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ICES Journal of Marine Science: Journal du Conseil Advance Access originally published online on March 14, 2008
ICES Journal of Marine Science: Journal du Conseil 2008 65(3):318-324; doi:10.1093/icesjms/fsn042
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© 2008 International Council for the Exploration of the Sea. Published by Oxford Journals. All rights reserved. For Permissions, please email: journals.permissions@oxfordjournals.org

This article appears in the following ICES Journal of Marine Science issue: 4th International Zooplankton Production Symposium: Human and Climate Forcing of Zooplankton Populations [View the issue table of contents]

Impact of climate change on long-term zooplankton biomass in the upwelling region of the Gulf of Guinea

George Wiafe1, Hawa B. Yaqub2, Martin A. Mensah2 and Christopher L. J. Frid3

1 Department of Oceanography and Fisheries, University of Ghana, PO Box LG 99, Legon, Ghana
2 Marine Fisheries Research Division, Fisheries Directorate, Ghana
3 University of Liverpool, Liverpool L69 7ZB, England

Correspondence to G. Wiafe: tel: +233 244 657475; fax: +233 21 502701; e-mail: wiafeg{at}ug.edu.gh.

Wiafe, G., Yaqub, H. B., Mensah, M. A., and Frid, C. L. J. 2008. Impact of climate change on long-term zooplankton biomass in the upwelling region of the Gulf of Guinea. – ICES Journal of Marine Science, 65: 318–324.

We investigated long-term changes in coastal zooplankton in the upwelling region in the Gulf of Guinea, 1969–1992, in relation to climatic and biotic factors. We considered the role of hydrographic and climatic factors, i.e. sea surface temperature (SST), salinity, sea level pressure, windfield, and Southern Oscillation Index (SOI), in the long-term variation of zooplankton in a multiple regression analysis, along with the abundance of Sardinella. Annual variation in zooplankton biomass was cyclical, with the annual peak occurring during the major upwelling season, July–September. Over the 24-year period, there was a downward trend in zooplankton biomass (equivalent to 6.33 ml per 1000 m3 per year). The decomposed trend in SST during the major upwelling revealed gradual warming of surface waters. This trend was believed to be the main influence on the abundance of the large copepod Calanoides carinatus (sensitive to temperatures above 23°C), which appears in the coastal waters only during the major upwelling season. The warming trend associated with global climate change could affect zooplankton community structure, especially during the major upwelling season. Global warming coupled with "top–down" (predation) control by Sardinella might be responsible for the long-term decline in zooplankton biomass in the upwelling region of the Gulf of Guinea.

Keywords: Calanoides carinatus, climate change, global warming, Gulf of Guinea, Sardinella, upwelling, zooplankton

Received 7 July 2007; accepted 11 February 2008; advance access publication 14 March 2008.


   Introduction
Top
 Introduction
Methodology
 Results
 Discussion
 References
 
The upwelling region of the Gulf of Guinea extends from the coast of Côte d'Ivoire around to Benin. The region is also referred to as the Central West African Upwelling (Frost et al., 2005), and the coastal oceanography has been described by several authors (Howat, 1945; Longhurst, 1962; Bakun, 1978; Houghton, 1983; Mensah and Koranteng, 1988; Binet and Marchal, 1993). Four distinct and predictable hydrographic seasons have been described: the minor (December–March) and major upwelling (July–September) interspersed with periods of stratification, typically with a thermocline 30–40 m below the surface.

Changes in local hydrography and climatic effects are not the only physical factors that influence zooplankton production in the Gulf of Guinea. It has been demonstrated that the entire Gulf of Guinea is influenced to a large extent by the meteorological and oceanographic processes of the South and North Atlantic Ocean (Merle and Arnault, 1985; Fontaine et al., 1999), principally their oceanic gyral currents, which in turn reveal relationships with global atmospheric changes, such as the El Niño Southern Oscillation (ENSO).

Zooplankton studies in the Gulf of Guinea date back to the late 19th century, when several expeditions visited the region and assessed the species composition and diversity. The Danish Atlantide expedition of 1945/1946 provides extensive coverage of the copepods of the region (Vervoort, 1963, 1965). By the mid-1960s, Ghana, Côte d'Ivoire, Sierra Leone, and Nigeria had set up fishery laboratories which, in addition to stock assessments, also carried out monitoring of the zooplankton biomass in relation to the fishery.

During the upwelling, zooplankton are more abundant, though with less species diversity, than during the thermally stratified periods (Bainbridge, 1972). This applies mainly to outer-shelf stations because, in the inshore waters, meroplanktonic larvae (e.g. polychaete, echinoderm, and caridean larvae), mask the effect. During periods of thermal stability formation, the zooplankton is relatively sparse, with high species diversity and a considerable proportion of carnivorous species.

In addition to the annual cycle of abundance, which is clearly related to the annual hydrographic cycle, zooplankton abundance is variable over a longer period. Given the importance of hydrography in shaping the annual cycle, it is logical to relate these variations quantitatively to changes in the physical environment or, more specifically, to climate change, which drives most of the physical factors in the oceans. Studies in the Atlantic (Taylor and Stephens, 1980; Colebrook, 1986; Fransz et al., 1991; Verheye, 1991) and the Pacific oceans (Brodeur and Ware, 1992; Francis and Hare, 1994; Mackas, 1995), for example, relate zooplankton distribution to oceanographic condition.

Variations in zooplankton abundance have also been examined at various temporal scales; diurnal (Lampert, 1989), seasonal (Colebrook, 1982), and long-term (Jossi and Goulet, 1993; Mollmann et al., 2000). Among the abiotic factors, temperature is considered to be one of the important factors influencing the distribution of planktonic communities (Parsons et al., 1984). Global warming has become a topic of concern (IPCC, 2007), and the commensurate rise in sea surface temperature (SST), therefore, might be expected to play an important role in the plankton dynamics of upwelling regions such as the Gulf of Guinea. Climatic trends in the Gulf of Guinea have been consistent with global changes (Koranteng and McGlade, 2000).

This study examines the time-series of zooplankton biomass from the Gulf of Guinea, the longest time-series of zooplankton in the region, to understand changes in the pelagic ecosystem. Mensah (1995) reported on the declining trend in the zooplankton without attributing any causal agent. In this study, patterns of long-term trend in zooplankton biomass are described and examined in relation to parallel changes in the environmental variables, including climatic drivers and biota.


   Methodology
Top
 Introduction
 Methodology
Results
 Discussion
 References
 
Zooplankton biomasses from 1969 to 1992 were obtained from the Marine Fisheries Research Division (MFRD) in Ghana, which carried out monitoring, monthly or fortnightly, along a transect off the coast of Ghana, within the Gulf of Guinea (Figure 1). Five stations (A0, A1, A2, B, and C) along this transect were sampled with an International Cooperative Investigations of the Tropical Atlantic (ICITA) net, with a mesh size of 330 µm, ring diameter of 1 m, and filtering section 2.4 m long. However, data obtained from Station A0 (the harbour jetty) were excluded from statistical analysis because the station was a late addition to the programme, and therefore data were incomplete.


Figure 1
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  		Figure 1. Map of the central eastern Atlantic Ocean showing the upwelling region of the Gulf of Guinea (shaded), and the sampling locations along the hydrographic transect (A0, A1, A2, B, C) off the coast of Ghana.

 
At each station, the net was towed in a step-oblique fashion at five steps for 10 min at a towing speed of 2 knots. A 10-m length of wire was released at each step, totalling 50 m of wire. The samples collected were fixed with buffered formaldehyde to a final strength of 4%. Later in the laboratory, zooplankton and Sardinella larvae were sorted out separately, and the displacement volume of each was measured and standardized as millilitres per 1000 m3 of seawater (Harris et al., 2000). Monthly data were calculated as averages over the pooled data for all stations, except Station A0.

Climatic and oceanographic data on SST, sea level pressure, and zonal and meridional windstress were obtained from the International Comprehensive Oceanic and Atmospheric Data Sets (I-COADS) of the National Oceanic and Atmospheric Administration (NOAA), USA. These were monthly data of 1° x 1° resolution from 1°W to 1°E and 5°N to 6°N. In addition, monthly data on the Southern Oscillation Index (SOI) of similar resolution and coverage were obtained from the Climate Diagnostic Centre of NOAA. The SOI was included among the environmental factors because of its significant influence on local hydro-climatic processes (Binet, 1996).

Variations added by seasonal or other cycles, in time-series analyses, make it more difficult to detect long-term trends. To overcome this problem, the data were decomposed into the four hydrographic seasons. Mensah (1991) and Wiafe (2002) have identified periods for the four hydrographic seasons in the Gulf of Guinea as minor upwelling (December–March), thermocline formation (April–June), major upwelling (July–September), and thermocline formation (October–November). In this study, the two thermally stratified periods will be referred to as hydrographic thermocline 1 (April–June) and hydrographic thermocline 2 (October–November).

A Mann–Kendall trend test was performed on the data, an improvement upon using regression as a trend test (Gilbert, 1987). The Mann–Kendall test statistic (Z) is calculated as follows:


Formula 042UM1

where


Formula 042UM2

the sign (Xj–Xk) is the sign of all n(n–1)/2 possible differences, n is the number of points in the distribution. The Z-statistic was referred to a standard cumulative normal distribution table (Pearson and Hartley, 1966) at null hypothesis acceptance level of p < 0.05. Significant correlations between time-series can be criticized because, if there is autocorrelation in the series, the true number of independent points could be overestimated. This problem was detected using the method of Quenouille (1952) to calculate the effective number of independent observations.

The effect of physical and/or biological factors on zooplankton biomass was determined from multiple regression analysis. The biomass of zooplankton and Sardinella larvae used in the analysis were log-transformed to improve homogeneity of variance for statistical analysis. The multiple regression analysis was performed in stepwise fashion, where independent variables were included one at a time to assess their contribution to the variation in the dependent variable.


   Results
Top
 Introduction
 Methodology
 Results
Discussion
 References
 
The anomalies in zooplankton biomass revealed cyclical variation, with peaks during the major upwelling season (Figure 2a). Periods in which peak abundance was above or below the long-term mean were considered as "high productive" and "low productive" years, respectively. Similarly, there was a cyclical variation in the Sardinella larvae, with peaks during the major upwelling but no discernible trend in their long-term biomass (Figure 2b).


Figure 2
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  		Figure 2. Anomalies of biomass of zooplankton and Sardinella larvae, 1969–1992, in the upwelling region of the Gulf of Guinea. Data points refer to averages for each hydrographic season; for each year it follows the minor upwelling, hydrographic thermocline 1, major upwelling, hydrographic thermocline 2 (see text).

 
Mann–Kendall trend analysis confirmed the negative trend in zooplankton biomass and the lack of any trend in Sardinella larval abundance. Linear trend, estimated by the least-squares method, revealed that the rate of decrease in zooplankton biomass was 6.33 ml per 1000 m3 of seawater per year (r2 = 0.320; Figure 3).


Figure 3
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  		Figure 3. Interannual variation in zooplankton biomass in the upwelling region of the Gulf of Guinea.

 
SST during the major upwelling and hydrographic thermocline 2 periods of the annual cycle have risen gradually (Table 1; see Figure 4). From the data shown in Figure 2a, we noted high production of zooplankton during the major upwelling season. A plot of SST vs. zooplankton biomass demonstrated a significant negative relationship (Figure 5), and that low zooplankton production coincided with high SST.


Figure 4
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  		Figure 4. Distribution of SST with respect to the hydrographic seasons. Values of r2 have been reported for positive trend lines only [i.e. major upwelling and thermocline 2].

 


Figure 5
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  		Figure 5. Relationship between zooplankton biomass and SST over a 24-year period, 1969–1992. Data points refer to monthly values.

 


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  		Table 1. Results of Mann–Kendall trend tests on biotic and abiotic time-series data.

 
Zooplankton temporal variation in each of the hydrographic seasons revealed that the rate of decline during the major upwelling was higher than the other seasons (Figure 6). From multiple regression analysis, Sardinella larvae biomass, SST, local sea level pressure, zonal windstress, SOI, and salinity were identified as significant predictors of zooplankton biomass during the various hydrographic seasons (Table 2). During the hydrographically stratified period from October to November, zooplankton production was strongly influenced by regional atmosphere–ocean dynamics, as indicated by the SOI.


Figure 6
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  		Figure 6. Seasonal variation in zooplankton biomass in the upwelling region of the Gulf of Guinea. Four hydrographic seasons are identified in the Gulf of Guinea (see text).

 


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  		Table 2. Percentage variance in the seasonal biomass of zooplankton accounted for by biotic and abiotic factors based on data, 1969–1992.

 
During the remainder of the year, the SST (in both upwelling periods) and/or the abundance of Sardinella larvae (April–September) were the principal factors influencing variation in zooplankton biomass. Comparison of seasonal variation in biomass between zooplankton and Sardinella larvae revealed a month's lag between their peaks (Figure 7). Multiple regression analysis based on seasonal biomass, averaged over the study period, revealed that SST alone accounted for 82.2% (p < 0.001) of the total variance in zooplankton biomass.


Figure 7
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  		Figure 7. Standardized monthly distribution of zooplankton and Sardinella larvae averaged over a 24-year period, 1969–1992.

 

   Discussion
Top
 Introduction
 Methodology
 Results
 Discussion
References
 
On a global scale, anthropogenic emissions of greenhouse gases have contributed to the radiative balance of the Earth, thereby increasing global temperature and altering the hydrological cycle and atmospheric and oceanic circulation, weather patterns, and precipitation (IPCC, 2007). Bakun (1990) has identified the trend towards increasing windstress over the world's major upwelling areas during the period from 1950 to the late 1980s as an effect that can be attributed to long-term global warming. For upwelling regions, this phenomenon could influence the biological dynamics, as noted for the zooplankton community in several ICES regions (ICES, 2006). In most regions, increasing windstress will increase upwelling; however, in the Gulf of Guinea, the upwelling is not locally forced but results from complex changes in the pressure field within the tropical Atlantic.

During this study, we noted that zooplankton biomass in the Gulf of Guinea, which experiences a seasonal upwelling, has declined significantly over a 24-year period. The gradually increasing trend in SST, especially during the upwelling season, accounted for >50% of the variability in the long-term biomass of zooplankton, suggesting that global warming could be an important factor in the declining trend in zooplankton of the region.

It has been reported that a significant proportion of total zooplankton biomass during the major upwelling is caused by the copepod Calanoides carinatus (Bainbridge, 1972; Mensah, 1974a). The species is advected into the coastal waters from South Atlantic Central Water as a result of the upwelling (Mensah, 1974a). This species is temperature-sensitive. It migrates down to 500 m as diapause Stage V copepodites when water temperatures exceed 23°C, reappearing the next upwelling season (Mensah, 1974a). In this study, we attempt to demonstrate that the changing conditions during the major upwelling, as a result of global warming, may be ecologically significant. The abundance of C. carinatus might be reduced by the observed surface warming, leading to a possible shift in zooplankton community structure. This will have direct consequences on the pelagic fisheries in the region.

The most abundant pelagic species in the upwelling region of the Gulf of Guinea are Sardinella aurita, S. maderensis, Engraulis encrasicolus, and, in certain years, Scomber japonicus (Mensah and Koranteng, 1988; Koranteng, 1995). Spawning of S. aurita commences in response to the start of the coastal upwelling (Quaatey and Maravelias, 1999). However, Binet (1995) suggested that plankton abundance, providing forage for juvenile or adult fish, is more important for sustaining the biomass of the stock than spawning success and larval survival. Of the large number of relationships between fish and zooplankton, the most important is that linking the latter with the recruitment of fish, for which information has been gathered for the past three or four decades (Cushing, 1995). Among other foods, fish larvae eat nauplii and copepodite stages, and part of the recruitment mechanism may depend on this process.

Mensah (1995) investigated the potential effect of zooplankton on the Sardinella fishery by considering whether the declining trend in zooplankton was affecting the fishery. He concluded that the zooplankton production would be adequate for survival of the fish stock. Thus, the fishery might not be resource-limited (i.e. bottom–up process). A month's lag exists between the peaks of Sardinella larval abundance and total zooplankton biomass, suggesting a "match" between the predators and larval food and, hence, the potential for a climate-change induced "mismatch" to compromise recruitment in S. aurita stocks (Cushing, 1974, 1975, 1982, 1990). This study has reported a significant decline in zooplankton biomass from the late 1960s to the early 1990s, and attributes the trend to global warming. Although biological (top–down) control was also important, there was no long-term trend in the abundance of the predatory fish larvae. Although the zooplankton time-series analysis was at the biomass level rather than species level, knowledge of the biology and distribution of the dominant species during the major upwelling (i.e. Calanoides carinatus; Mensah, 1974b) gives credence to the assertion that the current trend in warming of the ocean, especially during the major upwelling, might result in a shift in zooplankton community structure and impacts on fishery resources.


   Acknowledgements
 
The authors thank the Marine Fisheries Research Division of Ghana for data on zooplankton and fish larvae, and I-COADS for hydrographic and climatic data. Special thanks go to the Guinea Current Large Marine Ecosystem Project for financial support.


   References
Top
 Introduction
 Methodology
 Results
 Discussion
 References
 

    Bainbridge V. The zooplankton of the Gulf of Guinea. Bulletin of Marine Ecology (1972) 8:61–97.

    Bakun A. Guinea current upwelling. Nature (1978) 271:147–150.[CrossRef]

    Bakun A. Global climate change and intensification of coastal ocean upwelling. Science (1990) 247:198–201.[Abstract/Free Full Text]

    Binet D. Hypothesis accounting for the variability of Sardinella abundance in the northern Gulf of Guinea. In: Dynamics and Uses of Sardinella Resources from Upwelling off Ghana and Côte d'Ivoire—Bard F. X., Koranteng K. A., eds. (1995) Paris: ORSTOM Edition. 98–133.

    Binet D. Climate and pelagic fisheries in the Canary and Guinea currents 1964–1993: the role of trade winds and the southern oscillation. Oceanologica Acta (1996) 20:177–190.[Web of Science]

    Binet D., Marchal E. The large marine ecosystem of shelf areas in the Gulf of Guinea: long-term variability induced by climatic changes. In: Large Marine Ecosystem V: Stress, Mitigation and Sustainability of Large Marine Ecosystems—Sherman K., Alexander L., Gold B., eds. (1993) Washington: American Association for the Advancement of Science. 104–118.

    Brodeur R. D., Ware D. M. Long-term variability in zooplankton biomass in the Subarctic Pacific Ocean. Fisheries Oceanography (1992) 1:32–38.[CrossRef]

    Colebrook J. M. Continuous plankton records: seasonal variations in the distribution and abundance of plankton in the North Atlantic Ocean and the North Sea. Journal of Plankton Research (1982) 4:435–462.[Abstract/Free Full Text]

    Colebrook J. M. Environmental influences on long-term variability in marine plankton. Hydrobiologia (1986) 142:309–325.[CrossRef][Web of Science]

    Cushing D. H. The natural regulation of fish populations. In: Sea Fisheries Research—Harden Jones F. R., ed. (1974) London: Elek Science. 399–412.

    Cushing D. H. Marine Ecology and Fisheries (1975) Cambridge: Cambridge University Press. 278.

    Cushing D. H. Climate and Fisheries (1982) London: Academic Press.

    Cushing D. H. Recent studies on long-term changes in the sea. Freshwater Biology (1990) 23:71–84.[CrossRef][Web of Science]

    Cushing D. H. The long-term relationship between zooplankton and fish: IV. Spatial/Temporal Variability and Prediction. ICES Journal of Marine Science (1995) 52:611–626.[CrossRef][Web of Science]

    Fontaine B., Janicot S., Roucou P. Coupled ocean–atmosphere surface variability and its climate in the tropical Atlantic region. Climate Dynamics (1999) 15:451–473.[CrossRef][Web of Science]

    Francis R. C., Hare S. R. Decadal-scale regime shifts in the large marine ecosystems of the North-east Pacific: a case for historical science. Fisheries Oceanography (1994) 3:279–291.[CrossRef]

    Fransz H. G., Mommaerts J. P., Radach G. Ecological modeling of the North Sea. Netherlands Journal of Sea Research (1991) 28:67–140.

    Frost M. T., Hardman-Mountford N. J., Kennington K., Frid C. L. J., Griffiths C., Joint I., Hawkins S. J. Marine Environmental Change Network: Final Report. Report to DEFRA (Contract CDEP 84/5/311) from the Marine Biological Association of the UK (2005) Plymouth.

    Gilbert R. O. Statistical Methods for Environmental Pollution Monitoring. (1987) New York: Van Nostrand Reinhold.

    Harris R. P., Wiebe P., Lenz J., Skjoldal H. R., Huntley M., eds. ICES Zooplankton Methodology Manual (2000) London: Academic Press. 684.

    Houghton R. W. Seasonal variations of the subsurface thermal structure in the Gulf of Guinea. Journal of Physical Oceanography (1983) 13:2070–2081.[CrossRef][Web of Science]

    Howat G. R. Variations in the composition of the sea in West African waters. Nature (1945) 155:415.[CrossRef]

    ICES. Zooplankton monitoring results in the ICES area: summary status report 2004/2005. ICES Cooperative Research Report (2006) 281:43.

    IPCC. Climate Change 2007: Mitigation. Contribution of Working Group III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change (2007) 35.

    Jossi J. W., Goulet J. R. Zooplankton trends: US north-east shelf ecosystem and adjacent regions differ from north-east Atlantic and North Sea. ICES Journal of Marine Science (1993) 50:303–313.[Abstract/Free Full Text]

    Koranteng K. A. The Ghanaian fishery for sardinellas. In: Dynamics and Use of Sardinella Resources from Upwelling off Ghana and Ivory Coast—Bard F. X., Koranteng K. A., eds. (1995) Paris: ORSTOM Edition. 290–299.

    Koranteng K. A., McGlade J. M. Climatic trends in continental shelf waters off Ghana and in the Gulf of Guinea, 1963–1992. Oceanologica Acta (2000) 24:187–198.[CrossRef][Web of Science]

    Lampert W. The adaptive significance of diel vertical migration of zooplankton. Functional Ecology (1989) 3:21–27.[CrossRef]

    Longhurst A. R. A review of the oceanography of the Gulf of Guinea. Bulletin de l'Institute Africain Noire Serie A (1962) 24:633–663.

    Mackas D. L. Interannual variability of the zooplankton community off southern Vancouver Island. In: Climate Change and Northern Fish Populations—Beamish R. J., ed. (1995) Ottawa: National Research Council of Canada. 603–615.

    Mensah M. A. The occurrence of the marine copepod Calanoides carinatus (Krøyer) in Ghanaian waters. Ghana Journal of Science (1974) a 14:147–166.

    Mensah M. A. The reproduction of the marine copepod Calanoides carinatus (Krøyer) in Ghanaian waters. Ghana Journal of Science (1974) b 14:167–192.

    Mensah M. A. The Influence of Climatic Changes on the Coastal Oceanography of Ghana (1991) Abidjan: ORSTOM.

    Mensah M. A. The occurrence of zooplankton off Tema during the period 1969–1992. In: Dynamics and Use of Sardinella Resources from Upwelling off Ghana and Ivory Coast—Bard F. X., Koranteng K. A., eds. (1995) Paris: ORSTOM Editions. 279–289.

    Mensah M. A., Koranteng K. A. A review of the oceanography and fisheries resources in the coastal waters of Ghana, 1981–1986. Marine Fisheries Research Report, 8. (1988) 35.

    Merle J., Arnault S. Seasonal variability of the surface dynamic topography in the tropical Atlantic Ocean. Journal of Marine Research (1985) 43:267–288.[Web of Science]

    Mollmann C., Kornilovs G., Sidrevics L. Long-term dynamics of main mesozooplankton species in the central Baltic Sea. Journal of Plankton Research (2000) 22:2015–2038.[Abstract/Free Full Text]

    Parsons T. M., Takahashi M., Hargrave B. Biological Oceanographic Processes (1984) Oxford: Pergamon Press. 330.

    Pearson E. S., Hartley H. O. Biometrika Tables for Statisticians (1966) Cambridge: Cambridge University Press. 246.

    Quaatey S. N. K., Maravelias C. D. Maturity and spawning pattern of Sardinella aurita in relation to water temperature and zooplankton abundance off Ghana, West Africa. Journal of Applied Ichthyology (1999) 15:63–69.[CrossRef]

    Quenouille N. H. Associated Measurements (1952) London: Butterworth Scientific.

    Taylor A. H., Stephens J. A. Latitudinal displacement of the Gulf Stream (1966–1977) and their relation to changes in temperature and zooplankton abundance in the NE Atlantic. Oceanologica Acta (1980) 3:145–149.[Web of Science]

    Verheye H. M. Short-term variability during an anchor station study in the southern Benguela upwelling system: abundance, distribution, and estimated production of mesozooplankton with special reference to Calanoides carinatus. Progress in Oceanography (1991) 28:91–119.[CrossRef][Web of Science]

    Vervoort W. Pelagic Copepoda. Part I: Copepoda Calanoida of the Families Calanidae up to and Including Euchaetidae (1963) Copenhagen: Danish Science Press Limited.

    Vervoort W. Pelagic Copepoda. Part II: Copepoda Calanoida of the Families Phaennidae up to and Including Acartiidae, Containing the Description of a New Species of Aetideidae. (1965) Copenhagen: Danish Science Press Limited.

    Wiafe G. Spatial and temporal dynamics of plankton communities in the Gulf of Guinea ecosystem. (2002) Legon: Department of Oceanography and Fisheries, University of Ghana. 188.


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