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Climate change affects demography, geographic distribution and phenology of populations and species. Demographic effects are manifest as changes in recruitment, growth and survival (O’Brien et al. 2000; Pörtner & Knust 2007), distributional shifts as movements towards the poles or higher altitudes (Walther et al. 2002; Parmesan & Yohe 2003), and phenological effects as advances in the timing of spring-related events by > 2·3 days decade−1, with earlier flowering, egg-laying, plankton blooms and fish migrations creating potential for mismatching between and predator and prey populations (Crick & Sparks 1999; Sims et al. 2001; Parmesan & Yohe 2003; Edwards & Richardson 2004). Climate change-induced habitat loss and changing species distributions are predicted to result in species extinctions on land and population extinctions in the sea (Thomas et al. 2004; Drinkwater 2005). There is an increasing need to summarize the ecological complexity of climate impacts using biological indicators to inform managers, policymakers and society (EEA 2004; MCCIP 2006).
Climate variability and longer-term change (hereafter called climate change) have led to marked changes in North East Atlantic conditions over the last century (Cushing 1982; Stenseth et al. 2005). Sea surface temperatures of North Atlantic and UK coastal waters have warmed by 0·2–0·6 °C decade−1 over the past 30 years. These seas are warming faster than the adjacent land and faster than the global average (MacKenzie & Schiedek 2007). Within the North East Atlantic region, warming was fastest in the English Channel, North Sea and Baltic Sea (ICES 2006a; Joyce 2006; Marsh & Kent 2006; Sherman et al. 2007). Some marked changes in North Sea fish distributions have been attributed to climate change: two-thirds of North Sea fishes have shifted mean latitude or depth. Fishes with a northern distributional boundary in the North Sea have shifted northwards and southern boundary species have retracted northwards at rates up to three times faster than terrestrial species (Perry et al. 2005). Exotic fishes with southerly biogeographic affinities are becoming established in the North Sea, including; anchovy Engraulis encrasicolus L., red mullet Mullus surmuletus L., sardine Sardina pilchardus, Walbaum 1792, John Dory Zeus faber, L. and snake pipefish Entelurus aequoreus, L. (Beare et al. 2004; ICES 2006b; Kirby, Johns & Lindley 2006; Enghoff, MacKenzie & Nielsen 2007).
A key question is whether the individual responses of species are context-specific phenomena or whether they are symptomatic of a more systematic change in the North Sea ecosystem resulting from climate change. If such an ecosystem-scale change can be detected, this could underpin the development of a biotic indicator of climate change impacts. There is a wide range of desirable indicator properties, including specificity to a single pressure, sensitivity or strength of response, the lag in response and the spatial and taxonomic representativeness of the indicator (Rice & Rochet 2005). Here we summarize the effects of climate change on the demersal fish assemblage and develop an indicator that is taxonomically representative of a wide range of fish species.
We search for an assemblage-wide biotic indicator of climate change in the North Sea ecosystem by comparing the distribution changes of fish species and assemblages to temperature and climate change over the past 25 years. For each year, we calculated the distance moved north or south and the deepening and shallowing of each fish species or assemblage relative to the long-term average. Species distributional responses were aggregated into non-mutually exclusive assemblages reflecting differences in physiology, ecology, biogeographic origin and human impact. We demonstrate a coherent deepening of fish species in response to climate change and two distinct latitudinal responses to climate change: a northward shift in mean latitude and southward extension of minimum latitude.
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We used the North Sea English groundfish survey data to assess changes in the geographic distribution of 28 demersal fish species. The English Groundfish Survey (EGFS) samples a grid of trawl stations typically covering up to 84 statistical rectangles (between 51·75 to 61·75° N latitude) and has been fished annually throughout the North Sea as part of the International Council for the Exploration of the Sea (ICES) international bottom trawl survey in autumn (August–October). All fishes caught were identified and measured. Catch rates were raised to number of individuals caught per 60-min tow (for more details see Maxwell & Jennings 2005).
Species were included if they were reliably identified throughout the time period and effectively sampled by the net (Sparholt 1990; Knijn et al. 1993; Maxwell & Jennings 2005; Dulvy et al. 2006). Pelagic fish were excluded because of the likelihood that they were captured in the water column during net shooting or hauling. The 28 species retained for analysis were representative of the breadth of morphology, life histories, ecology and taxonomic diversity of the bottom-dwelling fishes sampled by the survey (Table 1) and represent most of the numerical abundance and biomass of the demersal fish assemblage (Jennings et al. 2002). The Latin names for all study species are presented in Table 1; hereafter, only common names will be used.
Table 1. Demersal North Sea fish species surveyed by the English Groundfish Survey, body size (cm), biogeographic affinity and thermal characteristics (°C), exploitation status, categorical numerical abundance and spatial occupancy and presence of a northern or southern range boundary. Thermal classification: W, warm thermal preference; C, cold thermal preference; g, generalist with broader thermal range; s, specialist with narrow thermal range. Numerical abundance: LA, less abundant; A, abundant. Spatial occupancy: LC, less common; W, widespread
|Common name||Latin binomial||Body size||Biogeographic affinity||Mean temperature||Temperature range||Thermal classification||Exploitation status||Abundance category||Spatial occupancy category||Range boundary|
|Pogge||Agonus cataphractus L.||20||Boreal||15·4||3·9||Cs||Non-target||LA||LC||N|
|Wolffish||Anarhichas lupus L.||125||Boreal||13·4||2·4||Cs||Bycatch||LA||W||S|
|Scaldfish||Arnoglossus laterna (Walbaum, 1792)||25||Lusitanian||16·4||3·2||Ws||Non-target||LA||LC||N|
|Solenette||Buglossidium luteum (Risso, 1810)||13||Lusitanian||16·4||4·5||Wg||Non-target||A||LC||N|
|Grey gurnard||Eutrigla gurnardus L.||45||Lusitanian||17·0||3·6||Ws||Bycatch||A||W||–|
|Cod||Gadus morhua L.||132||Boreal||13·8||2·3||Cs||Target||A||W||–|
|Witch||Glyptocephalus cynoglossus L.||60||Boreal||13·3||3·3||Cs||Bycatch||LA||W||S|
|Long rough dab||Hippoglossoides platessoides (Fabricius, 1780)||30||Boreal||13·8||2·4||Cs||Bycatch||A||W||–|
|Megrim||Lepidorhombus whiffiagonis (Walbaum, 1792)||61||Lusitanian||13·3||2·7||Cs||Bycatch||LA||LC||S|
|Dab||Limanda limanda L.||42||Boreal||17·0||4·5||Wg||Bycatch||A||W||S|
|Angler||Lophius piscatorius L.||75||Lusitanian||13·4||2·2||Cs||Target||LA||W||S|
|Haddock||Melanogrammus aeglefinus L.||76||Boreal||13·7||2·4||Cs||Target||A||W||–|
|Whiting||Merlangius merlangus L.||45||Lusitanian||13·2||3·2||Cs||Target||A||W||S|
|Hake||Merluccius merluccius L.||110||Lusitanian||13·8||5·8||Cg||Target||LA||W||S|
|Lemon sole||Microstomus kitt (Walbaum, 1792)||60||Boreal||15·2||2·3||Cs||Target||A||W||S|
|Ling||Molva molva L.||200||Boreal||13·1||2·1||Cs||Target||LA||LC||–|
|Plaice||Pleuronectes platessa L.||95||Lusitanian||17·0||4·4||Wg||Target||A||W||–|
|Saithe||Pollachius virens L.||130||Boreal||13·4||2·7||Cs||Target||A||W||S|
|Cuckoo ray||Leucoraja naevus (Müller & Henle, 1841)||70||Lusitanian||12·6||1·8||Cs||Bycatch||LA||LC||S|
|Starry ray||Amblyraja radiata (Donovan, 1808)||60||Boreal||13·7||2·4||Cs||Non-target||A||W||–|
|Four-beard rockling||Rhinonemus cimbrius L.||41||Boreal||13·9||4·6||Cg||Non-target||LA||LC||S|
|Lesser spotted dogfish||Scyliorhinus canicula L.||75||Lusitanian||12·4||2·1||Cs||Bycatch||LA||LC||S|
|Sole||Solea solea L.||60||Lusitanian||17·2||4·8||Wg||Target||LA||LC||S|
|Spurdog||Squalus acanthias L.||105||Atlantic||15·0||2·5||Cs||Bycatch||LA||W||–|
|Lesser weaver||Trachinus vipera (Cuvier, 1829)||15||Lusitanian||17·2||4·5||Wg||Non-target||A||W||S|
|Norway pout||Trisopterus esmarki (Nilsson, 1855)||25||Boreal||13·6||3·2||Cs||Target||A||W||S|
|Bib||Trisopterus luscus L.||46||Lusitanian||17·6||4·4||Wg||Non-target||LA||LC||N|
|Poor cod||Trisopterus minutus L.||40||Lusitanian||16·6||3·5||Ws||Non-target||A||W||N|
Species were categorized into a number of assemblages based on their thermal physiology, ecology, biogeography and exploitation status (Table 1). These assemblages are not mutually exclusive and each species appears in one or more assemblage categorization. This approach allows the identification of those traits most related to the climate change response with greater statistical power afforded by combining data from more than one species (Maxwell & Jennings 2005).
The autumn thermal preference of each fish species was described using: (i) the most preferred temperature, and (ii) the range of the preferred temperatures (for details see Supplementary Appendix S1). The preferred temperatures of fishes were bimodally distributed: species preferring temperatures below 15·5 °C were classified as relatively cold-tolerant and those preferring temperatures above that level as warm-tolerant. Most species (n = 21) had narrow thermal ranges spanning less than 4 °C; a few species had slightly wider thermal ranges, such as dab, sole, solenette, lesser weaver, bib, plaice, four-bearded rockling and hake (Table 1).
We used body size as a proxy measure of ecological performance. Body size is a good descriptor of life history and demography and also of production, consumption and metabolism (Reynolds et al. 2005; Jennings, De Oliveira & Warr 2007). Large-bodied species were defined as the 18 species with a maximum length ≥ 60 cm (Table 1). Species with numerical abundance lower than (or greater than) median numerical abundance were categorized as less abundant or abundant, respectively. The spatial extent of occurrence was measured as the mean number of ICES statistical rectangles occupied, and less common (or widespread) species had less than (or greater than) the median number of rectangles.
The biogeographic affinities [boreal (northern) and Lusitanian (southern)] of each species were derived from the scientific literature (Wheeler 1969; Yang 1982). Exploitation status was based on stock assessment reports and regional atlases, and species were categorized as ‘target’, ‘bycatch’ and subject to some fishing mortality and ‘non-target’.
Species’ geographic distributions were summarized using the centre of distribution estimated as the mean latitude weighted by the natural log of the mean abundance (survey catch) in each statistical rectangle (Rindorf & Lewy 2006). We used four measures of geographic distribution: the mean latitude, minimum latitude, maximum latitude and mean depth. Change in distribution was standardized by calculating anomalies of the departure from the mean over the 25-year study period. Latitude anomalies were converted from degrees to kilometres. Positive latitude anomalies represent northward change in species’ centre of distribution, whereas positive depth anomalies represent shallowing. Assemblage-scale distribution measures were calculated from the average of geographic anomalies across component species. All relationships between geographic response and time or a climate variable were tested using robust regression (Venables & Ripley 2002).
A systematically changing survey distribution could confound the detection of climate-related geographic shifts. The number of survey stations has varied over time particularly during 1980–1984, but since then a relatively constant grid of > 70 stations have been surveyed each year. In spite of the changing number of stations in the early period, mean depth and mean latitude of the stations has remained stable and the interannual variation in survey distribution explained relatively little interannual variance in fish distributions, except for the redfish Sebastes viviparus Krøyer, 1845 which was excluded from the analysis.
Long-term environmental data were provided by ICES (http://www.ices.dk). For the time series analysis, bottom temperatures (from the lower half of the water column) were averaged for winter (January–March) for 80 0·5° × 1° ICES statistical rectangles (there were insufficient replicate stations (< 15 rectangles) to perform an equivalent analysis for the summer period). Southern North Sea salinity data are collected from near-surface waters by ferries travelling between Harwich and Rotterdam at weekly intervals at approximately 52° N (Joyce 2006). The data were averaged by month and a winter mean taken for January–March. The North Atlantic Oscillation Index (NAOI) is the normalized sea level pressure difference between Gibraltar and Iceland. An annual index was calculated by averaging the winter (December–February) values and the data were sourced from http://www.cru.uea.ac.uk/cru/data/nao.htm (Jones, Jonsson & Wheeler 1997). The Gulf Stream Index (GSI) is a measure of the latitudinal height of the north wall of the Atlantic Gulf Stream and was sourced from web.pml.ac.uk/gulfstream/inetdat.htm (Taylor & Stephens 1980). GSI is not directly linked to North Sea conditions but is an indicator of regional North Atlantic climate. A composite index of North East Atlantic climate change was calculated as the first principal component axis of the 5-year running averages of five variables (winter bottom temperature, NAO, GSI, salinity and inflow). We used right-aligned 5-year running means calculated from the current year and the four previous years to approximate a fish's lifetime environmental experience. North Atlantic Current inflow into the North Sea is linked to regional climate variability, local biological productivity and fish recruitment success (Reid et al. 2003; Pingree 2005; ICES 2006a). Monthly predictions of net inflow across a section between Shetland and Orkney were derived from runs of a coupled physical, chemical and biological model system (NORWECOM) (Skogen et al. 1995). Water transport was measured in Sverdrups (106 m3 s−1) and increasing negative values represent greater southward inflow of Atlantic water. A demersal exploitation rate was calculated for each year between 1980 and 2003 as the catch-weighted sum of demersal fish fishing mortalities, as estimated in ICES North Sea stock assessments, for cod, haddock, saithe, whiting, plaice, and sole (Daan et al. 2005).
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We present evidence for a coherent deepening of the North Sea fish assemblage in response to climate change. The rate of deepening of the whole assemblage was 3·6 m decade−1 and for individual species ranges up to 10 m decade−1. This rate of deepening is analogous and comparable to upward altitudinal response of terrestrial organisms, which averages 6·1 m decade−1 (Parmesan & Yohe 2003). Before considering the indicator properties of the deepening of the demersal fish assemblage, we consider these three questions: (i) What is the ecological significance of deepening fishes? (ii) Why is the deepening response more coherent than the latitudinal response? (iii) Are changes in fish distribution largely a consequence of fisheries exploitation?
The ecological significance of upward-shifting alpine fauna is readily apparent. These species face shrinking habitats and greater likelihood of extinction (Grabherr, Gottfried & Paull 1994). However, the ecological significance of the deepening of the North Sea bottom-dwelling fishes is less clear. The ecological consequences may be more critical for geographically-restricted species that cannot deepen or shift to remain within their preferred temperature range in response to climate change. One such species, the eelpout Zoarces viviparous, L. 1758, has declined due to rapid warming in the shallow enclosed Wadden Sea (Pörtner & Knust 2007). For many coastal and offshore fishes, however, the geographic barriers to the shift of fishes toward thermally optimal habitats in deeper northerly waters are less apparent. However, the comparatively smaller area of deeper habitats > 80 m, in the North Sea suggests that deeper-dwelling shelf species (e.g. megrim) are more likely to be limited by habitat availability.
The deepening response was more coherent than the heterogeneous latitudinal response. The weak latitudinal response arises because it is a composite of two opposing latitudinal responses displayed by two ecologically distinct components of the demersal fish assemblage. The climate-driven northward shift in mean latitude of widespread abundant species has already been well-documented, along with some southward-shifting exceptions (Perry et al. 2005). We examine these exceptions further and find the southward shift of warm-tolerant southern species is consistent with the effects of (i) winter inflows of warm water into the northeastern North Sea in winter (Norway pout), and (ii) the warming and increasing availability of shallow winter habitats in the southern North Sea (e.g. sole, solenette and scaldfish). The southerly shifts in fish distributions may result from the peculiarities of winter hydrography in the North Sea (Holliday & Reid 2001; Perry et al. 2005). In winter, the Scottish east coast and central southern North Sea temperatures are comparable and relatively warm (~5–6 °C), and the coldest areas are found in the shallow coastal waters, particularly in the southeast (Fig. 2b). The relatively warm winter temperatures in the northwestern North Sea are apparent during positive NAO phases which result in stronger inflow of warmer North Atlantic Current waters (Edwards et al. 2002; Pingree 2005). Consequently, the main route into the North Sea for southern warm-tolerant species can be via the Shetland–Orkney gap as well as the English Channel. Indeed, many warm-water species first appear in the northwestern North Sea before expanding southward, such as the John Dory and snake pipefish which invaded earlier this decade (Ehrich & Stransky 2001; ICES 2006b, p. 82; Kirby et al. 2006; Harris et al. 2007).
Southern North Sea species were previously excluded from large areas of shallow inshore habitat in winter because these waters cool down to ~1 °C (Anonymous 1981). For example, sole overwinter in deeper warmer waters before returning to the shallows in spring (Henderson & Seaby 2005). There is anecdotal evidence that sole are arriving inshore earlier due to the rapidly warming seas (R. Millner, personal communication). We hypothesize that the southward shift of smaller, warm-tolerant southern species is due to increased warming and availability of shallow inshore habitat in winter and spring, although small species may have also benefited from the overexploitation of their predators (Daan et al. 2005). To summarize, the contrasting latitudinal responses of two ecologically distinct groups of fishes are consistent with climate change and the hydrographic conditions in the North Sea, and combining both results in an overall lack of latitudinal response.
A key question is whether the distribution changes of demersal fishes are a consequence of fisheries exploitation. Two lines of evidence suggest fisheries exploitation may contribute to changing fish abundance and distribution. First, exploitation influences the age structure, abundance and occupancy of target populations which might change their responsiveness to climate warming (Fisher & Frank 2004; Rindorf & Lewy 2006). Secondly, some coldwater species, such as Atlantic cod, are now relatively rare, yet were previously abundant in comparably warm stages such as the Stone Age (Atlantic period, 7000–3900 bc) and the latter part of the medieval warm period (c. 1200 ad) (Bolle et al. 2004; Enghoff et al. 2007). This suggests fisheries exploitation may be more important than warm temperature in determining the abundance of such species (Enghoff et al. 2007).
Understanding the relative contribution of fishing and climate change in determining North Sea fish dynamics has been the ‘holy grail’ of the European fisheries science community. The spatial pattern of fishing may change fish distributions in a manner similar to that expected from climate change. Fishing effort, particularly by beam trawls, has been greater in the southern North Sea compared to the northern part (Jennings et al. 2000). If a species was comprised of several subpopulations across its geographic range, then those in the more heavily fished areas would be depleted more than those in the less heavily fished areas, and this might be seen as having an effect on the range of the species. Ideally, any biotic indicator would respond specifically to a single driver or pressure (e.g. climate change) and be less specific and responsive to other pressures, (e.g. exploitation or eutrophication) (Rice & Rochet 2005). The climate response of the depth anomaly is relatively independent of fishing mortality and consistent across assemblages of species exposed to different levels of fishing mortality (Fig. 7). The lack of depth response of non-target species reflects the ecology and spatial pattern of winter warming of the North Sea rather than the absence of exploitation per se. These non-target southern North Sea species are responding differently to climate change by expanding southward. While there is little doubt that fisheries exploitation has had major effects, particularly on the abundance of fish populations, this analysis suggests that the depth response of the assemblage is highly specific to climate change.
Figure 7. Exploitation, climate and depth change of (a) all, (b) target, (c) bycatch, and (d) non-target demersal fishes, (e) a composite climate index and (f) a demersal exploitation index. (a–d) The solid line is the 5-year running mean of the first principal component axis representing climate change (e). Positive values indicate shallower distribution with negative anomalies representing deepening.
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The deepening response of the demersal fish assemblage to temperature could be used as one indicator of the biological effects of climate change in the North Sea and other semi-enclosed seas. The deepening response has a number of useful indicator properties, including high temperature sensitivity and high specificity to climate change (rather than to fishing). These indicators are readily measurable using routinely collected survey data, have high taxonomic representation of changes in the demersal fish assemblage of the North Sea ecosystem, and can be readily communicated to non-specialist audiences. However, the responsiveness of the depth (or latitude) indicator to temperature is relatively low, reflecting conditions in the current and preceding 4 years more strongly than in the present season or year. This is not surprising given the multiple direct and indirect pathways through which climate and environment influence population and assemblage dynamics and community turnover times (Salen-Picard et al. 2002; Blanchard et al. 2005; Rindorf & Lewy 2006). The lagged response suggests that the depth and latitude indicators are best suited for medium-term surveillance of the ecological effects of climate. We suggest that a latitude indicator may be more appropriate for north–south- oriented shelf seas (e.g. Iberian Peninsula or Bay of Biscay), and a depth indicator may be more suited to semi-enclosed seas (e.g. Mediterranean or Baltic Seas).
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Appendix S1. Thermal preferences of North Sea demersal fishes
Appendix S2. The effect of bottom temperature, year, and exploitation on the depth anomaly of the combined North Sea demersal fish assemblage
Fig. S1. The probability distribution of bottom temperatures encountered by the English Groundfish Survey in autumn from 1980–2004.
Fig. S2. Autumn thermal profiles of (a, b) saithe and (c, d) scaldfish.
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Please note: Wiley-Blackwell is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.