J. Parasitol., 95(4), 2009, pp. 823–828
F American Society of Parasitologists 2009
SEASONAL DYNAMICS OF TWO MORTALITY-RELATED TREMATODES USING AN
INTRODUCED SNAIL
Kristin K. Herrmann and Robert E. Sorensen*
Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand. e-mail: [email protected]
ABSTRACT:
Seasonal dynamics of 2 trematode species, Cyathocotyle bushiensis and Sphaeridiotrema globulus, were assessed in relation
to life history traits of the parasites and their hosts, as well as abundance of host species and abundance of infective stages. Both of
these trematodes are associated with recurrent mortality of migrating waterbirds on the Upper Mississippi River National Wildlife and
Fish Refuge. An invasive snail species, Bithynia tentaculata, serves as intermediate host for both trematode species. In total, 2,970
snails were collected at 2 study sites. Prevalence and mean abundance of the 2 trematode species varied among dates and was attributed
to several factors, including migration patterns of definitive hosts, snail population dynamics, and seasonal changes in temperature.
The surge of new infections of both parasites seems to be due to avian hosts foraging at this site during spring migration. The high
prevalence and abundance of metacercariae among the snail population promote mortality among molluscivorous birds by increasing
the probability of ingestion of a lethal dose. Additionally, mortality of non-molluscivorous birds can be explained by accidental
ingestion of a couple of highly infected snails resulting in a lethal dose.
Recurrent seasonal mortality of migrating waterbirds has been
occurring in Pool 7 of the Upper Mississippi River National
Wildlife and Fish Refuge (UMR Refuge) since 2002 (Blankenship, 2004) and is associated with 2 species of trematodes (Sauer et
al., 2007), Cyathocotyle bushiensis (Cyathocotylidae) and Sphaeridiotrema globulus (Psilostomidae). Mortality of waterbirds, due
to one, or both, of these trematode species has been commonly
reported in eastern North America since 1928, i.e., southern
Quebec (Gibson et al., 1972; Hoeve and Scott, 1988), southeastern
Ontario (Speckmann et al., 1972), Washington, D.C. area (Price,
1934), New Jersey (Roscoe and Huffman, 1982, 1983; Huffman
and Fried, 1983), Michigan (Cornwell and Cowan, 1963; Campbell and Jackson, 1977), and eastern Wisconsin (Trainer and
Fisher, 1963).
The recurrent mortality of migrating birds at Pool 7 suggests C.
bushiensis and S. globulus are maintained in resident intermediate
hosts when migratory definitive hosts are absent. Both trematode
species use freshwater snails as first and second intermediate
hosts, and the only known intermediate host of both trematodes
in Pool 7 is Bithynia tentaculata (Berntzen and Macy, 1969;
Gibson et al., 1972; Huffman and Fried, 1983; Huffman and
Roscoe, 1986; Mucha and Huffman, 1991). This snail is an
invasive species originally introduced into the Lake Michigan in
1870 (Mills et al., 1993; Harman, 2000). Although it is unknown
how long this snail has inhabited Pool 7, there are no records of
this snail in western Wisconsin or the Mississippi River before
these mortality events began (Sauer et al., 2007). Susceptible
waterbirds become infected with C. bushiensis and S. globulus by
ingesting second intermediate snail hosts containing metacercariae at UMR Refuge during spring and fall migrations. Metacercariae develop into adult worms within the digestive tract, where
they reproduce sexually. Trematode eggs are released into the
water with fecal material from infected birds (Khan, 1962;
Huffman et al., 1984). First intermediate hosts become infected
when miracidia penetrate snails (Schell, 1985). Within these first
intermediate hosts, miracidia of C. bushiensis develop into
sporocysts, and miracidia of S. globulus develop into sporocysts,
and then rediae. Asexual reproduction yields numerous cercariae
that emerge and encyst as metacercariae in either the same snail or
another snail (Dailey, 1996).
Previous studies on trematode-associated mortality of waterfowl in southern Quebec demonstrated that sentinel dabbling
ducks can ingest lethal doses of C. bushiensis and S. globulus
within a 24-hr period (Hoeve and Scott, 1988) and that death of
lethally infected birds usually occurs in 3 to 10 days (Hoeve and
Scott, 1988; Huffman and Roscoe, 1989; Mucha and Huffman,
1991). This confirms that mortality in Pool 7 begins within days
after the birds arrive during spring and fall migrations. As their
condition weakens, lethally infected birds are first unable to fly
and then unable to dive. These birds ultimately take refuge
along the rocky shore of islands until they succumb to the
infection. These observations support previous findings that
infected birds show general muscular weakness and an inability
to fly or hold a position on a lake in wind (Roscoe and
Huffman, 1982, 1983; Huffman and Roscoe, 1989; Mucha and
Huffman, 1991).
As the initial investigation of this host–parasite system in Pool
7, it is essential to examine the seasonal dynamics of these
trematodes, and their infective stages, in the intermediate host.
The main factors likely to affect temporal distribution of parasites
include (1) seasonal variation in behavior and abundance of the
definitive host (Dronen, 1978; Hoeve and Scott, 1988; Scott, 1988;
Fernandez and Esch, 1991; Esch and Fernandez, 1994; Sapp and
Esch, 1994; Sandland et al., 2001); (2) life history and distribution
of the intermediate snail host (Dronen, 1978; Hoeve and Scott,
1988; Fernandez and Esch, 1991; Esch and Fernandez, 1994; Sapp
and Esch, 1994; Gérard, 2001; Sandland et al., 2001; Kube, Kube
and Bick, 2002); (3) seasonal changes in temperature (Dronen,
1978; Sandland et al., 2001; Kube, Kube and Bick, 2002; Poulin,
2006); and (4) density of and heterogeneity in host exposure to
infective stages (Hoeve and Scott, 1988; Scott, 1988; Poulin,
2007).
The objective of this research was to examine the naturally
occurring temporal variation in the population dynamics of C.
bushiensis and S. globulus in B. tentaculata around Arrowhead
and Broken Gun Islands in Pool 7. In our effort to better
understand the factors promoting recurrent mortality of waterbirds at this site, we evaluated how temporal patterns were
associated with characteristics, such as life histories of the
parasites, life histories of hosts, abundance of infective stages of
the parasites, and densities of host populations.
Received 22 October 2008; revised 15 December 2008; accepted 6
February 2009.
* Department of Biological Sciences, Minnesota State University-Mankato, Mankato, Minnesota 56001.
DOI: 10.1645/GE-1922.1
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THE JOURNAL OF PARASITOLOGY, VOL. 95, NO. 4, AUGUST 2009
substratum at the 6 open-water sites with a benthic grab sampler (Petite
Ponar, Wildco, Buffalo, New York). Snails were transported on ice to
Minnesota State University Mankato, Mankato, Minnesota, and stored at
4 C until examined. Lepitzki et al. (1994) showed that cold storage of the
snails does not affect mean abundance of immature metacercariae
indicating that cercarial transmission was not occurring while the snails
were refrigerated. Water temperature data were collected at each site with
a digital surface thermometer at the time of collection.
Calipers were used to measure length of snail shells, which was used for
detection of new snail cohorts based on the range and frequency of snail
sizes that were found during each collection. Snails were individually
crushed, and presence of larval stages was assessed using a dissection
microscope. The C. bushiensis and S. globulus parasites in this system were
initially identified by the National Wildlife Health Center, and species
identification for this study was based on their description and
supplemented by cercariae and metacercariae morphology as described
by Khan (1962) and Schell (1985). Prevalence of rediae, sporocysts and
metacercariae in B. tentaculata was determined. Metacercariae in second
intermediate hosts were counted to determine mean abundance. Definitions of prevalence and mean abundance follow Bush et al. (1997).
Statistical analyses
Data were pooled across collection sites at each island to assess
temporal patterns in the population of these two trematode species. No
difference was found between individuals collected from shore sites and
open-water sites at each island. Differences in prevalence were analyzed
with a G-test. Temporal variation among dates in mean abundance of
metacercariae was analyzed with a Kruskal–Wallis test followed by
Dunn’s nonparametric multiple comparison (Q statistic). Differences in
mean water temperature between islands were assessed with a Mann–
Whitney U-test. A statistical significance of P , 0.05 was used for all
analyses.
FIGURE 1. Map of Pool 7 (Lake Onalaska) showing the two study sites,
Arrowhead and Broken Gun Islands, and collection sites (open circles)
around each island. Map is based on images from Google EarthTM
mapping service.
MATERIALS AND METHODS
Field site
Pool 7 (Lake Onalaska) is a 30-km2 impoundment in La Crosse County,
Wisconsin, created from the backwaters of Lock and Dam 7 on the
Mississippi River (Fig. 1). It is part of the 420-km-long UMR Refuge that
is used by almost 300 species of migrating birds of the Mississippi Flyway.
Migrating waterbirds are typically present at Pool 7 mid-March through
late April and mid-September through late November. The average water
depth is 1.0–1.3 m.
Arrowhead and Broken Gun islands were selected as study sites because
of the abundance of snails inhabiting the rip-rap (loose foundation rocks)
around the islands and the preponderance of infected or deceased birds
that have been collected around the islands during the seasonal epizootic
events. These C-shaped, artificial islands were built approximately 1.5 km
apart in 1989 by the U.S. Army Corp of Engineers; however, Arrowhead
Island was built on top of a small, pre-existing island with average water
depth of 1.0–1.3 m. Broken Gun is located in deeper water, averaging 1.3–
2.0 m.
Collection and dissection of snails
In May 2005, 11 collection sites were established around Arrowhead
Island and 10 collection sites around Broken Gun Island (Fig. 1). Site
selection was based on island morphology, locations of foraging and
diseased birds during migration, and presence of rip-rap structure serving
as snail habitat, resulting in 50–175 m of shoreline between adjacent sites.
Three open-water sites at each island were located 25–100 m from shore
with water depth between 1 and 2 m. Five collections were made in 2005
on 18 May, 6 June, 19 August, 6 September, and 11 October; an additional
collection was made on 17 May 2006. Collection at each site consisted of a
maximum of 30–40 snails haphazardly collected by hand from the bottom
of rocks within a 30-min time limit. Snails were collected from the bottom
RESULTS
Bithynia tentaculata
In total, 1,725 B. tentaculata were collected around Arrowhead
Island on 6 occasions: 360 in May 2006, 330 in June, 260 in
August, 268 in September, 261 in October, and 246 in May 2006.
Snail eggs were observed during the first collection on May 2005,
and small snails of this cohort were found in June. On the May
2006 collection, the first cohort of that year was observed at this
island.
In total, 1,245 B. tentaculata were collected around Broken
Gun Island on 6 occasions: 258 in May 2006, 330 in June, 120 in
August, 193 in September, 154 in October, and 190 in May 2006.
Snail eggs were observed during the first collection on May 2005,
and small snails of this cohort were found in June. Another
cohort of 2005 was detected in September. On the May 2006
collection, the first cohort of that year was observed at this site.
Cyathocotyle bushiensis
At Arrowhead Island, a difference among dates was found for
sporocyst prevalence (G 5 18.58, df 5 5, P , 0.005),
metacercariae prevalence (G 5 101.72, df 5 5, P , 0.001), and
metacercariae abundance (H 5 492.76, df 5 5, P , 0.001). In
2005, sporocyst prevalence began to increase in August, reaching
the highest prevalence in September (Fig. 2a). Metacercariae
prevalence was lowest in June, which was followed by an increase
in August and again in October (Fig. 2b). Mean abundance of
metacercariae decreased in June (Q 5 24.06, P , 0.001; Fig. 2c).
This mean abundance increased in August (Q 5 2.97, P , 0.05)
and again in October (Q 5 6.22, P , 0.001), after which it was
not different in May 2006 (Q 5 20.56, P . 0.05).
HERRMANN AND SORENSEN—SEASONAL DYNAMICS OF TWO TREMATODES
825
FIGURE 3. Mean water temperature between islands among 6
collection dates from May 2005 to May 2006 at Pool 7. Error bars
indicate the standard error of the mean.
FIGURE 2. Sporocyst/rediae prevalence (a), metacercariae prevalence
(b), and mean metacercariae abundance (c) of Cyathocotyle bushiensis and
Sphaeridiotrema globulus in the intermediate snail host population. Circles
indicate C. bushiensis, and triangles indicate S. globulus. Solid symbols and
lines indicate Arrowhead Island, and open symbols and dashed lines
indicate Broken Gun Island. Error bars indicate the standard error of
the mean.
At Broken Gun Island, a difference among dates was found for
sporocyst prevalence (G 5 14.79, df 5 5, P , 0.05), metacercariae
prevalence (G 5 50.09, df 5 5, P , 0.001), and metacercariae
abundance (H 5 209.18, df 5 5, P , 0.001). In 2005, sporocyst
prevalence began to increase in August, and a decrease was not
detected until May 2006 (Fig. 2a). In May 2006, 1 sporocystinfected snail was found. Metacercariae prevalence decreased in
June and then increased in August (Fig. 2b). There was a decrease
again in September followed by an increase in October and May
2006. Mean abundance of metacercariae was greater in May 2006
than in June (Q 5 5.12, df 5 5, P , 0.001) or September (Q 5
4.77, df 5 5, P , 0.001) of the previous year (Fig. 2c). However,
there were no differences between sequential collection dates.
Sphaeridiotrema globulus
At Arrowhead Island, a difference among dates was found for
rediae prevalence (G 5 102.85, df 5 5, P , 0.001) and
metacercariae abundance (H 5 209.18, df 5 5, P , 0.001).
However, no difference was found for metacercariae prevalence
(G 5 0.64, df 5 5, P . 0.05). Just 3 snails had rediae in May 2005
(Fig. 2a). Rediae prevalence decreased in June; peaked in August;
and subsequently decreased in September, October, and May
2006. In May 2006, 9 snails with rediae were found. Metacercariae
prevalence was never below 93.6% (in May 2005) and reached
100.0% in September (Fig. 2b). The mean abundance of
metacercariae was lowest in May 2005 and June (Fig. 2c). The
highest mean abundance was found in August (Q 5 5.19, P ,
0.001) and September (Q 5 3.05, P , 0.05). Mean abundance
decreased by October (Q 5 23.26, P , 0.05) to a level similar to
May 2006 (Q 5 21.45, P . 0.05).
At Broken Gun Island, a difference among dates was found for
rediae prevalence (G 5 22.10, df 5 5, P , 0.005) and
metacercariae abundance (H 5 90.21, df 5 5, P , 0.001).
However, no difference was found for metacercariae prevalence
(G 5 03.51, df 5 5, P . 0.05). Rediae prevalence increased in
August, peaked in September, and subsequently decreased in
October and May 2006 (Fig. 2a). Metacercariae prevalence was
never below 81.2% (in June) and reached 97.5% in August
(Fig. 2b). Mean abundance of metacercariae increased in August
(Q 5 3.19, P , 0.05; Fig. 2c), after which mean abundance did
not increase nor decrease through to May 2006.
Temperature
Mean water temperature had the same temporal pattern at both
islands, and average water temperature was greater at Arrowhead
Island than at Broken Gun for each collection (Fig. 3).
Furthermore, overall mean water temperature was greater at
Arrowhead Island (U 5 741519.5, df 5 1, P , 0.001).
DISCUSSION
Trematode infections in B. tentaculata varied temporally as
expected for allogenic parasites using migratory birds as definitive
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hosts (Esch and Fernandez, 1994; Kube, Kube, and Dieschke,
2002). Trematode eggs are being deposited among the snail
population only twice a year by the migrating definitive hosts.
Because egg hatching success would be expected to be low in the
fall due to decreasing water temperatures and a low proportion of
trematode eggs survive over winter (Menard and Scott, 1987a;
McKindsey and McLaughlin, 1993), only the eggs deposited
during the spring migration contribute notably to transmission.
Additionally, potential bird hosts arrive in large numbers
immediately after ice cover melts and spring migration is brief,
which results in trematode eggs being deposited among the snail
population in a pulse. In spring 2005, dead and diseased birds
were found 1 April–5 May, with a peak in mortality during 8–15
April (C. Gehri, U.S. Fish and Wildlife Service, pers. comm.).
Based on water temperature in the spring, egg incubation period
would be greater than 39 days for C. bushiensis (Menard and
Scott, 1987a) and greater than 18 days for S. globulus (McKindsey
and McLaughlin, 1993). These factors ultimately result in the
surge of new sporocyst/rediae infections observed later that year
(Fig. 2a). Sporocyst prevalence of C. bushiensis peaked in
September at both islands due to the long incubation period.
Rediae prevalence of S. globulus peaked in August at Arrowhead
due to a shorter incubation period; however, we acknowledge that
these infections could have exhibited a peak and/or increase in
July, but no collection was made that month. At Broken Gun
Island, S. globulus did not peak until September, most likely due
to lower water temperatures found at this island (Fig. 3).
Seasonal patterns of transmission are also affected by
seasonal patterns in the dynamics of the snail host population
(Gérard, 2001; Kube, Kube, and Bick, 2002). The low level of
infections found in June coincided with recruitment patterns in
the snail population as an influx of young snails, with
nonexistent or lower infection levels, occurred at both islands.
In August, levels of infection of both species increased even
though there was a decrease in the size of the snail population at
our study sites, possibly due to either an increase in snail
mortality after reproduction or snail movement away from the
islands. This indicates that parasite recruitment was high
enough to override loss due to host death or host movement.
However, mean metacercariae abundance of C. bushiensis did
not increase at Broken Gun, possibly due to a longer incubation
period, colder water temperature, and thus lowered cercariae
transmission.
Mean abundance of metacercariae of C. bushiensis at Arrowhead Island peaked in October, 1 mo after the peak in sporocyst
prevalence. Abundance of S. globulus metacercariae showed the
same pattern at Arrowhead Island, peaking in September after the
rediae prevalence peaked in August. Mean abundance did not
show a significant peak at Broken Gun Island for either species,
contrary to the observed pattern at Arrowhead. This may be
attributed to a new cohort of snails detected at Broken Gun
Island in September, but not at Arrowhead. The influx of young
and, therefore, more likely uninfected, snails at Broken Gun
cancels out the effect that transmission of cercariae should have
on mean abundance of metacercariae. Mean metacercariae
abundance of both trematodes stayed the same from October to
May 2006 at both islands, even though the first snail cohort of
2006 occurred in May. Thus, cercariae transmission seems to have
continued after the October collection, counteracting the recruitment of young, uninfected snails.
First intermediate snail hosts of S. globulus are able to
overwinter in Pool 7, supporting previous findings by Menard
and Scott (1987a). Surprisingly, 1 snail infected with C. bushiensis
sporocyst was found in May 2006 at Broken Gun Island,
indicating the possibility of this parasite species being able to
overwinter in first intermediate host snails. This finding has not
previously been reported in other studies of this trematode.
Survival of first intermediate hosts over winter for either of these
parasites may allow transmission of cercariae to occur earlier in
the season during the following year and consequently results in a
greater mean abundance of metacercariae among the snails living
in the immediate vicinity of surviving first intermediate hosts.
This is likely to be a bigger concern for S. globulus infections given
their higher frequency among snails collected in May.
Because migratory birds that are feeding at Pool 7 in the spring
serve as the source of new infections for first intermediate hosts, it
is essential that snails harboring metacercariae overwinter to
infect these migrants. Little change in metacercariae prevalence
and no difference in mean abundance were found for both species
at both islands between October and May 2006 (Fig. 2b, c). Thus,
second intermediate hosts do not experience differential mortality
over winter compared with uninfected snails.
Notably, this study found high prevalence in first intermediate
hosts compared with other studies on these species. Rediae
prevalence of S. globulus was as high as 15.8% in August and
12.3% in September at Arrowhead. Even though sporocyst
prevalence of C. bushiensis was not as high as for rediae
prevalence of S. globulus, prevalence of 2.2% at Arrowhead and
2.1% at Broken Gun in September was still greater than reported
in other studies in southern Quebec that estimated prevalence of
0.05% (Menard and Scott, 1987b) and 0.5% (Gibson et al., 1972).
Large populations and high densities of definitive bird hosts
promote transmission of infections (Scott, 1988) and high
prevalence of first intermediate hosts, which corresponds to what
we observed at Pool 7. As an important stopover on the
Mississippi Flyway with aerial surveys reporting community sizes
of waterbirds typically ranging between 30,000–100,000 birds
during migrations, this abundance of birds favors transmission of
trematodes by increasing the likelihood that an infected second
intermediate host is ingested by a susceptible bird. Furthermore,
the rapid rate of development of these trematodes within their
definitive avian hosts (3–5 days to maturity; Khan, 1962) allows
for the release of a large number of eggs before these birds
succumb to the infection or leave this site, which facilitates the
infection of a new cohort of first intermediate hosts and leads to
the high prevalence levels that were detected.
The overall high prevalence and abundance of metacercariae
have consequences for the definitive bird hosts by promoting
mortality among molluscivorous birds by increasing the likelihood they will ingest a lethal dose. Hoeve and Scott (1988)
showed that sentinel dabbling ducks can ingest lethal levels of
infection of C. bushiensis and S. globulus within a span of just
24 hr. Additionally, our data support those of Sauer et al. (2007)
who reported that only a couple of highly infected snails need to
be ingested to produce a lethal infection in the bird host. Thus,
non-molluscivorous birds may ingest a lethal dose by accidentally
consuming a few infected snails while foraging on vegetation.
Numerous species of waterbirds use the area where the
mortality is occurring, but according to carcass collections by
U.S. Fish and Wildlife personnel, the populations of American
HERRMANN AND SORENSEN—SEASONAL DYNAMICS OF TWO TREMATODES
coot (Fulica americana) and lesser scaup (Aythya affinis) are
experiencing the majority of die-offs (C. Gehri, U.S Fish and
Wildlife Service, pers. comm.). The increased susceptibility that
these bird species exhibit for these parasites may be affected by
their rate of exposure to the infective stage, which is influenced by
a number of factors, including behavior and life history traits of
potential hosts (Hoeve and Scott, 1988), density of host
populations, and density of infective stages. Hoeve and Scott
(1988) found different levels of infection among the species of
birds they studied in Ontario and suggested that these differences
are a result of dissimilar rates of exposure due to different feeding
habits of these species. At Pool 7, several of these factors may
favor C. bushiensis and S. globulus infections in coot and scaup.
Both of these species of birds prefer deep, open water habitats
with emergent vegetation and both feed largely on molluscs,
whereas other species of diving waterbirds prefer other invertebrates and vegetation (Thompson, 1973). The dense populations
of coot and scaup that are drawn to this site during spring and fall
migrations combined with their propensity to feed on snails that
may be harboring infections of C. bushiensis and S. globulus
compounds the probability that these parasites will be transmitted
between subsequent hosts.
Finally, most snails sampled in this study were collected from
the underside of fairly large rocks along the shore and thus not
accessible to potential bird hosts in the area. Although no
difference in infection levels was found between shore and openwater sites, it is imperative to understand the distribution of
infected snails throughout the entire pool. This becomes especially
important as B. tentaculata spreads in distribution, which is likely
now that this invasive snail is in a large river system. In fact,
infected B. tentaculata snails have already been found in Pools 4,
5, 8, and 9 (Sauer et al., 2007). Furthermore, as the abundance
and distribution of this snail increases, infected B. tentaculata are
increasingly likely to mix with populations of native snails. If
native species are susceptible to infection and if they occur in a
high enough abundance, they could be contributing to transmission of these parasites. Therefore, future studies into this system
should include all snail species and be conducted on a larger scale,
including other areas within Pool 7 and neighboring water bodies.
It also seems essential to better understand the role definitive
hosts have in transmitting these parasites from place to place
should B. tentaculata continue to spread to new sites.
ACKNOWLEDGMENTS
J. Nissen and C. Gehri from the U.S. Fish and Wildlife Service have
been invaluable sources of information and assistance. A thank you is
extended to the National Wildlife Health Center, especially R. Cole, for
identification of the trematode species. Many lab members contributed to
field work and data collection. This research was conducted in compliance
of federal laws and under Special Use Permit (#32572-05003) authorizing
research on the UMR Refuge. This project was partially funded by the
Department of Biological Sciences, Minnesota State University Mankato,
Mankato, Minnesota.
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