Download Potamopyrgus antipodarum(Mollusca

Hydrobiologia 493: 167–172, 2003.
© 2003 Kluwer Academic Publishers. Printed in the Netherlands.
167
Potamopyrgus antipodarum (Mollusca:Hydrobiidae) in continental aquatic
gastropod communities: impact of salinity and trematode parasitism
Claudia Gérard1 , Alexia Blanc1 & Katherine Costil2
1 UMR
Ecobio 6553, Equipe de Physiologie et Ecophysiologie, Université de Rennes I, Campus de Beaulieu,
Avenue du Général Leclerc, 35042 Rennes Cedex, France
2 Laboratoire de Biologie et Biotechnologies Marines, Université de Caen, Esplanade de la paix, 14032 Caen
Cedex, France
Tel: (+33)0223235037. Fax: (+33)0223235054. E-mail: [email protected]
Received 28 June 2002; in revised form 10 January 2003; accepted 10 January 2003
Key words: Potamopyrgus, gastropods, trematodes, salinity, community structure
Abstract
The structure of gastropod communities was examined from January to June 1999 in four sites of the streams
of Mont Saint-Michel Bay along a gradient of salinity, and the occurrence of larval trematodes infecting snails
was studied. Abundance and species richness of gastropods increased from polyhaline (95 snails, 1 species) to
oligohaline waters (6672 snails, 6 species). Whatever the salinity, the most abundant species was Potamopyrgus
antipodarum, an invasive non-indigenous species that represented 80% of the gastropods. Only one male was found
in P. antipodarum populations suggesting a predominantly parthenogenetic mode of reproduction. Among 7218
gastropods collected, 1.2% were infected by larval trematodes: 5 species in Lymnaea peregra (4.4%), 4 species
in Planorbis planorbis (12.0%), one echinostome in Physa acuta (0.2%), and a new species of Sanguinicola in
P. antipodarum (0.5%). This is the first record of infected P. antipodarum in Europe. No parasites were found in
polyhaline waters. The prevalence per host population varied from 0 to 100% depending on time of collection,
salinity and host species. In the lowest-salinity site, abundance of gastropods and prevalence of trematodes were
negatively correlated. The dominance of P. antipodarum in the gastropod communities is discussed in relation with
euryhalinity, parthenogenesis and weak rate of parasitism.
Introduction
The Mont St-Michel Bay is an assemblage of various ecosystems and has been the object of numerous
multidisciplinary studies (floro-faunistic inventories,
investigations of nutrient flux between ecosystems...).
Based on a synoptic study on the diversity of gastropods in the waters of the terrestrial basin adjacent to
the Bay (Costil et al., 2001), the current investigation
focused on a key-species, Potamopyrgus antipodarum
(Gray) (= P. jenkinsi), a successful invasive species
originally from New Zealand (for reviews, see Haynes
et al., 1985; Ponder, 1988; Hughes, 1996), that can
be classified either as a freshwater or a brackish species (salinity 0–15‰; Siegismund & Hylleberg, 1987;
Hughes, 1996). According to Costil et al. (2001),
there is a gradient of salinity across the terrestrial
basin, but alone this cannot explain the distribution
and abundance of aquatic gastropods. Physiology and
metabolism of the snails may be affected by parasites,
like larval trematodes which have life-history effects,
e.g. on growth, fecundity and survival (for reviews, see
Baudoin, 1975; Thompson, 1985; Hurd, 1990). The
aim of the present study is to investigate the potential
ecological force of parasitism and salinity in structuring aquatic gastropod communities, with special
attention for the invasion of P. antipodarum.
Materials and methods
The Mont Saint-Michel Bay is a basin of 441 km2 in
Western France (48◦ 40 N, 1◦ 40 W), including salt
marshes, polders (lowland claimed from the sea, with
168
Figure 1. Temporal variation of the abundance of gastropods (open circles) and the prevalence of trematodes (closed circles) in the West White
marsh from January to June 1999.
great variation in salinity), the ‘White’ marsh lakes of
Mont-Dol (ancient polders), the ‘Black’ marsh lakes
(old peat cuttings) and coppiced woodland and pasture
(Costil et al., 2001). The four study-sites distributed in
ditches and canals were visited monthly from January
to June 1999. They were significantly different in conductivity and salinity but not different for temperature,
depth and width during the study (Kruskal–Wallis test,
p < 0.05). The mean salinity (± standard error) was
1.00 ± 0.61‰ in Western White marsh (WWM), 1.25
± 0.78‰ in Black marsh (BM), 10.60 ± 1.34‰ in
Eastern White marsh (EWM), and 13.28 ± 5.27‰
in Polders (P). Snails were collected in a 20 m long
stretch of canal during 10 min with a net (mesh-size: 1
mm, square aperture: 0.5 × 0.5 m) over the full depth
of the water column. All gastropods were identified,
measured with a caliper (precision: 0.1 mm) (height
for conical shells, diameter for discoid shells), and
dissected under a stereoscopic microscope to record
parasite infection and sex for gonochoric species. Larval trematodes, when present (sporocysts or rediae,
and cercariae during patent period – no metacercaria
was found), were observed alive and drawn with the
help of a microscope equipped with a camera lucida.
Prevalence was calculated as the percentage of snails
harbouring parasites. Mean values of data are reported as means ± standard error (SE). Mann–Whitney
U and Kruskal–Wallis tests were used for statistical
comparison and results were considered statistically
significant at p < 0.05. Cricket Graph software was
used to calculate regression, and the Spearman coefficient was calculated to determine correlation between
trematode prevalence per month per host species and
snail host abundance.
Results
Structure of the gastropod communities in relation to
salinity (Table 1)
A total of 7218 gastropods in 6 species belonging to
Prosobranchia were collected: Hydrobiidae and Pulmonata: Lymnaeidae, Physidae and Planorbidae in
order of decreasing abundance. Species richness and
abundance decreased with salinity, and only one species, P. antipodarum, was found in polyhaline waters
(Polders). This species represented 80.2% of the gastropods collected from all sites, followed by Lymnaea
peregra (Müller) (12.2%), Physa acuta (Draparnaud)
(5.7%) and Planorbis planorbis (L.) (1.9%). Only
one male was found in the populations of P. antipodarum (May 1999, East White Marsh). Whatever
the site, gastropods fluctuated widely in the monthly
abundance (on the whole, mean abundance = 1203 ±
472), whereas the mean species richness was stable
(on the whole, 4.3 ± 0.2). Temporal fluctuations
of pulmonates, reflecting the vernal breeding period,
169
Table 1. Structure of the gastropod community, fluctuations from January to June 1999 and salinity in 4 sites of the Mont St-Michel Bay: West
White Marsh (WWM), Black Marsh (BM), East White Marsh (EWM), Polder (P) (N = number of gastropods collected, S = salinity (‰), SR =
species richness, F = frequency (%), SE = standard error)
WWM: S ± SE = 1.00 ± 0.61
Potamopyrgus antipodarum (Gray)
Lymnaea peregra (Müller)
Physa acuta (Draparnaud)
Planorbis planorbis (L.)
Anisus leucostoma (Millet)
Armiger crista (L.)
N
SR
BM: S ± SE = 1.25 ± 0.78
Potamopyrgus antipodarum (Gray)
Lymnaea peregra (Müller)
Physa acuta (Draparnaud)
Planorbis planorbis (L.)
N
SR
EWM: S ± SE = 10.60 ± 1.34
Potamopyrgus antipodarum (Gray)
Lymnaea peregra (Müller)
N
SR
P: S ± SE = 13.28 ± 5.27
Potamopyrgus antipodarum (Gray)
N
SR
Jan-99
Feb-99
Mar-99
Apr-99
May-99
Jun-99
N
Mean N ± SE
F
1389
107
5
13
1
0
1515
5
1425
65
80
30
0
1
1601
5
233
34
42
16
0
0
325
4
65
3
4
2
0
0
74
4
64
80
20
16
0
0
180
4
2093
569
262
53
0
0
2977
4
5269
858
413
130
1
1
6672
878 ± 355
143 ± 86
69 ± 40
22 ± 7
0.2 ± 0.2
0.2 ± 0.2
1112 ± 464
4.3 ± 0.2
78.97
12.86
6.19
1.95
0.01
0.01
68
1
0
0
69
2
61
9
1
1
72
4
4
2
0
0
6
2
7
2
0
2
11
3
60
2
0
0
62
2
46
4
0
1
51
3
246
20
1
4
271
41 ± 12
3±1
0.2 ± 0.2
0.7 ± 0.3
45 ± 12
2.7 ± 0.3
90.77
7.38
0.37
1.48
115
0
115
1
41
0
41
1
2
0
2
1
3
0
3
1
15
2
17
2
2
0
2
1
178
2
180
30 ± 18
0.3 ± 0.3
30 ± 18
1.2 ± 0.2
98.89
1.11
41
41
1
3
3
1
35
35
1
16
16
1
0
0
0
0
0
0
95
95
16 ± 7
16 ± 7
0.7 ± 0.2
100.00
were not different from those of the parthenogenetic
ovoviviparous P. antipodarum.
Structure of gastropod communities in relation to
parasitism (Table 2)
The overall prevalence was 1.16% (84 infected among
7218 snails). All gastropod species were parasitized by
larval trematodes, except Anisus leucostoma (Millet)
and Armiger crista (L.) of which a single individual
was collected during the study. Trematodes infecting
pulmonates were found only in the lowest-salinity site
(WWM), and the genus Sanguinicola Plehn that infected the prosobranch P. antipodarum was recorded in
oligo- (WWM, BM) and mesohaline waters (EWM).
No parasite was found in polyhaline waters (P). P.
planorbis and L. peregra were the major host species,
harbouring, respectively, 4 and 5 species with an over-
all prevalence of 11.94 and 4.43%. P. antipodarum and
P. acuta were infected by one species with a prevalence of 0.48 and 0.24%. Whatever the parasite and
host species, infected snails were significantly larger
than healthy ones, and in case of P. antipodarum, no
infected individual carried eggs. The prevalence per
host population varied from 0 to 100% depending on
the time of collection, host species and salinity. In
West White Marsh (WWM), temporal fluctuations of
the collective trematode prevalence and the abundance
of gastropods were interacting (Fig. 1), and abundance of a gastropod species was inversely related to
its parasite prevalence: Prevalence = 15.5 × 10−0.01
Abundance (Spearman coefficient = 0.51, p = 0.015,
N = 24).
170
Table 2. Structure of the trematode community in snail host species from January to June 1999 in 3 sites∗ of the Mont St-Michel Bay: West
White Marsh (WWM), Black Marsh (BM), East White Marsh (EWM); P = prevalence e.g. infected snails × 100 / collected snails, Xip =
xiphidiocercariae, Fur = furcocercariae, Cer = cercariae, Ech = echinostomes, Not = notocotyles. ∗ Absence of infected snails in the polder
WWM
P. antipodarum
L. peregra
P. acuta
P. planorbis
infected snails / total
Total P
BM
P. antipodarum
infected snails / total
Total P
EWM
P. antipodarum
infected snails / total
Total P
Jan-99
Feb-99
Mar-99
Apr-99
May-99
Jun-99
Total P
Larval Trematodes
0.43
9.35
0
15.38
18/1515
1.19
0.49
1.54
0
20.00
15/1601
0.94
0
20.59
0
18.75
10/325
3.08
0
66.67
25.00
100.00
5/74
6.76
0
0
0
6.25
1/180
0.56
0.18
3.34
0
3.77
24/2977
0.80
0.32
4.55
0.24
12.31
73/6672
1.09
Sanguinicola sp.
Xip, Fur, Cer, Ech, Not
Ech
Xip, Fur, Cer, Ech
0
0/69
0.00
0
0/72
0.00
0
0/6
0.00
0
0/11
0.00
1.67
1/62
1.61
19.57
9/46
19.56
4.07
10/271
3.69
Sanguinicola sp.
0
0/115
0.00
0
0/41
0.00
0
0/2
0.00
0
0/3
0.00
6.67
1/17
5.88
0
0/2
0.00
0.56
1/180
0.56
Sanguinicola sp.
Discussion
Salinity is clearly one of the most important abiotic
factors limiting species diversity and influencing the
distribution and abundance of aquatic macroinvertebrates (Colburn, 1988). As shown previously by Costil
et al. (2001) in the Mont St-Michel Bay, fewer species of gastropods are found with increasing salinity:
one species of prosobranch, P. antipodarum, in the
polyhaline waters of the polder versus this one and 5
species of pulmonates at the lowest salinity (WWM).
Among pulmonate species, L. peregra is the most salinity tolerant with an upper salinity limit of 11‰
(Machin, 1975) and it was present in oligo- (WWM,
BM) and meso-haline waters (EWM). The absence
of the other pulmonates in the mesohaline site is explained by their low salinity tolerance (Marazanof,
1969). Unlike most species, the alien prosobranch P.
antipodarum is euryhaline: it lives in waters in which
salinity may reach 26‰ and tolerates for a short time
a salinity of 32‰ (Lucas, 1965). Its salinity tolerance
is linked to osmoregulation processes, e.g. changes in
the osmotic concentration of urine in relation to the
environment, reflecting the capacity of this species to
adapt to variable field conditions. Originally an inhabitant of fresh waters in New-Zealand, it was first found
in Europe in tidal and brackish waters about the last
decade of the nineteenth century, and spread rapidly
to inland fresh waters (Robson, 1923). In freshwater
habitats, the osmotic balance is maintained by excretion of hypo-osmotic urine (Todd, 1964). Furthermore,
life histories are different with respect to salinity, and
for a salinity of 5‰, both freshwater and brackish
populations have a higher mean fecundity, size at maturity and growth (Jacobsen & Forbes, 1997). The
rarity of males in the Mont St-Michel bay (0.02%)
suggests that whatever the salinity, reproduction is
largely parthenogenetic as in New Zealand low-male
populations and all those from Europe and Australia
(Wallace, 1979). In the gastropod communities studied, P. antipodarum is dominant, even in oligohaline
waters where it was competing with sexual native pulmonates, suggesting a great environmental tolerance
and a better competitive aptitude (such as a greater
reproductive rate) of the parthenogenetic clones.
While physical and chemical factors, such as salinity, may exert primary control on community composition, biological factors like parasitism could also
influence species’ distributions and abundances (via
parasitic castration and increased mortality of infected
snails induced by trematodes – for reviews see Baudoin, 1975; Thompson, 1985; Hurd, 1990), as shown
here by the negative association between the density of
gastropods and the prevalence of larval trematodes in
the West White marsh. This relation, suggested for the
marine snail Cerithidea californica by Lafferty (1993)
171
and demonstrated for a lacustrine community of freshwater gastropods by Gérard (1997, 2001), revealed
the potential regulating impact of parasites on their
host populations in the field. Moreover, parasitism is
influenced by salinity: the species richness of trematodes, their frequency of occurrence and the number
of infected snails and host species decrease with increasing salinity. According to Colburn (1988), the
reduced number of species in inland waters as salinity increases could mean less interspecific competition
and fewer vertebrate and invertebrate predators. Consequently, it could also mean fewer parasites, not
only due to their possible low salinity tolerance, but
also, because the life-cycle of trematodes comprises a
molluscan intermediate host and a vertebrate definitive host, and in most species, a second intermediate
host (invertebrate or vertebrate). No infected snail
was collected in polyhaline waters and Sanguinicola
sp. (sporocysts and cercariae), parasite of P. antipodarum, was the single trematode living in oligoand mesohaline waters. Sanguinicola sp. was not recorded by Winterbourn (1973) and Jokela & Lively
(1995) among the 14 species of trematodes in the
New-Zealand populations, and according to Robson
(1923), P. antipodarum was never found infected in
European brackish waters where other species of Hydrobiidae (Hydrobia ulvae, H. ventrosa) were heavily
infected by larval trematodes (sometimes 90%). To
describe this sanguinicolid and its life-cycle, to determine if it is an introduced or indigenous parasite,
and to understand the origin of its recent association
with the introduced hydrobid will be the object of
further studies.
Numerous studies (among them Lively, 1992;
Jokela & Lively, 1995; Dybdahl & Lively, 1998;
Lively, 2001; Lively & Jokela, 2002) have focused
on interactions between P. antipodarum and Microphallus sp. (metacercariae). They indicate that the
quantity of males in New Zealand lacustrine populations is positively correlated to prevalence by larval
trematodes (Lively, 1992), and that, under experimental conditions, rare (vs common) clones were
significantly less infected and had an advantage under
parasite attack (Dybdahl & Lively, 1998). Investigations on the Sanguinicola sp. – P. antipodarum system
in the streams of the bay will provide new data on
parasitism–reproduction–habitat interactions and allow to compare different host–parasite systems where
the same original snail host species acts as the first
(with Sanguinicola sp.) or the second (Microphallus
sp.) intermediate host.
To conclude, in the terrestrial basin of the Mont
St-Michel Bay, the invasive P. antipodarum, dominant species of brackish and freshwater gastropod
communities, is a successful competitor with native
species. This success can be related to a set of welladapted original features: weak rate of parasitism (low
prevalence, with a single parasite species), euryhalinity (osmotic tolerance), parthenogenetic reproduction
(great production of clones). However, it is evident
that other factors, both abiotic (temperature, drying,
pollution...) and biotic (competition and predation),
can influence the performance of P. antipodarum in the
field, and should be examined to provide an explanation of the particular distribution of individual species
and the structure of aquatic communities.
Acknowledgements
We would like to thank V. Briand, M.C. Martin and M.
Steinhart for their help in the field, and J. Jokela and
C.M. Lively for scientific discussions.
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