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Book Review |
Department of Biology, University of Pennsylvania, Philadelphia, Pennsylvania 19104-6018 USA
On a global scale, ecologists have long recognized the importance of feedback between aboveground and belowground ecological systems. In our general ecology classes, we teach that major world biomes are characterized by distinctive vegetation types, which are influenced both by climate and soil types. Soils, in turn, are a product of the mineral composition of the bedrock, the particular soil weathering action caused by that climate, and the physical and chemical characteristics of the organic matter returned to the soil by the vegetation. Soils and vegetation, students learn, are inextricably connected with each defining the identity of the other.
In Communities and Ecosystems, Linking the Aboveground and Belowground Components, David Wardle examines how aboveground biological communities and ecosystems are linked to those in the soil at spatial scales smaller than a biome. He articulates his primary goal as considering terrestrial communities and ecosystems from a combined aboveground–belowground perspective in order to identify feedback between the two systems and to interpret how such feedback influences ecosystem functions such as carbon and nitrogen cycling. Wardle convincingly argues that understanding the linkages is important for predicting how changes in the components, including those caused by anthropogenic activity, affect ecosystem functions.
Most linkages between aboveground and belowground ecological systems directly or indirectly involve plants, and thus a consideration of how plants interact with other organisms serves as a major, but unstated, theme of this book. Plants earn this level of attention because input of plant litter is the primary resource for decomposer food chains in the soil, and by the nature of a vascular plant's existence it extends simultaneously above- and belowground. If interactions with other organisms in either system affect plant performance, repercussions are likely to occur in the other system simply because the plant exists there as well.
Although plants serve as a logical focal point, Wardle's task is still an enormous one. The goals he sets out for himself require that he consider nearly all terrestrial organisms—starting with the invertebrate and microbial components of decomposer soil food webs and including a consideration of the intraspecific and interspecific variation in plant traits that influence interactions with herbivores and the decomposers. By his inclusive definition of aboveground–belowground linkages, he must also consider the actions of all organisms that feed on or parasitize plants or interact with them in a beneficial fashion either above- or belowground. Even animals that feed at higher trophic levels cannot be ignored as their excretory wastes and decaying carcasses are sources of nutrient input into the soil. Most of us work with only one or a few components of these systems; we may not think about each system in its entirety, let alone all the connections between the systems.
Wardle emphasizes the degree that ecologists working in aboveground and belowground systems are isolated from each other:
... there have been few attempts to bring together the widely dispersed literature on aboveground and belowground communities or to interpret this in an ecosystem context. This is because aboveground and belowground ecology have traditionally developed largely independently of one another; the two subdisciplines usually publish in different journals or bodies of literature. In this light it is perhaps not surprising that often a finding that has been hailed as a breakthrough in one subdiscipline has long been common knowledge to the other.
The breadth of information Wardle covers in connecting these subdisciplines is, in fact, impressive. As a plant ecologist with little prior knowledge of soil fauna, I learned a great deal, for example, about the diversity and interactions of soil invertebrates. Wardle presents this literature by addressing the question of whether decomposer food webs are regulated by "top-down" predators or "bottom-up" resource availability. Understanding the nature of the controls is important to interpreting how these systems respond to changes in the quantity and quality of plant litter. This example serves as a nice illustration of why we must understand how a system operates before we can understand how a linkage to another system affects it.
Still, no one person can be an expert on the diverse subjects addressed here, and I think that a collaborative effort among aboveground and belowground ecologists would have been a more productive approach. A collaborative effort among experts in the disparate fields—perhaps beginning with a workshop—could have increased the level of information synthesis and served as a forum stimulating conversation between soil scientists and aboveground ecologists who, according to Wardle, have traditionally not talked to one another. Wardle himself has published extensively and broadly in the area of aboveground–belowground interactions and thus is as qualified as any single individual to write a book of this scope. Nevertheless, the quality of the synthesis and the readability of the material varies greatly, seemingly dependent on his familiarity with the literature.
Wardle devotes considerable attention to the questions of whether increased plant species diversity begets either increased net primary productivity or increased community or ecosystem stability. He has contributed previously to the literature debates these questions have generated, and he justifies their inclusion here because primary productivity ultimately determines the quantity of litter available to soil biota and because the diversity of plants and the diversity of soil organisms are potentially related. Central to both questions is whether an increase in the number of plant species generally represents either an increase in the number of plant functional types, with species exhibiting low overlap in niche space and greater resource partitioning, or an increase in positive interactions among species. Such phenomena are necessary to link productivity or stability to species diversity directly (Tilman et al., 1996
, 1997
). An alternative explanation, especially for studies that vary diversity experimentally by drawing different numbers of species at random from the same species pool, is based on purely statistical grounds. More diverse systems can be more productive or more stable simply because an increase in the number of species increases the probability that key productive (or resilient) species are included in a particular experimental plot (Aarssen, 1997
; Huston, 1997
). Wardle's strong preference for the latter explanation is apparent in his analysis of the literature.
Wardle does not give other potentially controversial topics as much attention. For example, he mentions the possibility that plants share carbon through mycorrhizal hyphae and cites but does not discuss studies pointing out the difficulties in demonstrating its functional importance (Fitter et al., 1998
; Newbery et al., 2000
). Still, he says, if fungal hyphae reduce competition then "fungal-regulated positive interactions might not be uncommon in plant communities." An examination of evidence that could shed light on whether hyphal connections among plants are common and biologically important to the plants (or the fungi) would have been welcome. Could we draw relevant information from the plant competition literature? Are the combined effects of competition between roots and any facilitation that might occur through fungal hyphal connections likely to result in net positive belowground interactions between neighboring plants? Just how common IS facilitation through belowground interactions, even if the mechanism cannot be identified?
The reduced level of synthesis applied to some subjects also made for dry reading. Again, I expect this reflects the fact that Wardle is less familiar with these particular subjects and not that the information is inherently less interesting or controversial. For example, the chapter "Belowground Consequences of Aboveground Foodwebs" mostly summarizes how herbivory varies with particular leaf traits and how these same leaf traits affect the quality of leaf litter returned to the soil, with little interpretation of the information. He makes a secondary point related to the "not-so-novel" idea that dung and urine impact soil resources, explaining that the animals making these deposits may travel over considerable distances and into different habitats, potentially impacting communities beyond the one in which they fed.
While linkages between aboveground and belowground ecological systems are indeed numerous and some of them complex, many can be collapsed into the framework of what is often called plant–soil feedback in the current literature. In this context, ecologists are particularly interested in how plants affect the abundance and diversity of soil organisms with which they interact and how these organisms, in turn, affect the performance of different plant species. The relevant soil organisms include root herbivores and both free-living microbes and those forming associations with plants, such as nitrogen-fixing bacteria and mycorrhizal fungi. Wardle includes several examples.
Plant–soil feedback is either characterized as positive, whereby a particular plant species propagates an associated biota that improves the performance of that species relative to other plants, or negative, whereby the associated biota reduce plant performance. Beneficial effects of microbes include increased levels of nutrient mineralization, nitrogen fixation, suppression of pathogens, and production of substances promoting plant growth. Negative feedback can be expressed through the action of host-specific pathogens or mechanisms by which plants and microbes compete for nutrients. Negative feedback may even involve mutualists, such as mycorrhizal fungi, if they differ in their level of host specificity or confer different levels of benefit to different hosts (Bever et al., 2002
). Such phenomena have clear implications for the maintenance of species diversity in both the soil and plant communities. Wardle mentions "a vast agronomic and biotechnological literature" about how several types of interactions with microbes affect the growth of crop plants, but he limits his discussion to ecological studies that have dealt with nutrient transformations, pathogens, and mycorrhizae and refers the reader to several reviews of the agricultural literature. I think it likely that many findings of agricultural studies could be applicable to ecological systems, and including some discussion of them here might have suggested new lines of research to ecologists.
In the introduction, Wardle discusses why studies of the soil biota are so challenging, making soil communities still a largely unexplored frontier: (1) The physical and chemical structure of the soil is complex, and it is difficult to study even macroorganisms in situ within such a complex, opaque matrix. (This explains, for example, why we know many times more about the activity and consequences of aboveground herbivores than about those operating strictly belowground.) (2) Soil communities generally contain far more species than aboveground communities occupying comparable space, perhaps because the microhabitats are more diverse and complex. (3) Countless species of soil organisms remain unidentified. It is estimated that less than 0.1% of soil microbial species and 10% of the soil microarthopods (André et al., 2002
) have been described.
Considering Wardle's broad statements about our limited knowledge of the underground biological world, I find it surprising that he omits coverage of recent technological advances that seem to be revolutionizing the ecological study of soil microbes, moving the field beyond traditional culturing techniques that have failed to capture so many species. One approach characterizes microbial communities based on phylogenetically relevant variation in important biological molecules such as nucleic acids or phospholipid fatty acids (Hill et al., 2000
). Microbial genes can be extracted directly from the soil and their sequences compared with those of known organisms, and fluorescently labeled taxon-specific oligoncleotide probes can be used to identify taxonomic groups within their natural microenvironments. Analyses of cell wall fatty acids are informative because unique fatty acids serve as signature molecules in specific groups of microorganisms. Additionally, because cell walls rapidly degrade upon cell death, phospholipids prove useful as a measure of active microbial biomass.
Still another approach examines microbial diversity through the physiological capabilities of community constituents (Hill et al., 2000
; Waldrop et al., 2000
). These profiles are often based on the activity of specific enzymes involved in the degradation of particular macromolecular carbon compounds, such as lignin or cellulose, or the microbes' ability to utilize a diversity of carbon-based substrates. Stable isotopes can be used as tracers to identify the role of microbes in carbon and nutrient cycling and to determine whether they compete with plants for the same pool of nutrient resources. These techniques allow researchers to examine the ecosystem functions of different microbial communities without determining their species compositions. While all of these methods have their limitations, their refinement should continue to speed progress in the exploration of the soil frontier, supplement information gained about ecosystem function from traditional experiments manipulating litter characteristics or soil inoculum (André et al., 2001
), and improve our understanding of how feedback occurs between aboveground and belowground systems.
Indeed, as Wardle points out, the more we learn about soil microbial communities, the more complicated their relationships with plants appear. Arbuscular mycorrhizal fungi were once thought to be nonspecific in their choice of hosts, but now it is clear that the performance and thus the level of benefit experienced by both the plant and the fungus often depends on the identity of the partner species. The performance of a host plant may vary with the number of fungal species associated with its roots (van der Heijden et al., 1998a
), and plant community diversity may be related to mycorrhizal fungal diversity (van der Heijden et al., 1998b
). Recent evidence shows how plant–soil feedback can occur at microscales, as plant roots can influence the rate of nitrogen mineralization performed by bacteria in the rhizosphere (Firestone et al., 2002
). The fact that plant performance and the outcome of plant competition can be greatly affected by the activity of soil microbes calls into question the ecological relevance of countless greenhouse experiments conducted over the last several decades without soil biota. These are studies where plants were grown in sterilized "soil-less" potting media, typically consisting of a mixture of ground peatmoss, vermiculite, or other inert ingredients to which inorganic nutrients were added.
Wardle's last substantive chapter tackles the broad topic of how human activities are impacting ecological systems through effects on linked aboveground–belowground components. Initially, I was surprised to find so much of the book, roughly a sixth, devoted to conservation issues, but this chapter turned out to be a lucid and comprehensive explanation of how even small changes in climate or species composition can have far-reaching ecological repercussions. Within the context of aboveground–belowground linkages, it is easy to appreciate how anthropogenic perturbations can potentially alter basic ecosystem functions of carbon and nutrient cycling and feed back to affect species composition at different trophic levels. This chapter would serve as a solid synthetic review of the subject for a class reading assignment.
Most of the major conservation issues are included: the introduction of exotic species, the selective removal of key ecologically important native species, large-scale and long-term changes in land use, increased nitrogen deposition, CO2 enrichment, and global climate changes caused by changes in the composition of atmospheric gases. Wardle explains very well how the introduction of invasive species can alter species interactions and interrupt normal ecosystem function, but his coverage of species extinctions or deliberate, selective removal of particular species by humans is less informative. He dwells too much on the occurrence of historical large-scale extinctions of megafauna, such as happened in North America 10 000–12 000 years ago, without much evidence for how such losses affected the ecosystem. He speculates that "these extinctions have almost certainly profoundly affected the functional composition of the vegetation" based on what has been learned from studies of contemporary systems, and he refers the reader to an earlier chapter.
Better data are apparently available on the ecological consequences of species additions. Wardle not only includes examples of exotic plants and aboveground herbivores but also exotic soil organisms. Earthworms have been well studied. Important consequences of non-native earthworms include changes to the physical soil structure, the overall composition of the soil biota, the accumulation of organic matter, and nutrient supply rates. Invasive plants can alter many of these same soil factors indirectly by causing changes in the quantity or quality of plant litter, with resultant changes in the cycling of carbon and nutrients and in the species composition of the decomposers. One active area of research with invasive plants focuses on how plant–soil feedback figures in their success, i.e., to what extent changes induced belowground by the invaders hinder the reestablishment of native vegetation (Klironomos, 2002
).
Wardle also presents a seemingly comprehensive description of how nitrogen and CO2 enrichment are likely to affect ecosystems, primarily through their fertilization effects on plants. By increasing primary productivity they can increase the quantity of litter available to decomposers, but they can also alter the chemical constituents of leaves in ways that alter the rate of decomposition and shift the constituents of decomposer food webs. Direct effects of nitrogen deposition on soil microbes can also occur but are less predictable. Climate changes as a consequence of elevated CO2 levels are expected to involve a 3°C increase in air temperatures, more temporal variability in precipitation, and more extreme weather events in general. He reviews how these changes may affect primary productivity, the composition of the vegetation, and the geographic ranges of plant species. Understandably, the soil biota is much more likely to respond directly to changes in moisture availability than to temperature increases of the expected magnitude, although large increases are predicted in the rate of decomposition and the loss of carbon through respiration of soil organisms. I would have liked more discussion of how climate-induced changes in the composition of the vegetation may mitigate or exacerbate soil carbon loss through increased soil respiration. He mentions some exchanges on these questions in the literature but does not elaborate.
Finally, I feel obligated to comment on the organizational style of the book. Although every chapter ends with a section entitled "Synthesis," these sections are largely chapter summaries, with the amount of synthetic analysis reflecting the amount contained in the chapter itself, which varies greatly. To the extent that these sections do provide a new synthesis of the material already covered, incorporating these ideas into the chapter would have made the factual material more interesting. The final chapter, entitled "Underlying Themes," likewise serves mainly as a summary and does little to tie the information together in new ways.
Wardle does do a commendable job summarizing the different ways that aboveground and belowground ecological processes are connected. However, given his uneven development of the diverse topics included in this book, I believe that aboveground and belowground ecologists would be better informed of and inspired by the others' research if they could speak for themselves. I am reminded of the story of how several blind men give completely different descriptions of an elephant based on the small portion of the animal each is able to touch. The same concept need not apply to the descriptions of ecosystems. The latter may be a case where the "elephant" could be better described and understood by the combined efforts of several individuals, each of whom is an expert on some component but who may be unfamiliar with the rest of the "animal."
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FOOTNOTES |
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LITERATURE CITED |
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 TOP LITERATURE CITED |
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André H. M. X. Ducarme J. M. Anderson D. A. Crossley Jr. H. H. Koehler M. G. Paoletti D. E. Walter P. Lebrun 2001 Skilled eyes are needed to go on studying the richness of the soil. Nature 409: 761.
André H. M. X. Ducarme P. Lebrun 2002 Soil biodiversity: myth, reality or conning?. Oikos 96: 3-24[CrossRef][ISI]
Bever J. D. A. Pringle P. A. Schultz 2002 Dynamics within the plant–arbuscular mycorrhizal fungal mutualism: testing the nature of community feedback. In M. G. A. van der Heijden and I. Sanders [eds.], Mycorrhizal ecology, 267–292. Springer-Verlag, Berlin, Germany
Firestone M. K. D. J. Herman K. DeAngelis 2002 Effects of soil microbial community composition on nutrient cycling dynamics in rhizosphere soil. Ecological Society of America Meeting Abstracts 87: 19
Fitter A. H. J. D. Graves N. K. Watkins D. Robinson C. Scrimgeour 1998 Carbon transfer between plants and its control in networks of arbuscular mycorrhizas. Functional Ecology 12: 406-412[CrossRef][ISI]
Hill G. T. N. A. Mitkowski L. Aldrich-Wolfe L. R. Emele D. D. Jurkonie A. Ficke S. Maldonado-Ramirez S. T. Lynch E. B. Nelson 2000 Methods for assessing the composition and diversity of soil microbial communities. Applied Soil Ecology 15: 25-36
Huston M. A. 1997 Hidden treasures in ecological experiments: reevaluating the ecosystem function of biodiversity. Oecologia 110: 449-460[CrossRef][ISI]
Klironomos J. 2002 Feedback with soil biota contributes to plant rarity and invasiveness in communities. Nature 417: 67-70[CrossRef][Medline]
Newbery D. M. I. J. Alexander J. A. Rother 2000 Does proximity to conspecific adults influence the establishment of ectomycorrhizal trees in rain forest?. New Phytologist 147: 401-409[CrossRef][ISI]
Tilman D. J. Knops D. Wedin P. Reich M. Ritchie E. Siemann 1997 The influence of functional diversity and composition on ecosystem processes. Science 277: 1300-1302
Tilman D. D. Wedin J. Knops 1996 Productivity and sustainability influenced by biodiversity in grassland ecosystems. Nature 379: 718-720[CrossRef][ISI]
van der Heijden M. G. A. J. N. Klironomos M. Ursic P. Moutoglis R. Streitwolf-Engel T. Boller A. Wiemken I. R. Sanders 1998a Different arbuscular mycorrhizal funal species are potential determinants of plant community structure. Ecology 79: 2082-2091[CrossRef][ISI]
van der Heijden M. G. A. J. N. Klironomos M. Ursic P. Moutoglis R. Streitwolf-Engel T. Boller A. Wiemken I. R. Sanders 1998b Mycorrhizal fungal diversity determines plant biodiversity, ecosystem variability and productivity. Nature 396: 69-72[CrossRef]
Waldrop M. P. T. C. Balsar M. K. Firestone 2000 Linking microbial community composition to function in a tropical soil. Soil Biology and Biochemistry 32: 1837-1846[CrossRef]
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