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Invasion of Pacific oysters (Crassostrea gigas) in the
Wadden Sea: competitive advantage over native mussels
Eingeführte Pazifische Austern (Crassostrea gigas) im Wattenmeer:
Konkurrenzvorteil gegenüber heimischen Miesmuscheln
DISSERTATION
zur Erlangung des Doktorgrades
der Mathematisch-Naturwissenschaftlichen Fakultät
der Christian-Albrechts-Universität
zu Kiel
vorgelegt von
Susanne Diederich
Kiel 2005
Oyster reef Crassostrea gigas in the northern Wadden Sea, Germany
Austernriff Crassostrea gigas im nordfriesischen Wattenmeer bei Sylt
Referent:
Prof. Dr. Karsten Reise
Korreferent: Prof. Dr. Martin Wahl
Tag der mündlichen Prüfung:
29.04.2005
Zum Druck genehmigt:
04.05.2005
Contents
Summary / Zusammenfassung
1
1
7
General Introduction
1.1
1.2
1.3
1.4
1.5
Marine bioinvasions
Invasion history of Crassostrea gigas
C. gigas and the ecology of mussel beds
Outline of the study
References
7
10
14
17
18
2
Introduced Pacific oysters (Crassostrea gigas) in the northern Wadden Sea:
invasion accelerated by warm summers?
25
3
Differential recruitment of introduced Pacific oysters and native mussels
at the North Sea coast: coexistence possible?
45
4
High survival and growth rates of introduced Pacific oysters may facilitate
displacement of native mussels in the Wadden Sea
67
5
Pacific oysters Crassostrea gigas in the Wadden Sea: invasion facilitated by
weak predation?
99
6
General Discussion
6.1
6.2
6.3
6.4
6.5
Factors affecting the establishment of C. gigas
Spread of C. gigas in the northern Wadden Sea
Interaction with recipient community
Conclusion
References
Acknowledgements
127
127
129
130
143
144
151
Summary
1
Summary
Pacific oysters (Crassostrea gigas Thunberg 1793) have been introduced into the Wadden Sea
(North Sea) by aquaculture in the 1980s. Subsequently, natural spatfalls occurred and wild
oyster populations became established. For settlement, oyster larvae need hard substrates to
which they attach themselves permanently. By settling on top of each other, they may create
massive biogenic reefs. On the sedimentary tidal flats of the Wadden Sea, epibenthic mussel
beds (Mytilus edulis L.) represent the main insular hard substrates, wherefore the oysters
attached themselves mainly to the shells of living and dead blue mussels.
Resident mussel beds became more and more overgrown by C. gigas and the question arose,
whether they all might soon be replaced by oyster reefs. In this context, the objective was to
assess the impact of C. gigas on the native ecosystem by investigating the population
development in the northern Wadden Sea, and by evaluating the scope for coexistence with
resident mussels. In general, this may be a test case whether an introduced species is capable
of displacing a native analogue in a sedimentary shore environment.
The invasion of C. gigas in the northern Wadden Sea started in 1991 when the first wild
oysters had settled on an intertidal mussel bed in the vicinity of an oyster farm that has started
its business in 1986 in the List tidal basin (island of Sylt, Germany). At first, abundances on
intertidal mussel beds remained low and patchy (1995: 3.56 ± 3.21 individuals m-2; 1999: 3.71
± 3.79 individuals m-2). The population slowly expanded its range from intertidal to subtidal
locations as well as from Sylt north- and southwards along the coastline. However, a
succession of three summers (2001 – 2003) with anomalous high water temperatures led to a
massive increase in oyster abundances (2003: 125.80 ± 119.47 individuals m-2, 2004: 244.44
± 172.84 individuals m-2). It is assumed that the further invasion of C. gigas in the northern
Wadden Sea will benefit from high late-summer water temperatures when these oysters
reproduce. However, length frequency distributions revealed that successful cohorts survived
for at least 5 years, allowing for population persistence even when warm summers are rare.
Studies on recruitment showed differential settlement of oysters and mussels that may lead to
niche separation and coexistence of both species. As oysters settle preferentially on
conspecifics, a positive feedback of adults on recruitment may facilitate rapid reef formation.
Mussels may find a refuge underneath a cover of the brown macroalga Fucus vesiculosus.
Potentially, mussels may overgrow oyster reefs in high recruitment years especially if a
facilitating barnacle cover is high. However, biotic interactions with C. gigas that reaches
2
Summary
about three to four times the size of mussels may prevent M. edulis to become abundant on
oyster reefs.
Growth experiments revealed a faster growth of C. gigas compared to M. edulis in intertidal
and subtidal habitats. Whereas oyster growth is not hampered by the presence of oysters,
mussels, and barnacle epigrowth, the growth of mussels is reduced in the presence of these
species, thus suggesting competitive inferiority.
In field experiments, a high survival rate of juvenile oysters was found and presumably
caused by very low predation pressure. About 70% of juvenile C. gigas survived the first
three months on an intertidal mussel bed and about 40% reached their first reproductive
period one year after settlement. Only early recruitment in the subtidal zone was reduced due
to predation. Laboratory feeding preference experiments confirmed that the main benthic
predators, shore crabs (Carcinus maenas L.) and starfish (Asterias rubens L.), strongly prefer
mussels to oysters. Size selective feeding by the main mussel predators together with an early
size refuge from predation due to faster growth and larger size may facilitate a competitive
advantage of C. gigas over M. edulis.
As C. gigas is well adapted to the Wadden Sea ecosystem and competitive superior to their
native congeners, a further increase of the oyster population in the Wadden Sea is expected.
The development of massive intertidal and possibly also subtidal oyster reefs that may contain
a variable amount of mussel epigrowth depending on recruitment success in different years is
considered as a likely future scenario. As oyster recruitment depends on high summer water
temperatures whereas high mussel recruitment usually follows severe winters, a possible
climate change leading to warmer summers and milder winters will further support the
displacement of M. edulis by C. gigas. This regime shift is expected to have profound impacts
on the Wadden Sea ecosystem, mainly because oysters are less integrated in the basic food
web. A massive increase of the oyster population may lead to food limitation of other
suspension feeders, especially in the wake of decreasing eutrophication, and to a decline of
benthic predators. However, in which way the resident community will adapt to this new
invader will be a future task to tackle. I conclude that the invasion of C. gigas in the Wadden
Sea is facilitated by a high efficiency of using space and food resources and by low predation
pressure by resident predators.
Zusammenfassung
3
Zusammenfassung
Die Pazifische Auster (Crassostrea gigas Thunberg 1793) wurde Mitte der 1980er Jahre zu
Aquakulturzwecken ins Wattenmeer eingeführt und hat sich seitdem durch natürliche
Larvenfälle an der gesamten Wattenmeerküste etabliert. Austernlarven benötigen zur
erfolgreichen Ansiedlung Hartsubstrate, an denen sie sich festzementieren können. Auf den
sandigen Böden des Wattenmeeres beschränken sich solche Hartsubstrate jedoch größtenteils
auf epibenthische Miesmuschelbänke (Mytilus edulis L.), die einer Vielzahl sessiler Arten als
Siedlungsraum dienen.
Da sich die Austern auf die Schalen der Miesmuscheln heften, wurden die heimischen
Muschelbänke zunehmend von den etwa drei- bis viermal größeren Austern überwachsen und
es stellte sich die Frage, ob die Miesmuscheln bald verdrängt werden könnten. Das Ziel dieser
Studie war es daher, die Ausbreitung und Einnischung von C. gigas im Wattenmeer zu
untersuchen und zu einer Prognose zu gelangen, ob eine Koexistenz von Miesmuscheln und
Austern in Zukunft möglich sein wird. Damit leistet die vorliegende Arbeit einen Beitrag zum
Verständnis der möglichen Auswirkungen eingeschleppter Arten auf die Lebensgemeinschaften der Sedimentküsten.
Nachdem 1991 die ersten freilebenden Austern auf einer eulitoralen Muschelbank in der Nähe
der Austernfarm im Lister Tidebecken (Sylt, nordfriesisches Wattenmeer) gefunden wurden,
fand zunächst eine regionale Verbreitung statt, die mittleren Dichten nahmen hingegen kaum
zu. So zeigten die ersten Kartierungen aus den Jahren 1995 (3.56 ± 3.21 Individuen m-2) und
1999 (3.71 ± 3.79 Individuen m-2) noch keinen nennenswerten Abundanzzuwachs, aber die
Austern hatten sich allmählich sowohl nord- und südwärts entlang der Küste als auch vom
Gezeitenbereich ins Sublitoral ausgebreitet. Erst eine Folge von drei Sommern (2001 – 2003)
mit überdurchschnittlich hohen Wassertemperaturen führten zu einer dramatischen Zunahme
des Austernbestandes (2003: 125.80 ± 119.47 Individuen m-2; 2004: 244.44 ± 172.84
Individuen m-2). Da in allen Jahren mit hohem Rekrutierungserfolg besonders hohe
Wassertemperaturen im Spätsommer herrschten, wird vermutet, dass die weitere
Bestandsentwicklung der Austern im nördlichen Wattenmeer vom Auftreten warmer Sommer
abhängt. Da Längenhäufigkeitsverteilungen jedoch zeigen, dass bestandsbildende Kohorten
mindestens 5 Jahre lang überleben, wird auch eine Periode mit kalten Sommern nicht zum
Verschwinden der Austern führen.
4
Zusammenfassung
Untersuchungen zur Rekrutierung von Austern und Miesmuscheln haben artspezifische
Unterschiede ergeben, die eine Koexistenz von beiden Arten ermöglichen könnten. Während
sich Austern bevorzugt auf Artgenossen ansiedeln, zeigen Miesmuscheln keine Präferenz für
Austern- oder Miesmuschelsubstrate, sie bevorzugen vielmehr mit Seepocken bewachsene
Schalen vor unbewachsenen. Die positive Verstärkung des Rekrutierungserfolges durch die
Anwesenheit adulter Austern wird die Ausbildung von Austernriffen beschleunigen. Da die
Rekrutierung von C. gigas jedoch durch das Vorhandensein der Braunalge Fucus vesiculosus
stark behindert wird, könnten Miesmuscheln unter Fucus einen Rückzugsraum finden und in
Jahren mit hohem Rekrutierungserfolg, wie sie meist auf kalte Winter folgen, die neuen
Austernriffe überwachsen. Dies wird jedoch unter anderem davon abhängen, inwieweit die
Miesmuscheln mit den Austern um potentiell limitierende Ressourcen konkurrieren können.
Wachstumsexperimente haben gezeigt, dass Austern schneller wachsen als Miesmuscheln.
Weder die Überdeckung mit der Braunalge F. vesiculosus, noch der Aufwuchs von
Seepocken oder die Anwesenheit von Miesmuscheln und Austern haben einen negativen
Einfluss auf die Wachstumsrate von C. gigas. Das Wachstum von Miesmuscheln wird
hingegen durch die Anwesenheit dieser Arten verlangsamt, was vermuten lässt, das M. edulis
konkurrenzschwächer ist.
Freilandexperimente haben ergeben, dass juvenile Austern sehr hohe Überlebensraten auf euund sublitoralen Miesmuschelbänken aufweisen. In Räuberausschlussexperimenten und
Nahrungswahlversuchen konnte gezeigt werden, dass geringer Prädationsdruck für die
niedrige Mortalität verantwortlich sein könnte. Sowohl Strandkrabben (Carcinus maenas L.)
als auch Seesterne (Asterias rubens L.) haben die heimischen Miesmuscheln den Austern
vorgezogen. Da die Austern schneller wachsen und größer werden als die heimischen
Miesmuscheln, wachsen sie zudem schneller aus dem Nahrungsspektrum von möglichen
Räubern heraus, was Ihnen einen weiteren Konkurrenzvorteil verschafft.
Da C. gigas sehr gut an den Lebensraum Wattenmeer angepasst und konkurrenzstärker ist als
M. edulis, ist zu erwarten, dass ihre Dichte weiter zunehmen wird und es zur Ausbildung von
großflächigen eu- und sublitoralen Austernriffen kommen kann. Die Miesmuscheln werden
wahrscheinlich weiter abnehmen und könnten zu einer Existenz als eine unter vielen
Aufwuchsarten auf Austernriffen zurückgedrängt werden. Diese Vorhersage wird durch
Klimaprognosen gestützt, die wärmere Sommer und mildere Winter vorhersagen. Falls die
Austern
sehr
stark
zunehmen
und
abnehmende
Eutrophierung
in
Zukunft
zu
Nahrungslimitierung im Wattenmeer führen wird, könnten die Austern auch andere
Zusammenfassung
5
Muschelarten zurückdrängen. Da die Austern zumindest gegenwärtig noch schlecht ins
Nahrungsnetz integriert sind, wird Ihre Zunahme auf Kosten anderer Arten auch deutliche
Auswirkungen auf höhere trophische Stufen wie benthische Prädatoren und Vögel haben.
Inwieweit sich jedoch das heimische Ökosystem an die eingeschleppte Art anpassen kann,
muss einer weiteren Untersuchung vorbehalten bleiben.
General Introduction
7
1 General Introduction
This study discusses an invasive species that may have profound impacts on ecosystem
dynamics in the Wadden Sea (North Sea). The spread and niche occupation of introduced
Pacific oysters (Crassostrea gigas) was investigated in field surveys as well as in field and
laboratory experiments. As the oysters are settling on top of native epibenthic mussel beds
(Mytilus edulis), the scope of coexistence for both species was assessed. The first section of
this introduction deals with general aspects of marine bioinvasions, whereas the second
section is focussed on the invasion history of C. gigas. The third section illustrates possible
effects of C. gigas on the benthic ecosystem and especially on the ecology of mussel beds.
Finally, the main questions of this study are presented.
1.1 Marine bioinvasions
Non-native species accumulating in marine ecosystems are a significant component of human
induced environmental change, leading to a homogenisation of the earth’s biota (Lodge 1993,
Lövei 1997, Vitousek et al. 1997, Occhipinti-Ambrogi & Savini 2003). Even though changes
in species compositions and interactions due to climatic and geographic variations have
occurred throughout evolutionary time, human mediated transport vectors are allowing a
much wider and faster distribution to new habitats. Especially the improvement of
intercontinental ship traffic largely enhanced the number of non-native species that were
transported in ballast water or attached to ship hulls and survived even long distance journeys
(Carlton 1985, Carlton & Geller 1993, Ruiz et al. 2000, Minchin & Gollasch 2003). The
deliberate or accidental release of aquaculture products is another important gateway, not only
for target species, but also for organisms associated with them, such as epifauna and
-flora as well as parasites and pathogens (Chew 1990, Naylor et al. 2001, Wolff & Reise
2002). Aquarium trade and plastic debris drifting on the sea surface are other anthropogenic
vectors with increasing significance (Barnes 2002, Semmens et al. 2004).
However, even though enormous amounts of organisms are transported beyond their native
ranges every day, only few of them are able to establish themselves in recipient habitats and
even less become invasive and develop an immense population growth (Lodge 1993,
Williamson & Fitter 1996a). Nevertheless, there are numerous examples of invasive species
8
Chapter 1
that have profound direct and indirect effects on the native community, ranging from specieslevel consequences to impacts on food-web properties and ecosystem processes (Grosholz
2002). One example for an invasion that has caused changes at ecosystem level is the
introduction of the estuarine Asian clam Potamocorbula amurensis into San Francisco Bay.
The bivalve interrupted the basic food chain by transferring most of the primary production
from the pelagic to the benthic food web, thereby enhancing benthic invertebrates and
bottom-feeding fishes on the expense of zooplankton and larval fish (Carlton et al. 1990,
Nichols et al. 1990, Kimmerer et al. 1994). Another example is the comb jelly Mnemiopsis
leidyi that was introduced into the Black Sea via ballast water in the early 1980s. The
voracious zooplanktonic predator devastated the food chain of the entire Black Sea basin and
caused a huge economic damage to the fishing industry by feeding on the food supply and on
the eggs and larvae of resident pelagic fish (Kideys 2002). However, eutrophication may have
played an important role in this process, thus supporting a theory that states that disturbed
habitats are more susceptible to invasions than undisturbed ones (Occhipinti-Ambrogi &
Savini 2003, Marvier et al. 2004). Assuming that successful invaders are habitat generalists
and that generalists are competitive inferior to habitat specialists because of a trade-off
between competitive ability and habitat breadth, habitat destruction and short-term
disturbances should favour invasion by habitat generalists despite their inferior competitive
ability (Marvier et al. 2004).
In order to predict or prevent further introductions, many studies have focussed on
characteristics of successful invaders (di Castri 1990, Lodge 1993, Kolar & Lodge 2001,
McMahon 2002) and on habitat characteristics (Crawley 1987, Case 1991) that may
determine susceptibility to invasion. Species with r-selected life history traits (rapid growth,
early maturity, short life spans, high fecundity, and extensive dispersal capacity) are generally
considered to be successful invaders because they are able to achieve massive population
densities soon after introduction to a new habitat (Lodge 1993, Williamson & Fitter 1996b,
McMahon 2002). The term ‘niche opportunity’ was employed to describe conditions that
promote invasions in terms of resources, natural enemies, the physical environment, and
interactions between these factors varying in time and space (Shea & Chesson 2002). How a
species responds to these conditions determines its ability to invade a certain habitat. In this
context, high species richness has been proposed as a prerequisite for a low susceptibility to
invasion – or low niche opportunity – because of a more complete utilization of resources by
resident species (Elton 1958, Stachowics et al. 1999). However, characteristics that may
General Introduction
9
facilitate invasion or invasibility are controversially discussed, because many successful
invasions are not following any of the general rules (Crawley 1987, Lodge 1993).
Climate change leading to changing maximum and minimum temperatures has frequently
been discussed as supporting biological invasions (Stachowicz et al. 2002). For example,
higher winter temperatures are promoting the spread of slipper limpets Crepidula fornicata,
and higher spring temperatures facilitate the expansion of the cord grass Spartina anglica in
the northern Wadden Sea (Thieltges et al. 2004, Loebl et al. submitted).
The spread and niche occupation of an introduced species offers opportunities to study basic
processes in population biology (Sakai et al. 2001). Assuming that an invasive species
encounters suitable environmental conditions in its new habitat, its population development
will depend on whether it is consumed by native predators (Robinson & Wellborn 1988,
Trowbridge 1995) or outcompetet by resident species (Moulton & Pimm 1983, Case 1991).
Exploitative competition between an introduced and a native species may occur if one species
has a more efficient way of using limiting resources (Byers 2000). Various case studies have
compared the ability to compete for space and/or food between exotic species and their native
congeners in order to explain or assess future invasion success (e.g. Byers 2000, Talman &
Keough 2001, Kotta & Ólaffson 2003, Cope & Winterbourn 2004). In addition, home and
away comparisons, that is, comparisons of species in their native and invaded ranges, are
considered to be important for the understanding of invasion processes (Lohrer et al. 2000).
Recently, the enemy release hypothesis has been widely discussed in invasion literature. It
states that the success of invaders is related to the scarcity of natural enemies such as
predators, parasites and pathogens, in the introduced range compared to the native habitat
(Torchin et al. 2001, 2003, Keane & Crawley 2002, Shea & Chesson 2002, Clay 2003, Drake
2003, Mitchell & Power 2003, Colautti et al. 2004). However, phenotypic plasticity may
enable native species to react to the invaders (Cox 2004). For example, in New England the
native periwinkle Littorina obtusata developed thicker shells in response to the introduction
of a new predator, the European green crab Carcinus maenas (Trussel 2000).
At the North Sea coast, about 80 non-native species became established, with ship traffic and
aquaculture being the most important introduction vectors (Reise et al. 2002). Most of these
species remained insignificant additions to the native biota, but there are some species that
may alter ecosystem functioning (Reise et al. 2005). Examples are the cord grass Spartina
anglica (Loebl et al. submitted), the Japanese seaweed Sargassum muticum (Buschbaum in
10
Chapter 1
press), the American slipper limpet Crepidula fornicata (Thieltges et al. 2004), and the
Pacific oyster Crassostrea gigas (Reise 1998).
As C. gigas is an ecosystem engineer that alters habitat characteristics by forming massive
epibenthic reefs, its introduction may have community-level effects proportional to its
abundance (Reusch & Williams 1999, Jones et al. 1994). Possible impacts of C. gigas on the
Wadden Sea ecosystem, and how competition with native mussels and predation by resident
predators may influence the invasion success, will be discussed in chapter 6 (General
Discussion).
1. 2 Invasion history of Crassostrea gigas
1.2.1 Global distribution
The Pacific oyster originates from Japan and has been introduced to various coastal areas due
to aquaculture activities (Korringa 1976, Andrews 1980, Chew 1990; Fig. 1). In many
regions, natural spatfalls occurred and wild oyster populations established: e.g. British
Columbia (Quayle 1988), California (Span 1978), South Africa (C. Griffith, pers. comm.),
Australia (Ayres 1991), New Zealand (Dinamani 1991), France (Grizel & Héral 1991), The
Netherlands (Drinkwaard 1999), and Germany (Reise 1998). It is important to note that
according to genetic studies the Portuguese oyster Crassostrea angulata is a strain of C. gigas
originating from Taiwan (Boudry et al. 1998, Huvet et al. 2002). C. angulata was accidentally
introduced to Portugal sometime between the early 16th and the late 18th century and was later
imported into France (1860s) and The Netherlands (19th century) for aquaculture (Wolff &
Reise 2002). However, gill disease and viral pathogens led to a severe decline of the
Portuguese oyster in the 1960s and 1970s, and stocks never recovered thereafter (Goulletquer
& Héral 1991).
General Introduction
11
Fig. 1 Worldwide distribution of C. gigas respectively C. angulata. Given is native range
(encircled; Japan and Korea for C. gigas, Taiwan for C. angulata), and years of first
introductions. Yellow: C. angulata; red: C. gigas from Japan; blue: C. gigas from the west
coast of the U.S. Map after Chew (1990) and Wolff & Reise (2002)
In Europe, imports of C. gigas started in 1964 with spat oysters from British Columbia that
were released in the Oosterschelde (The Netherlands) for aquaculture purposes (Drinkwaard
1999). The first natural spatfalls occurred during two exceptionally warm summers in 1975
and 1976 and subsequently a wild population established. From then on, the oyster population
increased enormously, from 15 - 35 ha oyster reef area in 1980 to 210 - 370 ha in 1990 and to
640 ha in 2002 (Kater & Baars 2003). The introduction of C. gigas to France, which started in
1966 with imports of spat from Japan, led to a similar population increase (Le Borgne et al.
1973, Grizel & Héral 1988). However, in Great Britain, where C. gigas is cultured since
1965, only sporadic natural spatfalls occurred in some estuaries (Spencer et al. 1994, Child et
al. 1995).
In the Wadden Sea, which is a 500 km long coastal stretch between Den Helder in The
Netherlands and Esbjerg in Denmark (Fig. 2), the invasion of C. gigas started from two
locations: from the island of Texel (The Netherlands) in 1983 and from the island of Sylt
(Germany) in 1991 (Bruins 1983, Reise 1998). The oysters near Texel in the Dutch Wadden
Sea are considered to have been accidentally introduced with mussel transports from the
Oosterschelde (Bruins 1983), whereas the oysters in the northern German and Danish Wadden
12
Chapter 1
Sea sprang from an oyster culture near Sylt (Reise 1998). From Texel, the oysters spread
eastwards along the coast and reached the German Wadden Sea in 1998 (Wehrmann et al.
2000). Meanwhile, extensive intertidal oyster reefs have developed near the islands of Texel
and Rottum in The Netherlands (Dankers et al. 2004), and also in the western German
Wadden Sea the formation of oyster reefs has recently begun (A. Schmidt, pers. comm.).
Near Sylt, the first wild oyster that had dispersed as a larva was found in 1991 on an intertidal
mussel bed Mytilus edulis in the vicinity of an oyster farm that started its business in 1986.
The wild oyster population slowly expanded its range from Sylt north- and southwards along
the coastline. However, abundances remained on a low level until a succession of three
consecutive summers (2001 - 2003) with anomalous high water temperatures led to an
immense increase in oyster densities and to the formation of oyster reefs in some locations by
2004.
2003
Site and year of introdution
Site and year of first record
DK
1999
Direction of spread
Sylt
1986
1991
1995
1995
North Sea
2000
D
2003
2004
1989
2000
1999
1999
2003
2003
2002
2001
1998
Texel
1995
1999
1998
1983
NL
Fig. 2 Distribution of C. gigas in the Wadden Sea. Given are years and sites of
introduction (red; asterisks) and years of first records (black, dots). Map after Reise
et al. 2005
General Introduction
13
1.2.2 History of oyster fishery in the northern Wadden Sea
Until the end of the 19th century the Wadden Sea was famous for a thriving oyster industry
based on extensive subtidal beds of the native European oyster Ostrea edulis. However,
overexploitation and diseases resulted in dramatic decline of the oyster population (Hagmeier
& Kändler 1927, Hagmeier 1941, Reise 1982, 1990). Karl Möbius came up with the concept
of an ecological community – or biocoenosis – by studying the declining oyster reefs (Möbius
1877). However, neither fishing regulations nor the import of seed oysters from France and
The Netherlands could prevent that O. edulis became extinct in the Wadden Sea in the 1940s
or 1950s (Reise 1990). To compensate for the loss of O. edulis, exotic oyster species were
introduced for aquaculture, but only the Pacific oyster Crassostrea gigas turned out to be
profitable. After some preliminary attempts to cultivate C. gigas in the north and east Frisian
Wadden Sea in the 1970s, the only commercial oyster farm started its business in 1986 off the
coast of Sylt in the List tidal basin (Fig. 3, 4).
Sylt
List tidal basin
Oyster farming
Mussel beds
Fig. 3 Study site (List tidal basin; 54°50’ - 55°10’ N, 0 8°20 ’- 08°40’ E). Marked are
intertidal mussel beds and the location of the oyster farm. Satellite picture from
GAF / Euromap
Spat oysters from hatcheries in Great Britain and Ireland are regularly imported and placed in
mesh bags that are deployed on trestles close to the low water line. It takes about 2 years until
the oysters reach marketable size and the annual production is about 2 million individuals.
14
Chapter 1
Fig. 4 Farming of C. gigas in the northern
Wadden Sea. The oysters are kept in mesh
bags on trestles in the low intertidal zone
1.3 C. gigas and the ecology of mussel beds
Shortly after oyster farming had commenced, natural spatfalls occurred and wild C. gigas
were found in the vicinity of the culture plot. In order to metamorphose, oyster larvae need
hard substrates to which they attach themselves by releasing cement drops from a foot gland
(Quayle 1988). From then on, the young oyster will be attached for life. However, hard
surfaces are scarce on the extensive mud and sand flats of the Wadden Sea. Only dead shell
material and epibenthic mussel beds Mytilus edulis provide secondary hard substrata for
sessile species. Therefore, the oysters are mainly
found as epibionts on mussel beds, attached to the
shells of living and dead mussels (Fig. 5). Mussels
generate epibenthic bed structures by attaching
themselves to each other and to other hard material
via byssal threads, which are protein fibres
Fig. 5 Juvenile C. gigas attached
to a living mussel
generated by certain foot glands (Fig. 6). This
creates a three dimensional matrix of connected
living and dead mussels that provides a habitat for a
diverse associated flora and fauna (Riesen & Reise 1982, Tsuchiya & Nishihira 1986,
Dittmann 1990, Matsumasa & Nishihira 1994). This high species richness and biomass
renders mussel beds important food resources for various benthic predators, fish, birds, and
humans (Seed 1969, Dankers & Zuidema 1995, Nehls et al. 1997, Saier 2001). Mussel beds
are also very important for the material flux in shallow water habitats, because they exchange
General Introduction
15
high amounts of particulate matter, nutrients, and oxygen with the water column (Asmus
1987, Dankers et al. 1989, Asmus & Asmus 1990, 1991, Prins & Smaal 1994).
Fig. 6 Intertidal mussel
bed Mytilus edulis.
Inset:
M. edulis attached to
each other with byssal
threads
The densely packed communities are now overgrown by C. gigas, a reef-building invader that
reaches about three to four times the size of native mussels. In comparison to the dynamic
mussel beds where mussels are able to move to a certain extend using their foot and byssal
threads, oyster reefs are more massive and fixed because the individuals are cemented to each
other (Fig. 7).
Fig. 7 Intertidal oyster
reef Crassostrea gigas
in the Oosterschelde,
The Netherlands.
Inset:
start of an oyster reef
with about 20 oysters
attached to each other
16
Chapter 1
In order to assess the future population development of C. gigas and the scope of coexistence
with native mussels, different aspects of biotic interactions between oysters and their recipient
habitat were studied. Firstly, population parameters like abundances and length-frequency
distributions were recorded in different locations and years. Secondly, field experiments were
conducted to compare recruitment, survival, and growth of C. gigas with native mussels,
thereby taking important biological interactions on mussel beds into account. For example,
mussel beds may be partly covered with a thick layer of the brown macroalga Fucus
vesiculosus forma mytili (Fig. 8). Fucus-cover reduces current velocities above the mussel
bed, enhances sedimentation, and has negative impacts on abundances of mussels and their
epibionts, but supports various herbivores and increases overall macrobenthic diversity
(Albrecht & Reise 1994). Another important factor for mussel bed dynamics is epibiosis
(Albrecht & Reise 1994, Wahl et al. 1997, Laudien & Wahl 1999, Buschbaum & Saier 2001,
Buschbaum 2002). In the Wadden Sea, the barnacles Semibalanus balanoides and Balanus
crenatus are the most abundant epibiont species on mussels (Fig. 8). Their impacts on mussels
are two sided: they reduce the growth rate of their basibiont, but enhance mussel recruitment
(Grant 1977, Saier 2001, Buschbaum 2002).
Fig. 8 Fucus-cover on mussel
bed (left); Barnacle overgrowth
on mussel shells (right)
As mussel populations are often limited by predation, field and laboratory experiments were
carried out in order to assess whether low predation pressure by the main benthic predators,
the shore crab Carcinus maenas and the starfish Asterias rubens, may facilitate a competitive
advantage of C. gigas over M. edulis (Fig. 9).
Fig. 9 Shore crab Carcinus
maenas (left) and starfish
Asterias rubens (right). Starfish
photo by C. Buschbaum
General Introduction
17
1.4 Outline of the study
This study is divided into four separate manuscripts each dealing with a different aspect of the
life history of C. gigas: population development (chapter 2), recruitment (chapter 3), survival
and growth (chapter 4), and predation (chapter 5). In chapter 6 results are summarised and the
impact of a possible regime shift with mussel beds being largely replaced by oyster reefs is
discussed on species and ecosystem level.
Chapter 2 describes the population development of C. gigas in the northern Wadden Sea
and links the recent massive increase in abundances to high recruitment success in years
with abnormally high summer water temperatures.
In chapter 3, recruitment patterns of C. gigas and M. edulis are compared in order to
assess whether habitat preferences may facilitate niche separation and coexistence of both
species.
Chapter 4 deals with survival and growth of C. gigas and M. edulis in relation to tide
level, substrate, barnacle epigrowth and algal cover. In field experiments it was
investigated whether habitat requirements of both species are similar or whether there are
species-specific refuges from potential competition.
In chapter 5, the hypothesis that low predation pressure by resident predators may
facilitate a competitive advantage of C. gigas over M. edulis was tested. Therefore,
predator exclusion experiments and laboratory feeding preference experiments with shore
crabs Carcinus maenas and starfish Asterias rubens as predators were conducted.
In chapter 6 it is concluded that most mussel beds will become replaced by oyster reefs
which may be overgrown with varying numbers of M. edulis. This will have consequences
on the food web and other ecosystem properties.
18
Chapter 1
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Invasion accelerated by warm summers?
25
Chapter 2
Introduced Pacific oysters (Crassostrea gigas) in the northern
Wadden Sea: invasion accelerated by warm summers?
Abstract
Among the increasing number of species introduced to coastal regions by man, only a few are
able to establish themselves and spread in their new environments. We will show that the
Pacific oyster (Crassostrea gigas) took 17 years before a large population of several million
oysters became established on natural mussel beds in the vicinity of an oyster farm near the
island of Sylt (northern Wadden Sea, eastern North Sea). The first oyster, which had dispersed
as a larva and settled on a mussel bed, was discovered 5 years after oyster farming had
commenced. Data on abundance and size frequency distribution of oysters on intertidal
mussel beds around the island indicate that recruitment was patchy and occurred only in 6 out
of 18 years. Significant proportions of these cohorts survived for at least 5 years. The
population slowly expanded its range from intertidal to subtidal locations as well as from Sylt
north- and southwards along the coastline. Abundances of more than 300 oysters m-2 on
mussel beds were observed in 2003, only after two consecutive spatfalls in 2001 and 2002.
Analyses of mean monthly water temperatures indicate that recruitment coincided with aboveaverage temperatures in July and August when spawning and planktonic dispersal occurs. We
conclude that the further invasion of C. gigas in the northern Wadden Sea will depend on high
late summer water temperatures.
Keywords
Crassostrea gigas, Introduced species, Recruitment, Water temperature, Wadden Sea
26
Chapter 2
1 Introduction
Marine ecosystems have always been subject to changes in species composition and
interactions, but natural migration of organisms due to climatic and geographic variations is
becoming superimposed by anthropogenic vectors facilitating a much faster and wider
distribution into new habitats. Important vectors are intercontinental shipping and the
commercial transport of aquaculture products from one coast to another (Chew 1990, Carlton
& Geller 1993, Carlton 1996, Reise et al. 1999, Gollasch et al. 2000, Ruiz et al. 2000, Naylor
et al. 2001, Wolff & Reise 2002). However, only about ten percent of these introduced species
are expected to become established and to spread in their new environments, and only a small
fraction may furthermore induce changes to the recipient ecosystem (Williamson & Fitter
1996).
In the North Sea, at least 80 non-indigenous species have established themselves in historical
time and most of them inhabit the coastal and estuarine zones (Reise et al. 1999, Wolff 1999).
Approximately 50% of these species were introduced through aquaculture, that is, either the
imported target species was released into the wild or associated organisms were
unintentionally co-introduced. Examples of species that were introduced with shellfish are the
American slipper limpet Crepidula fornicata (Hagmeier 1941, Werner 1948, Thieltges et al.
2003) and various parasites such as the copepods Mytilicola orientalis and M. ostreae (Stock
1993).
The oyster fishery industry and accompanying shellfish imports have a long tradition in the
North Sea. Until the end of the nineteenth century, the extensive subtidal beds of the
European oyster Ostrea edulis supported a thriving fishing business. Overfishing, however,
resulted in a dramatic decline in the native oyster population as the demand for fresh oysters
grew (Hagmeier & Kändler 1927, Hagmeier 1941, Reise 1982, 1990). Fishermen thereupon
started to import large numbers of seed oysters to restock the local oyster grounds but with no
success (Möbius 1877, Hagmeier 1941, Korringa 1976, Utting & Spencer 1992). Only the
cultivation of the Pacific oyster Crassostrea gigas turned out to be commercially successful.
This oyster originates from Japan and has been distributed in oyster cultures all over the
world since the early twentieth century (Andrews 1980, Quayle 1988, Arakawa 1990, Chew
1990). In most regions, the Pacific oysters did not remain restricted to their culture plots, but
reproduced and dispersed successfully in the new environments (e.g. British Columbia:
Qualye 1988, Australia: Ayres 1991, and New Zealand: Dinamani 1991). In the North Sea
Invasion accelerated by warm summers?
27
imports of C. gigas started in 1964 in the Netherlands (Drinkwaard 1999), followed by
transports to England (Walne & Helm 1979, Utting & Spencer 1992, Spencer et al. 1994),
France (Maurin & LeDantec 1979, Grizel & Héral 1991) and Germany (Neudecker 1985).
Whereas only sporadic natural spatfalls occurred in Great Britain (Spencer et al. 1994, Smith
1994, Eno et al. 1997), wild oyster populations are growing fast in France (Grizel & Héral
1991) as well as in the Netherlands (Drinkwaard 1999, Dankers et al. 2004). The success of
natural recruitment and the rate of spread are different in these locations and seem to depend
on abiotic factors such as water temperature and salinity (Quayle 1988, Ayres 1991, Spencer
et al. 1994).
The spread of the Pacific oyster in the northern Wadden Sea began 5 years after the first
German oyster farm had started its business off the island of Sylt in 1986 (Reise 1998). The
first oyster that had dispersed as a larva was found on an intertidal mussel bed (Mytilus edulis)
about 6.5 km north of the oyster farm. Oysters are found mainly as epibionts on natural
mussel beds because they need hard substrates to settle on. Oyster larvae use the shells of
living and dead mussels as attachment surface because mussel beds represent one of a limited
number of secondary hard substrata available on the extensive mud and sand flats in the
Wadden Sea. In this article, we describe the slow expansion of a wild C. gigas population
since the first settlement of spat in 1990 and suggest that the increase in population size may
be retarded by irregular recruitment, which we assume is limited by late-summer water
temperatures.
2 Methods
2.1 Study site
The Wadden Sea is a large intertidal area in the south-east part of the North Sea, characterized
by extensive mud and sand flats. First records of Crassostrea gigas on intertidal mussel beds,
revetments, and harbour constructions are given for the northern Wadden Sea, which extends
from Esbjerg (Denmark) in the north to the Elbe estuary (Germany) in the south (Fig. 1). The
quantitative surveys of C. gigas abundances and size distributions were carried out on
intertidal mussel beds close to the island of Sylt (North Frisian Wadden Sea, Germany; Fig.
2). Sylt is adjacent to two tidal basins: the List basin in the northeast and the Hörnum basin in
the southeast. The List tidal basin (54°50’ - 55°10’N and 08°20’ - 08°40’E) is largely closed
28
Chapter 2
by dams to the north and south and covers an area of about 404 km². It is connected to the
North Sea through a narrow tidal inlet of only 2.8 km in width (Reise & Riethmüller 1998).
Tides are semidiurnal and the mean tidal range is 2 m; the average salinity is close to 30 psu.
Long term mean water temperatures (based on monthly mean temperatures) range from
18.2°C in August to 2.3°C in February. Intertidal flats, which are mostly sandy, make up
33% of the area (Reise & Lackschewitz 1998), and intertidal mussel beds cover 1.5 km2
(Nehls 2003, Stoddard 2003). The Hörnum tidal basin in the south of Sylt is widely open to
the North Sea. It covers 290.2 km² (Spiegel 1997) and contains at present only five small
mussel beds that cover about 0.04 km² of the intertidal zone (Nehls 2003, Stoddard 2003).
2003 Esbjerg
Rømø
RØ
1999
Oyster farming
since 1986
KH
OW
BL
1991
KO
LH
Subtidal spatfall 2003
List basin
PT
Sylt
1995
2003
MM
2000
KE
RS
RA
PK
Helgoland
0
10
20
2003
Hörnum basin
2004
30 Kilometer
Föhr
0
Fig. 1 Northern Wadden Sea from Esbjerg
(Denmark) to Elbe estuary (Germany) with first
records of Crassostrea gigas. Grey areas
represent intertidal mud and sand flats
5
10
15 Kilometer
Fig. 2 Map of Wadden Sea near Sylt (List and
Hörnum tidal basin) with labelled intertidal
mussel beds (for abbreviations see Table 1)
Invasion accelerated by warm summers?
29
2.2 Abundance and size of C. gigas on intertidal mussel beds
Comprehensive field surveys on the abundance of C. gigas were carried out twice near the
island of Sylt. The first survey took place from March to May and from September to October
1999 on 12 intertidal mussel beds: 11 in the List tidal basin and 1 in the Hörnum tidal basin
(Fig. 2). The second survey was conducted in July and August 2003 on 10 intertidal mussel
beds: 8 in the List basin and 2 in the Hörnum basin. Two mussel beds were also visited in
spring and autumn 2001 and 2002 to detect changes in abundance on a smaller time scale. The
data are compared with those from a survey that was done in the same area and in the same
way in 1995 by Reise (1998).
The abundance of C. gigas on intertidal mussel beds was determined by randomly placing a
frame of 50 × 50 cm (0.25 m²) within the area covered by mussels. During the 2003 survey
we used a smaller frame (25 × 25 cm) on the mussel beds Munkmarsch and Königshafen
because of the very high oyster abundances. The oysters inside the frame were counted. If the
mussel bed patch was covered with fucoid algae, these were lifted and the oysters beneath the
algal canopy were counted. The number of replicates varied with the amount of time available
due to the turning tide and the size of the mussel bed (11 - 238 per site). Field surveys were
carried out before the recruitment of the same year took place or before the recruits were large
enough to be counted. The recorded abundances, therefore, did not include the 0-group of the
respective year and the spring and fall data from 1999 can be compared with those of July and
August in 1995 and 2003. The total amount of C. gigas in the List basin in 2003 was
calculated by multiplying the overall mean abundance of C. gigas by the total area within the
basin that was covered with mussel beds in 2003: 1.54 km² mussel bed area, mussel coverage
31%, i.e. 0.48 km² mussel ground. These data are derived from a regular monitoring program
that surveys the size of mussel beds with aerial views and ground inspection with a global
positioning system (GPS). Mussel coverage is determined by walking in linear transects
across the mussel beds and counting the amount of steps that hit areas covered with mussels
and steps that hit areas with no living mussels (Nehls 2003 and more recent data).
The length-frequency distribution of C. gigas was investigated by measuring the shell length
(largest diameter of the shell) of oysters that were randomly encountered on the mussel bed.
Shell length was measured with vernier callipers to the nearest millimetre.
Results are given as arithmetic means with standard deviations (SDs). Data of abundance
were analysed with non-parametric tests because of the heterogeneity of variances despite
transformation. We used Kruskal-Wallis analysis of variance (ANOVA) followed by Mann-
30
Chapter 2
Whitney U-tests (software STATISTICA 1999 by StatSoft). Differences were considered
significant at P < 0.05.
2.3 Biomass
Biomass of C. gigas on different mussel beds in 2003 was estimated by using an exponential
relation between dry weight (meat and shells) and length of 83 oysters collected on two
mussel beds (y = 0.0002x2.8072, R2 = 0.9122). With this equation we determined the biomass
of C. gigas on each mussel bed by converting the length of the oysters into dry weight data.
2.4 Abundance and size of C. gigas on subtidal habitats
Abundance of C. gigas on subtidal mussel beds in tidal channels around Sylt was estimated
by taking hauls with a traditional oyster dredge (see Reise et al. 1989). These dredge hauls
were carried out in 1999 (20 hauls at two locations), 2001 (22 hauls at two locations), 2002
(10 hauls at one location), and 2004 (30 hauls at three locations). The distance dredged and
the geographic position was noted for each haul. Furthermore, we counted the number of C.
gigas in each haul and measured the shell length as longest diameter of the oyster shell.
2.5 Water temperature
Since 1984, surface water temperatures are regularly measured (about twice weekly) in the
main tidal channel near List and at the entrance of Königshafen bay. Temperature data
presented in this paper are based on mean monthly values from 1987 to 2003. Results are
given as arithmetic means with standard deviations and analysed with t-tests for independent
variables. All data were tested for homogeneity of variances using the Levene test. Deviations
from the monthly mean water temperatures for the months July and August were calculated
by subtracting the mean water temperature in each year from the long-term average (1987 2003).
Invasion accelerated by warm summers?
31
3 Results
3.1 Distribution of C. gigas in the North Frisian Wadden Sea
Since 1986, the oyster farm located on the tidal flats east of the island of Sylt (List tidal basin)
produces about 2 million oysters per annum (Fig. 1). A wild oyster population developed in
the area due to larval dispersal and the first wild oysters were found in Königshafen bay in
1991. A quantitative survey in 1995 revealed that 14 out of 17 mussel beds in the List tidal
basin were colonised with C. gigas. In the Danish Wadden Sea north of the List basin, adult
C. gigas were found in the Juvre tidal basin near the island Mandø (1999) and at the northern
end of the Wadden Sea near Esbjerg (2003: 6.8 individuals m-2). South of Sylt, Pacific oysters
were found in Hörnum tidal basin (first record in 1995), east of the island of Amrum (1995),
at Nordstrand (2000), near the island of Pellworm (2003) and near Büsum (2004). On the
offshore island of Helgoland, wild C. gigas were found from 2003 onwards. Oyster densities
in the northern Wadden Sea outside the List basin are, however, still much lower than inside.
Abundances stayed below 1 m-2 in 2003 on all mussel beds in the North Frisian Wadden Sea
south of the List basin (except one mussel bed in Hörnum basin which contained 1.8
indiviudals m-2).
3.2 Abundance of C. gigas on intertidal mussel beds near Sylt
In 1995, some mussel beds on the tidal flats near Sylt and Rømø were still without oysters,
but by 1999 living C. gigas were found on all investigated intertidal mussel beds (Fig. 2,
Table 1). The mean abundance of oysters in the List tidal basin, however, did not increase. In
1995, Reise (1998) counted 3.6 individuals m-2, and in 1999, we found 3.7 m-2. This changed
profoundly by 2003, when the mean abundance of C. gigas reached 125.8 oysters m-2 on
intertidal mussel beds. This is equivalent to about 2,100 g dry weight (including shell and
meat) m-2.
Using the data of mean abundance (125.8 m-2) and the total area of intertidal mussel beds
(0.48 km²), we estimate for the List tidal basin a number of 60.4 million oysters in 2003 (i.e.
approximately 1,000 t dry weight). The population development of C. gigas stagnated in the
tidal basin in the south of Sylt (Hörnum basin). Abundances stayed on a low level throughout
the entire period from 1995 to 2003.
32
Chapter 2
Table 1 Abundance (individuals / 0.25 m² ± SD), number of samples, and biomass (grams dry weight
per square metre) of Crassostrea gigas on 15 intertidal mussel beds in the Sylt area: 13 in the List
tidal basin and 2 in Hörnum tidal basin. Blank cells: no data available. Asterisks indicate that mussel
beds no longer exist. For location of sites see Fig. 2. Data for 1995 from Reise (1998).
Site
Abundance
2
Individuals / 0.25 m
1995 1999 2003
List basin
RØ Rømø
KO Koldby
KH Königshafen
KH1 Mövenbergwatt
KH2 Ostfeuerwatt
KH3 Uth. Außenwatt
OW Oddewatt
BL Blidsel
LH Leghörn
PT Pander Tief
MM Munkmarsch
KE Keitum
RS Rauling-Sand
0
0
2.1
0.9
0.6
1.6
0.6
2.1
1.2
0
0.2
1.9
0.4
0.8
1.0
0.1
0.8
0.8
3.3
0.8
0.1
1.6
0.4
77.2
*
*
61.3
*
32.8
23.2
69.3
41.7
7.0
0.1
1995
Number of samples
SD
1999
0.4
2.0
1.1
2.3
1.5
0.8
1.8
0.9
2.0
1.1
1.4
1.3
4.4
1.5
Mean
0.1
0.4
0.1
0.1
0.5
0.7
0.3
Grams / m²
2003
1995
1999
2003
1995
1999
2003
2003
1.1
0.7
48.4
*
*
33.3
*
16.9
15.2
57.6
26.4
6.6
40
32
48
32
29
25
21
23
*
*
15
*
14
18
75
29
24
11
0
0
8.2
3.6
0.9
13.2
3.0
0.3
6.4
1.6
308.9
*
*
245.3
*
131.1
92.9
277.0
166.6
27.8
0.4
30.2
31.7
1967.1
*
*
1232.0
*
1381.7
793.9
11386.1
4168.5
469.2
0
3.6
3.7
125.8
2146.0
0.5
1.7
0.3
0.2
1.8
27.8
148.0
1.1
0.3
1.0
87.9
70
80
48
40
44
36
238
65
89
54
80
165
236
126
82
58
Mean
Hörnum basin
RA Rantum
PK Puan Klent
Individuals / m²
0.8
32
48
20
38
22
2.4
6.2
2.2
8.2
4.6
0
7.8
1.5
3.4
3.9
0.5
3.1
3.3
We focus on seven mussel beds, one at the northern end of the List basin (RØ), five adjacent
to the island of Sylt in the List basin (KH, BL, LH, MM, KE) and one in the southern basin
(PK) in order to describe the population development of C. gigas in more detail (Fig. 3). By
comparing the oyster densities in 1995 and 1999, it turns out that a significant increase in
abundance only occurred on two mussel beds in the List basin, MM (Kruskal-Wallis
ANOVA, P < 0.0001; Mann-Whitney U-test, P = 0.011) and KE (Kruskal-Wallis ANOVA, P
< 0.0001; Mann-Whitney U-test, p = 0.009), whereas on two other mussel beds, BL (KruskalWallis ANOVA, P < 0.0001; Mann-Whitney U-test, P < 0.001) and PK (Kruskal-Wallis
ANOVA, P = 0.001; Mann-Whitney U-test, P = 0.014), a significant decrease in numbers
occurred. Four years later, in 2003, abundances of C. gigas were significantly higher on all
mussel beds in the List basin, with Königshafen containing over 300 oysters m-2. It is
remarkable that the mussel bed in the north of the List basin (RØ) and the one in the southern
basin (PK) still showed comparatively low oyster densities (6.4 m-2 for Rømø, and 1.8 m-2 for
Puan Klent). The mean values of oyster abundance on the five mussel beds adjacent to Sylt in
the List basin increased from 4.3 m-2 in 1995 and 6.1 m-2 in 1999 to 145.5 m-2 in 2003.
Invasion accelerated by warm summers?
Individuals 0.25 m-2
1000
1995
1995
1999
2003
1999
100
33
RØ
0
0.2 (± 0.4)
1.6 (± 1.1)
List basin
PK
1.1 (± 0.8)
0.4 (± 0.7)
1.5 (± 1.1)
0.1 (± 0.3)
36.4 (± 26.2) 0.5 (± 0.8)
2003
***
10
*
**
*
1
0
0
0
RØ
KH
North
BL
LH
MM
List basin (Sylt)
KE
PK
South
Fig. 3 Mean abundance (individuals per 0.25 m² + SD; logarithmic scale) of C. gigas on 7
intertidal mussel beds (RØ, KH, BL, LH, MM, KE, PK) near Sylt surveyed in 1995, 1999, and
2003. Sample size varied between n = 14 and n = 238. Asterisks mark significant differences
between 1995 and 1999 data sets (Mann-Whitney U-test): * 0.05 > P ≥ 0.01, ** 0.01 > P ≥
0.001, *** P < 0.001. Inset: mean abundance of C. gigas (individuals per 0.25 m-2 ± SD) on
mussel bed RØ, over all five mussel beds in List basin (Sylt) and on mussel bed PK
3.3 Length-frequency distribution of C. gigas
In Fig. 4, we present length-frequency distributions of C. gigas on two mussel beds (KH and
MM) from 1999 to 2004. Based on these frequency distributions the age structure of the
population is described by distinguishing different year classes and calculating their length
increments. By growth experiments we verified that peaks in these graphs indicated yearclasses: juvenile oysters reach 20 - 33 mm shell length in the first spring after settlement in
the previous summer. They will continue to grow to 40 - 60 mm by the end of the growing
season in November and will remain this size until the next growing period starts in April
(own unpublished data). In spring 1999, oysters at the Königshafen site were represented by a
distinct year class between 25 and 65 mm shell length (cohort of 1997) and some older
individuals. The cohort of 1997 represented 53% of all oysters in this area. The distribution
looked similar at Munkmarsch, but with a higher proportion of oysters of the year class 1997
(86%). Until fall 1999, the 1997-year class grew by 20 to 30 mm in shell length to
approximately 50 to 100 mm.
34
Chapter 2
4
2
6
4
1
2
0
0
5
25
45
65 85 105 125 145 165
Length (mm)
4
2
45
65 85 105 125 145 165
Length (mm)
Apr 01
8
6
4
1
2
0
0
5
25
45
5
65 85 105 125 145 165
Length (mm)
4
25
45
65 85 105 125 145 165
Length (mm)
10
Apr 02
2
Apr 02
Oct 02
8
Ind. / m²
3
Ind. / m²
25
10
Ind. / m²
Ind. / m²
5
Apr 01
Nov 01
3
1
6
4
2
0
0
25
45
120
4
2
1
0
40
85
95 105 115 125 135 145 155 165
25
45
60
Apr 03
Aug 03
3
80
5
65 85 105 125 145 165
Length (mm)
65 85 105 125 145 165
Length (mm)
May 03
Aug 03
10
50
Ind. / m²
5
Ind. / m²
May 99
Sept 99
8
Ind. / m²
3
Ind. / m²
10
Apr 99
Nov 99
8
6
40
4
2
30
0
20
85
95 105 115 125 135 145 155 165
10
0
0
5
25
45
5
65 85 105 125 145 165
Length (mm)
120
45
65 85 105 125 145 165
Length (mm)
60
Apr 04
80
40
May 04
50
Ind. / m²
Ind. / m²
25
40
30
20
10
0
0
5
25
45
65 85 105 125 145 165
Length (mm)
5
25
45
65 85 105 125 145 165
Length (mm)
Fig. 4 Length-frequency distribution of C. gigas on two intertidal mussel beds near Sylt
(left Königshafen; right Munkmarsch) from 1999 to 2004. Number of individuals
measured varied between n = 68 and n = 307. Insets in 2003 graphs depict large size
classes on a lower scale to show survival of adults
Invasion accelerated by warm summers?
35
It is important to note that we did not consider oyster spat in the fall monitoring because these
oysters were still too small to be counted. The offspring of the summer of a certain year is,
therefore, first represented in the spring graphs of the following year. The spring graphs,
however, still show a lower abundance of juvenile oysters than the subsequent autumn graphs,
because the recruits of the previous summer were still too small to be included adequately in
the spring monitoring. By autumn, however, the oysters had grown to a larger size and were
more adequately represented. This is especially the case in the Königshafen 1999 and in the
Königshafen and Munkmarsch 2003 graphs.
The data set from April 2001 shows a much older population than in April 1999 for both
Königshafen and Munkmarsch. There were no signs of any significant recruitment or
mortality in 1999 and 2000. The size distribution of C. gigas in Königshafen for April 2002
was similar to that for 2001, but a strong recruitment was apparent at Munkmarsch with 60%
of the oysters measuring less than 30 mm. This 2001 cohort grew approximately 30 mm by
October 2002. In spring 2003, recruitment on both mussel beds was evident: the majority of
oysters belonged to the year class of 2002. This cohort grew by about 20 mm until August
2003 and represented 97% of the Königshafen population and 76% of the Munkmarsch
population. In April/May 2004, oyster recruitment from the previous summer was evident on
both mussel beds.
It is important to note that the 1997 cohort was still present in 2002 in almost the same
numbers as in the years before, that is, no detectable mortality occurred from 1999 to 2002,
suggesting a high survival rate of 2- to 5-year-old oysters. Even in 2003, the 1997 cohort was
still present (see insets in Fig. 4).
3.4 Mean water temperatures and C. gigas recruitment
The comparison of monthly mean water temperatures during years with notable C. gigas
recruitment (1991, 1994, 1997, 2001, 2002, 2003) and years with no measurable recruitment
(1987 - 1990, 1992, 1993, 1995, 1996, 1998 - 2000) revealed significantly higher water
temperatures in July and August in recruitment years (Fig. 5). No significant differences in
water temperatures occurred for all other months. Deviations of water temperatures from the
long-term mean (1987 - 2003) in July and August show that successful recruitment only
occurred in relatively warm summers (Fig. 6).
36
Chapter 2
Water temperature (°C)
25
High recruitment
**
**
6
7
Month
8
Low recruitment
20
15
10
5
0
1
2
3
4
5
9
10
11
12
Fig. 5 Monthly means of water temperature (°C) during year s with notable or
high C. gigas recruitment (1991, 1994, 1997, 2001, 2002, 2003) and years
with no or very low recruitment (1987-1990, 1992, 1993, 1995, 1996, 19982000). Significant differences in water temperature occurred in July (7) and
August (8; ** P = 0.008 and P = 0.001, respectively; t-test for independent
variables)
4
Temperature (°C)
3
July
August
2
1
0
-1
-2
-3
'87 '88 '89 '90 '91 '92 '93 '94 '95 '96 '97 '98 '99 '00 '01 '02 '03
Year
Fig. 6 Deviations of mean monthly water temperatures in July and August
from the long-term mean (1987 - 2003). Arrows mark years with high C.
gigas recruitment (1991, 1994, 1997, 2001, 2002, 2003)
3.5 Abundance and size of C. gigas in the subtidal zone near Sylt
Dredge hauls in subtidal channels around the island of Sylt in the time period from 1992 to
1996 did not yield any living C. gigas (Reise 1998). In 1999, we fished at two locations
(Munkmarsch and Königshafen) of subtidal mussel stocks and found only one and three adult
Invasion accelerated by warm summers?
37
oysters, respectively (Table 2). The Munkmarsch site was again investigated in 2001 and
2002 and we still only caught four and two oysters, respectively. In 2004, however, we found
95 oysters at Munkmarsch and 25 at Königshafen. There was a noticeably high proportion of
juvenile oysters present. Another 10 dredge hauls in the middle of the tidal basin yielded 428
living oysters of which 33% belonged to the 2003 year class.
Table 2 Dredge hauls in subtidal channels in the List tidal basin. Given are locations, number of hauls,
and area fished. The distance dredged varied between 150 and 470 m. Also total number and length
of C. gigas for each location are shown. Data for 1992 - 1996 from Reise (1998)
1992 - 1996
1999
2001
2002
2004
Location
Sylt area
MM
KH
MM
KO
MM
MM
KH
Bay
No. of hauls
Area (m²)
No. of C. gigas
216
108,000
0
10
4,000
1
10
2,000
3
10
4,000
4
12
3,000
12
10
3,000
2
10
3,700
95
10
2,100
25
10
3,000
428
108
70 - 109
Length (mm)
Min - max
Mean (±SD)
-
75 - 137
28 - 144
99.8 (±26.5) 94.5 (±31.9)
5; 120
5 - 134
8 - 146
2 - 97
56.7 (±28.7) 59.6 (±29.5) 38.5 (±23.4)
4 Discussion
Since 1986, a potential spawning population of Crassostrea gigas has been cultured for
commercial purposes at Sylt. Significant recruitment in the area only took place in 1991,
1994, 1997, 2001, 2002 and 2003 (i.e. in 6 out of 18 years). This indicates that the
reproductive success of C. gigas in the northern Wadden Sea is not a regular phenomenon but
occurred only in about one-third of the years since the local introduction of the species.
The expansion of Pacific oysters in the Wadden Sea near Sylt started off slowly with the
colonisation of certain intertidal mussel beds near the oyster farm. Successful recruitment did
not occur in all suitable habitats, and it was not before 1999 that all mussel beds in the List
tidal basin contained wild C. gigas. Nevertheless, strong recruitment was still confined to
certain locations within the basin. By 2003, some mussel beds in the area still had very low
oyster densities, whereas a massive population increase took place in other areas. In 2001, for
example, recruitment occurred on mussel beds in the southern part of the List basin but not in
the northern part (approximately 15 km apart).
The spread towards areas outside the List tidal basin also occurred slowly. Abundances of C.
gigas on mussel beds in the Hörnum basin in the south of Sylt remained at a low level until
2003, although living C. gigas had been found from 1995 onwards. Also near the islands
38
Chapter 2
further south (Föhr, Amrum, Pellworm) abundances are still low in comparison to northern
Sylt. The same is true for the Danish Wadden Sea, where C. gigas is now present although
still in low numbers. The origin of the oysters south of the island of Sylt is not clear, as
natural transport against the south-north current is unlikely and may only occur on rare
occasions. Transport from the List basin due to mussel farming activities is possible, as well
as further introductions from several experimental cultures in the North Frisian Wadden Sea.
Larval drift from the Oosterschelde or the Dutch Wadden Sea, however, seems to be rather
unlikely. Transport times between Texel and the North Frisian Wadden Sea amount to about
150 days (de Ruijter et al. 1988) and are, therefore, longer than the mean lifetime (3 - 4
weeks) of pelagic larvae (Neudecker 1985, Quayle 1988). The extended planktonic larval
period nevertheless allows a high dispersal by currents as has been described for C. gigas in
British Columbia, where settlement of wild oysters occurred 60 km away from the next oyster
farm (Elsey & Qualye 1939).
Larval retention in the List tidal basin, however, should be high as it is practically enclosed
and is only connected to the North Sea by a 2.8-km-wide channel. This is very favourable to
the oyster larvae because they remain on suitable sites close to their origin, and this certainly
facilitates population growth when adult stocks are still low. Larvae in more open areas may
be widely distributed and are, therefore, less likely to find suitable settling substrates and
subsequently perish. The List tidal basin thus offers ideal conditions for the spread of species
with planktonic larvae due to the continuous input of larvae from the local oyster farm and the
closed bay environment.
The fast development of oysters in the closed Oosterschelde and the much later spread into
the Dutch and western German Wadden Sea followed the same pattern (Wehrmann et al.
2000, Dankers et al. 2004). Within the bay, the slow and patchy expansion presumably does
not result from a lack of dispersal but from limited larval supply or poor initial survival after
settlement. This might also explain the slow colonisation of subtidal habitats. It is important
to note that the site where we found juvenile C. gigas used to be an important subtidal spatfall
area of blue mussels (Ruth 1994) and is located about 7 km from the nearest intertidal mussel
bed. These findings are thus the first clear indications of subtidal spatfall in Pacific oysters in
the Northern Wadden Sea. Even though C. gigas is considered to be more an intertidal
species, it has the capability to colonise subtidal habitats (Buroker 1985). In the Oosterschelde
(The Netherlands), where Pacific oysters have been introduced in the 1960s, C. gigas is now a
dominant species in intertidal and subtidal benthic communities (de Kluijver & Leewis 1994,
Invasion accelerated by warm summers?
39
Leewis et al. 1994, Meijer & Waardenburg 1994, Drinkwaard 1999). In British Columbia, C.
gigas is found only in intertidal habitats, presumably because low temperatures in deeper
waters limit the survival of larvae and juveniles (Quayle 1988).
The irregular recruitment of C. gigas in the northern Wadden Sea is apparently no threat to
the population because of the high survival rate after 1-year-old cohorts have become
established. As the cohort of 1997 showed high persistence during the subsequent 5 years, a
failure in reproductive success during 4 consecutive years is not expected to threaten
population maintenance. The long persistence of C. gigas populations has also been reported
from Great Britain, where adult oysters were still present 9 years after the closure of an oyster
farm (Smith 1994).
What could be the reason for this irregular recruitment success? We compared water
temperature regimes in years with notable or high oyster recruitment and those with no or low
reproductive success and found that high recruitment corresponded with higher than average
water temperatures in late summer. This is an important time period in the oyster life cycle:
spawning occurs, larvae are dispersed and juveniles settle on hard substrates. In the Wadden
Sea, C. gigas spawns in late July and August. After fertilisation, pelagic larvae develop and
will stay in the water column for 21-30 days before settlement occurs (Neudecker 1985,
Quayle 1988). The importance of temperature for oyster spawning and recruitment has been
described by various authors. In Japan, 23-25°C is considered as the optimum water
temperature for successful recruitment (Korringa 1976, Kobayashi et al. 1997), and even
though spawning has been observed in British Columbia (Canada) at 15°C, the optimal
temperature for larval development is considered to be 23°C (Quayle 1988). In Great Britain,
C. gigas has been observed to spawn from 18°C onwards but natural recruitment is sporadic
and occurred only in exceptionally warm summers (Mann 1979, Spencer et al. 1994). In the
Oosterschelde (The Netherlands), C. gigas was introduced in 1964 and the first natural
recruitment was observed in 1975 and 1976 during exceptionally warm summers with water
temperatures above 20°C in July and August of 1976 (Drinkwaard 1999). The next major
larval outbursts occurred in 1982, 1986, and 1989 (Drinkwaard 1999). The oyster population
increased dramatically from then onwards. Monitoring of the area expansion of oyster reefs in
the Oosterschelde revealed an increase from 0 ha in 1976 to 15-35 ha in 1980, 210-370 ha in
1990, and 640 ha in 2002 (Kater & Baars 2003). In France, C. gigas expanded much faster.
Since the introduction of broodstock from British Columbia and Japan in 1971, spat
recruitment was successful with the exception of three specific years (1972, 1981, and 1986)
40
Chapter 2
where abnormally low temperatures were held responsible for low spatfalls (Grizel & Héral
1991). A similar rapid rise in oyster densities occurred in New Zealand, where the first
naturally dispersed oysters were found in 1971 and a strong increase in spat abundance has
been observed ever since. A marked rise in temperature during the main spatting period was
held responsible for the dramatic increase of C. gigas spatfalls, which superseded those of the
native rock oyster Saccostrea glomerata in 1978 (Dinamani 1978, 1991). In Tasmania and
New South Wales (Australia), however, only erratic spatfalls occurred after the introduction
of C. gigas and low water temperature and high salinity were considered to be major limiting
factors (Ayres 1991). Nevertheless, large oyster reefs were formed about 9 years after the first
oyster spat was observed in Tasmania and a rapid spread was documented in some estuaries in
New South Wales. Comparing the spread and recruitment success of C. gigas in the Wadden
Sea with that in other areas, it can be assumed that Pacific oysters here are at the edge of their
physiological range and are expected to rely on high late summer water temperatures
occurring at least once every 5 years.
It is well known that the spread of exotic species may depend on temperature regimes and
may profit from climate change (Lodge 1993, Nehring 1998, Franke et al. 1999, Stachowicz
et al. 2002, Walther et al. 2002). In the Wadden Sea, the American slipper limpet (Crepidula
fornicata) is limited by cold winter temperatures and is expected to increase in abundance if
climate change should lead to milder winters (Thieltges et al. 2004). Another example is the
introduced cord-grass, Spartina anglica, which is increasing in the northern Wadden Sea
presumably as a result of warmer spring seasons (M. Loebl, J.E.E. van Beusekom, and K.
Reise, submitted). Regarding the Pacific oyster, a possible climate change involving warmer
late-summer water temperatures or a higher frequency of hot summers could have a profound
impact on its abundance in the northern Wadden Sea.
Acknowledgements
We thank the crew of FS “Mya” for assisting in subtidal sampling and Catharina Claus for her
help during the 2003 survey. Thomas Jensen (Vadehavscentret Ribe) provided a record for the
Juvre tidal basin, Maarten Ruth for Amrum, and Fritz Buchholz for Helgoland. The work of
Georg Nehls is carried out on behalf of the Regional Office for the Wadden Sea National Park
of Schleswig-Holstein. The methods used in this survey comply with the current laws in
Germany.
Invasion accelerated by warm summers?
41
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Differential recruitment of introduced Pacific oysters and native mussels
45
Chapter 3
Differential recruitment of introduced Pacific oysters and native
mussels at the North Sea coast: coexistence possible?
Abstract
Pacific oysters (Crassostrea gigas Thunberg 1793) have been introduced into the Wadden Sea
(North Sea) where they settle on native mussel beds (Mytilus edulis L.), which represent the
only extensive insular hard substrata in this soft sediment environment. As abundances of C.
gigas rose, some mussel beds became increasingly overgrown with oysters, whereas others
did not. Field experiments revealed that recruitment of C. gigas was higher in the lower
intertidal than in the upper subtidal zone, that it was higher on conspecifics than on mussels,
and that it was not affected by barnacle epigrowth except when settling on mussels. Mussel
recruitment is known from inter- and subtidal zones. It occurred equally on oyster and mussel
shells but showed a clear preference for barnacle epigrowth over clean shells. Assuming that
settlement and recruitment are key processes for species abundances on the North Sea coast, it
is predicted that the positive feedback in oyster settlement will lead to rapid reef formation of
this invader at the expense of mussel beds. Mussels, however, may escape competitive
exclusion by settling between or on the larger oysters especially when barnacles are abundant.
Experimental patches with mussels were more often covered by fucoid algae (Fucus
vesiculosus forma mytili Nienburg) than patches with oysters, and oyster recruitment was poor
underneath such algal canopies. Thus, fucoids may provide mussels with a refuge from the
invading oysters and the two bivalves may coexist, provided food is not limiting.
Keywords
Crassostrea gigas, Settlement, Mytilus edulis, Introduced species, Niche partitioning, North
Sea
46
Chapter 3
1 Introduction
Invasive Pacific oysters (Crassostrea gigas) and resident mussels (Mytilus edulis) are both
gregarious epibenthic suspension feeders that colonise coastal soft-sediment environments in
the North Sea. Both species require living or dead shells as substrate for attachment when
settling on mudflats. This brings the invading oysters potentially into competition with the
native mussels. Recruitment patterns were investigated in order to explore whether overlap in
spatial niches is complete or whether some spatial partitioning and co-existence may be
expected.
Pacific oysters originate from Japan, and have been cultivated in the northern Wadden Sea
since 1986. The cultured oysters have reproduced naturally and are now firmly established in
the wild, still spreading in abundance and range (Reise 1998, Diederich et al. in press). Oyster
larvae attach mainly onto clean, hard surfaces with a slight unevenness or groove by releasing
a cement drop from a foot gland and placing the left valve into the cement (Korringa 1976,
Quayle 1988, Arakawa 1990a). The Wadden Sea, which is characterised by its extensive
intertidal mud and sand flats, lacks primary hard substrata for sessile organisms. Dikes,
groins, and especially beds of empty shells and mussel beds (Mytilus edulis) are the only
major secondary hard substrate available as attachment surface for oyster larvae. Some mussel
beds in the Wadden Sea are already heavily overgrown by Pacific oysters (Reise 1998,
Dankers et al. 2004).
Mussel beds consist of a three-dimensional matrix of connected living and dead mussels on an
organo-rich bottom sediment layer (Seed & Suchanek 1992). In the Wadden Sea, mussel beds
may persist over many decades (Reise et al. 1989, Obert & Michaelis 1991, Hertweck &
Liebezeit 2002). Besides fishing activities (Dankers & Zuidema 1995, Herlyn & Millat 2000),
ice scour (Bahr 1950, Obert & Michaelis 1991, Strasser et al. 2001) and storms (Nehls &
Thiel 1993) may severely damage or dislodge mussel beds. Regeneration of mussel beds is
facilitated by a high dispersal capability and site-specific and gregarious settlement of mussel
larvae (Seed 1969, Petersen 1984), the latter caused by the structure of the substratum
(Chipperfield 1953, Seed 1969, Menge 1976, Grant 1977), biofilms (Dobretsov & Railkin
1994) and chemical cues exuded from macroorganisms (Dobretsov & Wahl 2001) or as a
result of passive entanglement of mussel larvae in filamentous structures such as algae or
byssus threads (Caceres-Martinez et al. 1994).
Differential recruitment of introduced Pacific oysters and native mussels
47
Recruitment patterns can also be affected by epibionts already present on the settlement
surfaces. In the Wadden Sea, the most abundant epibiont species on mussels are the barnacles
Semibalanus balanoides (L.) and Balanus crenatus (Bruguière) (Albrecht & Reise 1994,
Buschbaum & Saier 2001). Barnacles can cover almost 100% of mussel surface area but
abundances show high interannual and seasonal fluctuations (Buschbaum 2000).
Nevertheless, the presence of barnacles increases mussel recruitment (Grant 1977, Saier
2001).
Another important structure on North Sea intertidal mussel beds is the brown alga Fucus
vesiculosus forma mytili (Nienburg) Nienhuis (Nienburg 1925, Nienhuis 1970, Albrecht &
Reise 1994, Albrecht 1998). This perennial seaweed can cover intertidal mussel beds either
partly or completely in a thick layer. In association with mussels, this brown alga lacks a
holdfast and gas vesicles and is fastened by the mussels’ byssal threads. Reproduction is
vegetative by means of drifting thalli that are “captured” by mussels and attached to the bed.
On intertidal mussel beds in the Wadden Sea, dense Fucus patches reduce current velocities
and enhance sedimentation (Albrecht & Reise 1994). This has a negative influence on
abundances of mussels and their epibionts, but supports various herbivores and increases
overall macrobenthic diversity (Albrecht & Reise 1994).
This complex mussel bed biocoenosis is now invaded by the Pacific oyster. The question
arose of whether the oysters may outcompete the local mussels by invading their niche, or
whether niche partitioning would allow coexistence of the two bivalves. In the Wadden Sea,
stable and mature mussel beds are confined to sheltered parts behind the islands, because
storms and ice shear readily destroy young mussel beds on more exposed locations (Nehls &
Thiel 1993, Dankers et al. 2001). Spatial displacement to less favourable habitats may
therefore lead to short-lived, young mussel beds and this may pose a threat to mussel
populations. Recruitment of introduced Pacific oysters and native mussels in different
microhabitats was studied in an attempt to predict the further development of the oyster and
mussel populations in the Wadden Sea. Thus, the focus of this study is not the settlement
process (largely defined as the larval search for a suitable substratum, attachment and finally
metamorphosis), but the combined effects of settlement and subsequent post-settlement
survival.
48
Chapter 3
2 Material and methods
2.1 Experimental sites
Field experiments were carried out at two locations: the List tidal basin in the northern
Wadden Sea (Germany) and the Oosterschelde estuary (The Netherlands). The List tidal
basin, which is located between the islands of Sylt and Rømø (54°50’ - 55°10’N and 08°20’ 08°40’E) covers an area of about 404 km² and is closed by dams to the north and south (Fig.
1). A tidal inlet of 2.8 km width is the only connection to the North Sea. This inlet branches
into three main channels (maximum depth 40.5 m) that are responsible for the current and
transport regimes within the bay. Intertidal flats, which are mostly sandy, comprise 33% (134
km²) of the total area (Backhaus et al. 1998). Tides are semidiurnal and the mean tidal range
is 2 m. The average salinity is close to 30 psu. Monthly mean water temperatures range from
18.2°C in August to 2.3°C in February. Detailed information on hydrography, geology,
sediments and biota of the bay is given in Gätje and Reise (1998). Within the List tidal basin,
intertidal mussel beds cover 1.5 km2 (Nehls 2003) and are partly covered by the brown
macroalgae Fucus vesiculosus forma mytili (Albrecht 1998). Investigations were carried out
on two mussel beds, one at the northern end of the bay in Königshafen (KH), and one close to
the southern end of the bight south east of Munkmarsch harbour (MM). Experiments took
place in the intertidal near the low water line and in the shallow subtidal. Sites referred to as
intertidal had an exposure time of about 2 h per tide and subtidal sites were located 0.5 - 1 m
below low water level.
One recruitment experiment was carried out in the Oosterschelde estuary (The Netherlands), a
tidal bay of 351 km² surface area which was partly closed from the sea by a storm-surge
barrier in 1987. Tidal flats cover 118 km² and mean tidal range is 3.3 m (Nienhuis & Smaal
1994). Here, Pacific oysters were introduced for cultivation in 1964 and first natural spatfalls
occurred in 1975 and 1976 (Drinkwaard 1999). From 1982 onwards abundances of wild C.
gigas increased strongly (Wolff & Reise 2002) and in 2002 the area covered with oysters
amounted to 640 ha in the intertidal and about 700 ha in the subtidal zone (Geurts van Kessel
et al. 2003). Wild mussel stocks do not exist in this area, but mussels are kept in subtidal
culture plots that comprise an area of about 3000 ha (Kater & Kesteloo 2003).
Differential recruitment of introduced Pacific oysters and native mussels
North
Sea
8°30‘
8°40‘
Sylt
49
Fig. 1 Location of experimental
sites: two in the List tidal basin (KH
and MM, asterisks) in the northern
Wadden Sea (Germany) and one in
the Oosterschelde (The Netherlands). Map of List tidal basin after
Bayerl et al. (1998)
Rømø
Oosterschelde
KH
55°
List tidal basin
MM
Sylt
N
5 km
2.2 Effect of tidal height on recruitment (C. gigas)
Recruitment of C. gigas was studied in the intertidal and adjacent shallow subtidal of KH and
MM in August 2002 and 2003 using shell collectors. Each shell collector was constructed
from 10 clean oyster shells that had a hole drilled in the middle so that they could be strung
on a plastic covered clothesline. These lines were 30 - 40 cm long and were pinned with iron
bars horizontally on the mussel beds so that the shells touched the mussels underneath. In
2002, collectors were installed in the field from 10 to 30 August and in 2003 from 30 July to15
September. This time frame was chosen because it covered the main settlement period and
also allowed conclusions to be drawn about early recruitment patterns. At the end of periods,
the strings were brought back to the laboratory and attached juvenile oysters were counted
with a stereomicroscope.
50
Chapter 3
2.3 Substrate specificity of recruitment near Sylt (C. gigas and M. edulis)
Experimental oyster and mussel plots were built next to a natural intertidal mussel bed (MM)
in July 2001. Oyster plots were created by collecting wild oysters from a nearby mussel bed,
removing any attached mussels, and placing the oysters in four 2 × 2 m plots. The oysters
were densely packed, resulting in a three-layered aggregation with a density of about 500
oysters m-2. Mussel plots were built by collecting M. edulis clumps from a nearby mussel bed
and placing them on four 2 × 2 m areas. Mussel density in these plots was about 3400 ind m-2.
These oyster and mussel plots were randomly distributed along the edge of an existing mussel
bed (distance from the bed 10 - 20 m) on sand covered with dead mussel shells. As the
mussels attached themselves with byssal threads and most of the oysters were large and heavy
individuals, they remained on the plots without the aid of a fence. Samples from these
experimental plots and from the nearby mussel bed were taken in November 2001 (initial
abundance of C. gigas and M. edulis in the plots), in October 2002 and May 2003. October
2002 was chosen as the first sampling date, because oyster spatfall in this area occurs during
late summer and by October juveniles are large enough to be counted with the naked eye
(about 2 - 20 mm shell length). Two sub-samples were taken from each of the four
experimental oyster plots by placing a 25 × 25 cm frame randomly in the area and removing
all living bivalves and dead shells. On mussel plots (two sub-samples taken from each of the
four plots) and on the mussel bed (eight samples taken in 2002 and twelve in 2003) samples
were taken using a 14.5 × 14.5 cm box corer instead of a frame. This corer could not be used
on the oyster plots, because some oysters were up to 20 cm long. All material inside the frame
or box corer was sieved with a 5 mm mesh sieve. In the laboratory, all mussels and oysters
were measured with electronic vernier callipers to the nearest 0.01 mm. Also dead shell
material was searched for attached juvenile oysters. Percent coverage of the experimental
plots with Fucus vesiculosus was estimated visually to the nearest 5% at all three sampling
dates.
In a similar way, experimental Crassostrea and Mytilus plots were constructed in the adjacent
shallow subtidal, but these plots were 1 × 1 m in size. The smaller size was necessary because
of the difficulties in transporting the bivalves over longer distances. This was considered
legitimate because not absolute recruitment but recruitment differences dependent on the type
of substrate were tested. Samples were taken in the same way as described for the intertidal
area in October 2003 during an extreme spring low tide when plots were exposed.
Differential recruitment of introduced Pacific oysters and native mussels
51
2.4 Substrate specificity of recruitment in the Oosterschelde (C. gigas)
This experiment was conducted on a tidal flat near Yerseke in August 2001. Four substrate
types for oyster settlement were placed on 35 × 50 cm plots (six replicates for each substrate)
that were randomly distributed in a 100 × 100 m area on an intertidal sand flat close to the low
water line. A fence 8 cm high and made of plastic-coated wire netting (mesh opening: 1 cm)
surrounded each plot and prevented the substrates being washed away. The following
substrates for oyster attachment were used: (1) living adult C. gigas (mean shell length: 103.2
± 9.4 mm), (2) dead C. gigas shells (mean shell length: 96.6 ± 10.6 mm), (3) living adult M.
edulis (mean shell length: 59.8 ± 2.5 mm), (4) dead M. edulis shells (mean shell length: 62.7 ±
2.6 mm). It was estimated visually that the plots contained the same volume of substrate
material, which was freed from epigrowth with an iron brush. Plots were installed in the field
on 2 August 2001 and settlement of oyster spat occurred from 9 August 2001 onwards. On 20
August 2001 the substrates were removed and brought to the laboratory. From each plot 8
items (i.e. oysters, mussels or dead shells) were randomly chosen and searched for oyster spat.
On living oysters and mussels a mean was calculated from left and right valve so that number
of spat per valve is given. On dead shells the outer and inner surfaces of shells were
investigated separately. In this way the amount of spat on the outer surface of dead shells
could be compared with the number of spat on the shells of living bivalves.
2.5 Effect of barnacle epigrowth on recruitment (C. gigas and M. edulis)
This experiment was conducted on an intertidal mussel bed (MM) in summer 2003. Four
substrate types for oyster attachment were tested: living adult C. gigas with and without a
dense barnacle cover and living adult M. edulis with and without barnacles (Table 1). These
substrates were placed separately in plastic mesh cages (cages open at the top; diameter: 10
cm; height: 8 cm; mesh opening: 5 mm; 16 replicates) that were fixed onto the mussel bed
with iron bars. This experiment was done twice, once for mussel recruitment (10 July - 18
August 2003) and once for oyster recruitment (29 July - 12 September 2003) because mussel
settlement occurred earlier in the year than oyster settlement. As mussel substrate two mussels
were used together in one cage whereas as oyster substrate only one oyster was used in order
to outbalance the size difference. Caged mussels and oysters were measured with vernier
callipers to the nearest millimetre and their volume was estimated by placing the content of
each cage (two mussels and one oyster respectively) in a calibrated cylinder to calculate the
52
Chapter 3
volume of water displaced upon submergence. At the end of experimental time all attached
juvenile oysters and mussels were counted with a stereomicroscope.
Table 1 Size of mussels and oysters used as substrate in the experiment on the effect of barnacle
cover on recruitment of Crassostrea gigas and Mytilus edulis. Length, width and height are mean
values for individuals, but volume data are based on cage content, i.e. two mussels and one oyster
respectively
Exp. 1 (Mussel recruitment)
M. edulis without barnacles
M. edulis with barnacles
C. gigas without barnacles
C. gigas with barnacles
Length
(mm)
Width
(mm)
59.6
57.3
89.2
92.4
26.4
27.8
59.4
59.9
Height Volume
(mm)
(ml)
26.1
30.2
38.6
45.1
39.3
52.3
71.9
106.9
Exp. 2 (Oyster recruitment)
Length
(mm)
Width
(mm)
58.9
60.5
100.3
101.2
27.
34.3
63.6
63.7
Height Volume
(mm)
(ml)
26.4
40.1
39.7
46.9
39.0
61.5
86.3
112.5
2.6 Effect of Fucus cover on recruitment (C. gigas)
Adult C. gigas (110 - 120 mm shell length) were collected from an intertidal mussel bed
(KH), cleaned from epigrowth with an iron brush, and placed as attachment surfaces for
oyster larvae back on the same mussel bed. Twenty oysters were placed on top of a dense
mussel layer with no Fucus overgrowth and another 20 oysters were placed on nearby mussel
bed patches with a dense Fucus cover. The algal thalli were carefully lifted and the oysters
were placed underneath. Oysters were marked individually with an iron bar that was labelled
and placed next to them. The experiment started on 5 August 2003 and ended 30 days later
when all oysters were brought back to the laboratory and searched for oyster spat.
2.7 Statistical analysis
Results are given as arithmetic means with standard error (SE). Data on abundance of
juveniles were subjected to analysis of variance (ANOVA) or to Repeated Measures ANOVA
if data sets contained two or three time periods. The Levene test was used to test for
homogeneity of variances and data were log (x + 1)- or square root-transformed if variances
were heterogeneous. Data on recruitment of M. edulis in relation to barnacle overgrowth were
subjected to non-parametric tests (Kruskal-Wallis-ANOVA followed by Mann-Whitney UTests) because of the heterogeneity of variances despite transformation. Effects were
considered to be statistically significant if p-value was < 0.05.
Differential recruitment of introduced Pacific oysters and native mussels
53
3 Results
3.1 Effect of tidal height on recruitment (C. gigas)
The abundance of Crassostrea gigas spat was significantly higher on intertidal shell collectors
than on subtidal ones (Fig. 2; Table 2). This pattern was consistent over sites (KH and MM)
Juvenile C. gigas / shell
and years (2002 and 2003).
4
Intertidal
Subtidal
3
2
Fig. 2 Effect of tidal height on recruitment
of Crassostrea gigas (mean ± 1 SE, n = 6)
on oyster shells placed on two mussel
beds (KH and MM) in intertidal and
subtidal locations during August 2002 and
2003
1
0
KH
MM
2002
KH
MM
2003
Table 2 Effect of tidal height, substrate and barnacle epigrowth on recruitment of Crassostrea
gigas. Results of Repeated Measures ANOVA (effect of tidal height and substrate) and ANOVA
(barnacle epigrowth)
Source of variation
Tidal height
Site
Tidal height
Site x tidal height
Error
Time
Time x site
Time x tidal height
Time x site x tidal height
Error
Substrate specificity intertidal:
Crassostrea plot, Mytilus plot, mussel bed
Substrate
Error
Time
Time x substrate
Error
Barnacle epigrowth
Substrate (C. gigas – M. edulis)
Barnacle cover (yes – no)
Substrate x barnacle cover
Error
SS
df
MS
F
p
11.14
25.16
0.53
6.83
4.46
3.77
0.24
0.10
8.79
1
1
1
19
1
1
1
1
19
11.14
25.16
0.53
0.36
4.46
3.77
0.24
0.10
0.46
31.00
70.04
1.49
0.000
0.000
0.238
9.64
8.16
0.52
0.23
0.006
0.010
0.479
0.641
366.33
168.90
651.88
39.26
223.35
2
8
1
2
8
183.16
21.11
651.88
19.63
27.92
8.68
0.010
23.35
0.70
0.001
0.523
0.69
0.06
0.36
2.38
1
1
1
51
0.69
0.06
0.36
0.05
14.68
1.24
7.71
0.000
0.270
0.008
54
Chapter 3
3.2 Substrate specificity of recruitment near Sylt (C. gigas and M. edulis)
Substrate (Crassostrea plots, Mytilus plots or mussel bed) significantly influenced
abundances of juvenile C. gigas in October 2002 and in May 2003 (Fig. 3; Table 2). In
October 2002, i.e. about 2 months after settlement took place, abundance of 0-group juvenile
oysters was about three times higher on intertidal Crassostrea plots (804.0 m-2) than on
Mytilus plots (231.9 m-2) and on the natural mussel bed (285.4 m-2). In May 2003 abundance
on all three substrate types was about 75% lower, indicating that winter mortality did not
differ between substrates (no substrate × time interaction). Recruited M. edulis (< 25 mm shell
length) were equally abundant on Crassostrea, Mytilus and mussel bed sites in October 2002
(ANOVA, F = 0.53, df = 9, p = 0.604, i.e. no significant difference between plots). In May
2003 densities were reduced by 50% on all three substrate types, again indicating mortality to
be independent of substrate.
Oct 02
May 03
800
600
400
200
0
1000
Juvenile M. edulis m-2
Juvenile C. gigas m-2
1000
Oct 02
May 03
800
600
400
200
0
Crassostrea
plot
Mytilus plot
Mussel bed
Crassostrea
plot
Mytilus plot
Mussel bed
Fig. 3 Substrate-specific recruitment in the intertidal. Mean abundance (± 1 SE) of Crassostrea gigas
(< 20 mm in October, < 33 mm in May) and Mytilus edulis (< 25 mm in October and May) on
experimental Crassostrea plots (4 m², n = 4), Mytilus plots (4 m², n = 4), and on control mussel bed
areas (n = 8; n = 12) in October 2002 and May 2003
In the subtidal (Fig. 4), recruitment of C. gigas was about twelve times higher on Crassostrea
than on Mytilus plots (ANOVA, F = 39.70, df = 6, p < 0.001) while mussel recruitment
showed no difference (ANOVA, F = 0.03, df = 6, p = 0.869).
Differential recruitment of introduced Pacific oysters and native mussels
250
Juvenile M. edulis m-2
Juvenile C. gigas m-2
80
55
60
40
20
0
200
150
100
50
0
Crassostrea plot
(Subtidal)
Mytilus plot
(Subtidal)
Crassostrea plot
(Subtidal)
Mytilus plot
(Subtidal)
Fig. 4 Substrate-specific recruitment in the subtidal. Mean abundance (± 1 SE, n = 4) of Crassostrea
gigas (< 20 mm) and Mytilus edulis (< 25 mm) on experimental Crassostrea plots (1 m²) and Mytilus
plots (1 m²) in October 2003
3.3 Substrate specificity of recruitment in the Oosterschelde (C. gigas)
Recruitment of C. gigas was much higher on living oysters (100.6 juveniles/shell valve) than
on living mussels (1.1 juveniles/shell valve; Fig. 5). Taking into account that oysters used as
substrate were about twice as long and wide as the mussels, the amount of spat on M. edulis
should be multiplied by 4 to balance for the size difference. In addition, the undulated,
grooved surface of oyster shells has a much higher surface area than the smooth mussel shells.
This difference is roughly estimated to be about threefold. Thus, in this experiment, shell
surface area of living oysters is considered to be 7 times higher than the shell area of mussels.
But as the amount of spat on oysters was 100 times higher than on mussels, there is still a
difference by an order of magnitude.
Fig. 5 Substrate-specific recruitment of
Crassostrea gigas on an intertidal area in
the Oosterschelde (The Netherlands).
Mean number (± 1 SE, n = 6) of spat per
shell valve of living bivalves and per outer
surface of dead shell valves
Number of recruits
120
100
80
60
40
20
0
C. gigas
alive
C. gigas
shell
M. edulis
alive
M. edulis
shell
Comparing oyster recruitment on living substrates and dead shells showed no difference
between living and dead oysters, whereas there was a significantly higher recruitment on dead
mussel shells than on living mussels (ANOVA, F = 40.62, df = 10, p < 0.001). Recruitment of
56
Chapter 3
C. gigas was significantly higher on the rougher outer surface of oyster shells than on the
smooth inner surface (ANOVA, F = 5.51, df = 20, p = 0.029).
3.4 Effect of barnacle epigrowth on recruitment (C. gigas and M. edulis)
C. gigas or M. edulis as substrates had a significant influence on oyster recruitment; it
explained 19.7% of the variance (Fig. 6; Table 2). Barnacle cover on the other hand had no
significant effect; however, the interaction between substrate species and barnacles was
significant, showing that barnacles had an effect on recruitment on the less favoured substrate,
M. edulis.
Mussel recruitment was strongly affected by the presence of barnacles (Kruskal-WallisANOVA, p < 0.001); significantly more recruits were found on oysters and mussels with
barnacle overgrowth than on those without barnacles (Mann-Whitney U-Test, p < 0.001 and p
= 0.005 respectively). Even though slightly more recruits were found on mussels than on
oysters, the difference was not significant. In summary, recruitment of oysters largely depends
on the type of substrate while mussel recruitment is influenced by the presence of barnacles.
3
Juvenile M. edulis / cage
Juvenile C. gigas / cage
10
8
6
4
2
0
clean
C. gigas
C. gigas with
barnacles
clean
M. edulis
M. edulis with
barnacles
2
1
0
clean
C. gigas
C. gigas with
barnacles
clean
M. edulis
M. edulis with
barnacles
Fig. 6 Effect of barnacle epigrowth on shells for recruitment of Crassostrea gigas (left) and Mytilus
edulis (right). Substrates were placed in open cages on a mussel bed near Munkmarsch; for C. gigas
recruitment from 29 July to 12 September 2003; for M. edulis recruitment from 10 July to 18 August
2003. Mean number of juveniles (± 1 SE, n = 16) per cage (each cage containing 1 C. gigas or 2 M.
edulis)
3.5 Effect of Fucus cover on recruitment (C. gigas)
Recruitment of C. gigas was significantly reduced underneath Fucus cover (ANOVA, df = 32,
F = 42.46, p < 0.001). On Fucus-free adult oysters about 4 times more juvenile C. gigas (7.6 ±
1.0) were found than on Fucus-covered oysters (1.7 ± 0.4).
Differential recruitment of introduced Pacific oysters and native mussels
57
3.6 Fucus coverage on Crassostrea and Mytilus plots
Fucus cover varied during the investigation period but was always higher on experimental
Mytilus plots than on Crassostrea plots (Fig. 7; Table 3). Repeated Measures ANOVA
revealed significant effects of substrate, time and interaction of substrate and time; however,
substrate explained 45% of the variance, compared to a lower time (16%) and interaction
(15%) effect.
Fucus cover (%)
100
80
Fig. 7 Variability of Fucus cover (% ± 1
SE, n = 4) on experimental intertidal
Crassostrea plots (4 m²) and Mytilus plots
(4 m²) in November 2001, May 2002 and
October 2002
Crassostrea plot
Mytilus plot
60
40
20
0
Nov 01
May 02
Oct 02
Table 3 Repeated Measures ANOVA on effect of substrate
(experimental Crassostrea and Mytilus plots) on Fucus cover.
Source of variation
SS
Fucus cover
Substrate
Error
Time
Time x substrate
Error
7350.00
2766.67
2533.33
2500.00
1183.33
df
MS
1 7350.00
6 461.11
2 1266.67
2 1250.00
12
98.61
F
p
15.94
0.007
12.85
12.68
0.001
0.001
4 Discussion
This study showed differences and similarities in recruitment patterns of introduced oysters
and native mussels that may lead to niche separation and coexistence of the two species (Fig.
8). Recruitment of C. gigas and M. edulis occurred mainly in the intertidal zone (this study
and Buschbaum, unpubl. data). While oyster recruitment was highest on conspecifics, mussels
showed no preference for either oyster or mussel substrate. Barnacles, the most abundant
fouling organisms on both mussel and oyster shells, had a positive influence on mussel but
58
Chapter 3
not on oyster recruitment. Fucus vesiculosus, which can cover mussel beds with a dense
canopy, led to reduced abundances of juvenile oysters (this study) and mussels (Buschbaum,
unpubl. data). Recruitment patterns in relation to the different factors are discussed in the
corresponding order.
Fig. 8 Differential recruitment patterns of Crassostrea gigas and Mytilus edulis on intertidal
and subtidal habitats and in relation to Fucus and barnacle cover as revealed by experiments
in the northern Wadden Sea. Arrows indicate high (thick arrow), medium (thin arrow) or low
(dotted arrow) recruitment of oysters and mussels. Some arrows for mussels are based on
Buschbaum, unpubl. data
4.1 Tidal height
Crassostrea gigas has been described as an intertidal species that only occasionally occurs in
subtidal locations (Buroker 1985). Presumably, this is due to reduced recruitment success
because of sediment deposition on the settlement surfaces (MacKenzie 1970, Keck et al.
1973, Rothschild et al. 1994) or water temperatures being too low for larval or spat survival in
the subtidal zone (Quayle 1988). Also high current velocities could lead to oyster larvae
having difficulties in attaching to the substrate (Arakawa 1990b). In this study recruitment of
C. gigas was significantly higher on shell collectors in the intertidal than in the adjacent
shallow subtidal zone. Even though deposition of sediment on the settlement surfaces was
higher in the subtidal compared to the intertidal zone, on average only 10 - 20% of the surface
Differential recruitment of introduced Pacific oysters and native mussels
59
area was covered with sediment. As the temperature difference between surface water and
deep water in the gullies is very small (less than 1°C; van Beusekom, pers. comm., 2004),
water temperature is not a very likely reason for the lower recruitment in the subtidal zone.
High current velocities might be a cause of lower oyster abundances in the subtidal, but C.
gigas has settled successfully in tidal gullies with relatively high current speeds in the Dutch
Wadden Sea near Texel (Dankers, pers. comm., 2004). However, a comparison of the
performance of C. gigas in the Dutch and northern German Wadden Sea should take into
account that the oysters originate from different introductions. The oysters in the Dutch
Wadden Sea most likely originate from the Oosterschelde (Bruins 1983) whereas the oysters
in the northern German Wadden Sea sprang from an oyster culture near Sylt (Reise 1998).
Therefore, the populations could be genetically different. Another aspect could be higher
early post-settlement mortality due to predation in the subitdal zone: when shell collectors
were protected with mesh cover, recruitment of juveniles was similar on intertidal and
subtidal habitats (own unpubl. data).
Mytilus edulis is widespread from high intertidal to subtidal locations because it withstands
high fluctuations of salinity, desiccation, temperature and oxygen tension (Seed & Suchanek
1992). In the subtidal, however, it is limited by high predation pressure and competition
(Ebling et al. 1964, Kitching & Ebling 1967, Paine 1974). In the study area, M. edulis
recruitment in the subtidal also seems to be limited by predation (Buschbaum, unpubl. data;
Saier 2001). Thus, both oyster and mussel recruits may find a refuge from predation in the
intertidal.
4.2 Substrate specificity
Recruitment of C. gigas was higher on conspecifics than on mussels. Oyster larvae tend to
settle gregariously triggered by adult conspecifics (Bayne 1969, Keck et al. 1971, Hidu et al.
1978). The preference of oyster larvae for rough surfaces has been described before (Korringa
1976, Quayle 1988) and has been confirmed in this study, because the smooth mussel shells
caught much less oyster spat than the rough oyster shells and also the smooth inner surface of
the oyster shells received fewer recruits than the rougher outer surface. Protection from
predation in the shell crevices is considered to be a reason for high recruitment success on
rough shells (O’Beirn et al. 2000). The higher recruitment of oysters on conspecifics than on
mussels suggests that the oysters will aggregate and that the more oysters are present, the
more recruits are to be expected on these aggregations in future years. This positive feedback
60
Chapter 3
may soon generate compact oyster reefs like the ones already present in the Dutch Wadden
Sea near Texel (Dankers et al. 2004).
Mussel recruits were equally abundant on Crassostrea, Mytilus and mussel bed plots and
suffered the same winter mortality of about 50% on all three sites. This contradicts other
findings of gregarious behaviour of mussels and the avoidance of competition due to siteselective settlement (Suchanek 1981, Petersen 1984). Irregular, grooved and rough surfaces
have also been described to be especially suited for mussel settlement (Chipperfield 1953,
Seed 1969, Menge 1976, Grant 1977) and mussel fouling on oyster cultures is a common
phenomenon (Quayle 1988, Arakawa 1990b). Therefore the oyster shell is likely to be a good
settling substrate for mussels, which may even provide protection from predation in the
crevices of the shell.
4.3 Barnacle epigrowth
Barnacles had little influence on oyster recruitment: only on the less favoured mussel
substrate did barnacle cover increase oyster spat abundance. Presumably the rougher surface
structure due to the barnacle shells enhanced settlement and early post-settlement survival of
juvenile oysters. A similar effect was observed for C. virginica (Osman et al. 1989). On the
other hand, there may also be space and/or food competition between oysters and barnacles
(MacKenzie 1970, Abbe 1986, Arakawa 1990b) that could lead to differential settlement and
horizontal zonation (Bushek 1988). In this study, recruitment was measured after about one
month, and hence did not include post-settlement events over a longer period of time. For
example, oysters settling on barnacles instead of on living bivalves may have a greater risk of
dislodgement, because the barnacles may fall off the substrate as the oyster grows. The
juvenile oyster could then easily be washed away to unfavourable habitats. Juvenile oysters
attached to the remains of dead barnacles were indeed frequently found scattered on the tidal
flats in the study area (own obs.). On the other hand, this may as well be regarded as a way of
dispersal and may give rise to oyster reefs outside the mussel beds. In turn, massive
settlement of barnacles on juvenile C. gigas was not observed, while adult oysters may be as
heavily overgrown as mussels (own obs. and Görlitz, pers. comm., 2004). The reason for this
might be the smoother shell surface of juvenile compared to adult oysters, because barnacles
settle gregariously and preferentially on surfaces with cracks, crevices and pits (Chabot &
Bourget 1988, Berntsson et al. 2004).
Differential recruitment of introduced Pacific oysters and native mussels
61
In contrast to the effects on oysters, barnacles strongly increased mussel recruitment,
regardless of whether the barnacles were attached to oyster or mussel shells. This is attributed
to protection from predation and from unfavourable environmental conditions such as
desiccation and heat (Seed 1969, Navarette & Castilla 1990, Barnes 2000, Saier 2001). It can
be concluded that barnacles may have an influence on the further development of mussel beds
and oyster reefs in the area.
4.4 Fucus cover
The presence of Fucus vesiculosus on intertidal mussel beds reduced recruitment of C. gigas.
This corresponds with lower overall oyster abundances on Fucus-covered mussel bed patches
compared to Fucus-free areas (Reise 1998, own unpubl. data). Densities of juvenile mussels
are also reduced underneath Fucus cover (Buschbaum, unpubl. data). Total mussel biomass,
however, is only slightly lower and more persistent on Fucus-covered mussel bed areas
compared to Fucus-free patches, which leads to the conclusion that Fucus cover is not a major
factor for mussel bed dynamics (Nehls 2003). It is important to note that Fucus on mussel
beds lacks a holdfast and is attached to the mussel bed only by the byssus threads of the
mussels. This is the reason why oyster reefs will not be overgrown by Fucus, while mussel
beds can be almost completely covered (Nehls 2003). The Fucus cover varies considerably
over time, but some mussel bed areas are more often covered than others (Nehls 2003). These
densely covered mussel beds will catch less oyster spat than bare ones resulting in a very slow
increase in oyster abundance. Thus, oyster recruits will accumulate in areas free of Fucus
overgrowth where abundances of adult oysters are already high. Once the proportion of
mussels and oysters is in favour of oysters, these areas may stay free from Fucus overgrowth
and attract still more oyster spat. However, during years with high mussel recruitment, the
mussels may settle on top of the oysters and subsequently Fucus overgrowth could occur.
Thus, fucoids may give rise to a mosaic of oysters and mussels, which may show patch
dynamics as recruitment of the two species as well as of Fucus varies over the years.
5 Conclusion
The further development of the oyster population in the Wadden Sea and especially the spatial
distribution on existing mussel beds will depend on recruitment success in different habitats.
62
Chapter 3
Oyster reproduction in the northern Wadden Sea is confined to a short period in summer (July
to September) when spawning and settlement occurs. Recruitment success depends on high
water temperatures during this time and is therefore erratic: it occurred only in 6 out of 18
years since the first introduction of C. gigas in this area (Diederich et al. in press). Mussel
spawning and settlement, on the other hand, is extended and occurs throughout the year with
peaks in early summer and autumn (Pulfrich 1996). Strong year classes that lead to a
rejuvenation of mussel beds, however, are rare and usually follow severe winters (Beukema
1992, Beukema et al. 2001, Strasser et al. 2001). In the study area, the last mass recruitment
event occurred in 1996 (Nehls 2003) when oysters were still rare. Temperature may thus play
a key role in determining the balance between the two bivalves: hot summers will favour
oyster reproduction, while cold winters will lead to high mussel recruitment in the following
summer.
The experiments revealed sufficient differences in settlement and/or recruitment patterns
between oysters and mussels to predict that both species are likely to co-occur in mixed and
mosaic beds, provided other processes such as food competition do not overrule the studied
fine-scale performance with regard to substrate.
Acknowledgements
I am very grateful to Pauline Kamermans and colleagues from the Netherlands Institute for
Fisheries Research (RIVO, Centre for Shellfish Research, Yerseke) for their generous help. I
thank Werner Armonies, Karsten Reise, Norbert Dankers and one anonymous referee for their
valuable comments on the manuscript. Dina Schmidt, David Thieltges, Catharina Claus, Bodo
Schiwy, Kristin Scheuer, Stefan Görlitz and Jae-Sang Hong (Inha University, Korea) helped
in conducting the experiments in the field and laboratory.
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High survival and growth rates of introduced Pacific oysters
67
Chapter 4
High survival and growth rates of introduced Pacific oysters may
facilitate displacement of native mussels in the Wadden Sea
Abstract
Pacific oysters (Crassostrea gigas Thunberg 1793) were introduced to the northern Wadden
Sea (North Sea, Germany) by aquaculture in 1986 and finally became established. Even
though at first recruitment success was rare, three consecutive warm summers led to a
massive increase in oyster abundances and to the overgrowth of native mussel beds (Mytilus
edulis L.). These mussels constitute biogenic reefs on the sand and mud flats in this area.
Survival and growth of the invading C. gigas were investigated and compared with the
resident mussels in order to predict the further development of the oyster population and the
scope of coexistence for both species. Field experiments revealed a high survival of juvenile
C. gigas (approximately 70%) during the first three months after settlement. Survival during
the first winter varied between > 90% during a mild and 25% during a cold winter and was
independent of substrate (i.e. mussels or oysters) and tide level. Within their first year C.
gigas reached a mean length of 35 - 53 mm, and within two years grew to 68 - 82 mm, which
is about twice the size native mussels would attain during that time. Growth of juvenile
oysters was not affected by substrate (i.e. sand, mussels, other oysters), barnacle epigrowth
and tide level, but was facilitated by fucoid algae. By contrast, growth of juvenile mussels
was significantly higher on sand flats than on mussel or oyster beds and higher in the subtidal
compared to intertidal locations. Cover with fucoid algae increased mussel growth but
decreased their condition expressed as dry flesh weight versus shell weight. High survival and
growth rates may compensate for years with low recruitment, and may give C. gigas a
competitive advantage that may lead to the permanent displacement of native mussels to less
favourable habitats.
Keywords
Crassostrea gigas, Growth, Introduced species, Mussel bed, Mytilus edulis, Survival, Wadden
Sea
68
Chapter 4
1 Introduction
The accidental or deliberate release of ‘exotic’ (non-native) species into new habitats by
shipping and aquaculture activities is an increasing phenomenon in coastal ecosystems all
over the world (Carlton & Geller 1993, Reise et al. 1999, Ruiz et al. 2000, Naylor et al. 2001).
Most introductions fail to produce self-sustaining populations or develop only a limited
population growth (Williamson & Fitter 1996). Nevertheless, there are numerous examples of
invasive exotics that profoundly changed the recipient ecosystem (Nichols et al. 1990,
Grosholz & Ruiz 1996, Kideys 2002). The Pacific or Japanese oyster (Crassostrea gigas) is
an example of an invasive species that has been introduced to various coastal areas through
aquaculture activities and subsequently established in the wild (Andrews 1980, Chew 1990).
Examples include introduced oyster populations in British Columbia (Quayle 1988),
California (Span 1978), South Africa (C. Griffith, pers. comm.), Australia (Ayres 1991), New
Zealand (Dinamani 1991), France (Grizel & Héral 1991), The Netherlands (Drinkwaard
1999), and Germany (Reise 1998).
Recently a dramatic increase in oyster abundances has been observed in the Dutch and
German Wadden Sea (Dankers et al. 2004, Diederich et al. in press). As this area is
characterised by extensive intertidal mud and sand flats, it lacks primary hard substrata for
oyster settlement. However, epibenthic mussel beds (Mytilus edulis) and dead shell material
provide secondary hard substrata, which the oysters use as settlement surfaces. In the German
Wadden Sea, oysters are therefore mainly found as epibionts on intertidal mussel beds and are
at present turning some mussel beds into oyster reefs (Diederich et al. in press). Since mussel
beds take a prominent position in the Wadden Sea and generally constitute hot spots with
respect to productivity and filtering-capacity (Asmus 1987, Asmus et al. 1992, Dankers &
Zuidema 1995), biodiversity (Riesen & Reise 1982, Tsuchiya & Nishihira 1986, Dittmann
1990), and as a food resource for various crustaceans, fish, birds and man (Seed & Suchanek
1992, Nehls et al. 1997, Saier 2001), their overgrowth or possible displacement by oysters
might profoundly change the entire ecosystem. Up to now, recruitment of C. gigas in the
northern Wadden Sea was sporadic depending on years with high summer water temperatures.
However, three consecutive warm summers (2001-2003) and a positive feedback of adult
oysters on recruitment of juveniles, strongly increased oyster abundance and expansion of the
population (Diederich in press, Diederich et al. in press). Thus, abundance may be high
enough, by now, to ensure some recruitment even during ‘cool’ summers. Provided these
High survival and growth rates of introduced Pacific oysters
69
recruits suffer a low mortality and adults achieve high longevity, this might guarantee
population persistence and facilitate a further increase in the Wadden Sea. As a consequence,
oysters might permanently restrict the local mussels to less favourable habitats, especially if
they show higher growth and survival rates than the natives. However, no information is
available on survival and growth of C. gigas in the Wadden Sea. The present study aims to fill
that gap and attempts to find out whether oyster reefs may be regarded as a temporary
phenomenon or are likely to be habitat structures superseding mussel beds in the Wadden Sea.
Generally, survival or mortality of benthic bivalves is described as a change in abundance of
individuals or year classes present in a population over some period of time. In addition to
physical stress, competition and desease, predation is often a major cause of natural mortality
in bivalves (Walne & Davies 1977, Reise 1985, McGrorty et al. 1990, Strasser 2002). As
predation is especially effective on juveniles and under conditions of extended submersion,
survival largely depends on size and tide level (Theisen 1968, Seed 1969, 1993). Fast growing
species may rapidly outgrow predation pressure. Therefore, it is assumed that Pacific oysters,
which grow to about 30 cm in their native habitat as well as in the Dutch Wadden Sea
(Korringa 1976, Dankers et al. 2004) might have an advantage over the much smaller native
mussels (Mytilus edulis), which attain a maximum size of about 7 cm in the northern Wadden
Sea (Nehls 2003). The growth rates of both, mussels and oysters may depend on various
factors, including tidal exposure (Quayle 1988, Buschbaum & Saier 2001), interspecific
competition (Bertness & Grosholz 1985, Okamura 1986), and epibionts on the shells like
algae or barnacles (Arakawa 1990, Dittman & Robles 1991, Buschbaum & Saier 2001).
In the study at hand, survival of C. gigas and growth of both, C. gigas and M. edulis, were
investigated in relation to tide level, substrate, barnacle epigrowth and algal cover, in order to
assess whether habitat requirements are the same or whether there might be species specific
refuges from potential competition. Information on mussel survival and growth rates was
taken from literature but for a comparison of growth performance in different microhabitats
oyster and mussel growth was investigated simultaneously.
70
Chapter 4
2 Material and Methods
2.1 Study area
The study was conducted in the List tidal basin in the northern Wadden Sea (North Sea,
Germany, 54°50’ - 55°10’N and 08°20’ - 08°40’E). This basin (404 km² area) is surrounded
by the mainland and by two islands (Sylt and Rømø) that are connected to the mainland by
dams (Fig. 1).
8°30‘
8°40‘
North
Sea
Fig. 1 Study area in the northern
Wadden Sea (Germany) and
location of experimental sites (KH
and MM, asterisks). Shaded areas
indicate intertidal sediment flats
Rømø
KH
55°
List tidal basin
MM
N
Sylt
5 km
A narrow tidal inlet of 2.8 km in width is the only connection to the North Sea. This inlet
branches out into three main water channels (maximum depth 40.5 m; maximum current
velocity 1.2 m s-1), which govern the current and transport regimes within the lagoon.
Intertidal flats, which are mostly sandy, comprise 33% (134 km²) of the total area. Tides are
semidiurnal and the mean tidal range is 2 m; the average salinity is close to 30 psu. Monthly
High survival and growth rates of introduced Pacific oysters
71
mean water temperatures range from 18.2°C in August to 2.3°C in February. Primary
production is about 300 g C m-2 year-1. Detailed information on hydrography, geology,
sediments and biota of the bay is given in Gätje and Reise (1998). Within the List tidal basin,
natural intertidal mussel beds cover about 1.5 km2 (Nehls 2003) and are partly covered by the
brown macroalgae Fucus vesiculosus forma mytili (Nienburg) Nienhuis. Some of these
mussel beds extend into the shallow subtidal zone. A commercial oyster farm has been in
operation in this basin since 1986 and produces about 2 million oysters per annum.
Experiments were carried out in Königshafen (KH), a tidal bay at the northern end of the
island of Sylt, and in Munkmarsch (MM) approximately 15 km further south.
2.2 Survival of C. gigas
Survival of C. gigas was investigated via three experiments on different time scales (during
the first three months, the first winter, and the first year after settlement) and in relation to tide
level (intertidal and subtidal) and substrate (mussel and oyster bed).
To quantify the survival of early recruits on an intertidal mussel bed during the first three
months after settlement, six unglazed ceramic tiles (29 × 29 cm) were fixed on mussel bed
MM on 16 August 2002 as settlement surfaces for oyster larvae. Settlement onto the tiles
followed shortly thereafter with the main settlement period ending at the end of August, but
light settlement occurring until late September. As the tiles had an imprinted grid, the position
of each attached oyster could be exactly determined. The survival of juveniles was calculated
from the difference in numbers of oysters that were present at the first examination on 29
August and the subsequent sampling dates. Sampling occurred seven times in irregular
intervals until 26 November 2002.
To investigate the survival of oysters during their first year after settlement in relation to tide
level, I counted numbers of juveniles that were attached to shell collectors placed on two
mussel beds (KH and MM), at each site on intertidal and subtidal locations. Each collector
was made from 30 clean (i.e. with no epibionts), dead oyster shells (mean shell length ± SD:
101.0 ± 14.1 mm) that had a hole drilled in the middle so that they could be strung on a plastic
covered clothesline. These lines were about 1m long and were pinned with iron bars
horizontally on the mussel bed so that the shells touched the mussels underneath. The
collectors (6 at each location) were deployed in the field on 9 and 10 August 2002. Settlement
occurred shortly thereafter and the number and length (largest diameter of the shell) of
juveniles on the shell surfaces was recorded first on 29 and 30 August 2002 by removing 10
72
Chapter 4
oyster shells from the clothesline and searching them for oyster spat with a stereomicroscope
in the laboratory. On 27 and 28 November another 10 shells were removed from the string
and searched for living oyster spat. On 21 February and 4 March 2003 the remaining 10 shells
were returned to the laboratory and juvenile oysters were counted and measured.
The latter set of shells were kept in an indoor tank with continuous seawater flow for 1 to 2
days and then brought back to the field and installed on the same spot on the mussel beds to
follow their survival for another few months. On 7 and 16 May 2003 and finally on 7 and 10
July 2003 the oyster shells were again returned to the laboratory and the attached juveniles
were counted and measured. As significant settlement on the collectors exposed on site MM
occurred later than 29 August 2002, the numbers of juveniles present in November 2002 were
taken as starting value for mortality quantification, because there was no more settlement after
that date.
Two calculations were made: survival of juveniles from November 2002 to February 2003 to
determine survival over winter, and survival during the “first year” after settlement, that is
from November 2002 to July 2003. As the collectors on the subtidal MM site were lost before
the end of the experiment, the comparison of abundances from November 2002 with July
2003 could only be done for intertidal locations. 2-factor (site and tide level) analysis of
covariance was used to compare abundances of juveniles in November 2002 and February
2003. The percentage survival at the different sites and tide levels was analysed using 2-factor
(site and tide level) analysis of variance. Abundance data were log(x+1) transformed and
percentages were arcsine square-root transformed to achieve homogeneity of variances
(Levene test).
To quantify the dependence of survival on substrate quality, survival of juvenile C. gigas was
analysed during two consecutive winters on experimental intertidal Crassostrea plots, Mytilus
plots and on a nearby natural mussel bed (MM). Experimental Crassostrea and Mytilus plots
(n = 4) were randomly distributed along the edge of a mussel bed (MM) on sand covered with
dead mussel shells in July 2001. ‘Oyster plots’ were created by collecting live wild oysters
from the nearby mussel bed, removing all attached mussels, and placing the oysters on four 2
× 2 m plots. The oysters were densely packed, resulting in a three-layered aggregation with a
density of about 500 oysters m-2. ‘Mussel plots’ were constructed by collecting live M. edulis
clumps with no attached oysters from the adjoining mussel bed and placing them on four 2 ×
2 m areas. Mussel density on these plots was about 3400 m-2.
High survival and growth rates of introduced Pacific oysters
73
Samples were taken on each of the plots and on the adjoining mussel bed in November 2001,
May 2002, October 2002 and May 2003. Two sub-samples were taken from each of the four
experimental oyster plots by randomly placing a 25 × 25 cm frame on the plot area and
removing all living bivalves and dead shells underneath. On mussel plots (two sub-samples
taken from each of the four plots) and on the natural mussel bed (eight samples taken in 2002
and twelve in 2003) samples were collected using a 14.5 × 14.5 cm box corer instead of a
frame. The different sampling devices were used because of substantial size differences
between oysters that were forming solid aggregations often exceeding 15 cm in diameter and
the much smaller mussels. Therefore, the corer could not be used for oysters and the frame
would have been too time-consuming to use for mussel sampling. All material inside the
frame or box corer was sieved over a 5 mm mesh sieve. In the laboratory, all mussels and
oysters were measured with electronic vernier callipers to the nearest 0.01 mm. Dead shell
material was searched for attached juvenile oysters as well. Oysters were considered as 0group juveniles if their shell length was < 20 mm in the fall samples and < 33 mm in the
spring samples. These size cutoffs were chosen after an analysis of length-frequency data.
Numbers of juveniles in November 2001 were compared with numbers in the following
spring (May 2002) using a non-parametric test (Kruskal-Wallis ANOVA) because of
heterogeneity of variances despite transformation. Abundances in October 2002 and May
2003 were compared using Repeated Measures ANOVA.
2.3 Size and growth of C. gigas
Length frequency data of C. gigas were obtained at two mussel beds (KH and MM) by
measuring the shell length (largest diameter) of randomly encountered oysters (n = 68 - 307
for each sampling) with vernier callipers to the nearest millimetre (see Diederich et al. in
press). Sampling was conducted in 1999 (April/May and September/October), 2001 (April
and November), 2002 (April and October), 2003 (May and August), and 2004 (April/May and
September). The mean length of cohorts was determined by using Bhattacharya’s Method
(1967) with the program FISAT II (Version 1.1.2, FAO-ICLARM Fish Assessment Tools). A
von Bertalanffy growth function was established using electronic length-frequency analysis
(ELEFAN; Gayanilo et al. 1989, Pauly & David 1981) to calculate growth parameters. As
larger animals were poorly represented, the parameter L∞ was not determined iteratively, but
set to 180 mm according to the maximum length observed during this survey. As the oysters
did not grow during winter in this area (approximately November to February; own
74
Chapter 4
unpublished data and Fig. 6), the winter point was set to WP = 1. The calculation was run
with the starting point May 2003 for KH and May 2004 for MM, because of clearly defined
cohorts in these data sets. To verify these calculations I used the growth of 0-group juvenile
C. gigas that were attached to shell collectors described above.
2.4 Growth experiments with C. gigas and M. edulis
2.4.1 Substrate and tide level
A field experiment was carried out to investigate growth of juvenile C. gigas and M. edulis in
relation to substrate (sand flat, mussel bed, and oyster reef) and tide level. It is important to
note that this experiment was not designed to investigate differences in absolute growth
between oysters and mussels, but to find out how oysters and mussels perform in different
habitats. Therefore it was not essential to use oysters and mussels of the same age. Juvenile
oysters (mean shell length ± SD: 27.7 ± 1.0 mm) and mussels (mean shell length ± SD: 30.4 ±
1.8 mm) were collected from mussel bed MM in April 2002 and cleaned from all epigrowth
with an iron scraper and brush. Only oysters that were attached to dead shell material were
used to avoid possible interactions between basibiont and epibiont. The shell length (largest
diameter) of each oyster and mussel was measured with vernier callipers to the nearest
millimetre. Afterwards the oysters and mussels were placed separately (that is one bivalve per
cage) in cylindrical cages made from plastic covered wire netting (∅ 5 - 6 cm, length 8 - 9
cm, mesh opening 11 mm). 280 cages (20 containing oysters and 20 containing mussels for
each of 7 locations) were installed in the field in May and June 2002 by fixing each cage with
an iron bar to the ground. Seven different locations were chosen: (1) intertidal sand flat
(northern Sylt), (2) shallow subtidal sand (northern Sylt), (3) intertidal mussel bed (KH), (4)
subtidal mussel bed (KH), (5) intertidal mussel bed (MM), (6) experimental intertidal
Crassostrea plot (MM), (7) experimental intertidal Mytilus plot (MM). Subtidal habitats are
referred to as areas remaining submerged during spring low tides and comprise depths of
about 1 m at mean low tide. Intertidal sites had a mean exposure time of 2 - 3 hours per tide.
Experimental Crassostrea and Mytilus plots (n = 4) were built next to a natural mussel bed
(MM) in July 2001 (see above). The cages were randomly distributed on these plots but only
on areas without Fucus cover. The length of each individual oyster and mussel was measured
in the field in June, July, August, September and November 2002. Unfortunately, the cages at
the subtidal sand flat location were lost after August 2002. Daily growth rates were calculated
for a two months (49 - 64 days) period from June to August 2002 for all seven locations. The
High survival and growth rates of introduced Pacific oysters
75
daily growth rates on the 5 intertidal locations were compared using analysis of variance
(ANOVA). In a separate ANOVA the effect of tidal height was analysed for the sand flat and
mussel bed (KH) locations. Tukey’s HSD test for unbalanced data sets was used to compare
single sites. All data were square root transformed to obtain homogeneity of variances
(Levene test). Effects were considered to be statistically significant if p-value was < 0.05.
2.4.2 Fucus cover
A second set of field experiments was designed to study the effect of a dense fucoid cover on
intertidal mussel beds with respect to growth and condition of juvenile C. gigas and M. edulis.
This experiment was conducted three times, each time using a different intertidal mussel bed
in “Königshafen” in the north of Sylt: KH I (30 May to 28 August 1999), KH II (23 July to 20
September 1999), KH III (3 May to 8 August 2001). For each experimental site 40 juvenile
oysters (mean shell length ± SD: KH I: 51.3 ± 5.7 mm; KH II: 45.8 ± 2.8 mm; KH III: 40.6 ±
5.6 mm) were collected a few days prior to the experiments on intertidal mussel beds and
cleaned from all epigrowth with an iron scraper and brush. Only oysters attached to dead shell
material were used. Shell length and at site KH I also shell width of oysters was measured
with vernier callipers to the nearest millimetre and all oysters were marked individually. For
experiments KH I and KH II oysters were marked with bee numbers (2 mm in diameter) that
were glued to the upper shell valve. For experiment KH III the oysters were placed separately
in pouches made from plastic covered wire netting (240 × 180 mm; mesh opening 10 mm).
After marking the oysters, they were brought to the respective mussel beds. On each mussel
bed 20 oysters were placed on fucoid-free patches and 20 oysters on patches with a dense
Fucus canopy. In experiments KH I and KH II the oysters were placed between the byssus
threads of the mussels to prevent them from getting washed away. On algal covered areas the
oysters were placed between the mussels underneath the Fucus thalli. In experiment KH III
the cages were fixed to the mussel bed with iron bars. Over the following 2 - 3 months, fucoid
algae were removed several times from Fucus-free patches as necessary. At the end of this
period, the oysters were collected and length increment (on site KH I also width increment)
was measured in the laboratory. On location KH III also the growth of juvenile M. edulis was
investigated. Mussels (mean initial shell length ± SD: 36.5 ± 2.4 mm) were treated the same
way as described above for C. gigas.
To test whether the fucoid cover had an effect on the condition of C. gigas and M. edulis, the
condition index (CI) of the oysters and mussels was determined in experiment KH III. The
76
Chapter 4
condition index used here is among the most accurate ones that involve easily measured
parameters (Davenport & Chen 1987): CI = Dry meat weight / Dry shell weight × 100. For
dry weight determination, the oysters and mussels were stored in a deep freezer at –20°C for
several days. Then the bivalves were cooked in seawater for 4 minutes. Afterwards meat and
shell of the individuals were separated and dried to constant weight at 80°C (6-7 days). After
cooling in a desiccator, meat and shell were weighed on a torsion balance (± 0.01 g). Data on
growth and condition were subjected to ANOVA (see above).
2.4.3 Barnacle epigrowth
The effect of barnacle cover on the growth of juvenile and adult oysters was experimentally
tested during the growing season of 2003. 32 juvenile oysters (mean shell length ± SD: 20.25
± 3.96 mm) and 32 adult oysters (mean shell length ± SD: 50.32 ± 12.72 mm) which were
attached to living mussels were collected on mussel bed MM on 30 May 2003. 16 juvenile
and 16 adult oysters with their attached mussels were cleaned from barnacles with an iron
scraper and brush, whereas the other oysters with attached mussels were not cleaned and >
50% of their shell surfaces were covered with barnacles. The shell length of the oysters was
measured with electronic vernier callipers to the nearest 0.01 mm and afterwards the oysters
were placed separately in cages made from plastic covered wire netting (mesh opening 11
mm). The cages were fixed with iron bars on an intertidal mussel bed (KH) on 1 June 2003.
On 8 October 2003 the cages were returned to the laboratory and all oysters were measured
again. The growth of the oysters was determined by subtracting the initial length of each
oyster from the final length and data were analysed using ANOVA.
3 Results
3.1 Survival of C. gigas
On 29 August 2002 there were 11.0 ± 2.2 (mean ± SE) juvenile oysters attached to the tiles
that had been fixed on an intertidal mussel bed. From these 70.0% survived their first three
months until 26 November 2002 (Fig. 2). The decrease in abundance was estimated according
to M = 1/t ln(Nt/N0) with N0 = density at t0 and Nt = density at t = 89 days. The estimated
daily instantaneous mortality rate (M; d-1) during the period from late August to late
November was 0.004 ± 0.001 (mean ± SE).
High survival and growth rates of introduced Pacific oysters
77
Survival (%)
100
80
60
40
20
29
.0
8.
12
.0
9.
20
.0
9.
25
.0
9.
30
.0
9.
23
.1
0.
30
.1
0.
26
.1
1.
0
Fig. 2 Survival (% + SE) of juvenile C. gigas on tiles (n = 6 tiles
with 5-19 attached oysters each) that were fixed on an intertidal
mussel bed (MM) from August to November 2002
Abundance decreases of juvenile C. gigas on shell collectors were independent of site (mussel
beds KH or MM) and tidal height (Fig. 3, Table 1). The over winter survival rate (November
2002 to February 2003) amounted to 63.7 ± 7.1% (mean ± SE) and the daily mortality rate for
the same period was M = 0.005 ± 0.001 d-1. First year survival of juveniles (November 2002
to July 2003) was independent of site as well and averaged 42.6 ± 3.9%. The daily mortality
rate for this period was 0.004 ± 0.0004 d-1.
Juv. C. gigas / shell
4
Nov 02
Feb 03
May 03
Jul 03
3
2
1
X
0
Intertidal
KH
Subtidal
Intertidal
Subtidal
MM
Fig. 3 Abundance of juvenile C. gigas on shell collectors (mean
+ SE, n = 4-6 collectors on each location) on two mussel beds
(KH and MM) in intertidal and subtidal locations from November
2002 to July 2003. X = no data
78
Chapter 4
Table 1 Analysis of covariance of abundance of juvenile C. gigas (log
transformed) and analysis of variance of survival (%) of juvenile C. gigas
(arcsine square-root transformed). Bold face values: p < 0.05
Source of variation
Abundance Nov 02 - Feb 03
Site (KH – MM)
Tide level (intertidal – subtidal)
Site x Tide level
Abundance Nov 02
Error
Survival Nov 02 – Feb 03
Site (KH – MM)
Tide level (intertidal – subtidal)
Site x Tide level
Error
Survival Nov – July 03
Site (KH – MM)
Error
SS
df
MS
F
p
0.002
0.017
0.001
0.044
0.133
1
1
1
1
16
0.001
0.017
0.001
0.044
0.008
0.203
1.985
0.107
5.295
0.658
0.178
0.748
0.035
0.082
0.255
0.003
2.543
1
1
1
15
0.082
0.255
0.003
0.170
0.485
1.506
0.019
0.497
0.239
0.893
0.001
0.260
1
9
0.001
0.029
0.049
0.831
Following a strong recruitment event in the summer of 2002 abundances of 0-group C. gigas
were six to eight-folds higher in October 2002 than in November 2001 in all three locations
(Fig. 4). A decrease in numbers of juveniles could not be detected during the winter of
2001/2002 suggesting high survival (Crassostrea plot: 94.1% survival from November 2001
to May 2002). In the following winter (2002/2003) abundances decreased significantly
(Repeated Measures ANOVA, Factor Substrate: MS = 183.16, F = 8.68, p = 0.010, Factor
Time: MS = 651.88, F = 23.35, p = 0.001). The interaction between substrate and time was
not significant (MS = 19.63, F = 0.70, p = 0.523) showing that survival did not differ between
Juvenile C. gigas / m²
substrates (Crassostrea plot: 23.9%, Mytilus plot: 23.9%, mussel bed: 23.6%).
1000
Nov 01
May 02
Oct 02
May 03
800
600
400
200
0
0
Crassostreaplot
Mytilus-plot
x
Mussel bed
Fig. 4 Mean abundance (+ SE) of juvenile C. gigas (< 20 mm in
fall, < 33 mm in spring) on experimental intertidal Crassostrea
and Mytilus plots (4m², n = 4) and on control mussel bed areas
(n = 8-12) in November 2001, May 2002, October 2002 and May
2003. X = no data
High survival and growth rates of introduced Pacific oysters
79
3.2 Size and growth of C. gigas
Analysis of length-frequency data revealed that 0-group juvenile C. gigas reached a mean
shell length of 12.0 mm on site KH and 20.0 mm on site MM about eight to nine months after
settlement which occurred in August and September (Fig. 5). Within one year post settlement
they reached 39.6 mm (KH) and 48.1 mm (MM) and after two years they had grown to 74.2
mm (KH) and 75.4 mm (MM). Von Bertalanffy growth functions were fitted to both data sets
(sites KH and MM) with fixed L∞ = 180.00 mm and calculated growth constants of K(KH) =
0.26 and K(MM) = 0.30. Growth rates of C. gigas cohorts were slightly higher on site MM
than on site KH (Table 2) and lower in the winter half year than during the growing season
from spring to fall.
Table 2 C. gigas cohort length increment (in mm month-1) in two locations (KH, MM) during
the first winter after settlement (fall - spring), the first growing season (spring - fall), the
second winter and the second growing season, respectively. Data derived from lengthfrequency distributions and cohorts were separated using Bhattacharya’s method
Cohort of 1997
1st winter
1st growing season
2nd winter
2nd growing season
KH
MM
4.2
2.7
Cohort of 2001
KH
MM
2.7
4.8
0.3
Cohort of 2002
KH
1.5
7.2
1.5
5.7
MM
2.1
9.3
2.7
3.9
Cohort of 2003
KH
1.5
6.3
MM
2.1
7.2
The growth experiment with newly settled C. gigas revealed that juveniles grew from 1.7 ±
0.3 (mean ± SE) mm in August 2002 to 12.3 ± 2.5 mm in May 2003 and reached 31.5 ± 7.0
mm in July 2003 (Fig. 6). During the 2 months from 11 May 2003 to 10 July 2003 they
reached a mean growth rate of 9.6 ± 2.3 mm month-1. No growth occurred during winter from
November to February.
80
Chapter 4
100
Length (mm)
KH
80
60
cohort 1997
40
cohort 2002
20
cohort 2003
0
3
9
15 21 27 33 39 45 51 57 63
Months after settlement
100
Length (mm)
MM
80
60
cohort 1997
40
cohort 2001
cohort 2002
20
cohort 2003
0
3
9
15 21 27 33 39 45 51 57 63
Months after settlement
Fig. 5 Mean cohort shell length (± SD) of C. gigas at two
locations (KH, MM) during the first 5 years after settlement
Length (mm)
40
30
KH
MM
20
10
0
Aug 02
(0 mo.)
Nov 02
(3 mo.)
Feb 03
(6 mo.)
May 03 Jul 03
(9 mo.) (11 mo.)
Fig. 6 Mean shell length of juvenile C. gigas (± SE; n = 5-6
collectors on each location) that had attached to shell
collectors on two intertidal mussel beds (KH and MM) from
August 2002 (settlement) to July 2003 (11 months after
settlement). mo. = months after settlement
High survival and growth rates of introduced Pacific oysters
81
3.3 Growth experiments with C. gigas and M. edulis
3.3.1 Substrate and tide level
The length of individually marked juvenile C. gigas increased similarly on all intertidal sites
from 27.8 ± 0.6 mm (mean ± SE) in June to 45.9 ± 0.6 mm in November 2002 (Fig. 7; left).
For M. edulis there was a higher length increase on the sand flat than on all other intertidal
locations (Fig. 7; right). The mean daily growth rates of C. gigas on intertidal locations were
independent of site (Sand, mussel bed KH, mussel bed MM, experimental Mytilus plot and
experimental Crassostrea plot; Fig. 8, Table 3). However, comparing growth on the 2
intertidal and 2 subtidal sites (sand flat and mussel bed KH) tide level showed a significant
effect on growth on the sand flat (Tukey’s HSD test for unbalanced data, MS = 0.02, df = 63,
p = 0.001), but not on the mussel bed.
50
40
Sand
MB (KH)
40
MB (MM)
Length (mm)
Length (mm)
45
M-plot
C-plot
35
30
35
Sand
MB (KH)
MB (MM)
M-plot
C-plot
30
C. gigas
M. edulis
25
25
Jun
Jul
Aug
Sep
Jun
Nov
Jul
Aug
Sep
Nov
Fig. 7 Length (mean ± SE) of individually marked juvenile C. gigas (left, n = 16-20) and M. edulis
(right, n = 16-19) on 5 intertidal locations in the List tidal basin from June to November 2002
subtidal
0,3
0,2
0,1
0,0
0,2
M. edulis
-1
intertidal
Growth (mm day )
C. gigas
-1
Growth (mm day )
0,4
intertidal
subtidal
0,1
0,0
Sand
MB
(KH)
MB
(MM)
M-plot
C-plot
Sand
MB
(KH)
MB
(MM)
M-plot
C-plot
Fig. 8 Daily growth rate (mean + SE) of juvenile C. gigas (n = 16-20) and M. edulis (n = 16-19)
calculated from length increment from June to August 2002 on 5 intertidal and 2 subtidal locations.
Sand: sand flat; MB (KH): mussel bed KH; MB (MM): mussel bed MM; M-plot: experimental Mytilus
plot; C-plot: experimental Crassostrea plot
82
Chapter 4
The daily growth rate of juvenile M. edulis in the intertidal was significantly higher on the
sand flat than on mussel bed or oyster plot locations (Tukey’s HSD test for unbalanced data,
MS = 0.00, df = 82, p = 0.000). Tide level affected growth of M. edulis on both sand flat and
mussel bed, explaining 40.4% of the variation (Tukey’s HSD test for unbalanced data, MS =
0.00, df = 65, p(Sand) = 0.002, p(MB) = 0.000).
Table 3 Analysis of variance on daily growth rate of C. gigas and M. edulis (square-root
transformed). Bold face values: p < 0.05
Source of variation
SS
df
MS
F
0.110
0.930
4
81
0.028
0.011
2.398
0.057
Site (Sand – MB(KH))
0.110
1
0.110
7.000
0.010
Tide level (intertidal – subtidal)
Site x Tide level
Error
Daily growth rate M. edulis intertidal
Site (Sand - MB(KH) - MB(MM) - M-plot - C-plot)
Error
Daily growth rate M. edulis intertidal - subtidal
Site (Sand – MB(KH))
Tide level (intertidal – subtidal)
Site x Tide level
Error
0.217
0.058
0.989
1
1
63
0.217
0.058
0.016
13.834
3.691
0.000
0.059
0.293
0.228
4
82
0.073
0.003
26.314
0.000
0.135
0.290
0.029
0.263
1
1
1
65
0.135
0.290
0.029
0.004
33.468
71.730
7.287
0.000
0.000
0.009
Daily growth rate C. gigas intertidal
Site (Sand - MB(KH) - MB(MM) - M-plot - C-plot)
Error
Daily growth rate C. gigas intertidal - subtidal
p
3.3.2 Fucus cover
Growth of juvenile C. gigas was significantly higher on Fucus covered mussel bed patches
than on uncovered ones (Fig. 9, Table 4).
no Fucus
15
Fucus
Condition index
Growth (mm)
15
10
5
0
no Fucus
Fucus
10
5
0
KH I
KH II
KH III
KH III
KH I
KH II
KH III
KH III
C. gigas
C. gigas
C. gigas
M. edulis
C. gigas
C. gigas
C. gigas
M. edulis
Fig. 9 Growth (left; mean + SE, n = 17-20) and condition index (right; mean + SE, n = 17-20) of
individually marked juvenile C. gigas on three intertidal mussel beds (KH I, KH II, KH III) and of
juvenile M. edulis on one intertidal mussel bed (KH III) on patches without and with Fucus cover
High survival and growth rates of introduced Pacific oysters
83
This pattern was consistent over all three sites. On site KH I also width increment was
measured and was significantly higher on Fucus-patches (ANOVA, MS = 250.82, F = 9.32, p
= 0.004). Even though the condition of C. gigas on all three sites was lower on Fucus covered
patches than on uncovered ones, ANOVA revealed neither a significant effect of Fucus cover
on a 5% probability level nor a significant interaction between Fucus and site on condition
index. Juvenile M. edulis also showed a significantly higher growth rate when covered with
Fucus, but their condition was significantly reduced in the presence of algal canopy.
Table 4 Analysis of variance on effect of site (KH I, KH II, KH III) and Fucus
cover on growth and condition index of C. gigas and on effect of Fucus cover
on growth and condition index of M. edulis. Bold face values: p < 0.05
Source of variation
Growth C. gigas
Site (KH I, KH II, KH III)
Fucus cover (present - absent)
Site x Fucus cover
Error
Growth M. edulis
Fucus cover (present - absent)
Error
Condition index C. gigas
Site (KH I, KH II, KH III)
Fucus cover (present - absent)
Site x Fucus cover
Error
Condition index M. edulis
Fucus cover (present - absent)
Error
SS
df
MS
F
p
286.38
526.425
7.89
2372.25
2
1
2
107
143.19
526.43
3.94
22.17
6.46
23.74
0.18
0.002
0.000
0.837
12.34
96.74
1
35
12.34
2.76
4.47
0.04
4.97
0.03
0.02
1.04
2
1
2
107
2.49
0.03
0.01
0.01
256.62
3.53
0.82
0.000
0.063
0.441
0.19
0.39
1
35
0.19
0.01
17.28
0.000
3.3.3 Barnacle cover
Fouling barnacles had no effect on growth of juvenile and adult oysters (Fig. 10).
Growth (mm)
30
Oyster age group
Barnacles (present- absent)
Size x Barnacles
Error
df
1
1
1
31
MS
F
p
12.56 0.001
26.30 0.23 0.636
304.93 2.65 0.113
114.94
20
10
0
Juvenile
1
C. gigas
Juvenile
2
C. gigas +
barnacles
Adult
3
C. gigas
Adult
4
C. gigas +
barnacles
Fig. 10 Growth of juvenile and adult
C. gigas with and without barnacle
cover on the shells (mean + SE, n =
6-13) from 1 June 2003 to 8
October 2003. Inset: Results of
ANOVA
84
Chapter 4
4 Discussion
This study was conducted to detect differential performance in survival and growth of the
invading oysters compared to the native mussels in order to predict to what extend the former
might displace the latter. My data demonstrate that juvenile Crassostrea gigas have high
survival and growth rates independent of substrate and tidal height. Growth was not affected
by barnacle epigrowth but was enhanced underneath a cover of brown macroalgae Fucus
vesiculosus. Performance of mussels was more variable. Growth was higher on a sand flat
compared to mussels and oysters as substrate and higher in the subtidal than in the intertidal
zone. Fucus cover enhanced length increment but reduced condition. The high survival of
juvenile and adult oysters - the latter has been shown in a previous study (Diederich et al., in
press) - may compensate for years with low recruitment and may facilitate a further increase
in abundance and range. As the oysters grow faster and reach a larger size than the native
mussels, they might have a competitive advantage over the mussels and might displace them
to less favourable habitats. The survival and growth of both species is discussed in the
corresponding order.
4.1 Survival
Approximately 70% of juvenile C. gigas survived the first three months on the mussel bed,
and about 40% reached their first reproductive period in the summer one year after settlement.
Survival was independent of tidal height, i.e. intertidal or shallow subtidal mussel bed area,
and substrate, i.e. oyster or mussel bed. However, recruitment was much lower in the subtidal
compared to the intertidal zone and on the mussel substrate compared to the oyster substrate
(see also Diederich in press), which leads to the conclusion that recruitment patterns and not
post-settlement mortality may determine the distribution of the population regarding tidal
height and substrate. In comparison, the native mussels are known to be limited by predation
pressure in the subtidal zone (Ebling et al. 1964, Seed 1993, Saier 2001).
The mortality rates found for C. gigas in this study (0.004 d-1 during the first three months
post-settlement and 0.005 d-1 during the first winter) are very low compared to mortality rates
of other juvenile bivalves in the Wadden Sea (e.g. Strasser 2002). For example, daily
mortality rates for Macoma balthica of 0.034 d-1 to 0.093 d-1 and for Cerastoderma edule and
Mya arenaria of 0.056 d-1 were described for the first three months after settlement (van der
Veer et al. 1994 and references therein). From mussel populations in England annual
High survival and growth rates of introduced Pacific oysters
85
mortality rates of 1st year mussels of 95 - 100% have been described and only few mussels
survived beyond their second or third year (Dare 1976).
Over-winter survival of oysters varied widely between the two winters investigated. During
the winter of 2001/2002 more than 90% of the 0-group juveniles survived until the following
spring, but during the next winter of 2002/2003 only about 25% survived. It is notable that the
first winter was very mild with only one day of freezing air temperatures accompanied by
offshore winds that lead to prolonged emersion times. In the second winter, however, low air
and water temperatures caused by a cold spell of 37 days with freezing air temperatures
together with prolonged offshore winds (data from the local weather station of the German
Weather Service), may have caused the high mortality of juvenile oysters. However, adult
oysters seem not to be affected by cold winters. Data of length-frequency distributions
revealed that oysters above one year of age experienced no detectable mortality during the
next five years including the winter of 2002/2003 (Diederich et al. in press). This is in
accordance with a study from Reise (1998) who found that about 66% of the oyster
population in List tidal basin survived the anomalous severe winter of 1995/1996 with over 60
days of freezing air temperatures and formation of ice flows.
Also, the native mussels in the Wadden Sea seem to be very tolerant of freezing temperatures
(Beukema 1990, Strasser et al. 2001). However, ice scouring as well as storm events can
severely damage intertidal mussel beds (Nehls & Thiel 1993, Obert & Michaelis 1991,
Strasser et al. 2001). The destruction of mussel beds by storms or ice scouring could be a
reason for lower abundances of juvenile oysters after a severe winter. Young oysters together
with mussels will be more easily scraped off the ground than larger oysters that are partly
stuck in the sediment or that form solid reef structures. However, there is no evidence whether
the oysters in this study died or were simply washed to other locations by storms or ice.
Nevertheless, it can be assumed that the newly developed oyster reefs are more resistant to ice
and storms than the native mussel beds, because the oysters form more solid structures by
cementing their heavy and thick shells to each other (Fig. 11).
Survival of juvenile and adult C. gigas on intertidal and subtidal mussel beds in the Wadden
Sea is very high compared to survival rates of other bivalves, including mussels. As high
recruitment events that lead to a rejuvenation of the population occur only sporadic in oysters
as well as in mussels (Strasser et al. 2001, Diederich et al. in press), high survival is important
to ensure the persistence of the population and might permit population growth even if
numbers of recruits are low.
86
Chapter 4
4.2 Size and growth
Juvenile oysters reached a mean shell length of 35 - 53 mm after one year and of 68 - 82 mm
after two years on intertidal mussel beds in the northern Wadden Sea. A mean growth rate of
approximately 7 mm of shell length per month (maximum growth rate: 9.6 mm per month)
was obtained during their first growing season that lasts from April to October. During the
next growing season in the 2nd year, the growth rate was with 3 - 5 mm per month
considerably lower. A comparison of the growth performance of C. gigas in different
geographical regions reveals that in the Wadden Sea growth rates are somewhat lower
compared to other areas (Table 5). However, growth is only slightly lower than in the native
habitat (Japan and Korea). The oysters also do reach their maximum length of about 300 mm
that has been described for other areas (Dinamani 1971, Quayle 1988, Dankers et al. 2004).
Therefore it can be concluded that growth performance in the Wadden Sea is unlikely to
hamper the spread of Pacific oysters in the Wadden Sea.
Table 5 Growth of C. gigas at different geographical locations as indicated in literature
Length at time after
settlement
Location
Tide level
Japan
intertidal
60 mm
90 mm
(1 year)
(1.5 years)
Kobayashi et al. 1997
Korea
subtidal
70 mm
(1 - 1.5 years)
Hyun et al. 2001
New Zealand
intertidal
80 - 100 mm
(1 year)
Dinamani 1971
intertidal
60 mm
(1 year)
Dinamani 1991
subtidal
90 mm
(1 year)
Quayle 1988
subtidal
60 - 100 mm
70 - 110 mm
(1 year)
(2 years)
Brown and Hartwick 1988
California
intertidal
100 mm
(2 years)
Chew 1979
Mexico
intertidal
90 mm
(1 year)
García-Esquivel et al. 2000
Dutch Wadden Sea
intertidal
30 - 100 mm
130 mm
(1 year)
(2 years)
Dankers et al. 2004
intertidal
30 - 40 mm
60 mm
70 mm
(1 year)
(2 years)
(3 years)
Tydeman et al. 2002
intertidal
40 - 50 mm
70 - 80 mm
(1 year)
(2 years)
this study
British Columbia
North. Wadden Sea
Reference
High survival and growth rates of introduced Pacific oysters
87
Growth of mussels on intertidal mussel beds in the Wadden Sea is well documented,
including the sites of this study; juveniles reach about 10 - 30 mm shell length after one year,
30 - 40 mm after two years, and they approach their maximum size of 50 - 70 mm after three
to four years (Buschbaum & Saier 2001, Nehls 2003). In the subtidal, mussels grow to about
20 mm in one year and they reach 55 - 60 mm after 2.5 years (Dankers & Zuidema 1995). The
size differences in mussels and oysters are obvious, with oysters attaining about three times
the length of mussels after one year. An advantage of the larger size could be a possible
competitive advantage if food competition occurs on the densely packed mussel bed. Local
food depletion may occur immediately above mussel beds when populations of suspension
feeders occur at great densities or when currents are too low to replenish the food (Dame et al.
1984, Fréchette et al. 1989, Peterson & Black 1991). The filtration rate of large mussels (5 - 7
cm shell length) is with 70 l day-1 (Davenport & Woolmington 1982), much lower than of
medium-sized oysters (9 - 10 cm shell length) which reach a filtration rate of 30 l h-1 (Quayle
1988). A comparison of filtration rates of similar-sized C. gigas and M. edulis revealed that
filtration rates of C. gigas are two to three folds higher (Walne 1972). However, a different
feeding behaviour and possibly also different food sources utilised by C. gigas and M. edulis
lead to the assumption that mussels and oysters may not necessarily be strong competitors
(Bougrier et al. 1997, Riera et al. 2002). Whether or not the oysters and mussels in the
Wadden Sea are direct food competitors will need further study, as it is difficult to transfer
physiological studies from laboratory experiments to the actual field situation. Nevertheless,
the faster growth rate may enable the oysters to grow into a size refuge from predation much
earlier than the native mussels. Most benthic predators are described as size-selective feeders
that preferentially prey on food items that promise optimal energy gain (Elner & Hughes
1978, Hughes 1979). For example, mussels attain a size refuge from starfish predation when
they reach a length of 35 mm (O’Neill et al. 1983, Reusch & Chapman 1997) and shore crabs
seldom feed on mussels above 20 mm shell length (Ebling et al. 1964, Dare & Edwards
1976). The only predators that feed on larger mussels are shorebirds like oystercatchers and
eider ducks (Goss-Custard et al. 1981, Zwarts & Drent 1981). However, it is unlikely that
they will be able to feed on large oysters especially once the oysters are interconnected in
solid reefs. Therefore, I conclude that C. gigas will have a competitive advantage over M.
edulis because of faster growth and larger size.
88
Chapter 4
4.3 Factors affecting growth
4.3.1 Substrate
Growth of juvenile C. gigas was not affected by substrate, i.e. sand flat, mussel bed,
experimental mussel and oyster plot. Mussels on the other hand showed significantly higher
growth rates on the sand flat compared to all other locations. This could be a hint towards
density dependent growth in mussels but not in oysters. That mussel growth may be reduced
due to intraspecific competition has been described before, one reason being that juveniles
amongst the byssus of larger mussels are unable to compete successfully for food (Dare &
Edwards 1976, Kautsky 1982, Bertness & Grosholz 1985, Okamura 1986). However, also for
oysters reduced growth in the presence of intra- or interspecific competitors has been
described (Zajac et al. 1989, Arakawa 1990, Rheault & Rice 1996). On the other hand, oyster
reefs with a high profile have been described as bearing ideal conditions for oyster growth,
because of high current velocities caused by the reef structure that counteract food depletion
in boundary layers and smothering through sedimentation (Peterson & Black 1987, Fréchette
et al. 1989, Lam & Wang 1990). Bearing in mind that the oysters show a higher filtration rate
than mussels of similar size (Walne 1972), it is likely that the inferior mussels are more
affected by competition than the oysters and are therefore growing faster on the sand flat
compared to mussel or oyster beds.
4.3.2 Tide level
Mussel growth was strongly affected by emergence time with significantly higher growth
rates in subtidal than in intertidal zones on both sand flat and mussel bed. Oyster growth, on
the other hand, was only on the sand flat higher in the subtidal than in the intertidal zone. On
the mussel bed, no significant effect of emergence time on oyster growth occurred. Lower
growth rates in intertidal compared to subtidal zones is a well known phenomenon in mussels
(Seed 1969, Bertness & Grosholz 1985, Buschbaum & Saier 2001), and is seen as a
consequence of reduced feeding times (Peterson & Black 1987) or metabolic stress due to
anaerobiosis (Widdows & Shick 1985, De Zwaan & Mathieu 1992). Growth of C. gigas
seems to be less affected by emergence time. Roegner and Mann (1995) describe no effect of
exposure on oyster growth as long as the aerial exposure stays below 25% as in the study at
hand. Another study found reduced growth in the intertidal (20% exposure during a tidal
cycle) only during the first month after settlement, but not thereafter (Crosby et al. 1991).
Hydrodynamic factors that may enhance the food supply on the shore due to resuspension of
High survival and growth rates of introduced Pacific oysters
89
orgainc matter are considered to compensate for reduced feeding times in the intertidal
(Bayne et al. 1988). In conclusion it may be assumed that emergence time has a stronger
effect on mussels than on oysters. This may hint towards oysters having a broader
physiological niche.
4.3.3 Fucus cover
Fucus cover on intertidal mussel beds significantly enhanced shell growth of both, mussels
and oysters. However, condition indices of both species were lower underneath Fucus cover,
but this effect was significant only for mussels. This shows that the enhanced shell growth
was not accompanied by a corresponding increase in meat content and that this effect was
stronger in mussels than in oysters, indicating that oysters may benefit from Fucus cover,
whereas mussels might be negatively influenced.
The enhanced shell growth underneath Fucus canopy compared to uncovered mussel bed
patches is surprising, because the algal canopy leads to higher sedimentation due to reduced
current velocities (Albrecht & Reise 1994), which is known to be disadvantageous for
shellfish growth (Loosanoff & Tommers 1948, Widdows et al. 1979, Barillé et al. 1997). On
the other hand, the modified flow regimes caused by the Fucus canopy may lead to
accumulation of food (Leonard 1999) and thereby promote growth. However, the shape of M.
edulis and C. gigas is known to vary with environmental factors such as density and type of
substrate on which they are growing (Seed 1968, Quayle 1988). On very soft ground, like it
occurs on mussel beds underneath Fucus canopy, oysters grow longer and narrower, possibly
because they want to escape suffocation in mud. But as shell width also showed a higher
increase underneath Fucus cover, the higher growth rate underneath Fucus canopy cannot be
sufficiently explained by an elongated shape. Additionally, during the experiment on site KH
III where growth of C. gigas and M. edulis in relation to Fucus cover were compared, oysters
and mussels were kept in mesh cages above the surface and were therefore prevented from
sinking into the mud. In conclusion, the lower condition index of Fucus covered mussels is a
hint that Fucus interferes with mussel performance, while C. gigas is less affected or may
even benefit from the algal cover.
4.3.4 Barnacle epigrowth
Whereas growth of C. gigas was not affected by barnacle cover (this study), mussel growth is
significantly reduced by barnacle epigrowth (Buschbaum & Saier 2001). The reason for lower
90
Chapter 4
mussel growth is considered to be not food competition but changed hydrodynamic conditions
and modified microcurrents due to the barnacle shells (Buschbaum & Saier 2001). As oyster
shells are undulated and much rougher than mussel shells, it is likely that barnacle epigrowth
on oyster shells will not change hydrodynamic conditions in the same way as on the smooth
mussel shells. Another possible reason for reduced mussel growth is a drag-induced trade-off
effect caused by epigrowth, because mussels with epibionts have a greater surface area and
are more vulnerable to being washed away by currents. Therefore, the mussels need to invest
more energy in byssus thread production (Price 1983, Okamura 1986). As the oysters do not
produce byssus but attach themselves very firmly to hard substrates and to each other by
releasing cement from a food gland, this would explain why mussels are affected by barnacles
and oysters are not. Further, the much larger size of oysters relative to barnacles than the size
ratio of mussels to barnacles may render epigrowth of barnacles as insignificant to the oyster.
In conclusion, the very common and widespread barnacle fouling on mussels and oysters may
interfere with mussel growth while oysters remain unaffected.
5 Conclusion
The persistence and further increase of the oyster population in the Wadden Sea will be
facilitated by high survival rates in juveniles and adults, because this may compensate for
years with low recruitment. The settlement preference of C. gigas for conspecifics in the
intertidal zone (Diederich in press) leads at present to the formation of massive oyster reefs
that are expected to be more resistant to environmental stress like storms and ice scouring
than the native mussel beds, which they replace (Fig. 11). In addition, high growth rates
independent of tide level, substrate, Fucus cover and barnacle epigrowth, contribute a wide
niche. The faster growth of invading oysters compared to native mussels might give them a
competitive advantage if food and/or space is limiting. Therefore it can be concluded that the
recent massive increase of C. gigas in the northern Wadden Sea following high recruitment
during three consecutive anomalously warm summers (Diederich et al. in press), and a
positive feedback of adult oysters on settlement (Diederich in press) is likely to lead to a
permanent transformation in the benthic community of this area.
High survival and growth rates of introduced Pacific oysters
91
Fig. 11 Resident mussel bed (Mytilus edulis) and non-native oyster reef (Crassostrea gigas) in the
northern Wadden Sea in summer 2004. Inset: start of oyster reef formation. Photos: K. Reise, S.
Diederich
Acknowledgements
I am very grateful to Werner Armonies and Karsten Reise for discussions and thoughtful
reviews of the manuscript. Andreas Schmidt (Senckenberg Institute) helped with the use of
FISAT.
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Invasion facilitated by weak predation?
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Chapter 5
Pacific oysters Crassostrea gigas in the Wadden Sea:
invasion facilitated by weak predation?
Abstract
In the Wadden Sea (North Sea), bivalve populations are often limited by benthic predation,
with shore crabs Carcinus maenas and starfish Asterias rubens being important predators.
Introduced Pacific oysters Crassostrea gigas recently increased in abundance and range,
overgrowing resident epibenthic mussel beds Mytilus edulis. Even though recruitment success
of C. gigas is confined to years with particularly high summer water temperatures, high
survival rates of juveniles and adults compensate for years with low recruitment. Using
predator exclusion experiments and laboratory feeding preference trials, I tested the
hypothesis that C. gigas is subjected to low predation pressure because the main benthic
predators prefer mussels to oysters. Predation was only found to affect oyster recruitment in
the subtidal, but not subsequent survival in either intertidal or subtidal locations. Juvenile and
adult shore crabs and starfish strongly preferred mussels to oysters in feeding trials. It is
concluded that the invasion success of C. gigas is supported by (1) selective feeding by the
main mussel predators, (2) a possible mismatch between oyster recruitment and predator
abundances and (3) a larger size and faster growth of oysters compared to native mussels that
may facilitate an early size refuge from predation. The competitive advantage of C. gigas over
M. edulis may lead to a permanent displacement of mussels and to a shift in the food web of
the Wadden Sea.
Keywords
Introduced species, Predation, Size refuge, Competitive advantage, Mussel beds
100
Chapter 5
1 Introduction
Predation may have a profound impact on structuring marine benthic communities (Reise
1985a, b, Seed 1993, Hunt & Scheibling 1997). By keeping their prey below carrying
capacity, predators may allow coexistence of competing species and thus prevent
monopolization by a dominant species (Paine 1974). This steady state may be threatened by
invaders if these escape predation pressure by resident predators and become superabundant
(Keane & Crawley 2002, Colautti et al. 2004).
Pacific oysters Crassostrea gigas have been introduced to the Wadden Sea by aquaculture in
the 1980s (Reise 1998). They reproduced naturally and recently started to increase
dramatically in abundance and range (Dankers et al. 2004, Smaal et al. 2004, Diederich et al.
in press). As they need hard substrates for settlement, they are overgrowing shell beds as well
as resident epibenthic mussel beds Mytilus edulis, thus posing a threat to this native species.
Mussel beds are characterized by a high productivity (Asmus 1987, Dankers & Zuidema
1995) and biodiversity (Riesen & Reise 1982, Tsuchiya & Nishihira 1986, Dittmann 1990),
which makes them important food resources for various crustaceans, fish, birds, and humans
(Seed & Suchanek 1992). Their overgrowth and possible replacement by oyster reefs may
therefore have a profound impact on the benthic community of the coastal North Sea.
As recruitment success of C. gigas in the northern Wadden Sea is confined to a few years
with exceptionally high summer water temperatures, the high survival rates of juveniles and
adults that have been found in a previous study are important prerequisites for the invasion
success, because they compensate for recruitment failures (Diederich et al. in press, Diederich
submitted). The question arose, whether a lack of predation may cause the high survival rates
and may facilitate the invasion process by giving C. gigas a competitive advantage over its
native congener.
Mussel populations in the Wadden Sea are often limited by predation and depend on high
recruitment success in years when predator abundances are low, usually following severe
winters (Beukema 1991, Strasser et al. 2001, Strasser 2002). Especially epibenthic predators
like shore crabs Carcinus maenas and starfish Asterias rubens have profound impacts on the
density and distribution of mussels (Scherer & Reise 1981, Jensen & Jensen 1985, Dankers &
Zuidema 1995, Kristensen & Lassen 1997, Saier 2001). Even though shrimps Crangon
crangon and various fish species like gobies Pomatoschistus microps, flounders Platichthys
flesus and plaice Pleuronectes platessa are known to prey on juvenile bivalves, their impact is
Invasion facilitated by weak predation?
101
considered to be low (Reise 1977, Jensen & Jensen 1985). Birds like eiders Somateria
mollissima, oystercatchers Haematopus ostralegus and herring gulls Larus argentatus may
intensively prey on medium to large sized mussels (Zwarts & Drent 1981, Hilgerloh et al.
1997, Nehls et al. 1997). However, under the premise that population dynamics are largely
determined by survival of juveniles, the impact of birds seems to be low compared to benthic
predators (Reise 1985b). Thus, in this study the focus will be on predation by shore crabs and
starfish, because they are abundant and voracious mussel consumers in the Wadden Sea and
are known to feed on oysters on other shores (e. g. Parsons 1974, Walne & Davies 1977,
Chew 1998).
Predator exclusion experiments were conducted on intertidal and subtidal mussel beds in
order to assess the impact of benthic predation on recruitment and survival of juvenile C.
gigas. Laboratory feeding preference experiments with different sized C. maenas and A.
rubens were added to show whether species and size selective predation preferences may
explain the high survival rate of juvenile C. gigas. In this respect the possible advantage of
faster growth and larger size of an introduced species compared to a native congener is
discussed in view of size refuge from predation and missing predators in the recipient
ecosystem.
2 Material and methods
2.1 Study site
Field experiments on survival of juvenile Crassostrea gigas were carried out in the List tidal
basin in the northern Wadden Sea (North Sea, Germany, 54°50’ - 55°10’N and 08°20’ 08°40’E). This shallow basin (404 km² area) is surrounded by the mainland and two islands
(Sylt and Rømø) that are connected with the mainland by dams. Intertidal sand flats, seagrass
meadows, and natural epibenthic mussel beds characterize the area. Tides are semidiurnal and
the mean tidal range is 2 m; the average salinity is close to 30 psu. Primary production is
about 300 g C m-2 y-1. Monthly mean water temperatures range from 18.2°C in August to
2.3°C in February. Detailed information on hydrography, geology, sediments and biota of the
bay is given in Gätje and Reise (1998). A commercial oyster farm that produces about two
million oysters per annum has been in operation in this basin since 1986.
102
Chapter 5
2.2 Predator exclusion experiments
Three separate predator exclusion experiments were conducted in order to assess the impact
of benthic predation on recruitment and survival of juvenile C. gigas on intertidal and subtidal
mussel beds. The first experiment, designed to test whether predation may limit early
recruitment of C. gigas, was carried out from 31 July to 15 September 2003, which is the
settlement period of oysters in this area. Shell collectors made from eight clean (i.e. with no
epigrowth) dead oyster shells (mean shell length ± SD: 87.7 ± 7.9 mm) that were strung on a
plastic covered line were used as attachment surfaces for oyster larvae. The experimental
design included full cages to exclude all possible predators, partial cages to control for
potential cage artefacts and shell collectors without any protection (Fig. 1).
(a)
(b)
dead oyster shell
(c)
Fig. 1 Schematic diagram of the experimental set-up used in the
predator exclusion experiments: (a) shell collector protected by a full
cage, (b) shell collector with partial cage and (c) shell collector
without cage
Although partial cages cannot control for all possible artefacts of caging, they were employed
in consideration of known artefacts such as changes in light, hydrodynamics and
attractiveness for predators that may influence settlement and survival (e.g. Connell 1997). To
achieve full protection, shell collectors were placed separately in cylindrical cages (250 mm
long, 125 mm diameter) made from plastic rings and gauze (1 mm mesh opening). Partial
cages were constructed in the same way, but two holes (70 × 15 mm) were cut into the gauze
at opposite sides. Shell collector lines without a cage around them were used as control
treatments. All experimental units (six replicates for each treatment and two tidal levels) were
pinned with iron bars horizontally on intertidal and subtidal parts of a natural mussel bed so
that the shells touched the mussels beneath. The intertidal location had an exposure time of
about 2 h per tide and the subtidal location was located 0.5 - 1 m below the surface level at
low tide. At the end of the experimental period, all collectors were brought back to the
laboratory and attached juvenile oysters were counted and shell length (largest diameter of the
shell) was measured with electronic vernier callipers accurate to 0.1 mm. Analysis of variance
(ANOVA) followed by Tukey’s HSD test was used to compare abundances of recruits on the
Invasion facilitated by weak predation?
103
shell collectors in relation to tidal level and cage protection. Data on shell length of recruits
were compared using non-parametric tests (Kruskal-Wallis-ANOVA) because of a failure to
satisfy the heterogeneity of variances assumption. Effects were considered to be statistically
significant if p-value was < 0.05.
The survival of juvenile C. gigas was investigated on a subtidal mussel bed from 10 October
2003 (which is about 1 - 2 months after settlement) until 19 March 2004. The experimental
setup consisted of full and partial cages and no protection controls as described above. The
same cages and no cage setups were used (eight replicates), but only two dead oyster shells
with two juvenile C. gigas attached to each shell were strung on the line. The oysters had an
initial shell length of 2 - 12 mm (on each shell there was one juvenile oyster with 2 - 6 mm
shell length and one with 6 - 12 mm). At the end of the experimental period all remaining
oysters were counted and measured and the length increment of individual oysters was
determined.
A third caging experiment was conducted in order to assess survival of juvenile C. gigas on
an intertidal mussel bed during the first three to four months after settlement. This time frame
was used because Carcinus maenas, which is one of the most common predators that may
prey on juvenile C. gigas in the intertidal, is only present in this area from spring to fall (Reise
1977). Thus, it was not necessary to extend this experiment over the winter period. The
experimental setup was similar to the one described above, consisting of full cages, partial
cages and no cage replicates, but the cages differed somewhat. Dead oyster shells with 1 - 3
attached juvenile C. gigas were screwed on wooden boards (150 × 100 mm), which were
fixed on an intertidal mussel bed with iron bars. On 20 of these boards, cylindrical mesh cages
were mounted (80 mm height, 100 mm diameter, 5 mm mesh opening). On another 20 boards
the same cages were mounted, but these had two openings (70 × 40 mm) cut into opposite
sides of each cage. Altogether 60 experimental units were deployed on an intertidal mussel
bed from 11 September to 12 December 2002 when the remaining juvenile C. gigas were
counted and measured. Data for abundance, length and growth of juvenile C. gigas were
analysed using ANOVA.
2.3 Length – meat weight relationship for Crassostrea gigas and Mytilus edulis
The relationship between shell length and meat dry weight was established for C. gigas and
M. edulis in order to assess whether shell length would be an appropriate parameter to be used
in feeding preference experiments. Shell length and dry meat weight of 83 oysters (shell
104
Chapter 5
length: 24 - 160 mm) and 109 mussels (shell length: 20 - 71 mm) was obtained from bivalves
collected on two different mussel beds in May 2002. For dry weight determination, the
oysters and mussels were stored in a deep freezer at –20°C for several days. The bivalves
were then cooked in seawater for 4 minutes. Afterwards meat and shell of the individuals
were separated and dried to constant weight at 80°C (6 - 7 days). After cooling in an
exsiccator meat and shell were weighed separately on a torsion balance accurate to 0.01 g. An
exponential relationship between meat dry weight and length was established (Fig. 2). For
bivalves from 20 to 40 mm shell length there was no difference in meat content in relation to
shell length. For larger bivalves, however, meat content was higher in C. gigas than in M.
C. gigas
1,6
C. gigas
6
Meat dry weight (g)
Meat dry weight (g)
edulis of similar size.
M. edulis
4
2
0
M. edulis
1,2
0,8
0,4
0
0
20
40
60 80 100 120 140 160
Shell length (mm)
20
30
40
50
Shell length (mm)
60
Fig. 2 Meat dry weight of C. gigas and M. edulis in relation to shell length (left) and enlargement of the
20 - 60 mm shell length section (right). Equations for regression lines are: C. gigas y = 0.00004x2.387,
R2 = 0.834, n = 83; M. edulis y = 0.0001x2.028, R2 = 0.750, n = 109 with y = meat dry weight (g) and x =
shell length (mm)
2.4 Feeding preference experiments
Laboratory feeding preference experiments with different sized Carcinus maenas (13 - 73 mm
carapax width, the latter is about the maximum size of C. maenas in this area) were carried
out in July 1999, June 2002 and September 2003. For each set of experiments, crabs were
collected by hand on intertidal mussel beds in the List tidal basin and kept in an indoor
aquarium tank (1000 l) with running seawater (ambient water temperature; in July and August
approximately 18°C) prior to experiments. Only undamaged crabs free of parasite Sacculina
carcini infestations were selected. Prey items, i.e. Mytilus edulis and Crassostrea gigas of
different size classes, were collected on the same intertidal mussel beds. All bivalves were
measured with vernier callipers to the nearest millimetre (shell length = largest diameter of
the shell) and cleaned from epigrowth with an iron scraper to avoid confounding artefacts,
Invasion facilitated by weak predation?
105
because epibionts may alter predator preferences (see Enderlein et al. 2003). For the same
reason, only oysters attached to dead shell material were used in the feeding trials.
Table 1 Carcinus maenas. Laboratory feeding preference experiments with different
sized shore crabs which were offered different sizes of Crassostrea gigas and Mytilus
edulis as prey. f = female, m = male, n = number of replicates (each C. maenas is
one replicate), Cra = Crassostrea, Myt = Mytilus. Consumed bivalves = bivalves
consumed crab-1 day-1 divided by bivalves offered crab-1 day-1
Trial
a
b
c
d
e
f
g
h
i
Carapax
width Sex
(mm)
13 - 17
23 - 25
34 - 42
47 - 50
61 - 69
10 - 15
20 - 25
20 - 25
60 - 73
f
m
m
m
m
f
m
m
m
n
Time
(days)
3
2
4
13
10
8
6
6
5
10
2
14
14
16
2
2
3
16
No. and size of Consumed
prey
C. gigas
(mm length)
(% ± SE)
Consumed
M. edulis
(% ± SE)
2 Cra (6-8)
2 Myt (6-8)
0
66.7 ± 0.0
2 Cra (6-8)
2 Myt (6-8)
0
100.0 ± 0.0
4 Cra (10-30)
4 Myt (10-30)
5.8 ± 0.8
4 Cra (20-30)
4 Myt (20-30)
1.6 ± 0.9
5 Cra (30-40)
5 Myt (30-40)
2.7 ± 0.8
2 Cra (3-5)
2 Cra (6-8)
2 Cra (9-11)
2 Myt (3-5)
3 Myt (6-8)
3 Myt (9-11)
8.3 ± 8.3
0
4.2 ± 4.2
2 Cra (3-5)
2 Cra (6-8)
2 Cra (9-11)
2 Myt (3-5)
3 Myt (6-8)
3 Myt (9-11)
0
0
0
2 Cra (4-6)
2 Cra (6-8)
2 Myt (4-6)
2 Myt (6-8)
2 Myt (8-10)
26.7 ± 3.3
20.0 ± 0.0
1 Cra (20-30)
1 Cra (35-40)
1 Myt (20-30)
1 Myt (35-40)
18.8 ± 4.1
6.3 ± 2.2
57.6 ± 1.7
56.4 ± 2.8
15.0 ± 1.9
62.5 ± 4.2
69.4 ± 8.3
8.3 ± 2.8
100.0 ± 0.0
100.0 ± 0.0
91.7 ± 2.8
100.0 ± 0.0
90.0 ± 5.8
73.3 ± 13.3
98.8 ± 0.9
23.1 ± 3.4
At the start of each experiment, crabs were placed separately in 25 × 15 × 17 cm aquaria filled
with aerated seawater (5 l, circa 18 - 20°C), a sand layer and a Fucus cluster to provide shelter
from visual stress. Carapax width of C. maenas was measured with vernier callipers to the
106
Chapter 5
nearest millimetre. After starving the crabs for 4 days to standardize hunger levels, mussels
and oysters of different sizes were added. Each day of the experimental periods, which lasted
between 2 and 16 days, the water inside the aquaria was changed and the number and size of
consumed mussels and oysters was noted (see Table 1 for experimental set-up).
Subsequently, all eaten bivalves were replaced by bivalves of the same species and size.
Results are expressed as mean number of consumed bivalves per crab per day divided by the
number of bivalves of the respective species offered per day:
% Consumed = No. of consumed bivalves crab-1 day-1 / No. of offered bivalves crab-1 day-1.
This method of data presentation was chosen, because prey choice was the focus of this
investigation and not absolute numbers of bivalves that are consumed by C. maenas.
Prey choice experiments with different sized Asterias rubens (14 - 151 mm arm length, the
latter being the largest starfish size class present in this area) were conducted in August and
September 1999, in June 2002 and in September and October 2003 in similar experimental
set-ups as described above. All starfish used in the experiments were fished with a traditional
oyster dredge from subtidal habitats in the List tidal basin and only undamaged individuals
were selected. Mean arm length of each A. rubens was determined by measuring the distance
from the tip of each arm to the mouth opening with vernier callipers to the nearest millimetre.
Mussels and oysters used as prey items were collected on intertidal mussel beds, cleaned from
all epigrowth and stored in an indoor tank (1000 l) with running aerated seawater. Each
starfish was placed in a separate aquarium (size of aquaria depending on starfish size: 30, 60,
and 110 l) with running aerated seawater (circa 18°C) and was offered a choice of sets of
large and small M. edulis and C. gigas of similar size (see Table 2 for experimental set-up).
Number and size of prey items consumed was recorded daily and every bivalve eaten was
replaced with an individual of the same species and size. Experiments lasted from 1 to 37
days.
From September to October 1999 an additional feeding experiment was conducted with 17
large A. rubens (mean arm length 103 - 130 mm) that were placed together in a 1000 l indoor
tank with running aerated seawater. 100 mussels and 100 oysters (shell length of both species
30 - 60 mm) were added and number of individuals eaten was recorded every day for 2
weeks. Consumed bivalves were replaced with individuals of the same size and species. After
2 weeks, the remaining mussels were removed and for the next 37 days only oysters remained
as food items. Again, numbers of individuals eaten were recorded and replaced every day.
Invasion facilitated by weak predation?
107
Table 2 Asterias rubens. Laboratory feeding preference experiments with different
sized starfish which were offered different sizes of Crassostrea gigas and Mytilus
edulis as prey. n = number of replicates (each A. rubens is one replicate), Cra =
Crassostrea, Myt = Mytilus. Consumed bivalves = bivalves consumed starfish-1 day-1
divided by bivalves offered starfish-1 day-1
Trial
Arm length
(mm)
n
Time
(days)
a
19 - 22
5
1
b
c
d
e
f
g
h
26 - 31
14 - 17
23 - 28
31 - 35
35 - 41
84 - 102
122 - 151
5
6
6
6
6
9
8
1
5
5
5
5
11
37
No. and size of
prey
(mm length)
Consumed
C. gigas
(% ± SE)
2 Cra (6-8)
2 Myt (6-8)
20.0 ± 12.2
2 Cra (6-8)
2 Myt (6-8)
Consumed
M. edulis
(% ± SE)
60.0 ± 24.5
30.0 ± 20.0
60.0 ± 24.5
2 Cra (6-8)
2 Cra (9-11)
2 Myt (6-8)
2 Myt (9-11)
25.0 ± 10.9
18.3 ± 3.1
2 Cra (6-8)
2 Cra (9-11)
2 Myt (6-8)
2 Myt (9-11)
28.3 ± 8.6
31.7 ± 4.9
2 Cra (6-8)
2 Cra (9-11)
2 Myt (6-8)
2 Myt (9-11)
16.7 ± 3.7
11.7 ± 5.0
2 Cra (6-8)
2 Cra (9-11)
2 Myt (6-8)
2 Myt (9-11)
30.0 ± 4.2
16.7 ± 4.6
2 Cra
2 Cra
3 Myt
3 Myt
(10-25)
(26-40)
(10-25)
(26-40)
1.3 ± 0.8
2.7 ± 1.2
4 Cra (40-50)
4 Cra (50-60)
4 Myt (40-50)
4 Myt (50-60)
0.3 ± 0.1
0.2 ± 0.1
41.7 ± 5.9
31.7 ± 9.6
71.7 ± 4.2
86.7 ± 4.2
90.0 ± 3.1
86.7 ± 4.2
88.3 ± 7.3
85.0 ± 3.1
38.4 ± 5.4
44.4 ± 6.3
9.7 ± 1.2
2.2 ± 0.5
Data analysis of feeding preference experiments is difficult because of a lack of independence
of variables and inappropriate use of controls (Peterson & Renaud 1989, Roa 1992). Solutions
proposed for this problem which suggests physically pairing experimental chambers
containing a predator and randomly arranged multiple food items with a control chamber
containing no predator but the same food items (Prince et al. 2004) were not applicable for the
experiments presented here, because the prey items would not change without a predator
present and therefore a control chamber would provide no additional information. As there is
108
Chapter 5
no unimpeachable solution for this problem, and the results obtained during the feeding
experiments were clear-cut, I refrained from statistical analysis.
3 Results
3.1 Predator exclusion experiments
Recruitment of juvenile C. gigas was significantly affected by tide level, cage coverage and
interaction between the two factors (Fig. 3, Table 3). For the intertidal location, Tukey’s HSD
Test revealed significant differences only between full and partial cages, suggesting cage
artefacts confounded the results. On the subtidal location, however, abundances of recruits
were about three times and significantly higher on fully protected oyster shells (2.29 ± 0.33
juveniles shell-1) than on unprotected (0.77 ± 0.17 juveniles shell-1) and on partly protected
ones (0.71 ± 0.12 juveniles shell-1), suggesting a predation effect on abundance of 0-group C.
gigas. The length of juveniles in the subtidal locations did not differ between the three
treatments (mean length ± SD = 5.5 ± 1.3 mm; Kruskal-Wallis ANOVA, H (2, N = 18) =
1.73, p = 0.421), but in the intertidal cage cover had a significant influence on shell length
Number of juvenile C. gigas shell-1
(Kruskal-Wallis ANOVA, H(2, N = 18) = 7.45, p = 0.024).
3
2
1
0
Full
cage
Partial No cage
cage
Intertidal
Full
cage
Partial No cage
cage
Subtidal
Fig. 3 Crassostrea gigas. Mean abundance (+ SE) of juveniles
that settled on dead oyster shells with and without cage
protection in intertidal and subtidal locations. Cages (n = 6) in the
field from 31 July 2003 - 15 September 2003
Invasion facilitated by weak predation?
109
Table 3 2-way analysis of variance (a) and Tukey’s HSD Test (b) on effect of predation on
abundance of juvenile C. gigas in intertidal and subtidal locations. Bold face values: p < 0.05
(a)
df
MS
F
p
Tide level
Cage
Tide level x Cage
Error
1
2
2
30
6.46
5.42
1.02
0.27
23.69
19.85
3.74
< 0.001
< 0.001
0.035
(b)
Full cage
Intertidal
Full cage
Partial cage
No cage
0.022
0.845
Subtidal
Full cage
Partial cage
No cage
< 0.001
< 0.001
Partial cage
No cage
0.022
0.845
0.263
0.263
< 0.001
< 0.001
1.000
1.000
There was no significant difference in survival of juvenile C. gigas in relation to cage
protection in either the intertidal or the subtidal location (Fig. 4, Table 4). In the intertidal,
survival varied between 82% on shells in full cages and 61% and 59% on partly and
unprotected shells, respectively. In the subtidal, 64 - 75% of juveniles survived. Length and
growth of juveniles was independent of caging, in the intertidal as well as in the subtidal
experiment (ANOVA).
100
100
A. Intertidal
80
Survival (%)
Survival (%)
80
B. Subtidal
60
40
60
40
20
20
0
0
Full cage
Partial cage
No cage
Full cage
Partial cage
No cage
Fig. 4 Crassostrea gigas. Mean survival (% + SE) of 0-group juveniles on intertidal (A) and subtidal (B)
mussel beds with and without cage protection. A: n = 14 -19 replicates with 1-3 juvenile oysters each;
from 11 September to 12 December 2002. B: n = 8 replicates with 4 juvenile oysters each; from 10
October 2003 to 19 March 2004
Table 4 Analysis of variance (ANOVA) on
effect of predation on survival of juvenile C.
gigas in intertidal and subtidal locations
Intertidal
Cage
Error
Subtidal
Cage
Error
df
MS
F
p
2
46
2939.7
1341.2
2.19
0.123
2
20
218.4
912.9
0.24
0.789
110
Chapter 5
3.2 Feeding preference experiments
Prey choice experiments showed that juvenile and adult Carcinus maenas strongly preferred
mussels to oysters (Table 1, Fig. 5). When offered different size classes of mussels and
Consumed bivalves (%)
Consumed bivalves (%)
100
a
80
60
40
20
0
6 - 8 mm
C. gigas
M. edulis
b
80
60
40
20
0
6 - 8 mm
C. gigas
M. edulis
c
40
20
0
60
10 - 30 mm
10 - 30 mm
C. gigas
M. edulis
d
40
20
0
20
20 - 30 mm
20 - 30 mm
C. gigas
M. edulis
e
15
10
5
0
30 - 40 mm
30 - 40 mm
C. gigas
M. edulis
f
80
60
40
20
0
3-5
mm
6-8
mm
9 - 11
mm
3-5
mm
100
6-8
mm
9 - 11
mm
M. edulis
g
80
60
40
20
0
3-5
mm
6-8
mm
9 - 11
mm
3-5
mm
C. gigas
Consumed bivalves (%)
60
6 - 8 mm
100
C. gigas
Consumed bivalves (%)
100
6 - 8 mm
100
6-8
mm
9 - 11
mm
M. edulis
h
80
60
40
20
0
4-6
mm
6-8
mm
4-6
mm
C. gigas
Consumed bivalves (%)
Consumed bivalves (%)
Consumed bivalves (%)
Consumed bivalves (%)
Consumed bivalves (%)
oysters, smaller individuals were preferred.
100
6-8
mm
8 - 10
mm
M. edulis
i
80
60
40
20
0
20 - 30
mm
35 - 40
mm
C. gigas
20 - 30
mm
35 - 40
mm
M. edulis
Fig. 5 Carcinus maenas. Feeding preference experiments
with different sized shore crabs offered different sized
Crassostrea gigas (grey) and Mytilus edulis (black) as prey.
Given are percent of bivalves consumed crab-1 day-1 (+ SE) in
relation to bivalves offered crab-1 day-1. (a) – (i): different
feeding trials as described in Table 1. Length data on the xaxis show shell length of bivalves. Sizes of crab drawings
indicate different sizes of C. gigas used in experiments
Invasion facilitated by weak predation?
111
Prey choice experiments with Asterias rubens showed that starfish with arm lengths greater
than 20 mm strongly preferred mussels to oysters (Table 2, Fig. 6). Only one feeding trial (c)
with the smallest size class of A. rubens (14 - 17 mm arm length) showed no clear preference
Consumed bivalves (%)
100
a
80
60
40
20
0
6 - 8 mm
C. gigas
M. edulis
b
80
60
40
20
0
50
6 - 8 mm
6 - 8 mm
C. gigas
M. edulis
c
40
30
20
10
0
100
60
40
20
0
C. gigas
100
60
40
20
0
C. gigas
50
d
60
40
20
0
6 - 8 mm 9 - 11 mm 6 - 8 mm 9 - 11 mm
M. edulis
M. edulis
g
40
30
20
10
0
10 - 25
mm
26 - 40
mm
C. gigas
M. edulis
80
C. gigas
f
6 - 8 mm 9 - 11 mm 6 - 8 mm 9 - 11 mm
Consumed bivalves (%)
Consumed bivalves (%)
100
M. edulis
80
6 - 8 mm 9 - 11 mm 6 - 8 mm 9 - 11 mm
C. gigas
e
80
6 - 8 mm 9 - 11 mm 6 - 8 mm 9 - 11 mm
Consumed bivalves (%)
100
6 - 8 mm
Consumed bivalves (%)
Consumed bivalves (%)
Consumed bivalves (%)
Consumed bivalves (%)
for either of the prey species.
10
10 - 25
mm
26 - 40
mm
M. edulis
h
8
6
4
2
0
40 - 50
mm
50 - 60
mm
C. gigas
40 - 50
mm
50 - 60
mm
M. edulis
Fig. 6 Asterias rubens. Feeding preference experiments with different sized starfish
offered different sized Crassostrea gigas (grey) and Mytilus edulis (black) as prey.
Given are percent of bivalves consumed crab-1 day-1 (+ SE) in relation to bivalves
offered crab-1 day-1. (a) – (g): different feeding trials as described in Table 2. Length
data on the x-axis show shell length of bivalves. Size of starfish drawings represent
different sizes of A. rubens used in feeding trials
112
Chapter 5
Large starfish with 102 - 130 mm arm length exclusively fed on M. edulis when given the
choice between M. edulis and C. gigas for 14 days (Fig. 7). When M. edulis were removed
and C. gigas remained as only prey items from day 14 on, they stopped feeding for about 2
weeks until they started to eat increasing amounts of C. gigas up until the end of the
No. of consumed bivalves
experiment at day 51.
40
+
30
M. edulis
C. gigas
20
10
0
1
5
9 13 17 21 25 29 33 37 41 45 49
Time (day)
Fig. 7 Asterias rubens. Laboratory feeding preference experiment with 17 large
starfish (102 -130 mm arm length) together in one aquarium tank. During the first
14 days 100 Mytilus edulis and 100 Crassostrea gigas (30 - 60 mm shell length)
were offered as prey. Consumed bivalves were replaced every day. At day 14,
mussels were removed and from then on 100 C. gigas were the only food items.
Given is the number of consumed bivalves from day 1 to day 51
4 Discussion
This study was conducted in order to assess whether low predation pressure may explain high
survival rates of introduced Crassostrea gigas and may facilitate a competitive advantage
over resident mussels. Predator exclusion experiments revealed high survival rates of juvenile
C. gigas and no significant mortality due to predation. Only recruitment in the subtidal might
have been affected by predation pressure. In laboratory feeding preference experiments it was
demonstrated that two of the main predators in this area, the shore crab Carcinus maenas and
the starfish Asterias rubens, strongly preferred mussels to oysters.
Invasion facilitated by weak predation?
113
4.1 Predator exclusion experiments
The experiment on predation effects on recruitment of C. gigas showed significant effects
only subtidally, where about three times as many recruits survived in the exclusion cages than
in partial and no cage treatments. In the intertidal, however, no clear results were obtained,
because a significant difference occurred only between full cages and partial cages, but not
between full cages and no cages. The experiments on survival of juvenile oysters during the
first months after settlement revealed no differences in mortality between exclusion cages and
partial and no cage treatments in the intertidal as well as in the subtidal location, suggesting
predation to play a minor role for post-settlement mortality. However, caging experiments are
susceptible to misinterpretation due to cage artefacts confounding the results (Connell 1985,
Peterson & Black 1994, Hunt & Scheibling 1997, Anderson & Connel 1999, Strasser 2002).
In most cases, it is not possible to separate effects of differential recruitment versus
differential post-settlement mortality among treatments, because cages may enhance
settlement that will be erroneously interpreted as lower post-settlement mortality (Keough &
Downes 1982). The method of using partial cages to test for caging artefacts is not free of
implications either, because the effects due to caging artefacts and due to the variable of
interest could both occur to some extent within partial cages, but neither to the extent that they
occur in the full cages or no cage treatments (Kennelly 1991). However, a profound
knowledge of the characteristics of the species studied may help to evaluate possible artefacts.
Caging, for example, often leads to changed hydrodynamic conditions that may have an
influence on settlement and survival of sessile species because of sediment accumulation
(Kennelly 1991, Ólafsson et al. 1994, but see also Strasser 2002). In the study at hand, no
enhanced sedimentation on the oyster shells inside cages was observed that could potentially
lead to lower recruitment because of smothering of settlement surfaces (Rothschild et al.
1994). Also, length and growth of juveniles was not affected by cage coverage, except for in
the recruitment experiment in the intertidal location, where juveniles in the no cage treatments
were significantly smaller than in the full and partial cages, supporting the assumption that
this part of the experiment was confounded with cage artefacts. A possible attraction of larvae
by the mesh cover seems to be unlikely, because oyster larvae settle preferentially on the
shells of conspecifics (Diederich in press) and are not capable of byssus drifting (Quayle
1988). Another problem with partial cages is the fact that predators such as shore crabs seek
shelter inside these cages which may lead to a higher predation effect in partial cages
compared to uncaged plots rendering them useless as controls (Strasser 2002). However, in
114
Chapter 5
the study at hand no significant differences in oyster abundance or survival between partial
cages and no cage controls occurred.
In summary, the results obtained by the predator exclusion experiments suggest that low postsettlement predation pressure might be one reason for the high survival rate of juvenile C.
gigas in this area. This has also been observed in a previous study (Diederich submitted)
where about 70% of juvenile C. gigas survived the first three months after settlement on an
intertidal mussel bed and approximately 65% survived their first winter, independent of tide
level. However, the generally lower abundances of juvenile oysters in subtidal compared to
intertidal locations in this area (Diederich in press) may not only be caused by differential
settlement but also by predation pressure acting directly after settlement.
4.2 Feeding preference experiments
To verify the low predation pressure acting on introduced C. gigas, laboratory feeding
preference experiments with two of the main resident predators for juvenile bivalves were
conducted. Both, Carcinus maenas and Asterias rubens strongly preferred mussels to oysters.
Only juvenile starfish < 20 mm did not show a clear preference for mussels. However, it is
important to note that species may behave differently in the field than under laboratory
conditions. Additional food sources, predation, and competition stress may alter foraging
behaviour (Lawton & Zimmer-Faust 1992). For example, juvenile starfish < 10 mm arm
length strongly prefer the very abundant balanid epibionts (Semibalanus balanoides, Balanus
crenatus, Elminius modestus) to mussels (Hancock 1955, Mertel 2002), suggesting predation
pressure exerted by juvenile starfish to be low for oysters as well as for mussels in the field
situation.
The feeding behaviour of C. maenas and A. rubens generally follows the optimal foraging or
energy maximization premise, whereby a predator should choose its diet in order to maximize
net energy intake per unit of handling or feeding time (Elner & Hughes 1978, Hughes 1979,
O’Neill et al. 1983). Size-selective and species-selective feeding of shore crabs and starfish is
well known. When feeding on mussels, a linear increase between crab and preferred prey size
has been observed with crabs generally preferring mussels that are small enough to be easily
crushed (Elner & Hughes 1978, Ameyaw-Akumfi & Hughes 1987). On the other hand, when
feeding on oysters (Ostrea edulis and Crassostrea gigas), large C. maenas (55 - 70 mm
carapax width) showed no preference for any particular size of oyster species within a range
of 10 to 40 mm shell length, which might be explained by weak parts of the more irregular
Invasion facilitated by weak predation?
115
shell where crabs can insert their claws (Dare et al. 1983, Mascaró & Seed 2001). However,
whether the crabs would invest this extra time in the field situation, when they themselves are
in danger of predation, remains doubtful (see Ameyaw-Akumfi & Hughes 1987). Regarding
species selective feeding, it has been shown that shore crabs seem to prefer mussels and clams
to oysters, which has been attributed to the different shell morphology (Dare et al. 1983,
Chew 1998, Mascaró & Seed 2001). However, crabs are able to learn handling skills that may
enable them to feed more effectively on novel and larger prey (Hughes 1979, Cunningham &
Hughes 1984, Kaiser et al. 1993, Hughes & O’Brian 2001). Especially if a suboptimal bivalve
becomes more abundant, a switching of prey preferences may occur (Ameyaw-Akumfi &
Hughes 1987).
For A. rubens, similar size and species-specific feeding patterns have been observed, with
small starfish preferring barnacles and larger individuals showing the following preference
order: mussels Mytilus edulis > slipper limpets Crepidula fornicata > oysters Ostrea edulis
(Hancock 1955, Dolmer 1998, Saier 2001). One reason for this pattern might be explained by
the more irregular, scaly and sharp-edged oyster shell compared to mussel shells that may
hamper attachment of the starfish’s tube feet to the shell. Studies on the impact of epigrowth
on mussel shells on prey selection showed that starfish prefer clean mussels to mussels fouled
with barnacles, possibly because the epigrowth interferes with the feeding mode and hampers
attachment of the tube feet (Laudien & Wahl 1999, Saier 2001).
In summary, the results obtained in the feeding preference experiments stand in line with
previous studies, which highlighted size- and species-selective feeding of C. maenas and A.
rubens. Both predators prefer relatively small and easy to open prey, which leads to a higher
predation pressure on juvenile mussels compared to juvenile oysters. However, as both
predators are able to feed on C. gigas and may improve their opening techniques by learning,
they may switch to C. gigas once these outnumber M. edulis in the Wadden Sea.
4.3 Implications for the invasion success of Crassostrea gigas
Pacific oysters recently started to increase dramatically in abundance and range and are
locally overgrowing resident mussel beds in the Wadden Sea (Dankers et al. 2004, Diederich
et al. in press). The question arose whether the oysters might outcompete the local mussels
and which factors might be responsible for a possible competitive advantage of C. gigas.
Previous studies have shown that the recent strong increase in abundance was caused by high
recruitment success during three consecutive years with high summer water temperatures and
116
Chapter 5
a positive feedback of adult oysters on settlement (Diederich et al. in press, Diederich in
press). A larger size and faster growth compared to mussels, together with high survival rates
that may compensate for recruitment failures, suggest a competitive advantage of C. gigas
over M. edulis (Diederich submitted). The question arose, whether low predation pressure
might explain the high survival rates of C. gigas and might facilitate a possible displacement
of mussels.
Predation may have a profound impact on structuring mussel populations (Seed 1969, Seed &
Suchanek 1992, Strasser 2002). Whereas epibenthic predators like shore crabs and starfish are
important sources of mortality for juvenile mussels in the Wadden Sea (Scherer & Reise
1981, Jensen & Jensen 1985, Dankers & Zuidema 1995, Kristensen & Lassen 1997), adult
mussels are more often preyed upon by birds like eiders Somateria mollissima, oystercatchers
Haematopus ostralegus and herring gulls Larus argentatus (Zwarts & Drent 1981, Hilgerloh
et al. 1997, Nehls et al. 1997). Even though most of these resident predators are known to feed
on oysters in other areas (Korringa 1976, Walne & Davies 1977, Quayle 1988), information
about predation on C. gigas in the Wadden Sea is scarce.
Predation pressure on early juveniles is considered to have a stronger quantitative effect on
population dynamics than predation that acts on later development stages (Reise 1985b,
Gosselin & Qian 1997, Hunt & Scheibling 1997). Therefore, predation by birds is expected to
play a minor role in determining the population dynamics of C. gigas and M. edulis.
However, if predation intensity is very high, birds like herring gulls, oystercatchers and
especially eiders may severely decrease adult mussel densities (Goss-Custard et al. 1981,
Nehls et al. 1997). Only herring gulls are known to have already learned to prey on introduced
C. gigas in the Wadden Sea, however, feeding on oysters was less effective than feeding on
mussels because only about 30% of the oysters were broken by shell-dropping whereas
almost 100% of mussels broke (Cadée 2001). Even though nothing is known about
oystercatchers preying on C. gigas in this area, they might be able to switch to oysters if other
food sources are scarce. The similar sized American oystercatcher Haematopus palliates
feeds predominantly on oysters Crassostrea virginica in Virginia, because of shorter handling
times compared to the mussel Geukensia demissa (Tuckwell & Nol 1997a, b, Crockett et al.
1998). However, the most important bird predator in the Wadden Sea, the eider, is not likely
to switch to oyster prey because of their feeding mode which includes diving and swallowing
mussels whole. This method would not work with sharp edged oysters that are cemented to
Invasion facilitated by weak predation?
117
each other in a solid reef structure. Therefore, predation pressure by birds seems to be
unimportant for oysters while it could deplete adult mussels.
In the intertidal, 0-group C. maenas are the main predators that may limit mussel populations
(Scherer & Reise 1981, Jensen & Jensen 1985, Dankers & Zuidema 1995). From July to mid
October they are very abundant on intertidal mussel beds where they seek shelter from
predation (Klein Breteler 1976, Thiel & Dernedde 1994). A temporal mismatch between the
occurrence of 0-group C. maenas and 0-group bivalves caused by severe winters has been
shown to greatly enhance bivalve survival, including mussels (Strasser & Günther 2001,
Strasser 2002). Settlement of M. edulis in the northern Wadden Sea may take place during the
whole year, but peak settlement occurs from May to September (Strasser & Günther 2001),
which is the time when abundances of juvenile C. maenas are highest (Klein Breteler 1976).
Higher survival rates, that ensure population persistence, mainly occur after severe winters,
when the advent of predators is delayed and in lower densities on the tidal flats (Strasser
2002). The settlement period of C. gigas is confined to a short period in late summer (August
to mid September). At this time, abundance of 0-group C. maenas has already declined (Klee
2001) and the remaining crabs might be too large to feed on small oysters (Fig. 8). This
temporal mismatch between predator and prey may facilitate high survival rates of juvenile C.
gigas even if crabs may learn to feed on this novel prey.
Max. size:
C. gigas
200 – 300 mm
5 - 55 mm
70 – 85 mm
70 mm
M. edulis
10 - 40 mm
30 – 45 mm
J F M A M J J A S O N D J F M A M J J A S O N D J F M A M J J A S O N D
Year 0
Year 1
Year 2
Fig. 8 Schematic diagram of predation pressure by Carcinus maenas on Crassostrea gigas and
Mytilus edulis during different life stages. Bold horizontal lines indicate main settlement period of C.
gigas and M. edulis. Shaded areas indicate time periods when 0-group C. maenas (small crab) and
adult C. maenas (large crab) are present on tidal flats (after Reise 1977). Given are mean shell
lengths of C. gigas and M. edulis during the time periods when C. maenas is present and maximum
shell lengths (shell lengths of M. edulis after Nehls 2003, of C. gigas after Diederich submitted). Bold
arrows indicate high predation, medium arrows medium predation and dotted arrows very low
predation as inferred from feeding trials
118
Chapter 5
During the winter months, shore crabs are absent from the intertidal zone, but adults reappear
in mid April. Then, juvenile mussels will have attained a size of 10 - 20 mm and will grow to
20 - 40 mm by autumn (Nehls 2003). Juvenile oysters grow in the same period from 5 - 35
mm in spring to 35 - 55 mm in autumn (Diederich submitted). Concerning the size- and
species selective feeding preference of shore crabs, the predation pressure on M. edulis is
expected to be much higher than on C. gigas during this time. As large shore crabs are able to
open mussels up to 50 mm shell length (Elner & Hughes 1978, Ameyaw-Akumfi & Hughes
1987), they will not find a size refuge from predation before their third or fourth year of life
(Nehls 2003). Oysters will reach a size refuge much earlier; they may reach 50 mm shell
length during their first year after settlement. However, studies from Britain have shown that
C. maenas can open larger oysters than mussels because of weak parts of the oyster shell,
which enable the crabs to open larger sized individuals (Dare et al. 1983). Large crabs of 75
mm carapax width were able to open oysters of 55 - 60 mm shell length, whereas they could
not feed on mussels > 45 mm (Dare et al. 1983). Nevertheless, these size differences seem to
be of minor importance compared to the much faster growth of C. gigas. In summary, the late
settlement period and fast growth rate of juvenile C. gigas are likely to lead to a temporal
mismatch between predator and prey and an early size refuge from predation. These factors
may facilitate high survival rates even if crabs might switch their feeding preference from
mussels to oysters.
Starfish are voracious predators that may control the distribution and abundance of mussels in
low intertidal and subtidal zones (Seed 1969, Dare 1976, Seed & Suchanek 1992, Kristensen
& Lassen 1997, Saier 2001). They are size-selective feeders and generally prefer mussel size
classes below the maximum size that they are able to open (Reusch & Chapman 1997,
Dolmer 1998). In the study at hand, the largest starfish that occur in the area (120 - 150 mm
arm length) strongly preferred mussels with a shell length of 40 - 50 mm over larger mussels.
However, Saier (2001) showed that large starfish in the Wadden Sea do feed on the largest
mussels available (about 70 mm shell length), indicating that mussels do not reach a size
refuge from starfish predation. However, abundance of A. rubens is highly variable and mass
occurrences alternate with periods of relatively low densities, presumably triggered by food
availability (Dare 1982, Saier 2001). In the Wadden Sea, the erratic distribution of A. rubens
and the preference for barnacles as prey items by juvenile starfish reduces the direct impact of
starfish predation on mussel populations (Saier 2001). However, as juvenile starfish prey
severely on barnacles, they have an indirect negative effect on mussel recruitment, because
Invasion facilitated by weak predation?
119
barnacle epigrowth strongly enhances mussel recruitment (Navarette & Castilla 1990, Saier
2001, Diederich in press). As oyster recruitment does not depend on the presence of barnacles
(Diederich in press), this indirect negative effect of starfish predation does not affect C. gigas.
Species-selective feeding of shore crabs and starfish may facilitate a competitive advantage of
C. gigas over M. edulis. As predation pressure on juvenile oysters is low, they show high
survival rates that may compensate for years with low recruitment success due to
unfavourable environmental conditions such as cold summer water temperatures. Mussels, on
the other hand, are strongly limited by predation pressure. High recruitment success is
therefore erratic depending on low predator densities, normally in the wake of a cold winter.
Under the premise that the invasion success of C. gigas will continue and mussels will
become more and more displaced by oysters, they might experience an ever-increasing
predation pressure because the remaining mussels are the preferred prey. However, as C.
maenas and A. rubens are both able to feed on oysters, they might at some stage switch to
oyster prey. It has been shown that C. maenas is able to adapt to larger sized prey by
developing larger crusher claws (Smith 2004). Nevertheless, as oysters reach an early size
refuge from predation and are a less profitable prey because of longer handling times, a
possible regime shift from mussel beds to oyster reefs may impair predator performance.
Unfortunately, there is a lack of information about predation pressure on C. gigas in its native
habitat of Japan and Korea. However, as these areas host very large predatory crabs like
Scylla serrata, it is likely that C. gigas is subjected to higher predation pressure in its native
habitat than at the temperate Atlantic and North Sea coasts (Vermeij 1977). For example,
Crassostrea virginica, a native to the east coast of the United States with similar shell
morphology as C. gigas, is subjected to heavy predation by the large crab Callinectes sapidus
(carapax width up to 190 mm) and Menippe mercenaria (carapax width up to 128 mm;
Menzel & Hopkins 1955, Vermeij 1977, Bisker & Castagna 1987, Egglestone 1990). At the
North Sea coasts, C. maenas (maximum carapax width 75 mm) and Cancer pagurus
(maximum carapax width 250 mm) are the largest crab species, however, the latter is rare and
confined to subtidal parts of rocky shores (Hayward & Ryland 1995). Even if a local trend
towards an increase of C. pagurus densities will continue (Buschbaum, pers. observation),
they would most likely first decimate subtidal mussel populations before switching to oyster
prey, because they also prefer mussels to oysters (Mascaró & Seed 2001).
120
Chapter 5
5 Conclusion
It is concluded that low predation pressure by the main benthic predators, Carcinus maenas
and Asterias rubens, will facilitate a competitive advantage of C. gigas over M. edulis.
Whereas mussel populations are strongly limited by predation pressure and depend on high
recruitment success during years when predator abundances are low, the high survival rates of
juvenile and adult C. gigas may facilitate population persistence and growth even if cold
summers lead to low oyster settlement. A possible regime shift with mussel beds being
largely replaced by oyster reefs may have profound impacts on the Wadden Sea food web.
Acknowledgements
I would like to thank the writing circle of the Wadden Sea Station Sylt and especially K.
Reise for valuable comments on the manuscript. Thanks also to D. Schmidt, K. Scheuer and
B. Lafargue for their help in the laboratory and field.
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General Discussion
127
6 General Discussion
Different aspects of spread and niche occupation of introduced Pacific oysters were
highlighted in the previous chapters. It was shown that high recruitment success is facilitated
by high summer water temperatures, a positive feedback of adults on settlement, and low
predation pressure by resident predators. In addition, high growth and survival rates found in
different locations suggest a broad ecological niche. Comparisons with resident blue mussels
indicate that C. gigas might be a stronger competitor if space and/or food are limiting, mainly
because of higher survival and growth rates, and less predation pressure. In the general
discussion these results will be combined in order to generate an overall picture of possible
impacts of C. gigas on the recipient community.
6.1 Factors facilitating the establishment of C. gigas
Pacific oysters are habitat generalists with a broad environmental range (Quayle 1988). They
have been distributed to various parts of the world due to aquaculture activities, and in many
locations wild oyster populations have established soon after oyster farming had commenced
(e.g. Korringa 1976, Andrews 1980, Quayle 1988, Chew 1990). C. gigas is able to reproduce
and grow in salinities of 14 - 32 psu, and to settle in intertidal as well as in subtidal locations
of rocky coasts and sandy flats (Quayle 1988, Mann et al. 1991, de Kluijver & Leewis 1994,
Leewis et al. 1994). They are able to grow in temperatures ranging from 5 to 35°C and to
survive temperatures as low as -5°C; however, for reproduction they need more than 20°C
(Korringa 1976, Buroker 1985, Mann et al. 1991). Together with an r-selected life history trait
(high fecundity and dispersal capacity, fast growth), the broad environmental tolerances
predispose C. gigas as a species likely to be a successful invader (Lodge 1993, Williamson &
Fitter 1996, McMahon 2002).
In addition, aquaculture seems to be a very efficient vector that leads to a high probability of
species becoming established in the recipient habitat (Reise et al. 1999, Naylor et al. 2001).
The continuous input of larvae from the local oyster farm will surely have facilitated the
invasion of C. gigas. Young oysters are imported regularly from hatcheries in England and
Ireland, and placed on the culture plot where they grow to marketable size. When the oysters
128
Chapter 6
found suitable conditions for reproduction, natural spatfalls occurred and oysters settled in the
wild. Due to the general aquaculture practice to crossbreed different strains in order to select
for preferable characteristics, a high genetic variability within the newly established
population can be assumed (Quayle 1988). This is important because it prevents that genetic
drift caused by a population bottleneck due to a small number of initial colonists will lead to a
low genetic variability within the new population (Sakai et al. 2001). A reduced genetic
diversity would then limit population growth and the likelihood of persistence because it
reduces the potential of the population to evolve (Sakai et al. 2001, Cox 2004).
Another factor that may have facilitated the establishment of C. gigas within the area is the
location of the aquaculture plot in the List tidal basin, an almost enclosed bay. High larval
retention will certainly facilitate the establishment of a species with a planktonic larval stage
because it prevents the larvae to drift away from suitable habitats. Therefore, even low initial
numbers of larvae may be sufficient to allow a population to increase.
The recipient habitat, namely the Wadden Sea, is a very dynamic and relatively young habitat
that exists in its present state only since about 7,000 years. No endemic species have evolved
and species richness is relatively low, suggesting the presence of empty habitats and free
resources for invading species (Reise 1985, Armonies & Reise 2003). In addition,
disturbances like storms and ice winters frequently lead to a change in species abundances
and composition (Beukema 1992, Nehls & Thiel 1993, Strasser et al. 2001). These factors,
low species richness, free resources, and frequent disturbances, are considered to enhance the
invasibility of an ecosystem (Elton 1958, Crawley 1987, Lodge 1993, Stachowics et al. 1999).
In fact, even though about 80 nonindigenous species are established in the North Sea, they
have driven no native species to extinction; the exotics are rather considered as an addition to
the resident community (Reise et al. 2002). Nevertheless, exotic species irreversibly changed
the North Sea ecosystem, and as the rate of successful introductions is still increasing, there is
a severe risk of new invaders becoming established that may have negative impacts on
ecosystem functioning and/or human health (Reise et al. 2002). In addition, the increasing
number of established exotics may facilitate the invasion by other species, a phenomenon that
is called invasional meltdown (Simberloff & Von Holle 1999).
In summary, the successful establishment of C. gigas in the northern Wadden Sea may have
been facilitated by species-specific characteristics of the invader, by an efficient vector, and
by characteristics of the recipient habitat that renders it susceptible to invasion (see Box 1).
General Discussion
129
Box 1 Generalisations about biological invasions applied to the invasion of C. gigas in
the northern Wadden Sea
(after Crawley 1987, Di Castri 1990, Lodge 1993, Williamson & Fitter 1996, Sakai et al. 2001,
McMahon 2002, Shea & Chesson 2002).
Characteristics of a successful invader:
r-selected trait (high fecundity, high dispersal and growth rate)
habitat generalist
high genetic variability
Efficient vector:
continuous input of larvae
no population bottleneck
Recipient habitat with characteristics of high invasibility:
free habitat and resources, low species richness
high disturbance rate
C. gigas
Yes
Yes
Yes
Aquaculture
Yes
Yes
Wadden Sea
Yes
Yes (ice, storms)
6.2 Spread of C. gigas in the northern Wadden Sea
In 1991, 5 years after the local oyster farm had started its business, the first wild oysters were
found on intertidal mussel beds about 6.5 km north of the culture plot (Reise 1998). However,
the expansion of the wild oyster population in the List tidal basin started off slowly. In 1995,
14 out of 17 investigated mussel beds contained living C. gigas, but mean abundances
remained low (3.6 individuals m-2; Reise 1998). By 1999, all mussel beds in the area were
colonised by C. gigas, but densities were still on a low level (3.7 individuals m-2). Only after
three consecutive years with high recruitment success (2001, 2002, and 2003), a massive
population increase occurred with mean densities of 126 individuals m-2 and maximum
densities of over 300 oysters m-2 on single mussel beds in 2003 (chapter 2). In 2004, about
2000 - 3000 t oyster biomass were calculated for the List tidal basin; in comparison, mussel
biomass was about 3000 t (G. Nehls and own unpubl. data).
The colonisation of the subtidal zone occurred much slower and up until 2004 only scattered
oysters were found in subtidal locations. However, in 2004, spatfall was observed on former
mussel culture plots, indicating that C. gigas is able to colonise subtidal habitats and might be
able to generate subtidal oyster reefs as has happened in the Oosterschelde (The Netherlands,
Kater & Baars 2003) and in the Dutch Wadden Sea near Texel (N. Dankers, pers. comm.).
130
Chapter 6
Outside the List tidal basin, abundances of C. gigas are still low although the oyster
population did spread north- and southwards along the coastline. Only on one intertidal
mussel bed east of the island of Amrum (about 40 km south of the List tidal basin)
abundances of over 150 oysters m-2 were recorded in summer 2004 (G. Nehls, unpubl. data).
In summary, the wild oyster population in the northern Wadden Sea increased slowly. It took
about 17 years until a population of several million oysters became established, even though
C. gigas is a species with an r-selected life history trait that includes high fecundity and
dispersal capacities (Quayle 1988). The main reason for the relatively slow expansion is the
fact that high recruitment events were erratic and occurred only in years with abnormally high
summer water temperatures (1991, 1994, 1997, 2001, 2002, and 2003). Therefore, climatic
conditions are considered to play a key role in determining the future population development
of C. gigas in the northern Wadden Sea. That C. gigas is a reef building species that creates
its own habitat might be another reason for a so called lag period, which is a common
phenomenon in invasion processes and describes the time between the initial colonisation and
the onset of rapid population increase (Sakai et al. 2001). As the oysters settle preferentially
on conspecifics, a positive feedback of adults on recruitment is assumed with higher
recruitment proportional to the amount of oysters already present (chapter 3).
6.3 Interaction with recipient community
In order to assess the future development of the oyster population and possible impacts on the
recipient ecosystem, the study of biotic interactions with the native community is essential.
Unfortunately, I have no information on the population ecology of C. gigas in its native
habitat from Japan to Taiwan. Therefore, a comparison of species interactions in the native
habitat versus the introduced habitat is not possible at this stage, even though the importance
of home and away comparisons is unquestionable (Lohrer et al. 2000, Hierro et al. 2005).
In the Wadden Sea, C. gigas is not invading free habitat patches, but is settling on top of
epibenthic mussel beds Mytilus edulis (Reise 1998). These are centres of high species
richness, biomass, and production, and represent the only extensive habitat for sessile
organisms (Seed & Suchanek 1992). In addition, mussels and their associated organisms are
an important food resource for various benthic predators, fish, birds, and humans (Dankers &
Zuidema 1995, Nehls et al. 1997, Saier 2001). Therefore, C. gigas is invading a complex
General Discussion
131
community, and various interactions with resident species are likely to occur that determine
the impact of C. gigas on the recipient ecosystem.
6.3.1 Spatial coexistence of C. gigas and M. edulis
Pacific oysters are large, suspension-feeding bivalves that need hard substrates for settlement.
As mussel beds are the only extensive hard substrata available on the mud and sand flats of
the Wadden Sea, the oysters are attaching themselves to the shells of living and dead mussels.
Therefore, competition for space and food may occur, if these resources are limiting. Space is
not considered a limiting factor in the Wadden Sea in general; however, habitat for sessile
organisms is restricted to mussel beds and therefore scarce. Mussel beds are very stable and
may persist for decades provided that no mussel fishery occurs (Obert & Michaelis 1991,
Reise et al. 1994, Dankers et al. 1999). However, stochastic events such as ice scouring and
storms may severely damage and dislodge mussel beds (Obert & Michaelis 1991, Nehls &
Thiel 1993, Strasser et al. 2001). Therefore, mussel beds are generally confined to semiexposed locations, where they are sheltered from wave action, but where currents are still
high enough to guarantee adequate food supply (Brinkman et al. 2002). In addition, a tidal
zonation is apparent, because locations too high up the shore are less favourable because of
food limitation by short submersion periods and by desiccation stress, and the locations at or
below the low water line are susceptible to heavy predation by crabs and starfish (Seed &
Suchanek 1992, McGrorty et al. 1993, Saier 2001, Brinkman et al. 2002). That suitable
habitat for stable mussel beds may be limited in the Wadden Sea is supported by the fact that
mussel beds that were destroyed often reappear at the same location (Obert & Michaelis
1991).
High mussel recruitment, however, is rare and confined to years when predator densities
happen to be low, usually following severe winters (Beukema 1992, Beukema et al. 2001,
Strasser et al. 2001). High oyster recruitment, on the other hand, is facilitated by high summer
water temperatures (chapter 2); post-settlement mortality due to predation seems to play only
a minor role (chapter 5). Therefore, a succession of warm summers as has recently occurred
(2001, 2002, and 2003) is expected to lead to an overgrowth of mussel beds by C. gigas and
to a transition from mussel beds to mixed beds and finally to oyster reefs (Fig. 1). However, a
dense cover of Fucus vesiculosus that frequently occurs on intertidal mussel beds reduces
oyster settlement and may provide a spatial refuge for M. edulis, albeit under suboptimal
conditions. The next cold winter may then lead to high mussel recruitment and to an
132
Chapter 6
overgrowth of oyster reefs by M. edulis. As mussels have a high reproductive capacity, they
may reach a strong population increase even if numbers of adults are low (Seed 1975, Sprung
1983). However it may be possible that mussel recruitment will be reduced on oyster reefs,
because of predation by oysters that filter mussel larvae from the water column (Troost 2004).
Furthermore, biotic interactions like food competition and high predation pressure might
repress the overgrowth of mussels on oyster reefs even if initial recruitment success is high.
Recruitment
Mussel bed
Mixed bed
High oyster
recruitment
Storms,
waves
Oyster reef
High mussel
recruitment
Mixed bed
Oyster reef
Storms,
waves
High mussel
recruitment
?
Mixed bed
>
Hot summer
Oyster reef with variable
mussel epigrowth
Cold winter
Fig. 1 Schematic diagram of the possible development of intertidal mussel beds and oyster reefs
based on differential recruitment success of Crassostrea. gigas and Mytilus edulis. High oyster
recruitment is facilitated by high summer water temperatures and the presence of conspecifics,
whereas mussel recruitment is facilitated by low predator densities after sever winters and the
presence of barnacles. The future development will primarily depend on climatic conditions. Climate
change leading to a higher frequency of hot summers and a lower frequency of cold winters will favour
the dominance of oyster reefs
General Discussion
133
As climatic conditions seem to be important for determining recruitment success of both,
oysters and mussels, a possible climate change leading to warmer summers and milder
winters in the wake of an increasing North Atlantic Oscillation index (Roeckner 2001,
Meincke et al. 2003), will favour the development of oyster reefs that may contain a variable
amount of mussel epigrowth depending on recruitment success in different years.
Whether or not mussels may find a spatial refuge higher in the intertidal zone will depend on
different tolerances towards desiccation and freezing temperatures. Zonation as a consequence
of predation or interspecific competition is a well known phenomenon on rocky shores (e.g.
Connell 1961, Underwood 1992, Paine 1994). For example, M. edulis finds a spatial refuge
from competition with M. galloprovincialis by settling higher on the shore at the coast of
Washington (Suchanek 1981), and barnacles Balanus balanoides avoid competition with M.
edulis by settling in the upper intertidal where only Balanus can exist (Peterson 1979).
However, even though a zonation with mussels remaining higher up the shore and oyster reefs
emerging in the lower intertidal zone is apparent in some locations in the northern Wadden
Sea, further studies are needed to test for performance of both species under suboptimal
conditions that prevail in the high intertidal zone.
Another interesting aspect is the fact that C. gigas might be able to create its own habitat on
the sandy flats of the Wadden Sea. Especially in years with high barnacle abundances on
oyster and mussel shells, juvenile oysters are often not attached to the bivalve, but to barnacle
shells. Subsequently, the barnacles become overgrown, die, and get easily detached from their
basibiont. Then, the young oysters are without substrate and are prone to drift with the
currents away from the mussel bed. Oysters attached to dead barnacle shells are frequently
found on the sand flats of the Wadden Sea (Fig. 2). There, they seem to survive and grow well
because they do not sink even into muddy
sediments and can free themselves from
sediment cover (own unpubl. data). The
species selective settlement of oyster larvae
– they settle preferentially on conspecifics
– may then lead to the generation of oyster
reefs on formerly bare sand flats. Storms
may act in the same way and may lead to
Fig. 2 Juvenile C. gigas attached to dead
barnacles
dislodgement not only of mussel clumps
(Nehls & Thiel 1993), but also of oysters,
134
Chapter 6
thereby facilitating the creation of new reef structures. The generation of new oyster reefs on
formerly bare sand is expected to be strongly facilitated by low predation pressure on juvenile
oysters. The development of new mussel beds, on the other hand, is considered to be limited
firstly by unfavourable conditions like currents being too strong or too low (Brinkman et al.
2002), and secondly by predation, because juvenile mussels are subjected to high predation
pressure and the bare sand flats provide no spatial refuges from predation (Scherer & Reise
1981, Revelas 1982, Dankers & Zuidema 1995, Frandsen & Dolmer 2002). As oyster reefs
might be more stable and resistant to high currents, storms and ice scouring, they may
develop on areas that are not suitable for mussel beds, suggesting that oyster reefs may
potentially become more abundant than mussel beds have ever been.
In the subtidal zone, the situation might be different, because of different factors influencing
population dynamics. For example, higher predation pressure and stronger currents than in the
intertidal are known to limit subtidal mussel populations (Kitching et al. 1959, Ebling et al.
1964, Seed 1993, Saier 2001, Brinkman et al. 2002). In the List tidal basin, recruitment of C.
gigas was much lower in shallow subtidal compared to intertidal locations (chapter 3), which
may partly be explained by higher predation pressure on early recruits (chapter 5). Another
reason could be differential settlement of C. gigas that is widely considered as an intertidal
species and might be limited by cold water or high currents in the subtidal zone (Buroker
1985, Quayle 1988, Arakawa 1990). However, as the oysters suffer much less predation
pressure compared to mussels, they are likely to be able to survive and grow well in subtidal
locations. This is supported by the fact that single adult oysters are frequently found in the
subtidal zone and that in 2004 the first significant subtidal spatfall was recorded with
juveniles being attached to dead shells and to scattered adult oysters. Therefore, the
development of subtidal oyster reefs as has occurred in the Oosterschelde (western
Netherlands; Kater & Baars 2003) is expected, albeit with a longer lag phase than in the
intertidal zone.
In summary, oyster reefs are expected to develop in intertidal as well as in subtidal locations.
Whether or not mussels will be able to recolonise oyster reefs in high recruitment years needs
to be awaited because the last high recruitment event of M. edulis dates back to 1996 (Nehls
2003). However, the mussels may find a spatial refuge in the high intertidal zone provided
that they are better adapted to the suboptimal conditions prevailing there.
General Discussion
135
6.3.2 Is C. gigas a stronger competitor than M. edulis?
High survival rates of juvenile and adult C. gigas and the ability to reach an old age on mussel
beds as well as on sand flats are assumed to guarantee population persistence and growth even
if ‘cool’ summers will lead to low oyster recruitment during most years. A competitive
displacement of native mussels may occur if C. gigas is a stronger competitor for limiting
resources. As mentioned above, space might be a limiting factor, however, as both species
show high fecundity and dispersal capacities and are able to settle on top of each other,
coexistence may be possible. Nevertheless, the stronger competitor might displace the weaker
congener to less favourable habitats and may cause a severe population decline.
Comparisons of life-history characteristics of C. gigas and M. edulis may allow tracing
possible competitive advantages (summarised in Table 1). Both species are habitat generalists
with a broad global distribution (e.g. Quayle 1988, Gosling 1992). However, as mentioned
above, C. gigas is at its northern distributional limit in the Wadden Sea, because the oysters
need about 20°C water temperature for successful reproduction (Korringa 1976, Mann 1979,
Buroker 1985).
Table 1 Summary of life history characteristics of Crassostrea gigas and Mytilus edulis as derived
from literature
Life history trait
C. gigas
M. edulis
Tolerance to abiotic factors
Habitat generalist
Habitat generalist
Adapted to climatic conditions
of the Wadden Sea
Yes, but northern limit of distribution
Yes
Size and life span
Max. size: 30 cm
Max. age: ~ 30 years
Max. size: 7 cm
Max. age: ~ 20 years
50 - 100 million eggs per female
rapid (30 - 70 mm during 1st year)
1 year
7 - 8 million eggs per female
rapid (10 - 30 mm during 1st year)
1 year
Dispersal rate
High
(planktonic larval period: 3 - 4 weeks)
High
(planktonic larval period: 1 - 4 weeks,
secondary byssus drifting possible)
Relative juvenile survivorship
High
Low
(exception: low predator densities
after cold winters)
Predation pressure
Low
High
Resistance to disturbances
(ice scouring, storms)
High
(solid reef structure)
Medium
(mussel beds dislodged by ice and
storm)
r-selected life history traits:
high fecundity,
high growth rate
early maturity
136
Chapter 6
Oysters and mussels are both long-living, but C. gigas is much larger and reaches about 3 to 4
times the size of M. edulis. Both bivalves have a high dispersal capacity due to an extended
larval period, but C. gigas has a higher fecundity with adult females releasing 50 - 100 million
eggs whereas large mussels produce only 7 - 8 million eggs (Quayle 1988, Seed & Suchanek
1992).
One important difference between oyster and mussel recruitment is the fact, that oyster
settlement is confined to a short period from late July to early September, whereas mussel
settlement may occur year round with the main peak in spring and minor peaks in summer
and/or autumn (Pulfrich 1995, Strasser & Günther 2001). This may in part explain the low
predation pressure on juvenile oysters, because a temporal mismatch between predator
abundances and oyster recruitment is assumed (chapter 5). Studies on biological factors
affecting recruitment of C. gigas and M. edulis revealed that oyster recruitment is facilitated
by the presence of conspecifics, while mussel recruitment is enhanced in the presence of
barnacle cover (Fig. 4). A dense layer of the brown macroalga Fucus vesiculosus reduced
recruitment of both, mussels and oysters (C. Buschbaum unpubl. data and chapter 3).
However, as survival rates of newly settled oysters are very high (about 70% survived their
first three months on the mussel bed), presumably due to low predation pressure, the oysters
are expected to be stronger competitors compared to mussels and to be able to increase even if
number of recruits are still low.
A regular plankton survey (10 l seawater sampled per day) revealed that abundances of C.
gigas larvae are increasing in the List tidal basin since 2002, when the first oyster larvae were
found (8 individuals in total). In 2003, 27 larvae were recorded and in 2004 the number of
larvae increased even further (M. Strasser, pers. comm.), reflecting the increasing oyster
Juvenile C. gigas / shell
recruitment that has been observed on spat collectors (Fig. 3).
Fig. 3 Abundance of Crassostrea gigas recruits on spat
collectors made from dead oyster shells (mean + SE, n
= 6 collectors with 8 shells each) on two intertidal
mussel beds (KH and MM) in August 2002, 2003, and
2004.
12
8
4
0
KH
MM
2002
KH
MM
2003
KH
MM
2004
General Discussion
137
Growth experiments revealed a much higher growth rate of C. gigas compared to M. edulis
(chapter 4). Whereas 1-year-old mussels reach about 10 - 30 mm shell length on intertidal
mussel beds (Nehls 2003), oysters will grow to a length of about 30 - 70 mm. In addition,
growth of C. gigas was neither affected by barnacle overgrowth nor by the presence of
mussels and oysters (Fig. 4). Mussel growth, on the other hand, is reduced due to barnacle
cover (Buschbaum & Saier 2001), and the presence of mussels and oysters, indicating
competitive inferiority. A larger size paired with a filtration rate an order of magnitude higher
– medium sized oysters of 90 - 100 mm shell length reach filtration rates of 30 l h-1 (Quayle
1988) whereas large mussels of 50 - 70 mm filter about 3 l h-1 (Davenport & Woolmington
1982) – will be of competitive advantage if food limitation is occurring in dense aggregations
of suspension feeders. Especially in low current situations food depletion may occur directly
above mussel beds (Dame et al. 1984, Fréchette et al. 1989, Peterson & Black 1991). In
addition, if the trend towards decreasing eutrophication leading to reduced phytoplankton
biomass is continuing (van Beusekom et al. 2005), food competition may become more
important as carrying capacity for filter feeders declines. However, a different feeding
behaviour and possibly also different food sources utilised by C. gigas and M. edulis lead to
the assumption that mussels and oysters are not necessarily strong competitors (Bougrier et al.
1997, Riera et al. 2002). Whether or not C. gigas and M. edulis may compete for food in the
Wadden Sea will need further study, because it is difficult to transfer results from
physiological laboratory experiments to the actual field situation.
Another advantage of faster growth and larger size is an early size refuge from predation,
because most benthic predators are size-selective feeders which prey preferentially on food
items that promise optimal energy gain (Elner & Hughes 1978, Hughes 1979). Lack of
predation pressure by resident mussel predators is considered to be a main reason for the
observed high survival rate of juvenile and adult oysters (chapter 5). Species- and sizeselective feeding of crabs (Carcinus maenas) and starfish (Asterias rubens) which both
strongly prefer mussels to oysters, will certainly give C. gigas a competitive advantage,
because mussel populations are known to be strongly limited by benthic predation (Seed
1969, Seed & Suchanek 1992, Dankers & Zuidema 1995, Saier 2001, Strasser 2002). In
addition, birds like eiders Somateria mollissima, herring gulls Larus argentatus, and
oystercatchers Haematopus ostralegus may severely decrease adult mussel densities (GossCustard et al. 1981, Nehls et al. 1997). However, even though herring gulls learned to feed on
138
Chapter 6
C. gigas (Cadée 2001), their impact on oyster densities is considered to be low, especially if
oysters are cemented to each other in massive reefs.
Epibionts
I Recruitment
Substrate
Substrate
Predation
Epibionts
II Growth
0
0
Substrate
0
Substrate
Fig. 4 Biotic factors affecting recruitment (I) and growth (II) of Crassostrea gigas and Mytilus edulis.
Positive effects (+) are marked in red, negative (-) and neutral (0) effects are marked in black. Thick
arrows indicate strong effects, thin arrows weaker effects
General Discussion
139
Nevertheless, whether or not birds will be able to use oysters as a food resource needs further
study, especially in the face of impacts that a possible shift from mussel beds to oyster reefs
might have on bird populations that use the Wadden Sea as an essential feeding ground.
In conclusion, C. gigas seems to be the stronger competitor compared to M. edulis, especially
because of high survival rates due to low predation pressure. However, as food and space is
abound in the Wadden Sea ecosystem, not a displacement, but a shift in dominances is
expected with oyster reefs becoming abundant in intertidal and possibly also in subtidal
locations and mussels being mainly restricted to the existence as one of many epifauna
species on oyster reefs. Their densities are expected to vary according to recruitment success
in different years, a well known phenomenon known for many bivalves in the area (Strasser et
al. 2001, Strasser 2002). A similar phenomenon occurs in the Sea of Japan, where
Crassostrea reefs are subjected to a succession of epifauna communities dominated by
barnacles (Balanus improvisus) and mussels (Mytilus trossulus) that settle on the oyster shells
during summer and die off in winter (Zvyagintsev 1992). In late fall, the oyster reef may look
like a mussel bed due to the heavy overgrowth and in spring the oyster reef comes back into
view after the mussels have died off (Zvyagintsev 1992).
6.3.3 Impacts on the Wadden Sea ecosystem
A possible regime shift with mussel beds being largely replaced by oyster reefs may have
profound impacts on ecosystem dynamics and functioning. First of all, a different associated
community may develop on oyster reefs. Even though oyster reefs are known to harbour a
diverse associated community by providing settlement surfaces for sessile species and shelter
for mobile organisms (Arakawa 1990, Zvyagintsev 1992, Soniat et al. 2004), their structure
differs from mussel beds, because the oysters are larger and they are forming more solid reef
structures by cementing themselves to each other. Mussel beds, on the other hand, are more
dynamic because mussels are able to move with their foot and byssal threads. This is expected
to have impacts on organisms seeking shelter form predation in between and underneath the
mussels and that may not find suitable hideouts in oyster reefs. For example juvenile shore
crabs (< 10 mm carapax width) are more abundant on mussel plots compared to oyster plots,
whereas larger shore crabs were more abundant on oyster plots (own unpubl. data). For sessile
species like barnacles, however, no significant differences in abundances between oyster and
mussel substrate were found (S. Görlitz and own unpubl. data). In general, the composition
and diversity of epi- and endobenthic species did not differ between intertidal oyster reefs and
140
Chapter 6
mussel beds (S. Görlitz, unpubl. data). However, the brown macroalga Fucus vesiculosus that
may cover mussel beds in dense layers and supports various herbivores and increases overall
macrobenthic diversity (Albrecht & Reise 1994, Albrecht 1998) will be missing on oyster
reefs because it lacks a holdfast and is attached to the mussel bed only by the mussels’ byssal
threads. Therefore, the occurrence of these algae depends on the presence of mussels.
However, a recent invader in the Wadden Sea, the Japanese seaweed Sargassum muticum
readily grows on oyster shells in the shallow subtidal and hosts a more diverse associated
community than F. vesiculosus (Buschbaum in press).
To follow up a possible development of subtidal oyster reefs would certainly be very
interesting, because it may facilitate the establishment of an associated community that may
be similar to the one that existed on the former reefs of the native European oyster Ostrea
edulis, which became extinct in the Wadden Sea at the start of the 20th century (Möbius 1877,
1893, Hagmeier & Kändler 1927, Hagmeier 1941, Reise 1982). However, it has to be taken
into account that O. edulis was restricted to the subtidal habitat and possessed different life
history characteristics than C. gigas, such as smaller size (maximum size about 12 cm), lower
fecundity and dispersal capacity, and lower temperature and salinity tolerance (Möbius 1877,
Korringa 1952, Mann 1979, Andrews 1980, Buroker 1985). Therefore, the establishment of
C. gigas cannot be considered as a substitute for the loss of O. edulis. Especially as C. gigas is
much larger, it may have different impacts on the food web because of higher filtration
capacity and lower risk of predation (Walne & Mann 1975, Korringa 1976, Dean 1979, Mann
1979).
If oysters will become superabundant in the Wadden Sea, the higher filtration rate of oysters
may have impacts on food availability for other suspension feeders, like mussels, cockles
(Cerastoderma edule), and clams (Macoma balthica, Mya arenaria). In addition, oyster reefs
may become more abundant than mussel beds have ever been, mainly because of a presumed
wider ecological niche. Even though at present food is not considered to be a limiting factor
for suspension-feeding bivalve populations, and only locally food depletion may occur
directly above dense aggregations of filter feeders (Fréchette & Bourget 1985, Fréchette et al.
1989, Peterson & Black 1987, 1991), a massive increase in oyster abundances may lead to a
depletion of phytoplankton in the water column (Dame & Prins 1998). In addition, decreasing
phytoplankton biomass caused by reduced riverine nutrient inputs (van Beusekom et al. 2005)
may contribute to food limitation. Therefore, food competition between C. gigas and other
filter feeders may occur, as is assumed for cockles and oysters in the Oosterschelde (The
General Discussion
141
Netherlands; Geurts van Kessel et al. 2003) and for the oyster cultivation area of MarennesOléron bay in France (Sauriau et al. 1989). A possible top-down control of phytoplankton
biomass may modify benthic-pelagic coupling by forcing a shift from pelagic to benthic
consumers because of food depletion in the water column (Leguerrier et al. 2004). However,
as the oysters release nutrients into the water column, phytoplankton productivity may
increase (Righetti 1999, Mazouni et al. 2001). In addition, pseudofaeces production may
increase food for meiofauna that in turn provides food for juvenile and adult nekton
(Leguerrier et al. 2004). In oyster cultivation areas in France high oyster densities caused a
severe decline in macrofauna and zooplankton but enhanced bacteria, microfauna and
meiofauna which in turn promoted the more active trophic fluxes towards birds and nektonic
fishes (Leguerrier et al. 2004).
As the oysters suffer very low predation pressure in the Wadden Sea, a possible regime shift
with oysters dominating the benthic filter feeding population may have profound impacts on
the food web, because oysters may constitute a more or less dead end in the food chain (Fig.
5). However, it has to be taken into account that benthic predators like shore crabs and starfish
as well as herring gulls are known to feed on C. gigas in other countries and may learn to feed
on novel prey (Korringa 1976, Walne & Davies 1977, Quayle 1988, Cadée 2001). In addition,
as the associated community of oyster reefs and mussel beds is not expected to differ in great
extent, their impact on the food web will not change. Nevertheless, large oysters are not
expected to be preyed upon by any of the resident predators and if C. gigas will once
constitute the majority of the benthic biomass, their large filtration capacity will transfer most
of the primary production into oyster reefs. A possible decline of benthic predators may have
impacts on higher levels of the food web such as migratory birds. For example, in the Dutch
Wadden Sea the declining cockle populations have caused a severe decrease in oyster catcher
abundances (Verhulst et al. 2004).
However, these predictions are drawn from studies on the present situation and may not be
valid for processes that may occur once a regime shift has occurred, because then other
interactions may appear whose outcome is impossible to predict. Many introduced species
experience a boom phase with a massive population increase that is followed by a bust period
when abundances decline and remain on a low level from then on (Simberloff & Gibbons
2004). The reasons for the population crash often remain unknown, however, predation or
competition by subsequently introduced species is frequently considered as a likely cause. For
example, in the Black Sea the arrival of a predatory ctenophore (Beroe ovata) may have
142
Chapter 6
caused a decline of the previously introduced comb jelly Mnemiopsis leidyi and therewith
contributed to the recovery of the ecosystem (Kideys 2002, Bilio & Niermann 2004).
However, the recipient ecosystem may also adapt to the invader (Cox 2004). For example,
resident species may evolve new characteristics like growing larger or learning new prey
handling skills (Townsend 1996, Trussel 2000, Hughes & O’brian 2001, Smith 2004).
PHYTOPLANKTON
PHYTOPLANKTON
Fig. 5 Simplified food chain in the Wadden Sea. Before the introduction of Crassostrea
gigas (left): mussels feeding on phytoplankton and being preyed upon by starfish, crabs
and birds. After a possible regime shift (right): large oyster reefs replacing other filter
feeders and taking up most of the phytoplankton biomass. Low predation pressure on C.
gigas may lead to declining predator densities (including birds) and a transformation of
the Wadden Sea ecosystem
In comparison, previously introduced filter feeders, the American slipper limpet Crepidula
fornicata and the American razor clam Ensis americanus, did not cause major changes in the
Wadden Sea ecosystem. C. fornicata was introduced with American oysters in the 1870s and
now inhabits shallow subtidal zones. However, even though slipper limpets reduce survival
and growth of mussels if attached to mussel shells, their abundances are limited by high
mortality in cold winters (Thieltges et al. 2004, Thieltges 2005), which reduces their overall
impact. Ensis americanus, on the other hand, became very abundant after its accidental
introduction in the 1970s and is now a prominent member of the macrobenthos in shallow
subtidal sands (Armonies & Reise 1999). However, as E. americanus invaded a sparsely
faunated habitat, no significant interactions with resident species occurred.
General Discussion
143
6.4 Conclusion
The further increase of the oyster population in the Wadden Sea may lead to a regime shift
with mussel beds being largely replaced by oyster reefs. Intertidal and possibly also subtidal
oyster reefs with a varying amount of mussel overgrowth is considered to be a likely future
scenario. Even though oyster recruitment depends on high summer water temperatures, high
survival rates due to low predation pressure and a higher efficiency of using space and food
resources compared to resident mussels are considered to facilitate a strong increase in oyster
abundances. This may have profound impacts on the Wadden Sea food web, because oysters
are not as well integrated in the food chain as resident bivalves. This may have consequences
not only for benthic predators, but also for foraging birds, and may transform the Wadden Sea
ecosystem. However, it has to be taken into account that the Wadden Sea is a very dynamic
habitat and that another regime shift has occurred before when the native European oyster
Ostrea edulis was driven to extinction due to overfishing. Then, mussels occupied the vacant
niche thereby causing a shift in species composition (Reise et al. 1989). However, this species
shift was restricted to the subtidal zone and therefore had fewer impacts on overall ecosystem
dynamics.
Concerning impacts on human issues, different advantages and disadvantages are likely. For
example, the traditional mussel fishery might be hampered because seed mussels become
overgrown by oysters (N. Dankers, pers. comm.). Fishery on wild oyster stocks, on the other
hand, seems to be unprofitable because of the low commercial value of unshaped oysters
cemented to huge bulks. However, collection of wild oyster spat instead of importing seed
oysters may reduce the possible introduction of new invaders, like epibionts or parasites and
pathogens. Whether or not oyster reefs may facilitate coastal protection would be an
interesting subject to study.
In general, the worldwide distribution and subsequent establishment of C. gigas is a striking
example of a species that has not caused species extinctions, but changed ecosystem dynamics
and has a share in an advancing similarity between coastal biota around the world.
144
Chapter 6
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Acknowledgements
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Acknowledgements
Many people have contributed to this thesis and I would like to mention those to whom I am
particularly grateful.
First of all, I would like to thank my supervisor Prof. Dr. Karsten Reise for academic advice,
trust and patience, and especially for his enthusiasm for the subject of my thesis. Dr. Werner
Armonies greatly improved two manuscripts with good ideas and valuable comments. Special
thanks also to Dr. Georg Nehls for letting me in on mussel bed miracles – his criticism and
comments definitely improved this thesis.
Dr. Pauline Kamermans and colleagues from the RIVO Institute in Yerseke enabled me to
study "real" oyster reefs – thanks a lot for the uncomplicated and friendly stay at Yerseke!
All people from the Wadden Sea Station Sylt were extremely helpful and supportive, not only
in providing material and ideas, but also in creating a relaxed, amiable atmosphere. I would
like to acknowledge the invaluable help of Dr. Peter Martens and Dr. Carsten Pape in solving
all my computer problems. Reimer Magens helped in constructing lots of different cages for
field experiments, and Lilo Herre proved to be the one person always being able to provide
material urgently needed together with good ideas on how to use it. Special thanks also to the
varying crew of FS "Mya", Nils Kruse, Peter Elvert, Dieter Pogoda, Alfred Resch and Timo
Wieck for cheerful sampling trips and "rescue" from distress at sea.
I would like to thank the students Dina Schmidt, Catharina Claus, David Thieltges, Beatrice
Lafargue, Kristin Scheuer, Jan Herrmann, Bodo Schiwy, Stefan Görlitz and Andreas Schmitz
for being courageous, tireless and reliable – and good company! – in the field and lab.
Without your help this thesis would not exist to this extend. Carsten Pape, Tobias Dolch,
Kristin Kosche and Dylan Robertson read final drafts of this thesis and helped with correcting
the English and setting the layout - thanks for your straightforward help!
My parents Doris and Jürgen Diederich, my grandparents Edith and Jochen Diederich and my
brother Kai always supported and encouraged me.

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