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THE SPREAD OF AN ALIEN BIVALVE ( MUSCULISTA SENHOUSIA)
IN THE SACCA DI GORO LAGOON (ADRIATIC SEA, ITALY)
M. MISTRI, R. ROSSI AND E. A. FANO
Department of Biology, University of Ferrara, via L. Borsari 46, I-44100 Ferrara, Italy
(Received 7 July 2003; accepted 30 December 2003)
ABSTRACT
The Asian date mussel, Musculista senhousia (Mytilidae), which is endemic in the western Pacific,
appeared and became abundant in the Sacca di Goro, a brackish lagoon in the Po River Delta (northern
Adriatic Sea, Italy) in the early 1990s. The course of the invasion was documented through a macrobenthic monitoring programme at three sites in the Sacca. From 1994, when the new mussel was first
collected, M. senhousia spread throughout the lagoon and, within a few years, reached densities exceeding 10,000 individuals m–2. Mussel effects on biodiversity were assessed by comparing macrobenthic
community structure and composition: over a 5-year period some changes in the macrobenthic community seem to be apparent, suggesting a positive effect of the mussel on the number of species and
benthic richness. Considering trophic guilds, significant positive correlations were found between
M. senhousia and detritivores and herbivores, while suspension feeders probably suffered competition
from the mussel. Musculista senhousia was initially successful because it exploited a naturally disturbed,
sparsely occupied environment. The well-dated documentation of the first collections, increasing
abundance and spread of M. senhousia at our study sites provided an opportunity to observe a biological
invasion of a habitat in progress.
INTRODUCTION
The invasion of non-indigenous species is altering the composition of biotic communities worldwide (Vitousek, 1990). One
species capable of both interspecific effects and habitatalteration is the Asian date mussel, Musculista senhousia (Benson
in Cantor, 1842). The date mussel is an outstanding example of
a species that has dispersed outwards from its native area
through human-mediated transport, establishing sustaining
populations in distant parts of the world. Endemic to the Asian
continent, the date mussel was introduced to northwestern
America in the 1920s (Dexter, 1983), and to Australia and New
Zealand in the 1980s (Willan, 1987). Around the Mediterranean Sea, a few beached shells were found in Tel Aviv in 1964,
and in Bardawil Lagoon in 1969; these Israeli and Egyptian
records, if not accidentally transported, are thought to be
lessepsian migrants of the Red Sea species locally called Modiola
(Arcuatula) arcuatula (Hanley, 1844) (Barash & Danin, 1972).
In the western Mediterranean, M. senhousia was first discovered
in the late 1980s in several lagoons of the Marseille area (Etang
de Tau, Balaruc les Bains, Languedoc-Roussillon, Etang d’Or)
(Hoenselaar & Hoenselaar, 1989), at the beginning of the 1990s
on the northern Adriatic coasts (Lazzari & Rinaldi, 1994), in the
late 1990s in the Gulf of Olbia (Sardinia, northwestern Tyrrhenian Sea) (Savarino & Turolla, 2000), and in 2001 in Mar Piccolo
of Taranto (Apulian Peninsula, Ionian Sea) (Mastrototaro,
Matarrese & D’Onghia, 2003).
Estuaries and brackish water environments are common sites
of biotic invasions (Ruiz et al., 1997). We report here the establishment of M. senhousia in a northern Adriatic lagoon (Sacca di
Goro), and its increase in numbers and spread between 1994
and 1998. The Sacca is a microtidal, coastal lagoon located in
the southernmost Po Delta area. It has a surface area of ~26 km2,
an average depth of ~1.5 m, and receives nutrient-rich fresh
water primarily from two deltaic branches of the Po River. In the
last years, many non-indigenous organisms have been detected
Correspondence: M. Mistri; e-mail: [email protected]
J. Moll. Stud. (2004) 70: 257–261
in the Sacca (Turolla, 1999). Most of these species have the
potential to proliferate and spread, and some of them have
grown to large populations (Mistri, Rossi & Ceccherelli, 1988).
Analyses of species invasions (Carlton et al., 1990) suggest that,
while the success of any given species introduction is not very
predictable, the important factors to be considered are the availability of a suitable habitat, the characteristics of that species,
and the nature of the community present in the invaded area.
Our early detection of the invasion of the Sacca di Goro by
M. senhousia allow us to discuss these factors.
MATERIAL AND METHODS
Three sampling sites (A, B and C) were chosen along a NW–SE
transect, reflecting a gradient of confinement. Site A
(44°50.112N, 12°17.422E) was located in the northernmost,
quite confined area of the Sacca; site B (44°49.617N,
12°18.478E) was located in the central area of the lagoon, and
site C (44°49.094N, 12°19.960E) was positioned in the easternmost part of the lagoon. At the three sites seasonal proliferation
of fast-growing macroalgal beds occurr. A monitoring programme, with monthly/bimonthly sampling frequency, was
conducted between December 1992 and December 1998, and
considered both macroalgal beds and the macrofauna associated with sediments. From the latter date, the monitoring
programme on these sites was interrupted (other studies on the
date mussel have recently been carried out, but in different
areas of the Sacca, e.g. Mistri, 2002).
Macroalgal beds (mostly Gracilaria verrucosa and Ulva rigida,
together with Cladophora liniformis), whenever present, were
sampled from December 1992, in triplicate, by means of a handtowed sledge (40 cm-wide mouth), dragged for 1 linear metre
20 cm from the bottom. Macrofauna associated with macroalgal
beds was separated and counted.
Benthic sampling was initiated in 1994. Sampling was by
means of a Van Veen grab (area 0.06 m2): three randomly positioned replicates were removed from the substratum at each
sampling site; the contents of the grab were gently washed on a
© The Malacological Society of London 2004
M. MISTRI ET AL.
0.5-mm sieve. The material retained on the sieve was fixed in 8%
buffered formalin, and stained with rose bengal to facilitate
sorting and identification. The abundance of individuals of
each taxon, identified to species level when possible, was
measured for each sample. Macrobenthos was also classified
into different feeding groups, identifying guilds such as detritivores (surface-deposit feeders, subsurface-deposit feeders and
suspension feeders), herbivores and carnivores.
Benthic macroinvertebrate community structure was
described at each site at each sampling date on the basis of the
following parameters: abundance (N), number of taxa (S), richness (as Margalef’s d), diversity (as Shannon-Wiener’s H), and
evenness (as Pielou’s J). Differences in univariate indices were
tested using two-way ANOVA with sites and years as fixed factors
and, whenever Levene’s tests indicated significant heterogeneity of variances, the data were log-transformed. Factors
detected to be significant by ANOVA were further analysed
using the a posteriori Tukey HSD test. The effect of M. senhousia
on benthic community structure was tested by means of
Spearman rank-correlation analysis, after recalculation of the
univariate indices excluding the Asian date mussel whenever
present. Rank-correlation analysis was also used to examine
relationships among feeding guilds and mussel occurrence
(obviously after exclusion of M. senhousia from the guild of
suspension feeders), and significance assessed by t-tests.
The initial distribution and increasing abundances of Musculista
senhousia over the total associated fauna to macroalgal beds
from 1992 to 1998 are shown in Figure 1. The first specimens of
Asian date mussel in the Sacca di Goro were collected in April
1994 at site A (2.5 ind. m–2 4.3 SD), in January 1995 at site B
(0.8 ind. m–2 1.5 SD), and in July 1995 at site C (0.4 ind
m–2 1.0 SD). Earlier collections (from December 1992
onwards) contained no M. senhousia, thus it would appear
unlikely that the mussel was abundant in the lagoon prior to
1994. From 1997 onwards, date mussels constituted the most
abundant animal taxon associated with macroalgal mats, with
densities sometimes exceeding 6,000 ind. m–2, e.g. March 1997
at site B (6940 ind. m–2 3,857.9 SD), and December 1998, at
site A (7646.5 ind. m–2 10,516 SD).
From the benthic samples, the first M. senhousia specimens
were collected in December 1994 at site B (3 ind. m–2 2.5 SD),
in January 1995 at site A (5.6 ind. m–2 7.1 SD), and in May 1995
at site C (25.3 ind. m–2 20.8 SD). By autumn 1995 the species
was well established in the Sacca. The time course of M. senhousia (Fig. 2) shows a rapid abundance increase at site C in
1995–96, followed by the other two sites in 1996–97. As might be
expected following such large settlements (e.g. February 1998
at site C: 12,452.6 ind. m–2 10,053.8 SD), densities fell off
dramatically with population ageing during the remainder of
each year. Mismatching abundance patterns at the three sites
further suggest a complex picture of patchy recruitment in
space and time. Since 1996–97 M. senhousia has been the most
abundant benthic macrofaunal organism in the Sacca, generally
occurring in greater numbers than those of any other species
(Fig. 2).
Table 1 reports ANOVA significance for log-transformed
community attributes through the period 1995–1998. Sites dif-
Figure 1. Mean abundance (individuals m–2) of total macrofauna (black diamonds) and Musculista senhousia (white squares) associated with macroalgal
mats at the three study sites, from December 1992 to December 1998.
Figure 2. Mean abundance (individuals m–2) of total macrofauna and
Musculista senhousia (symbols as in Fig. 1) from bottom samples at the three
study sites, from January 1994 to December 1998.
RESULTS
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fered in species number (Tukey HSD test: A vs B and A vs C,
both P 0.05), abundance (C vs A and C vs B, both P 0.01),
richness and evenness (A vs B, P 0.01), and diversity (A vs B
and A vs C, P 0.001 and P 0.05, respectively) while, among
years, differences were evident in number of species (95–96 vs
97–98, P 0.05) and richness (95–96 vs 97–98, P 0.05). The
abundance of M. senhousia correlated positively with macrofaunal abundance at Site C (r 0.62, P 0.001), but negatively
with number of species (r –0.38, P 0.01), richness (r –0.39, P 0.01), and diversity (r –0.29, P 0.05) at Site B.
Table 2 reports Spearman’s rank correlations and their significance through t-tests between abundances of M. senhousia and
trophic guilds (SSDF: subsurface-deposit feeders; SDF: surfacedeposit feeders; SF: suspension feeders; HER: herbivores; PR:
predators). Significant positive correlations were found
between date mussels and SDF at Site A and C, and with HER at
Site C. Conversely, negative correlations were found with SF at
Site B, and PR at both Sites B and C.
Table 1. Two-way ANOVA (factors: sites
and years) on community attributes (logtransformed data).
The absence of M. senhousia from intermediate localities
between Mediterranean areas where the species was first
detected and the northern Adriatic Sea, preclude its natural
transport to the Po River deltaic lagoons. While in Australia and
New Zealand the dramatic increase of Asian date mussel populations are presumed to be due to transfer in the ballast water of
ships (Willan, 1987). The initial invasion of the west coast of
America is attributed to a transport with oysters imported from
Japan (Kincaid, 1947). In the Mediterranean too, the invasion
of the Asian date mussel appears to have been strictly linked to
shellfish farming and trading. Mussel populations inhabiting
French lagoons have probably been introduced with oysters
from Japan (Hoenselaar & Hoenselaar, 1989), and mollusc
farms have served as gateways into Mediterranean coastal
waters. So, we hypothesize that, through a leapfrog effect of further human transfer, M. senhousia in the Sacca di Goro has possibly been introduced with oysters or clams from French cultivation. Finally, Sardinian and Apulian mussel populations have
possibly been introduced with cultured mussels (Mytilus galloprovincialis Lamarck, 1819), which are imported from the northern Adriatic. The sudden arrival of the Asian date mussel in the
Sacca di Goro (but also its spread in other distant areas which all
support mollusc cultures) appears to be related to such an
extensive shellfish trading activity. Many other cases of unintentional introductions of pathogens, parasites and pest species,
resulting from unrestricted transport of commercially important alien bivalves, are known for the Mediterranean Sea (Galil,
2000).
In the Sacca di Goro, we collected the first specimens of M.
senhousia in 1994, but the date of introduction may be difficult to
establish with certainty. It is possible that the mussel was introduced at a considerably earlier date, and underwent an initially
slow population expansion as it established reproducing populations, since many alien species appear to have long lag times
between initial introduction and subsequent population explosions (Crooks & Soulé, 1999). Biological surveys of the region
have been carried out over many years, with intensive benthic
sampling surveys in the Valli di Comacchio in 1974 (Colombo,
Ceccherelli & Gaiani, 1977), in the Sacca di Goro in 1982–84
(Franzoi et al., 1986) and 1989–90 (Ceccherelli et al., 1994), in
the Sacca di Scardovari in 1976 (Ceccherelli et al., 1985) and
1989 (Mistri, Ceccherelli & Rossi, 2000a), and in the Sacca del
Canarin in 1984–85 (R. Rossi, unpublished data); individuals of
uncommon species were sometimes collected during these surveys, but never Asian date mussels. There is anecdotal evidence
that shellfish farmers occasionally began to find uncommon,
small greenish mussels since 1993, which we presume to have
been M. senhousia. In the Sacca di Goro, the colonization process and population spread of the date mussel seemed to have
different dynamics from that exhibited in another well-studied
area (Mission Bay, San Diego, CA, USA) where the mussel
appeared in the mid-1960s, but it was not until the early 1980s
that M. senhousia could be found commonly in high-density
patches (Crooks & Soulé, 1999). In the Sacca, the population
spread of the date mussel was explosive and only a few years after
its first discovery, it carpeted thousands of square meters of the
lagoon’s subtidal. An important role in determining the patchy
F
P
Site
4.21
0.018
Year
3.35
0.023
Site year
0.66
0.679
Site
7.48
0.001
Year
1.91
0.135
Site year
1.21
0.308
Site
4.58
0.013
Year
5.82
0.001
Site year
1.87
0.095
Site
5.28
0.007
Year
1.45
0.233
Site year
1.85
0.1
Site
7.72
0.001
Year
0.62
0.601
Site year
1.81
0.106
DISCUSSION
Number of species (S)
Abundance (N)
Richness (d)
Evenness (J)
Diversity (H)
Table 2. Spearman’s correlations and significance between
abundances of Musculista senhousia and trophic guilds.
Site A
Site B
Site C
M. senhousia – SDF
R 0.269
R 0.34
R 0.461
t 1.527
t 2.4
t 3.24
P 0.137
P 0.021
P 0.002
M. senhousia – SSDF
R –0.307
R 0.072
R 0.27
t 1.767
t 1.476
t 1.751
P 0.087
P 0.636
P 0.088
M. senhousia – SF
R –0.322
R –0.311
R 0.258
t 1.862
t 2.175
t 1.669
P 0.072
P 0.035
P 0.103
M. senhousia – HER
R 0.152
R 0.118
R 0.683
t 0.84
t 0.787
t 5.84
P 0.407
P 0.436
P 0.0001
M. senhousia – PR
R 0.13
R –0.32
R –0.375
t 0.716
t 2.24
t 2.53
P 0.479
P 0.03
P 0.015
259
M. MISTRI ET AL.
1989, 0.0 mg l–1; July 1990, 0.4 mg l–1; Colombo et al., 1994). At
the beginning of the 1990s, to increase seawater inflow the
southern sandbank, which spatially enclosed the Sacca, was
artificially cut. So, when M. senhousia was introduced, the Sacca
di Goro was mostly inhabited by a depauperate benthic community. Depauperate biota and extreme natural disturbance
events are factors known to facilitate non-indigenous species
establishment in new habitats (Cohen & Carlton, 1998). We
suggest that the Asian date mussel was initially successful
because it exploited a naturally disturbed, sparsely occupied
environment.
The dominance of M. senhousia in the macrobenthic community was not limited to these study sites. In fact, the Asian date
mussel has recently spread to most other areas of the Po River
delta, such as Valle Fattibello (Mistri et al., 2000b) and Valle Lido
di Magnavacca (Munari et al., 2003), two enclosed lagoons;
Sacca di Scardovari (E. Turolla, personal communication), an
open lagoon: Logonovo Channel (G. Caramori, personal communication), a tidal creek; and Lido degli Scacchi (M. Mistri,
personal observation), a truly marine site. Ongoing field
sampling in some of these areas will allow us to evaluate better
how successful the mussel is at colonizing other habitats, and its
role in pre-established benthic communities.
distribution of M. senhousia was probably also played by macroalgal mats. In the Sacca, the Asian date mussel spawns from the
end of summer to late autumn (Sgro et al., 2002); later juveniles
will settle onto the bottom during winter, just when pleustophytic macroalgae start their growing season (Viaroli, Pugnetti
& Ferrari, 1992). Spat and dispersing post-larvae may actively
recruit where macroalgal mats are developing because of the
altered physical environment. At relatively low biomass, it is
known that stands of macroalgae may facilitate the recruitment
of fauna through the entrainment of larvae (Raffaelli, Raven &
Poole, 1998). Then, the settled mussels may undergo a secondary redistribution throughout the Sacca by ‘rafting’ on the drifting macroalgae, in response to hydrodynamic conditions.
The successful colonization of the lagoon by M. senhousia suggests that a number of trophic-level effects (direct or indirect
interactions with other guilds), and benthic dynamic effects
(differential inhibition/enhancement of infauna/epifauna due
to substrate alteration) should take place. By removing a huge
volume of suspended organic material from the water column,
M. senhousia deposits that filtered material on the bottom as
faeces and pseudofaeces and thus alters the nature of the sediment (Creese et al., 1997). Mussels may modify the nutritional
quality of sediments (Mistri, Modugno & Rossi, 2003), have
the potential to affect the resident fauna (Crooks, 2001), and
render the environment within or under mats unsuitable to
adults of other species and/or larval recruitment, through
diminishing the depth of the redox potential discontinuity
layer, suppressing growth and affecting survival (Morton, 1974;
Creese et al., 1997; Crooks, 1998). In the Sacca di Goro, from the
community point of view, and over a short-term period
(1995–98), some differences seemed evident between community descriptors through time (number of taxa and richness),
suggesting a positive effect of mussels on at least a part of the
benthic community. We speculate that this may be due to the
fact that M. senhousia creates novel three-dimensional episurface structures that can provide increased habitat heterogeneity on an otherwise soft bottom, including hard-surface
areas and crevices, holes or cracks for the colonization of sessile
and vagile species. These species are likely responding to a
variety of proximate factors that result from the modification of
the habitat, including a refuge from predation, an amelioration
of environmental factors (desiccation and temperature), and
an increase in food supplies for detritivores. De Montaudouin,
Audemard & Labourg (1999) came to a similar conclusion
while studying the effects of the common slipper limpets
[Crepidula fornicata (Linnaeus, 1758)] on macrobenthic assemblages. In the Sacca, differences in macrobenthic community
structure were also detected among sites, but these probably
reflected the gradient from the back to the front of the lagoon
due to different hydrodynamic conditions at the three sites.
From a trophic-dynamic point of view, on the other hand, a
negative relationship was detected between mussel and the
abundance of other suspension-feeders, suggesting strong competitive relationships within the guild. Because M. senhousia is a
densely living suspension feeder, its filtration of near-bottom
water may locally deplete food supplies (Reusch & Williams,
1999) and, as recently observed in Mission Bay by Crooks
(2001), strongly affects other suspension-feeding bivalves.
Furthermore, suspension-feeder mussels could destroy the
larvae of potential recolonizing organisms.
The characteristics of benthic communities in the Sacca di
Goro prior to the arrival of M. senhousia were summarized by
Franzoi et al. (1986). In the 1980s, annual patterns in benthic
community structure in the Sacca were mostly coupled with
limited water circulation and the pattern of development of
macroalgal mats (mostly Ulva rigida). Macrobenthic communities were commonly subjected to harsh summer dystrophic
and anoxic crises (e.g. dissolved oxygen concentration: July
ACKNOWLEDGEMENTS
This study is part of ALIEN (Impatto della specie alloctona
Musculista senhousia su allevamenti di bivalvi di interesse commerciale nell’Alto Adriatico e strategie di contenimento), supported by MiPAF, the Italian Ministry for Agricultural and
Forest Policies, VI Triennial Programme for Fishery and Aquaculture. Dr Elizabeth M. Harper and an anonymous reviewer are
acknowledged for constructive criticism.
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