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Behavioral Ecology Vol. 10 No. 3: 234-241
© 1999 International Society for Behavioral Ecology
Parasite-induced change in host behavior of a freshwater snail: parasitic manipulation or byproduct of infection?
Department of Biology, Indiana University, Bloomington, IN 47405, USA
Address correspondence to E. P. Levri, c/o Maureen Levri, Department of Biology, Seton Hill College, Greensburg, PA 15601, USA.
Received 25 November 1997; revised 23 June 1998; accepted 8 August 1998.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Host behavioral changes due to parasitism are often assumed to be adaptations of the parasite. However, behavioral effects of parasites may be a generalized response to parasitism and only coincidentally beneficial for parasite transmission. For this reason, alternatives to the manipulation hypothesis should be tested. Previous work demonstrated that the trematode parasite Microphallus sp. influences the behavior of the snail Potamopyrgus antipodarum in a way that may increase the probability of transmission. Here I report work conducted to test alternatives to the manipulation hypothesis. In a field study, the effect of Microphallus on behavior was compared to that of two other castrating parasite groups to determine if the behavioral change is simply a byproduct of parasitism. Also, the foraging behaviors of infected and uninfected snails were examined in the presence and absence of food resources to determine if the hunger level of Microphallus-infected snails could account for the parasite-induced behavioral change. First, Microphallus-infected snails were found on top of rocks during the day less often than the two other parasite groups. This evidence suggests that the behavioral change caused by Microphallus is specific to Microphallus-infected snails. Second, Microphallus-infected snails responded to the lack of food differently from uninfected snails. Uninfected snails retreated to safer positions under rocks when the food source was removed from the top of the rocks, while Microphallus-infected snails remained on top of the rocks where the risk of consumption by the final host is greater. Taken together with previous studies, these results suggest that infection by Microphallus results in behavior that enhances parasite transmission.
Key words: foraging, host behavior, Microphallus, parasitism, Potamopyrgus antipodarum, snails, trematodes.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Parasites often have striking effects on the behavior of their hosts (Dobson, 1988
;
Holmes and Bethel, 1972;
Moore and Gotelli, 1990).
These behavioral changes can be classed as adaptations on the part of the
host, on the part of the parasite, or as nonadaptive byproducts of infection.
In many cases it seems that these changes in behavior are adaptive for the
parasite because they appear to facilitate transmission of the parasite to the
next host in the parasite's life cycle. However, caution must be used in
inferring that adaptive behavioral manipulation is occurring because simple
byproducts of infection can have transmission-enhancing effects
(Holmes and Zohar, 1990;
Moore and Gotelli, 1990). In
fact, in instances where host behaviors are altered, parasites that appear to
benefit from behavioral changes often have less dramatic effects on host
behavior than parasites that do not appear to benefit from altered behaviors
(Poulin, 1994).
In cases where parasitic manipulation is likely, the manipulation
hypothesis can be strengthened in one of two general ways: supporting
predictions of the manipulation hypothesis, and rejecting alternatives to the
manipulation hypothesis. Evidence supporting the manipulation hypothesis often
includes demonstrations of increased overlap in time and/or space between
infected intermediate hosts and the next host in the life cycle as a result of
the behavioral change (Dobson,
1988; Holmes and Bethel,
1972; Moore and Gotelli,
1990). Furthermore, the onset of transmission-enhancing behavioral
changes should occur only when parasite is transmissible—i.e., mature
enough for transmission to occur (Bethel
and Holmes, 1974; Hurd and
Fogo, 1991; Levri and Lively,
1996; Poulin et al.,
1992; Tierney et al.,
1993).
Rejecting alternatives to the manipulation hypothesis seems to be less
common (Moore and Gotelli,
1990). This may be because it is often difficult to predict
exactly what the behavioral byproducts of infection should be. One possible
way to assess the effects of byproducts of infection is to examine the effects
of different parasites on the behavior of infected hosts, especially parasites
whose transmission is not necessarily enhanced by altered host behavior. The
manipulation hypothesis would likely have different predictions for parasites
with different life cycles. However, few studies have used this approach (but
see Bethel and Holmes, 1973;
Moore and Lasswell, 1986).
In a previous study, the trematode parasite Microphallus sp. was
found to influence the behavior of its intermediate host, the snail
Potamopyrgus antipodarum (Levri
and Lively, 1996). P. antipodarum is a small prosobranch
snail found in New Zealand lakes and streams
(Talbot and Ward, 1987). It
feeds predominantly on green algae, diatoms, and detritus
(Haynes and Taylor, 1984;
Winterbourn, 1970;
Winterbourn and Fegley, 1989),
and in areas with rocky substrates it forages on the tops of rocks,
predominantly at night (Levri and Lively,
1996). Fish (Jellyman,
1989; Levri, 1998;
McCarter, 1986;
McDowall, 1990) and waterfowl
are common predators of the snail.
The predominant parasite of P. antipodarum is an undescribed
species of Microphallus (Trematoda: Microphallidae;
Lively, 1987). Mature
Microphallus produce eggs in waterfowl, which pass out of the bird
with the feces. The eggs ingested by P. antipodarum develop and
encyst within the snail, castrating the snail as the parasite larvae develop.
The cysts hatch upon ingestion by waterfowl, where they mature in the bird's
intestine to complete the life cycle. P. antipodarum is also the
first intermediate host to at least a dozen other castrating trematode
parasites (Winterbourn, 1973)
that occur at low frequencies (Lively,
1987; Jokela and Lively,
1995). Any change in behavior of the snails due to
Microphallus infection is unlikely to be adaptive for the host due to
the irreversible castration caused by the parasite.
Microphallus-infected snails foraged on top of rocks in a similar
frequency to nonbrooding females in the early morning and foraged similarly to
brooding females for the remainder of the day
(Levri and Lively, 1996).
Nonbrooding females were found on top of the rocks more than any other class
of snail throughout the day and thus were likely to be at the greatest risk of
predation. Brooding females were on the bottom of the rocks more than any
other class of snail. Hence, Microphallus-infected snails exposed
themselves to predation in the early morning and moved to a safer environment
in the late morning and afternoon. The final hosts of Microphallus
(waterfowl) were found to feed most often in the early morning
(Levri and Lively, 1996), and
other predators (fish) that cannot serve as a host for the parasite were found
to feed more in the late morning and afternoon
(Levri, 1998). Thus,
Microphallus seems to induce foraging behavior that increases the
probability of the snail being eaten when the final host is feeding and
decrease the probability of being eaten when other predators are active. Also,
only transmissible Microphallus (those parasites that are mature
enough for transmission to occur) induce the transmission-enhancing behavior
in the early morning (Levri and Lively,
1996). Nontransmissible Microphallus-infected snails were
more likely to be found on the bottom of the rocks.
These results support the manipulation hypothesis, but it is still possible that the effect of Microphallus could simply be a byproduct of parasitism. I consider a byproduct of infection to be nonadaptive, and it may result from damage caused by the parasite or from the host response to infection. I tested two alternatives to the manipulation hypothesis in this system. First, I compared the behavior of snails infected by Microphallus to snails infected with two other independent groups of castrating trematode parasites. If the daily foraging pattern of Microphallus-infected snails is simply a byproduct of infection, then snails infected with other parasites are likely to forage in a similar way. In stating the above, I am explicitly assuming that behavioral byproducts of infection are similar from one species of parasite to another in the same host. In this case, each parasite assessed is a castrating digenetic trematode, but it is possible that the behavioral effects of different parasites (or genotypes of the same parasite) may vary without regard to behavioral manipulation.
Second, I examined the effect of food availability on the foraging behavior of the snail. The snails face a trade-off while foraging. Being on top of the rocks allows them to feed on algae, but it also makes them more vulnerable to avian and piscine predators. I conducted several experiments in which I removed the benefit (food) of being on top of the rocks in one treatment. Uninfected snails were predicted to move to the bottom of the rocks when food was not present; infected snails were predicted to remain on the top of rocks in the early morning when waterfowl feed most intensively regardless of the presence of food. Later in the day, when waterfowl foraging declines and fish foraging increases, Microphallus-infected snails were expected to retreat to the bottom of the rocks if food is no longer present.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The effect of non-Microphallid parasites on foraging behavior
I undertook a survey to determine the effects of size, gender, brooding condition, and parasitism on the foraging behavior of P. antipodarum. The data were collected as described in Levri and Lively (1996
) from shallow, rocky
areas (approximately 0.5 m deep) on the margin of Lake Alexandrina on the
South Island of New Zealand (170°27' E, 43°56' S). Lake
Alexandrina is a clear-water, mesotrophic lake where P. antipodarum
is the most abundant mollusk species. I took a total of 27 samples in, 1993,,
1994, and, 1995. In, 1993, I collected snails nine times over a 24-h period
beginning on 10 February at 1530 h. In, 1994, snails were sampled 10 times
over a 24-h period beginning on 23 January at 0800 h. Five smaller samples
were also taken on 25 January (1000 h), 5 February (1500 h), 6 February (0600,
0900, and 1500 h), and 27 February (0600 and 0900 h). In 1995 a sample was
collected at 1000 h on 9 January. Each sample from each year was collected
from the same site on the lake. During each collection, I selected at least
eight rocks and carefully lifted them to the surface to minimize the number of
snails that became detached. I separated the snails based on whether they were
collected from the top or bottom of the rocks (I excluded snails judged to be
on the sides of rocks) and preserved them in 70% ethanol. I recorded the size
(distance from the apex to the basal lip of the shell), sex, brooding status,
infection status, and parasite type of all collected snails. I measured snail
size (length) using an ocular micrometer. Males can be distinguished from
females by the presence of a verge behind the right tentacle at sizes >2.1
mm. All snails <2.1 mm in length were labeled juveniles. Parasites were
identified using the descriptions provided by Winterbourn
(1973).
I sampled 12,411 snails during the study. When analyzing the data, I
separated the snails into seven mutually exclusive classes based on their
reproductive status and whether or not they were infected: (1) uninfected,
adult, nonbrooding females, (2) uninfected adult males, (3) uninfected
brooding females, (4) juveniles, (5) Microphallus-infected
individuals, (6) snails infected by externally encysting metacercariae, and
(7) snails infected by unencysted cercariae. Microphallus-infected
males were grouped together with Microphallus-infected females
because there was no difference between the two groups in their behavior
patterns found in a previous study (Levri
and Lively, 1996). Infected juveniles and brooding females are
rare (<0.1% of each class), and when encountered, they were classified as
parasitized (classes 5, 6, or 7). Only snails infected with encysted
(transmissible) Microphallus metacercariae were counted as
Microphallus infected. If the snail was infected with an earlier
stage of the parasite or if the snail was infected by multiple parasites (both
of these occurrences were rare), it was not counted in this study.
Classes 6 and 7 include multiple species of trematode parasites. This
grouping was necessary because of the rarity of each parasite species. Each of
the classes of parasites have different life cycles. Class 6 includes what
appear to be two or three undescribed species of monostome cercariae with
similar life cycles (Winterbourn,
1973). These monostome species are similar to each other in that
they castrate the snail, mature as swimming cercariae, and then swim out of
the snail and encyst on the shell and operculum of the snail as well as other
nearby surfaces. Microphallus never passes through the swimming
cercariae stage and encysts internally within the snail. Thus, like
Microphallus, externally encysting metacercariae are transmitted
trophically, through the food chain, to their final host (probably waterfowl).
Hence, if manipulation is occurring with these parasites, it is expected that
they will exhibit behavior that increases the probability of the infected
snails being eaten by waterfowl. I hereafter refer to all of the snails
infected by trophically transmitted parasites besides Microphallus as
externally encysting metacercariae infected. The other parasite group
(unencysted cercariae) include six species that castrate and mature as
cercariae that swim to the next host in the life cycle (Winterbourn, 1974);
i.e., they are not transmitted trophically. Thus, host manipulation, if it
occurs, by these parasites would be expected to have different behavioral
effects from those caused by trophically transmitted parasites. This
nontrophically transmitted group includes the Telogaster
opisthorchis, two undescribed species of furcocercariae, one undescribed
species of xiphidiocercariae, and two undescribed Gymnocephalous spp.
cercariae (Winterbourn,
1973).
I made comparisons between groups by calculating the percentage of each
group on top of the rocks over the course of the sampling period. I assume
that snails are foraging while on tops of rocks because algal food sources are
abundant there. I analyzed the data using SAS software
(SAS Institute, 1990) using a
modified multiple logistic regression procedure described in Levri and Lively
(1996) to determine whether
the daily foraging patterns differed between the snail classes. The logistic
regression was modified by using sine and cosine functions to account for the
daily cycle. The resulting regression curve, therefore, results in sine waves
rather than the typical logistic regression sigmoidal functions. The analysis
was performed identically to that in Levri and Lively
(1996), except that day of
sampling was not used in the analysis. This was done to increase sample sizes
in the rare parasite-infected classes. Thus data were combined across day and
year. I used the variables time of day and snail class to estimate the
probability of finding a snail on top of the rocks. A Bonferroni correction
was used to adjust the alpha level for the number of tests.
The effect of food availability on foraging behavior
I conducted four separate experiments to determine the effect of food
availability on behavior. The first three were nearly identical. The
differences between the experiments are presented in
Table 1. In each experiment,
snails were collected using a dip net from Lake Alexandrina. The snails were
taken from the shore bank habitat of the lake, where they could easily be
collected. The snails from this subpopulation of the lake yielded infection
rates of Microphallus from 4% to 9% from various collections (Levri,
unpublished data). I set up 40-1 opaque plastic tanks along the lake shore and
filled them with lake water. In half of the tanks used in two of the
experiments, enough rocks from the lake were placed in the tanks (food tanks)
to cover the entire bottom of the tanks. The snails fed upon algae that coated
the tops of the rocks. The remaining tanks (nonfood) contained rocks that were
found above the water level of the lake (no algae had been growing on them).
Thus there were two treatments: the snails were exposed to food or nonfood
rocks. The tanks were arranged by alternating treatments.
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In the other two experiments both treatments were represented in each tank with each treatment occupying half of the tank space (Table 1). The number of snails added to each tank varied depending on the experiment (Table 1). I controlled infection rate by mixing the snails together before adding them to the tanks and by adding approximately the same number of snails to each tank. Shade cloth was put over the tanks to minimize the temperature increase during the daylight hours. The snails were allowed to acclimate for 3 days. Snails were sampled from the rocks at the times indicated in Table 1, and they were separated by whether they were found on the top or bottom of the rocks. I continued the sampling until all the snails were removed from the top and bottom of the rocks (approximately 15-25 min per tank). In experiment 4, only snails from the tops of the rocks were sampled. This was done to speed up the sampling so that samples could be taken at several times over the course of the day. The snails were taken back to the laboratory and dissected in the manner described previously. The mature snails were separated into one of four mutually exclusive classes: (1) uninfected, nonbrooding females, (2) uninfected, brooding females, (3) uninfected males, and (4) Microphallus-infected snails infected with transmissible parasites [some snails were infected by nontransmissible (immature) Microphallus, but too few were found for analysis].
I analyzed the data for the first three experiments using chi-square tests.
Pairwise comparisons were made by pooling data across replicates within
treatment for each class of snail. The data for the fourth experiment were
analyzed using a logistic regression analysis. Once again, to increase sample
sizes, the data were pooled across replicates and grouped by whether the
snails were collected in the morning (0500 and 0700 h), afternoon (1200 h), or
evening (2000 h). The dependent variable in the analysis was the ratio of the
number of snails of each class found on top of the nonfood rocks to the number
of snails of each class found on top of the food rocks. The independent
variables in the analysis were time of day (morning or afternoon) and class of
snail. I chose nonbrooding females as the reference uninfected class because
they were found to be similar to Microphallus-infected snails in the
early morning in examining the effect of infection in behavior (present study)
and in a previous study (Levri and Lively,
1996). The morning sample was compared to the afternoon and then
the evening sample. A third comparison was made by analyzing the morning
sample versus the pooled afternoon and evening samples. I did this to increase
the sample sizes in the Microphallus-infected classes in the
afternoon + evening sample. Afternoon and evening samples were pooled only
after I determined that there was no significant difference between the two
samples in sample size or ratio of snails on food to nonfood for either class
(nonbrooding females and Microphallus-infected snails).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The effect of non-Microphallid parasites on foraging behavior
Of the 12,412 snails collected in the study, 3699 were nonbrooding females, 2993 were brooding females, 2209 were males, 1669 were juveniles, 1428 were Microphallus-infected snails, 265 were snails infected by unencysted cercariae, and 149 were infected by externally encysting metacercariae. Nine different castrating parasite species were identified from the collections.
All snail classes were more likely to be found on top of the rocks at night than during the day. Microphallus-infected snails foraged significantly different from any other snail group, including the other two infected classes (Table 2). The resulting logistic regression curves are presented graphically in Figure 1. Unencysted-cercariae-infected and externally encysting-metacercariae-infected snails did not forage significantly different from each other (hence they were grouped together in Figure 1) or each from nonbrooding females (although the difference is marginally significant; see Table 2; a Bonferroni correction set the critical alpha level to 0.002). These three groups foraged on top of rocks more than other classes in the late morning and early afternoon (Figure 1). The patterns shown by uninfected adult males and juveniles were similar to brooding females, except that males and juveniles foraged more frequently during the day.
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The effect of food availability on foraging behavior
The first three experiments yielded similar results to each other
(Figure 2). In each experiment,
uninfected, nonbrooding females moved to the bottom of the rocks significantly
more in the nonfood treatment than did nonbrooding females in the food
treatment. Microphallus-infected snails did not exhibit significant
movement to the bottom of the rocks in the nonfood treatment compared to the
food treatment, except in experiment 3. Pairwise comparisons using chi-square
analysis of Microphallus-infected snails and nonbrooding females
within each treatment are indicated in
Figure 2. A Bonferroni
correction set the 5% risk level at 0.008 within each experiment.
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The data for experiment 4 are given in Figure 3. Significantly fewer snails were found on top of the rocks in the nonfood treatment, except for Microphallus-infected snails in the morning when compared to the afternoon. There was a significant class by time-of-day interaction (morning versus afternoon) on the proportion of snails found on top of the rocks from the food versus nonfood portions of the tank (Table 3). A significant class by time-of-day interaction was also found in the comparison between the morning and afternoon + evening samples (pooled) (Table 3). A significant class by time-of-day interaction was not found when comparing the morning and evening samples.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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The results from this study address two alternative hypotheses to the manipulation hypothesis in the Potamopyrgus-Microphallus system. First, the behavioral effects of Microphallus on Potamopyrgus are unlikely to be exclusively a simple byproduct of parasitism because other castrating parasites do not induce the same foraging behavior. Second, the foraging behavior of Microphallus-infected individuals does not seem to be driven simply by hunger.
The effect of non-Microphallid parasites
Microphallus-infected snails behaved significantly different from
snails infected by two other trematode groups
(Table 2). Moreover, behavior
of snails infected by the two other parasite groups were not significantly
different from each other. These results suggest that effects on foraging
behavior induced by Microphallus are specific to
Microphallus. Effects on foraging behavior that are simply byproducts
of parasitism are likely to be demonstrated by the
unencysted-cercariae-infected and externally encysting-metacercariae-infected
snails in this study because the two groups foraged similarly despite being
infected with parasites with different life cycles. In this case, the
unencysted-cercariae-infected and externally encysting-metacercariae-infected
snails foraged on top of the rocks, similar to nonbrooding females
(Figure 1), although
Microphallus-infected snails were more likely to be on the bottom of
the rocks, compared to the other infected groups, especially in the middle of
the day.
Several studies have demonstrated different effects on behavior of multiple
species of parasites on the same host
(Bethel and Holmes, 1973;
Curtis, 1985;
Moore and Lasswell, 1986).
Moore and Lasswell (1986)
found that the nematode Dispharnax nasuta induced different behaviors
in the isopod Armadillidium vulgare than in the acanthocephalan
Plagiorhyncus cylindraceus. They suggested that this difference
indicated that the change in behavior due to at least one of the parasites
could not simply be a generalized response to infection.
Unencysted-cercariae-infected and externally
encysted-metacercariae-infected snails did not forage significantly different
from nonbrooding females, although in both comparisons the results are close
to being significant (Table 2).
In any case, the foraging patterns of nonbrooding females,
unencysted-cercariae-infected snails, and externally
encysted-metacercariae-infected snails seem to parallel each other
(Figure 1). This similarity may
indicate that the general behavioral effect of parasitism is to cause
individuals to forage similarly to nonbrooding females. This is perhaps not
surprising because nonbrooding females feed more than any other class of snail
(Levri and Lively, 1996), and
infection is likely to be energetically costly to the host
(Holmes and Zohar, 1990). Thus
by feeding more, the snail (and the parasite) may survive longer.
It is possible that the behavior patterns of hosts infected with the two other parasite groups are simply a compilation of specific behavioral responses to the different parasite species. If this were true, the grouped results would mean little. When the results are examined for each species independently, they are similar to the patterns generated by the groups of species. The analysis could not be run on individual species because the sample sizes for each species were very small. In the externally encysting metacercariae, though, there are few species (two to three), and they are likely to be closely related based on morphological and life-cycle similarities.
In a previous study, the behavior induced by Microphallus was
dependent on the transmissibility of the infection
(Levri and Lively, 1996). Only
snails infected by transmissible Microphallus (those parasites that
were mature enough for transmission to occur) foraged on top of the rocks in
the early morning. Snails with nontransmissible infections were more likely to
be found on the bottom of the rocks throughout the daylight hours. If the
general effect of parasite infection is to cause the snails to forage more on
tops of the rocks throughout the day, as suggested in this study, then it
would seem that nontransmissible Microphallus-infected snails also
have a unique behavior pattern. The behavior pattern induced by
nontransmissible Microphallus-infected snails may decrease the
probability that the snail would be eaten by any large predator, most likely
waterfowl or fish. There are few examples of advantageous behavioral changes
induced by nontransmissible parasites. Tierney et al.
(1993) present data consistent
with the idea that nontransmissible parasites may induce predator-avoidance
behaviors in three-spined sticklebacks. Although the aim of their study was
not specifically to address this idea, their data suggest that fish infected
with nontransmissible cestode plerocercoids have a faster recovery time to a
predator attack, a decreased duration of pectoral sculling, and an increased
amount of time spent motionless compared to uninfected controls. Tierney et
al. (1993) suggest that these
behaviors seem to decrease the probability of predation on the fish.
The effect of food availability on behavior
The absence of food had a noticeable effect on nonbrooding females in each
of the first three experiments. In each case nonbrooding females moved to the
bottom of the rocks when food was not present on top of the rocks. This
behavior makes sense in that the snails should not risk predation if the
benefits of being on top of the rocks are removed. Previous studies have
demonstrated that P. antipodarum responds to fish predators by moving
to the bottom of the rocks (Levri, in
press).
In the early morning, Microphallus-infected snails were on top of
the rocks as frequently as nonbrooding females
(Levri and Lively, 1996). If
manipulation is occurring, snails, in the absence of food, should be on top of
the rocks as frequently as nonbrooding females in the food treatment. In each
experiment infected snails did not respond to the lack of food and remained on
the top of the rocks as frequently as did nonbrooding females in the food
treatment. This result suggests that Microphallus is inducing the
snails to remain on the top of the rocks despite the absence of food, which is
consistent with the manipulation hypothesis. These experiments were performed
in the early morning, when Microphallus-infected snails are most
likely to be found on top of the rocks and when the final host of
Microphallus feeds most (Levri
and Lively, 1996). Thus if Microphallus is manipulating
the behavior of the snail, the parasite should induce the snail to be on top
of the rocks in the early morning regardless of food availability. In the
third experiment, Microphallus-infected snails did show a significant
increase in the percentage on top of the rocks in the food treatment compared
to Microphallus-infected snails in the nonfood treatment. The reason
for the difference in behavior of the Microphallus-infected snails in
the food treatment of the third experiment is not known.
Another interpretation of these data is that Microphallus-infected
snails are nutrient limited due to parasitism, thus they are on top of the
rocks more often in an effort to find food. This interpretation is not likely
to be correct because in a previous field study, nonbrooding females were on
top of the rocks more than any other group over the course of the day
(Levri and Lively, 1996).
Because the major benefit of being on top of the rocks is nutrient
acquisition, it is assumed that nonbrooding females need to forage more than
any other group, including infected snails. Given that nonbrooding females
need to forage more, Microphallus-infected snails should have been on
top of the rocks less than nonbrooding females in this experiment (i.e., the
lack of food should have affected the nonbrooding females to the greatest
degree). This was not the case. The behavior of Microphallus-infected
snails was distinctly different from any of the uninfected classes
(Levri and Lively, 1996).
Hence, it seems that infection by Microphallus results in the
snails remaining on top of the rocks in the early morning regardless of food
availability. In the field it was found that Microphallus-infected
individuals moved to the bottom of the rocks in the late morning and
afternoon. This period is when fish fed most intensely, and they cannot serve
as the definitive host (Levri,
1998; Levri and Lively,
1996). If the lack of a response to the absence of food in
parasitized snails observed in the present study is adaptive, then the
response is expected to appear in the late morning and afternoon when
waterfowl feed less and fish feed more. Snail samples in the fourth experiment
were taken over time. In the fourth experiment, significantly fewer
nonbrooding female snails were found on the top of the rocks in the nonfood
treatment in the morning and the afternoon
(Figure 3), suggesting that it
is better to avoid predation when food benefits are eliminated. Similarly to
the first three experiments, in the early morning
Microphallus-infected snails were just as likely to be found on top
of the rocks in the food and nonfood treatments, suggesting that the parasite
is manipulating the snails to enhance transmission to the final host. However,
in the comparison between morning and afternoon samples, a significant
time-by-class interaction was found (Table
3), indicating that in the afternoon, there were fewer infected
snails found on top of the rocks in the nonfood treatment than in the food
treatment. The same time-by-class interaction was found when data from the
afternoon and evening were pooled. This would seem to indicate that the
parasite-induced effect is "turned off" when other predators are
feeding more. The morning versus evening comparison did not yield a
significant time-by-class interaction, but the trend was in the expected
direction. These time-specific effects are exactly what was predicted by the
manipulation hypothesis.
In summary, the results suggest that the foraging behavior induced in
P. antipodarum by Microphallus is specific to
Microphallus. Microphallus-infected snails behaved differently from
snails infected with two other independent groups of parasites. Also,
Microphallus-infected snails responded differently from uninfected
snails when food availability changed. Microphallus-infected snails
remained exposed to predators when the final host feeds most, regardless of
food availability. Uninfected snails moved to a safer habitat when food was
removed. Taken together with previous findings
(Levri, 1998, unpublished
data; Levri and Lively, 1996),
these results provide support for the hypothesis that Microphallus is
manipulating the behavior of P. antipodarum to enhance its
probability of transmission.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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I thank J. Jokela and C. Lively for assistance in the field, J. Jokela and B. Flury for statistical advice, and T. Frankino, J. Jokela, A. Krist, M. Levri, C. Lively, A. Peters, P. L. Schwagmeyer, and two anonymous reviewers for helpful comments on previous versions of this manuscript. I am grateful to the faculty and staff in the Zoology Department, University of Canterbury, New Zealand, for continued support, including M. Winterbourn, I. McLean, T. Eldon, J. Van Berkel, and especially J. McKenzie. This study was supported by National Science Foundation grants to C. Lively (BSR-9008848) and to E.P.L. and C. Lively (DEB-9509286), and by grants from the Indiana University Research Training Grant in Animal Behavior and the Indiana Academy of Science.
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REFERENCES |
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