Download invaders in suspension-feeder systems: variations along the

Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems: variations along the regional
environmental gradient and similarities between large basins. In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
221
INVADERS IN SUSPENSION-FEEDER SYSTEMS:
VARIATIONS ALONG THE REGIONAL
ENVIRONMENTAL GRADIENT AND SIMILARITIES
BETWEEN LARGE BASINS
Sergej Olenin, Darius Daunys
Coastal Research and Planning Institute, Klaipeda University, Klaipeda, Lithuania
Abstract:
Biological invasions increasingly alter taxonomical and functional
structure of benthic communities. Among the invasive benthic
invertebrates, the suspension-feeders are the most widespread type.
Species belonging to that trophic group constitute from half to two thirds
of total invasive species in various European seas. The importance of the
alien suspension-feeders is particularly obvious in evolutionary young,
species poor brackish water bodies, such as the Baltic Sea. We analyzed
changes in suspension-feeder systems formed by both alien and native
species along the salinity and depth gradients from a river mouth (the
Curonian Lagoon) down to the halocline area of the Baltic Proper. There
was a clear shift in the biomass dominance from the alien species in the
lagoon to the native suspension-feeders in the sea. Both the native and
alien obligatory suspension-feeders occupied shallow coastal marine and
lagoon habitats and did not form stable communities below the 30 m
depth.
Key words: bioinvasions, trophic guilds, salinity gradient, functional homogenization
INTRODUCTION
Biological invasions mix previously isolated organisms on global
scale causing their genetic, taxonomic and functional homogenization
(Leppäkoski et al. 2002a, Olden et al. 2004). This human-mediated addition to
local fauna and flora is defined as xenodiversity (Gr. xenos – strange) to
indicate diversity caused by non-indigenous, invasive species (Leppäkoski
and Olenin 2000a). The influence of xenodiversity is traced at different
hierarchical levels of biological organization, including functional/community
level due to alterations of food webs and ecosystem functioning, emergence
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
222
of novel functions, and changes in structure of trophic/functional guilds (e.g.
Olenin and Leppäkoski 1999; Karatayev et al. 2002; Ojaveer et al. 2002;
Baltic Sea Alien Species Database 2003, and references therein).
The importance of biological invasions in alteration of trophic
structure of benthic communities is especially obvious in evolutionarily
young, species-poor water bodies, such as the Baltic Sea (Leppäkoski et al.
2002b). In this study, we consider the suspension-feeding systems formed by
both alien and native species along environmental gradients from a river
mouth (the Curonian Lagoon) down to the halocline area of the Baltic Proper.
The studied habitats differ in topography, substrate, hydrological regime,
biological communities as well as the level and type of human impact.
Analysis of the structural changes along such gradients can give insights into
how physical and biological features of habitats influence the suspensionfeeder systems and their susceptibility to invasion.
Although many recent works address functional changes in benthic
communities caused by invasion on a local scale (e.g. Zettler 1996; Karatayev
et al. 2002) the broader; basin wide aspect of these changes is still lacking. In
this study, we assess the trophic guild composition of invaders in different
geographical regions, investigating how common suspension feeding is
among the invasive benthic invertebrate species. Thus, we consider two
aspects of structural change in the benthic communities, caused by the
invasion of suspension-feeding invertebrates: 1) suspension-feeder systems
formed by both invasive and native species at the scale of a regional habitat
gradient (“invasive versus native”), and 2) suspension-feeding as one of the
trophic types of invasive invertebrate groups at the basin wide scale.
MATERIALS AND METHODS
Study Sites Along the Southeastern Baltic Environmental Gradient
We considered suspension-feeder systems in seven habitats along an
environmental gradient in the southeastern part of the Baltic Sea (Fig. 1). The
Curonian Lagoon is a large shallow (mean depth 3.8 m) coastal water body
connected to the Sea by a narrow (400 m) strait (Klaipeda port area), which is
artificially deepened down to 14 m. In the open sea, the depths ranged from
ca. 5 m in the coastal zone down to 80 m in the halocline area (Table 1).
In the Lagoon, there is a gradient in mean annual salinity from the
Klaipeda Strait (STR, Fig. 1) through the northern part (LAG) towards the
central area (DEL). The later is under strong freshwater influence of the
Nemunas River. Episodic inflows of the sea water cause irregular rapid
(hours-days) salinity fluctuations in the Strait and to a less extent, in the
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
223
northern part of the Lagoon (Daunys 2001 and references therein). In the Sea,
the salinity is relatively uniform and stable down to approximately 55 m,
increasing in the halocline zone (ca. 55-80 m).
Temperature range is most variable in the Curonian Lagoon and more
stable in the halocline area. In summer, the coastal marine areas (COS, COH)
are within a warm upper layer of water, while the intermediate depth zone
(INT) lays beneath the summer thermocline (ca. 25-30 m) within the cold
intermediate water layer (Olenin 1997a and references therein). In winter, the
Lagoon (except the strait) is covered by ice. In the sea the ice occurs only as a
narrow (less than several tens of m) stripe along the shoreline.
Fig. 1. Study sites in the southeastern part of the Baltic Sea: DEL (delta) – the central part of
the Curonian Lagoon in front of the Nemunas River mouth; LAG (Lagoon) – the northern part
of the Lagoon; STR (strait) – the outlet of the Curonian Lagoon (Klaipeda Strait); COS (coastal
soft bottoms); COH (coastal hard bottoms); INT (intermediate depth zone); HAL (halocline
area).
The main bottom sediments in the Lagoon are sand and silt, on sites
with shell deposits (mainly of invasive bivalve Dreissena polymorpha and
native gastropods of the genus Valvata). In the Klaipeda strait, the bottom
sediments are greatly influenced by constant dredging for the waterway
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
224
maintenance. In the Sea, there is a well defined depth dependent gradient in
distribution of bottom substrates, from sand (COS, Fig. 1) and mixture of
stones and gravel (COH) in the coastal zone to silt in the intermediate zone
(INT) and mud with clay in the halocline area (HAL). Wave exposure is the
most important factor shaping stony and sandy bottom biotopes and bottom
macrofauna communities in the coastal zone (COS, COH), where the wave
height may reach up to 8 m. The waves and near-shore currents transport sand
and gravel, that cause strong abrasive effects on benthic organisms in the
uppermost part (<10 m depth) of the coastal slope (Olenin 1997b, and
references therein).
Eutrophication is recognized as the most serious environmental
problem in the Curonian Lagoon and in the coastal areas of the southeastern
Baltic (Olenina and Olenin 2002). Heavy blue-green algae blooms are usual
phenomena in summer and early autumn, especially in the Lagoon. However,
due to intensive mixing of water there is no oxygen deficiency in all studied
sites except the halocline area, where the oxygen content drops sharply from
6-9.5 (saturation 70-100%) to 2 ml/l (saturation <20 %) causing permanent
hypoxia in the lower part of the halocline (Olenin 1997a).
Table 1. Environmental changes along the salinity and depth gradients from the Curonian
Lagoon to the halocline area of the Baltic Sea*. The study sites abbreviations shown in Fig. 1.
DEL
Depth
range,
m
1-3
Salinity
range,
PSU
<0.5
Temperature
range,
°C
0-24
LAG
1-3
0.0-3.0
0-24
STR
5-14
0.5-7.5
0-22
COS
5-30
6.0-8.0
COH
5-30
INT
HAL
Study
site
Bottom
substrate
Wave
exposure
Anthropogenic
disturbance
Sand, silt,
shell deposits
Sand, silt,
shell deposits
Sand,
moraine clay,
artificial hard
substrates
Moderate
Eutrophication
Weakmoderate
Weak
Eutrophication
0-20
Sand
6.0-8.0
0-20
30-55
7.0-8.8
0-11
Stones,
gravel
Silt
55-80
8.0-10.5
3-6
Mud, clay
Strongmoderate
Strongmoderate
Weaknone
None
Eutrophication,
dredging,
industrial and
municipal
wastes
Oxygen
deficiency
* Based on Olenin 1997a; Daunys 2001 and references therein
Thus, there were two well defined environmental gradients in the
study area: one related to the salinity change, from the fully lacustrine or
riverine in the Lagoon’s delta area to the mesohaline conditions of the open
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
225
sea habitats, and another one associated with the depth dependent changes in
hydrodynamic activity and bottom substrates, from the coastal areas down to
the halocline zone.
Sampling of Benthic Macrofauna
The quantitative data used for the analysis of structural changes in
suspension-feeder systems along the environmental gradient were extracted
from the database on benthic macrofauna of the Curonian Lagoon and the
southeastern part of the Baltic Sea (Olenin and Daunys, unpublished).
In the Lagoon, the field material has been collected in May and
October-November between 1980 and 2001 using a 0.025 m² Petersen-type
grab. In the Baltic, collections were made in April and August between 1981
and 2002 using the 0.1 m² Van Veen type grab. On stony bottoms, the
samples were obtained by scraping of macrofauna from the measured surface
of boulders lifted by the grab or a SCUBA diver. All samples were washed
through a 0.5 mm mesh sieve and preserved with 4 % formalin neutralized
with NaHCO3. Further treatment of material was performed according to a
standard procedure (HELCOM 1988). All groups of suspension-feeders were
identified to species level. Biomass was determined as formalin wet weight (g
m-2). A total of 549 samples were analyzed, quantitative data were averaged
for each of the habitats.
Trophic Classification of Benthic Invertebrates
Trophic classification of benthic invertebrates found in the Baltic Sea
was based on works of Turpaeva (1953), Fauchald and Jumars (1979),
Järvekülg (1979), Kuznetzov (1980), Lee and Swartz (1980), TsikhonLukanina (1987) and Pearson (2001) with modifications discussed in our
earlier papers (Olenin 1997a, c; Olenin and Leppäkoski 1999).
Some species (e.g. polychaetes Nereis diversicolor and Pygospio
elegans, gastropods Valvata piscinalis and Viviparus viviparus, bivalve
Macoma balthica, etc) are known to use more than one feeding mode, e.g. to
get particles from the water column (by filtering or using mucus nets) and also
collect detritus from the surface of the bottom sediments (Fauchald and
Jumars 1979; Kuznetzov 1980; Tsikhon-Lukanina 1987). These species were
defined as “facultative suspension-feeders” to distinguish them from those
which exclusively suspension-feed, i.e. “obligatory suspension-feeders”, such
as the bivalve Mytilus edulis trossulus, the barnacle Balanus improvisus or the
bryozoan Electra crustulenta. In our analysis we considered only true benthic
dwelling species, excluding the mobile nektobenthic crustaceans (such as
amphipods Pontoporeia femorata, Bathyporeia pilosa, Chaetogammarus
ischnus and Corophium volutator and the mysids Limnomysis benedeni and
Paramysis lacustris).
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
226
To estimate the proportion of obligatory and facultative suspensionfeeders among invaders, we used recently published lists of invasive species
in the Baltic Sea including Kattegat (Leppäkoski and Olenin 2000b; Baltic
Sea Alien Species Database 2003), North Sea including Skagerrak (Reise et
al. 2002), Black Sea including the Sea of Azov (Gomoiu et al. 2002) and the
Caspian Sea (Aladin et al. 2002). Trophic classification of these species was
based on the same principles as those used in the Baltic Sea.
Statistical Analysis
The similarity analysis of the suspension-feeder species composition
in different habitats along the southeastern Baltic environmental gradients was
performed using multidimensional scaling (MDS) procedure in Primer
software (Plymouth Marine Laboratory, Clarke and Warwick 1994).
RESULTS
Changes in Suspension-feeder Systems Along the Salinity and Depth
Gradients in the Southeastern Baltic Sea
Species Composition
The suspension-feeding benthic macrofauna in the Curonian Lagoon
and the southeastern Baltic Sea was represented by 30 species: 17 of them
were defined as obligatory and 13 as facultative (Table 2).
All polychaetes, hydroids, crustaceans, bryozoans and four bivalves
(Mytilus edulis trossulus, Cerastoderma lamarcki, Mya arenaria and Macoma
balthica) are euryhaline marine or brackish water species, while the rest of
bivalves and all gastropods are of freshwater origin. There are six invasive
species within the studied systems: three obligatory (Cordylophora caspia,
Balanus improvisus, Dreissena polymorpha and M. arenaria) and two
facultative (Marenzelleria viridis and Lithoglyphus naticoides) suspensionfeeders.
The highest total species richness within the studied suspensionfeeder systems was found in the northern part of the Lagoon (LAG, 20
species) and in the delta area (DEL, 19 species), mainly due to presence of the
freshwater bivalves and gastropods (Fig. 2). In these habitats, the only
brackish water suspension-feeders were the invasive species: the hydrozoan
C. caspia and the polychaete M. viridis. The number of invasive species in
these two habitats was comparatively low: 3 - 4 species. The highest ratio of
invasive to native species was in the Klaipeda strait (STR): 5 to 6,
respectively. In the marine habitats (COS, COH and INT) the number of
invasive species was the same as inside the Lagoon (3 – 4 species), while in
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
227
Sabellariidae
CRUSTACEA
Cirripediae
GASTROPODA
Bithyniidae
Lithoglyphidae
Valvatidae
Viviparidae
BIVALVIA
Dreissenidae
Mytilidae
Cardiidae
Myidae
Tellinidae
Unionidae
Sphaeriidae
Balanus improvisus
O
Bithynia tentaculata
B. leachi
Lithoglyphus naticoides
Valvata klinensis
V. piscinalis
V. pulchella
V. trochoidea
Viviparus viviparus
V. contectus
F
F
F
F
F
F
F
F
F
Dreissena polymorpha
Mytilus edulis trossulus
Cerastoderma lamarcki
Mya arenaria
Macoma balthica
Unio tumidus
U. pictorum
Anodonta cygnea
A. piscinalis
Sphaerium corneum
S. nitidum
Pisidium amnicum
Euglesa sp.
O
O
O
O
F
O
O
O
O
O
O
O
O
Electra crustulenta
O
X
DEL
F
F
F
O
O
LAG
Nereis diversicolor
Pygospio elegans
Marenzelleria viridis
Fabricia sabella
Manayunkia aestuarina
STR
O
COS
Cordylophora caspia
COH
HYDROZOA
Clavidae
POLYCHAETA
Nereidae
Spionidae
Species
INT
TAXON/Family
O
F
HAL
Table 2. Composition of native and invasive (highlighted) obligatory (O) and facultative (F)
benthic suspension-feeders in the southeastern Baltic habitats (HAL-DEL, see Fig. 1)
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
BRYOZOA
Membraniporidae
X
X
X
X
X
X
X
X
X
X
228
Invasive
Native
No. of species
20
15
10
5
0
HAL
INT
COS
COH
STR
LAG
DEL
Fig. 2. Changes in number of invasive and native suspension-feeding species along
the southeastern Baltic environmental gradient (HAL-DEL, see Fig. 1).
the halocline zone the suspension-feeding organisms were represented by two
native species only: M. balthica and P. elegans, both being facultative
suspension-feeders.
Due to prevalence of the freshwater suspension-feeders LAG and
DEL habitats clearly differed in species composition from the rest of the
studied sites, where only marine organisms occurred (Fig. 3). The presence of
marine suspension-feeders in the Klaipeda Strait determined the affinity of
this habitat to the COS, COH and INT areas. Finally, the halocline zone
showed clear dissimilarity due to absence of the most of suspension-feeders
common in the upper marine benthic areas.
Biomass
Within the Lagoon, the biomass of suspension-feeders showed a clear
decline trend from the delta area (1037±353 and 139±48 g/m2, invasive and
native species, respectively) towards the strait (7.4±4.2 and 2.7±0.9 g/m2)
(Fig. 4). The invasive species dominated, composing from 73 (in the strait) to
88% (delta) of total suspension-feeder biomass. The zebra mussel D.
polymorpha was the biomass dominant species in the Lagoon (LAG and DEL
areas), while the native unionids were subdominants. In the Klaipeda Strait,
the biomass of the suspension-feeders was low; besides the invasive species
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
229
(B. improvisus and M. arenaria) two native suspension-feeders (M. edulis
trossulus and M. balthica) were dominant on sites. All four species are of
marine origin, having no stable populations in the strait. In contrast, their
biomass in the marine areas was higher by one-two orders of magnitude.
Within the marine suspension-feeder systems, the highest biomass (925
and 97 g/m2, native and invasive species, respectively) was characteristic for
the coastal hard bottoms, dominated mostly by the blue mussel M. edulis
trossulus with the barnacle B. improvisus as the subdominant.
Fig. 3. The MDS plot based on suspension-feeding species composition in the study sites along
the southeastern Baltic environmental gradient (HAL-DEL, see Fig. 1).
The Baltic tellin, M. balthica, a facultative suspension-feeder, was the
most important biomass dominant species (up to 95% of total) throughout all
soft bottom habitats, from the coast down to the halocline area. The invasive
soft clam M. arenaria, an obligatory suspension-feeder, was the subdominant
in the COS area; however it did not occur in the deeper (INT, HAL) habitats.
Another obligatory suspension-feeder dwelling in the soft bottoms, the
Lagoon cockle C. lamarcki also was found only in the coastal areas.
SUSPENSION-FEEDERS AND OTHER TROPHIC TYPES OF
INVASIVE BENTHIC MACROFAUNA
The total number of invasive benthic invertebrate species presently
known from the Caspian, Black, Baltic and North Seas is 94. Their feeding
types are as diverse as that of native macrofauna, including suspension and
deposit feeders, herbivores, omnivores and predators. The invasive
suspension-feeding macrofauna comprised 64 species: 41 obligatory and 23
facultative suspension-feeders (Table 2, Fig. 5).
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
230
Invasive
Native
1000
100
10
Biomass, g/m2
10000
1
HAL
INT
COS
COH
STR
LAG
DEL
Fig. 4. Changes in biomass of invasive and native suspension-feeding species along the
southeastern Baltic environmental gradient (HAL-DEL, see Fig. 1).
Table 2. Species richness in major taxonomic groups of invasive obligatory (O) and facultative
(F) suspension-feeders in the Caspian, Black, Baltic and North Seas*.
Caspian
Taxon
Anthozoa
Hydrozoa
Polychaeta
Crustacea
Gastropoda
Bivalvia
Ectoprocta
Entoprocta
Tunicata
TOTAL
O
Black
F
O
3
1
2
2
1
1
1
2
Baltic
F
3
2
2
2
O
North
F
O
4
4
3
4
1
3
3
5
4
1
1
1
1
6
1
2
5
2
O
5
1
1
1
1
1
9
Total**
F
4
12
6
16
1
9
23
8
4
12
5
4
1
8
4
2
1
41
F
11
6
2
4
23
*Based on: Leppäkoski and Olenin 2000b; Reise et al. 2002; Gomoiu et al. 2002; Aladin et al.
2002; Baltic Sea Alien Species Database 2003.
** Species common for two or more regions were counted once.
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
231
The most diverse groups among the invasive suspension-feeders were
cnidarians (both anthozoans and hydroids, together comprising 16 species)
and polychaetes (16 species), followed by bivalves (12 species) and
crustaceans (10 species). In the later group, all obligatory suspension-feeders
were represented by barnacles only (Balanus amphitrite, B. improvisus, B.
eburneus and Elminius modestus).
Seventeen invasive suspension-feeder species were common to at
least two of the studied regions; four species (the barnacle Balanus eburneus,
the mud snail Potamopyrgus antipodarum, bivalves Crassostrea gigas and M.
arenaria) were found in three seas and one species (B. improvisus) occupied
all four regions. The total number of invasive suspension-feeders was the
highest in the North Sea (31 species), 17 of them did not occur in the other
Fig. 5. The share of obligatory (OSF) and facultative (FSF) suspension-feeder species
among other trophic types of invasive benthic invertebrates in various European Seas
(n = total number of species). Other feeding types included predation, deposit feeding
and grazing on macrophytes.
three regions. The number of such “unique” species in the Black and in the
Baltic Sea was the same (11), while there were fewer (8) in the Caspian Sea.
Although the share of suspension-feeders varied slightly from 61% in
the Baltic to 72% in the North Sea, the general rule was that this feeding type
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
232
was the most common among the invasive bottom macrofauna species (Fig.
5).
DISCUSSION
Native and Invasive Suspension-feeders: Similar and Dissimilar
Distribution Patterns Along the Environmental Gradients
Many works on trophic distribution along environmental gradients
have shown that the diversity and biomass of the suspension-feeding
macrofauna are the highest in coastal areas with active hydrodynamics, and
both parameters gradually decline with increasing depth (e.g. Kuznetzov
1980; Dame 1996; Boaventura et al 1999 and references therein). In our study
area, this model of suspension-feeder distribution along the depth gradient
was true for both native and invasive species (Fig. 2 and 4, Table 2). For
instance, the most indicative group, the obligatory suspension-feeders (either
native or invasive) reached the highest biomass only in the Lagoon and
coastal habitats, while in the intermediate depth zone they were insignificant
and absent in the halocline area.
In contrast to the depth/hydrodynamics related distribution there was
no common pattern in native and invasive suspension-feeder systems in
relation to the salinity gradient. The native species richness is essentially
higher in the nearly lacustrine conditions of the Curonian Lagoon (DEL and
LAG sites) than in the mesohaline environment of marine habitats. This result
fits well into the classical Remane (1934) curve showing that within the
gradient from the fresh to fully saline marine waters the minimum in species
number corresponds to the salinity range of 5-8 PSU. In our case, this matches
the salinity in COS, COH and INT habitats. Despite the higher salinity in the
HAL habitat, the number of native suspension-feeder species was the lowest
in this deeper zone due to depleted oxygen and weak hydrodynamic activity.
Bonsdorff and Pearson (1999) also showed the overall gradual decrease in all
functional groups of benthic macrofauna, including suspension-feeding
species, from the fully marine Baltic approaches to its inner brackish water
parts.
Distribution of the invasive suspension-feeder species, nevertheless,
did not follow the same pattern. Their highest number was found in Klaipeda
Strait, i.e. where the salinity regime is most variable. However, here these
species did not form stable populations being dependant on larvae transport
either from the Sea or from the Lagoon (Daunys 2001). The number of
invasive species in the remaining habitats, except the halocline zone, was
nearly the same: 3 - 4 species (Fig. 6).
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
233
Fig. 6. Number of invasive suspension-feeder species plotted against the number of native
suspension-feeder species in the southeastern Baltic benthic habitats (HAL-DEL, see Fig. 1)
This “breach” of the Remane’s rule by the invasive suspensionfeeders may be explained by their ecological plasticity, which is generally
characteristic for invaders (e.g. Carlton 1996, Ruiz and Hewitt 2002). In the
Baltic Sea, most of the alien benthic invertebrates, including the suspensionfeeders, originate from the brackish waters of the North American east coast,
the Ponto-Caspian region and the South-East Asia (Leppäkoski et al. 2002b).
Capability to cope with low salinity conditions is the common trait of these
mostly estuarine species, and this probably explains why their distribution
within the salinity range 0 – 8 PSU did not follow the native species pattern.
Studies on invasive suspension-feeder systems across a broader salinity
interval may determine if these generalizations are also true for other brackish
water seas.
Invasive Versus Native: Occupation of Empty Niches and Species
Displacement
We noticed a clear shift in the biomass dominance from the invasive
species in the Curonian Lagoon (D. polymorpha) to the native suspensionfeeders in the Baltic Sea (M. edulis trossulus, M. balthica). D. polymorpha is
known to inhabit fresh waters, where the niche of sessile byssate suspensionfeeders is usually unoccupied (Orlova 2002; Burlakova et al. 2004). In the
oligohaline stable salinity coastal waters of the north-eastern Baltic, the zebra
mussel may co-occur with the native M. edulis trossulus on sites, though it
does not displace the later (Kotta and Møhlenberg 2002).
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
234
Another invasive suspension-feeding species within our study area,
which was able to fill an empty niche, was the barnacle B. improvisus. This is
the only sessile benthic animal which is able to withstand harsh conditions of
constant wave action and abrasive effect of sand in the uppermost part of the
coastal slope (Olenin and Daunys, unpublished). The barnacles form seasonal
settlements on large boulders (at the depth < 1.5 m), which usually disappear
in winter time. The third example is the hydroid Cordylophora caspia, which
produces dense bush-like colonies on firm substrates both in the Lagoon and
in the Sea.
In spite of these three examples, our results do not support theories
predicting that species-rich communities should be more resistant to invasions
because of a more complete utilization of resources (see Ruiz and Hewitt
2002 for a comprehensive review). The number of invasive suspensionfeeders was the same in the comparatively species-rich communities of the
Curonian Lagoon and in the species-poorer Baltic marine communities.
The significance of species invasion for functional changes might be
much higher in species poor communities than in species rich ones. Variety of
species of the same functional guild within a system (functional redundancy)
may be a measure of the overall system’s ability to perform a given function.
Extinction of a species in the Baltic Sea may cause the loss of entire process
(e.g. biodeposition), while the same event, e.g., in the North Sea would mean
only a minor shift in the species composition and overall role of the functional
group. The invasion of new species in such species poor systems as the Baltic
Sea in many cases means the increase in functional redundancy and denser
“packing” of available niches. In the Baltic Sea, invasions have caused serious
structural and functional changes, especially in its coastal Lagoons and inlets
(Olenin and Leppäkoski 1999), however they have not yet triggered extinction
of native species.
INVASIVE SUSPENSION-FEEDERS AND FUNCTIONAL
HOMOGENIZATION OF AQUATIC BIOTA
Asmus and Asmus (2004) showed that the share of suspensionfeeding species in total species number is much lower than that of non
suspension-feeders on different scales from global to local ones, suggesting a
minor influence of suspension-feeding type to total diversity of systems. Our
study, however, showed an opposite result in regard to the invasive benthic
macrofauna. In all major European brackish water bodies (Baltic, Black and
Caspian seas) as well as in the fully saline North Sea, suspension-feeding was
the prevalent trophic type among benthic invertebrate invaders.
It is unclear, how the species ability to filter-feed may promote their
invasion success. Possibly, suspension-feeding as the most optimal foraging
Olenin, S. Daunys, D., 2005. Invaders in suspension-feeder systems:variations along the regional
environmental gradient and similarities between large basins.
In: Dame, R. and Olenin, S. (ed-s). The Comparative Roles of Suspension-Feeders in Ecosystems.
NATO Science Series. Earth and Environmental Series – Vol. 47. Springer, 2005: 221-237
235
strategy (Gili and Coma, 1998) adds to other common traits of invaders:
ecological plasticity, profitable reproductive strategy, ability to use different
substrates, etc (Ruiz and Hewitt 2002 and references therein). Increased
pelagic food through eutrophication may also promote the relative success of
suspension-feeder invaders, especially in the coastal areas, which are mostly
exposed to new introductions. Further studies on these observations may help
to better identify potential successful benthic invaders.
Olden et al. (2004) consider ecological and evolutionary
consequences of biotic homogenization caused by invasions, including the
functional ones. Our findings indicate that the suspension-feeders are the
prevalent group among invasive benthic invertebrates and assume the vector
of that functional homogenization. If the rate and the scope of invasions
remain at the recent high level then the role of suspension-feeding as a trophic
type will grow in the future.
ACKNOWLEDGEMENTS
This study was supported by the EU FW6 project EVK3-CT-200100065 CHARM “Characterization of the Baltic Sea Ecosystem: Dynamics
and Function of Coastal Types” and EU FW6 IP 506675 ALARM “Assessing
Large-scale environmental risks with tested methods”. We thank Erkki
Leppäkoski (Åbo Akademi University, Turku, Finland) and an anonymous
reviewer for their comments and suggestions to improve this manuscript.
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