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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 581 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 582 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 583 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. 584 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). 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