amphipod (>5.0 mm
rostrum-telson length) was placed in a 3-ml microtube filled with seawater. We
then collected two amphipods from the substrate within 10 cm of the crawling
amphipod that were of the same sex and approximate size (within 2 mm). We
placed both of these amphipods in an adjoining microtube. All three amphipods
were subsequently squashed to determine if nematodes were present (viewed at
40x magnification). Parasites were identified as early-stage larvae
(stages I and II) or late-stage larvae (stage III) using characters described
by Wong and Anderson (1988).
Although Wong and Anderson
(1988) did not describe stage
IV larvae from amphipods exposed in the laboratory, we occasionally found
larvae in amphipods which, based on their size and the extent to which the
spicules of males were developed, were best described as stage IV. We also
considered these as late-stage larvae.
We counted crawling male and female amphipods during the day and at night
(using flashlights) in 1997. To sample crawling activity before sandpiper
arrival (28 June-1 July), we placed a 0.5x0.5 m quadrat randomly within
each plot just as the water receded from it. For day trips after sandpiper
arrival (27-30 July), we used a larger 1x1 m quadrat because C.
volutator is known to greatly reduce its crawling activity at this time
(Boates et al., 1995), and we
wanted to collect at least some daytime crawling amphipods from quadrats for
comparison. Amphipods that emerged to crawl during the first 5 min after the
tide receded were collected using live-specimen forceps (most amphipods that
crawled emerged almost immediately and rarely emerged after 5 min;
Boates and Smith, 1989; McCurdy
DG, personal observations). In the laboratory, all amphipods were sexed using
the criteria of Schneider et al.
(1994) and classified as
either juveniles (<5.0 mm) or adults (5.0-12.0 mm).
Laboratory studies
To infect C. volutator with S. morrisoni experimentally
in the laboratory, we collected 91 adult male amphipods from the mudflat at
Blomidon, Nova Scotia (45°13' N; 64°22' W). Blomidon is
close to Starrs Point (<10 km) but is not visited by shorebirds
(Matthews et al., 1992). In
addition, amphipods at this site were not infected by nematodes (McCurdy DG,
unpublished data). Thus, we were able to avoid potentially confounding effects
of natural infections. We collected amphipods on 30 July 1996 and housed them
in a 1-1 container with aerated artificial seawater (Instant Ocean) at
18
(20°C).
To obtain nematode eggs, we shot 10 adult C. pusilla on 31 July 1996. We dissected each bird in the field and removed the section of its digestive tract containing the proventriculus and placed it in avian saline (8 g NaCl/l distilled water). In the laboratory, we plucked all nematodes from the proventriculus (procedure and data on infection levels available upon request). We then cut each worm into four pieces and placed these in a microtube containing avian saline and shards of cover slips. We agitated the microtube on a vortex shaker for 5 min. This method effectively teased out and separated the eggs, which we then placed in a 1-1 container filled with artificial seawater.
To help ensure adequate numbers of infected males, we took 72 amphipod
males and added them to the solution containing the nematode eggs. We then
added the cultured diatom Thalassiosira sp. (25,000 cells/ml) to
elicit the feeding response of amphipods (as the nematode eggs must be
ingested in order to develop; Wong and
Anderson, 1988). We exposed many males because we expected only
some of them to become infected, and we also needed to track the development
of the parasites, which required that we periodically dissect an exposed
amphipod. Obviously, these dissected amphipods could not be used in
experimental trials. The remaining 19 males were housed in a separate
container and fed Thalassiosira sp., but were not exposed to nematode
eggs.
After 36 h, each male was removed and placed in an individual culture tube
containing 32 ml of artificial seawater (18), 1 cm filtered mud (0.42
mm mesh), and a nonovigerous adult female C. volutator. The females
provided males with well-maintained burrows (only females construct burrows;
Meadows, 1964). We added
penicillin-G (100 ug/ml) and streptomycin sulfate (100 µg/ml) to reduce
variability in mortality and growth rate of amphipods
(Pelletier and Chapman, 1996).
Each culture tube was constantly aerated, and 10 ml of water was changed every
3 days. After each water change, we fed each pair of amphipods
Thalassiosira sp. (200,000 cells/ml). We then observed and recorded
whether males and females were on the surface or in their burrow at the
beginning of the experiment (3 days postexposure/post-nonexposure) and before
the removal of males for other experiments (after 17 days).
On 18 August, we removed all males from their culture tubes and used them in a series of experiments. First, each male was individually placed on a 30-cm pan lined with 1 cm of fresh mud. Seventy-two holes (0.2-0.3 cm diam) were uniformly excavated in the mud to simulate entrances to the burrows of female amphipods. We then placed each male in the center of the pan facing a random direction and allowed him to crawl for 5 min, during which time his path was filmed. We gently rinsed the surface of the pan with seawater between male placements to ensure that artificial burrows remained in the same locations and to minimize any influences of the previous male. We recorded trail complexity, total distance traveled, time spent crawling, the number of artificial burrows probed, and the number of burrows passed over (not probed).
We recorded phototactic responses of exposed and unexposed males while they
were crawling and swimming on 19 and 20 August (17 and 18 days
postexposure/post-nonexposure, respectively). We used phototactic chambers
based on Moore's (1983)
design. Chambers were constructed using two 25-cm Pyrex pie plates. One plate
was placed upside down on top of the other and half of the chamber was painted
black. For experiments on phototactic responses of crawling amphipods, we
lined the bottom of the chambers with fresh mud. For experiments on
phototactic responses of amphipods while swimming, we filled the bottom of the
chamber with artificial seawater (18). In each case, we placed a
cardboard divider between the light and dark sides of the plate, with a 1 cm
space remaining between the bottom of the divider and surface of the bottom
plate. This space was needed to ensure that amphipods had easy access to
either side of the plate. During each trial, we placed males, either exposed
or not exposed to nematode eggs, individually into either the light or dark
side of a chamber. We allowed males to crawl for 2.5 min or swim for 1 min,
after which we recorded the location of each male. After this, we squashed
each male to look for S. morrisoni.
Analysis
We used chi-square tests of independence to analyze data on prevalence of
nematodes in crawling and noncrawling amphipods. We transformed
[ln(x+1)] counts of crawling amphipods to correct for normality and a
lack of homogeneity of variance, assessed using Kolmogorov-Smirnov and
Bartlett's tests, respectively (Zar,
1996). Using parametric analyses of variance, we then compared
crawling activity between day versus night and before versus after sandpiper
arrival. The inferences we draw from this study apply specifically to
nematodes and amphipods from Starrs Point. Thus, we considered samples from
each plot as independent.
We used fractal analysis to compare the complexity of trails of parasitized
and unparasitized C. volutator. We used With's
(1994) variation of the
dividers method (Dicke and Burrough,
1988). First, the trail of each male was traced from a video
screen onto a transparency and scanned into Design CAD 2-D
(American Small Business Computers,
1989). Next, we generated circles of eight fixed diameters
(0.4-3.2 cm in 0.4-cm intervals) and overlaid them on each trail (as in
With, 1994). We then tallied
the number of circles required to completely cover each trail to calculate the
total path length of the trail (circle diameter x number of circles
used). Finally, we calculated a fractal dimension (D) for each trail
by plotting the natural logs of the circle diameters by their corresponding
total path lengths and subtracting the resulting line-of-best-fit from 1.
D values may range between 1 and 2 (1 represents a perfectly straight
line; 2 describes a line so complex that it fills the entire plane).
We used a multiple analysis of variance (MANOVA) to examine whether
multivariate measures of behavior based on trail complexity, total path
length, time spent crawling, number of artificial burrows probed, and number
of burrows not probed differed between parasitized and unparasitized
amphipods. Each response variable was recorded over a single 5-min period. We
used MANOVA over a series of univariate tests to reduce the probability of
finding a significant result by chance and because we expected that the
dependent variables were correlated. Due to the relatively small sample size
of the control group (n<20), we used univariate tests to verify
that data met assumptions of normality and homogeneity of variance
(Mardia, 1980;
Scheiner, 1993). The
statistical software package Statistica 4.3D
(Statsoft Inc., 1993) was used
for all analyses, following Zar
(1996).
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RESULTS |
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Nematodes and crawling amphipods (field results)
We present results on crawling activity of uninfected male and female amphipods during day and night first because these results influence some of the predictions concerning crawling of infected animals. We found no significant difference in the mean number of male amphipods crawling between day and night before sandpiper arrival in 1997 (F1,28 = 1.98, ns). However, there was a significant decrease in crawling daytime activity of males after sandpiper arrival (F1,28 = 44.59, p <.0001; Figure 1). In comparison, the mean number of nighttime crawling males did not change after sandpiper arrival (F1,28 = 1.35, ns). Accordingly, the numbers of crawling males were far higher at night than during the day after sandpiper arrival (F1,28 = 53.10, p <.0001). As with males, we found no significant difference between the mean number of crawling females during the day and night before sandpiper arrival (F1,28 = 1.28, ns; Figure 1). After sandpiper arrival, however, more females were observed crawling at night than during the day (F1,28 = 16.21, p <.0005).
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To obtain data on the distribution of S. morrisoni in natural
populations of C. volutator, we examined 1153 crawling amphipods and
2060 amphipods from the substrate (Table
1). We found that nematodes were present only in samples collected
from mid-late August in all 3 years of study. Within these time periods during
the day, we found that crawling amphipods were more likely to be infected with
nematodes than amphipods removed from the substrate (males: 
2
= 10.33, df = 1, p <.005; females: 2 = 6.70, df =
1, p <.01). On trips at night during this time, however, we found
no significant difference in prevalence of nematodes between amphipods that
were crawling or present in the substrate (males: 2 = 0.26, df
= 1, ns; females: 2 = 0.001, df = 1, ns). Male and female
amphipods were equally likely to be infected by nematodes (2 =
0.52, df = 1, ns).
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In considering developmental stages of parasites, we found that a higher
proportion of amphipods crawling on the surface during the day were
parasitized by late-stage (infective) nematode larvae than amphipods collected
from the substrate (2 = 26.10, df = 1, p <.0001).
However, crawling amphipods were no more likely to be infected by early-stage
nematode larvae than those collected from the substrate (2 =
2.35, df = 1, ns). There was no significant difference in the proportion of
amphipods infected by early- or late-stage larvae in crawling versus substrate
samples taken at night (late-stage larvae: 2 = 0.03, df = 1,
ns; early-stage larvae: 2 = 0.48, df = 1, ns).
Behavior and survival of male amphipods (laboratory results)
In the laboratory experiment, all 72 males exposed to eggs of S.
morrisoni became infected by third-stage larvae (mean±SD intensity
= 13.7±7.0). By examining exposed males that died during the
experiment, we determined that it took about 13 days for nematodes to develop
into stage III larvae in the laboratory. Nine males died during the course of
the experiment and all were infected by nematodes; however, survivorship over
the experiment did not differ significantly between the infected and
uninfected amphipods (2 = 2.64, df = 1, ns). In addition,
there was no significant difference in the size of infected and uninfected
males at the end of the experiment (t = 0.74, df = 78, ns). In
examining behavior, we found no significant difference in the number of
parasitized versus unparasitized males on the surface at the start of the
experiment (3 days postexposure/post-nonexposure: 2 = 1.39, df
= 1, ns), but significantly more parasitized than unparasitized males were
recorded on the surface when checked 18 days postexposure/post-nonexposure
(2 = 7.56, df = 1, p <.01;
Figure 2). By this time,
nematodes had developed into their infective stage.
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From film analysis, we found no significant differences between parasitized
and unparasitized males in mean complexity or total length of trails, time
spent crawling, number of burrows probed, and number of burrows passed over
during a 5-min period (Wilk's 
= 0.95, n = 83, ns;
Table 2). With respect to
phototactic responses, we found no significant difference between parasitized
and unparasitized amphipods while crawling (2 = 0.03, df = 1,
ns; 87% of parasitized and 88% of unparasitized amphipods used the dark side
of the chamber) or swimming (2 = 1.24, df = 1, ns; 84% of
parasitized and 72% of unparasitized amphipods used the light side of the
chamber).
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DISCUSSION |
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Nematodes and crawling amphipods
Our results verify that C. volutator is an intermediate host for S. morrisoni in a natural population. Parasites infected only the summer generation of amphipods (June-September) and did not overwinter in the fall generation. Either these amphipods were not infected or, if infected, amphipods did not survive to be sampled in the spring. Development time for nematodes in amphipods was 4-5 weeks in the field because sandpipers began to arrive in mid- to late July and late-stage larval parasites did not begin to show up in field collections until mid-August. This means that the parasite only has a short time to complete its life cycle because most of the migratory sandpipers remain in the Bay of Fundy for only 4-6 weeks (Boates, 1980
). Furthermore,
there is limited opportunity for transmission of nematodes because most of the
potential intermediate hosts are from the summer generation which does not
survive until the return of sandpipers the following summer
(Matthews et al., 1992;
Peer et al., 1986). We never
found nematodes in amphipods collected at a nearby mudflat where sandpipers do
not feed (n = 516; McCurdy DG, unpublished data) which suggests that
sandpipers are the only final hosts for S. morrisoni.
We suggest that adaptive manipulation by parasites, and not a host
response, was responsible for the increased daytime presence of infected hosts
on the surface of the mud. Manipulation of host behavior is likely for this
system because passive transmission rates for parasites that infect amphipods
that remain in the substrate are likely low, as overall numbers of substrate
amphipods at Starrs Point are high (>10,000/m2;
McCurdy et al., 1997). Our
results further support the manipulation hypothesis because we found that only
late-stage/infective parasites were more often found in crawling than in
substrate-dwelling male and female amphipods during the day. The fact that
infected females were more likely to crawl than uninfected ones provides
strong evidence in support of parasite manipulation because uninfected females
rarely crawl (< 1%, Boates et al.,
1995; this study), and such increases are likely nonadaptive for
females (Forbes et al.,
1996).
We predicted context-dependent changes in parasite manipulation of host behavior (i.e., parasites should not manipulate crawling effort at night because this could be maladaptive for the parasite). Our results are consistent with this because males and females were no more likely to be found crawling than in the substrate at night.
Behavior and survival of male amphipods
Our laboratory results also support the idea that nematode parasites
adaptively cause amphipods to be more susceptible to predation by birds.
Specifically, we found that infected males were more likely to be on the
surface, but only after the parasites had developed to their infective stage.
Similar results were found in laboratory experiments by Mouritsen and Jensen
(1997), who observed that
C. volutator infected by the trematode Maritrema subdolum
Jaegerskioeld were observed more often on the surface of the mud than in the
substrate. We did not find other differences in crawling activity of males,
even though amphipods had intensities of infection that were much higher than
those recorded from our field collections. We also found no difference in
phototactic behavior between infected and uninfected amphipods housed in the
laboratory. One possible explanation for this is that parasites manipulate
responses of amphipods to natural cues that were absent in the laboratory
(e.g., sandpiper feeding cues or tidal cues can effect responses by C.
volutator). Alternatively, manipulation of only one behavior that
increases the susceptibility of amphipods to final host predators would be an
efficient use of resources for the parasite, if specific manipulations are
costly. Additionally, the relation between these other behavioral changes and
susceptibility to predation was less obvious, and any alterations could
reflect host decisions rather than parasite manipulation.
Nematode larvae reached their infective stage (stage III) faster in the
laboratory (13 days) than in the field (4-5 weeks). Our results agree with
those of Wong and Anderson
(1988), who also found that
development time of S. morrisoni in amphipods was 13 days. The
difference in development time between the laboratory and the field likely
relates to differences in ambient temperatures. Laboratory studies
(Wong and Anderson, 1988; this
study) have used a constant temperature of 20°C, whereas substrate
temperatures at Starrs Point are usually lower (see
Piccolo et al., 1993). These
results highlight the fact that behavioral changes are tuned to development of
nematodes, even though field and laboratory conditions vary greatly.
Finally, our results indicate that nematodes have few measurable fitness
costs to the male amphipods beyond increasing the amphipod's susceptibility to
predation. We found no difference in survivorship of male amphipods over 20
days and no difference in the final body size between parasitized and
unparasitized amphipods. This is not surprising, as killing the host before
reaching maturity would mean death for the parasite (although killing the host
after maturity may not because amphipods also come to the surface when they
are near death; McCurdy DG, personal observation). The fact that sandpipers
continue to feed on crawling amphipods despite the increased risk of ingesting
parasites suggests that the costs of parasitism by nematodes may be lower to
the birds than the benefits of consuming readily visible prey
(Lafferty, 1992). Our results
suggest that manipulation of even simple aspects of host behavior may allow
parasites with complex life cycles to persist in situations where there is
little temporal overlap between intermediate and final hosts.
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ACKNOWLEDGEMENTS |
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We thank Wai-Ming McCurdy, Carina Gjerdrum, Dan McPhee, Chris Yourth, Matthew Lavers, Keiko Lui, and Andrew Barry for their assistance in the laboratory and in the field. Michelle Gunness was helpful with the multivariate analysis. Tim Cathcart-Black of Instructional Media Services at Carleton University provided help with the video tape analysis, and Tom Herman generously provided us with laboratory facilities at Acadia University. Logistical support was provided by the Nova Scotia Department of Natural Resources and the Canadian Wildlife Service (scientific collection permit #SC1496). Funding was provided by a Natural Sciences and Engineering Research Council (NSERC) scholarship to D.G.M. and an NSERC grant to M.R.F. We also thank Jim Wolford and Graham Daborn for their discussions about Corophium and two anonymous reviewers for extremely helpful suggestions in preparing the manuscript for final submission.
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