This document summarizes an internship project conducted at the NIOZ institute in the Netherlands to study predation and interspecific competition on the common mussel (Mytilus edulis) in the Dutch Wadden Sea. The project focused on measuring predation by birds and competition from other filter-feeding species in mussel beds. Fieldwork was conducted to count birds, measure mussel bed coverage, and sample the density of mussels and other filter feeders at random points within beds. Bird counts were performed from a distance before sampling mussel beds. At each sampling point, a quadrat was used to collect and identify macrofauna, and the strength of mussel attachment was measured. Preliminary results showed variation

1. Université de La Rochelle
3ème
année de Licence générale Biologie et Ecologie marine
Promotion 2010-2011
Internship, from April 17th to June 24th 2011
Predating and interspecific
competition on Mytilus edulis in
the Dutch Wadden sea
By Aaron HARTNELL
M
A
R
I
N
E
E
C
O
L
O
G
Y
Directed by Andreas Waser
[andreas.waser@nioz.nl]
At the NIOZ institute
*Landsdiep 4, 1791 ‘t Horntje (Texel), The Netherlands+

2. Abstract
Français
Les moulières de la mer de Wadden constituent une ressource en coquillages
consommables importante avec la présence de la moule Mytilus Edulis. En début des années
1990, la quasi-totalité des moulières avaient disparues dû à une pêche intensive et une
mauvaise période de ponte. Cette baisse a provoqué des conséquences sur les populations de
leurs prédateurs et sur d’autres bivalves à propriétés invasives. Depuis, les moulières sont
contrôlées et retrouvent leur densité connue auparavant. Ce rapport démontre quelles sont les
procédures employées pour essayer de comprendre l’intensité de la predation ainsi que de la
competition interspécifique pour l’espace et la nourriture sur les moules Mytilus edulis.
English
The Wadden sea mussel beds are an important resource in sea food with the presence
of the mussel Mytilus edulis. In the early nineties, almost all mussel beds have been
disappeared due to an intensive fishing and a bad spawning year. The decrease occasioned big
consequences on their predators’ populations and on invasive bivalve species. Since then,
mussel beds are controlled and showing a high increase in their populations’ density. This
report shows the methods applied to try to understand and measure the predation intensity and
the interspecific competition for food and space on the mussels Mytilus edulis.

3. Glossary
AFDW : Ash free dry weight
NIOZ : The Netherlands institute for sea research
Filter feeders : Species capable of feeding on suspended organic material by filtering the
water column
Acknowledgments
First of all, I want to thank Prof. Dr. Jaap van der Meer, who offered me the opportunity to
realize this internship at the NIOZ institute.
I’m also grateful to M. Andreas Waser, my internship supervisor, for his backing, his availability
and for the scientific knowledge he taught me.
Sytze Terpstra helped us for the field work. I thank him for his contribution to the project
progress.
Finally, I express my gratitude to M. Gilles Radenac for agreeing to be my personal tutor, and
more generally to the University of La Rochelle for the education received.

4. Summary
Context.............................................................................................................................................. 1
1. The NIOZ institute ............................................................................................................... 1
2. Project description .............................................................................................................. 2
Introduction...................................................................................................................................... 3
Methods............................................................................................................................................ 4
1. Studied zone........................................................................................................................ 4
2. Main species involved ......................................................................................................... 5
2.1. Filter feeders ............................................................................................................... 5
2.2. Birds............................................................................................................................. 6
3. Sampling preparation.......................................................................................................... 6
4. Field work ............................................................................................................................ 7
4.1. Bird counts................................................................................................................... 7
4.2. Mussel bed sampling................................................................................................... 7
5. Filter feeders measurement................................................................................................ 8
Results............................................................................................................................................... 9
1. Example of a mussel bed evolution over time: De Cocksdorp............................................ 9
2. Intercompetition in-between filtering species.................................................................. 10
2.1. Filter feeders’ density of 4 mussel beds analyzed..................................................... 10
2.2. Interspecific competition frequency histograms ...................................................... 11
2.3. Bird predating results................................................................................................ 12
Discussions...................................................................................................................................... 13
Conclusion....................................................................................................................................... 14
Bibliography.................................................................................................................................... 15

5. 1
Context
1. The NIOZ institute
The Royal Netherlands Institute for Sea Research, known as NIOZ, was founded in
1876.
The institute is located on the Texel island at the border between the North Sea and
the Wadden Sea, and situated about 100 km from north of Amsterdam.
The NIOZ mission is to gain and communicate scientific knowledge on seas and oceans
for the understanding and sustainability of our planet, and to facilitate and support marine
research and education in the Netherlands and Europe.
The research is organised in five multi-disciplinary themes (“Open ocean processes”; “Sea
floor dynamics”; “Wadden and shelf sea systems”; “Climate variability and the sea”;
“Biodiversity and ecosystem functioning”) carried out by five scientific departments
(“Physical Oceanography”; “Marine Geology”; “Marine Organic Biogeochemistry”;
“Biological Oceanography”; “Marine Ecology”).
Figure 1 : The NIOZ
location in the Netherlands

6. 2
2. Project description
The work realized at NIOZ concerns the “Wadden and shelf sea systems” theme and the
“Marine Ecology” scientific department. This department aims to obtain a mechanistic
understanding of the structure and dynamical behaviour of marine macrobenthos populations.
The general approach that is followed is to try to understand the properties of populations and
communities on the basis of characteristics of individual organisms.
Within the department, several research clusters occur. This project is included in a more
general project directed by Jaap van der Meer: “Understanding population dynamics on the
basis of individual behaviour”.
The internship was supervised by Andreas Waser, a PhD student working more precisely
on the predation on littoral mussel banks. His research is included in the MOSSELWAD
project. Launched in 2008, this last aims to define the factors responsible for the lack of
stability of the Dutch Wadden sea mussel beds.
Thus, M. Waser tries to highlight the biotic factor roles on mussel beds evolution by
studying the crab and bird predation pressure. Two different monitoring programmes are
used:
- the “big brother” beds program using cameras to realize continuous bird counts
- the 20-bed-program involving 20 random mussel beds (10 west / 10 east) where birds
counts are realized 6 times a year and mussel sampling twice a year.
The internship is part of the 20-bed-program and focus only on the West Wadden sea
Dutch coast. This report will able you to understand the fieldwork and the database treatment
which were done on the Western Wadden sea coast during the internship.

7. 3
Introduction
The common mussel Mytilus edulis is one of the main species found in the Wadden sea
(S. Munch-Petersen et al. 2001; N. Dankers et al. 1995). It’s an important sea food resource
for humans and for its predators such as crabs and birds (Cor J. Smit et al. 1998). The figure 2
shows that this last was almost instinct in the 1990’s. The reasons were mainly a bad
spawning year and fisheries pressure (Cor J. Smit et al. 1998). The high mussel density
decrease in the sea caused major fluctuations in the trophic chains related to them. A lot of
common bird species mainly feeding on mussels changed to other preys which engendered a
higher pressure on their populations (Cor J. Smit et al. 1998). Some other bird species
commonly found in the area started migrating elsewhere lowering their density on the
Wadden sea coast (Cor J. Smit et al. 1998). Furthermore, other intercompetitive filter species
such as the pacific Japanese oyster Crassostrea gigas (known as an invasive species), started
spreading out and replacing mussel beds (F. Fey et al.2009).
Since, laws have been put in place (Cor J. Smit et al. 1998) to redevelop the mussel beds
in all the Wadden sea. The figure 2 shows a high population increase since 1994. Every bed
and region has a different development explained by the variability of biotic and abiotic
factors acting on them. A major
disparity is found between East and
West Wadden sea with a higher
abundance in the East. To explain
this difference, it’s necessary to
analyze the factors influencing the
mussel beds.
Birds feeding on mussels could have a major role on the variability in between West and
East. As the West coast has less mussel beds, the predation could have a higher effect for a
same feeding intensity. To find out if this is a factor potentially acting on the beds, this report
shows the methods applied to analyze their feeding and the filter species found on each bed.
As the project is only at its first stages, only a few beds have been observed and analyzed on
the West coast.
Figure 2 : East and West mussel beds evolution in biomass over time

8. 4
Methods
1. Study zone
In North Netherlands, a chain of island separates the Wadden sea from the North sea. The
substrate composing the country coast is heterogeneous from sandy to muddy grounds. The
Wadden sea has a high percentage in shallow muddy areas that can extend to a few kilometers
from the coast. Such a location is a good place for mussel beds development. The studied
plots were mainly realized on those off shore muddy floors shown on the figure 3.
The biotic and abiotic factors influence the mussel bed dynamics, which have become
heterogeneous throughout the coast. The sampling plots locations, showed on figure 3, were
realized to try to encompass all the different possibilities. Thus, a general overview of the
mussel bed development and their predators’ population in function of the location can be
made.
Figure 3 : Sampling plots inthe Wadden
sea

9. 5
2. Main species involved
2.1. Filter feeders
Common or blue mussel
(Mytilus edulis)
Baltic tellin
(Macoma balthica)
Common cockle
(Cerastoderma edule)
Habitat: wave-washed rocks,
attached by millions through their
foot and their byssus (threads)
Description: blue-black shell,
sometimes covered by others
individuals such as barnacles (Balanus)
Size: up to 10 cm [1]
Spawning: March to October
Habitat: first centimetres of the
sediment, intertidal zones
Description: various colours
(pink, yellow, white) often in
bands
Size : 1,5 to 3,5 cm [3]
Spawning: February to May
Habitat: first centimetres of the
sediment, intertidal zones
Description: white shell
sometimes slightly striate
Size: up to 5cm [3]
Spawning: March to July
Pacific oyster
(Crassostrea gigas)
Slipper limpet
Crepidula fornicata
Sea squirt
Styela clava
Habitat: hard surfaces (rocks or
shells), intertidal zones
Description: bluish-grey shell with
deep purple patches
Size: up to 18 cm [2]
Spawning: June to September
Imported in Europe from the
Northwest Pacific (Japan, Russia…) for
commercial purposes.
Became Invasive
Habitat: hard surfaces (rocks or
shells), intertidal zones
Description: colour varies
(white to pink) with brown
blotches
Size : up to 5cm [1]
Spawning: February to March
Imported in Europe from
North America in association
with oysters (Crassostrea
virginica). Became invasive
Habitat: hard surfaces, shallow
water
Description: long club-shaped
body with a slender stalk
Size: up to 12cm [2]
Spawning : summer/autumn
Imported in Europe from
Northwest pacific on the hulls of
war ships (Korean war).
Became invasive
Figure4 : Common mussel
(Mytilus edulis) with barnacles
Figure 6 : Common cockle
(Cerastoderma edule)
Figure 7 : Baltic tellin
(Macoma balthica)
Figure 8 : Slipper limpet
(Crepidula fornicata)
Figure 9 : Sea squirt
(Styela clava)
Figure5 : Pacific oyster
(Crassostrea gigas)

10. 6
2.2. Birds
3. Sampling preparation
To estimate the predation presence of the different predators on the different mussel beds
it’s necessary to analyze the mussel bed and bird population development every 6 months.
To begin, a first field trip on the mussel bed is necessary to delimit it. The procedure is to
walk around the bed with a GPS. This last one is set to save the latitude and longitude
coordinates of its actual position every 5 seconds. Once the mussel bed has been totally
walked around, the coordinates are transferred to a computer. The exact mussel bed
Eurasian Oystercatcher
(Haematopus ostralegus)
Eider
(Somateria mollissima)
Herring gulls
(Larus argentatus)
Figure 4: Pied oystercatcher
(Haematopus ostralegus)
Figure 5: Male Common eider
(Somateria mollissima)
12 species
The most common species :
the pied oystercatcher
(Haematopus ostralegus)
Habitat: sandy coasts or salt
marsh, sometimes inland
Description: black and white
plumage, long orange beak
Size: 40 to 45 cm [4]
Food: shells, crabs, worms -
Shell eating type: opens the shell
and eats the inside
Spawning: May or early June
3 species
The most common species:
the common eider
( Somateria mollissima)
Habitat: rocky and sandy coasts,
sometimes inland
Description: black and white
(male) or brown (female) plumage
Size: 50 to 71 cm [5]
Food: shells, crabs, sea urchins –
Shell eating type: swallows the
entire shell
Spawning: May to June
6 species
The most common species:
The European herring gull
(Larus argentatus)
Habitat: rocky and sandy coasts,
sometimes inland
Description: white and grey
plumage
Size: 55 to 67 cm [4]
Food: garbage, shells, eggs, fish…
Shell eating type: breaks the shell
or swallows all of it
Spawning: April to May
Invasive species due to an
anthropogenic adaptation
Figure 6: European herring gull
(Larus argentatus)

11. 7
emplacement and circumference are obtained by integrating and analyzing the data with
Garmin Mapsource, R and GPS Babel software.
By using Garmin Mapsource, 50 sampling spots are spread out randomly on the
mussel bed surface. The coordinates of every spot are integrated on the GPS. This last is set to
calculate the shortest track in between the sampling points.
4. Field work
4.1. Bird counts
Before arriving on the mussel bed, the samplers stop at a distance in between 300 and
500 m and install the scope. One of the samplers counts all the birds on the mussel bed helped
with hand counters and the scope. The birds are counted and separated in function of their
species. This count is done 1 to 3 hours before low tide.
4.2. Mussel bed sampling
The mussel bed sampling program is conducted by a 3 people team. Each sampling
spot is reached when the GPS gives a sound signal (with an 8 meter precision). While walking
in between each spot, one person estimates the mussel coverage by using the boot method,
where steps on mussels and steps on mud/sand are counted using hand counters. To achieve
the most precise estimation by doing a straight line in between 2 spots, the person in charge of
the coverage estimation waits at the previous spot until the rest of the team reaches the next
one. After their arrival, he can estimate the coverage by walking straight up to them.
After arrival on each spot, the GPS holder looks if he’s standing on mussels or on
mud/sand. If there are no mussels, this is noted down and the team moves to the next spot. If
there are mussels, the team has to realize a sampling procedure by measuring the mussel
attachment strength and the filter feeders’ density.
The density sampling is done with a 15cm*15cm quadrate which is put on top of
where the GPS holder is standing. The macro-fauna existing in the quadrate is gathered and

12. 8
cleaned by using an iron sieve with 0.5mm holes. The samples are then put in plastic bags
with an identification number.
The attachment strength is measured with a
clamp and force scale represented in figure 8. A
random mussel near the GPS holder is chosen,
grabbed with the clamp and pulled off the rest of the
bed. This last mussel is rinsed and put in a plastic
bag with an identification number. The scale needle
blocks on the maximum force exerted to detach the
mussel which is then noted down.
After sampling the 50 spots on the bed, the bags are then kept in a -18°C room.
5. Filter feeders measurement
Before measuring the filter feeders individuals, the samples are properly cleaned with
fresh water and sorted out. The filter feeders are the only macrofauna kept. The rest is thrown
back in the sea.
Every individual is identified and its length is measured with a caliper. The
measurements are written down on an Excel sheet with a 0.1mm precision. This sheet is
composed with columns indicating the location, mussel bed number, date, month, sectors
(when they are some), sampling number, sampling size, individual species, barnacle coverage
and length measurement of each individual.
The mussels counted per bed are sorted in function of their length by separating them
per 2.5mm±0.5mm. After counting all the individuals, 15 random mussels are picked from
each length group to measure their ash free biomass. The ash free biomass is measured by
putting the samples in a high temperature oven until only ash is left. This ash is then measured
with a scale. By calculating the dry biomass in grams, it is possible to determine the bivalve
shell thickness.
Figure 12 : System used to measure the mussel
attachment strength

13. 9
Figure 13 : De Cocksdorp mussel bed evolution over time
Results
During the internship, the field work and measurement mainly concerned four eastern
beds (De Cocksdorp; Balgzan/Kuitje; Balgzand/Amsteldiep; Texel/Krassekeet).
1. Example of a mussel bed evolution over time: De Cocksdorp
This image shows an
evolution example of a mussel bed
over time between September 2009
and March 2011. The colored lines
are the bed contours for every
sampling date. The mussels tend to
modify their composition every time a
sampling is realized. In March 2011,
the juvenile bed near land was
existing but forgotten to be sampled.
These histograms show the Mytilus
edulis population development over time in the
De Cocksdorp mussel bed over a winter. The
population tends to decrease in numbers but
increase in size. Almost a third of the
population died after the winter.
Figure 14 : De Cocksdorp frequency histogram over the
winter 2010-2011

14. 10
2. Intercompetition in-between filtering species
2.1. Filter feeders’ density of 4 mussel beds analyzed
The density of every filter feeder species is highly different in function of the location.
The Standard deviations are important due to the high heterogeneity of the sample counts and
can’t answer the significant difference in between the beds.
The only filter feeders with high numbers are the mussels Mytilus edulis and the
oysters Crassostrea gigas. Mytilus edulis is found in high abundance on all the beds
compared to the other species. But we can still observe a certain high density of Crassostrea
gigas in Amsteldiep and Krassekeet.
Kuitje is the only location with a lower abundance in filtering species compared to the
rest of the locations.
Figure 15 : Filters' population on each bed analyzed during the internship

15. 11
2.2. Interspecific competition frequency histograms
It’s observed that Mytilus edulis has a maximum size not extending above 65mm
compared to Crassostrea gigas that can measure up to 20cm. The 2 beds show that Mytilus
edulis has a higher number of adult individuals compared to the oysters which have a high
juvenile density.
The higher number of individuals in Amsteldiep compared to Krassekeet is due to the
higher number of samples done on the bed and its bigger surface.
Amsteldiep shows lower sizes for its different filtering species compared to
Krassekeet.
Figure 16 : Size frequency histograms of the 2 beds showing a higher
interspecific competition

16. 12
2.3. Bird predating results
Tableau 1 : Bird countings and food consumption
To estimate the bird predation pressure on each mussel bed, the total dry-biomass of
food eaten by the three main species per day has been calculated. The average food per
day eaten by each bird was determined by Laursen et al. (2010).
Tableau 2 : Mussel beds dry biomass
The total dry-biomass of the mussels on each bed has been estimated through the bed
surface, the density and the mussel average weight. S. Munch-Petersen et al. (2001) have
created a formula linking the average length (L) and the average weight (W) of mussels
thanks to the coefficient “q”:
Bed Date Species Average food per day (g)
Count
estimation
Total food per
day (g AFDW)
Balgzand /
Amsteldiep
01/03/2011
Oystercatcher 45 18
810Herring gull 91 0
Eider 165 0
03/05/2011
Oystercatcher 45 6
361Herring gull 91 1
Eider 165 0
Texel /
Krassekeet
21/02/2011
Oystercatcher 45 47
13217Herring gull 91 122
Eider 165 0
08/03/2011
Oystercatcher 45 42
10626Herring gull 91 96
Eider 165 0
18/04/2011
Oystercatcher 45 19
4791Herring gull 91 36
Eider 165 4
Balgzand /
Kuitje
16/02/2011
Oystercatcher 45 603
27135Herring gull 91 0
Eider 165 0
04/05/2011
Oystercatcher 45 75
13385Herring gull 91 110
Eider 165 0
Location Date
Number of
samples
Mytilus
counts
Average
length
L(mm)
Coefficient q
Average
weight W(g)
Density
(ind/m
2
)
Bed
surface
(ha)
Total AFDW
(g)
Balgzand /
Amsteldiep
05_2011 19 810 31,72 3,73E-06 0,119 729,47 4,2 36448,0
Balgzand /
Kuitje
11_2010 23 402 34,55 3,73E-06 0,154 500,27 19,9 1529389
05_2011 19 471 41,81 3,73E-06 0,272 292,16 16,9 134441,0
De
Cocksdorp
08_2010 58 3542 24,90 3,73E-06 0,057 1117,18 ?? ??
01_2011 55 2850 27,85 3,73E-06 0,081 1175,06 8,9 84207,6
03_2011 45 2014 28,66 3,73E-06 0,088 1167,68 8,6 88073,6
Texel /
Krassekeet
04_2011 21 458 38,60 3,73E-06 0,214 588,69 2,7 34060,2

17. 13
W(g) = q . L(mm) with q=3,72E-06
This formula has been established through mussel samplings from the Denmark
Wadden sea coast. Consequently, it can give enough accurate results for the Netherlands
Wadden sea coast.
Discussions
Mytilus edulis has recovered its numbers since the 1990’s and is now the species found
in higher numbers on most mussel beds coming from the Wadden sea.
The figure 15 shows that the main competitor is Crassostrea gigas as the other filter
feeders have very low numbers compared to Mytilus edulis. But this oyster can still be found
in high numbers on some mussel beds. Because of its length, shown in the frequency
histograms on figure 16, it can highly minimize the food resources available for Mytilus edulis
due to a high filtering consumption. The competition for space in between these 2 species is
hard to estimate. They could have a certain competition for space as they’re found in the same
areas but some other research proves that Mytilus edulis is commencal on Crassostrea gigas.
F. Fey et al. (2009) showed that Crassostrea gigas shells can be used as a solid support for
Mytilus edulis to fix on to. Furthermore, he demonstrated that predators tend to have more
difficulties catching the mussels stuck in between the oysters. These 2 researches point that
Crassostrea gigas is used as a shelter for Mytilus edulis.
The correlation between interspecific competition for space and commencal relations
for these 2 species makes it difficult to understand if Crassostrea gigas has a negative or
positive effect on Mytilus edulis. Although, the results on figure 15 tend to show that there’s
an inhibitor effect by Crassostrea gigas on Mytilus edulis population. On the beds observed,
Mytilus edulis tends to have a lower density when the oysters have a higher one. This
tendency can show a certain trend that these species have a negative effect on each other.
The project is at its first results and it’s still hard to give any conclusions on the real
effect of bird predating on Mytilus edulis but trends can still be made. The table 2 shows that

18. 14
the mussels have a high potential food resource for birds. The table 1 demonstrates that birds
can eat a high volume of mussels per day. It’s impossible to calculate the percentage of
mussels eaten on a bed each day as the birds don’t only feed on one unique species. But still,
the feeding intensity can have a real effect on the mussel populations and decrease their
numbers. We can see the bird feeding is really high compared to the total mussel dry biomass
of each bed. These results only prove a rough idea and are probably wrong or not precise.
The “big brother” bed program (realized in the same project) will hopefully able to create a
modeling capable to measure the precise intensity effect on mussels by bird predating. This
modeling would take in account the other food resources available for the birds, for example:
other bivalves (mainly Crassostrea gigas) and other preys as fish or crustaceans.
Beds on the East Wadden sea (not observed during our internship) are bigger in size
and in numbers compared to the West side (figure 3). The only hypothesis that could explain
the cause of this distribution is the high intensity of predation and the interspecific
competitors keep the mussel populations constant. The results coming up in the next years
with the project will probably be able to have a better view on the understanding of that
distribution.
Conclusion
The project is still at its first stages and no conclusions on the results can still be made.
This report showed trends proving a real effect of other bivalve and birds’ predation but the
intensity can’t yet be measured. The birds are one of the 2 main mussel predators with crabs.
The rest of this internship will be spent on finding a method to estimate the crab predating
pressure on mussels.
The project is having more and more data and will be able after a couple of years to
determine more precisely the causes of the mussel beds evolution and their distribution.
Models will then be set up to try to calculate future mussel bed apparitions and eventually
determine the evolution of artificial mussel beds.

19. 15
Bibliography
N. DANKERS. 1995. The Role of the Mussel (Mytilus edulis L.) and Mussel Culture in the
Dutch Wadden Sea. Estuaries Vol. 18, No. 1A, p71-80
S. MUNCH-PETERSEN. 2001. On the dynamics of the stocks of blue mussels (Mytilus
edulis L.) in the Danish Wadden Sea – Marine biodiversity Volume 465, Numbers 1-3, 31-
43, DOI: 10.1023/A:1014539414345
COR J. SMIT et al. 1998. Birds, mussels, cockles and shellfish fishery in the Dutch Wadden
Sea: How to deal with low food stocks for eiders and oystercatchers? – Marine biodiversity
Volume 29, Numbers 1-6, 141-153, DOI: 10.1007/BF03043952
S. DIEDERICH et al. 2004. Introduced Pacific oysters (Crassostrea gigas) in the northern
Wadden Sea: invasion accelerated by warm summers
LAURSEN et al. 2010. Assessment of Blue Mussel Mytilus edulis Fisheries and Waterbird
Shellfish-predator Management in the Danish Wadden Sea
F. FEY el al. 2009. Development and distribution of the non-indigenous Pacific oyster
(Crassostrea gigas) in the Dutch Wadden Sea
[1] http://doris.ffessm.fr/
[2] http://www.marlin.ac.uk
[3] http://www.eol.org
[4] http://www.oiseaux.net
[5] http://www.seaduckjv.org