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5.5
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Functional diversity
M. Lavaleye, J. A. Craeymeersch, and G. C. A. Duineveld
5.5.1
Introduction
The way in which benthic species acquire their food determines various other parameters of
their lives and reflects their adaptation to the environment. Thus, differences in the
environment will be reflected in the distribution of feeding types. The latter may also reflect
differences in the energy transfer from surface production to the benthos. These are the
reasons to focus on the feeding types as an aspect of the functional diversity of the benthos.
The main benthic feeding types can be divided in two ways: what they feed on and how they
feed. The first category can be divided into herbivores, carnivores, and detritivores, and the
second into suspension-feeders, filter-feeders, deposit-feeders, scavengers, and predators
(www.aqualex.org).
Herbivores are organisms that feed on plant material. They live mainly on plants or on the
sediment surface, usually in shallow areas, and have special mouth parts (e.g. radulae), which
enable them to cut and chew vegetal material.
Carnivores/predators are organisms that feed on live individuals of various sizes. They have
well-developed sensory organs, which enable them to detect prey; they are highly mobile in
order to pursue their prey; and they have special mouth parts, jaws, teeth, and extendible
pharynxes to capture and consume their prey. Scavengers can be considered as a subcategory
of carnivores. They are of similar body construction and feed on dead bodies or remnants of
either benthic or pelagic organisms.
Suspension-feeders have appendages covered by mucus to which suspended particles from the
water column become attached. They are then carried by means of the cilia and antennae to
the mouth. This category of organisms does not have much mobility and lives attached to the
substrate; they prefer hard substrate and usually construct special hard cases or tubes into
which they retreat when they sense danger. In hydrodynamically energetic areas, very fine
sediment is not a favourable environment for suspension-feeders because resuspension causes
their feeding appendages to clog up.
Filter-feeders find their food in much the same way as suspension-feeders: the only difference
is that they themselves create water currents towards the special food retention appendages by
means of siphons or articulated appendages. Their ecological preferences do not differ in
general from those of suspension-feeders, with the only important difference being their
ability to colonize environments with a sparser food supply.
Deposit-feeders feed on organic material contained in the soft sediments of the seabed. The
ways in which they acquire their food are quite diverse and range from a simple swallowing of
the sediment and the digestion of the organic material contained in it, to spreading mucus on
the sediment surface and then the swallowing of particles of organic material and/or bacteria
that become attached to it. They are differentiated as selective and non-selective depositfeeders according to their ability to select the type and the size of the particles they swallow,
and as surface and subsurface deposit-feeders according to their ability to feed on particles on
the surface or to exploit food located deeper in the sediment (though not deeper than a few
centimetres).
5.5.2
Material and methods
For all macrobenthic species/taxa recorded in 1986 and 2000, the feeding type was determined
from the literature or by expert judgment. Only a small percentage of the total (1.5%) could
not be allocated, based on current knowledge, while allocation to a further 5.9% was
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inappropriate owing to taxonomic imprecision (e.g. unidentified bivalves). The feeding types
were eventually divided into four main groups (Table 5.5.1). The parasites were put into a
separate (fifth) group, but this was very small in terms of density and biomass and is not dealt
with further in this account.
Table 5.5.1. Feeding groups.
FEEDING GROUP
DESCRIPTION
I
Suspension- or filter-feeder
II
Interface-feeder, surface deposit-feeder, facultative suspension-feeder
III
Subsurface deposit-feeder, grazer
IV
Predator, omnivore, scavenger
V
Parasite
na
Not appropriate at the recorded taxonomic level
U
Unknown
For the four main feeding guilds, distribution plots were made based on the data of 1986 and
2000 separately. The percentage of each feeding group was plotted for those stations where it
exceeded 40% of the total density. For this reason, only two maps are needed to illustrate the
distribution of the feeding guilds (Figure 5.5.1 and Figure 5.5.2).
The relationship between latitude and percentage of each feeding group was inspected using
X-Y scatterplots, further visualized by adding a lowess smoother for both the 1986 and 2000
data.
Differences between 1986 and 2000 in the proportion of each feeding group were tested for
significance using the following tests:
•
•
•
unpaired and paired t-test
analysis of similarities (ANOSIM)
non-parametric MANOVA (NPMANOVA)
For these tests, the data (percentages) were arcsin transformed. Furthermore, for the last two
multivariate analyses, the feeding groups were treated as variables, i.e. descriptors of the
community. All the analyses were done for the three main areas of the North Sea as delineated
by the community analysis of 1986 (TWINSPAN groups I, II, and III, based on species
abundances; Künitzer et al., (1992)).
5.5.3
Results
The percentage of suspension-feeders is large on the Oyster Ground and (in 2000) in parts of
the German Bight (Figure 5.5.1 and Figure 5.5.2). On the Dogger Bank and to the north in the
deeper water of the North Sea, filter-feeders form a minority of the macrobenthos. In the
shallow part south of the Frisian Front, the percentage of suspension-feeders is also small.
This is also the case along the Belgian and French coasts and in the English Channel, though
there are some stations with large percentages. (Note that, in the last case, a large number of
stations are situated close together).
Interface-feeders form the most important part of the infauna over the whole North Sea,
except for the Oyster Ground. At many stations, the percentage of this feeding guild is larger
than 50%. Subsurface deposit-feeders form a minority in the North Sea. Only in the German
Bight, in the Channel, and along the Belgian and French coasts are they found in greater
numbers, but not often exceeding 50%. Predators, scavengers, and omnivores together
demonstrate a pattern similar to that of subsurface deposit-feeders, though with slightly larger
percentages, especially in the coarser sediments along the UK coast.
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The large proportion of suspension-feeders in the Oyster Ground is also apparent from the
latitudinal gradient (Figure 5.5.3). Interface-feeders demonstrate a drop in their proportion in
that area. Subsurface feeders fluctuate around a low value, but without obvious peaks or dips.
The proportion of predators appears to be similar over the whole latitudinal range, except in
the south where there is evidence of an increase. Overall, there was no evidence of a marked
change in the proportion of feeding types along the latitudinal gradient in 1986 and 2000, and
the lowess lines of both years (1986 and 2000) are quite similar for each feeding guild (Figure
5.5.3).
In all three North Sea assemblages (based on Künitzer et al., 1992), there is a difference in the
proportion of the feeding groups between 1986 and 2000 (ANOSIM, NPMANOVA: Table
5.5.2). The t-tests reveal that, in assemblage 1, covering the shallowest stations, there is a
significant difference between the proportion of interface-feeders and subsurface depositfeeders in 1986 and 2000 (Table 5.5.2). In the somewhat deeper (30–70 m) stations with finer
sediments (assemblage 2), 1986 and 2000 differ in the proportion of all feeding groups. In the
deeper area (assemblage 3), there is a difference in the proportion of subsurface depositfeeders and carnivores.
Table 5.5.2. Differences between 1986 and 2000 in the proportion of each feeding group (I–IV),
tested for significance using unpaired and paired t-tests and community analyses (ANOSIM,
NPMANOVA). * = significantly different, ** = highly significantly different.
ASSEMBLAGE
ANALYSIS
I
1
unpaired t-test
p = 0.305
p = 0.005**
p <0.001**
p = 0.250
paired t-test
p = 0.268
p <0.001**
p <0.001**
p = 0.120
2
unpaired t-test
p = 0.06
p <0.001**
p = 0.049*
p <0.001**
paired t-test
p = 0.006*
p <0.001**
p = 0.018**
p <0.001**
unpaired t-test
p = 0.442
p = 0.648
p = 0.020*
p <0.001**
paired t-test
p = 0.311
p = 0.638
p = 0.008*
p <0.001**
3
ASSEMBLAGE
1
2
3
5.5.4
ANALYSIS
NPMANOVA
II
III
IV
P-VALUE
p <0.001**
ANOSIM
p <0.001**
NPMANOVA
p = 0.002**
ANOSIM
p = 0.001**
NPMANOVA
p = 0.005**
ANOSIM
p = 0.001**
Discussion
Surprisingly, in this comparison of the density of the different feeding types between 1986 and
2000, we found a statistically significant difference for the three main faunal assemblages
(1−3) in the North Sea, as identified by Künitzer et al. (1992). However, the nature of the
changes appears to be different between assemblages, and possible causes are considered
below.
In assemblage 2, centred on the Oyster Ground at moderate depth (30–70 m) and with a high
mud content, all feeding types exhibited change. The Oyster Ground is characterized by a
high-density and a high-proportional contribution of suspension-feeders, which is the case for
1986 as well as 2000. This is caused mainly by the brittlestar Amphiura filiformis. From the
yearly biomonitoring of the benthos in the Dutch sector covering the Oyster Ground, there is
evidence that Amphiura has declined since the 1990s (Daan and Mulder, 2005). There are
several possible explanations for this change, including fishing activity, increased
resuspension caused by higher windstress, and an ecological “regime shift” as the Amphiura
population at the low point of a natural cycle of variation in densities is displaced by larger
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Structure and dynamics of the North Sea benthos
numbers of Callianassa subterranea and Upogebia deltaura (van Nes et al., 2007). A large
change in the Amphiura population can explain not only the difference in the proportion of
suspension-feeders, but also of other feeding types because, expressed in this way, they are
dependent variables. High densities of suspension-feeders in an area are often seen as an
indication of an unpolluted or unstressed environment, and this is reflected in the scoring
systems for many marine biotic indices (e.g. Borja et al., 2000; Word, 1978). It follows that a
decrease of suspension-feeders would point to increased stress.
In assemblage 1, covering mainly the southern part of the North Sea with sandy sediment and
shallow depths, there was a significant change in the proportion of the interface-feeders and
subsurface feeders. The interface-feeders increased, while the subsurface feeders decreased.
For the interface-feeders, these changes were mainly caused by the greater numbers of
Spiophanes bombyx and Magelona spp. in 2000. These short-lived polychaetes, however, can
demonstrate large year-to-year differences in their populations. This is evident from long-term
monitoring of the macrobenthic fauna in the Dutch sector of the North Sea (1990–2005: Daan
and Mulder, 2006), and instead of an increase, they note a somewhat decreasing trend in
Spiophanes densities. For Magelona spp., they cannot show a clear trend. Scoloplos armiger
and Ophelia borealis were responsible for the decrease of subsurface feeders in our
comparison between 1986 and 2000. Here the same argument applies as for Spiophanes and
Magelona, namely that the changes are probably caused by normal year-to-year variations in
the densities of these short-lived species, rather than pointing to a clear long-term trend.
In assemblage 3, located in the deeper area of the North Sea, a difference in the proportion of
subsurface deposit-feeders and carnivores was found. The subsurface feeders demonstrated a
proportional decrease from 1986 to 2000. Among the species causing this change, the
Capitellidae had the highest contribution, but no single species could be held responsible for
the change. The main species responsible for the increase of carnivores was Paramphinome
jeffreysii. As for the changes in assemblage 1, we argue that these are mainly caused by yearto-year fluctuations in the population of short-lived species.
We conclude that, based on the proportional contribution of the four feeding guilds, there is a
clear change in the central North Sea (Oyster Ground and surroundings), which is backed up
by annual monitoring. For the other parts of the North Sea, we noted a change, but could not
designate this as a continuous trend over the years. It is unfortunate that these North Sea-wide
quantitative exercises cannot be conducted on a more frequent (even annual) basis, because
long-term trends can now be difficult to separate from annual fluctuations in the macrobenthic
populations. We stress that, in response to increasing concerns over global warming, the
possibility of declining fishery effort in the future (because of regulations or stock depletion)
and the designation of marine protected areas in the North Sea, it is very important to monitor
the consequences for the benthic fauna at appropriate frequencies. After decades of increasing
fishing effort and concerns over pollution and other human activities, it is surprising that the
first quantitative survey of the macrobenthic fauna of the whole North Sea was only carried
out in 1986. Further, it has taken another 15 years to achieve a repeat assessment on a
comparable scale. This seems to be an unacceptably low frequency, given the continued
importance of the North Sea for mankind and nature.
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Figure 5.5.1. Distribution of the feeding groups for 1986. The feeding group per station is shown
only if larger than 40%. The symbols representing the four different feeding types have different
colours as well as different sizes to make a possible overlap visible in the case of two feeding types
having more than 40% of the total density at the same station.
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Figure 5.5.2. Distribution of the feeding groups for 2000. The feeding group per station is shown
only if larger than 40%. The symbols representing the four different feeding types have different
colours as well as different sizes to make a possible overlap visible in the case of two feeding types
having more than 40% of the total density at the same station.
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Suspension feeders
Interface feeders
80
100
data 2000
data 1986
lowess data 1986
lowess data 2000
60
data 1986
data 2000
lowess data 1986
lowess data 2000
80
60
40
40
20
20
0
0
50
52
54
56
58
60
50
Latitude
52
54
56
58
60
Latitude
Predators, Omnivores & Scavengers
Subsurface deposit feeders
100
100
data 1986
data 2000
lowess data 1986
lowess data 2000
80
80
60
60
40
40
20
20
0
data 1986
data 2000
lowess data 1986
lowess data 2000
0
50
52
54
56
58
Latitude
60
50
52
54
56
58
Latitude
Figure 5.5.3. Latitudinal gradients in proportion of feeding groups (the Y axes are % feeding
type). The lowess line is a locally weighted regression line used to smooth and visualize
fluctuations.
References
Aqualex. 2007. www.aqualex.org.
Borja, A., Franco, J., and Perez, V. 2000. A marine biotic index to establish the ecological
quality of soft-bottom benthos within European estuarine and coastal environments.
Marine Pollution Bulletin, 40: 1100–1111.
Daan, R., and Mulder, M. 2005. The macrobenthic fauna in the Dutch sector of the North Sea
in 2004 and a comparison with previous data. Royal Netherlands Institute for Sea
Research, NIOZ–RIKZ Rapport 2005–3. 95 pp.
Daan, R., and Mulder, M. 2006. The macrobenthic fauna in the Dutch sector of the North Sea
in 2005 and a comparison with previous data. Royal Netherlands Institute for Sea
Research, NIOZ–RIKZ Rapport 2006–3. 93 pp.
Künitzer, A., et al. 1992. The benthic infauna of the North Sea: species distribution and
assemblages. ICES Journal of Marine Science, 49(2): 127–143.
van Nes, E. H., Amaro, T., Scheffer, M., and Duineveld, G. C. A. 2007. Possible mechanisms
for a marine benthic regime shift in the North Sea. Marine Ecology Progress Series, 330:
39–47.
Word, J. Q. 1978. The Infaunal Trophic Index, pp. 19–39. Coastal Water Research Project
Annual Report. Southern California Coastal Water Research Project, El Segundo, CA.
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