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Biological Soil Crusts (Biocrusts) As a Model System in Community, Landscape and Ecosystem Ecology

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Biological Soil Crusts (Biocrusts) As a Model System in Community, Landscape and Ecosystem Ecology Biodivers Conserv (2014) 23:1619–1637 DOI 10.1007/s10531-014-0658-x ORIGINAL PAPER Biological soil crusts (biocrusts) as a model system in community, landscape and ecosystem ecology Matthew A. Bowker • Fernando T. Maestre • David Eldridge • Jayne Belnap • Andrea Castillo-Monroy • Cristina Escolar • Santiago Soliveres Received: 1 November 2013 / Revised: 14 February 2014 / Accepted: 25 February 2014 / Published online: 9 March 2014 Ó Springer Science+Business Media Dordrecht 2014 Abstract Model systems have had a profound influence on the development of eco- logical theory and general principles. Compared to alternatives, the most effective models share some combination of the following characteristics: simpler, smaller, faster, general, idiosyncratic or manipulable. We argue that biological soil crusts (biocrusts) have unique combinations of these features that should be more widely exploited in community, landscape and ecosystem ecology. In community ecology, biocrusts are elucidating the importance of biodiversity and spatial pattern for maintaining ecosystem multifunctionality due to their manipulability in experiments. Due to idiosyncrasies in their modes of facil- itation and competition, biocrusts have led to new models on the interplay between environmental stress and biotic interactions and on the maintenance of biodiversity by competitive processes. Biocrusts are perhaps one of the best examples of micro-land- scapes—real landscapes that are small in size. Although they exhibit varying patch Communicated by Guest Editors of S. I.: Biocrust. M. A. Bowker (&) School of Forestry, Northern Arizona University, 200 E. Pine Knoll Drive, Flagstaff, AZ 86011, USA e-mail: [email protected] F. T. Maestre Á C. Escolar Á S. Soliveres A´ rea de Biodiversidad y Conservacio´n, Departamento de Biologı´a y Geologı´a, Universidad Rey Juan Carlos, c/Tulipa´n s/n., 28933 Mo´stoles, Spain D. Eldridge Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia J. Belnap Canyonlands Research Station, Southwest Biological Science Center, US Geological Survey, 2290 SW. Resource Blvd., Moab, UT 84532, USA A. Castillo-Monroy Departamento de Ciencias Naturales, Universidad Te´cnica Particular de Loja, San Cayetano Alto, Marcelino Champagnat, Loja, Ecuador 123 1620 Biodivers Conserv (2014) 23:1619–1637 heterogeneity, aggregation, connectivity and fragmentation, like macro-landscapes, they are also compatible with well-replicated experiments (unlike macro-landscapes). In eco- system ecology, a number of studies are imposing small-scale, low cost manipulations of global change or state factors in biocrust micro-landscapes. The versatility of biocrusts to inform such disparate lines of inquiry suggests that they are an especially useful model system that can enable researchers to see ecological principles more clearly and quickly. Keywords Biodiversity Á Biological soil crusts Á Ecosystem function Á Global change Á Landscape heterogeneity Á Micro-landscape Á Model system Á Species interactions Overview: historical importance of model systems in ecology A brief glance at any ecology textbook will offer many examples of model systems being used to test and elucidate general principles. For example, the variation in beak size and shape in Galapagos finches was crucial to the development of Darwin’s theory of natural selection (Weiner 1994). If Hutchinson (1959) had not observed three different species of water boatmen swimming in a fountain in a cave shrine, we may have waited much longer for the current concept of the realized ecological niche to emerge. Tilman’s concept of resource competition and the definition of a best competitor for a given resource may grace every plant ecology textbook, but was initially developed and refined using easily dis- tinguished freshwater diatoms (Tilman 1977). A final example is oceanic archipelagos, such as Hawaii, which were formed via volcanism and are composed of similar parent material of different ages. Peter Vitousek used Hawaii as a model to study how biogeo- chemistry changes as ecosystems age (Vitousek 2006). These examples demonstrate how model systems have been instrumental in the development of theory in biosciences in general and in ecology in particular. What makes a good model system? Vitousek (2002) states that model systems in ecology may be a gene, a species, a com- munity, or an ecosystem that ‘‘displays a general process or property, in an understandable way’’. Compared to alternative study systems, a model system ought to exhibit one or more of the following characteristics, the first five being derived from Vitousek (2002). Systems with several of these properties allow us to learn about nature in a maximally efficient way. (1) It might be simpler, so that the property of interest is not obscured by other prop- erties or processes. Soil nematode communities in the Antarctic dry valleys consist of only four species, thus they serve as a simple model to study intra-trophic species interactions among other processes (Hogg et al. 2006). We note that systems may sometimes be too simple which could limit generality (number 5, below). (2) It might display more rapidly the process of general interest. Due to fast generation time, compelling arguments have been made for the use of microbial model systems in ecology (Jessup et al. 2004). As an example, McGrady-Steed et al. (1997) observed that microbial communities constructed with more species were more resistant to invasion by a new species. (3) It might be smaller. Herbaceous plants are easier to observe and measure than, for example, trees. Therefore when addressing general processes and properties relevant to all 123 Biodivers Conserv (2014) 23:1619–1637 1621 plants, the herbaceous plant would be the preferred model except in situations where the height and mass of the tree make it instructive (see below). Much of the seminal work on the relationship between plant biodiversity and production used herbaceous plants grown in combinations in small plots (e.g. Tilman and Downing 1994). (4) It might be idiosyncratic or distinctive in a useful way that makes it instructive. For example, the coastal redwood is the tallest tree in the world, making it an excellent model to examine how hydraulic processes limit plant height (Koch et al. 2004). (5) It should (usually) be generalizable. Vitousek (2002) considers ecological model systems to often be real and persistent examples of a larger set of systems. We tend to agree that to improve inference about other systems, a model should ideally (at least in most cases) have the property of generality. An important exception is when a model’s idiosyncrasies or distinctions are what make it useful for study. (6) It might be more amenable to experimentation. Perhaps because of his focus on large spatial scale and long temporal scale and taking advantage of ‘‘natural experiments’’, Vitousek (2002) did not elaborate on characteristics that would make a model system easier for experimentation. Being simpler, faster, or smaller are all characteristics that might simplify or improve observations made in experiments, but in addition, a good model can be manipulated. The manipulation may come in the form of an altered resource, an added or removed species, imposed climate variation, etc. Vitousek (2002) also was careful to distinguish true model ecosystems from two other types of study systems: the well-studied system and the artificial microcosm. All of these types can overlap, but have distinct characteristics. A well-studied system offers a wealth of information already gathered, saves the researcher the burden of learning basic properties of the system, and attracts new research to build on the old. However, unless some of the above six model system properties are displayed by the system, it does not necessarily allow us to learn about nature in a maximally efficient manner, and is therefore not always a model system. Construction of microcosms, with some properties of natural systems but omitting or holding others constant, is a useful means of reductionism and isolation of a process. These too can be model systems in our view, but the danger of these systems lies in simplifying them to the extent that the process of interest does not operate in the same manner as it would in a complex natural system, making results difficult to generalize. We have collectively conducted several studies that can be considered to have exploited the model system characteristics of biocrusts to learn about ecological properties, principles, and processes. The purpose of this review is threefold: (1) To assert that biocrusts have many characteristics that fit the above Vitousekian concept of an ecological model system, and describe these key characteristics; (2) To review examples from our work, and that of others, which we believe highlights the utility of biocrusts for the study of ecological properties, principles and processes; and (3) To promote and encourage the use of this study system to further the study of ecology. All of these goals seek to inspire new ideas and new lines of research in both the biocrust and general ecological research communities. Biocrusts as model systems Model characteristics of biocrusts Simple biocrusts? The entire biocrust community, including primary producers, and multiple levels of con- sumers in the dependent food web, generally consists of hundreds of species (Bowker et al. 123 1622 Biodivers Conserv (2014) 23:1619–1637 2010a, b). Thus, considering this a simple community is misleading. However within trophic levels, and within taxonomic groups within trophic levels, levels of diversity may be more tractable than in many communities. For example, in a given study area, biocrusts might have the potential to support around up to perhaps 40, but usually fewer bryophyte and lichen species. The true diversity of the cyanobacteria is currently being resolved; at this time, North American biocrusts support less than 20 generic or sub-generic taxa (Garcia-Pichel et al. 2013). This level of richness is comparable to, or less than, that of vascular plant communities in similar dryland environments.
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