ALIEN SPECIES STEFAN NEHRING KARSTEN REISE NORBERT DANKERS PER SAND KRISTENSEN - NEOBIOTA (BFN)
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7 Alien species
WADDEN SEA ECOSYSTEM No. 25
Quality Status Report 2009
Thematic Report No. 7
Alien Species
Stefan Nehring
Karsten Reise
Norbert Dankers
Per Sand Kristensen
2009
Common Wadden Sea Secretariat
Trilateral Monitoring and Assessment Group
Wadden Sea Ecosystem No. 25 2009
7 Alien species
Colophon
Publisher
Common Wadden Sea Secretariat (CWSS), Wilhelmshaven, Germany;
Trilateral Monitoring and Assessment Group (TMAG).
Editors
Harald Marencic, Common Wadden Sea Secretariat (CWSS)
Virchowstr. 1, D - 26382 Wilhelmshaven, Germany
Jaap de Vlas, Rijkswaterstaat, Waterdienst
NL - Lelystad, The Netherlands
Language support
Seabury Salmon
Lay-out and technical editing
Common Wadden Sea Secretariat
Graphic support
Gerold Lüerßen
Published
2009
ISSN 0946896X
This publication should be cited as:
Stefan Nehring, Karsten Reise, Norbert Dankers and Per Sand Kristensen, 2009. Alien species. Thematic
Report No. 7. In: Marencic, H. & Vlas, J. de (Eds), 2009. Quality Status Report 2009. WaddenSea Ecosystem
No. 25. Common Wadden Sea Secretariat, Trilateral Monitoring and Assessment Group, Wilhelmshaven,
Germany.
Wadden Sea Ecosystem No. 25 2009
7 Alien species
1. Introduction
The dispersal of organisms is a natural process agreements, and to offer the signatory states
limited by multiple barriers, among which geo possibilities to deal with alien species. However,
graphical barriers are the most evident. However, until now, most of these measures have so far only
for centuries, alien species have been introduced been declarations of intentions which lack the
to new areas in which they were previously ab extensive detailed planning necessary to prevent
sent and to which they have been introduced by alien introductions. Therefore, the implementation
humans as mediator. With increasing global trade of sound strategies and instruments to deal with
the introduction of alien species, both intentional biological invasions must be an urgent conserva
and unintentional, has increased concomitantly tion priority.
and has increased in complexity. Next to global Especially in the Wadden Sea area, a diverse
habitat loss and climate change, this biological range of alien species has established permanent
globalization has become a key process in altering populations (Reise et al., 2005). The rate of alien
the biosphere. introductions is continuously increasing and no
Alien species bring both costs and benefits change is as yet in sight. Many of the introduced
which may accrue to different sectors of soci species have become abundant and several can
ety. Benefits are wide-ranging and examples in be regarded as invasive in the sense of having
the aquatic environment include stocking and a significant effect on the recipient ecosystem
re-stocking operations, new aquaculture op (Jensen and Knudsen, 2005; Wolff, 2005; Gollasch
portunities and tools in coastal protection and and Nehring, 2006). The guiding principle of the
reclamation schemes (a.o. Minchin and Rosenthal, trilateral Wadden Sea policy “is to achieve, as far
2002). By contrast, viewed on a global basis, alien as possible, a natural and sustainable ecosystem in
species are one of the key threats to native species which natural processes proceed in an undisturbed
and ecosystems and other aspects of biodiversity way”. Invasive alien species pose a particularly
(Rabitsch et al., 2008). Furthermore, biological serious threat to such nature conservation inter
invasions may turn into serious threats to humans, ests. Moreover, as concluded in the Quality Status
their health and economical possibilities. In Ger Report 2004, species introductions are irreversible
many for example, the economic losses caused and accumulating over time. This issue may be
by only 20 analysed terrestrial and aquatic alien considered to be more important than reversible
species are estimated to a level of 156 million effects of overfishing, eutrophication and con
Euro annually (Reinhardt et al., 2003). We here taminants. For the Wadden Sea, the net effect of
consider the effects of alien species on the envi unhampered introductions would be a regional
ronmental quality of the Wadden Sea, and thus increase in species richness and a growing biotic
adopt a nature protection perspective. similarity with other coasts. The unique character
The worldwide implications of alien species of the Wadden Sea would still be manifest in the
have been identified by both non-governmental physical environment but not any more in its
and governmental organizations, and have been living component (Reise et al., 2005). However,
emphasized in numerous international conven up to now a purposeful strategy on how to deal
tions and other legally binding and non-binding with alien species introduced into the Wadden
instruments (Shine, 2006). On the basis of the Sea is lacking (Nehring and Klingenstein, 2005).
Convention on Biological Diversity (CBD, 1992), To respond effectively to threats by alien species,
the European Strategy on Invasive Alien Species the trilateral policy and management should
was finalized in 2003 (Council of Europe, 2003) take the issue of alien species into account to a
to combine existing regulations established under greater extent.
the Bern Convention in 1979 and its subsequent
Wadden Sea Ecosystem No. 25 2009
7 Alien species
2. Instruments and impact assessment
More than fifty international and regional conven the issue. Thus we propose a set of key terms and
tions, codes of conduct and other instruments now definitions as an operating tool (see box below)
deal directly or indirectly with the spreading of that does not lead to further confusion. The set
alien species (SCBD, 2001; Shine, 2006). Nearly all is based on terms and definitions mainly used in
of them have their own institutional mechanisms work done under the Convention on Biological
and decision-making procedures. These binding Diversity (CBD, www.biodiv.org).
or voluntary instruments often provide the base The aims of the Convention on Biological Diver
line from which domestic legislatures develop sity, which was adopted in 1992 and enforced in
policy, legislation and management frameworks 1993, are the conservation of biological diversity,
to address alien species issues (Council of Eu the sustainable usage of biological resources, and
rope, 2003). The main international instruments the fair and equitable sharing of benefits arising
for nature conservation that specifically address from the use of genetic resources. Article 8 of the
alien species includes the Convention on Biologi Convention requires all Contracting Parties “as
cal Diversity (Rio de Janeiro, 1992), the Conven far as possible and as appropriate, to prevent the
tion on the Conservation of Migratory Species introduction of, control or eradicate those alien
of Wild Animals (Bonn Convention, Bonn, 1980), species which threaten ecosystems, habitats or
the Convention on the Conservation of European species”. This statement was specified by the de
Wildlife and Natural Habitats (Bern Convention, cision VI/23 “Guiding Principles on Invasive Alien
Bern, 1979), and the Convention on Wetlands of Species” by the 6th Conference of the Parties to
International Importance as Waterfowl Habitat the Convention in 2002. Its adoption suggests
(Ramsar Convention, Paris, 1994). However, in comprehensive national strategies on the basis of
struments at all levels use variable terminology, a hierarchical approach (prevention, early detec
sometimes inconsistently or without adequate tion, measures).
definitions. On the other hand, a consensual set The Bonn Convention highlights in Article III.4.c
of definitions regarding alien species is essential that the Contracting Parties agree “to the extent
in order to facilitate discourse among the science, feasible and appropriate, to prevent, reduce or
policy and management communities dealing with control factors that are endangering or are likely
Definitions Introduction
The transfer, by direct or indirect human agency,
Native species of a species or genetically distinct population
A species, including genetically distinct popula outside of its natural range (past or present) and
tions, occurring within its natural range (past dispersal potential; this movement can be either
or present) and dispersal potential (i.e. within within a country or between countries or areas
the range it occupies naturally or could occupy beyond national jurisdiction. Human involve
without direct or indirect introduction or care ment here does not include habitat changes,
by humans). global warming, eutrophication, etc.
Alien species Intentional introduction
A species, including genetically distinct popula Deliberate transfer and/or release by humans
tions, occurring outside of its natural range (past of a species or genetically distinct population
or present) and dispersal potential (i.e. outside outside its natural range (past or present) and
the range it occupies naturally or could not oc dispersal potential (such introductions may be
cupy without direct or indirect introduction or authorised or unauthorised); this includes also
care by humans); includes any part, gametes or species which subsequently escape or which are
propagules of such species that might survive released into the environment.
and subsequently reproduce.
Unintentional introduction
Invasive alien species All other introductions which are not inten
An alien species which is known or expected to tional; this also includes parasites, symbionts
exert effects on native populations and species, etc. of intentionally introduced species.
natural habitats and ecosystems beyond of
which can be considered to be within the range
of average regional conditions.
Wadden Sea Ecosystem No. 25 2009
7 Alien species
to further endanger [migratory] species, including eleven qualitative descriptors, one of them being
strictly controlling the introduction of, or control- “Non-indigenous species”. In Annex 1 of the Direc
ling or eliminating, already introduced exotic spe- tive it is mentioned as: “Non-indigenous species
cies.” Article V.5.e of this Convention states that introduced by human activities are at levels that
Contracting Parties should protect “habitats [of do not adversely alter the ecosystems”.
migratory species] from disturbances, including For coastal and inland wetlands, the Ramsar
strict control of the introduction of, or control of Convention has recognized the threat to their
already introduced exotic species detrimental to ecological character and to terrestrial and marine
the migratory species”. wetland species if alien species become invasive.
The Bern Convention, to which 39 European In Resolution VII.14 (1999) on invasive species
states and the EC are party, provides a regional and wetlands Contracting Parties are urged, where
framework for implementation of the Convention necessary, to adopt legislation or programmes to
on Biological Diversity in Europe (Council of Eu prevent introduction of “new and environmentally
rope, 2003). Article 11.2.b of the Bern Convention dangerous alien species” into their jurisdiction and
states, that Contracting Parties should “strictly to develop capacity for identifying such alien spe
control the introduction of non-native species”. cies. In Resolution VIII.18 (2002) the Conference
Bern Convention Parties should also inform gov of the Parties to the Ramsar Convention urged
ernments of neighbouring countries if accidental Contracting Parties to address the problems posed
introductions have occurred (Recommendation by invasive species in wetland ecosystems in a
No. R (84) 14, 1984) and set up mechanisms for decisive and holistic manner. Further, Contract
inter-State co-operation, notification and consul ing Parties are urged to identify the presence of
tation in order to co-ordinate precautionary and invasive alien species in Ramsar sites and other
control measures for invasive species (Recom wetlands in their territory, the threats they pose
mendation No. 77, 1999). to the ecological character of these wetlands, and
In 2000, the Bern Convention’s expert group on to undertake risk assessments of alien species that
invasive alien species began developing elements may pose a threat to the ecological character of
for a European Strategy on Invasive Alien Species. wetlands.
The finalized European Strategy, approved by the Despite these and other efforts, alien species
Bern Convention Standing Committee in 2003 in the Wadden Sea are still perceived only at a
(Recommendation No. 99), is a comprehensive descriptive level. To mitigate present, and avoid fu
document addressed to nature conservation agen ture, negative impacts of aliens in the Wadden Sea,
cies and all other sectoral agencies with respon legal and organisational implementation in the
sibility for activities relevant to the prevention or three bordering countries, Denmark, Germany and
management of invasive alien species (Council of The Netherlands are of utmost importance. How
Europe, 2003). The European Strategy promotes ever, invasion processes ignore political boundaries
the development and implementation of national between countries. Consistent with the ecosystem
strategies, coordinated measures and cooperative approach as developed under the Convention
efforts throughout Europe to prevent or minimise of Biological Diversity, inter- and intra-regional
adverse impacts of invasive alien species on Eu cooperation is essential for effective frameworks
rope’s biodiversity, as well as their consequences and development of an alien management plan
for the economy and human health and well-being on the level of the Trilateral Cooperation on the
(Council of Europe, 2003). Protection of the Wadden Sea. Efficiency can be
The recent Marine Strategy Framework Direc increased by sharing information and intensifying
tive (European Parliament and Council, 2008) cooperation, ensuring basic consistency in policies,
extends EU water legislation to the marine en legislation and practice.
vironment and follows an approach similar to The impacts of alien species on ecosystems vary
that of the Water Framework Directive (European significantly depending upon the invading species,
Parliament and Council, 2000). It came into force the extent of the invasion, and the vulnerability
on 15 July 2008 and establishes a comprehen of the ecosystem being invaded. An initial step
sive structure within which Member States are towards an alien management plan is to assess and
required to develop and implement cost effective present the evidence that invasive alien species
measures, necessary to achieve or maintain Good are a major threat to natural biodiversity in that
Environmental Status (GES) in the marine environ area and that action is mandatory to be taken. The
ment. GES must be achieved by the year 2020 at preparation of a preliminary assessment is a crucial
the latest. Within the Directive, GES is defined by step and should be based on existing information,
Wadden Sea Ecosystem No. 25 2009
7 Alien species
which can be accessed from various sources (lit species which cause serious harm. However, spe
erature, databases, etc.). Loss and degradation of cies lists and the according decision-making needs
native biodiversity due to alien species can occur to be based on transparent scientific criteria that
throughout all levels of biological organization are regularly reviewed and on accurate, precise,
from the genetic and population levels to the generally applicable, and widely accepted assess
species, community, and ecosystem levels, and ment protocols. Various methods of performing
may involve major alterations to physical habitat, risk analyses on specific groups of alien species
water quality, essential resources and ecological have been employed (e.g. Morse et al., 2004; Copp
processes. These impacts can vary in terms of the et al., 2005; Hewitt et al., 2006), but there is still
lapse of time between the initial introduction no international standardised methodology.
and subsequent spread of an alien species, its For German nature conservation activities,
severity of impact, the likelihood of synergistic criteria based risk assessment for evaluating the
interactions with other threatening processes, ecological threat of both alien plants and ani
and the potential for initiation of a cascade of mals in aquatic (freshwater, brackish and marine
effects ramifying throughout an entire ecosystem waters) and terrestrial habitats are now being
(Mooney and Hobbs, 2000; Kowarik, 2003; Reise developed (Essl et al., 2008). The method allows
et al., 2006). allocating species (or infraspecific taxa, as ap
Up to now, concern has been mainly confined propriate) in one of the three following impacts
to the species level and introductions from outside categories: invasive (Black List), potential invasive
the Northeast Atlantic biogeographic province. (Grey List), and non-invasive (White List). The
This may be too narrow in perspective. Particularly, main focus is on threats imposed by alien species
benthic species may show considerable genetic on native species which can be summarized into
structure variation within that region (i.e. Lut five general categories:
tikhuizen et al., 2003a; Olsen et al., 2004). This • Hybridisation with native and other alien spe
may not be surprising for benthic organisms lack cies, producing reproductive offspring;
ing pelagic means of dispersal, but it also seems to
• Competition;
occur in species with pelagic larvae, such as the
European cockle Cerastoderma edule (Krakau et • Predation and herbivory;
al., submitted) and Macoma balthica which even • Introduction of parasites and disease agents
shows genetic differences between the Wad which affect indigenous species;
den Sea and adjacent North Sea coastal regions • Habitat alteration, resulting in changes of
(Luttikhuizen et al., 2003b). Obviously, shifting biological structures and water budget.
organisms from one coast to another, a common
These threats have to be considered in the con
practice in aquaculture with mussels and oysters,
text and in conjunction with other effects in the
may dilute the adaptations evolved within local
ecosystem such as the provision of a novel and
populations. It is probable that this practice has
beneficial food supply, a more efficient coastal
contributed to the collapse in many local popula
filter function, diversion of parasites from native
tions of the European oyster in the 19th and early
to introduced species or the provision of complex
20th centuries. We usually lack sufficient genetic
habitat structures where none have been before.
information and the knowledge to anticipate the
The basis for assessment is the net endanger
effects of lost subspecific adaptations. This is ur
ment of native species by alien species, e.g. verified
gently needed, as is evident from recent transfers
by listing in a Red List. Distribution in the assess
of mussels from British coasts into the northern
ment area, the applicability of control measures
Wadden Sea which may entail the introduction
and specific bio-ecologically traits (e.g. occurrence
of alien genes. In order to protect intraspecific
in protected areas, reproduction and spreading
genetic diversity, alien proveniences of native
potentials, facilitation by climate change) serve
species (“gebietsfremde Herkünfte heimischer
as additional classification criteria. The German
Arten”) should be taken more into consideration
assessment method allows for (1) identifying
in authorization procedures in future.
those species that threaten natural biodiversity
The European Strategy on Invasive Alien Spe
and other ecological functions and values, and (2)
cies (Council of Europe, 2003) recommends that
prioritizing species for management efforts (e.g.
all aliens have to be sorted into three categories:
mitigation, control, monitoring). While designed
(1) a white list of species which are harmless and
for use in Germany and Austria, the protocol can
might even be of use or benefit; (2) a grey list of
be applied to any other region, and may also be
species which impact is unclear; (3) a black list of
applicable to assess the impact in the non-native
Wadden Sea Ecosystem No. 25 2009
7 Alien species
range of a species that is also present elsewhere nation of natural aquatic ecosystems. In coastal
in a region as a native. waters the macrozoobenthic communities of the
On basis of the routine outlined above, a pre mesohaline zone in estuaries are characterized by
liminary assessment of alien species occurring in the highest number of alien species as well as by
the Wadden Sea shows that presently most of the the highest percentage of alien species compared
alien species cause no, or only minor, impacts on to the respective total indigenous species numbers
the natural biodiversity of the Wadden Sea, but (Wolff, 1999; Nehring, 2006) (Fig. 1). The high sum
it is also clear that several of them involve far- total of aliens may be more significant than the
reaching ecological consequences (in detail see effects of the individual alien species. Also, the
chapter 7.3). However, it should be noted that interactions between aliens may give rise to an
the impact of alien species, even those that may ‘invasional meltdown’ in the sense that already-
be invasive, is often insufficiently known because established aliens facilitate the establishment of
appropriate studies have not been attempted; ef others. The conclusion is that the assessment of
fects often develop over many years and it is often ecological quality status needs to be undertaken
difficult to distinguish the effects of alien species in an ecosystem context. Specific indices should
from those of many other simultaneous, natural, be established to aid identification of invasive
and anthropogenic effects on ecosystems (Reise species, as recommended by Arbaicauskas et al.,
and van Beusekom, 2008). Apart from ecological (2008) and Panov et al., (2009) for inland and
consequences by invasive alien species, any alien coastal waters.
species invasion constitutes a biological contami
Figure 1:
Estuaries - one hotspot of
invasion. It seems that the
combination of brackish
water with its unsatu-
rated ecological niches
and intensive international
ship traffic is responsible
for the observed high
infection rate with alien
macrozoobenthic species
in the Elbe estuary (after
Nehring, 2006).
Wadden Sea Ecosystem No. 25 2009
7 Alien species
3. Hotspots of invasion in the Wadden Sea
Figure 2:
Hotspots of bioinvasions at
the vertical habitat gradient
in the Wadden Sea. Spartina
and artificial hard struc-
tures around high tide level,
Crassostrea and other alien
suspension feeders with
epibionts around low tide
level, and alien plankton.
In the Wadden Sea, invasive alien species have Asian shore crabs Hemigrapsus sanguineus and H.
not spread randomly across the depth gradient takanoi which hide underneath boulders and may
from the upper beaches and salt marshes to potentially interfere with juveniles of the native
the deepest bottoms of the tidal inlets. Instead, shore crabs. Since 2007 both crabs are spread
there are three hotspots of alien impacts (Fig. 2): throughout the entire Wadden Sea.
The first is encountered around high tide level Extensive habitats in the Wadden Sea, the vast
on sheltered shores. Either the invasive Spartina mud and sand flats around mean tide level, with
grass dominates the vegetation or introduced or without seagrass, are almost devoid of alien
hard substrates prevail as a coastal defence or species. Only in the estuarine parts the invasive
harbour walls. Spartina is dealt with in detail polychaetes Marenzelleria neglecta and M. viridis
below. The artificial hard substrates host rocky temporarily achieved high densities (Fig. 3) (Ne
shore species which otherwise would be absent hring and Leuchs, 2001; Essink and Dekker, 2002).
from the Wadden Sea but are native to the region Also sandy beaches are virtually free of alien in
(i.e. the common sea slater Ligia oceanica). These vaders. By contrast, the transition from the lower
boulder walls may also serve as gateways for intertidal into the upper subtidal zone alongside
alien species which arrived by ship from overseas tidal channels is again a hotspot where the
(Reise and Buschbaum, 2007). Examples are the benthos is becoming dominated by alien species,
Figure 3:
High abundance of two
American spionid poly-
chaetes, Marenzelleria
neglecta and M. viridis in
the sublittoral of the Weser
estuary, differentiated
by the salinity gradient
(BfG Estuary Monitoring
Programme 1999, modified
after Nehring and Leuchs,
Wadden Sea Ecosystem No. 25 2009
7 Alien species
above all by the Pacific oyster Crassostrea gigas, Africa and southwest Europe or possibly has been
Ensis americanus, locally Crepidula fornicata and introduced a long time ago into the latter region.
others. This is an invasional meltdown where aliens Along other coasts in the world, including the
facilitate each other. At greater depth of channels Wadden Sea, various other plants such as species
and in the adjacent offshore zone, the share of of the genera Salicornia and Puccinellia used
aliens is again quite low up to now. to dominate the pioneer zone of salt marshes.
Potentially, a third hotspot may be in the coast However, this has changed. Today Spartina grasses
al waters flowing in and out of the Wadden Sea abound at most sheltered shores of temperate
with the tides. Some alien holoplanktonic species climate zones because of deliberate introductions
at times abound including the ctenophore invader which aimed to enhance salt marsh development.
Mnemiopsis leidyi and larvae of introduced aliens. Spartina species hybridized, natural vegetation
As well as these three hotspots, one could also became displaced and coastal landscapes trans
regard specific localities as potential hotspots of formed. Spartina is a classic example of global
alien species, where they can be expected to show biological homogenization through its mixing
up first after arrival in the Wadden Sea. These with once-distinct coastal vegetations.
localities include ports, marinas, on buoys and in Particularly widespread are S. alterniflora and
inner estuaries where the species are introduced S. anglica. The latter originates from accidental
with ships and are expected to arrive and have a hybridization between S. maritima and introduced
good chance to get off board or reproduce. Other S. alterniflora in southern England. In the sterile
hotspots are around oyster and mussel cultures. hybrid, a doubling of chromosomes happened to
Such localities should be particularly surveyed for occur and a fertile species was born, named S.
early detection of alien invaders (see chapter 4). anglica in 1892. This new species turned out to be
a more vigorous pioneer of salt marsh vegetation
3.1 Spartina – the most impor- than its parents, strongly facilitating sediment
tant invasive plant in the Wad- accretion and thereby transforming tidal flats into
den Sea salt marshes. This has attracted coastal engineers
Already intentionally introduced eight decades ago and systematic planting of S. anglica commenced
to aid in land claims and now well rooted with in the 1920s, including the introduction at various
extensive populations along the sheltered shores sites in the Wadden Sea between 1925 and 1944
of the Wadden Sea and adjacent coasts, the Spar- (Nehring and Hesse, 2008). These plantings were
tina grass has become a characteristic feature of partly successful and Spartina spread further on
the transition zone between marsh and tidal flats its own. However, disillusionment soon followed
(Fig. 4). Nevertheless, it is still not generally known the initial euphoria. König (1948) concluded that
that this conspicuous grass does not belong to the Spartina cannot protect any coast but grows well
native flora and constitutes an artificial element only where it is protected by the coast itself.
in the Wadden Sea, just as dikes and revetments, Also die-backs occurred, marshes with Spar-
linear ditches and brushwood groins. What is the tina became water-logged and unsuitable for
history and what are the prospects, what the ef grazing, and ditching for irrigation increasingly
fects on the ecosystem and biodiversity, and what cumbersome. Finally, in the 1960s, even tests
could be done about it? with herbicides were conducted in the German
Grasses of the genus Spartina are indigenous Wadden Sea to eradicate Spartina, in the end
to the Americas and the species S. maritima to without success.
Figure 4:
A belt of Spartina anglica
between native salt marsh
vegetation (Halimione) and
bare tidal flats with some
seagrass (Zostera noltii)
on the island of Sylt (July
2008).
Wadden Sea Ecosystem No. 25 2009
10 7 Alien species
On vegetation maps for the Wadden Sea, salt warmer temperature and increasing hydrodynam
marshes were generally categorized into pioneer, ics in the wake of accelerating sea level rise may
low and high salt marsh zones but did not provide ultimately set a limit to the further spread of
information on the areal share of Spartina. Only for Spartina in response to global warming, relegating
salt marshes along the Schleswig-Holstein coast, its distribution in the Wadden Sea to the sheltered
the areal share of a “Spartina anglica Typy” was locations in the upper tidal zone. Thus, a general
given as 18% for the mainland and 13% for the cover of bare sediment by Spartina down to mid
islands in 2001 (see Stock et al., 2005). However, tide level, as it commonly occurs at the more
this does not comprise Spartina growing outside sheltered Atlantic shores of North America, may
that type in the unspecified pioneer and lower salt never happen in the Wadden Sea.
marsh zone. Thus, there are no data on the areal Patches and swards of Spartina are a strong
extent of Spartina in the Wadden Sea. Knowledge habitat transformer or ecosystem engineer by
is confined to a few selected sites showing how accreting sediment, accumulating organic mate
this invader spread initially, and that it is still rial, penetrating the ground with a dense mesh of
spreading (i.e. Vinther et al., 2001; Stock et al., roots and rhizomes, and offering a complex habitat
2005; Loebl et al., 2006). It has been suggested structure above the ground which also shades the
that reductions in domestic grazing and in irriga bottom and calms down hydrodynamics. A mul
tion works (Stock et al., 2005), climate change in titude of effects has been recorded, varying with
the form of mild winters (Vinther et al., 2001), the phase of succession, the physical environment
and warmer and earlier spring times since 1988 and the organisms considered (Table 1).
(Loebl et al., 2006) have contributed to a renewed The role of Spartina as food to herbivores is
acceleration in the spread of Spartina. minor compared to being a source of detritus and
Global warming may prolong the growth season physically changing the habitat structure. Effects
of Spartina in the Wadden Sea because it belongs on biodiversity depend on location, the organisms
to plants with a C4 pathway with physiological and the scale which is considered. Spartina tends
thresholds of 4°C for germination and 7°C for to grow in monospecific stands which displace
effective photosynthesis. Loebl et al. (2006) as more diverse native vegetation but on a larger
sume that the improved temperature conditions scale it adds one more type of habitat patch to
may have helped the grass to grow also on more the dynamic mosaic of the salt marsh vegetation
exposed sandy tidal shores where it has been ab (Fig. 5). The diversity and complexity of effects
sent before. However, interactive effects between of Spartina on the environment precludes any
Table 1: Effects Habitat/Organisms References
Effects of Spartina on the Shoots and roots are food for foraging geese Esselink et al., 2000
habitat and other organ-
isms Shoots provide shelter for ducks and other birds Zedler, 1993
Shoots provide habitat Littorina, Hydrobia Armbrecht, 2008; Bouma et al., 2009
Dense swards prevent edge erosion of old marsh see Fig. 7.4
Dense swards accrete sediment more than other vegetation Gray et al., 1991
Shade out native plants Puccinellia, Salicornia Scholten and Rozema, 1990; Gray et
al., 1991
Raise the ground too high for Zostera noltii Reise et al., 2005
Culms increase abundance of macrobenthos Rader, 1984
Roots inhibit burrowing fauna Arenicola and other infauna Armbrecht, 2008; Bouma et al., 2009
Growth phases have different effects in infauna Neira et al., 2007
Patch edge and center differ in effects on bivalves Dumbauld et al., 1994 in Daehler and
Strong, 1996
Inhibit suspension feeders Cerastoderma edule Armbrecht, 2008
Roots create oxic microhabitats nematodes Osenga and Coull, 1983
Accumulation of detritus creates anoxia and die-back Nehring and Hesse, 2008
Sediment accretion eventually facilitates native plants Dijkema, 1983
Invasion of bare tidal flats reduces feeding area for shorebirds Evans, 1986; Goss-Custard and Moser,
1988
Monospecific swards may be susceptible to epi Thompson, 1991
demics
Wadden Sea Ecosystem No. 25 20097 Alien species 11
Figure 5:
Spartina anglica invades
(1) upper tidal flats in
patches, (2) dominates in
swards the seaward edge of
salt marshes, and invades
(3) the high marsh with
dynamic patches. Effects
on habitat structures and
other species differ at
these sites.
simple normative statement whether it is good
or bad, and the net balance will vary with time
3.2 Invasional meltdown around
and location. From a nature conservation point of low tide level
view, however, the magnitude of deviation from Similar to Spartina, also the Pacific oyster Crassos-
natural conditions caused by the Spartina invasion trea gigas is a universal habitat transformer of
is relevant and could justify measures of eradica temperate shores, regardless whether muddy,
tion or control (see chapter 4). sandy or rocky (Ruesink et al., 2005). Different from
Nehring and Hesse (2008) have reviewed Spartina, the invasion of Crassostrea began only
mechanical, chemical and biological methods two decades ago and it is still too early to venture
which have been employed or have been sug a sound projection on the final outcome. So far,
gested to control Spartina. To restore natural there is hardly any other invaded region which
processes in the upper tidal zone of the Wadden happened to be so readily invasible for this alien
Sea, it would be desirable to have shores again oyster as the Wadden Sea. How could that happen,
without Spartina. However, methods to eliminate what is the impact like and is there anything which
established Spartina should fulfil the following could be done about it? C. gigas is spreading above
requirements: and below low tide level where it is not the only
successful alien invader. The interactive effects
1. Mechanical elimination must not have disturb
with other aliens exacerbate the situation. The
ing effects on other organisms and natural
benthic community around low tide level is often
habitat structures lasting longer than a few
dominated by alien species.
years.
Without the depletion of natural beds and
2. Applied chemicals must not poison other subsequent extinction of the European oyster
organisms. Ostrea edulis in the Wadden Sea and adjacent
3. Biological agents such as diseases or herbivores waters, there would not have been an incentive
must be specific to Spartina and not spread to to introduce alien oysters (Reise, 2007). Early
regions where these are not wanted. attempts failed to introduce O. edulis from else
4. Must be successful in the long run, be cost- where in Europe, C.virginica from Atlantic America
effective and acceptable to the public. and various strains of C. gigas from the western
Pacific. However, the C. gigas introduced into the
In addition, any management measures should be
Oosterschelde estuary in 1964 spread into the wild
avoided which promote Spartina in the Wadden
from 1976 onwards. In the Western Wadden Sea
Sea. The Natura 2000 programme ought to be cor
specimens probably originating from seed oysters
rected. The invasive alien S. anglica should not fall
imported from a French hatchery (Smaal et al.
any more into the natural habitat type Spartinion
2009) were introduced in the cooling basin of the
maritimae code 1320.
electricity plant in Texel in the late 1970s (Tyde
Wadden Sea Ecosystem No. 25 200912 7 Alien species
Figure 6:
Pacific oysters growing ad-
jacent to an oyster farm at
the island of Sylt (August
2007).
man, 2008) and adult specimen were encountered The reproductive success in C. gigas has been
outside that basin in 1983. Spread from there linked to mean water temperatures >18°C dur
was rather slow at first but since the late 1990s ing July and August (Diederich et al., 2005), and
the invasion progressed rapidly throughout the particularly strong recruitment was observed in
Wadden Sea (for details see Dankers et al., 2004; summers between 2002 and 2006. A representa
Reise et al., 2005; Nehls and Büttger 2007; Fey et tive course of oyster reef development on former
al. in press). Another source of this species was mussel beds is given in Fig. 7. Oysters settle on any
regular farming of C. gigas with spat from British hard substrate but are most common on mussel
and Irish hatcheries near Sylt since 1986. A wild beds or where these had been before. The vertical
population, started close to that farm in 1991, distribution ranges from below mid tide level down
invaded the Danish Wadden Sea and also spread into the shallow subtidal with a maximum found
to the south (Fig. 6). around low tide level, copying the pattern of mus
sel beds. Abundances generally attain densities up
Figure 7:
to 1,000 to 2,000 oysters m-2 with a total weight
Above: mean abundance of of 30 to 50 kg m-2, but on established reefs they
the Pacific oyster Crassos- may go as high as 140 kg m-2 (Fey et al. in press).
trea gigas on mussel beds
which since 2005 appeared
In 2006, the oyster mass including shells was
to be all oysters reefs near estimated to be at least 61,000 t in the Wadden
Munkmarsch harbour on Sea (Nehls and Büttger, 2007).
Sylt. Below: mean abun-
dances of the American
Ecologically, the spread in the Wadden Sea
slipper limpet Crepidula started with a paradox. In spite of strong crowd
fornicata adjacent to mussel ing between Mytilus edulis on mussel beds, oyster
beds in 2000 and to oyster
reefs in 2006 at about
larvae successfully attached to individual mussels,
spring low tide level near grew faster and larger, soon smothered their ba
the island of Sylt (Reise, sibionts and began to dominate the beds (Fig. 8).
unpubl.).
Mussels have not reversed this hostile takeover
by settling on top of the oysters and smothering
them in turn. Instead, mussels settled in the un
derstory between the much larger oysters, escap
ing predators. Oyster larvae, by contrast, settled
preferentially on top of their older conspecifics
which gives rise to reef formation (Diederich,
2005). There are also wide areas with scattered
clusters of oysters. These are mostly dislodged
from the reefs, continue to grow and may serve
as nuclei for new beds where bare sediment had
been before.
Wadden Sea Ecosystem No. 25 20097 Alien species 13
There are probably no more mussel beds Figure 8:
without any oysters in the entire Wadden Sea. Succession of the conver-
Will the Pacific oysters eventually displace the sion of a mussel bed into an
oyster reef in the Wadden
native mussels? Up to now, the observations are Sea within 3 to 5 years.
inconclusive (Nehls et al., 2006; Nehls and Bütt First, Pacific oysters settle
ger, 2007). Within and between mussel beds, all upon mussels. Then new
mussels settle in the under-
combinations of high and low abundances have story, while settling oysters
been encountered. Also the temporal development attach to the tops of live
provides no clue. Since 1998, mussels increased and dead oysters, creating
an oyster reef.
in the Dutch and decreased in the German and
Danish Wadden Sea, while oysters proliferated
everywhere. The decrease in mussels commenced
already before the oysters began to increase
significantly. The area of mussel beds in Dutch
Wadden Sea has remained relatively stable over
the last years while oyster reefs and mixed beds
are increasing (Fig 9).
Long-term experience with mussels indicates
that severe winters have regularly resulted in
population expansion in the subsequent summer
(Nehls et al., 2006). This has been linked to a gap
in predation pressure caused by high predator
mortality and/or their retarded development.
However, such gaps may also occur for other
reasons as the development of the mussel popu
lation in the Dutch Wadden Sea shows. Thus, the
climatic trend alone, with no more severe winters A field experiment with mussels and oysters re
since 1996, will not suffice to predict the future vealed that differences in the habitat matrix gen
proportions of mussels to oysters in the Wadden erated by these two bivalve aggregates entailed
Sea. The microspatial pattern suggests that mus different abundances of associated infauna and
sels have a chance to coexist under the dominance epifauna (Kochmann et al., 2008). Further, a cover
of oysters (Fig. 8). with fucoid algae common on sheltered mussel
The spectrum of species associated with mus beds rarely develops where oysters prevail. As a
sel beds and oyster reefs is roughly the same but coastal filter the oyster reefs may be a functional
strongly varies with location (Markert et al., 2009). analogue to the mussel beds but the structural
3500 Figure 9:
Area of intertidal mussel
beds and the “takeover” by
3000 the Pacific oyster in the
Dutch Wadden Sea (Fey et
al. in press).
2500
2000 Oyster reef (>80% oysters)
Area (ha)
Combined reef (40%-80% oysters)
1500
Mussel bed with oysters (14 7 Alien species
Figure 10:
Stack of the American
slipper limpet Crepidula
fornicata (left) and stacks
scattered on shallow
subtidal bottom forming a
dense bed of limpets (Sylt,
September 2008).
effects differ. In particular, the Pacific oysters are imported from the Oosterschelde, and switched
still poorly integrated into the food web of the from the fading oyster grounds to subtidal mussel
Wadden Sea. Birds like eider, oystercatcher and beds near Sylt (Thieltges et al., 2003). There it now
herring gull which particularly feed on mussels abounds in the shelter of mussel beds or oyster
may run into a shortage of food because most reefs, forming a halo virtually paved with stacks
oysters are too large for consumption or fused into of individuals attached to each other (Fig.10)
clusters, and shells are too strong for the birds to (Nehls et al., 2006; Thieltges et al., 2009). Also
break them open (Blew and Südbeck, 2005; but around low tide line, the razor clam Ensis (directus)
see also Cadée, 2008 a,b). americanus attains its highest densities since the
May the Pacific oysters cause food shortage in 1980s (Armonies and Reise, 1999). Attached to
native suspension feeders by competition? In line the empty shells protruding out of the sediment
with such a process, native bivalves did decrease as well as to oysters and slipper limpets, the Asian
over the last decade (Beukema and Dekker, 2005; ascidian Styela clava frequently occurs in bunches
Nehls et al., 2006). As pointed out above, the trend of individuals with up to 232 m-2 just below mean
of warming is more likely to be the cause. This en low tide level (Fig. 11) (Liebich, 2007).
tails an increasing predation by shrimp and shore Altogether, Crassostrea, Crepidula, Ensis, Styela
crabs on bivalve spat rather than competition with and a few others have launched a striking invasion
the alien suspension feeders. Further, one should of alien suspension feeders in the zone around low
note that C. gigas is not the only suspension feeder tide line. The level of primary production may be
that invaded the Wadden Sea. Concurrently with still high enough to supply them all (Brinkman and
the increase in oysters, the American slipper limpet Jansen 2007; Reise and van Beusekom, 2008). In
Crepidula fornicata increased in abundance (Fig. addition to competition and predation, parasit
7). It was already introduced into the northern ism has to be considered as an important biotic
Wadden Sea seven decades ago with O. edulis interaction altered through alien bioinvasions.
Figure 11:
Aggregate of the invasive
ascidian Styela clava on
shallow subtidal bottom
(Sylt, June 2007)
Wadden Sea Ecosystem No. 25 20097 Alien species 15
Alien molluscs generally have arrived without Figure 12:
their parasites, but parasites of native molluscs Dead Pacific oysters serve
also infected the alien hosts (Krakau et al., 2006). as substrate to subsequent
settlement which may glue
Experiments have shown that Pacific oysters and together the empty shells
American slipper limpets actually mitigate the (Photo: N. Dankers).
parasite burden of the native mussels (Thieltges et
al., 2009). From the oysters as intermediate hosts,
trematodes cannot reach their final hosts because
oysters are not (yet) consumed by the birds.
Slipper limpets actually prey on cercarial stages
and do not get infected. In recent years massive
mortality occurred locally in late summer (Dank
ers et al., 2004). From the French Atlantic coast
there are reports of very high summer mortalities
in Crassostrea gigas (Samain et al. 2004). In the
Wadden Sea, oyster beds do not disappear after
mortality events. The shells remain and new spat
fall even solidifies the bed as a whole (Fig. 12)
Slipper limpets attached to mussels have been
shown to reduce growth and increase mortality
in their basibionts, while they provide protection
against predator attacks by shore crabs and star
fish (Thieltges et al., 2006). The web of interac
tions becomes even more complex when the large
In conclusion, the Pacific oyster has estab
invasive kelp Sargassum muticum is considered
lished firmly in the Wadden Sea. Neither the
(Fig. 13). It forms dense canopies in the shal
final population size nor the impacts on native
low subtidal of Sylt with positive effects on the
species can be clearly projected but it may cause
diversity of native species which attach or roam
a change in the ecosystem which may surpass
between the manifold branched thalli (Buschbaum
that of Spartina. Together with several other alien
et al., 2006; Polte and Buschbaum, 2008). Usually,
invaders parallel to or interacting with C. gigas,
clusters of oysters and stacks of slipper limpets
the benthos around low tide level has already been
provide the main anchorage at the bottom for
overturned with cascading effects on foraging
this invasive macroalgae. However, this is often
birds and the functioning of the ecosystem. Thus,
not perfect because the algae attain lengths of
efforts to protect Crassostrea reefs in the Natura
up to 3 m in July and the resulting drag lifts the
2000 programme as natural habitat type of com
anchorage off the bottom, and both together end
munity interest (Reefs, code 1170) have not to be
up in the wash line on the beach.
put into action.
Figure13:
The invasive Sargassum
muticum forms a dense
kelp forest adjacent to the
oyster farm at the island of
Sylt (July 2007).
Wadden Sea Ecosystem No. 25 200916 7 Alien species
Apparently, the spread of C. gigas into the wild might be susceptible for Bonamia disease or if
was not considered to be a problem until the late resistant they might carry the disease and might
1990s. Although Crassostrea successfully repro form a stepping stone between infected regions
duced in the Oosterschelde since the mid 1970s, it (Dutch Delta) and non-infected regions such as
was still assured in 1986 that starting a Crassostrea Limfjorden.
farm near Sylt is not violating National Park law
because it was assumed that the Pacific oysters 3.3 Alien invaders in the
were unable to breed under our latitude and would plankton
not spread into the wild. Concern has arisen only In drifting planktonic organisms, an occurrence
after the invading population had passed the line in the North Sea cannot be set apart from the
of no return. In view of the sheer number already Wadden Sea. These organisms are largely at the
present, together with its enormous potential of mercy of currents and thus their abundance in the
reproduction and dispersal, no mechanical control Wadden Sea is highly variable. What evidence is
of this invader is conceivable. Wild aggregates of known that aliens in the plankton exert effects on
C. gigas may not be commercially harvestable for natives or on the ecosystem in the Wadden Sea?
consumption, and large scale dredging for low At least nine taxa in the phytoplankton are
quality meat, manure or chalk production would likely to have been introduced with ballast water
be devastating for the environment. Thus, fishery or oysters, and of these the diatoms Odontella
on oysters would be no sensitive option for the sinensis, Coscinodiscus wailesii (Fig. 14) and Tha-
Wadden Sea ecosystem. Seed oysters might be lassiosira punctigera, the frequently re-named
collected but very few are suitable for further dinophyte Karenia (=Gymnodinium) mikimotoi
culturing because most are attached firmly to (=aureolum) and Fibrocapsa japonica belonging
clusters and cumbersome to detach. Removal of to the Rhaphidophyceae have been occasionally
entire reefs with bulldozers or by dredging from reported as abundant (Gollasch et al., 2008). To
a ship is not feasible on the large scale required what extent these introduced alien species have
for control without harming all other organisms effects on other phytoplankton or on consumers
including natives, and the success is likely to be has not yet been shown.
only short term. Other means of control could be As a corollary of the many alien invaders in
the introduction of potent predators or diseases. the benthos, there are times when their larvae
However, such biocontrols are difficult to keep are abundan in the coastal waters. As an extreme
under control (Hoddle, 2004; Thomas and Reid, example, larvae of the American razor clam Ensis
2007). Potential collateral damage to non-target americanus dominated with 92% all identified
species as well as to cultured oysters is usually bivalve larvae in the plankton samples taken in
impossible to rule out. summer 2004 near Sylt (M. Strasser, pers. comm.).
However, as a partial reparation for the over As with phytoplankton, the cascading effects in
exploitation of the native oysters and the intro the food web are not known.
duction of alien ones, attempts could be made In the warm summer of 2006, the lobate cteno
to re-introduce the native oyster O. edulis. Other phore Mnemiopsis leidyi was sighted at several
than the mainly intertidal C. gigas, this species had coasts in northern Europe including the Wadden
occurred subtidally and so may not suffer from Sea, but may have been introduced several years
spatial competition with C. gigas if re-introduced. earlier with ballast water (Faase and Bayha, 2006;
The maintenance of dense commercial stocks of O. Boersma et al., 2007; Tendal et al., 2007). Normally,
edulis may provide the key to a redevelopment of only specialists care about such comb jellies. How
native oyster beds by providing initial brood stock ever, M. leidyi had already a bad name from the
nuclei from which larvae can spread. A problem Black and Caspian seas. This American ctenophore
might be to obtain a genotype similar to the one found ideal conditions after first encounters in
which once thrived in the Wadden Sea before over 1982, spread massively and was blamed for having
exploitation led to its extinction. Care should also caused the collapse of the Black Sea fishery on
be taken not to introduce the Bonamia-disease. anchovy by competing for planktonic food (Bilio
Presumably, O. edulis living today in Limfjorden and Niermann, 2004). After 1995 the same cteno
(Kristensen, 1997) could be a proper source for the phore also invaded the Caspian Sea, and again
re-introduction. An unintended re-introduction of this was associated with a dramatic decrease in
O. edulis has turned into a success in Strangford other zooplankton and fish, in this case kilka, the
Lough, Northern Ireland (D. Roberts, pers. comm.). most common anchovy there. Similar effects were
However care should be taken as these oysters suspected in North European waters.
Wadden Sea Ecosystem No. 25 20097 Alien species 17
Figure14:
The invasive diatom
Coscinodiscus wailesii forms
dense blooms, up to 90 %
total algal biomass (Photo:
K. Hesse).
However, M. leidyi on average remained smaller wetlands, is attempting to nest on a Wadden
than in southern waters, mostly18 7 Alien species
Figure 5:
Mature female of Cal-
linectes sapidus Rathbun
caught in German Weser
estuary on 20 July 2007
(Photo: J. Albersmeyer).
is not known what the consequences for survival elsewhere, i.e. the Pontocaspian fish Neogobius
and for species interactions may arise from such melanostomus, the Pacific whelks Rapana venosa
genetic mixing. The invasion of Crassostrea gigas and Ocinebrellus inornatus, the Asian clam Tapes
is already severe but it could become even worse if philippinarum, the small mussel Musculista sen-
in addition other Pacific species such as C. sikamea housiana and the sizable blue crab Callinectes
and C.ariakensis are introduced. Morphologically sapidus (Fig. 15). Decisions whether these should
these are almost indistinguishable from C. gigas. be met with resistance to prevent establishment
Nevertheless, there are important ecological differ should be based on experiments testing the inter
ences with respect to vertical range and exposure actions with native species as well as on models
to hydrodynamics. predicting the invasional pressure and thus the
Some invaders are almost certainly about to chances to keep particular invaders out. Thus, in
invade the Wadden Sea if they are not already addition to regular surveys by experts, a consider
present before this volume is published. Some able research effort is needed.
have an impressive career as successful invaders
Wadden Sea Ecosystem No. 25 20097 Alien species 19
4. Conditions and measures
The significant effects of alien species on aquatic Alien policy in the Danish
ecosystems require that efforts should be made Wadden Sea
to prevent and control their further spread. The
In 2008 Denmark prepared a National Action Plan
strategies to minimize impacts caused by alien
for Alien Invasive Species. The Action Plan gives
species are known. However, the countries’ abili
a number of recommendations on prevention,
ties to address issues on alien species varies.
eradication, control and research on alien species.
Alien policy in the Dutch Wadden Sea Regarding the marine environment, prevention
There is no specific alien policy for the Wadden is much preferred as eradication most often is
Sea. In October 2007 the Ministry of Agriculture, impossible. Therefore one of the recommenda
Nature and Food Quality send a policy statement tions is implementation of the Ballast Water
(Beleidsnota Invasieve Soorten) to the Dutch par Convention.
liament. It mentions several of the above indicated The Action Plan also includes the first Danish
international agreements and also the IMO bal “black list” of species regarded as the “worst”
last water agreement (to be ratified in 2009) but alien invasive species in Denmark. Furthermore
not the RAMSAR convention which is specifically there is an “observation list” of species either not
important for the Wadden Sea. yet present in Denmark but known to be invasive
A general conclusion of the statement is that in neighbouring countries or present in Denmark
preventing introductions of invasive alien spe but still rare.
cies is the most important and (cost) effective Alien policy in the German
policy option. Possible management options
that contribute to prevention are creating public
Wadden Sea
awareness of this problem and making agreements In accordance with the CBD’s guiding principles
with stakeholders, such as companies that import (CBD, 2000), Germany has recently been preparing
plants, plant products or animals. a national strategy on invasive alien species (Hubo
The Ministry of Agriculture, Nature and Food et al., 2007). The overall strategy for alien species
Quality set up an Invasive Species Team, consisting comprises two main components: dealing with
of several civil servants. The formal starting date the problem of alien species already present, and
for this team was January 2009. In co-operation the prevention of further introductions including
with an expert network this Invasive Species Team the response if prevention should fail. Depending
will work on: a) gathering information on (new) on the species, efforts should target one of the
alien species, b) setting up monitoring programs five categories: (a) prevention of introductions
(early detection of new alien species), c) risk through education and regulations; (b) monitor
analysis (carried out by experts), d) advising the ing and early detection by effective monitoring
Ministry on invasive species (risks and possible programs; (c) rapid measures to eliminate newly
management options), e) informing the public on introduced invasive alien species; (d) minimization
invasive species (raising awareness). The Invasive of impacts of established invasive alien species
Species Team mainly focuses on alien species by eradication and control; and (e) acceptance
that (potentially) impact biodiversity. Most of the of established non-invasive species.
(alien) organisms that threaten human health or a. Prevention
the economy (agriculture) are dealt with in other Prevention is the first line of defence. In aquatic
organizations and ministries. When an initial environments, alien species can be hard to detect
analysis indicates possible impacts on biodiversity and organisms disperse rapidly. It is a well-known
and more information is needed, a risk analysis will fact that the eradication of an introduced spe
be carried out by experts. If needed, further moni cies, once it has established in our waters, will be
toring will be carried out to determine the spread very difficult (and expensive), or even impossible.
of the alien species. Based on this information the Therefore, the prevention of introductions (at best
Invasive Species Team advises the Ministry on the at source) is the most effective and least costly
possible impacts of the alien species and possible management strategy. Moreover, prevention is the
management actions. only option where different measures for intended
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