Not to be cited without prior reference to the author ICES CM 2009/G:11

Comparative study of climate impact on coastal and continental shelf ecosystems in the ICES area: assessment and management.

RECENT CLIMATIC CHANGES IN THE SE BAY OF AFFECTING PELAGIC AND COASTAL ECOSYSTEMS.

V. VALENCIA1, A. FONTÁN1, A. BORJA1, N. GOIKOETXEA1 and J. SÁENZ2.

1AZTI Foundation, Marine Research Division. Herrera Kaia, Portualdea, z/g, 20110-Pasaia (). Tel: +34-943-004800; fax: +34-943-00480. E-mail: [email protected] 2Department of Applied Physics II, Fac. of Science and Technology, University of the Basque Country, Barrio Sarriena s/n, 48940-Leioa (Spain).

Abstract Troughout the last decade, several regime shifts and anomaly patterns for different climatic indices (ENSO, NAO, EA, etc.) have been described, due to unusual values and/or persistent cumulative anomalies. For the inner (southeastern) , the prevalence of positive values of the East Atlantic (EA) pattern, since 1998, affects the transport and subsequent properties of the upper water masses. The mesoscale effect, related mainly to the intensification of the British Isles low atmospheric pressure centre, drives also the moisture transport, storm frequency and intensity, etc. As a consequence of the shift in the EA pattern, several structural factors of the coastal and pelagic ecosystems show seasonal and/or annual anomaly patterns, in recent years. For instance, assessment of the recruitment of the Bay of Biscay anchovy, as well as of the benthic communities (macroalgae, barnacles, etc.), based upon climatic and oceanographic variables, show also responses to these anomaly patterns. Factors such as the turbulence-stability and upwelling-downwelling dualities; saline stratification and coastal fertilisation by precipitation and continental runoff; and other coupled oceano-meteorological variables are considered. The patterns observed are representatives of the response, in terms of local and seasonal or annual anomalies in the coastal and pelagic ecosystems, to the shifts in some mesoscale or large scale climatic indices such as the EA pattern. Keywords: oceano-meteorological coupling, pelagic ecosystem, East Atlantic pattern, Bay of Biscay.

Introduction Throughout the last decade, several regime shifts and anomaly patterns for different modes of atmospheric and oceanic variability (ENSO, NAO, EA, etc.) have been described, due to unusual values and/or persistent cumulative anomalies (Conrad et al., 2003; Bode et al., 2006; Beaugrand, 2009; Drinkwater et al., 2009). Consequently, there has been a growing concern about changes in climate in the North Atlantic Ocean. Many studies concerning decadal changes in climate and ecosystems are being undertaken: invasive species management (Occhipinti- Ambrogi, 2007; Rahel et al., 2008); changes in biodiversity (Beaugrand et al., 2008; Hemery et al., 2008; Menge et al., 2008; Molinero et al., 2008); or impacts on fisheries (Stenevik and Sundby, 2007; Travers et al., 2007; Tourre et al., 2007; deYoung et al., 2008; Hiddink and ter Hofstede, 2008; Cury et al., 2008; Borja et al., 2008). Such changes in climate are related often to changes in climatic indices. The North Atlantic climatic variability is driven largely by the North Atlantic Oscillation (NAO). The second main pattern in the Atlantic basin is the East Atlantic pattern (EA) (Conrad et al., 2003). Whilst the variability of climate linked to the NAO has been widely studied so far (Hurrell and Deser, 2009), the impacts of the EA on the climate has not been so widely documented (Wallace and Gutzler, 1981). The wintertime NAO exhibits significant multi-decadal variability (Hurrell, 1995; Parsons and Lear, 2001). The negative phase of the NAO dominated the circulation from the mid-1950's through the 1978/79 winter. An abrupt transition, to recurring positive phases of the NAO, occurred during the 1979/80 winter, with the atmosphere remaining constrained within this mode through to the 1994/95 winter season. During this 15-year interval, a substantial negative phase of the pattern appeared only twice, in the winters of 1984/85 and 1985/ 86. However, November 1995 - February 1996 (NDJF 95/96) was characterised by a return to the strong negative phase of the NAO (Halpert and Bell, 1997). Also, the EA pattern exhibits very strong multi-decadal variability in the 1950-2004 record, with the negative phase prevailing during much of 1950- 1976, and the positive phase occurring during much of 1977-2004. The positive phase of the EA pattern was particularly strong and persistent during 1997-2004 (Climate Prediction Center, NOAA). The changes in climate, as illustrated by changes in climatic indices, result in changes in atmospheric/oceanic variables, such as: local solar incoming radiation and temperature, moisture transport and regional rainfall, circulation and stratification, among others (Sáenz et al., 2001a; Trigo et al., 2002; Krichak and Alpert, 2005; Sutton and Hodson, 2005). Finally, these effects are transmitted to marine ecosystems, with substantial impacts on the species distribution and abundance (Parsons and Lear, 2001; Southward et al., 2005; Bode et al., 2006; Mackenzie et al., 2007; Hemery et al., 2008; Hiddink and ter Hofstede, 2008; Drinkwater et al., 2009). Within the Northeastern Atlantic, coupling mechanisms between climatic indices and water masses properties (Eastern North Atlantic Central Water: ENACW) and circulation (Iberian Poleward Current (IPC), North Atlantic Current (NAC), etc.) have been documented (Pérez et al., 2000; García-Soto et al., 2002; Pingree, 2005). The correlation level between atmospheric and oceanic patterns depends on the spatial scale, as well as the integration period considered. Although the NAO influences greatly the circulation in the North Atlantic, its influence is less significant in the Northeastern Atlantic, especially in the intergyre zone and the inner Bay of Biscay. Within the Bay of Biscay, the NAO influences to a lesser extent, when comparing with that observed at the North Atlantic. The most influential atmospheric pattern appears to be the EA, particularly for the southeastern Bay of Biscay, by means of the influence of a low pressure centre to the west of the British Isles. Several studies have demonstrated that, over the area adjacent to the Bay of Biscay, the EA pattern is related to the variability of: precipitation through the position of the Atlantic storm track (Rogers, 1997); winter land temperature through heat fluxes (Sáenz et al., 2001a); anchovy recruitment (Borja et al., 2008); or oceanic latent heat fluxes (Cayan, 1992), amongst others. The British low pressure centre determines the prevalence of northwesterly wind conditions over the southeastern Bay of Biscay. This wind regime modulates, in turn, air temperature and precipitation. Conversely, the south-southewesterly regime (in winter) and the north-northeasterly regime (in summer) are related to the position of two centres of activity: the Azores High and the Iceland Low. Within this context, the influence of wintertime NAO pattern in the atmospheric/oceanic variables can be anticipated in the southeastern Bay of Biscay; however, it accounts for a much lower fraction of variance, than the EA index (Sáenz et al., 2001a, b). Additionally, the EA index influences the water circulation patterns, since the relative occurrence of ENACWT y ENACWP (sensu Ríos et al., 1992) in the area is related to events of intensification or moderation of the eastward and poleward transports (Valencia et al., 2003). Moreover, this index influences the upwelling-downwelling balance over the area (Borja et al., 2008). In this context, the aims of the present study are to: (i) examine the anomalous patterns observed within the 1998-2008 period; and (ii) discuss the potential impact on pelagic and coastal ecosystems, in the southeastern Bay of Biscay.

Data and Methods

Study area The study area is located in the innermost part of the Bay of Biscay (Basque coast), lying between the west-east oriented coast of Spain and the north-south oriented coast of France (Figure 1).

49º N 500 m 2000 m

47º N FRANCE

NOAA 45º N BAY OF BISCAY AQUARIUM San Sebastián 43º N MO

SPAIN

41º N 10º W 8º W 6º W 4º W 2º W 0º W Figure 1. Location of the study area, showing the position of the data series. Bathymetric contours show the 200 m and 500 m isobaths. Key: MO - Meteorological Observatory of San Sebastián; NOAA - PFEL-NOAA; and AQUARIUM - Aquarium of San Sebastián (Oceanographic Society of Gipuzkoa).

The Basque coast is clearly a marginal area of the northeastern Atlantic and even of the Bay of Biscay itself; it has some distinctive climatic and geographic characteristics. Thus, the concavity of the southeastern corner of the Bay of Biscay results in a continental influence in this region and, consequently, the shelf waters of the area are colder in winter and warmer and less saline in summer, than the waters of western areas at equivalent latitudes (Valencia et al., 2003, 2004).

Oceanographic and meteorological data A description of the available data, including their source, record length and sampling rate, is presented in Table 1. Further, the location of the monitoring sampling stations is shown in Figure 1. The meteorological data were obtained from the Observatory of San Sebastián (Spanich Meteorological Agency); SST daily data were obtained from the Aquarium of San Sebastián (Oceanographic Society of Gipuzkoa); and vectorial data of wind velocity were provided by the PFEL-NOAA.

Climatic indices NAO and EA indices were selected for use in this investigation. Such indices were obtained from the Climate Prediction Centre (CPC) of the National Centre of Environmental Prediction (NCEP) (http://www.cpc.noaa.gov/). One of the most prominent climatic patterns throughout all seasons, is the NAO (Barnston and Livezey 1987). The NAO combines parts of the East-Atlantic and West Atlantic patterns, identified originally by Wallace and Gutzler (1981) for the winter season. The NAO consists of a north-south dipole of anomalies, with one centre located over Greenland and the other centre (of opposite sign) spanning the central latitudes of the North Atlantic, between 35°N and 40°N. Strong positive phases of the NAO tend to be associated with below-average temperatures across southern Europe; they are associated also with below-average precipitation over southern and central Europe. Contrasting patterns of temperature and precipitation anomalies are observed typically during strong negative phases of the NAO. The EA pattern is the second predominant mode of low-frequency variability over the North Atlantic. It is most prominent in autumn and winter (Barnston and Livezey 1987; Conrad et al., 2003) and is characterised by three centres: one located to the southwest of the Canary Islands (25°N, 25°W), another to the west of Great Britain (55°N, 20°W), and a third near the Black Sea (50°N, 40°E). The anomaly centres of the EA pattern are displaced southeastward, in relation to the approximate nodal lines of the NAO pattern. The positive phase of the EA pattern is associated with above-average surface temperatures in Europe, throughout all months, together with below-average precipitation across southern Europe.

Biological data Anchovy fishery and recruitment have been studied over an extended period for the Bay of Biscay (Uriarte et al., 1996; Motos et al., 1996). In addition, the relationship between climate, oceanography and recruitment has been described (Borja et al., 1996, 1998, 2008). Other species has been investigated also in recent times, such as the biomass of the algae Gelidium corneun, in relation to spring sun hours and waves (Borja et al., 2004), or the biomass and density of the gooseneck barnacle Pollicipes pollicipes, in relation to wave energy (Borja et al., 2006).

Table 1. Summary of the datasets utilised, including source, record length and sampling rate (for locations, see Figure 1). Data Location Source Record length Sampling rate Oceanographic Society of SST San Sebastián 1947-2008 Daily Gipuzkoa Spanish Meteorological Meteorological San Sebastián 1961-2008 Monthly Agency Vectorial data of 45º N, 2º W PFEL-NOAA 1967-2008 6 hours wind velocity NAO --- CPC 1950-2008 Monthly EA --- CPC 1950-2008 Monthly Anchovy Bay of Biscay Borja et al. (2008) 1967-2004 Annual recruitment Updating of Borja et al. Annual, with Gelidium corneum Basque coast 1983-2009 (2004) gaps Updating of Borja et al. Pollicipes pollicipes Basque coast 2004-2008 Annual (2006)

Results and Discussion

Climatic trends and variability The NAO and the EA pattern are two of the atmospheric climatic patterns identified as important factors explaining the interannual variability of climate over southwestern Europe. Figure 2 shows, in terms of the regression of the NAO (a) and EA indices (b) indices, the spatial distribution of the anomalous sea level pressure and wind fields corresponding to each of these indices. The NAO shows a dipolar structure over the Atlantic. A positive NAO index corresponds to low pressures over Iceland and positive pressure anomalies over the Atlantic mid- latitudes. Conversely, a positive value of the EA index is characterised by lower than normal sea level pressures, to the west of the British Isles. The surface wind field anomalies corresponding to each index, as represented by the regression analysis, are consistent with the geostrophic wind that would correspond to the pressure anomalies (Figure 2). It can be seen that over the Bay of Biscay, the changes in wind speed or direction induced by the EA pattern are larger than those corresponding to the NAO, due to the fact that the gradient of the anomalous sea level pressure field is greater over the area. Therefore, despite the fact that the NAO is an important driver on a hemispheric scale, the role of the EA pattern on the climatic variability can not be neglected at a local scale. Although, a shift in the EA index occurred in 2006, the positive phase of the EA pattern was particularly persistent during much of 1998-2008. In contrast, the negative phase of the NAO index dominated the circulation from 1997 to 2008, excluding 2001 and 2004 (Figure 3).

Figure 2. Regression maps of the Sea Level Pressure and surface winds with the NAO index (a) and the EA index (b). The maps have been established using the NAO/EA indices from the Climate Prediction Center (NOAA) and sea level pressure and surface wind from the NCEP Reanalysis (January 1950-June 2009).

1.5 NAO+ (a) 1 NAO-

0.5

0 NAO -0.5

-1

-1.5 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010

1.5 EA+ (b) 1 EA-

0.5

0 EA

-0.5

-1

-1.5 1950 1955 1960 1965 1970 1975 1980 1985 1990 1995 2000 2005 2010 Figure 3. Annual North Atlantic Oscillation (a) and East Atlantic Index (b) from 1952 to 2008 (NAO/EA indices from the Climate Prediction Center (NOAA); http://www.cpc.noaa.gov/). Time series have been normalised, detrended and smoothed with a 3-year running mean.

Influence of climatic patterns on atmospheric and oceanographic variables The anomaly patterns observed within the period 1998-2008 are examined here. On a seasonal basis, whilst the NAO index does not show any significant correlation with atmospheric/oceanic variables (not shown), the EA index shows good agreement with some of the variables analysed, for the southeastern Bay of Biscay. The best agreement between the EA index and atmospheric/oceanic variables was obtained in autumn and winter seasons (Figure 4). In fact, the effect of EA is particularly strong in autumn and winter (Barnston and Livezey 1987; Conrad et al., 2003).

1 0.8 0.6 t n 0.4 0.2 coefficie

n 0 -0.2 EV -0.4 HR Correlatio -0.6 T UPW/DOWN -0.8 95% -1 NDJ DJF JFM FMA MAM AMJ MJJ JJA JAS ASO SON OND Figure 4. Seasonal correlation coefficients between EA index and atmospheric/oceanic anomalies. Other variables have smaller and less relevant correlation values. Dashed lines denote value significant at the 95% confidence level. Key: NDJ-November-January; DJF-December-February; JFM-January-March; etc. EV, HR and T are the evaporation, moisture and air temperature in San Sebastián, respectively. UPW/DOWN is the upwelling- downwelling balance in the Landes-Basque Country area. The correlation coefficients are computed separately for each of twelve sliding three-monthly seasons. All seasonal values have been normalised and detrended.

The EA pattern correlates significantly with the autumn-winter air temperature, evaporation and moisture in San Sebastián. However, these variables show a very low correlation with the NAO index. This is in agreement with Sáenz et al. (2001a, b), who noted that the EA is the most important variation pattern explaining temperature variability over southewestern Europe. These authors concluded that the main factor contributing to warm winters, over the southwestern Europe, is related to southwesterly fluxes, associated with geopotential anomalies present during positive EA. On the basis of the oceanographic time series analysed, the autumn-winter upwelling/downwelling balance correlates significantly with the EA index, within the period 1998-2008. In fact, a southwesterly wind regime (i.e. a positive EA) produces upwelling unfavourable conditions within the French and Basque coasts (Borja et al., 2008). In this context, the period 1998-2008 (positive EA) is characterised by the prevalence of southwesterly wind anomalies and, consequently, the prevalence of downwelling conditions in autumn and winter. Similar results were obtained by deCastro et al. (2008), who noted that the positive phase of the EA was related directly to upwelling unfavourable conditions along northwestern Spain. The correlation strength depends greatly on the selected time period, as well as the integration period considered (monthly, seasonal, annual, etc). In this context, the period 2001- 2005 was characterised by extreme events that tend to favour/establish “deseasonality”, in comparison with the classical seasonal cycle of the Atlantic climatic regime, at mid-latitudes (Fontán et al., 2008; Goikoetxea et al., 2009). This observation means that winter-summer duality prevailed against the establishment (in terms of values and mean duration), of spring and autumn as transitional seasons. For instance, although the Basque coast is characterised by downwelling conditions in autumn, upwelling conditions prevailed in autumn 2005. Moreover, the period 2003-2005 was characterised by the prevalence of warm spring and summer seasons, with cold autumn and winter periods (Fontán et al., 2008). The cumulative anomalies of normalised seasonal averages are shown in Figure 5. The relationship between the EA index and evaporation, air temperature and moisture are clearly observable within the period 1998-2008. A shift of the EA pattern occurred in 2006; consequently, the agreement between the EA pattern and the atmospheric variables is even better if the period 1998/2000-2006 is considered (coinciding with the prevalence of the positive phase of EA, see Figure 3). Within this period, the anomaly patterns show a sustained trend, coinciding with the positive phase of the EA. The changes in climate result in changes in atmospheric variables and, therefore, in oceanic variables. For instance, evaporation in San Sebastián is related positively to solar radiation, air temperature and sea surface temperature; it is related negatively to moisture transport, cloudiness and precipitation.

8 7 6 EA EV 5 HR 4 T 3 2 1 0 -1 -2 -3 Cumulative anomalies -4 -5 -6 -7 -8

1986 1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 Figure 5. Cumulative plot of normalised seasonal averaged anomalies of: the EA index (EA), evaporation (EV), moisture (HR) and air temperature (T), in San Sebatián.

Impacts of climatic patterns on pelagic and coastal ecosystems The response of climatic impacts associated to pelagic ecosystems has been explained in Borja et al. (1996, 1998). Additionally, the recent climatic changes associated with the positive phase of the EA pattern have been noted by Borja et al. (2008). These authors concluded that the Bay of Biscay anchovy recruitment was related to upwelling over the spawning area; this was driven, in part, by the EA pattern. During positive EA phases (since 1998), the general wind regime over the area is from the southwest; this increases downwelling and, subsequently, this leads, probably, to the dispersion of anchovy food and larvae, together with increasing mortality and decreasing recruitment. On the other hand, the influence of climatic changes in coastal ecosystems appears to be related to changes in solar radiation and temperature, as well as wind and wave regimes. In recent times, the relationship between biomass, coverage, and density of the gooseneck barnacle (Pollicipes pollicipes), with environmental factors, such as wave height and wave energy incident at the coast, have been described within the Basque Country (Borja et al., 2006). Hence, increasing energy levels produce enhanced coverage and abundance, providing a larger standing stock. Numerical models to simulate the energy produced by waves have been used to predict the potential biomass of the goose barnacle, along the coast. The results have been validated with field data, over several years. From the ongoing investigations it seems that, increasing future wave heights over the Bay of Biscay, produced by climate change, will enhance the stock of this species. However, overexploitation of the species will mask this increase in biomass. In turn, the summer biomass of the macroalgae Gelidium corneum, which is the most abundant species in the Basque subtidal areas, is governed by the number of sun hours in winter and spring (Borja et al., 2004). However, wave energy is responsible for detaching algae from the substrata, reducing biomass (Borja et al., 2003). In recent times, Gelidium biomass has reduced progressively. This reduction is related to a decrease in winter-spring sun hours since 2006, coinciding with the shift in variables such as moisture (cloudiness) and therefore, solar radiation (Figure 5). In 2007-2008, solar radiation was around 20% lower than the average for 1986–2008 (Hughes et al., 2008). Additionally, after 2006 the number of occasions with wave heights >5 m, increased for the period March-June. Both factors have produced a reduction in the algae biomass; consequently, the period 2007-2009 is characterised by the lowest biomass values, since 1983. In conclusion, it appears that the positive phase of EA, after 1997, is producing less easterly winds in spring (producing upwelling in the southeastern Bay of Biscay), together with an increase in westerly wind circulation (producing downwelling). This factor reduces anchovy recruitment success. From 2006, the increasing wave energy in the coastal area has increased the Pollicipes biomass. In addition to this factor, increasing cloudiness (decreasing solar radiation), coinciding with a shift in the EA pattern, has reduced Gelidium biomass.

Conclusions The main conclusions of this study are summarised below. • The study confirms that the most influential atmospheric pattern is the EA, particularly over the southeastern Bay of Biscay, by means of the influence of the low pressure centre to the west of the British Isles. The EA pattern exerts its influence mainly in autumn and winter, being less persistent in spring and summer. • The period 1998-2008 can be characterised by the prevalence of positive phases of the EA pattern in autumn and winter; this caused drier and warmer than normal autumn and winter periods in the Bay of Biscay. Additionally, the prevalence of southwesterly wind anomalies produced upwelling unfavourable conditions in the southeastern part of the Bay of Biscay. • The positive phase of EA, after 1997, producing an increase of westerly wind circulation (producing downwelling), has reduced anchovy recruitment success. From 2006, the increasing wave energy in the coastal area has increased the Pollicipes biomass. In addition to this factor, increasing cloudiness (decreasing solar radiation), coinciding with a shift in the EA pattern, has reduced Gelidium biomass. • The physical environment plays an important role in coastal and pelagic species productivity; as such, it should be taken into account in fisheries assessment and management. Acknowledgements The meteorological data were obtained from the Observatory of San Sebastián (Spanish Meteorological Agency). The daily sea surface temperature data were provided by the Aquarium of San Sebastián (Oceanographic Society of Gipuzkoa). The wind data were furnished by NOAA-PFEL. The climatic indices were obtained from the Climate Prediction Centre (CPC) of the National Centre of Environmental Prediction (NCEP) (http://www.cpc.noaa.gov/). This study has been funded partially by the ETORTEK Strategic Research Programme (Department of Industry, Trade and Tourism and Department of Transport and Civil Works of the Basque Government), through the projects EKLIMA21 and ITSASEUS. The Basque Government (Department of Agriculture, Fisheries and Food) has funded the project “VARIACIONES” that includes acquisition of the in situ data and the review of external time series. Finally, we acknowledge Professor Michael Collins (SOES, UK and AZTI-Tecnalia) for his comments on the manuscript.

References Barnston A.G., Livezey, R.E., 1987. Classification, seasonality and persistence of low-frequency atmospheric circulation patterns. Monthly Weather Review, 115: 1083-1126. Beaugrand, G., Edwards, M., Brander, K., Luczak, C., Ibanez, F., 2008. Causes and projections of abrupt climate-driven ecosystem shifts in the North Atlantic. Ecology Letters, 11: doi: 10.1111/j.1461-0248.2008.01218.x. Beaugrand, G., 2009. Decadal changes in climate and ecosystems in the North Atlantic Ocean and adjacent seas. Deep Sea Research Part II: Topical Studies in Oceanography, 56: 656- 673. Bode, A., Alvarez-Ossorio, M.T., Cabanas, J.M., Porteiro, C., Ruiz-Villarreal, M., Santos, M.B., Bernal, M., Valdés, L., Varela, M., 2006. Recent changes in the pelagic ecosystem of the Iberian Atlantic in the context of multidecadal variability. ICES CM 2006/ Theme Session C:07. Borja, Á., Uriarte, A., Valencia, V., Motos, L., Ad., Uriarte, 1996. Relationships between anchovy (Engraulis encrasicholus) recruitment and the environment in the Bay of Biscay. Scientia Marina, 60 (suppl. 2): 179-192. Borja, Á., Uriarte, A., Egaña, J., Motos, L., Valencia, V., 1998. Relationships between anchovy (Engraulis encrasicolus) recruitment and environment in the Bay of Biscay (1967-1996). Fisheries Oceanography, 7: 375-380. Borja, A., Fontán, A., Gyssels, P., González, M., Mader, J., 2003. El seguimiento de la explotación de Gelidium sesquipedale en el País Vasco: el estudio del arranque y de la recuperación de las algas de arribazón. Informes Técnicos (Departamento de Agricultura y Pesca, Gobierno Vasco), 100: 1-75. Borja, A., Aguirrezabalaga, F., Martínez, J., Sola, J.C., García-Arberas, L., Gorostiaga, J.M., 2004. Benthic communities, biogeography and resources management. Borja, A. and Collins, M. (Eds.). Oceanography and Marine Environment of the Basque Country, Elsevier Oceanography Series, 70: 455-492. Borja, A., Liria, P., Muxika, I., Bald, J., 2006. Relationships between wave exposure and biomass of the goose barnacle (Pollicipes pollicipes, Gmelin, 1790) in the Gaztelugatxe Marine Reserve (Basque Country, northern Spain). ICES Journal of Marine Science, 63: 626-636. Borja, A., Fontán, A., Sáenz, J., Valencia, V., 2008. Climate, oceanography, and recruitment: the case of the Bay of Biscay anchovy (Engraulis encrasicolus). Fisheries Oceanography 17(6): 477-493. Cayan, D.R., 1992. Latent and sensible heat flux anomalies over the northern oceans: Driving the sea surface temperature. Journal of Physical Oceanography, 22: 859-881. Conrad, K.F., Wood, I.P., Perry, J.N., 2003. East atlantic teleconnection pattern and the decline of a common arctiid moth. Global Change Biology, 9: 125-130. Cury, P.M., Shin, Y.-J., Planque, B., Durant, J.M., Fromentin, J.-M., Kramer-Schadt, S., Stenseth, N.C., Travers, M., Grimm, V., 2008. Ecosystem oceanography for global change in fisheries. Trends in Ecology & Evolution, 23: 338-346. deCastro, M., Gomez-Gesteira, M., Alvarez, I., Cabanas, J.M., Prego, R., 2008. Characterization of fall-winter upwelling recurrence along the Galician western coast (NW Spain) from 2000 to 2005: Dependence on Atmospheric forcing. Journal of Marine Systems, 72: 145- 158. deYoung, B., Barange, M., Beaugrand, G., Harris, R., Perry, R. I., Scheffer, M., Werner, F., 2008. Regime shifts in marine ecosystems: detection, prediction and management. Trends in Ecology and Evolution, 23: 402-409. Drinkwater, K.F., Mueter, F.J., Friedland, K.D., Taylor, M., Hunt Jr., G.L., Hare, J.A, Melle, W., 2009. Recent climate forcing and physical oceanographic changes in Northern Hemisphere regions: a review and comparison of four marine ecosystems. Progress in Oceanography, 81: 10-28. Fontán, A., V., Valencia, Á., Borja, N., Goikoetxea, 2008. Oceano-meteorological conditions intheSEBayofBiscayfortheperiod2001–2005.Acomparison with the last two decades. Journal of Marine Systems, 72: 167-177. Garcia-Soto, C., Pingree, R.D., Valdés, L., 2002. Navidad development in the southern Bay of Biscay: climate change and swoddy structure from remote sensing and in situ measurements. Journal of Geophysical Research, 107(C8) (10.1029/2001JC001012). Goikoetxea, N., Borja, Á., Fontán, A., González, M., Valencia, V., 2009. Trends and anomalies in sea-surface temperature, observed over the last 60 years, within the southeastern Bay of Biscay. Continental Shelf Research, 29: 1060-1069. Halpert, M.S., Bell, G.D., 1997. Climate Assessment for 1996. Bulletin of American Meteorological Society, 78: S1-S49. Hemery, G., D'Amico, F., Castege, I., Dupont, B., D'Elbee, J., Lalanne, Y., Mouches, C., 2008. Detecting the impact of oceano-climatic changes on marine ecosystems using a multivariate index: The case of the Bay of Biscay (North Atlantic-European Ocean). Global Change Biology, 14: 27-38. Hiddink, J. G., ter Hofstede, R., 2008. Climate induced increases in species richness of marine fishes. Global Change Biology, 14: 453-460. Hughes, S.L., Holliday, N.P., Beszczynska-Möller, A. (Eds), 2008. ICES Report on Ocean Climate 2007. ICES Cooperative Research Report No. 291. 64 pp. Hurrell, J.W., 1995. Decadal trends in the north Atlantic oscillation: regional temperature and precipitation. Science, 269: 676-679. Hurrell, J.W., Deser, C., 2009. North Atlantic climate variability: The role of the North Atlantic Oscillation. Journal of Marine Systems, 78: 28-41. Krichak, S.O., Alpert, P., 2005. Decadal trends in the east Atlantic-west Russia pattern and Mediterranean precipitation. International Journal of Climatology, 25: 183-192. Mackenzie, B.R., Gislason, H., Mollmann, C., Koster, F.W., 2007. Impact of 21st century climate change on the Baltic Sea fish community and fisheries. Global Change Biology, 13: 1348-1367. Menge, B.A., Chan, F., Lubchenco, J. 2008. Response of a rocky intertidal ecosystem engineer and community dominant to climate change. Ecology Letters, 11: 151-162. Molinero, J.C., Ibanez, F., Souissi, S., Buecher, E., Dallot, S., Nival, P., 2008. Climate control on the long-term anomalous changes of zooplankton communities in the Northwestern Mediterranean. Global Change Biology, 14: 11-26. Motos, L., Uriarte, A., Valencia, V., 1996. The spawning environment of the Bay of Biscay anchovy (Engraulis encrasicolus L.). Scientia Marina, 60: 117-140. Occhipinti-Ambrogi, A., 2007. Global change and marine communities: Alien species and climate change. Marine Pollution Bulletin, 55: 342-352. Parsons, L.S., Lear, W.H., 2001. Climate variability and marine ecosystem impacts: a North Atlantic perspective. Progress in Oceanography, 49: 167-188. Pérez, F.F., Pollard, R.T., Read, J.F., Valencia, V., Cabanas, M., Ríos, A.F., 2000. Climatological coupling of the thermohaline decadal changes Eastern North Atlantic Central Water. Scientia Marina, 64(3): 347-353. Pingree, R., 2005. North Atlantic and North Sea climate change: curl up, shut down, NAO and ocean colour. Journal of the Marine Biological Association of the United Kingdom, 85(6): 1301-1315. Rahel, F.J., Bierwagen, B., Taniguchi, Y., 2008. Managing Aquatic Species of Conservation Concern in the Face of Climate Change and Invasive Species. Conservation Biology, 22: 551-561. Ríos, A.F., Pérez, F.F., Fraga, F., 1992. Water masses in the upper and middle North Atlantic Ocean east of the Azores. Deep-Sea Research I, 39: 645-658. Rogers, J.C., 1997. North Atlantic Storm Track Variability and Its Association to the North Atlantic Oscillation and Climate Variability of Northern Europe. Journal of Climate, 10: 1635-1647. Sáenz, J., Rodríguez-Puebla, C., Fernández, J., Zubillaga, J., 2001a. Interpretation of interannual winter temperature variations over Southwestern Europe. Journal of Geophysical Research, 106(D18): 20641-20652. Sáenz, J., Zubillaga, J. and Rodríguez Puebla, C., 2001b. Interannual winter temperature variability in the north of the Iberian Peninsula. Climate Research, 16: 169-179. Southward, A.J., Langmead, O., Hardman-Mountford, N.J., Aiken, J., Boalch, G.T., Dando, P.R., Genner, M.J., Joint, I., Kendall, M.A., Halliday, N.C., Harris, R.P., Leaper, R., Mieszkowska, N., Pingree, R.D., Richardson, A.J., Sims, D.W., Smith, T., Walne, A.W., Hawkins, S.J., 2005. Long-term oceanographic and ecological research in the western English Channel. Advances in Marine Biology, 47: 1-105. Stenevik, E.K., Sundby, S., 2007. Impacts of climate change on commercial fish stocks in Norwegian waters. Marine Policy, 31: 19-31. Sutton, R.T., Hodson, D.L.R., 2005. Atlantic Ocean forcing of North American and European summer climate. Science, 309: 115-118. Tourre, Y.M., Lluch-Cota, S.E., White, W.B., 2007. Global multi-decadal ocean climate and small-pelagic fish population. Environmental Research Letters, 2: 1-9. Travers, M., Shin, Y.-J., Jennings, S., Cury, P., 2007. Towards end-to-end models for investigating the effects of climate and fishing in marine ecosystems. Progress in Oceanography, 75: 751-770. Trigo, R.M., Osborn, T.J., Corte-Real, J.M., 2002. The North Atlantic Oscillation influence on Europe: climate impacts and associated physical mechanisms. Climate Research, 20: 9-17. Uriarte, A., Prouzet, P., Villamor, B., 1996. Bay of Biscay and Ibero Atlantic anchovy populations and their fisheries. Scientia Marina, 60: 237-255. Valencia, V., Borja, Á. Fontán, A., Pérez, F.F., Ríos, A.F., 2003. Temperature and salinity fluctuations in the Basque Coast (Southeastern Bay of Biscay), from 1986 to 2000, related to the climatic factors. ICES Marine Science Symposia, 219: 340-342. Valencia, V., Franco, J., Borja, Á., Fontán, A., 2004. Hydrography of the southeastern Bay of Biscay. In: Borja, A. and Collins, M. (Eds.). Oceanography and Marine Environment of the Basque Country, Elsevier Oceanography Series 70: 160-194. Wallace, J.M., Gutzler, D.S., 1981. Teleconnections in the geopotential height field during the Northern Hemisphere Winter. Monthly Weather Review, 109: 784-812.