17 Geographic variation in the diversity of microbial communities: research directions and prospects for experimental biogeography J o a q u í n H o r t a l Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales (CSIC), Madrid, Spain; and Azorean Biodiversity Group – CITA A, Department of Agricultural Sciences, University of the Azores, Angra do Heroísmo, Terceira, Açores, Portugal 17.1 Introduction Traditionally, most ecologists understand the world from a human scale. Ecosystems are often understood as large visible units of the landscape,1 u s u - ally homogeneous land patches or a series of adjacent patches with intense fl ows of individuals, energy or biomass and nutrients. However, there is more in a landscape than meets the eye. An arguably homogeneous land patch within a 1 C o m m o n l y ‘ a l l t h e visible features of an area of land’ ( Compact Oxford English Dictionary , revised edition 2008; my italics). In ecology, a series of spatial units occupied by an heterogeneous species assemblage (e.g. Polis et al., 2003). Biogeography of Microscopic Organisms: Is Ever y thing Small Ever y where?, ed. Diego Fontaneto. Published by Cambridge University Press. © The Systematics Association 2011. 336 BIOGEOGRAPHY OF MICROSCOPIC ORGANISMS landscape hosts many small ecosystems, or microhabitat patches, where many diff erent communities of microbes 2 dwell and interact. For example, imagine you are standing in a clearing of an open forest in a temperate region. A terrestrial ecologist studying macroscopic organisms would think he is looking at part of a single ecosystem. On the contrary, a microbial ecologist will identify a plethora of diff erent ecosystems, including leaf litter of diff erent degrees of humidity, the bark of each diff erent tree and shrub species, treeholes, temporary puddles and pools, moss cushions of diff erent life forms growing over diff erent substrates, etc. Not to mention soil communities. In other words, a 1 ha clearing within a forest could be considered a whole landscape for many groups of microbes. A key question in microbial ecology is thus whether the patterns and organisation of microbial communities diff er from those of macroscopic organisms just in terms of scale or they are so radically diff erent that the rules aff ecting macrobes cannot be extrapolated to microbes. Th e debate on this question extends to the biogeography of microorganisms. Strikingly, it has been argued that most microorganisms do not have biogeography; that is, that contrary to macroorganisms, the distributions of microorganism species are just limited by local environmental conditions (e.g. Fenchel and Finlay, 2003 , 2004 and below). But, are microbes so diff erent from their larger relatives than they follow diff erent ecological and biogeographic rules? Here I will argue that when it comes to the spatial distribution (and basic ecol- ogy) of their communities, many microbes (especially multicellular ones) are just smaller than large organisms, rather than radically diff erent in their ecological organisation and biogeographic responses. More precisely, I will fi rst argue that not everything small is everywhere, and then provide a brief account of current evidence on the spatial distribution of microbe diversity at the community level. Given the purpose of this chapter, this review will be argumentative rather than exhaustive. Based on such review, I will propose the study of microbes as a way of advancing current biogeographic and macroecological theory, 3 under the hypoth- esis that some biogeographic principles can be evaluated with success on micro- organisms, controlling for many of the confounding factors acting at large scales, or even allowing to develop experiments in biogeography. 2 By microbes I refer to all microscopic and small-sized organisms. I will use this term (and eventually microorganisms for style reasons) throughout. Microbes are often defi ned as organisms less than 1–2 mm in size (in opposition to macrobes, i.e. those larger than 2 mm; see Finlay, 2002 ), but here I will use a relaxed defi nition of microorganisms, and follow the common use of including also bryophytes, ferns and fungi, whose spores are smaller than 2 mm. 3 Note that I refer to patterns at the community level (i.e. species richness, species replacement or functional diversity); complementarily, Jenkins and colleagues (Chapter 15) propose using microbes to study a series of biogeographical principles at the species level, namely the relationships between species distributions and abundance, body size and niche characteristics, and the phylogenetic structure of species across space. GEOGRAPHIC VARIATION IN THE DIVERSITY OF MICROBIAL COMMUNITIES 337 17.2 Spatial variations in the diversity of microscopic organisms 17.2.1 Is everything small everywhere? Perhaps the most striking diff erence between the known spatial distributions of macrobe and microbe species is that while restricted distributions are the rule for the former, it has been argued that they may be exceptions for the latter (Fenchel and Finlay, 2003 , 2004 ; Kellogg and Griffi n, 2006 Fontaneto and Hortal, 2008 ). However, the level of knowledge about the spatial distribution of microbial diver- sity is not comparable to that of macroscopic organisms. Despite the causes of the spatial distribution of diversity still being under debate (see section 17.4 below), the current degree of knowledge on macrobes is rather good. Although most of the groups with well-known diversity patterns at the global scale are vertebrates (Grenyer et al., 2006 ; Schipper et al., 2008 ), the variations in the numbers of spe- cies of plants (Kreft and Jetz, 2007 ) or insects (Dunn et al., 2009 ) throughout the globe are also starting to be well-known, and at least partly understood (Lomolino et al., 2006 ). In contrast, the level of knowledge on the spatial distribution of most (if not all) groups of microorganisms is quite limited (Foissner, 2008 ; Fontaneto and Hortal, 2008 ). Whether such defi cit in knowledge is the cause of the apparent lack of biogeography of most microorganisms or not is perhaps the hottest debate in current microbial ecology. Th e realisation that, apparently, many microbial species are found in quite dis- tant localities led to the proposition of the ‘Everything is everywhere’ (EiE ) hypoth- esis at the beginning of the twentieth century (Beijerinck, 1913 ; Baas Becking, 1934 ). Th is hypothesis is further supported by the high dispersal potential (sensu Weisse, 2008 ) of most microbes (Finlay, 2002 ). Th eir small size, large population numbers and, especially, the ability to either enter dormant states or produce small spores allow many microorganisms to produce vast numbers of propagules that are easily dispersed in a passive way (i.e. ‘ubiquitous dispersal’: Fenchel, 1993 ; Finlay et al., 1996a , 2006 ; Cáceres, 1997 ; Wilkinson, 2001 ; Fenchel and Finlay, 2004 ). Arguably, this would permit many microbes to maintain cosmopolitan distribu- tions. Although the EiE hypothesis has been the dominant paradigm for micro- bial biogeography until relatively recently (O’Malley, 2007 , 2008 ), it has been hotly debated during the last decade, dividing microbial ecologists into two factions (Whitfi eld, 2005 ). Some argue that the rule for microorganisms is ‘Everything is everywhere, but the environment selects’ (Finlay, 2002 ; de Wit and Bouvier, 2006 ; Fenchel and Finlay, 2006 ). Others counter that many apparently cosmopolitan ranges are actually artifacts of the defi cient taxonomy of microbes, which does not permit distinguishing between morphologically similar but spatially and genetic- ally isolated lineages (Coleman, 2002 ; Foissner, 2006 , 2008 ; Taylor et al., 2006 ). 338 BIOGEOGRAPHY OF MICROSCOPIC ORGANISMS In my opinion there is now enough information to develop a theoretical (and analytical) framework that will resolve the EiE debate and lay the foundations for a general theory of microbial biogeography. However, this is beyond the intended scope of the chapter; more information can be found in several chapters of this book, or by consulting the references above (see also Martiny et al., 2006 ; Green and Bohannan, 2006 ; Telford et al., 2006 ; Green et al., 2008 ). Having said this, any study on the spatial distribution of microorganism communities shall necessarily address the question of whether everything small is everywhere. Should microbes be locally abundant and extremely widespread, their local diversity would be the result of random colonisation processes, as argued by, for example, Finlay et al. ( 1999 , 2001 ). Here, diff erences among communities would be determined only by local environmental conditions. However, such cosmopolitanism seems to be far from universal. Many microbe species have been found to have restricted distri- butions (Mann and Droop, 1996 ; Smith and Wilkinson, 2007 ; Frahm, 2008 ; Segers and De Smet, 2008 ; Vanormelingen et al., 2008 ; Spribille et al., 2009 ). Hence, the dependence of range size on body size hypothesised by Finlay and colleagues (e.g. Finlay et al., 1996b ; Finlay, 2002 ; Finlay and Fenchel, 2004 ) is not as general as they argue (Valdecasas et al., 2006 ; Pawlowski and Holzman, 2008; but see Martiny et al., 2006 ). More importantly, the EiE hypothesis is challenged in its assumption that the large dispersal potential of microbes necessarily results in high rates of eff ective dispersal (i.e. successful dispersal events, see Weisse, 2008 ). Rather, the propagules of