© 2004 by ICES/CIEM International Council for the Exploration of the Sea/Conseil International pour l'Exploration de la Mer
Zooplankton variability and climatic anomalies from 1994 to 2001 in the Balearic Sea (Western Mediterranean)
Spanish Institute of Oceanography, Baleares Center PO Box 291, ES-07080 Palma de Mallorca, Spain
*Correspondence to M. L. Fernández de Puelles: tel: +34 971 401561; fax: +34 971 404945. e-mail: mluz.fernandez{at}ba.ieo.es.
The long-term and seasonal changes in biomass and zooplankton abundance at a station off Mallorca Island (Balearic Sea) were studied in relation to the main physical and chemical conditions. The results are based on a total of 276 samples collected every 10 days during 8 years by means of oblique hauls from bottom to surface. At this neritic station (77-m depth) located in a hydrographic area between northern Mediterranean and Atlantic southern waters, salinity ranged from 37 to 38.4 psu and temperature from 13.4°C (February 1996) to 27.4°C (August 1998). With the exception of salinity, the other environmental parameters and the most abundant zooplankton groups showed irregular but seasonal cycles. Interannual variability was also observed, with higher zooplankton abundance during the cooler and more saline years when the influence of northern water was stronger. Zooplankton abundance decreased during a warm period in 1998. Copepods were the most abundant group (54%) and their abundance was significantly correlated with temperature (negatively) and salinity (positively). Here, we summarize the changes in the zooplankton community abundance and how hydrographic forcing and other climatic factors have changed during the period from 1994 to 2001 in the Balearic Sea (Western Mediterranean).
Keywords: Balearic Sea, copepods, hydrography, NAO, time-series, zooplankton
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Introduction |
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The Balearic Sea is a hydrographical transition area into the Western Mediterranean between two sub-basins: the Gulf of Lions, with cold, saline water, and the Alborán basin, recipient of warmer and less saline Atlantic Water (García et al., 1994). The Balearic Islands form a topographical barrier between the two, and their coasts are affected by one or other of these waters coming from the east, depending on the time of year and the mesoscale processes in the adjacent areas (Pinot et al., 2002). The pronounced slope of the platform towards the edge of the continental shelf around the islands allowed us to sample an offshore station on a frequent basis. This enabled us to obtain a good knowledge of the temporal variation of zooplankton in the open sea.
The seasonal cycles of zooplankton in the Balearic Sea have been studied by Vives (1966) and Fernández de Puelles et al. (1997, 2003a) during short time periods, while longer studies have been undertaken in other areas of the Mediterranean (Baranovic et al., 1993; Mazzocchi and Ribera d'Alcala, 1995; Christou, 1998). The lack of long time-series of zooplankton in the area and the strategic situation of the Balearic Islands in the central part of the Western Mediterranean motivated the present study.
The main objective was to determine the main patterns in the variability of zooplankton abundance during the 8 years of our study and relate these patterns to the hydrography of the area and other climatic factors affecting the open waters of the Balearic Sea.
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Material and methods |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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From January 1994 to December 2001, a monitoring station at 77-m bottom depth (Station 1, Figure 1) was visited every 10 d at the same time of day (10:00 to 12:00). Duplicate zooplankton samples were collected by oblique hauls of a 250-µm mesh bongo net from 75 m to the surface. The net was fitted with a flowmeter (General Oceanic model 2030) in order to measure the volume of water filtered. To determine hydrographic factors and nutrients, water samples were collected with 5-l Niskin bottles at 0-, 15-, 25-, 50-, and 75-m depth. CTD data were also used to describe the hydrographic conditions.
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One sample was preserved in 4% neutralized formaldehyde buffered with borax and used for taxonomic analysis. The other was frozen at –20°C and the zooplankton biomass analysed 15 days later (Lovegrove, 1966). The subsamples for taxonomic studies were obtained using a Folsom Plankton splitter and then treated statistically as recommended in Horwoord and Driver (1976).
Linear regression was used to relate the environmental variables and zooplankton groups. To group the dates according to the hydrographic parameters as well as their relation to zooplankton abundance, multidimensional scaling ordination (MDS) was carried out using the Bray–Curtis similarity index and square root transformation from environmental variables and abundance data. These analyses were performed using the PRIMER programme (Plymouth Marine Laboratory, UK).
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Results |
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Environmental factors
Temperature showed a clear seasonal pattern (Figure 2a), with mean water column (0–75 m) temperatures ranging from 14.3°C (in February) to 22.2°C (in August). Nevertheless, considerable interannual variability was also observed. In 1997 and 1998, temperatures were higher compared to other years, such as 1996 or 2000. While some years (1997 and 1998) were warmer all year round, other years such as 1999 or 1995 were characterized by a warm winter or a cool summer, respectively. The year 2000 registered the lowest autumn temperatures during the study period.
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The water column was strongly stratified from May to October, whereas it was mixed during the winter months as expected for these temperate latitudes. Sea surface temperature (SST) ranged from 13.4°C in February (1996 and 2000–2001) to 27.4°C in August (1998). Smaller oscillations (around 3°C) were observed at 75-m depth, recording the highest temperatures at this depth in mid-1997 and in 1998 (when temperature reached 17°C in late autumn); the lowest temperature at the same depth was found in winter but also in May–June of 2000 (13.4°C). A statistically significant difference was found between the annual means at this depth between the years 1997 and 1998 and the others (ANOVA, p<0.05). When the annual mean values were calculated, a temperature anomaly was clearly observed during both warm years (Figure 3).
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Salinity did not show any seasonality due to the irregular influence of different water masses in the studied area. However, it was usual to find higher salinity during the winter (>38 psu) and lower values during the summer and autumn (37 psu; Figure 2b); interannual monthly variability was observed. During 1996, 2000, and 2001, salinities were throughout the year (38 psu), indicating the influence of northern Mediterranean waters in the study area. The lowest salinities of the time-series were observed during 1995 and 1998, reflecting the inflow of southern Atlantic waters (Figure 3). During 1999 there was an unusual seasonal variability, with higher values during spring.
The nitrate concentrations did not show any clear seasonality. Nevertheless, higher concentrations were usually observed during the winter and particularly in the last three years of the time-series (Figure 3), when salinity was also higher (>37.7 psu). This suggested an enrichment in nutrients when cold northern waters were present in the area. Nitrates and salinity showed a positive correlation (p<0.01), on the contrary nitrates and temperature were negatively correlated (p<0.01) as were temperature and salinity (p<0.05).
Regarding the temporal trend, both salinity and nitrates showed an increasing trend (p<0.05) but no trend was observed in temperature.
Seasonal and interannual zooplankton variability
Zooplankton biomass during the 8 years was low (<6 mg m–3 annual mean values) compared to other areas of the Western Mediterranean. When the abundance of zooplankton was considered, abundances were observed during 1996, as well as during 2000 and 2001 (Figure 4). Significant differences were found between these years and the others (1994, 1995, 1997, 1998, and 1999) (ANOVA, p<0.05). Copepods were the most abundant zooplankton group (54% of total abundance), followed by the gelatinous organisms (25%), in particular appendicularians (19%), but to a lesser extent also doliolids and salps. The cladocera were the next group in abundance (11%), and were particularly important during the stratified season and the last two years of the study. Zooplankton biomass and abundance were significantly correlated (r=0.8; p<0.01), suggesting that both depicted the same main changes in zooplankton community. Copepod abundance showed a similar pattern to that of total zooplankton, with highest abundance during 1996 and lowest during 1998. The abundance of copepods and appendicularians was highest during spring (Figure 5a) and summer depending on the year (Figure 5b). With the exception of a long-term increase in the abundance of zooplankton during the summer, no other general trends were observed.
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More than 80 copepod species were identified, but only 10 species account for 60% of total copepod abundance. Clausocalanus furcatus (12%), C. pergens (8%), and C. arcuicornis (4%) were the most abundant all year round. Paracalanus parvus (8%) and Centropages typicus (6%) were particularly abundant in late spring, Acartia clausi (7%) during summer, Oncaea mediterranea (4%), Temora stylifera (2%), and Oithona plumifera in autumn, and Ctenocalanus vanus (5%) and Diaixis hibernica (5%) in winter. Among the cladocera, Evadne spinifera was the most abundant in late spring and Penilia avirostris in mid-summer. These species showed a higher increase during the last three years. Although A. clausi and T. stylifera showed an increase in abundance during the warming period, no significant trends were found.
The MDS of the total abundance of zooplankton shows a clear decrease in their abundance from 1996 to 1998, corresponding to an increase in temperature (Figure 6a): during the warmest year (1998) zooplankton abundance was the lowest and during the coldest year (1996) zooplankton abundance was highest. According to temperature values, it seems that the spring conditions are important for the main zooplankton groups (see Figure 5), but also the previous winter conditions might constitute a critical period for the increase in their abundance. During late spring (May–June) and early summer of 2000, when the lowest temperatures (
13.4°C) were registered at 75 m, the highest abundance of cladocera and gelatinous groups was observed.
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) and annual mean temperature superimposed (°C in 
) based on the Bray–Curtis similarity matrix. (b) MDS ordination of copepod abundance (ind. m–3 in In the case of the copepods, during the coldest and most saline year (1996) their abundance was highest and clearly differentiated from the other years. The abundance of copepods was lowest during those years when the temperature was higher (Figure 6b, see years 1996 and 1998) and salinity lowest (Figure 6c). A statistically significant relationship was found between temperature (R2=0.44; p<0.05), salinity (R2=0.47; p<0.05), and zooplankton abundance, but a closer relationship was found between copepod abundance and salinity (R2=0.59; p<0.01) and temperature (R2=0.3; p<0.01).
When considering the relationship between the annual mean copepod abundance and large-scale climate indexes, such as the Gulf Stream North Wall (GSNW) and the North Atlantic Oscillation (NAO; Figure 7), no correlation was found with the GSNW, but a significant correlation was found with the winter NAO index (R2=0.54; p<0.05). The highest copepod abundance in the time-series coincided with the lowest winter NAO value (–2.86) in 1996, when there was a strong negative NAO anomaly.
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Discussion |
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TopIntroductionMaterial and methodsResultsDiscussionReferences |
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The data presented here provide basic information about the zooplankton community in the surface waters of the Western Mediterranean and its variability during an 8-year period. The location of Mallorca in a boundary area between northern and southern Mediterranean waters (Pinot et al., 2002) allowed us to observe the influence of different water masses on the hydrography and the zooplankton populations. The zooplankton data collected during the time-series study showed low biomass but moderate abundance, comparable to oligotrophic areas of the Eastern Mediterranean (Siokou-Frangou, 1996; Christou, 1998), and much lower than in other areas of the Western Mediterranean (Rodríguez, 1983; Mazzocchi and Ribera d'Alcala, 1995; Gaudy and Champalbert, 1998). According to these authors, low production is evident from the low concentrations of nutrients and zooplankton biomass; this, however, could not be applied to the abundance of zooplankton (predominantly small organisms), whose seasonal distribution may vary irregularly in relation to the influence of different water masses and changes in the circulation of the Balearic Sea (Pinot et al., 2002). The importance of the small-sized organisms in the zooplankton community has also been noted in neighbouring areas (Calbet et al., 2000). According to other authors (Razouls and Kouwenberg, 1993), oceanic areas in the north Mediterranean Sea might have notable concentrations of small zooplankton and they could vary from year to year. Very complex interactions occur in the zooplankton abundance pattern, but they seem to be related to the changes in the proportion of the water masses they inhabit.
In the Western Mediterranean, cold years tend to be more productive, partly because winter mixing may reach greater depth and in part because the formation of deep water in the Gulf of Lions may flow over a larger area (Estrada et al., 1985; Gaudy, 1985). This enhanced production in colder winters and springs also means an increase in zooplankton, as was observed in our data during the coldest years, 1996 and 2000 (spring and autumn). The increase in zooplankton abundance and biomass during 1996 was clearly related to northern Mediterranean waters, whose fertility is higher in relation to the rest of the basin (Flos, 1985). Several surveys carried out during spring and autumn in 2000 in the Mallorca Channel (0–700 m) demonstrate the presence of northern water during this year in the area (Lopez-Jurado et al., 2001; Lopez-Jurado, 2002).
On the contrary, a high influence of recent Atlantic waters was observed during 1998 (Pinot et al., 2002). In this sense, the lowest zooplankton abundance during 1998 could be a clear response to warming, when the waters were more stratified (Fernández de Puelles et al., 2003b). Nutrient depletion related to higher temperatures and subsequent stratification was also found during 30 years of observations in the California Current (Roemmich and McGowan, 1995).
The negative correlation found between copepod abundance and temperature and the positive correlation with salinity have also been previously mentioned in the Western Mediterranean (Razouls and Kouwenberg, 1993). It could suggest the higher zooplankton preference for cooler and more saline waters, or the influence of northern Mediterranean waters. In the present study, no significant trends in the long-term changes of zooplankton or copepod abundance were found. But when considering only the period 1994–1999 an overall decrease of zooplankton was observed in the Mallorca Channel in relation to atmospheric heating of coastal waters (Fernández de Puelles et al., 2003b). In other mediterranean areas, a zooplankton decline has been observed during the 1980s (Mazzocchi and Ribera d'Alcala, 1995) and in the early 1990, with copepods being more abundant during periods with higher salinities (Christou, 1998). We acknowledge that factors other than temperature and salinity could be contributing to the patterns observed in the plankton, but the recognition of large-scale dependence on the physical environment (Frost, 1983; Mackas, 1984; Sabatés et al., 1989) is a first and necessary step to our understanding the distribution of zooplankton in the Balearic Sea.
The relationship between zooplankton variability and long-term climatic indicators, such as the Gulf Stream North Wall (GSNW) and the North Atlantic Oscillation (NAO), has been found in the North Atlantic, as well as the associated mechanisms involved (Taylor et al., 1992; Fromentin and Planque, 1996). The GSNW is a climatic indicator of weather across the North Atlantic that has been related to temperature and zooplankton. However, in our data we did not find any significant correlation with the zooplankton, which might be due to the short time-series analysed. On the other hand, it is the state of the NAO that determines the speed and direction of westerly winds across the North Atlantic as well as winter temperature. The persistence of an exceptionally strong positive NAO is the source of recent temperature anomalies and changes in the atmospheric moisture transport (Hurrell, 1995). A clear effect of the NAO on pelagic ecosystems appears together with clear evidence that changes in wind conditions affect Atlantic plankton communities. Although the long-term SST and circulation in the Western Mediterranean Sea has been related to the NAO (Bolle, 2002; Vignudelly et al., 1999), very little is known about the relationship between zooplankton and the mechanisms involved with the NAO.
An interesting signal was found when the winter NAO index (Hurrell, 1995) was strongly negative and the highest zooplankton abundance was obtained (1996). It seems that a negative NAO index (<–1) has a strong influence in the Western Mediterranean (Vignudelly et al., 1999) and could be related to the highest zooplankton abundance in the Balearic Sea. Positive winter NAO is not always clearly related to lower zooplankton abundance, as was the case in 2000, when winter conditions differed from what would be expected from the NAO in the ICES Area (Turrell and Holliday, 2003). Although a clear relationship was observed between zooplankton abundance and the very negative NAO index, this should be explored further when the time-series is extended.
Climate and ocean circulation patterns are closely linked; hence climate changes will have profound consequences for zooplankton. As in many tropical regions, an increase in global temperature causes stronger stratification and lower zooplankton production (Williamson, 2000). However, a negative NAO index brings cold air to northern Europe and moist air into the Mediterranean with cooler winters. This suggests a possible link between atmospheric forcing and zooplankton abundance in the Balearic Sea. A direct influence of an atmospheric teleconnection seems to merge throughout air–sea interaction processes in the northern Mediterranean Sea (Vignudelly et al., 1999), with cold northern winds when negative winter NAO is observed. If cold winters (negative winter NAO) favour rich northern Mediterranean waters, higher amounts of zooplankton, and particularly copepods, could be expected in waters of the Balearic Sea. The lack of westerly winds in the west of Europe, characteristic of the positive NAO, would favour the input of northern winds (Turrell and Holliday, 2003) and northern upper waters in the Balearic area. During a positive phase of the winter NAO, the westerly winds reaching the Iberian mainland would favour the input of Atlantic Water in the Mediterranean. As a consequence, this water could reach the Balearic Sea and a warmer temperature would be observed in the area. In the North Atlantic, the abundance of plankton has been related to the NAO index (Fromentin and Planque, 1996; Irigoien et al., 2000), but it has not always the same effect for all planktonic groups. Therefore different groups of zooplankton and copepods in particular could be a very interesting community to clearly reflect climatic and hydrographic changes in the regime of the Western Mediterranean.
In this sense, we know that 8 years of data are very preliminary, but though definite conclusions cannot be reached an overall pattern and anomalies can be proposed. More investigations should be conducted especially to further determine the relationship between NAO (positive and negative) and zooplankton populations, and much longer data series have to be encouraged, particularly in the Mediterranean. All this information may help towards a better understanding of the zooplankton variability in transitional and oligotrophic areas of other temperate latitudes in the world.
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Acknowledgements |
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Thanks to Pedro Sanchez and Mariano Serra for their continuous assistance in collecting samples and to our colleagues in the laboratory – Tomeu Amengual for the nutrient analysis and Ana Morillas for the identification of many zooplankton organisms. This project was carried out within the framework of "oceanographic time-series" of the Spanish Institute of Oceanography. Finally, we thank the two reviewers and Roger Harris at the Plymouth Marine Laboratory (UK) and Fernando Villate at the Basque University for their suggestions on manuscript revision.
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  M. L. Fernandez de Puelles and J. C. Molinero Decadal changes in hydrographic and ecological time-series in the Balearic Sea (western Mediterranean), identifying links between climate and zooplankton ICES J. Mar. Sci., April 1, 2008; 65(3): 311 - 317. [Abstract] [Full Text] [PDF]
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