Plant physiological ecology: An essential link for integrating across disciplines and scales in plant ecology

Plant physiological ecology: An essential link for integrating across disciplines and scales in plant ecology

ARTICLE IN PRESS Flora 202 (2007) 608–623 www.elsevier.de/flora Plant physiological ecology: An essential link for integrating across disciplines and...

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ARTICLE IN PRESS

Flora 202 (2007) 608–623 www.elsevier.de/flora

Plant physiological ecology: An essential link for integrating across disciplines and scales in plant ecology Wolfram Beyschlaga,, Ronald J. Ryelb a

Lehrstuhl fu¨r experimentelle O¨kologie und O¨kosystembiologie, Universita¨tsstraße 25, 33615 Bielefeld, Germany Department of Wildland Resources and the Ecology Center, Utah State University, Logan, UT 84322-5230, USA

b

Received 31 May 2007; accepted 31 May 2007 Dedicated to Prof. Dr. Dr. h.c. mult. Otto Ludwig Lange on the occasion of his 80th birthday

Abstract A sizeable number of scientists and funding organisations are of the opinion that the relevance of plant physiological ecology as an important discipline has declined to the point that it is no longer considered as one of the important topics of ecological research. Plant physiological ecology is typically associated with the autecological plant research conducted during the latter portion of the 20th century or, even worse, simply with gas exchange measurements. However, taking a closer look, it becomes obvious that, by focusing on the intermediate integration levels (individuals, populations), this discipline represents an essential link between the high integration levels (communities, ecosystems, biosphere) and the disciplines at the bottom of the complexity hierarchy (physiology, molecular biology). In this paper we show that the principal question of all ongoing community and ecosystem level research – What is the mechanistic background of vegetation composition, biodiversity structure and dynamics and how is this linked to fluxes of matter at the community and higher levels of organisation? – can only be answered if the mechanism of interactions between the relevant organisms are understood. In consequence, the classical discipline of plant physiological ecology will continuously develop into a truly interdisciplinary experimental ecology of interactions and its importance will rather increase than diminish. Promising activities of this kind are already underway. Scientists needed for this new direction should have a rather broad scientific perspective, including knowledge and experience in fields outside of typical ecological research, instead of being specialists for single ecophysiological aspects. r 2007 Elsevier GmbH. All rights reserved. Keywords: Plant physiological ecology; Bridging scales; Plant interactions; Experimental ecology

Introduction The role of natural science as a discipline has always been to help humanity understand nature. Regardless of Corresponding author.

E-mail addresses: [email protected] (W. Beyschlag), [email protected] (R.J. Ryel). 0367-2530/$ - see front matter r 2007 Elsevier GmbH. All rights reserved. doi:10.1016/j.flora.2007.05.001

the phenomenon being investigated, two steps are necessary to achieve understanding. First, a description is needed: what is the phenomenon, what are its characteristics, what are patterns of behaviour of the system? Generations of natural scientists have successfully proven that a rather complete view of nature can be derived from careful observations. At present, phenomena are often well described in many disciplines of

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natural sciences through collection and interpretation of observations. Nevertheless, as soon as a phenomenon has been thoroughly described, the question changes from what happened to why do the phenomenon happen? And most importantly, which mechanisms lay behind the observations? For humankind the ‘‘why’’ question can be essential for effective use of resources. Without appreciating the mechanisms behind important natural phenomena, we are often unable to capably predict the effects of anthropogenic manipulation. Attempts by humans to manipulate nature are analogous to chimpanzees learning to operate a complex electronic device: ecosystem management, like operation of the complex equipment, requires more than a trial-and-error approach. If the mechanisms are understood, better predictions can be made about what will happen if the system is altered. Unfortunately, unlike most electronic devices, nature is not equipped with a manual and we are often left seeing empirically what happens when we alter or manipulate. It is not an exaggeration to say that most of our present knowledge in natural science comes from similar accumulated experience of our ancestors. The formalization of natural science disciplines has resulted in the creation of hypotheses, predictions and extrapolations about the workings of nature, and design of experiments to reveal even more of the hidden, but inherent mechanisms. However, recent human-induced natural catastrophes clearly indicate we are still far from our goal of understanding many important mechanisms and interrelationships. It is apparent that the risk of failure or loss of sustainability when we manage natural systems will be reduced only if our limited knowledge of ecological mechanisms is markedly extended. Not all facets of nature are equally complex. However, when organisms are involved, complexity is often high. Thus, with a focus on living organisms, the discipline of biology faces arguably the most complexity in the canon of natural sciences. And within biology, the highest complexity is faced by the science of ecology as it integrates across scales from the molecular level to the biosphere, involving both the abiotic and biotic environments. As with other scientists, ecologists have benefited greatly from descriptive work like the works of Charles Darwin and Alexander v. Humboldt and many others, however, elucidating the underlying mechanisms is often difficult because of the great complexity of most ecosystems. For much of the ecological phenomena scientists have described, our knowledge consists of a preponderance of evidence supporting specific hypotheses instead of considerable knowledge of the true mechanisms. Effective study to reveal mechanisms will require research at all scales of organisation with linkages between scales. In this paper we focus on plant ecology. By supplying energy for nearly all organisms and many processes,

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plants are by far the most important organisms of the biosphere. Understanding the mechanisms driving the composition, dynamics and function of plant communities, therefore, are vital to unravelling the mysteries underlying ecosystem structure and function. Certainly, much research has been devoted to this issue, but linking across scales and traditional disciplines is providing new challenges for plant ecologists. Here we make a case for plant physiological ecology to be a central research focus in plant ecology, as it elucidates mechanisms crossing scales and disciplines.

Scale and ecological complexity: current research in plant biology Nature can be subdivided into a hierarchical system of increasing biological integration or levels of organisation, with scales beginning at the molecular level and extending up to the biosphere (Fig. 1). One of the basic rules of hierarchy theory in complex systems is that each scale has its own mechanisms, which amend the mechanisms from underlying scales (Allan and Starr, 1981; Nielsen and Mu¨ller, 2000). In addition, emergent properties are characteristic at each level of organisation based on the interactions among and inherent limitations of mechanisms at lower levels of organisation. Thus, while it is impossible to extrapolate from mechanisms at the bottom levels to explain processes at the highest level of organisation, linkages between disparate levels (and scales) can be effectively made by characterising mechanisms at intermediate levels. Presently, three significant ‘‘hot topics’’ of research can be identified in plant biology (Fig. 2). These research topics are at importantly different levels of organisation High Level of Integration

Biosphere Ecosystem Community Population Individual

Low

Organ Tissue Cells Molecules

Fig. 1. The levels of biological integration ( ¼ complexity) in nature.

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Ecosystem Level Processes

Vegetation Composition, Structure and Dynamics

underlying plant physiological processes is, therefore, essential for any causal understanding of the role plants at scales above the individual.

Plant population biology (sensu lato) and community ecology Plant Physiological Ecology

Plant Physiology and Molecular Biology

Fig. 2. The position of plant physiological ecology in relation to the three major research fields in plant biology.

and are largely assessed as nearly independent research disciplines. We review the essential facets of these research areas and then make a case that for linking among these somewhat disparate disciplines will require revelation of mechanisms at intermediate level of organisation.

Plant physiology and molecular biology The rapid methodological progression in the field of molecular biology has provided important new tools for plant physiology. With these tools, it is now possible to analyse the molecular mechanisms behind plant physiological processes that have been illuminated. Genetically engineered plants can be effectively used to analyse metabolic pathways and regulation processes (Jackson et al., 2002; Zhang and Forde, 1998). The rate of increase in knowledge in this arena is breathtaking. This is due in part to the field of biotechnology where the application of the new knowledge has fashioned the development of plants with defined traits that can be utilised to meet specific human needs (e.g. Fiechter and Sautter, 2007). Likely, the molecular mechanisms behind the most important physiological reactions within plants will be explicated in the near future, although more time may be needed to understand the regulation of all these processes (e.g. Hall, 2006; Humphreys, 1991; Leegood et al., 2000; Rock, 2000; Wardlaw, 1990). For ecologists trying to identify mechanisms related to the function of plants in ecosystems, the molecular approaches represent a big step forward in understanding because plants interact with their environment predominately through the physiology processes of the individual (unlike animals where behaviour has a large influence). Detailed knowledge of the mechanisms

In the field of plant population biology and ecology, enormous progress has been made during recent years toward comprehensive understandings of vegetation composition, distribution, structure and dynamics (Crawley, 1997; Freckleton and Watkinson, 2002; Gurevitch et al., 2003; Harper, 1977; Silvertown and Charlesworth, 2001), including the behaviour of alien species (e.g. Bossdorf et al., 2005; Cox, 2004; Dietz and Steinlein, 2004; Keane and Crawley, 2002; Sakai et al., 2001). Most of the major phenomena described at the plant community level have been quantitatively linked to the behaviour of plant populations and metapopulations (Bazzaz, 1996; Szabo and Meszena, 2006). The newly established discipline of ecogenomics gives new insights into basic mechanisms of evolutionary adaptation and phenotypic variation on the species and on the population level (Ouborg and Vriezen, 2007). In addition, a close link has been established between community ecology (e.g., to the numerous still unsolved problems of biodiversity) and ecosystem theory (e.g. Chesson, 2000; Waide et al., 1999). As such, most of the current research in the realm of plant population ecology deals with community (biodiversity) metapopulation dynamics and ecosystem related issues (Luck et al., 2003; McCann, 2000; Schmid and Pfisterer, 2003; Worm and Duffy, 2003).

Ecosystem level processes Research concerning fluxes of energy and matter are the ‘‘third hot’’ spot of plant science. Although there are various connections between the two, studies can be divided into two topic areas: (1) fluxes within the biosphere and (2) fluxes between the biosphere and the atmosphere. Research activities in the first area typically focus on fluxes within individual ecosystems. Thanks to this work, contemporary understanding of biogeochemistry and other related issues is rather profound (e.g. Bashkin, 2006; Matzner, 2004; Meir et al., 2006; Scherer-Lorenzen et al., 2005; Schlesinger, 2003). Nevertheless, there are still numerous unanswered questions that are too important to overlook (see below). Research in the second category involves scaling up from individual plant communities or ecosystems to global fluxes. Concern over global warming and the associated linkages to elevated atmospheric CO2 and other so-called ‘‘greenhouse gases’’ (e.g. Bazzaz, 1990; Buchmann, 2002; Hyvo¨nen et al., 2007; Monson and

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Holland, 2001; Reich et al., 2006; Schulze et al., 2001), as well as the rapid development of eddy covariance techniques and the commercial availability of relevant measurement systems, have greatly enhanced this research area (e.g. Reichstein et al., 2005). These approaches have made possible the measurement of fluxes of matter between biosphere and atmosphere with satisfying accuracy. The fact that multiple mechanistic atmospheric transport models work quite successfully (Jacob et al., 1997; Rebmann et al., 2005) strongly suggests that mechanisms driving atmospheric processes are relatively well understood. However, at the interface between vegetation and the atmosphere, our knowledge of mechanisms concerning fluxes of matter drops substantially as our understanding is based principally on empirical relationships (e.g. Katul et al., 1997; Valentini, 2003).

Plant physiological ecology: the missing link between scales and disciplines It is evident that considerable overlap occurs between the above-discussed research topics (Fig. 2). For instance, fluxes of matter between biosphere and atmosphere are highly dependent on vegetation cover, composition and dynamics in the area of measurement. And certainly fluxes and vegetation traits are linked to the behaviour of individual plants, linking with their environment through physiology. However, mechanisms involved in these linked processes are generally only poorly understood. For example, a mechanistic basis for the interaction of vegetation and the atmosphere that explains the measured fluxes of matter is still not well understood (Valentini, 2003) and little is known about the specific mechanisms involved in competition, a primary driving force behind vegetation dynamics (e.g. Casper and Jackson, 1997; Grace and Tilman, 2003). In addition, the links between molecular characteristics that limit physiological processes, and population and community dynamics, are similarly lacking in understanding. The science that is at the appropriate level of organisation and can be used to elucidate the mechanistic links in processes among the three ‘‘hot topics’’ is plant physiological ecology (Fig. 2). With the perspective that predictions of ecosystems responses to anthropogenic disturbance are only possible if the underlying mechanisms are sufficiently understood, one could conclude that plant physiological ecology would be an additional ‘‘hot topic’’ of botanical ecological science. Surprisingly, this is not yet the case. We spend the rest of this article presenting perspectives and an overview of opportunities for future research in the realm of plant physiological ecology.

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Physiological plant ecology of the past – a story of success In contrast to a prominent role in illuminating mechanisms (Fig. 2; see also Ackerly et al., 2000; Chabot and Mooney, 1985; DeLucia et al., 2001; ESA, 2000; Monson, 2003; Mooney, 1991; Mooney et al., 1987; Osmond et al., 1980), a sizeable number of scientists and funding organisations are of the opinion that the relevance of plant physiological ecology as an important discipline has declined to the point that it is no longer considered as one of the important topics of ecological research. The foremost reason for this attitude is that the subject area of plant physiological ecology is typically associated with the autecological plant research conducted during the latter portion of the 20th century or, even worse, simply with gas exchange measurements. Beginning in the late 1960s and based in large part on the pioneering work of Stocker, Lange, Billings and colleagues (Billings, 1985; Billings and Mooney, 1968, 1985; Koch et al., 1971; Lange et al., 1975; Schulze et al., 1972a, b; Stocker, 1970, 1971, 1972), field methods were developed that made possible the measurement of photosynthesis and transpiration of intact plant parts (typically leaves) in situ with an accuracy previously known only in laboratory settings (Beyschlag et al., 1986; Koch et al., 1971; Lange et al., 1985, 1987; Pearcy et al., 1989; Schulze et al., 1982). Subsequently, an overwhelming number of studies on plant primary production and water relations under natural field conditions were undertaken worldwide. Species from all components of the plant kingdom and from a large variety of habitats and ecosystems were investigated, with the analysis of stress as a major focus (e.g. Kappen and Friedman, 1983; Lange et al., 1969; Mooney et al., 1980; Tenhunen et al., 1987; Tranquillini, 1979). Close links were established with plant physiology and assessments of how physiological processes (e.g., pathways of photosynthesis) would function under actual environmental conditions became important research areas (e.g. Kluge and Ting, 1978; Osmond et al., 1982; Schulze and Caldwell, 1994; Schulze and Hall, 1982). These research developments were enhanced by the commercially available field-worthy instruments such as PAM chlorophyll fluorescence measuring devices that allowed non-destructive analysis of photosystem II activity throughout days and seasons (Papageorgiou and Govindjee, 2004; Schreiber et al., 1994). The new methods were applied in the context of contemporary environmental issues (e.g. Arntz et al., 2000) and valuable contributions were made that helped our understanding of plant behaviour under elevated UV-B and CO2, as well as various environmental and pollution stresses (Day and Neale, 2002; Ko¨rner, 2006; Lumsden, 1997; Mooney et al., 1987, 1991; Nowak et al., 2004; Sandermann et al., 1997; Schulze et al.,

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1989). In parallel, rather sophisticated mechanistic photosynthesis models were developed that allowed not only the calculation of photosynthesis rates of leaves under dynamics environmental conditions, but could also be used to scale up from the leaf to the canopy (Beyschlag and Ryel, 2007; Farquhar and Von Caemmerer, 1982). The latest additions to the ecophysiological toolbox were analyses of stable isotopes. Starting in the 1970s with the measurement of 12C/13C ratios for identification of plant photosynthetic pathways (e.g. Winter et al., 1978) and subsequently for determination of long-term water-use efficiency values (Farquhar and Richards, 1984), the application of stable isotopes for the analysis of various ecophysiological and ecological questions rapidly increased and belongs now to the most important tools in experimental ecological research. In between, isotope measurements of 13C, 2H, 17O, 18O, 15 N, 32S, 34S and 36S have been very successfully employed in a broad range of studies mainly to analyse reaction kinetics and quantify fluxes of matter. The applications range from autecology and mechanistic analyses of plant interactions up to the study of food webs and the quantification of fluxes of matter in entire ecosystems (Dawson et al., 2002; Ehleringer et al., 2000; Ho¨gberg, 1997; Lajtha and Michener, 1994; Maguas and Griffiths, 2003; West et al., 2006). The frequent use of the term ‘‘ecophysiology’’, which emphasised the physiological mechanisms, was very appropriate for this scientific work because it extended knowledge of plant physiology beyond the controlled environment of the laboratory and linked it to ecologically relevant conditions. Certainly our present knowledge of photosynthesis and water relations of individual plants and the physiological basis for these processes has been substantially improved by ecophysiological research throughout the last decades. As research topics, individual leaf and plant photosynthesis and water use patterns as related to physiological mechanisms have been well worked out. Nevertheless, there are aspects where mechanisms are still not fully understood (e.g., stomatal control, Buckley, 2005; Roelfsema and Hedrich, 2005, and the mechanisms of allocation of matter, Blakeley and Dennis, 1993; Cannel and Dewar, 1994; Lacointe, 2000). Perspectives that restrict the realm of physiological ecology to these subjects have aided in reducing the perceived importance of this discipline.

Physiological ecology of plant interactions – a research frontier Are the above-described mechanisms related to plant photosynthesis and water relations sufficient to mechanistically understand the role of plants in ecosystems? To

answer this question we have to take a closer look at the available literature. A critical evaluation exposes that most of the studies of physiological mechanisms linked to plant interactions originate from laboratory experiments with single plant individuals. Using photosynthesis as an example, the limitations in current knowledge are clear. Typically, the analysis of the photosynthetic behaviour of a plant (individuals or parts of plants, e.g., intact leaves) has two steps. First, diurnal courses of all relevant parameters (photosynthesis, transpiration and stomatal conductance) are measured in situ under typical field conditions (e.g. Beyschlag et al., 1986; Lo¨sch et al., 1982; Pereira et al., 1986; Zotz et al., 1997). Of course, these diurnal courses represent an integrated response of the plant to a variety of habitat conditions. To mechanistically interpret these patterns, plant individuals are then taken from the field into the laboratory or to a growth chamber where the measurement of single factor response curves is possible. Typically, the plant response to light, temperature, air humidity and CO2 partial pressure is analysed, under the realistic assumption that these are most important parameters for photosynthesis (e.g. Tenhunen et al., 1980a, 1981). Due to the development of new gas exchange systems during the 1980s single factor response curves can also be obtained in situ (e.g. Beyschlag et al., 1987; Tenhunen et al., 1984, 1985). The response curves may be used to parameterise largely mechanistic simulation models in order to estimate the integrated diurnal behaviour for given site conditions. On a short-term basis this strategy works quite well and there is a good agreement between calculated values and independently measured validation data (e.g. Beyschlag et al., 1990; Ryel et al., 1993; Tenhunen et al., 1980b, 1987). However, whenever longer time periods are considered and growth and allocation are considered, knowledge of pertinent mechanisms is minimal. This situation is reflected by the fact that nearly all relevant growth and allocation models are mostly based on empirical data and contain plenty of assumptions and hypotheses (e.g. Gayler et al., 2006; Osone and Tateno, 2005; Thornley, 1995). Unfortunately, limits in our knowledge of these mechanisms highlight our inability to fully understand the function of plants in the ecosystems. Thus, it is not only important to know how much carbon a particular individual plant assimilates, but also how this acquired carbon is used by this plant, how the allocation is regulated and how this allocation is affected not only by the abiotic but also the biotic environment of the plants. In particular, understanding mechanisms associated with plant biotic interactions adds a whole new dimension to plant ecophysiological research: the physiological ecology of plant interactions. Ample, but

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primarily descriptive information is available indicating that above- and belowground growth and allocation of plants growing with other plants of either the same or a different species can differ dramatically from that of isolated plant individuals (e.g. Ballare´, 1999; Bartelheimer et al., 2006; Callaway, 2002). However, the mechanisms behind these phenomena are not clearly understood. But it is very clear, that these are the mechanisms needed to causally link the processes at the community and ecosystem scale to the individually based physiological scale. This discussion highlights why plant physiological ecology sits as a linkage between molecular, population, community and ecosystem levels of organisation (Figs. 2 and 3). In other words, without the causal understanding of the various plant interactions, it is not possible to describe the mechanistic basis for the phenomena presently described empirically at the community, ecosystem and global levels. In addition, reliable predictions at these higher levels of organisation are compromised. What becomes apparent is that physiological plant ecology is arguably the heart of plant ecology rather than a peripheral entity. Unfortunately, this perspective is not appreciated by many plant and system ecologists, although a clear signal for the general importance of plant physiological ecology has been given by the ‘‘Scaling physiological ecology in the future’’ discussion during the year 2000 annual meeting of the ESA (DeLucia et al., 2001; ESA, 2000). Certainly, part of the problem is the breadth of disciplines involved for this research (see below) and appropriate perspectives for conducting this research are not universally recognised. The following list of contemporary questions in plant ecology will help to clarify this point.

Population Biology

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The principal ecosystem and community level question Mechanisms involved in determining vegetation composition and dynamics of plant communities, as well as emergent properties such as fluxes of matter, are largely undocumented, both at the level of individual communities and as generalisations (e.g. Bazzaz, 1996; but see Engelbrecht et al., 2007). Certainly, much importance has been placed on documenting mechanisms during the last years, but our understanding has often been limited by the lack of appreciation for the importance of physiological processes. We present a single, broad question that encompasses the topics and open questions of the following subsections (see also Fig. 3). What is the mechanistic background of vegetation composition, biodiversity structure and dynamics and how is this linked to fluxes of matter at the community and higher levels of organisation?

Plant–plant interactions Main open questions in this area are: What are the mechanisms of competition, facilitation and coexistence strategies, and what are the roles of resources, stresses and disturbance? Due to an increasing number of experimental investigations, it seems that many of the responsible plant traits for this have now been identified (e.g. Cahill and Casper, 2000; Caldwell and Richards, 1986; Callaway and Walker, 1997; Casper and Jackson, 1997; Casper et al., 2003; Fitter et al., 2002; Shea et al., 2004; Wright, 2002) and some experimental and modelling studies have already been carried out or are underway (e.g. Caswell and Etter, 1999; Lauenroth et al., 1993; Monteglio and Stoll, 2004; Zavala and De La Parra, 2005).

Global Fluxes Biodiversity

Interactions with the Abiotic Environment

Biotic Interactions Temporal and Spatial Distribution of Individuals

Stand Fluxes

Competitive Interactions Abiotic Site Conditions

Physiological Ecology of Plant Interactions

Symbiosis, Facilitation Parasitism, Herbivory

Balance of Matter of Individuals Ecological Plasticity of Species

Physiological Processes Genetics

Fig. 3. The central role of physiological ecology in causal understanding plant interactions with the environment at the higher complexity levels.

How do these interactions affect fluxes of matter within the community as well as between the community and the atmosphere? Driven by the burning mechanistic questions connected with global change, research activity in this realm is presently rather high (e.g. Baldocchi et al., 2002; Bormann and Likens, 1994; Lauenroth et al., 1993; Law et al., 2002; Margolis and Ryan, 1997; see also Monson, 2003). However our state of knowledge is still far from allowing general conclusions. How do such interactions affect the diversity and the stability of ecosystems? Numerous research activities have addressed the relationship between ecosystem stability and biodiversity, showing the dominant role of biotic interactions (particularly food webs) in this connection (Balvanera

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et al., 2006; Berlow, 1999; Kahmen et al., 2005; May, 1973; McCann, 2000). The role of plant–plant interactions is still rather unclear, but studies like the one of Kikvidze (1996) show that it may be worth to take a closer look on this issue. In summary, there is already a sizeable amount of interesting theoretical and descriptive perspectives pertinent to these questions (e.g. Grace and Tilman, 2003; Grime, 2001; Kinzig et al., 2002; Tilman, 1982, 1988; Tilman and Kareiva, 1997), but despite the numerous ongoing research activities, little is still known about the mechanistic background of these interactions and how specific plant strategies are developed and implemented. The necessity for further experimental research, as already demanded by Campbell et al. (1991), is quite obvious.

Plant–fungus interactions Although sizable information exists on the molecular basis of mycorrhization and the plant fungus interactions (e.g. Hause and Fester, 2005; Martin et al., 2007; Paszkowski, 2006; Reinhardt, 2007; Smith and Read, 1997; Van der Heijden and Sanders, 2002), the following questions have received little attention: How do mycorrhizal fungi affect resource acquisition (both nutrients and water), allocation and growth patterns in the context of the competitive abilities of plant individuals as related to community dynamics? While significant information exists on the important role of mycorrhizal fungi for plant resource acquisition per se (e.g. Auge´, 2004; Smith and Read, 1997; Takacs and Voros, 2003) only very few is known about the role of mycorrhiza in competitive interactions and the related community level effects. However the few available studies (Aerts, 2002; Van der Heijden and Sanders, 2002; Van der Heijden et al., 1998a, b, 2003) clearly indicate the potential for very important, but still unknown ecophysiological mechanisms in this area. How does functional response of mycorrhizal fungi to various stress conditions affect plant performance in the context of community dynamics? Most of the stress-relevant mycorrhiza literature deals with the importance of mycorrhizal fungi for the stress tolerance of higher plants (e.g. Langenfeld-Heyser et al., 2007). However, the stress physiology of the fungi themselves, which may have important effects on the resource supply of the host plants, has seen minimal analysis (e.g. Mexal and Reid, 1973). How do pathogenic fungi affect the competitive ability of plant individuals, and how does this affect community dynamics? Pathogens typically lower the fitness of plant individuals (e.g. Talbot, 2004). In contrast to this rather clear situation, the related effects at the community level are

rather unclear, as most of the available literature is largely descriptive (e.g. Burdon, 1991; Thrall et al., 1997). Some promising mechanistic activities are presented in a special issue of Plant Biology (Vol. 7 (6) (2005) pp. 557–744; e.g. Mattyssek et al., 2005). Are there interactions between fungi, soil microbes and/or soil fauna, which are relevant in community dynamics, and if so, what are the mechanisms of interaction? Presently, interactions within the mycorrhizosphere receive increasing attention, however, most of the existing studies are still primarily descriptive (e.g. Bever, 2003; Fitter and Garbaye, 1994; Mulder, 2006; Reinhart and Callaway, 2006; Scheu, 2005; Scheu et al., 2004). How do these interactions affect fluxes of matter within the community as well as between the community and the atmosphere? Currently, little is known about this. Most of the present work focuses on quantifying ecosystem fluxes of matter and determining their origins (e.g. Reichstein et al., 2005).

Plant–microbe interactions Most of the available literature about this topic deals with (mostly molecular) aspects of microbial diversity, plant–microbial interaction and, particularly, plant– microbial symbioses (e.g. Garbeva et al., 2004; Long, 2001; Nannipieri et al., 2003; Sessitsch et al., 2006; Tikhonovich et al., 2004), while the following questions are still largely unexplored: How do soil bacteria affect resource acquisition, allocation and growth patterns and in consequence the competitive abilities of individual plants as related to community dynamics? Are there also effects of the plant community on the bacterial communities? This seems to become an increasingly active field of research and besides of descriptive work there is also some mechanistic information available (e.g. Bonkowski and Roy, 2005; Buscot and Varma, 2004; Stephan et al., 2000; Whipps, 2001). How do N-fixing bacteria, as well as biological soil crusts, affect individual plant performance and affect community dynamics? Most of the research on N-fixing bacteria focuses on the N-fixation itself, while the ecological consequences are much less documented and still controversial (Boring et al., 1988; Quispel, 1974; Rai et al., 2000). There is certainly not enough information for generalisations, but the amount of data concerning 15N natural abundances continue to increase. Relationships between N-fixation and community dynamics have insufficiently been described and the existing studies are rather site specific and sometimes contradictory (Chapin et al.,

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1994; Uliassi and Ruess, 2002; Vitousek and Howarth, 1991). Primarily descriptive studies and some experimental data on the ecological importance of N-fixers from biological crusts and the role of disturbance in this connection can be found in Belnap (2001), Beyschlag et al. (2007) and Evans and Lange (2001). Is the functional response of soil bacteria to various stress conditions relevant to community dynamics, and if so, how? There are reports on stress response of soil bacteria (e.g. Morley et al., 1983; Rokitko et al., 2004), but the relationship between bacterial stress and community dynamics has not yet been explicitly addressed. Nevertheless, since pronounced links between the bacterial community in the soil and the related plant community have been reported (Bonkowski and Roy, 2005; Reynolds et al., 2003; Stephan et al., 2000), further mechanistic research on these effects is needed. How do these interactions between plants and microbes affect fluxes of matter within the community as well as between the community and the atmosphere? As already stated above, most of the ecosystem flux research focuses on the quantification and the origins of matter fluxes. Nevertheless, information on the causal background of primary fluxes becomes increasingly available (e.g. Marschner, 2007).

Plant–animal interactions Animals have profound effects on plant performance and function. Organisms range in size from soil invertebrates to large herbivores and their predators. While it is well understood that the size of the organism is not necessarily related to its importance on community dynamics, the important mechanisms related to these animals are not universally known. However, promising work related to soil zoology as well as herbivory is already ongoing (e.g. Karban and Baldwin, 1997; Mulder, 2006; Reinhart and Callaway, 2006; Scheu, 2005; Scheu et al., 2004). The important questions here are: Does soil fauna affect resource acquisition, allocation and growth patterns and in consequence the competitive abilities of individual plant as related to community dynamics? Besides of the above-cited references there are numerous case studies (e.g. Bardgett et al., 1999; Hodge et al., 1998; Moore et al., 2003) but the available amount of information is not yet sufficient for generalisations. Is the functional response of soil fauna to various stress conditions relevant to community dynamics, and if so, how? Some effects of reductions in soil fauna biodiversity have been studied by various authors (e.g. Griffiths

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et al., 2000; Taylor et al., 2004) but much more information is needed for generalised theory. Are there interactions between soil fauna, soil microbes and/or fungi, which are relevant to community dynamics, and if so, what are the mechanisms? Some descriptive studies are available (e.g. Bradford et al., 2002; De Deyn et al., 2003) but most of the relevant mechanisms are still unknown. How does herbivory affect resource acquisition, biomass allocation, growth patterns and in consequence the competitive abilities of individual plants as related to community dynamics? The available information on this is interesting but mainly descriptive and rather heterogeneous (e.g. Heil, 2007; Hendon and Briske, 2002; Holland et al., 1996; Karban and Baldwin, 1997; Robertson, 1991; Skogsmyr and Fagerstrom, 1992). Nevertheless, there are also some promising results on community level effects (e.g. Rinker et al., 2001; Wirth et al., 2003). How do these interactions affect fluxes of matter within the community as well as between the community and the atmosphere? Descriptive work on whole ecosystem effects of plant–animal interactions has been presented by various authors (e.g. Jones et al., 1994) and there is also information available on the coupling between atmospheric conditions and plant–animal interactions (Ehleringer et al., 2002). Again, most of the mechanisms behind these phenomena are hardly known.

Concluding perspectives Our presentation makes it exceedingly clear that future research to address these questions will take research that involves and integrates across multiple disciplines. It is important to realise that not all mechanisms will be equally important in driving observed ecological patterns, but that some will have greater influence under specific or perhaps most conditions. However, to identify and demonstrate these mechanisms will require assessing a broad range of potential mechanisms across disciplines. While the breadth of individual discipline researchers will need to increase (see discussion below), frameworks for effectively integrating scientists are needed. Problems arise when disciplines work at different scales or levels of organisation and approach research issues from philosophically diverse perspectives (Eigenbrode et al., 2007). The first step in overcoming this paradoxical situation is to clearly define research questions that are relevant and testable. Often individual disciplines have specific types of problems they address and are relatively inflexible in addressing novel perspectives. Another

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important step is to develop organisational environments that are designed to facilitate cooperative efforts instead of building hierarchical settings that effectively rank disciplines in order of perceived importance. The effective interdisciplinary research environment has to encourage cooperation, not build animosity among disciplines vying for control of the research effort (often for monetary, not scientific reasons). From the above list of questions, it becomes obvious that the scientific profile of the plant physiological ecologist of the future extends markedly beyond what has been traditionally considered relevant. What is needed is less a specialist for a single aspect of plant ecophysiology but instead a scientist with a rather broad scientific perspective, including knowledge and experience in fields outside of typical ecological research. The spectrum which needs to be covered reaches from molecular biology, plant physiology, morphology and systematics and microbiology to plant population ecology, community and systems ecology. A working perspective of chemistry, physics and mathematics will be desired as well as exposure to zoology, geology, meteorology, soil science, geography, mathematical modelling and resource management approaches. Of course, since meeting these criteria as an individual at an operational scientific level is nearly impossible, interdisciplinary cooperation of several scientists with different disciplinary focus is essential for successful future research of this kind. To effectively make this happen, two key issues have to be encouraged during academic study. First, after having learned the basics of biology and ecology, students need to be exposed to an integrative view of ecological problems and problem solving, and simultaneously be trained to incorporate their research findings into a broader ecological context. They have to become clearly aware of the interdisciplinary nature of the related problems and the respective classes should necessarily have an interdisciplinary perspective, perhaps enhanced by team teaching by educators from different disciplines. Second, the students need to learn to incorporate themselves into an interdisciplinary environment and how to deal with the naturally arising communication problems inherent in such working groups. A new generation of ecologists trained in interdisciplinary perspectives will permit discovery and exploration of the still hidden treasures of plant physiological ecology and finally expose the missing causal links in the core of our understanding of the biosphere.

Acknowledgement This paper is dedicated to Prof. Dr. Otto Lange on the occasion of his 80th birthday for his pioneering, inspirational and valuable contributions to the field of plant physiological ecology.

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