Table Of ContentJ. Helminthol. Soc. Wash.
64(2), 1997 pp. 169-175
A Transmission Study of Two Sympatric Digeneans:
Spatial Constraints and Solutions
PIERRE BARTOLi AND JOHN C. HOLMES
1 2
1 Laboratoire de Biologic Marine et d'Ecologie du Benthos, EP CNRS No. 75,
Faculte des Sciences de Luminy—Case 901, 13288 Marseille Cedex 09, France and
2 Department of Biological Sciences, University of Alberta, Edmonton, Alberta, Canada T6G 2E9
(e-mail: [email protected])
ABSTRACT: The distributions of infected molluscan hosts of the digeneans Maritrema misenensis, a parasite of
charadriid birds, and Lepocreadium pegorchis, a parasite of sparid fishes, were examined along a transect span-
ning the mediolittoral and upper infralittoral zones at the edge of a protected small bay in southeastern France,
western Mediterranean. In both parasites, the first intermediate host occurs in an area separated spatially from
the definitive host; in each case, only a small fraction of the potential first intermediate hosts, those nearest the
source of eggs, are infected. In both cases, second intermediate hosts overlap in distribution only slightly (or
not at all) with the first intermediate hosts (and, in the case of L. pegorchis, with the definitive hosts). We
analyze the strategies evolved to overcome these spatial constraints on transmission.
KEY WORDS: Maritrema misenensis, Lepocreadium pegorchis, Digenea, Mediterranean, transmission con-
straints, adaptations.
A successful life cycle necessitates that the warmer surface waters when temperatures drop
parasite be adapted not only to each required below about 15°C. Shiff also showed that the
host, but also to the potential ecological prob- miracidia switch from being negatively photo-
lems of transmission between those hosts. The tropic at high temperatures to positively photo-
extent of these problems can be markedly af- tropic at lower temperatures; this switch oc-
fected by the structure of the habitat (Sousa and curred at the same temperature as for the snails.
Grosholz, 1991) and is minimized if all hosts In addition, Goater et al. (1995) found that me-
overlap. As a result, high levels of infection in tacercariae of Psilostomurn brevicolle in cockles
1 host species often show a strong relationship (Cerastoderma edule) were more widely dis-
with proximity to high numbers of the other re- persed in the Exe estuary than were cysticer-
quired hosts (e.g., Robson and Williams [1970]; coids of Microsomacanthus rectacantha. They
Matthews et al. [1985]; Carrol et al. [1990]; suggested that the actively motile cercariae can
Goater [1993]). At relatively large scales, the be more easily distributed by tidal currents than
pattern of overlap can also determine the distri- the passively transported eggs of the cestode,
bution of the parasite. Bartoli (1981) has shown which appeared to be dependent on local trans-
that 2 closely related gymnophallid digeneans of mission. Indeed, Bartoli (1989) and Bartoli and
birds are transmitted in different parts of the Ca- Combes (1986) have shown that a variety of
margue because of differences in the distribu- specific behavioral patterns of cercariae can
tions of the first and second intermediate hosts. bring them from the habitat of the first host to
On a regional scale, K0ie (1983) has provided very different habitats occupied by the second
excellent examples of distributions of parasites intermediate hosts.
of flounder (Limanda limanda) that are limited Protected shallow waters in the Mediterranean
by the distributions of their required molluscan provide particularly good systems to study the
hosts. potential constraints parasites face when their
On smaller scales, hosts of parasites do not hosts do not occupy the same habitats, and to
have to coexist sympatrically if the life cycles investigate the mechanisms that have evolved to
include free-living stages (or a mobile interme- overcome those constraints. The virtual absence
diate host) that can actively migrate between lo- of tides or currents and the very gentle slopes
cations. For example, Shiff (1974) has shown of some bays and lagoons magnify any con-
that, under summer conditions in Zimbabwe, the straints generated by occupation of different
snail hosts of Schistosoma haematobium are habitats by successive hosts and may result in
found in deep, shaded waters but migrate to situations in which only a small part of the po-
169
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BARTOLI AND HOLMES—SPATIAL DISTRIBUTIONS OF SYMPATRIC DIGENEANS 171
tential host population, those occupying a mar- logical aspects, has been reported by Bartoli
ginal habitat, may actually be exposed to infec- (1967, 1983).
tion. This small proportion of the host popula- In this paper, we present quantitative data on
tion may therefore be critical to survival of the the spatial distributions of these parasites in their
local parasite population. molluscan intermediate hosts and identify the
In this study, we examine the distributions of major transmission constraints faced by each of
2 species of digeneans in such a bay. One is a the parasites. We then discuss adaptations of the
parasite of birds, the other of fish. The life cycles 2 parasites to overcome spatial constraints on
of both of these digeneans are well known, and their transmission.
both require molluscan hosts that are distributed
primarily in the very shallow waters not regu- Materials and Methods
larly used by either of these definitive hosts. The study was conducted at the southern edge of the
Maritrema misenensis (Palombi, 1940) adults Bale du Brusc, near the Isle de Embiez, just west of
are found in a variety of charadriiform birds, Toulon, France (in the western Mediterranean). The
bay is protected on 3 sides by 2 islands and the main-
especially Charadrius alexandrinus and C. hia-
land, and on the fourth by an extensive bed of living
ticula. These birds feed along the water's edge, Posidonia oceanica reaching the surface, so is virtu-
never venturing into the infralittoral, but may ally waveless. The bay is small (surface area about 50
defecate while flying over that region, dispersing hectares), shallow (maximum depth 1.2 m), and opens
to the north, facing the dominant winds, the mistral
eggs. The first intermediate host in the bay is the
(Molinier, 1961). Like the rest of the Mediterranean
prosobranch Cerithiurn mediterraneurn Deslayes
Sea, there is a very small tidal flux (±10 cm); there
1843, which occupies the infralittoral, never en- are, however, barometric tides (maximum 30 cm), pri-
tering the mediolittoral. The second intermediate marily due to atmospheric conditions associated with
host is the talitrid amphipod Orchestia mediter- the dominant mistral winds (Hopkins, 1984). The site
is near a private research station (Fondation Scienti-
ranea, which inhabits the beach wrack. This life
fique Ricard) and has been studied extensively as an
cycle was described by Prevot et al. (1976), and example of Mediterranean calm-water areas (e.g., Vi-
an ecological study, from the same bay and the cente [1974]).
surrounding region, was reported by Bartoli and The survey was conducted between 8 and 10 July
1991, along a single 150-m transect perpendicular to
Prevot (1978).
the shore. The transect started at the lower edge of the
Lepocreadium pegorchis (Stossich, 1900)
beach wrack. The first 15 m (the upper mud zone, "1"
adults are found in several sparid and other fish- in Fig. ID) is frequently exposed, and the next 10 m
es (Saad-Fares, 1985) that feed throughout the (the lower mud zone, "2") is occasionally exposed;
bay, except in the shallowest waters. The first the substrate of both is soft and unvegetated. The next
10 m (the sparse seagrass zone, "3") is rarely exposed;
host in the bay is the nassid prosobranch Amy-
the substrate is soft, with scattered seagrass (Cyrno-
clina corniculum (Olivi, 1792), which occurs docea nodosd). These 3 zones, plus that occupied by
mainly in the mediolittoral, and disappears in the the beach wrack, constitute the mediolittoral. The re-
infralittoral, where the seagrass becomes dense. maining part (the infralittoral, "4") is never exposed
and has a dense cover of C. nodosa. At every 5 m
The second intermediate hosts are the venerid
along the transect, the upper 20 cm of substrate within
lamellibranchs Venerupis aurea (Gmelin, 1790)
a 1-m2 iron quadrat were removed and sieved, and all
and Venus verrucosa L. and the cardiid Ceras- individuals of the 3 major species of molluscs involved
toderma glaucum (Bruguiere, 1798), all of in the life cycles (see below) were collected. Snails
which occupy only the infralittoral. In this study, were crushed and examined for sporocysts or rediae;
tissues of the lamellibranchs were removed and
we focussed only on V. aurea, the most common
pressed between 2 glass plates, and all metacercariae
of the second intermediate hosts; the others are of Lepocreadium pegorchis were counted.
rare in this location. This life cycle, and its eco- Voucher specimens of Lepocraedium pegorchis
Figure 1. Transect through the edge of Baie du Brusc, southern France, western Mediterranean. (A)
Distribution of Maritrema misenensis; distribution of definitive and second intermediate hosts after Bartoli
and Prevot (1978). The dashed distribution of the second intermediate host of M. misenensis indicates
migration to the water's edge to replenish moisture supplies. (B) Distribution of potential hosts of Lepo-
creadium pegorchis; distribution of definitive hosts after Bartoli (1983). (C) Distribution of molluscs in-
fected with L. pegorchis. (D) Profile of the studied zone. Note the vertical exaggeration. Region 1 is the
upper mud zone; 2, the lower mud zone; 3, the sparse seagrass zone; and 4, the infralittoral.
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172 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 64(2), JULY 1997
have been deposited in the British Museum (Natural constraint is the minimal (at best) overlap be-
History) (BM(NH)1997.2.17.1-23). Voucher specimens
tween the areas occupied by the definitive hosts
of Maritrema misenensis are in the collection of the
and the snail first intermediate hosts. For M. mis-
senior author.
enensis, infections in C. mediterraneum are con-
Results centrated in a small part of the snail population,
those closest to the source of infection. Note,
Cerithium mediterraneum, the first interme-
however, that because of the very shallow slope
diate host of M. misenensis, is restricted to the
and sandy substrate of the shore, most of the
infralittoral zone, with density being highest in
eggs shed high on the shore are probably lost to
the lower reaches. The trematode, however, at-
rainwater percolating into the sand; relatively
tains its highest prevalences in the few snails in
few are likely to be available to snails. Some
the upper infralittoral (Fig. 1A). Only 24% of
eggs are undoubtedly shed by birds defecating
the snails, but 80% of the infected snails, were
as they fly over the water further from shore;
found in the shallowest 30 m of the dense C.
these eggs are probably the source of the small
nodosa bed; only 3% of the snails in the rest of
proportion of infected snails found further off-
the transect were infected.
shore. For L. pegorchis, infections in A. corni-
Amyclina corniculum, the first intermediate
culum are also concentrated in a small part of
host of L. pegorchis, was found in large numbers
the snail population, this time those closest to
in the lower mud zone and declined rapidly both
deeper water, again the primary source of infec-
above and below that zone (Fig. IB). However,
tion.
the prevalence of the trematode increased rap-
There are 3 possible explanations for these
idly with depth, reaching its highest levels in the
distributions of infected snails: (1) Larger, older
relatively few snails in the upper infralittoral
individuals could preferentially move to the
(Fig. 1C).
"zone of infection" (e.g., Blower and Rough-
Venerupis aurea, the common second inter-
garden [1988]). Such older individuals would
mediate host of L. pegorchis, was widespread,
have been exposed for a longer period and
and in fairly similar numbers, throughout the in-
would therefore be more likely to be infected.
fralittoral (Fig. IB). Because the clams were
No such size-related pattern of distribution was
found in similar numbers throughout the infra-
obvious, but we do not have the detailed size or
littoral, we have used the mean number of me-
age data, for either species, that would allow us
tacercariae per clam (a measure of relative den-
to rule out this possibility. (2) Individuals could
sity) as an index of the true density of metacer-
have been infected in a wider area but exhibit
cariae along the transect. Most of the metacer-
altered behavior, so that they preferentially mi-
cariae (93%) were found in the 21% of the
grate into the "zone of infection" (e.g., Curtis
clams collected from the first 30 m of the upper
[1987, 1990]). The flat topography and relatively
infralittoral, close to the zones occupied by the
long distances make this unlikely, but again, we
infected first hosts (Fig. 1C).
cannot rule out this possibility. If infected snails
do migrate into the zones observed, the altered
Discussion
behavior could constitute an adaptation for
Data from this transect provide a snapshot of transmission. (3) Prevalences of infection could
the distributions of the 2 species of digeneans. be determined by proximity to the source of in-
The distributions differ, but the patterns are very fection, i.e., the area most frequented by the de-
similar. For one of the species, M. misenensis, finitive hosts (and therefore the highest concen-
the pattern is repeatable: Bartoli and Prevot trations of eggs). This is the distribution pre-
(1978) demonstrated similar distributions of in- dicted by diffusion processes. It is clearly the
fected snails at each end of a transect between most parsimonious interpretation; if correct,
one of the islands and the mainland. only those snails that occupy the "zone of in-
In many life cycles, the areas occupied by the fection" are likely to serve as first intermediate
definitive first and second intermediate hosts hosts of these digeneans.
overlap broadly so that their spatial arrange- Different solutions to this constraint have
ments do not constrain transmission. However, evolved in the 2 species of digeneans. In M. mis-
in these 2 digeneans, spatial arrangements do enensis, both prevalence and intensity of infec-
constrain transmission. For both species, the first tion are very high in several species of charad-
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BARTOLI AND HOLMES—SPATIAL DISTRIBUTIONS OF SYMPATRIC DIGENEANS 173
riids (Bartoli, unpubl.). The life span of each encounter the amphipods. Thus, contact between
adult worm appears to be short (no more than 5 the cercariae and the amphipods is a conse-
days), but birds are apparently infected repeat- quence of the behavior of each, which brings
edly throughout the several months they occupy them to the same location (Bartoli, 1986). As a
the region. Each adult worm produces only a result, over 70% of the larger amphipods are in-
relatively small number of eggs (no more than fected (Bartoli and Prevot, 1978).
about 200); these eggs are released only when The second constraint in L. pegorchis is due
the worm dies, is egested with the feces, and to the slight overlap in distribution of the first
disintegrates (Bartoli, unpubl.)- The net result, and second intermediate hosts. Two responses
however, is a large number of eggs deposited have evolved: a long period of shedding cer-
each day over a large part of the year. The mech- cariae (Bartoli, unpubl.) and the behavior of the
anisms evolved to overcome the first constraint cercariae. After release from the snail, the cer-
are therefore low definitive host specificity and cariae swim upwards for a short time, then slow-
a large number of eggs because of high trans- ly descend into the water layer just above the
mission rates to the definitive hosts and a rapid bottom, where they can be sucked into the in-
turnover in the population of adults over a rel- current siphon of the clams. If not taken in by a
atively large proportion of the year. clam, the cercariae may repeat this swimming
Lepocreadium pegorchis also exhibits broad pattern (Bartoli, 1989). Although the cercariae
host specificity (numerous species of sparid and are weak swimmers and spend most of their time
other fishes—Saad-Fares [1985]). However, this close to the bottom (Bartoli and Combes, 1986),
parasite has never been recorded at the high this behavior, along with minor water move-
prevalences or intensities of M. misenensis. The ment, does allow the parasite to extend the dis-
adults are more long-lived (probably more than tribution of its metacercariae somewhat further
1 mo) and release eggs (at the rate of about 10 offshore.
eggs per day) throughout most of this period Lepocreadium pegorchis, but not M. misenen-
(Bartoli, unpubl.). This protracted, low rate of sis, is also constrained by the restricted overlap
egg production provides more opportunities for between the areas occupied by the infected sec-
some eggs to be lain in proximity to the few ond intermediate hosts and the definitive hosts.
potential first intermediate hosts at the edge of In the case of M. misenensis, the extensive over-
the bay. lap between the distribution of the infected am-
Both species are also constrained by the re- phipods and the feeding areas of the charadriid
stricted overlap between the areas occupied by birds make most of the latter potentially avail-
the first and second intermediate hosts. In M. able as definitive hosts for M. misenensis. How-
misenensis, this constraint is due to the fact that ever, for L. pegorchis, only those fish that come
the first host is limited to the infralittoral, where- closest to shore to feed in the waters inhabited
as the second intermediate host lives in the by the infected clams are likely to be definitive
beach wrack, above the water. However, these hosts. Note that metacercariae in the clams fur-
amphipods periodically move to the water's ther offshore should be more available to fish
edge (represented by the dashed extension of the than the more abundant metacercariae in the
range of the amphipods in Fig. 1A) to replenish clams nearest the shore and may play a more
their moisture content (Bartoli, 1986). Females, significant role in the population dynamics of L.
which need to keep the eggs or young in then- pegorchis. An alternative view, that the distri-
brood pouches moist, enter the water more fre- bution of the metacercariae in the clams reflects
quently than males or juveniles and are more the intensity of predation on infected individuals
frequently infected. Even when they enter the by fish, is unlikely. The weak swimming ability
water, however, they are usually far from the of the cercariae (Bartoli and Combes, 1986)
source of cercariae. The primary mechanism se- makes extensive infections far from the infected
lected to overcome this constraint is the behav- snails unlikely. In addition, the metacercariae, in
ior of the cercaria. Immediately after emergence, the labial palps, do not appear to affect the be-
cercariae swim actively to the sea surface, attach havior of the clam (Bartoli, unpubl.), as is so
to the surface film, and capture an air bubble. obvious, for example, in clams infected with
Wind and wavelets push some of the cercariae various species of Meiogymnophallus (Bowers
towards the edge of the water, where they may et al., 1996).
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174 JOURNAL OF THE HELMINTHOLOGICAL SOCIETY OF WASHINGTON, 64(2), JULY 1997
Thus, both species have evolved mechanisms interesting aspects of parasite life histories. Sec-
to overcome these spatial constraints on their ond, similarities in the selection pressures and
transmission in the bay ecosystem. These adap- adaptations would contribute to the correlated
tations are apparently more effective for M. mis- spatial heterogeneity regarded by Lafferty et al.
enensis than for L. pegorchis. However, both (1994) as a significant contributor to community
species also exist in other nearby systems. In processes.
rocky areas adjacent to the bay, and very pos- We expect that spatial constraints and restrict-
sibly in other areas, M. misenensis is capable of ed local distributions may be common in la-
infecting a different (but related) suite of hosts. goons, other protected marine systems (e.g., Laf-
In those rocky areas, the first host is Cerithium ferty et al. [1994]), and particularly in lentic
rupestre and the second is Orchestia montagui. freshwater systems (e.g., Williams and Esch
Once again, C. rupestre is limited to the infra- [1991]), characterized by shallow slopes and
littoral, but O. montagui is limited to banks of weak water movements. In systems with steeper
dead leaves of P. oceanica that accumulate in slopes, where the successive hosts are not as
the supralittoral, and never enters the water. In widely separated, these distributional constraints
this case, the more extensive wave action carries should be less important, as seen in the sandy
the cercariae (with their bubbles) with sea spray ecosystem patterns with L. pegorchis. Such
to the surface of the banks of Posidonia (Bartoli, problems should also be less important in lotic
1986). These banks of P. oceanica retain more or marine systems with more extensive tides,
moisture than does the beach wrack, so that the currents, or wave action, which can transport in-
amphipods do not need to move to the water. fective stages of the parasites over longer dis-
Thus, in this case, the cercariae are carried to tances (e.g., James et al. [1976]).
the normal habitat of the amphipods directly.
Acknowledgments
Bartoli and Prevot point out that far fewer shore-
birds feed in the Posidonia beds than along the We thank 2 anonymous reviewers for com-
shallow lagoon margins. Therefore, this alter- ments on a previous draft. Our collaboration has
native system is probably of less importance to been supported by LBMEB and by NSERC
the maintenance of the life cycle of M. misenen- Canada.
sis in this region. Note that the selection pres-
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