Provided for non-commercial research and educational use only. Not for reproduction, distribution or commercial use. This chapter was originally published in the book Advances in Ecological Research, Vol. 43, published by Elsevier, and the attached copy is provided by Elsevier for the author's benefit and for the benefit of the author's institution, for non-commercial research and educational use including without limitation use in instruction at your institution, sending it to specific colleagues who know you, and providing a copy to your institutions administrator. All other uses, reproduction and distribution, including without limitation commercial reprints, selling or licensing copies or access, or posting on open internet sites, your personal or institutions website or repository, are prohibited. For exceptions, permission may be sought for such use through Elsevier's permissions site at: http://www.elsevier.com/locate/permissionusematerial From: Robert Ptacnik, Stefanie D. Moorthi and Helmut Hillebrand, Hutchinson Reversed, or Why There Need to Be So Many Species. In Guy Woodward, editor: Advances in Ecological Research, Vol. 43, Burlington: Academic Press, 2010, pp. 1-43. ISBN: 978-0-12-385005-8 © Copyright 2010 Elsevier Ltd. Academic Press Author's personal copy Hutchinson Reversed, or Why There Need to Be So Many Species ROBERT PTACNIK, STEFANIE D. MOORTHI AND HELMUT HILLEBRAND Summary . 1 I. Introduction . 2 II. Peculiarities of the Plankton . 4 III. Dispersal Limitation in the Plankton . 7 IV. Present Evidence for B–EF Relationships in the Plankton. 12 A. Primary Production and Resource Use . 12 B. Resource Use in Heterotrophic Bacteria . 12 C. Secondary Production and Trophic Interactions . 13 D. Underyielding and Superspecies . 14 V. Mechanisms Underlying Pelagic B–EF Relationships . 15 A. Environmental and Trait Dimensionality . 15 B. Productivity–Environmental and Trait Dimensionality . 20 C. Spectral Coexistence and Stoichiometry . 24 D. Stoichiometry of Ecosystem Functioning . 26 VI. Outlook and Conclusions . 31 Acknowledgements . 33 Appendix. Ptacnik, Moorthi and Hillebrand: Hutchinson Reversed or Why There Need to be so Many Species . 33 References . 33 SUMMARY There is compelling evidence for dispersal limitation among microscopic organisms, including phyto- and zooplankton, especially from studies addressing spatial patterns in taxon richness. This evidence is not in conflict with the widely accepted importance of strong local interactions in the plankton. However, the simultaneous importance of dispersal limitation and strong local interactions can only be understood when taking high temporal turnover rates into account. Current observational and experimental evidence suggests that biodiversity– ecosystem functioning (B–EF) relationships do not differ systematically from those known from higher organisms. Plankton communities are not saturated by default. ADVANCES IN ECOLOGICAL RESEARCH VOL. 43 0065-2504/10 $35.00 # 2010 Elsevier Ltd. All rights reserved DOI: 10.1016/S0065-2504(10)43001-9 Author's personal copy 2 ROBERT PTACNIK ET AL. Although the pelagial has little spatial structure, it is rich in environmental dimensionality when considering the dimensionality in time and chemical and physical properties, resulting in complex biotic interactions. We propose a conceptual model explaining B–EF effects in plankton, which contrasts environmental dimensionality with trait dimensionality of the community. This model, which is applicable to ecological communities in general, predicts that positive B–EF relationships depend on sufficient envi- ronmental dimensionality. We show how this model can be applied to understand B–EF relationships along gradients of productivity and stoichiometry. Our major conclusions are that local community dynamics of plankton communities may be better understood when putting them into a wider spatial context, that is, considering regional species pools. Moreover, the framework of environmental and trait dimensionality can be used to make concise predictions for the occurrence and strength of B–EF relationships. I. INTRODUCTION The increasing awareness of the accelerating loss of global biodiversity (Worm et al., 2006) has supported a major shift in ecological research in the past decade or so. Initially, researchers were mainly interested in how diversity is regulated in natural communities, and how apparently similar species may coexist, but the focus has now moved towards understanding diversity effects on ecosystem processes and services (Hillebrand and Matthiessen, 2009; Hooper et al., 2005; Reiss et al., 2009). Starting from Tilman’s seminal grassland experiments (Tilman et al. 1996), research on biodiversity–ecosystem functioning (B–EF) relationships has progressed rapidly, especially in terrestrial ecology (Hooper et al., 2005). In aquatic habitats, most of the experimental work to date has focused on B–EF relationships in either microbial microcosms (e.g. Petchey et al., 1999) or, more commonly, among the benthic macrofauna (e.g. Perkins et al., 2010), with very few studies including both micro- and macro-organisms (but see Reiss et al., 2010b). Benthic communities are in many ways much more similar to terrestrial communities than are their pelagial counterparts, which have so far received least attention in B–EF research. In fact, only 7 of 84 studies in the synthesis data set assembled by Cardinale et al. (2006b) deal with pelagic organisms, and these are all laboratory, rather than field, experiments. Nevertheless, this experimental work with artificial plankton communities played a pivotal role in the process of progressing from the early focus on grassland communities and primary producers into how diversity affects trophic interactions and food web dynamics (McGrady- Author's personal copy HUTCHINSON REVERSED, OR WHY THERE NEED TO BE SO MANY SPECIES 3 Steed et al., 1997; Naeem and Li, 1997). However, while these experiments used planktonic organisms as model communities, they were not specifically designed to address pelagic systems, but to test first principles applicable to ecological communities in general. The fact that diverse plankton communities exist within a seemingly homogenous environment with only a small number of limiting resources (light and one or few nutrients) has led to the notion of ‘The paradox of the plankton’, as first proposed in Hutchinson’s classic 1961 paper. This appar- ent paradox implies a high degree of redundancy within these communities, in terms of, for instance, comparable resource requirements, similar uptake mechanisms of resources and similar vulnerability regarding predation, and is based on the intuitive assumption that local diversity of highly mobile organisms largely reflects local dynamics. The biological distinctness of planktonic communities in lakes, as well as the fact that they represent sensitive indicators to environmental stress, such as acidification and eutro- phication (e.g. Watson et al., 1997), has supported a ‘locally centred’ view on plankton communities, implicitly assuming that spatial processes are of secondary importance (see Section II). This local focus has been further supported by the apparent ubiquitous distribution of many planktonic morphospecies (Fenchel and Finlay 2004). For decades, microscopic organisms have been considered as not being limited by dispersal, implying that local community composition simply reflects local processes. Baas-Becking’s tenet ‘everything is everywhere’ (de Wit and Bouvier, 2006) has apparently been reinforced and fostered by the results of many studies. It has been argued that microbial organisms such as phytoplankton are highly abundant and disperse rapidly and thus are not prone to local extinction; moreover, the local diversity is considered so high that a reduction in ecosystem functioning with the loss of species is not expected, since many species can potentially perform similar roles (Finlay, 2002). These views have been challenged by the more critical evaluation of signs of biogeography in microbes and protists (Green and Bohannan, 2006; Martiny et al., 2006; Smith et al., 2005; Vyverman et al., 2007) and new molecular techniques in particular have challenged the perceived existence of global diaspora (Hurd et al., 2010). Increasingly, recent evidence suggests that despite this seeming ‘ubiquity’ of micro-organisms biogeographic diversity patterns are indeed manifested among the bacterioplankton (Fuhrman et al., 2008), phytoplankton (Ptacnik et al., 2010; Smith et al., 2005) and zooplankton (Rutherford et al., 1999) and that micro-organism diversity often follows similar patterns found for macro-organisms, for example, in relation to productivity (Irigoien et al., 2004; Smith, 2007)or area (Horner-Devine et al., 2004). Recent meta-analyses suggest that such Author's personal copy 4 ROBERT PTACNIK ET AL. patterns indeed exist across microbial taxa, even though they may be weaker or responses less steep than for macro-organisms (Drakare et al., 2006; Hillebrand, 2004; Soininen et al., 2007). An increasing number of studies find strong support for regional diversity control in both phyto- and zoo- plankton (see Section III). At the same time, there is accumulating evidence that comparable scaling relationships between biodiversity and functioning exist both in the microscopic and in the macroscopic world, contradicting the assumption that fundamental differences necessarily exist (see Section IV). Both the ongoing paradigm shift regarding dispersal limitation in