Download Ecotypes as a concept for exploring responses to

ICES Journal of Marine Science (2011), 68(3), 580 –591. doi:10.1093/icesjms/fsq183
Ecotypes as a concept for exploring responses to climate
change in fish assemblages
Georg H. Engelhard 1*, Jim R. Ellis 1, Mark R. Payne 2, Remment ter Hofstede 3, and John K. Pinnegar 1
1
Centre for Environment, Fisheries and Aquaculture Science, Lowestoft Laboratory, Pakefield Road, Lowestoft, Suffolk NR33 0HT, UK
DTU Aqua, National Institute of Aquatic Resources, Technical University of Denmark, Jægersborg Allé 1, DK-2920 Charlottenlund, Denmark
3
Wageningen IMARES, Institute for Marine Resources and Ecosystem Studies, PO Box 68, 1970 AB IJmuiden, The Netherlands
2
*Corresponding Author: tel: +44 1502 527747; fax: +44 1502 513865; e-mail: [email protected]
Engelhard, G. H., Ellis, J. R., Payne, M. R., ter Hofstede, R., and Pinnegar, J. K. 2011. Ecotypes as a concept for exploring responses to climate
change in fish assemblages. – ICES Journal of Marine Science, 68: 580 – 591.
Received 16 July 2009; accepted 10 November 2010; advance access publication 22 December 2010.
How do species-rich fish assemblages respond to climate change or to other anthropogenic or environmental drivers? To explore this,
a categorization concept is presented whereby species are assigned with respect to six ecotype classifications, according to biogeography, horizontal and vertical habitat preference, trophic guild, trophic level, or body size. These classification schemes are termed ecotypology, and the system is applied to fish in the North Sea using International Bottom Trawl Survey data. Over the period 1977 –2008,
there were changes in the North Sea fish community that can be related to fish ecotypes. Broadly speaking, there were steady increases
in abundance of species that were either Lusitanian, small-bodied, or low-/mid-trophic-level ecotypes, and generally declining or only
marginally increasing trends of most Boreal, large-bodied, or high-trophic-level ecotypes or combinations of them. The post-1989
warm biological regime appears to have favoured pelagic species more than demersal species. These community-level patterns
agree with the expected responses of ecotypes to climate change and also with anticipated vulnerability to fishing pressure.
Keywords: biogeography, classification, climate change, ecotype, North Sea, time-series.
Introduction
Predicting the potential effects of climate change on fish assemblages, including their structure, diversity, and function, may be
complicated, because assemblages may contain a wide variety of
species, and there will likely be important differences in how
various species respond (Cheung et al., 2009; Rijnsdorp et al.,
2009). Such understanding might, however, be facilitated by classifying the many species into a smaller set of ecotypes, i.e. groups
of species that show similarities in certain relevant biological
characteristics, so may respond in comparable ways to environmental change. Often, scientists have limited information on
certain species in an ecosystem, particularly those that are less
commercially important and not subject to the extensive data collection programmes that underpin fisheries stock assessments. In
such cases, it may be beneficial to select a species where data are
plentiful to represent the group or ecotype generally, although
this will depend on the assumption that species that have been
grouped have similar dynamics and will respond in a similar
way to common pressures (whether anthropogenic or
environmental).
As a term, “ecotype” was originally coined by the Swedish botanist Turesson (1922) and has been widely used to describe “a
genetically unique population that is adapted to its local environment”. Use of the term in fisheries science, however, has recently
been broadened to apply to different species that are adapted to
a specific set of ecological conditions, e.g. animals adapted to a
particular climate envelope or trophic niche (Rijnsdorp et al.,
2009). Other than traditional taxonomic groupings, there are
other ways to classify fish species, for instance according to their
biogeographic affinity, habitat preference, trophic guild and
trophic level, reproductive mode, or body size. To characterize
these various classification schemes, a new term is introduced
here, “ecotypologies”.
Our aim was to test the utility of the ecotype concept by investigating, for six ecotypology schemes separately, whether there
were significant differences in abundance dynamics between
groups of species belonging to contrasting ecotypes. If no such
differences can be observed, or if animals allocated to the same
ecotype do not co-vary in time, then the concept is neither
useful nor meaningful for exploring the possible implications of
long-term climate change and fishing pressure changes. The
specific hypotheses to be tested include the following.
(i) The sets of species assigned a priori to the same ecotype will
show significant differences in temporal trends when compared with sets of species in contrasting ecotypes.
(ii) Following long-term environmental change, species classified
according to their biogeographic affinity show more pronounced differences in abundance dynamics than species
aggregated according to other ecotypology schemes, e.g.
trophic guild or habitat preference.
Crown Copyright # 2010. Published by Oxford journals on behalf of the International Council for the Exploration of the Sea.
All rights reserved.
Ecotypes as a concept for exploring responses to climate change in fish assemblages
The North Sea ichthyofauna is both diverse and relatively
well-studied (Wheeler, 1969; Yang, 1982a, b; Rogers et al., 1998).
Here, 253 species known from the North Sea are categorized
according to six ecotypologies related to the species’ thermal preferences, habitat requirements, feeding characteristics, and body
size. Having assigned each species a priori to these ecotypologies,
we test the two hypotheses above using relative abundance data
from the North Sea International Bottom Trawl Survey (IBTS).
Defining ecotypologies and ecotypes
The following ecotypologies have been applied to the North Sea
fish assemblage: (i) biogeographic affinity, (ii) horizontal and
(iii) vertical habitat preference, (iv) trophic guild and (v)
trophic level, and (vi) body size. Each of these may relate to specific
characteristics of the species’ ecology, behaviour, and/or lifehistory traits. For example, biogeographic affinities are often
related to the thermal preferences of fish, and body sizes are generally linked to life-history traits such as growth, maturation, and
longevity (Jennings et al., 1999). This section defines, within each
ecotypology, the different ecotypes found in the North Sea (see
Supplementary material for a classification of all North Sea fish
species according to ecotype).
Biogeographic affinity
We follow Yang (1982a) in attributing biogeographic ecotypes to
North Sea fish species, with some modifications and inclusion of
species recorded from the North Sea since then (Wheeler et al.,
2004). Yang’s (1982a) approach has been adopted in several subsequent studies that explored the possible implications of
climate change (e.g. Dulvy et al., 2008; Tulp et al., 2008).
Boreal fish are considered to be northern taxa that extend north
to the Norwegian Sea and Icelandic waters, and south to around
the British Isles or west of Brittany, although some may still be
found farther south, in small numbers or as vagrants. Lusitanian
fish tend to be abundant from the Iberian Peninsula (including
the Mediterranean Sea) to as far north as the British Isles and
may have northern limits in the southern or central North Sea,
although many do extend to more northern latitudes on the
western seaboard of the British Isles, so can also be found in the
northwestern North Sea. Many of these species have distributions
extending into the Mediterranean and off Northwest Africa.
Atlantic species are those (often pelagic or deep-water) species
that are widespread in the North Atlantic, and include many of
the deeper-water or mesopelagic species distributed along the continental slope.
Horizontal habitat preference
Here, we attribute each species both to a horizontal habitat,
ranging from coast to high seas, and to a vertical habitat, indicating where the species is found in the water column (see below).
Fish habitats may vary temporally, ranging from diurnal to seasonal, and ontogenetically, e.g. the juveniles of many marine species
are found in shallower water than the adults. In the ecotypology
here, the habitat of a given fish species was defined as that where
the adult or adolescent life-history stages are found. The horizontal habitat ecotypes are listed below.
Coastal
Some fish species are more prevalent in shallow-water coastal
areas, although the population as a whole may extend farther offshore. For example, various pipefish, labrids, and blennies are
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most often recorded in shallow rocky habitats, whereas other
species are found almost exclusively in estuaries, e.g. flounder
(Platichthys flesus) and grey mullets (Mugilidae).
Shelf, inner shelf, and outer shelf
The continental shelf accounts for the greatest proportion of fish
in enclosed seas such as the North Sea. With shelf ecotypes, we
refer to species widespread over (nearly) the entire continental
shelf of the North Sea, living in shallow and deeper parts; examples
are the commercially important cod (Gadus morhua), haddock
(Melanogrammus aeglefinus), and plaice (Pleuronectes platessa).
Inner shelf ecotypes are defined as species generally limited to shallower water (,50 m deep) and (nearly) absent from the deeper
parts (.50 m deep) of the shelf, such as sandeel (Ammodytes
marinus), sand goby (Pomatoschistus minutus), and sole (Solea
solea). Outer shelf ecotypes are species found mainly over the
outer, deeper parts of the shelf; examples are Norway pout
(Trisopterus esmarkii) and megrim (Lepidorhombus whiffiagonis).
Slope
These are deep-water species primarily inhabiting the slope and
not typically reported from the shelf. Examples are boarfish
(Capros aper) and bluemouth (Helicolenus dactylopterus),
although infrequently considerable numbers of both these
species may be transported up onto the continental shelf
(Heessen et al., 1996; Pinnegar et al., 2002). Species such as blue
whiting (Micromesistius poutassou) and pearlside (Maurolicus
muelleri) that are abundant in oceanic water masses and found
in large numbers in the deeper-water masses of the North Sea
are also included here.
Vertical habitat preference
The vertical habitat ecotypes include pelagic species inhabiting the
water column and demersal species living on or close to the
seabed. Other distinct ecotypes include reef-associated, benthopelagic, bathypelagic, and bathydemersal species, but none of
these are found in large numbers in the North Sea and they have
not been included in the statistical analysis here (although they
are included in the list in Supplementary material).
Trophic guild
Categorization of fish into trophic guilds has been undertaken for
many sea areas including the North Sea (Garrison and Link, 2000;
Bulman et al., 2001). Feeding habits (diets) of most commercially
important species in the North Sea are relatively well known (see
Section 10 of ICES, 2005, and references therein). However,
dietary data of small benthic and many deep-water fish are limited.
Most North Sea fish are categorized here as either piscivores,
which as adults eat primarily fish (and cephalopods), planktopiscivores, which consume a variety of larger zooplankton and fish,
planktivores, feeding primarily on (zoo)plankton, benthopiscivores, which consume various larger epifaunal invertebrates and
fish, or benthivores, which feed primarily on (epi)benthic
invertebrates. Additional categories are attributed (in the
Supplementary material) to a much smaller number of specialized
feeders, but these subcategories were not used in the statistical
analysis. Benthivorous species (e.g. smoothhounds Mustelus
spp.) that eat almost exclusively crustaceans are termed carcinophages. Adult lampreys are ectoparasites, feeding off a variety of
fish and marine mammals. Although many demersal fish may
forage opportunistically on discarded fish and offal, as well as
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invertebrates or fish injured or killed by fishing gear, only species
that are nearly exclusively scavengers were classified as such, e.g.
hagfish (Myxine glutinosa). A few species were categorized as detritivores, e.g. grey mullets (Mugilidae), which typically eat organic
material from the sediment and graze algae. Many of these specialized trophic guilds are poorly represented within the North Sea
ichthyofauna.
Trophic level
To allow consistency across all taxa, information on the trophic
level was taken from FishBase (Froese and Pauly, 2007). Trophic
levels of European fish generally range from 2.0 –2.5 (for detritivores and omnivores) to 4.5 (for piscivores). In the analysis
here, each species was categorized as having a low (,3.5),
medium (3.5– 3.8), or high (.3.8) trophic level based on their
adult dietary preference.
Body size
Body size is an informative life-history parameter that often correlates with vulnerability to anthropogenic pressure. Not only do
larger species generally live longer and reproduce more slowly,
they also tend to be more likely to be caught by fishing gear and
are more often targeted by commercial fisheries. Here, as a
measure of body size, we use the maximum observed length
(Lmax), a parameter available for the vast majority of taxa. Most
fish species are measured as total length, though for species with
long, thin, fragile caudal fins, other dimensions, e.g. standard
length, fork length, or disc width, are more appropriate. For the
purposes of this study, much of the maximum size information
is from FishBase (Froese and Pauly, 2007) or from Whitehead
et al. (1984–1986), with minor amendments made for species
where extensive length frequency data were available from
fishery-independent surveys. Each species was categorized a
priori into small (,35 cm), medium (35 –60 cm), or large
(.60 cm).
Testing the ecotype concept
Multivariate statistical procedures were applied to examine the
usefulness of the ecotype concept for studying changes in a
species-rich fish community. Specifically, principal component
analysis (PCA) and analysis of variance (ANOVA) were used,
with procedures that partly followed those of Kenny et al.
(2009), used previously for integrated assessment of the wider
North Sea ecosystem (fish, plankton, seabirds, mammals, etc.).
The multivariate statistical approach has the advantage of providing a relatively simple framework for studying patterns in the large
number of fish species belonging to a wide range of ecotypes,
grouped according to six ecotypologies, although there are some
disadvantages of this methodology (discussed below).
Fish abundance data were extracted from the ICES DAtabase
for TRAwl Surveys (DATRAS), and necessary corrections were
applied (ter Hofstede and Daan, 2008). These data were collected
during IBTS, covering most ICES rectangles of the North Sea
during the years 1977–2008. In principle, each rectangle (18 longitude by 0.58 latitude) is sampled by research vessels from two
different countries during each survey. Gears varied initially, but
since 1983, a standard otter trawl net (chalut à Grande
Ouverture Verticale, GOV trawl) has been used by all, hauled
over the seabed for 30 min. The catch is sampled to provide
length frequency distributions for all fish species caught. Details
of gear and sampling strategies can be found in the Manual for
G. H. Engelhard et al.
the North Sea IBTS, revision VII (ICES, 2006). IBTS data were
taken for the first quarter of the year. Although the IBTS has a
large number of stations distributed over the entire North Sea
sampled with great consistency, as with any survey it cannot
provide a complete picture of the full North Sea fish community,
and species possibly undersampled include some fast-swimming
pelagic fish living close to the sea surface (the gear used is a
bottom trawl), species limited to very shallow inshore waters
(out of reach of the survey vessel), those that dig into the
seabed, and/or highly migratory species scarcely present in the
North Sea during winter (ICES, 2006).
Of a total of 147 species or species categories sampled by the
IBTS during winters of 1977– 2008, 95 were included in this
ecotype analysis. Exclusion of taxa was based on (i) species
being rare vagrants, (ii) “bucket” categories of similar species
hard to identify rigorously to species level on board (so mistakes
in identification would have been likely), (iii) species where the
sampling gear was not considered appropriate, e.g. those inhabiting rocks, wrecks, crevices, or gullies that cannot be sampled
by trawl, and (iv) entries that were most likely erroneous.
However, a few closely related species belonging to the same
genera were included as single entities, i.e. the genera Mustelus,
Alosa, Ammodytes, and Pomatoschistus. In the list of ecotypes for
253 North Sea fish species (Supplementary material), the species
included in this analysis are indicated with an asterisk.
For each taxon, a time-series of annual catch per unit effort
(cpue) was calculated, first averaging the catch rate (number of
individuals caught per hour, including only the time where the
trawl was on the seabed) of all hauls within a rectangle, then
taking the mean of the rectangle-averaged catch rates over the
entire North Sea. Values of cpue were log-transformed for multivariate statistical analysis. For zero values, which cause problems
for PCA and log-transformation, we followed the procedure of
Maxwell and Jennings (2005) and replaced them by half the smallest non-zero cpue value in the time-series of a given species. We
also examined different methods of treating zeroes, e.g. replacing
them with a fixed value of 0.001, or adding a fixed value of
0.001 or 0.005 to all zero and non-zero cpue data before
log-transformation.
The average abundance changes by ecotype over the years
1977–2008 were examined for the six ecotypologies: biogeography, horizontal and vertical habitat preference, trophic guild,
trophic level, and body size. Annual average ecotype cpues were
calculated as the geometric mean of the annual cpue for all
species belonging to that ecotype, where the geometric mean was
selected to preclude the dominance of a few abundant fish
species in the analysis.
The log-transformed data for all species were mean-centred by
subtracting each species’ mean log cpue. Mean subtraction is
needed for performing PCA to ensure that the first principal component (PC) describes the direction of maximum variance; it is
needed here to preclude the first PC axis simply corresponding
to the long-term means of each species’ cpue, rather than describing the dominant pattern of change.
The first hypothesis was tested by examining whether the
values of ecotypes varied significantly along either of the PC
axes, using ANOVA of PC1 and PC2 loadings by species, with
ecotype as explanatory variables. Initial Kolmogorov–Smirnov
tests were used to show that on the whole, species were normally
distributed with respect to ecotype and the values along PCs (so
the assumptions of ANOVA were not violated). The second
Ecotypes as a concept for exploring responses to climate change in fish assemblages
hypothesis was tested by examining whether the three biogeographic ecotypes (Boreal, Lusitanian, and Atlantic) could explain
a greater proportion of the variation along the first PC axis than
any of the other ecotypologies.
To assess whether or not ecotypes formed cohesive and significantly different clusters when PC1 and PC2 scores for individual
species were plotted as a scatterplot, mean PC1 and PC2 scores
were calculated by ecotype, and 95% confidence ellipses were
drawn around these means using the “FactoMineR” Library
within the statistical package R. Overlapping confidence ellipses
indicate that particular ecotypologies provide little explanatory
power, whereas clearly non-overlapping ellipses demonstrate that
particular ecotypes are statistically resolved along the two PC axes.
Results
From 1977 to 2008, there has been an increase in the average
number of fish per species caught per hour in the North Sea
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IBTS, although increases have not been in all ecotypes or at
similar levels (Figure 1). Within the biogeographic affinity ecotypology (Figure 1a), the geometric mean of the cpue values of 48
Lusitanian species showed a steep increase, picking up particularly
in the 2000s; in contrast, 41 Boreal species showed a clear increase
until the 1990s, followed by a flattening to a somewhat declining
trend. The geometric mean cpue of six Atlantic species has generally increased since the 1990s. Within the horizontal habitat ecotypology (Figure 1b), there was a much more marked geometric
mean abundance increase in 49 shelf species than in 30 coastal
or 16 slope species. Within the vertical habitat ecotypology
(Figure 1c), a far more marked abundance increase was found in
24 pelagic than in 71 demersal species, especially after the
mid-1990s. In the trophic guild ecotypology (Figure 1d), 40
benthivores, 13 benthopiscivores, and 23 piscivores showed
similar, steady increases in geometric mean species cpue,
whereas 16 planktivores showed a steep increase especially after
Figure 1. Geometric mean of species cpue values by ecotype, as represented in the North Sea IBTS over the period 1977 – 2008, shown
separately for six ecotypologies: (a) biogeographic affinity, (b) horizontal and (c) vertical habitat preference, (d) trophic guild, (e) trophic level
(lower, ,3.5; medium, 3.5– 3.8; higher, .3.8), and (f) body size (small, ,35 cm; medium, 35– 60 cm; large, .60 cm Lmax). See Supplementary
material for details of the species included.
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Figure 2. Time-series of PC1, PC2, and PC3 over the period 1977–
2008, for PCA of annual log-transformed species cpue values.
the mid-1990s. In line with this, within the trophic-level ecotypology (Figure 1e), 30 species of the lower trophic level showed much
greater increases than 36 medium and 29 higher trophic-level
species. Within the sixth, body size, ecotypology (Figure 1f), geometric mean species cpue of 32 small and 32 medium species
increased throughout the period, whereas that of 31 species
belonging to the large ecotype has not changed appreciably since
the 1980s.
PCA on log-transformed cpue indices revealed that 31.7% of
the total variance could be explained by PC1, and 11.2 and 8.3%
was explained by PC2 and PC3, respectively (Figure 2). Here,
PC1 shows a linear trend from low negative values in the late
1970s to high positive values in the 2000s. PC2 shows a parabolic
trend from very low negative values at the start of the time-series,
rapidly increasing to high positive values in the 1980s and 1990s,
down to moderately negative values in the 2000s. PC3 shows a
low frequency sinusoidal trend with mostly positive values in the
1980s and mostly negative values between the late 1990s and the
early 2000s. In summary, these temporal patterns can be described
as: PC1 low–high; PC2 very low–high–moderate; PC3 low –
high–low–high. These patterns imply that fish species that
strongly and linearly increased from 1977 to 2008 are characterized
by large positive values of PC1, in contrast to species that declined
strongly and which are characterized by large negative PC1 values.
Intermediate PC1 values are attributed to species that showed
different or intermediate temporal patterns.
There was little evidence that species belonging to different ecotypes clearly and distinctly separated according to their first three
PC projections. This is illustrated by PCA scatterplots of all species
according to their first and second PC axes (Figure 3). There was
much overlap in PC1 and PC2 projections (and hence temporal
trends) between different ecotypes, as indicated by the lack of
distinct clusterings of ecotypes in the PCA scatterplots. This
was the case regardless of whether ecotypes were classified
according to biogeographic affinity (Figure 3a), horizontal
habitat (Figure 3b), vertical habitat (Figure 3c), trophic guild
(Figure 3d), trophic level (Figure 3e), or body size (Figure 3f).
Similarly, examination of the scatterplots of species coordinates
according to their first and third PC axes (not illustrated) revealed
overlap in PC3 projections between different ecotypes.
Despite the absence of distinct clusterings, most ecotypologies
revealed significant differences in temporal trends between sets of
species belonging to contrasting ecotypes (as described by species
coordinates along PC axes). This was indicated by a lack of overlap
G. H. Engelhard et al.
between the 95% joint confidence ellipses for the mean PC1 and
PC2 projections for some, but generally not all, ecotypes within
one ecotypology (Figure 3a –f). Along PC1, this was most clearly
the case with the biogeographic affinity of fish species: whereas
most Boreal species showed negative or only slightly positive
PC1 values, most Lusitanian species had positive PC1 values
(Figure 3a). Given that the trend in PC1 loadings with time was
increasing linearly (compare Figure 2), this is in line with mostly
increasing trends for Lusitanian species (PC1 values .0) and by
comparison, more often declining trends for Boreal species (PC1
values ,0). ANOVA (Table 1) confirmed that differences in PC1
values between the biogeographic ecotypes were significant (p ,
0.0005; explaining 15.6% of the variation in PC1 values), Boreal
species having lower values than Lusitanian species (p ,
0.0005), and the six Atlantic species not differing significantly
from either of the other two types (p . 0.2).
The ecotypology with the second most significant pattern along
PC1 (14.3% of the variation explained, Table 1) was body size
(Figure 3f). Indeed, most large species showed negative PC1
values (associated with a high–low trend), and ecotypes of large
body size had significantly lower values of PC1 than medium or
small ecotypes (Table 1; ANOVA p , 0.001). A third ecotypology
with a significant pattern along PC1 was that of trophic level
(Table 1; ANOVA p ¼ 0.029; 7.4% of variation explained; cf.
Figure 3e). Higher trophic-level species had significantly (p ¼
0.022) lower PC1 values (a high–low trend) than medium-level
species (a low– high trend), although those of lower trophic level
did not differ from either the mid- or higher-level species (p .
0.2). Fourth, the vertical habitat ecotypology explained 4.9% of
variation along PC1, pelagic species showing significantly higher
values of PC1 than demersal species (Table 1; ANOVA p ¼
0.032). The other two ecotypologies did not reveal statistically significant differences in PC1 values between their respective ecotypes
(Table 1; ANOVA: horizontal habitat p . 0.3, and trophic guild
p . 0.05).
Along PC2 (Figure 3), the three ecotypologies biogeography,
body size, and trophic level did not reveal any significant patterns
(Table 1; ANOVA: biogeography p . 0.5, trophic level p . 0.2,
and body size p . 0.7). There was, however, evidence of patterns
along PC2 in both habitat ecotypologies. In terms of horizontal
habitat (Figure 3b), almost all slope (including outer shelf)
species displayed negative PC2 values, significantly lower than
both coastal and shelf species (Table 1; ANOVA p , 0.001;
explaining 14.1% of the variation in PC2). For vertical habitat
(Figure 3c), demersal species had significantly higher values of
PC2 than pelagic species (Table 1; ANOVA p ¼ 0.020; explaining
5.7% of the variation in PC2). This is in line with (very) low –
high–moderate trends more commonly found in demersal
species, and moderate–low –(very) high trends in pelagics
(compare with Figure 2b). The trophic guild ecotypology did
reveal a significant overall pattern along PC2 (Table 1; ANOVA
p ¼ 0.012; explaining 11.6% of the variation in PC2), but post
hoc paired comparisons showed that this was mainly attributable
to two contrasting ecotypes, planktivores having significantly
lower values of PC2 (moderate –low–high pattern) than
benthivores.
Shadeplots provide a means of visualizing the positioning
of all individual species along the PC axes as well as their
abundance trends. In Figure 4, all species are sorted according
to their PC1 values in descending order, so sharply increasing
species with high positive values of PC1, e.g. anchovy (Engraulis
Ecotypes as a concept for exploring responses to climate change in fish assemblages
585
Figure 3. Scatterplots showing the results of PCA of temporal changes in cpue in 95 North Sea fish species, with symbols showing the
coordinates of individual species along the first and second PC axes. In (a), species are colour-coded by biogeography; in (b) by horizontal and
in (c) by vertical habitat; in (d) by trophic guild; in (e) by trophic level (lower, ,3.5; medium, 3.5 –3.8; higher, .3.8); and in (f) by body size
(small, ,35 cm; medium, 35– 60 cm; large, .60 cm Lmax). For each ecotype, colour-coded ellipses show the 95% joint confidence regions for
the mean coordinates along PC1 and PC2. See Supplementary material for details of the species included.
encrasicolus), horse mackerel (Trachurus trachurus), pilchard
(Sardina pilchardus), and red mullet (Mullus surmuletus), are on
top, and strongly declining species with low negative PC1 values,
e.g. cod, wolffish (Anarhichas lupus), and redfish (Sebastes viviparus), at the bottom. On the right side of the figure, the ecotypology of all species is indicated according to biogeography, habitat,
trophic level, and body size class (trophic guild is not shown
here). Again it becomes apparent that biogeography and
(though less so) body size and trophic level are ecotypologies
that are fairly clearly separated: Boreal, often large (high trophic
level), species tend to be towards the bottom of the graph (decreasing trends), and Lusitanian, often small, species towards the top
(increasing trends). Note that nine of the ten lowest-ranking
species along PC1 (most decreasing) are Boreal ecotypes (only
one of small body size and two of lower trophic level) and that
nine of the ten highest-ranking species along PC1 (most increasing) are Lusitanian ecotypes (none of large body size, one of
higher trophic level).
For Figure 5, all species were sorted in descending order
according to their values of PC2. Towards the top (compare
586
G. H. Engelhard et al.
Table 1. ANOVA comparing PC values between contrasting ecotypes within six ecotypologies: biogeographic affinity, horizontal and
vertical habitat preference, trophic guild, trophic level, and body size.
ANOVA
Axis
PC1
PC2
Ecotypology
Biogeography
Horizontal habitat
Vertical habitat
Trophic guild
Trophic level
Body size
d.f.
2, 92
2, 92
1, 93
3, 88
2, 92
2, 92
F-value
8.479
0.981
4.756
2.667
3.686
7.6861
p-value
<0.0005
0.379
0.032
0.053
0.029
<0.001
Percentage
15.6
2.1
4.9
8.3
7.4
14.3
Biogeography
Horizontal habitat
Vertical habitat
Trophic guild
Trophic level
Body size
2, 92
2, 92
1, 93
3, 88
2, 92
2, 92
0.609
7.593
5.604
3.861
1.612
0.271
0.546
<0.001
0.020
0.012
0.205
0.763
1.3
14.1
5.7
11.6
3.4
0.6
Post hoc test (Tukey HSD)
Boreal , Lusitanian
Demersal , pelagic
Medium , higher
Large , (small, medium)
Slope , (coastal, shelf)
Pelagic , demersal
Planktivore , benthivore
Values of p , 0.05 are shown emboldened, and percentage is the percentage variation explained by each ecotypology (r 2). If a significant difference was
found, a Tukey honest significant difference test was applied for post hoc paired comparisons between ecotypes: the symbol “,” refers to the direction of
significant difference (p , 0.05).
with Figure 2b) are species with a trend matching very low –
high–moderate, e.g. eelpout (Zoarces viviparus), herring
(Clupea harengus), and bluemouth, whereas several species with
the reverse pattern of moderate –low–very high are towards the
bottom, e.g. blue whiting, and snake pipefish (Entelurus
aequoreus). None of the biogeography, trophic level, or body size
ecotypologies clearly separate along PC2 (see the right side of
the Figure; cf. Table 1). The exceptions were the horizontal and
the vertical habitat ecotypologies: horizontal habitat, with more
inner shelf/coastal species at the top of the Figure (PC2 . 0),
outer shelf/slope species at the bottom (PC2 , 0), and shelf
species having a wide range of either positive or negative PC2
values; vertical habitat, with relatively more pelagic than demersal
species having low negative values of PC2, accounting for the presence of many more demersal than pelagic species in this dataset.
Notably, cpue time-series revealed that many of the coastal/
inner shelf species showed rapid increases during the late 1970s
and mid-1980s, then stabilized towards marginally decreasing
abundance in the 1990s and 2000s. Conversely, many slope/
outer shelf species were in relatively great abundance during the
late 1970s and from the mid-1990s on, but at lesser abundance
during the intervening years.
Sensitivity testing of our analysis to examine whether or not the
way we treated zero values had any impact on the overall conclusions revealed that, in detail, the results of the study were
affected by the choice of methodologies for treating zero cpue
values to allow log-transformation, but that this had no impact
on the key conclusions. If zeroes were replaced by a fixed value
of 0.001 (instead of half the smallest non-zero cpue, as
implemented above), the sign of PC2 and associated ecotype coordinates was flipped (notice that the sign in PCA projections is arbitrary and can flip around). This was also the case if 0.001 was
added to all cpue values (zero and non-zero), but not if 0.005
was added. None of the alternative methodologies to treat zero
values resulted in anything more than a marginal shift in significance of the results from the ANOVA tests for differences in
PC1 or PC2 values between ecotype; p-values remained either consistently below or above the 0.05 significance level. Depending on
zero treatment, the detailed placement of individual species’ principal coordinates could shift slightly along the PC axes. For
example, redfish and cod swapped place as species with second
and third lowest PC1 coordinates, and likewise for horse mackerel,
pilchard, and red mullet as species with second to fourth highest
PC1 coordinates.
Discussion
We have here introduced the ecotype concept as a means to facilitate research on dynamics of species-rich communities, reducing
the complexity imposed by large numbers of species to a relatively
small number of ecotypes. The concept is applied to the North Sea
fish community as sampled by the IBTS during the years 1977–
2008, and important changes were found in community structure
that can be related to fish ecotype. PCA was used here as a broadbrush approach to examining the utility of the concept, by capturing the principal patterns of change in the North Sea fish community. Use of PCA was motivated by the regional integrated
assessment of the North Sea ecosystem (REGNS; Kenny et al.,
2009), but other approaches such as Canonical Correspondence
Analysis or Generalized Additive Modelling might have been
equally suitable for the task and might also have offered insight
into multifactorial ecotypes. Our results are to some extent influenced by data pretreatment choices, necessary to carry out the
PCA, in particular the inability of PCA to cope adequately with
zero values. Fortunately, a comparison of the outcome from different methodologies of handling zero values for log-transformation
and centring revealed that this has a marginal impact on the
outputs for particular species, and virtually no impact on the
overall conclusions.
Differences in trends between ecotypes were exemplified within
the biogeographic ecotypology by sharp increases in mean abundance of Lusitanian ecotypes relative to marginal increases or
declines in Boreal ecotypes. Further, within the trophic-level ecotypology, there were far greater mean increases in lower than in
medium- or high-trophic-level ecotypes, and within the vertical
habitat ecotypology, there were greater mean increases in pelagics
than demersals. Not all ecotypes within an ecotypology necessarily
showed differences in mean trends. For example, there was great
similarity between three of the four ecotypes within the trophic
guild ecotypology where trends were very similar. Therefore,
there is only partial support for our first hypothesis, that sets of
Ecotypes as a concept for exploring responses to climate change in fish assemblages
587
Figure 4. Shadeplot showing the changes in relative abundance (as anomalies of log-transformed cpue) during 1977 – 2008 for 95 North Sea
fish species, where the species are sorted according to their PC1 values in descending order. On the right side, the ecotypologies of all species
are indicated, as classified according to biogeography, horizontal habitat, vertical habitat, trophic level, and body size class.
588
G. H. Engelhard et al.
Figure 5. Shadeplot showing the changes in relative abundance (as anomalies of log-transformed cpue) during 1977 – 2008 for 95 North Sea
fish species, with the species sorted according to their PC2 values in descending order. On the right side, the ecotypologies of all species are
indicated, as classified according to biogeography, horizontal habitat, vertical habitat, trophic level, and body size class.
Ecotypes as a concept for exploring responses to climate change in fish assemblages
species assigned a priori to the same ecotype are likely to show significant differences in temporal trends when compared with sets of
species in contrasting ecotypes.
Despite there often being significantly different trends between
sets of species comprising ecotypes, there was also considerable
variation in the trends of species belonging to the same ecotype,
and indeed, all the ecotypology schemes together explained just
39.8% of the variance in PC1 and 25.7% of the variance in PC2.
When individual species were examined separately, the general
finding was that species belonging to different ecotypes did not
show clearly distinct cpue time-series trajectories; rather there
was considerable overlap in the patterns. This was revealed by
PCA scatterplots, in which none of the six ecotypologies examined
formed highly distinct clusters along PC axes. Hence, the dynamics
of a single species cannot be regarded as representative of those of
other species within its ecotype, so the ecotype concept is potentially useful in understanding community level rather than singlespecies effects of environmental and anthropogenic drivers
(Rijnsdorp et al., 2009). In particular, it should not be assumed
automatically that if some species of one ecotype show a distinct
temporal pattern, it will as a rule also be the case for other
species of the same ecotype.
The lack of representivity of a single species for its ecotype was
exemplified by herring, a pelagic species depleted in the North Sea
in the 1970s, and which subsequently recovered in the late 1990s,
but in recent years has been declining again (Payne et al., 2009).
With this marked low –high–low pattern, herring showed one of
the highest positive PC2 scores among the entire fish community;
by contrast, most other pelagics showed low negative PC2 values
(a high–low–high pattern). That one species is not to be seen as
a direct proxy for its ecotype is unsurprising if one considers
that species of the same ecotype according to one ecotypology
(here, vertical habitat), may well belong to different ecotypes
according to other ecotypologies, e.g. biogeography, trophic
guild. Another interpretation could be within-guild (withinecotype) compensation, sensu Auster and Link (2009): where
with functional redundancy and high spatial overlap in distribution of members of one ecotype, the role of a species in
decline is replaced by others with concomitant increases in
abundance. Therefore, to make generalizations about an ecotype,
a reasonable sample of species covering a range of trends needs
to be regarded.
Duplisea and Blanchard (2005) used an iterative method to
assign fish species to groups based on time-series covariance
(almost the inverse of the process followed here). The method
yielded reasonable aggregations of species that feed on similar
benthic food resources, although such species typically belonged
to very different taxonomic groups. It also indicated that several
heavily exploited species, such as cod and haddock, were not
assigned to the same group, as might have been anticipated a
priori, despite being impacted by similar human and climate
pressures.
In accord with our second hypothesis, when comparing the
different ecotypologies, that of biogeographic affinity explained
the greatest proportion of the variation (15.6%) along the PC1
axis. In particular, Boreal ecotypes were mainly characterized by
declining or only marginally increasing trends over the years
1977–2008, and Lusitanian ecotypes by increasing trends. In
close concordance, several studies recently reported increasing
prevalence of various species with southern biogeographic affinity
in the North Sea (Corten and van de Kamp, 1996; Beare et al.,
589
2004), northward distribution shifts (Perry et al., 2005), increased
distribution ranges of species of southern origin and decreasing
ranges of northern ones (Hiddink and ter Hofstede, 2007), and
a deepening shift (Dulvy et al., 2008). The notion that climate
change is currently positively affecting southern, warm-water
species in the North Sea, and negatively affecting northern ones,
is supported by an increasingly wide body of evidence for fish
(Quéro et al., 1998; Pinnegar et al., 2008; Cheung et al., 2009),
plankton (Beaugrand et al., 2003; Beaugrand, 2004; Pitois and
Fox, 2006) and intertidal taxa (Mieszkowska et al., 2006). There
is also evidence of differential responses to warming between
warm- and cold-water species for fish communities in the
Northwest Atlantic (Murawski, 1993; Collie et al., 2008; Nye
et al., 2009).
Two further ecotypologies with significant patterns along PC1
were body size and trophic level. Species classed as large generally
showed decreasing or only marginally increasing trends in abundance indices (lower PC1 values), and small species more often
low–high trends (often higher PC1 values). Analogously, species
belonging to the higher trophic-level ecotype had significantly
lower values of PC1 than medium trophic-level ecotypes. Given
that larger fish tend to feed at higher trophic levels, it comes as
no surprise that the time-series patterns in these two ecotypologies
are related (cf. Jennings et al., 2001, 2002). Both climate change
and fishing might have contributed to these changes. First, northern (Boreal) species on average have larger body size than southern
(Lusitanian) species and also tend to live longer (Atkinson and
Sibly, 1997). Polar gigantism, i.e. species in northern latitudes
attaining larger body size, has been well documented (e.g.
Atkinson and Sibly, 1997; Angilletta and Dunham, 2003), and
Bergmann’s Rule suggests that also within species, body size
tends to increase with a cooler environment. Several North Sea
fish species attain a larger size the farther north they live, e.g.
starry skate (Amblyraja radiata; Stehmann and Bürkel, 1984).
Second, as a result of commercial fisheries, large or slow-growing
species with late maturity typically decline in abundance more
rapidly than smaller, faster-growing species (Frid et al., 1999;
Jennings et al., 1999). With larger species generally feeding at
higher trophic levels, fishing is expected to reduce the mean
trophic level of exploited fish communities (Pauly et al., 2001).
Therefore, the significant patterns of both body size and
trophic-level ecotypologies along PC1 may also relate to the
phenomenon referred to as fishing down the foodweb (Pauly
et al., 2001), whereby commercial fisheries initially exploit and
deplete the larger, economically more valuable species, then gradually shift to smaller species and so lead to a reduction in mean body
size in the fish community. Such changes have been described for
the North Sea (Jennings et al., 2002) and elsewhere (Celtic Sea,
Pinnegar et al., 2002; Black Sea, Daskalov, 2002; northeastern
United States, Collie et al., 2008).
Both habitat ecotypologies (horizontal and vertical habitat)
revealed significant differences along the PC2 axis (Figure 2),
where high positive values would be indicative of a parabolic,
low–high–moderate abundance trend over the 1977–2008 timeseries. In terms of horizontal habitat, many inner shelf/coastal
species (with high values of PC2) showed increases from the late
1970s to the 1980s, then stabilized to somewhat declining abundance thereafter. For vertical habitat, this pattern was common
in demersal but rarely seen in pelagic species, with the abovementioned exception of herring. By contrast, outer shelf/slope
species tended to show the opposite pattern along PC2 with
590
declines up to the late 1980s but increases thereafter, and pelagics
(and planktivorous fish species) showed moderate mean abundance until the late 1980s but particularly strong increases from
the 1990s on. In accord, in the Northwest Atlantic, a progressive
shift with warming, from demersals to pelagics dominating two
coastal communities, has also been observed in the northeastern
United States (Collie et al., 2008). We suggest that the non-linear
temporal patterns along PC2, associated with both habitat ecotypologies might relate to the documented regime shift in the
North Sea from a cold to a warm biological regime, which took
place around 1989 (Reid et al., 2001) or slightly before
(Beaugrand and Ibanez, 2004); or to warm or cold episodic
events of shorter duration, which have also restructured the
North Sea phyto- and zooplankton community structure
(Edwards et al., 2001; Beaugrand, 2004). The cold episodic event
of 1978–1982 has been related to the “Great Salinity Anomaly”,
a pulse of cold, low salinity water that entered the North Sea
from the North Atlantic in the late 1970s (Dickson et al., 1988).
This short period of particularly low temperature coincided with
very low phytoplankton indices (Edwards et al., 2001) and calanoid copepod abundance, except for Subarctic species including
Calanus finmarchicus, which increased (Beaugrand, 2004). The
warm episodic event of 1989–1991 led to increases in phytoplankton (Edwards et al., 2001) as well as total numbers of calanoid
copepods of various biogeographic affinity, except for Subarctic
species such as C. finmarchicus, which decreased (Beaugrand,
2004). This might explain why many pelagic fish species
(feeding on zooplankton) with low negative values of PC2 initially
decreased during the late 1970s cold episodic event, but later
increased from the late 1980s on (a warm-biological regime).
The opposite pattern observed in herring could relate to the similarly reversed pattern of its main prey C. finmarchicus (Beaugrand
and Ibanez, 2004), although fishery effects have also been a dominating factor in herring population dynamics (Payne et al., 2009).
In summary, the past three decades have seen a steady increase
of many Lusitanian, small-bodied, low-/mid-trophic-level ecotypes, and a steady decline (or at the most a marginal increase)
of most Boreal, large-bodied, high-trophic-level ecotypes.
Intriguingly, of no less than 95 species included in our analysis,
two charismatic species, cod and wolffish, showed the lowest
values along PC1 associated with the most marked declines.
Both are boreal, demersal, and of large body size; cod is of high
trophic level, wolffish of lower trophic level but feeding on large
molluscs. Indeed the ecotype characteristics of these two species
according to a range of ecotypologies appear to have conspired
to make them particularly vulnerable to climate change and
fishing (cf. Jennings et al., 1999; Beaugrand et al., 2003). Still,
although cod and wolffish as species fit the ecotype concept and
our preconceptions neatly, we argue that the concept is less suitable to draw conclusions for single species than for fish assemblages and communities (Dulvy et al., 2008; Tulp et al., 2008;
Rijnsdorp et al., 2009).
We have used a single-ecotype approach to analyse North Sea
fish community change, analysing different ecotypologies separately, one at a time. A possible extension of this methodology
would be to use multidimensional ecotypes, e.g. Boreal –large –
high trophic level, Lusitanian –small –low trophic level.
Multidimensional ecotypes might be better at explaining community change than single-dimension ecotypes, although the total
number of possible combinations could become unmanageable.
We conclude that an ecotype concept whereby species or groups
G. H. Engelhard et al.
of species are examined according to a priori defined ecotypes,
where possible using different ecotypologies (biogeography,
habitat, etc.) can be a meaningful and potentially useful way of
examining how climate change or other pressures may impact
the wider regional fish community. The concept may well be applicable too to other policy-relevant questions, and extendable to
other animal groups and plants.
Supplementary material
Supplementary material is available at ICESJMS online. It is a
taxonomic listing of fish species recorded from or about the
North Sea, including classifications of their ecotypes according
to ecotypologies: biogeographic affinity, horizontal and vertical
habitat preference, trophic guild, trophic level, and body size.
Source of information on presence in the North Sea is indicated,
and information on trophic level is derived from FishBase
(Froese and Pauly, 2007). The listing is reasonably exhaustive,
but may exclude some rare vagrants; moreover, species new to
the North Sea continue to be reported occasionally.
Acknowledgements
The study formed part of the EU FP6 project RECLAIM
(Resolving the Impacts of Climate Change on Fish and Shellfish
Populations), with additional funding from the UK Department
for Environment, Food and Rural Affairs (Defra) contracts
MA010 (Fisheries Supporting Studies) and MF1108 (100 Years
of Change). Adriaan Rijnsdorp, Sophie Pitois, Andrew Kenny,
David Maxwell, and three anonymous reviewers gave valuable
feedback on earlier drafts, and we particularly acknowledge the
contribution of editor Verena Trenkel in focusing our ideas.
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