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