Hortal, J. (2011) In Biogeography of micro-organisms. Is everything small everywhere? (ed. by D.Fontaneto) in press
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Chapter 17
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Geographical variation in the diversity of microbial communities: research directions
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and prospects for experimental biogeography
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Joaquín Hortal1,2*
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Naturales (CSIC), C/José Gutiérrez Abascal 2, 28006 Madrid, Spain.
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851 Angra do Heroísmo, Terceira, Açores, Portugal.
Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias
Azorean Biodiversity Group – CITA-A, Universidade dos Açores, Terra-Chã, 9700-
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* e-mail: jhortal@mncn.csic.es
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Accepted for publication:
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Hortal, J. (2011). Geographical variation in the diversity of microbial communities:
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research directions and prospects for experimental biogeography. In Biogeography of
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micro-organisms. Is everything small everywhere? (ed. by D. Fontaneto), pp. in press.
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Cambridge University Press.
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Hortal, J. (2011) In Biogeography of micro-organisms. Is everything small everywhere? (ed. by D.Fontaneto) in press
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17.1 Introduction
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Traditionally, most ecologists understand the world from a human scale. Ecosystems are
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often understood as large visible units of the landscape1, usually homogeneous land
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patches or a series of adjacent patches with intense flows of individuals, energy or
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biomass and nutrients. However, there is more in a landscape than meets the eye. An
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arguably homogeneous land patch within a landscape hosts many small ecosystems, or
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microhabitat patches, where many different communities of microbes2 dwell and
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interact. For example, imagine you are standing in a clearing of an open forest in a
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temperate region. A terrestrial ecologist studying macroscopic organisms would think
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he is looking at part of a single ecosystem. On the contrary, a microbial ecologist will
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identify a plethora of different ecosystems, including leaf litter of different degrees of
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humidity, the bark of each different tree and shrub species, treeholes, temporary puddles
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and pools, moss cushions of different life forms growing over different substrates, etc.
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Not to mention soil communities. In other words, a 1 ha clearing within a forest could
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be considered a whole landscape for many groups of microbes.
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A key question in microbial ecology is thus whether the patterns and
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organization of microbial communities differ from those of macroscopic organisms just
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in terms of scale or they are so radically different that the rules affecting macrobes
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cannot be extrapolated to microbes. The debate on this question extends to the
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biogeography of microorganisms. Strikingly, it has been argued that most
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microorganisms do not have biogeography; that is, that contrary to macroorganisms, the
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distributions of microorganism species are just limited by local environmental
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conditions (e.g. Fenchel & Finlay, 2003, 2004 and below). But, are microbes so
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different from their larges relatives than they follow different ecological and
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biogeographical rules?
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Here I will argue that when it comes to the spatial distribution (and basic
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ecology) of their communities, many microbes (especially multicellular ones) are just
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smaller than large organisms, rather than radically different in their ecological
Commonly “all the 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., 1997).
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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 defined as organisms with less than 1-2
mm of size (in opposition to macrobes, i.e. those larger than 2 mm; see Finlay, 2002), but here I will use a
relaxed definition of microorganisms, and follow the common use of including also bryophytes, ferns and
fungi, whose spores are smaller than 2 mm.
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Hortal, J. (2011) In Biogeography of micro-organisms. Is everything small everywhere? (ed. by D.Fontaneto) in press
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organization and biogeographical responses. More precisely, I will first argue that not
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everything small is everywhere, and then provide a brief account of current evidence on
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the spatial distribution of microbe diversity at the community level. Given the purpose
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of this chapter, this review will be argumentative rather than exhaustive. Based on such
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review, I will propose the study of microbes as a way of advancing current
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biogeographical and macroecological theory3, under the hypothesis that some
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biogeographical principles can be evaluated with success on microorganisms,
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controlling for many of the confounding factors acting at large scales, or even allowing
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to develop experiments in biogeography.
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17.2 Spatial variations in the diversity of microscopic organisms
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17.2.1 Is everything small everywhere?
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Perhaps the most striking difference between the known spatial distributions of macrobe
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and microbe species is that while restricted distributions are the rule for the former, it
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has been argued that they may be exceptions for the latter (Fenchel & Finlay, 2003,
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2004; Kellogg & Griggin, 2006; Fontaneto & Hortal, 2008). However, the level of
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knowledge about the spatial distribution of microbial diversity is not comparable to that
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of macroscopic organisms. Despite the causes of the spatial distribution of diversity are
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still under debate (see section 17.4 below), the current degree of knowledge on
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macrobes is rather good. Although most of the groups with well-known diversity
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patterns at the global scale are vertebrates (Grenyer et al., 2006; Schipper et al., 2008),
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the variations in the numbers of species of plants (Kreft & Jetz, 2007) or insects (Dunn
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et al., 2009) throughout the globe are also starting to be well-known, and at least partly
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understood (Lomolino et al., 2006). In contrast, the level of knowledge on the spatial
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distribution of most (if not all) groups of microorganisms is quite limited (Foissner,
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2008; Fontaneto & Hortal, 2008; and many chapters of this book). Whether such deficit
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in knowledge is the cause of the apparent lack of biogeography of most microorganisms
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or not is perhaps the hottest debate in current microbial ecology.
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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.
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The realization that, apparently, many microbial species are found in quite
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distant localities led to the proposition of the Everything is Everywhere (EiE)
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hypothesis at the beginning of the twentieth century (Beijerinck, 1913; Baas-Becking,
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1934). This hypothesis is further supported by the high dispersal potential (sensu
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Weisse, 2008) of most microbes (Finlay, 2002; Kellogg & Griffin, 2006). Their small
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size, large population numbers and, especially, the ability either to enter dormant states
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or produce small spores allow many microorganisms to produce vast numbers of
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propagules that are easily dispersed in a passive way (i.e. ‘ubiquitous dispersal’:
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Fenchel, 1993; Finlay et al., 1996a, 2006; Cáceres, 1997; Wilkinson, 2001; Fenchel &
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Finlay, 2004). Arguably, this would permit many microbes to maintain cosmopolitan
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distributions. Although the EiE hypothesis has been the dominant paradigm for
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microbial biogeography until relatively recently (O’Malley, 2007, 2008), it has been
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hotly debated during the last decade, dividing microbial ecologists into two factions
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(Whitfield, 2005). Some argue that the rule for microorganisms is ‘everything is
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everywhere, but the environment selects’ (Finlay, 2002; de Wit & Bouvier, 2006;
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Fenchel & Finlay, 2006). Others counter that many apparently cosmopolitan ranges are
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actually artifacts of the deficient taxonomy of microbes, which does not permit
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distinguishing between morphologically similar but spatially and genetically isolated
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lineages (Coleman, 2002; Foissner, 2006, 2008; Taylor et al., 2006).
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In my opinion there is now enough information to develop a theoretical (and
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analytical) framework that will resolve the EiE debate and lay the foundations for a
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general theory of microbial biogeography. However, this is beyond the intended scope
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of the chapter; more information can be found in several chapters of this book, or by
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consulting the references above (see also Martiny et al., 2006; Green & Bohannan,
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2006; Telford et al., 2006; Green et al., 2008). Having said this, any study on the spatial
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distribution of microorganism communities shall necessarily address the question of
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whether everything small is everywhere. Should microbes be locally abundant and
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extremely widespread, their local diversity would be the result of random colonization
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processes, as argued by, e.g. Finlay et al. (1999, 2001). Here, differences among
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communities would be determined only by local environmental conditions. However,
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such cosmopolitanism seems to be far from universal. Many microbe species have been
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found to have restricted distributions (Mann & Droop, 1996; Smith & Wilkinson, 2007;
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Frahm, 2008; Segers & De Smet, 2008; Vanormelingen et al., 2008; Spribille et al.,
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2009). Hence, the dependence of range size on body size hypothesized by Finlay and
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colleagues (e.g. Finlay et al., 1996b; Finlay, 2002; Finlay & Fenchel, 2004) is not as
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general as they argue (Valdecasas et al., 2006; Pawlowski & Holzmann, 2008; but see
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Martiny et al., 2006). More importantly, the EiE hypothesis is challenged in its
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assumption that the large dispersal potential of microbes necessarily results in high rates
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of effective dispersal (i.e. successful dispersal events, see Weisse, 2008). Rather, the
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propagules of many (but not all) microorganisms are not ‘universally successful’ in
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maintaining significant levels of gene flow between geographically remote populations
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(Jenkins, 1995; Jenkins & Underwood, 1998; Bohonak & Jenkins, 2003; Foissner,
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2006, 2008; Jenkins et al., 2007; Weisse, 2008; Frahm, 2008).
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As a direct consequence of the total or partial isolation of populations in relation
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to distance, phylogeographic variations (i.e. geographically structured genetic
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differences) have been found for many microbial taxa. Increasing spatial distance
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between populations results in genetic divergence and isolation even for prokaryotes
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(Whitaker et al., 2003; Prosser et al., 2007; Vos & Velicer, 2008). This may emerge as
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the common rule for many protists and multicellular microbes, once traditional
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approaches to their taxonomy are complemented with more detailed molecular studies
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(Foissner, 2008; Weisse, 2008; Pawlowski & Holzmann, 2008). In fact, many recent
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studies finding significant hidden genetic divergence within morphologically-based
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microbial species find also that these genetically different populations or species occupy
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geographically distant areas (Gómez et al., 2007; Mills et al., 2007; Weisse, 2008;
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Fontaneto et al., 2008a; Xu et al., 2009). Therefore, it could be expected that as
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knowledge of the phylogeny of microorganisms and their taxonomy improves, the
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number of microbe with restricted distributions will increase as well. The actual
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proportion of microbe species with reduced range sizes remains as a mystery, although
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some estimates indicate that at least one third of protist species will show restricted
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distributions (according to the moderate endemicity model; see Foissner, 2006, 2008).
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Nevertheless, such hidden microbial diversity will have an impact on the patterns of
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diversity observed at the community level.
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17.2.2 Spatial variations in microbe communities
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If the distributions of microorganisms are not cosmopolitan, microbe communities in
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similar substrates situated in geographically distant areas ought to show significant
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differences in their diversity and species composition. The spatial replacement of
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species in macrobial communities is typically the result of both environmental
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differences and geographical distance, no matter whether they are lake fishes (Genner et
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al., 2004), mammals (Hortal et al., 2005), birds or land snails (Steinitz et al., 2006).
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Microbes are to some extent similar to macrobes in this particular aspect. Although
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environmental heterogeneity is the main driver of the decay of compositional similarity
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with distance in microorganisms (see Martiny et al., 2006; Green & Bohannan, 2006), it
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is not the only source of spatial variation. Using an array of studies on lake diatoms
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encompassing several continents, Verleyen et al. (2009) found that, although
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environment accounts for the larger part of the spatial replacement of species,
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connectivity4 also explains a large proportion of the compositional similarities between
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lakes: all else being equal, the closer the lakes, the more similar their species
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composition. Similar patterns were found in the phytoplankton communities of the
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Swedish lakes studied by Jankowski & Weyhenmeyer (2006). Interestingly, the strength
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of such replacement may vary according to the kind of habitat for both micro- and
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macrobes. Macrobial communities often show different patterns of distance decay of
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similarity5 in different kinds of habitats (e.g. palm trees, Bjorholm et al., 2008; birds
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and land snails, Steinitz et al., 2006). Similarly, the degree of compositional similarity
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of the communities of bdelloid rotifers in a valley of northern Italy varies from one
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ecological systems to another: whereas stream communities were relatively similar to
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one another throughout the valley, the species integrating the communities from
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terrestrial habitats and lakes were highly variable (Fontaneto et al., 2006).
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In contrast with these qualitative similarities between small- and large-sized
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organisms, the magnitude of the distance-driven changes in species composition across
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similar habitats may not be comparable. The slope of the taxa–area relationship in
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contiguous habitats can be used as a raw measure of the accumulation of species or
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other taxonomic units with area, and hence of compositional changes in space (Prosser,
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2007; Santos et al., 2010; see also Rosenzweig, 1995 and Whittaker & Fernández-
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Palacios, 2007 for extensive reviews on the species–area relationship). To date, the
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slopes recorded for microbes are typically smaller than those of macrobes; while the
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Connectivity measures distance as perceived by the studied organisms; that is, how difficult would be to
move between two sites or colonize a given one taking into account the existence of barriers or
facilitations to dispersal (e.g., mountains or wind currents in the direction of the dispersal, respectively).
Therefore, it can be considered a biologically meaningful analogue to distance.
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The similarity between several ecological and evolutionary phenomena often decreases or decays as the
distance between them increases; the distance decay relationship is thus defined as the negative
relationship between distance and the similarity of biological communities (see Nekola & White, 1999;
Soininen et al., 2007).
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former may range from 0.043 to 0.114 in natural systems, the latter are typically larger
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than 0.15 (in a power model; Finlay et al., 1998; Azovsky, 2002; Green et al., 2004;
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Smith et al., 2005; Bell et al., 2005; Green & Bohannan, 2006; Prosser et al., 2007).
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This indicates that in the absence of environmental differences, the spatial replacement
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in the composition of local communities occurs at much larger scales for microbes,
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varying in the range of a few hundreds to thousands of km, instead of the hundreds or
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even tens of km usually found for macrobes.
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Strikingly, however, when taxa–area relationships are calculated for habitat
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islands (i.e. separate territories/habitat patches instead of contiguous habitats), the
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slopes may reach values well over 0.2 for bacteria, which are similar to those for large-
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sized organisms (Bell et al., 2005; van der Gast, 2005; see also Green & Bohannan,
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2006; Prosser et al., 2007). This indicates that in spite of their minute size, habitat area
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plays a critical role in determining the number of bacterial species that can coexist in a
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given place, as it does for macroorganisms. In other words, although microbial
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communities change with distance at a lower pace than macrobes, the increase in the
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number of species with area is similar for both groups. Further study is required to
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determine whether this dependence on area is due to the carrying capacity of the locality
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(which increases with its area), the increase of habitat diversity with increasing area, or
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to passive sampling mechanisms (i.e. larger areas receive more propagules and therefore
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may be colonized by more species).
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The similarities between the macroecological patterns of micro- and
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macroorganisms do not end with their shared dependence on area. As with their larger
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counterparts, the diversity of microbe communities varies along environmental
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gradients. One of the most studied is the altitudinal gradient: species richness varies
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with altitude, increasing or decreasing for localities closer to or farther from an optimal
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altitudinal band (Rahbek, 1995, 2005). These changes in richness are often accompanied
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by changes in species composition (e.g. the Alpine dung beetles studied by Jay-Robert
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et al., 1997). This macroecological pattern has been also observed in many
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microorganisms. A good example is the altitudinal variations in richness shown by
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rotifers in the Alps (Fontaneto & Ricci, 2006; Fontaneto et al., 2006; Obertegger et al.,
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2010). The diversity of tardigrades inhabiting moss and leaf litter at the Guadarrama
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mountain range also shows a typical hump-shaped relationship with elevation (Guil et
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al., 2009a). Alike macrobes, altitudinal variations in microbe species richness are
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caused by the varying environmental conditions at different elevations. Sometimes the
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decrease in productivity with altitude limits local diversity, as occurs for phytoplankton
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richness in a series of Swedish lakes (Jankowski & Weyhenmeyer, 2006). In other
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cases, the climatic variations associated with elevational changes cause spatial gradients
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in local richness, as with epiphytic bryophyte communities in Guiana (Oliveira et al.,
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2009) or NW Spain (N.G. Medina, B. Albertos, F. Lara, V. Mazimpaka, R. Garilleti, D.
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Draper & J. Hortal, unpublished manuscript). Such climate-driven diversity variations
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in microbes may arise simply because of habitat sorting (i.e. due to the differences in
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niche requirements of each of the species regionally available; see e.g. Whittaker,
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1972). In fact, in the two examples given above many species of both bdelloid rotifers
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and tardigrades show strong habitat selection (i.e. habitat sorting; Fontaneto & Ricci,
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2006 and Guil et al., 2009b, respectively). This is consistent with a high potential for
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dispersal and local environmental selection (although this process may involve an
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important degree of stochasticity, see Fontaneto et al., 2006).
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However, geographical changes in the diversity of microbe species inhabiting
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similar microhabitats are not only the result of local productivity and/or carrying
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capacity and environmental variations. The pool of species that can colonize each
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microhabitat varies also in space, therefore limiting the number and identity of the
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colonizing species. The regional differences produced by changes in the species pool
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are one of the major determinants of the geographical variations of assemblage diversity
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for macroorganisms (Ricklefs, 1987, 2004, 2007; Huston, 1999; Hawkins et al., 2003a;
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Hortal et al., 2008; Hawkins, 2010). Some environments or particular habitats may host
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fewer species simply because fewer of the available species have evolved adaptations to
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these environments, either because these environments are rare in nature, they are too
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recent in the region, or they were affected by important changes in the past, like
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glaciations. In fact, although the dispersal distances and the location of refugia may
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differ, the diversity of several microbial groups has been shaped by post-glacial
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dispersal (e.g. Gómez et al., 2007; Smith & Wilkinson, 2007; Smith et al., 2008). More
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importantly, the composition of the regionally available species pool varies among
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continents, at least for lake diatoms (Verleyen et al., 2009). As with macrobes, these
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differences in the species pool produce different responses to elevational or climatic
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gradients, as shown also for lake diatoms by Telford et al. (2006).
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The ultimate consequence of the spatial variations in microbe communities is the
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existence of geographic differences in ecosystem functioning. Community richness,
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composition, assembly and functional dissimilarity affect ecosystem productivity and
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functioning (Laakso & Setälä, 1999; Fukami & Morin, 2003; Heemsbergen et al., 2004;
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Sánchez-Moreno et al., 2008). Given that microbes perform many ecosystem services,
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geographic variations in community composition are likely to have important functional
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consequences (Naeslund & Norberg 2006; Green et al. 2008). However, the impact of
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these geographic differences in the functions provided by microbial communities in
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ecological processes at regional and global scales is, to date, poorly known.
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17.3 A frontier of biogeography
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An overall insight from the short review above is that the biogeography and
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macroecology of microbial assemblages presents both similarities and differences with
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those of macroorganisms. To synthesize, microbes and macrobes both show distance
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decay in community similarity. It follows that not everything is everywhere. Hence,
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although the decay of similarity and the associated compositional changes are mainly
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caused by environmental gradients, they are also driven by geographical variations in
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the composition of the species pool and the degree of connectivity or the presence of
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barriers to dispersal between localities. The geographical variations in microbe
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assemblages typically occur at larger distances than for macrobes, and thus they show a
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shallower increment of species with increasing area. In spite of this, the relationships
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between local richness and area and environmental gradients are comparable to the ones
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found in macrobes. The differences between micro- and macroorganisms seem thus
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limited to their differences in size and dispersal power, which link microbes to smaller
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microhabitats and make their distributions typically larger.
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Some of the challenges awaiting biogeography are right in front of our eyes,
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rather than in distant places. Whether the similarities and differences between the
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diversity of macrobe and microbe assemblages arise from fundamentally similar or
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different processes needs further investigation. Here I outline a research agenda to help
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explore this particular frontier of biogeography (see also Martiny et al., 2006; Green &
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Bohannan, 2006; Prosser et al., 2007; Green et al., 2008). To understand the spatial
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variations in the diversity of microbial assemblages, research in four main areas is
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needed: microbial taxonomy, description of biogeographical and macroecological
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patterns, community ecology and assembly, and the study of functional diversity and
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ecosystem functioning.
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17.3.1 Microbial taxonomy
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One key question is to determine the extent to which the patterns observed for microbes
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so far are due to their deficient taxonomy, as argued by e.g. Foissner (2008). Strikingly,
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in a recent study on moss-dwelling bdelloid rotifers from the UK and Turkey, the
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pattern of variations in species richness based on traditional taxonomy varies when
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DNA-based taxonomy is applied, not only in the numbers of species identified, but also
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in the relative differences in richness between localities, and their similarity in
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composition (Kaya et al., 2009). In fact, many recent detailed studies reveal large
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amounts of hidden genetic, physiological and ecological diversity in microorganism
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communities (Mann & Droop, 1996; Weisse, 2008; Guil, 2008; Guil & Giribet, 2009;
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Fontaneto et al., 2009). Therefore, the establishment of a solid taxonomy based on the
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identification of ecological and evolutionarily meaningful units through DNA and
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ecophysiological analyses is a necessary prerequisite to the study of the diversity of
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microbes. Importantly, current genetic techniques allow the identification of operational
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taxonomic units (OTUs) just from the divergence in a reduced number of DNA
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sequences with relatively small costs. Thus, a final definition of the species concept
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(which remains elusive for some microbial groups) may not be necessary for describing
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the geographical (and ecological) variations in microorganism diversity.
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17.3.2 Description of macroecological and biogeographical patterns
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Once a good taxonomy is established, it will be possible to describe the patterns of
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variation of the diversity of any group of microorganisms. We know relatively little
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about how the richness and composition of microbes vary around the world. In
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particular, the relationships and compositional similarities between different regions,
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islands and continents are typically unknown, as well as whether the latitudinal diversity
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gradients observed for most groups of macroorganisms hold out for microbes. In the
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same way, the relationships between many microorganisms and the environmental
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conditions (temperature, nutrients, etc.) are often known in lab conditions, but how
313
these responses translate to the real world is unknown. This prevents an accurate
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determination of the influence of climate change on the distribution of microbial
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species, one of the needs identified by Prosser et al. (2007).
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Given current knowledge of the patterns of microbial diversity, three main lines
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of research need development within this particular area. Some of this research must
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first be conducted at the species (or species-group) level, since a degree of basic
319
knowledge is necessary before questions can be addressed at the level of the community
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or assemblage.
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i) Descriptive biogeography: the pure description of geographical patterns of variation
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at the species level or higher (see e.g. Lomolino et al., 2006). This includes the
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identification of biogeographical regions and the inventory of their faunas or floras, as
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well as the study of the geographical gradients of diversity. Achieving this particular
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objective for any microorganism group may need a large amount of fieldwork, but the
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establishment of standardized survey protocols, the focus on one or a set of particular
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microhabitats and the cooperation between experts from different parts of the world
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may facilitate progress within relatively short periods of time. A good example of this
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kind of cooperation is the recent analysis of the global variations in ant richness
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performed by Dunn et al. (2009), who were able to compile over 1000 ant assemblages
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from all over the world coming from standardized surveys within a few years (N.J.
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Sanders, personal communication). Such kind of data can be used to study the
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relationships of diversity with climate, to describe latitudinal gradients, to determine or
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define biogeographical regions, and for other purposes (see also the Macroecology
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section below).
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ii) Phylogeography: assessing the impact of geographical structure on the evolutionary
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relationships among populations of a particular taxon (Avise, 2009). This particular
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research line is already under development for a few microbial groups (e.g. Lowe et al.,
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2005; Gómez et al., 2007; Mills et al., 2007; Mikheyev et al., 2008; Fontaneto et al.,
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2008b). However, these efforts are still dispersed: a goal during the next few years or
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decades must be to develop a coordinated long-term research program to facilitate a
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systematic characterization of the recent evolution and geographical relationships
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between microorganism populations in nature. Thus, as before, some little discussion
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and coordination effort in this area, including the identification of specific research
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goals and certain geographical areas (e.g. islands, archipelagos or the borders of
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continents or biogeographical regions) will certainly enhance current knowledge of the
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phylogeographical patterns of microorganisms. Of particular importance is the potential
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role of humans as dispersal vectors for free-living and parasitic terrestrial
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microorganisms. As Wilkinson (2010) recently stated, the imprint of human-facilitated
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dispersion on the current biogeography of many microorganisms may have been
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underestimated. Determining the impact of increasing biotic homogenization at the
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global scale needs large-scale phylogeographical studies on a number of cosmopolitan
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microbe species.
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iii) Macroecology. Once the basic biogeographical patterns are described for a
358
microorganism group, macroecological analyses can determine the impact of climate,
359
productivity and historical effects on its distribution and diversity. Martiny et al. (2006)
360
review some particular topics that need further research in this area, and provide an
361
analytical framework to study them. In particular, they advocate the study of the effects
362
of environment and history, as well as the processes shaping microbial biogeography,
363
including dispersal and colonization, diversification and extinction, or the relationship
364
between body size and distribution range. Apart from these research topics, the scaling
365
of the relationship between microorganisms and climate needs further study. On the one
366
hand, it is necessary to determine what is the relationship between the responses to
367
environmental factors observed in lab conditions, and the responses to the same factors
368
that are observed in the field. On the other hand, we need to identify the correct scale to
369
assess the effects of large-scale environmental gradients (such as climate) on the
370
diversity of microbial communities inhabiting minute microhabitats. Perhaps
371
surprisingly, climate variables measured with a scale of 1 km2 (i.e. yearly or monthly
372
precipitation and temperature) are good predictors of the spatial variations in the
373
richness of both tardigrades inhabiting 9 cm2 moss and leaf litter samples (Guil et al.,
374
2009) and bryophytes found over oak trunks using quadrats of 400 cm2 (N.G. Medina,
375
B. Albertos, F. Lara, V. Mazimpaka, R. Garilleti, D. Draper & J. Hortal, unpublished
376
manuscript). Thus, some particular research on the extent to which coarse-scale climate
377
and/or microclimatic conditions are affecting microorganism diversity in microhabitats
378
is needed (see also section 17.3.3 below).
379
380
All these lines of research, particularly the first two, will benefit considerably
381
from the cooperation and coordination among the experts of each microbial group.
382
Thus, specific effort should be devoted to scientific networking, particularly among the
383
associations of microbiologists or experts in particular groups. An additional goal is to
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Hortal, J. (2011) In Biogeography of micro-organisms. Is everything small everywhere? (ed. by D.Fontaneto) in press
384
increase the participation of microbiologists in the International Biogeography Society
385
(IBS; http://www.biogeography.org/): a multidisciplinary association that seeks the
386
advancement of all studies of the geography of nature. The results of these efforts could
387
be enhanced with help and interest from the editorial board of journals in both
388
biogeography and microbial ecology, the inclusion of chapters on microbial
389
biogeography in the general books on both disciplines, as well as the organization of
390
specific symposia, such as the one entitled ‘The importance of being small: does size
391
matter in biogeography?’ organized by Diego Fontaneto, David Roberts and Juliet
392
Brodie (held within the 7th Systematics Association Biennial Conference, Leiden, The
393
Netherlands, August 2009), which led to the compilation of this book.
394
395
17.3.3 Community ecology and assembly
396
397
In parallel with the description and analysis of patterns in nature, the ecology of
398
microbial communities needs further research. Two aspects deserve particular attention:
399
disentangling what determines the number of species that a given system can host; and
400
assessing whether the presence of some species (or any other taxa) prevents or
401
facilitates the entrance of other species in the local assemblage.
402
Apart from climate and habitat gradients, the richness of local communities is
403
typically related with their area (MacArthur & Wilson, 1963, 1967; Rosenzweig, 1995),
404
habitat diversity (Triantis et al., 2003; Hortal et al., 2009) and productivity (Wright,
405
1983; Srivastava & Lawton, 1998). As discussed above (section 17.2.2), the richness of
406
microbial communities is related to their area. However, the origin of such dependence
407
on area requires further study, and the same occurs with the relationship with
408
productivity. Here, experiments under laboratory and, especially, natural conditions
409
may help to clarify the relative importance of these factors. Field experiments may not
410
be particularly difficult to set up (see, e.g. Srivastava & Lawton, 1998), by: (i) selecting
411
a particular microhabitat (such as treeholes, temporary ponds, moss cushions or tank
412
bromeliads) that is patchily distributed in a relative small territory (e.g. a valley, a forest
413
patch or a segment of coastline); (ii) measuring or perhaps altering the area, habitat
414
diversity and productivity (in terms of raw provision of nutrients) of these
415
microhabitats; (iii) sterilizing them (or at least washing away as much of the pre-
416
existing communities as possible); (iv) letting these communities develop again by
13
Hortal, J. (2011) In Biogeography of micro-organisms. Is everything small everywhere? (ed. by D.Fontaneto) in press
417
dispersal and colonization from other microhabitats in the territory; before (v)
418
measuring the diversity of the resulting assemblages.
419
Determining whether the coexistence of some species (or taxa) is determined by
420
facilitation or exclusion during the assembly process due to the presence of other
421
species may prove more difficult. One of the most controversial and bitter debates in
422
ecology during the late twentieth century has been elucidating whether there are some
423
assembly rules determining the composition of local communities, and the eventual
424
nature of these rules (for review and synthesis see Gotelli & Graves, 1996; Weiher &
425
Keddy, 1999; Gotelli, 2001; Gotelli & McCabe, 2002; Jenkins, 2006; Sanders et al.,
426
2007). To study their role in microbial communities requires knowledge of the
427
composition of the assemblage before and after the arrival of any new species. This
428
makes it extremely difficult to use field experiments to study the determinants of
429
coexistence and community assembly, although they reveal the effects of dispersal
430
(Oliveira et al., 2009). Rather, lab experiments in controlled conditions, where species
431
are added to previously set up communities, will be a more effective approach here (see
432
Liess & Diehl, 2006 for an example). One particular topic that can be studied using field
433
experiments would be the influence of the richness and composition of the species pool
434
on local communities. In this case, experiments placed in geographically distant
435
territories of environmentally similar regions, together with exhaustive surveys that
436
allow identifying the whole species pool in each territory, could be used to determine
437
how and to what extent local communities are shaped by the species available in their
438
pool.
439
440
17.3.4 Functional diversity and ecosystem functioning
441
442
Describing the functional role of species within an ecosystem might at first be viewed
443
as an unrelated, ‘purely ecological’ research topic. However, the attention of
444
biogeography and community ecology is shifting to consider the geographic distribution
445
of functional traits, species interactions and the organization of the ecosystems provided
446
by the distributions of these traits and interactions (Naeem & Wright, 2003; McGill et
447
al., 2006; Petchey & Gaston, 2006; Green et al., 2008; Schemske et al., 2009). The
448
relationship between biodiversity, biotic interactions and ecosystem functioning is well
449
studied in microbial systems, particularly soil communities (Allsopp et al., 1994;
450
Kennedy & Smith, 1995; Heembsbergen et al., 2004; Wardle, 2006; Bruno et al., 2006;
14
Hortal, J. (2011) In Biogeography of micro-organisms. Is everything small everywhere? (ed. by D.Fontaneto) in press
451
Srivastava & Bell, 2009). New techniques that facilitate the measurement of traits and
452
functioning in microbial communities (in comparison to macrobes; e.g. Lowe et al.,
453
2005) offer encouraging possibilities for the future pursuit of this particular research
454
topic (Green et al., 2008). This could be achieved through fieldwork and analyses
455
designed in a similar way than the ones here argued for macroecology above (section
456
17.3.2), but measuring specific functional traits and/or facets of ecosystem functioning
457
instead of just the diversity of the communities and the inputs of materials and energy.
458
459
17.4 The biogeographer’s wish list: how microbial ecology could reinvigorate the
460
development of biogeographical theory
461
462
Adding a biogeographical perspective to the study of the diversity of microorganism
463
communities will certainly improve current knowledge of their ecology and evolution,
464
their responses to anthropogenic environmental changes, and the effect of these
465
responses on the ecosystem services they provide. However, the field of biogeography
466
itself stands to gain at least as much from this association. One of the main limitations
467
of biogeographical research compared to other fields of biology is that large temporal
468
and spatial scales are not conducive to field experiments, and when manageable long-
469
term experiments are designed, they are often flawed by the limited number (or lack) of
470
independent replicates, thus compromising the generality of the final results. This tends
471
to limit biogeography to conceptual experiments, the analysis of the predictions of null
472
and neutral models, or extrapolating the patterns observed in a few natural experiments
473
such as island groups.
474
In contrast, the study of microbes may allow to measure the equivalent to large-
475
scale biogeographical effects within relatively small extents (see above). Generation
476
times are also typically shorter than for large-sized organisms, permitting the study of
477
the assembly and development of a community within limited time spans. In addition,
478
they can be (and are) used for closed or semi-open experiments (i.e. performed in
479
controlled lab conditions or natural field conditions, respectively), thus allowing to
480
work with multiple replicates. Further, their minute size and the analytical tools
481
currently available make it possible to measure virtually all components of an
482
ecosystem, from the inputs of energy and materials, to the species present in the
483
assemblage, the functioning of the ecosystem itself, and its output in terms of biomass
484
or ecosystem services.
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Hortal, J. (2011) In Biogeography of micro-organisms. Is everything small everywhere? (ed. by D.Fontaneto) in press
485
Here I advocate the use of microscopic organisms for the development of a
486
purely experimental biogeography of the diversity of biological communities. I do it in
487
parallel with Jenkins and colleagues (Chapter 15), who propose a similar approach to
488
the study of the geographical responses and environmental requirements of single
489
species (or similar taxa). This will permit assessing the generality of many aspects of
490
current biogeographical and macroecological theory, from the relationship between
491
diversity and productivity/energy, to community composition or metacommunity
492
dynamics. A careful choice of study system is important in the design of successful field
493
experiments, which may eventually permit the exhaustive description of variations of
494
microorganism diversity in space. The perfect candidates for such small-scale
495
biogeography are a number of types of microhabitats, such as moss cushions, tank
496
bromeliads, treeholes or temporary ponds, among others, that often appear scattered
497
across apparently homogeneous territories or land patches (e.g. Gonzalez, 2000). By
498
assuming no dispersal limitations within a sensible area and amount of time (which are
499
taxon dependent), any field experiment could assume that this aspect has been
500
controlled for, and therefore that no effect of dispersal would remain in the results. The
501
scale of the localities (i.e. microhabitats) to study can allow manipulating dispersal
502
itself, by restricting the arrival of propagules or inoculating the selected ones.
503
Implementing microbial experiments for biogeographical research might need
504
some contention and preparation. Depending on the system studied, it would be
505
necessary to determine how transferable would be the results to the macroecological
506
world. And also, some preparatory work may be needed to find a proper way of taking
507
samples and measure functioning without having spurious effects on the studied
508
assemblages. Nevertheless, many groups of unicellular organisms, and in particular
509
bacteria, may not be appropriate for this kind of research, if the goal is to allow
510
extrapolating the results obtained to macrobes. Their different evolutionary modes can
511
result in substantially different patterns of diversity than those of any large-sized
512
organism (e.g, bacteria can rapidly interchange significant amounts of genetic material,
513
impeding any direct comparison with multicellular organisms). However, as discussed
514
above, many multicellular microorganisms can be directly comparable to large-sized
515
organisms in these respects.
516
Many areas of research in biogeography may benefit from micro-
517
biogeographical experiments with multicellular microbes. In particular, designing
518
experiments on island biogeography would be straightforward, providing powerful tools
16
Hortal, J. (2011) In Biogeography of micro-organisms. Is everything small everywhere? (ed. by D.Fontaneto) in press
519
for the research in many of the current debates and questions in this area. Good
520
examples of currently debated questions that would benefit from these experiments are:
521
How predictive are Hubbell’s (2001) Neutral Theory or current models of
522
metacommunity dynamics (e.g. Mouquet & Loureau, 2003)? Which are the influences
523
of dispersal and connectivity on species assembly (and assemblage composition)? What
524
is the exact relationship between habitat diversity and species richness, and to what
525
extent does this depend on area, versus the niche width of the species available in the
526
species pool (Hortal et al., 2009)? How well does the recently proposed general
527
dynamic theory of oceanic island biogeography (Whittaker et al., 2008) predict the
528
patterns of diversity and regional endemism in microhabitat islands? How can
529
speciation occur in the absence of proper allopatric populations (i.e. speciation in
530
sympatry; e.g. Phillimore et al., 2008)?
531
The current theory on the causes and consequences of geographical biodiversity
532
gradients can also be largely improved by studying the variations in the diversity of
533
microbes across relatively small territories. In spite of the level of knowledge on the
534
latitudinal diversity gradient reached to date, its causes are still under debate. The role
535
and relative importance of several processes in shaping species richness gradients is still
536
unknown (i.e. water-energy dynamics, energy and/or resource availability, regional
537
constraints and other historical effects and temporal changes, among others; Hawkins et
538
al., 2003a,b, 2007; Willig et al., 2003; Currie et al., 2004; Wiens & Donoghue, 2004;
539
Storch et al., 2006; Ricklefs, 2007; Mittelbach et al., 2007; Hawkins, 2008; Hortal et
540
al., 2008; Qian & Ricklefs, 2008). Further, the study of microbial communities may
541
help understanding the geographical variations in functional diversity, including
542
gradients in functional traits (e.g. Diniz-Filho et al., 2009), functional structure (e.g.
543
Rodríguez et al., 2006), or the effects of these spatial variations on ecosystem
544
functioning and resilience.
545
546
17.5 Conclusion
547
548
The biogeography of microbial communities is in large part not qualitatively different
549
from the biogeography of macroorganisms. Under current level of knowledge, most
550
differences between the macro- and micro-assemblages are due to the large dispersal
551
potential and the affinity of microbes to microhabitats. This results in a different scaling
552
of the distance decay in community similarity and a higher patchiness of microbe
17
Hortal, J. (2011) In Biogeography of micro-organisms. Is everything small everywhere? (ed. by D.Fontaneto) in press
553
communities. However, the current lack of knowledge on the geographical variations of
554
microorganisms is yet a challenge for both microbiologists and biogeographers. In my
555
opinion, further research on microbial biogeography will not find the processes
556
underlying the assembly of microbe communities to be fundamentally different from the
557
ones already described for macrobes. Rather, the similarity between macrobial and
558
microbial communities allows examining biogeographical theory with a completely
559
different perspective using microbes. Thus, here I argue for the development of an
560
experimental research program in microbial biogeography. Regardless of which
561
particular question is studied, I am certain that the biogeography of small things and the
562
experimental approach it permits will generate significant advances in biogeographical
563
theory.
564
565
Acknowledgements
566
567
I wish to thank Diego Fontaneto for the invitation to write this chapter and participate in
568
the corresponding symposium, and to an anonymous referee for a thoughtful review of
569
the previous version of this manuscript. I am also indebted to Noemí Guil, Sara Sánchez
570
Moreno and Diego Fontaneto, for introducing me to the world of the very very small
571
things, as well as for many insightful discussions throughout the last ten years. JH is
572
funded by a Spanish CSIC JAE-Doc research grant, and obtained additional funding
573
from a travel grant of the Azorean Biodiversity Group – CITA-A.
574
575
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