Elsevier

Progress in Oceanography

Volumes 97–100, May–July 2012, Pages 92-107
Progress in Oceanography

The influence of phytoplankton productivity, temperature and environmental stability on the control of copepod diversity in the North East Atlantic

https://doi.org/10.1016/j.pocean.2011.11.009Get rights and content

Abstract

The patterns of copepod species richness (S) and their relationship with phytoplankton productivity, temperature and environmental stability were investigated at climatological, seasonal and year-to-year time scales as well as scales along latitudinal and oceanic–neritic gradients using monthly time series of the Continuous Plankton Recorder (CPR) Survey collected in the North East Atlantic between 1958 and 2006. Time series analyses confirmed previously described geographic patterns. Equatorward and towards neritic environments, the climatological average of S increases and the variance explained by the seasonal cycle decreases. The bi-modal character of seasonality increases equatorward and the timing of the seasonal cycle takes place progressive earlier equatorward and towards neritic environments. In the long-term, the climatological average of S decreased significantly (p < 0.001) between 1958 and 2006 in the Bay of Biscay and North Iberian shelf at a rate of ca. 0.04 year−1, and increased at the same rate between 1991 and 2006 in the northernmost oceanic location. The climatological averages of S correlate positively with those of the index of seasonality of phytoplankton productivity (ratio between the minimum and maximum monthly values of surface chlorophyll) and sea surface temperature, and negatively with those of the proxy for environmental stability (monthly frequency of occurrence of daily averaged wind speed exceeding 10 m s−1). The seasonal cycles of S and phytoplankton productivity (surface chlorophyll as proxy) exhibit similar features in terms of shape, timing and explained variance, but the relationship between the climatological averages of both variables is non-significant. From year-to-year, the annual averages of S correlate negatively with those of phytoplankton productivity and positively with those of sea surface temperature along the latitudinal gradient, and negatively with those of environmental stability along the oceanic–neritic gradient. The annual anomalies of S (i.e. factoring out geographic variation) show a unimodal relationship with those of sea surface temperature and environmental stability, with S peaking at intermediate values of the anomalies of these variables. The results evidence the role of seasonality of phytoplankton productivity on the control of copepod species richness at seasonal and climatological scales, giving support to the species richness–productivity hypothesis. Although sea surface temperature (SST) is indeed a good predictor of richness along the latitudinal gradient, it is unable to predict the increase of richness form oceanic to neritic environments, thus lessening the generality of the species richness–energy hypothesis. Meteo-hydrographic disturbances (i.e. SST and wind speed anomalies as proxies), presumably through its role on mixed layer depth dynamics and turbulence and hence productivity, maximise local diversity when occurring at intermediate frequency and or intensity, thus providing support to the intermediate disturbance hypothesis on the control of copepod diversity.

Highlights

► Patterns of copepod richness (S) in the NE Atlantic were examined using CPR data. ► S was related with temperature, phytoplankton productivity and environmental stability. ► Temperature is a good predictor of S along the latitudinal gradient. ► Phytoplankton seasonality controls S along latitudinal and oceanic–neritic gradients. ► Meteo-hydrographic disturbances at intermediate frequency/intensity maximise S.

Introduction

The study of the patterns of species richness and their causes is one of the central and oldest questions in ecological and evolutionary theory (Darwin, 1839). The latitudinal, equatorward increase in species richness has received much attention. This pattern has being reported for an ample number of taxa independently of the geographic context (terrestrial or oceanic) or time domain (contemporary or paleontological) considered (Willing et al., 2003). However, while the patterns have become increasingly well documented, especially in the last decade due to the concerns about the impacts of global change on the erosion of diversity and its effect on ecosystem function and dynamics (Chown and Gaston, 2000, Worm et al., 2006), the relative importance of the factors and mechanisms proposed to account for the temporal and spatial changes of diversity remains a matter of debate (Willing et al., 2003, Mora and Robertson, 2005). Most causal hypotheses can be classified into those based on the variability of environmental factors (productivity, energy supply and environmental stability), null models (the mid-domain effect) or other patterns, such as the Rapoport effect (Rohde, 1992, Roy et al., 1998, Colwell and Lees, 2000).

The knowledge of diversity patterns in the pelagic realm is still scarce compared to that for terrestrial ecosystems (Hillebrand, 2004, Webb, 2009). It has being suggested that species richness varies along latitudinal, oceanic–neritic and bathymetric gradients (Angel, 1997). Proposed explanations to account for present day patterns invoke numerous interacting factors which operate on a wide range of spatial and temporal scales, from global/geological (104 km/millennia) to local/diel (metres/hours) (Angel, 1997). The co-variability observed between species richness of different pelagic taxa and environmental descriptors, such as sea surface temperature, concentration of inorganic nutrients or chlorophyll, gives support to the hypotheses that stress the role of environmental factors as controllers of diversity. Among them, the species richness–ambient energy and the species richness–productivity hypotheses (Currie, 1991, Willing et al., 2003) have received the greatest support among pelagic taxa (e.g. Roy et al., 1998, Rutherford et al., 1999, Macpherson, 2002, Rombouts et al., 2009). The ambient energy hypothesis states that the input of solar energy determines a physical environment that affects organisms through their physiological responses to temperature. This hypothesis includes other explanations, such as climatic stability, environmental stability, environmental predictability, seasonality and harshness (Willing et al., 2003). The productivity hypothesis posits that energy availability, productivity and biomass, also tightly linked to the input of solar energy, are the main controllers of diversity. Both hypotheses share the common theme of energy but differ in the ultimate pathways by which available energy controls diversity. Gillooly and Allen (2007) suggest that the two forms of energy, kinetic and chemical potential energy, should be kept separate because they regulate diversity in different ways: the first through its effects on metabolic rates, the second through its effects on total community abundance. Discrimination between hypotheses is complicated by the multi-factorial and multi-scale control of diversity (Angel, 1997) and by the potential bias induced by spatial autocorrelation and co-linearity among environmental explanatory variables (Mora and Robertson, 2005, Rombouts et al., 2009), which makes it difficult to determine which of the environmental factors are causal or coincidental (Colwell and Lees, 2000).

Among the biotic components of the pelagic ecosystem, zooplankton play a fundamental role because of their importance in terms of both abundance and biomass and their contribution to a variety of ecosystem processes (Richardson, 2008). Copepods, the most prominent taxa of zooplankton, act as major grazers in oceanic food-webs, channelling energy from primary producers to higher trophic levels, and contribute to biogeochemical cycles by means of the regeneration of nutrients through excretion and the sequestration of organic matter into the seafloor via sinking of faecal pellets and corpses, thus contributing in a fundamental way to the biological pump (Longhurst and Harrison, 1989). In addition, copepods are also good indicators of climate change because their growth, reproduction and distribution are under strong bottom-up control (Mauchline, 1998, Richardson, 2008). Consequently, knowledge of the patterns of copepod diversity, both at regional and basin scales, and the underlying factors and mechanisms controlling their patterns of distribution and diversity is fundamental in the present scenario of global change (i.e. over exploitation, pollution and climate change – deYoung et al., 2008, Cury et al., 2008). Whereas the patterns of copepod diversity have been documented in recent years at several temporal and spatial scales (Beaugrand et al., 2000a, Beaugrand et al., 2002b, Wood-Walker, 2001, Wood-Walker et al., 2002, Piontkovski et al., 2006, Rombouts et al., 2009), the investigation on the environmental controls has received less attention (Beaugrand et al., 2000a, Beaugrand et al., 2003, Beaugrand and Ibanez, 2004, Rombouts et al., 2009).

The Continuous Plankton Recorder (CPR) Survey (http://www.sahfos.org/) provides the scientific community long-term, near-surface abundance of phyto- and zooplankton data in the North Atlantic (Richardson et al., 2006). The application of time series, multivariate and geostatistical techniques to different spatial and temporal aggregations of CPR data have provided new insights on the distribution of copepod diversity in the North Atlantic and the hydroclimatic factors that control its spatial (from meso- to basin-scale) and temporal (from daily to multi-decadal) variability (Beaugrand et al., 2000a, Beaugrand et al., 2000b, Beaugrand et al., 2001, Beaugrand et al., 2002a, Beaugrand et al., 2003, Beaugrand, 2004a, Beaugrand, 2004b). Here we have applied time series analysis techniques to spatial compartments (selected CPR Standard Areas) (Beare et al., 2003 and references therein) distributed along oceanic, latitudinal and temperate, oceanic–neritic gradients in the North East Atlantic to: (1) characterise the patterns of copepod species richness at climatological, seasonal and year-to-year time scales along these gradients, and (2) analyse the relationship between copepod species richness and phytoplankton productivity, temperature and environmental stability to investigate the role of these factors on the control of copepod diversity.

Section snippets

Indices of copepod species richness from CPR data

The CPR Survey, initiated in 1931 by Sir Alister Hardy (Hardy, 1939), is the largest plankton monitoring programme in the world (Reid et al., 2003). Sampling is carried out by means of a high speed plankton recorder device towed by ‘ships of opportunity’ along their standard routes (Hays, 1994, Warner and Hays, 1994, Reid et al., 2003). Each sample corresponds to approximately 3 m3 of near-surface (ca. 7 m depth) seawater filtered by a slow moving band of silk of 270 μm mesh size along ca. 10

Mean taxonomic richness (S)

Along the oceanic, latitudinal gradient, the climatological average of mean taxonomic richness of copepods per sample (S) increased equatorward (Fig. 2a). Seasonality was a prominent mode of variation in the monthly time series, although its contribution to total variability decreased from subpolar to temperate latitudes (ca. 65% in B6–C6 to ca. 40–50% in E6–F6) (Table 1). The seasonal cycle showed a marked latitudinal pattern (Fig. 3a): the unimodal character of the cycle was significantly

Time series analysis and the estimation of species richness

Two methodological considerations must be taken into account before interpreting the results presented here. First, although the application of time series analysis methods on spatial compartments have been and still are (e.g. Kirby et al., 2009) commonly applied to CPR data in order to extract the components of variability of the series (e.g. overview of statistical methods by Beaugrand et al., 2003, Beare et al., 2003) biases may arise as a result of the possible interaction between temporal

Acknowledgements

We gratefully thank the Sir Alister Hardy Foundation for Ocean Sciences responsible of the maintenance of the Continuous Plankton Recorder Survey. Special thanks to David Johns for kindly providing the CPR data requested. G.G.-N. acknowledges the ‘Consejería de Educación y Cultura del Principado de Asturias’ for the pre-doctoral fellowship. Thanks are also given to two anonymous referees who improved the final version of the manuscript. The authors dedicate this paper to the memory of our

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    Present address: Intergovernmental Oceanographic Commission, UNESCO, 1 Rue de Miollis, 75732 Paris, France.

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