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Oecologia. 2012 March; 168(3): 621–629.
Published online 2011 October 5. doi:  10.1007/s00442-011-2138-2
PMCID: PMC3277708
Copyright © The Author(s) 2011
Microbiology of the phyllosphere: a playground for testing ecological concepts
Katrin M. Meyerspacer 1,2 and Johan H. J. Leveau1,3
1Department of Microbial Ecology, Netherlands Institute of Ecology (NIOO-KNAW), Droevendaalsesteeg 10, 6708 PB Wageningen, The Netherlands
2Faculty of Forest Sciences and Forest Ecology, Ecosystem Modelling, University of Göttingen, Büsgenweg 4, 37077 Göttingen, Germany
3Department of Plant Pathology, University of California, One Shields Avenue, 476 Hutchison Hall, Davis, CA 95616 USA
Katrin M. Meyer, Phone: +49-0-551393795, Fax: +49-0-551-393465, Email: kmeyer5/at/uni-goettingen.de.
spacer Corresponding author.
Communicated by Roland Brandl.
Received March 29, 2011; Accepted August 27, 2011.
  •  Other Sections▼
    • Abstract
    • Introduction
    • Ecological concepts addressed in the phyllosphere
    • Points of departure for future investigations of ecological concepts in the phyllosphere
    • Concluding remarks
    • Electronic supplementary material
    • References
Abstract
Many concepts and theories in ecology are highly debated, because it is often difficult to design decisive tests with sufficient replicates. Examples include biodiversity theories, succession concepts, invasion theories, coexistence theories, and concepts of life history strategies. Microbiological tests of ecological concepts are rapidly accumulating, but have yet to tap into their full potential to complement traditional macroecological theories. Taking the example of microbial communities on leaf surfaces (i.e. the phyllosphere), we show that most explorations of ecological concepts in this field of microbiology focus on autecology and population ecology, while community ecology remains understudied. Notable exceptions are first tests of the island biogeography theory and of biodiversity theories. Here, the phyllosphere provides the unique opportunity to set up replicated experiments, potentially moving fields such as biogeography, macroecology, and landscape ecology beyond theoretical and observational evidence. Future approaches should take advantage of the great range of spatial scales offered by the leaf surface by iteratively linking laboratory experiments with spatial simulation models.
Electronic supplementary material
The online version of this article (doi:10.1007/s00442-011-2138-2) contains supplementary material, which is available to authorized users.
Keywords: Ecological theories, Diversity, Biogeography, Niche, Leaf surface
  •  Other Sections▼
    • Abstract
    • Introduction
    • Ecological concepts addressed in the phyllosphere
    • Points of departure for future investigations of ecological concepts in the phyllosphere
    • Concluding remarks
    • Electronic supplementary material
    • References
Introduction
Ecological concepts, theories, and models have traditionally been investigated from a perspective centered on macroorganisms. However, many tests of ecological theories using macroorganisms have not been decisive because it is difficult to find sufficient true replicates and to implement the necessary experiments. Recently, more and more studies have appeared in the literature that use microorganisms to test ecological concepts (Konopka 2006). They cover a wide range of microbiomes, among them the plant leaf surface, also referred to as the phyllosphere (Ruinen 1961). The phyllosphere supports numerous microorganisms, including bacteria, fungi, yeast, and protozoa (reviewed in Andrews and Harris 2000; Beattie and Lindow 1995; Hirano and Upper 2000; Kinkel 1997; Leveau 2006; Lindow and Leveau 2002; Lindow and Brandl 2003; Whipps et al. 2008). Bacteria are the most abundant members of the phyllosphere community, and have been shown to colonize leaves at densities of up to 108 cells cm−2 (Leveau 2006). The description of microbial community structure and the quantification of microbial diversity associated with leaf surfaces has been much improved by the application of culture-independent methods. These have provided many new insights into the microbial species that are common and unique to all plant leaf surfaces, the specific adaptations that bacteria and fungi possess and express to meet the chemical and physical challenges of the phyllosphere environment, and the factors that determine community composition, such as the plant species and weather conditions.
There are several reasons for considering the phyllosphere as a model system for testing ecological concepts and theories. One is its great environmental heterogeneity. For example, the availability of nutrients to microorganisms on leaves is highly variable in space and time (Leveau and Lindow 2001; Monier and Lindow 2003), thus providing ideal grounds for investigating environmental variation as a major property of ecological interactions. This spatiotemporal variability covers a great range of scales (Fig. 1), from micrometer leaf sections to individual leaves on a plant, and from leaves on different plant individuals or species up to whole plant communities. This notion aligns well with the growing awareness of the importance of scales for ecological patterns and processes (Levin 1992; Meyer et al. 2010). Testing ecological concepts in the phyllosphere can thus make a major contribution to landscape ecology (Andrews and Harris 2000). Phyllosphere microbiology also has the potential to test highly controversial ecological theories such as theories of biodiversity (e.g. Hubbell 2003; Ricklefs 2003). Moreover, the phyllosphere is highly accessible to experimental manipulation, facilitating experiments with sufficient replication and therefore statistical tests with considerable power. Visualization techniques such as confocal and epifluorescence microscopy and tools based on fluorescent protein markers improve the experimental options even further. The use of green fluorescent protein (GFP) has truly revolutionized our ability to monitor the whereabouts, behaviours and interactions of individual bacterial cells colonizing the leaf surface (Leveau and Lindow 2001; Remus-Emsermann and Leveau 2010). These and other molecular tools make microbal communities of the phyllosphere more tractable for experimental tests of concepts ranging from landscape ecology and macroecology to biogeography. Contrary to traditional macroecological approaches, the manipulation of island size or shape is relatively easy in the phyllosphere. Finally, the considerable commercial interest in the prevention of foliar diseases in agriculturally important crops and the growing concern over unwanted human pathogens on leafy greens adds extra weight to the need for ecological studies in the phyllosphere (Whipps et al. 2008).
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Fig. 1
Scales in the phyllosphere. Patterns such as clumped spatial distributions of bacterial populations or communities arise from ecological processes that occur at the individual level. Scale-explicit ecological concepts such as patch dynamics or species-area (more ...)
The aims of this review are to (1) compile and evaluate the conclusions that have been drawn in studies addressing ecological concepts in the phyllosphere to date, (2) identify gaps in these studies that would benefit from increased research efforts, and (3) pinpoint essential characteristics of future approaches to testing ecological concepts in the phyllosphere for the benefit of micro- and macroecology.
  •  Other Sections▼
    • Abstract
    • Introduction
    • Ecological concepts addressed in the phyllosphere
    • Points of departure for future investigations of ecological concepts in the phyllosphere
    • Concluding remarks
    • Electronic supplementary material
    • References
Ecological concepts addressed in the phyllosphere
Thus far, the focus of phyllosphere microbiologists has been predominantly on concepts from autecology and population ecology, such as fitness, habitat, niche, population dynamics, and competition, as listed in detail in Electronic supplementary material (ESM) 1 and 2. For instance, bacterial profiles of nutrient source utilization in vitro have been used to estimate niche overlap and to quantify the degree of ecological similarity or niche differentiation of bacterial species (Wilson and Lindow 1994). Among the autecological concepts, the application of life-history strategies to phyllosphere organisms is noteworthy. Originally designed for the classification of plants, concepts such as Grime’s (2001) C-S-R triangle theory on the trade-offs between competitiveness (C), stress tolerance (S), and a combination of high reproduction and low longevity (R, for ruderality) were applied to phyllosphere fungi (Nix-Stohr et al. 2008), for which generally an S strategy is assumed, which involves maximizing stress tolerance. Contrary to this expectation, however, these fungi were found to maximize the occupation and exploration of resources, thus implying R and C strategies instead (Nix-Stohr et al. 2008).
In phyllosphere population ecology, population dynamics and competition are the predominating concepts (ESM 2). Studies on population dynamics are plentiful, but very few identify spatiotemporal patterns or go beyond reporting static population densities. In one of the few studies that do (Ellis et al. 1999), populations of fluorescent pseudomonads were sampled from sugar beet leaves to reveal a dynamic, nonrandom and continuous turnover of ribotypes within that population. Such cyclic population dynamics and their underlying mechanisms are a highly debated topic in ecology (Turchin and Hanski 2001), which future phyllosphere studies may help to elucidate.
A recurring pattern in phyllosphere population dynamics that might benefit from further investigation is the great temporal variability in population sizes (Dreux et al. 2007; Nix et al. 2008). Only recently have techniques been developed that allow the quantification of the fate and reproductive success of individual bacteria on leaf surfaces. For example, Remus-Emsermann and Leveau (2010) showed that individual immigrants to leaf surfaces contribute unequally to population sizes.
Competition has not only been inferred from nutrient overlap indices (Wilson and Lindow 1994), but also from pre-emptive exclusion of competitors by primary colonizers of the leaf surface (Lindow and Leveau 2002; Lindow and Brandl 2003), which can be an important mechanism underlying the success of biocontrol against plant pathogens (Mohamed and Caunter 1995). This is particularly true when the pathogen is an r-strategist with a fast reproduction and low competitiveness (Marois and Coleman 1995), or wh
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