Progress in Physical Geography

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Goal functions in ecosystem and biosphere evolution Jonathan D. Phillips Progress in Physical Geography 2008; 32; 51 DOI: 10.1177/0309133308089497

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Progress in Physical Geography 32(1) (2008) pp. 51–64

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Goal functions in ecosystem and biosphere evolution Jonathan D. Phillips*

Tobacco Road Research Team, Department of Geography, University of Kentucky, Lexington, KY 40506-0027, USA Abstract: Although natural selection operates at the gene or individual level, a number of proposals, hypotheses and theories exist postulating the evolution of entities such as ecosystems, and indeed the entire biosphere. Further, there exist theories of evolution that are based not on the relative advantages (be they competitive or mutualistic) conferred on individuals, populations, or taxa, but on community, ecosystem, or biosphere-level goal functions, typically related to productivity criteria. A key question is why nature would seek to optimize energy flux or efficiency, biogeochemical cycling, or anything else. While development along some optimal pathway does occur, whether this is a rule, a tendency, or merely a possibility is not clear. This paper reviews theories of evolution and ecosystem development based explicitly or implicitly on goal functions. If the environment is conceptualized as a multidimensional resource space allocated among organisms, then only three assumptions are necessary for a developmental pathway toward increasing productivity: (1) higher rates of resource procurement and use are associated with ecological or selective advantages; (2) the environment is biologically saturated (or tending in that direction); and (3) the resource space is not contracting due to external abiotic forcings. This suggests that a tendency for evolution along a pathway toward maximum energy and/more matter fluxes, storages, transformations, or cycling does not require goal functions or natural selection operating at levels beyond the individual. Key research needs involve rigorous testing of these assumptions (particularly the first two), and the relative importance of, and relationships between, various notions of productivity. Key words: biosphere, ecosystem, evolution, Gaia theory, goal functions, resource space allocation.

I Introduction Biological evolution proceeds by the mechanism of natural selection. Natural selection, in turn, operates via mechanisms at the level of genes or individuals, and is manifest in populations and species. Advantageous traits and relationships, be they competitive

or symbiotic, are more likely to be preserved and transferred to succeeding generations. Without delving into debates over how differential traits arise, or the relative importance of mutualism versus competition (see Margulis, 1998; Smil, 2002), no one has proposed any plausible mechanisms

*Email: [email protected] © 2008 SAGE Publications

DOI: 10.1177/0309133308089497


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Progress in Physical Geography 32(1)

(as opposed to phenomenologies) of natural selection operating at broader scales such as communities, ecosystems, or the entire biosphere. Nevertheless, a number of proposals, hypotheses and theories exist postulating the evolution of entities such as ecosystems, and indeed the entire biosphere. Further, there exist theories of evolution that are based not on the relative advantages (be they competitive or mutualistic) conferred on individuals, populations, or taxa, but on community, ecosystem, or biosphere-level goal functions (eg, Smith, 1986; 1989; Lovelock, 1988; 1991; 1995; Margulis, 1998; Levchenko, 1999; Eagleson, 2002; Lapenis, 2002; Lenton and van Oijen, 2002; Ackland, 2004). The key challenge, as Downing and Zvirinsky (1999) state it, is to ‘explain the emergence of biotic communities that are capable, via their implicit coordination, of regulating large-scale biogeochemical factors such as the temperature and chemical composition of the biosphere, but to assume no evolutionary mechanisms beyond contemporary natural selection’. With respect to goal functions, a nagging issue is the question of why, in the absence of a guiding hand, nature would seek to optimize energy flux or efficiency, biogeochemical cycling, or anything else (and, for that matter, why and how a guiding hand would pursue these optima). Strong evidence exists that, in many cases, development along some optimal pathway does occur, but whether this is a law, a possibility, or something in between is not clear. These problems also appear in the literature on ecosystem development (eg, Patten, 1995; Jorgensen, 1997; Fath et al., 2001; 2004; O’Neill, 2001; Reynolds, 2002). The goal of this paper is to review ideas with respect to biosphere and ecosystem goal functions, and to address the issue of whether goal functions are necessary to achieve trends toward increasing ecosystem productivity. The study is motivated by efforts to determine whether evolution at the ecosystem level can be conceptualized

as an emergent phenomenon arizing from microscopic natural selection, independent of any a priori assumptions about the goals or direction of evolution. II Background 1 Gaia and biogeochemical selection The best-known ideas regarding evolution at macroecological scales arise from the Gaia theory/hypothesis. Early versions of Gaia (Lovelock, 1988) saw the earth system as a sort of superorganism, and evolution directed by the goal of increasing the habitability of the planet for the self-maintenance of the entire biosphere. Superorganic concepts have largely been abandoned, but Gaia theory does postulate biosphere-scale evolution. Developed chiefly by Lovelock and Margulis (Lovelock and Margulis, 1974a; 1974b; Lovelock, 1988; 1991; 1995), Gaian theories of evolution continue to be developed by others (Free and Barton, 2007). According to Lenton (2002) Gaia theory proposes that the Earth system self-regulates in a habitable state, with a focus on the effect of life on the state of the Earth and its response to forcing and perturbation. Lenton argued that life has not survived for >3.8 billion years purely by chance; rather, the Earth system possesses regulatory mechanisms. The system is more resistant and resilient to many (but not all) perturbations with life present, and Earth is predicted to remain inhabitable for longer with life present than it would be in the absence of feedbacks from the biosphere to the abiotic environment. It appears that there may be an innate tendency for regulatory properties to accumulate and strengthen as the biota evolve. Four basic tenets underlie Gaian evolutionary theory (Lenton and van Oijen, 2002; Lenton and Wilkinson, 2003): Life alters the environment, life forms grow and reproduce, environment constrains life, and natural selection occurs. This leads to global environmental effects and feedbacks, and (global) environmental feedback on


Jonathan D. Phillips: Goal functions in ecosystem and biosphere evolution selection. Regulation is thus seen as an emergent property in many systems even in the absence of active selection for it. The role of biogeochemical cycling is emphasized, not only with respect to maintenance of favourable atmospheric chemistry, but also with respect to mutualistic relationships between organisms. Lenton and Wilkinson (2003; see also Volk, 2007) argue that the problem of evolutionary ‘cheating’ disappears if Gaia is built of byproducts. Gaia theory is controversial in many respects, but particularly with regard to evolution. As Lenton and van Oijen (2002) note, ‘a challenge for Gaia theory is to find principles that explain how regulation can emerge at the global scale from natural selection of environment-altering traits at the individual level. To what degree the ontogeny … of Gaia is unique or deterministic is a major question’ (p. 683). They also note a key challenge from evolutionary biologists ‘to explain how order, especially self-regulation, can arise at the global scale without invoking teleology or selection at the level of the planet’ (p. 687). Selection at the level of ecosystems or broader is untenable, Lenton and van Oijen (2002) acknowledge, but it may be that life-forbidding state variable levels are difficult to reach: whenever organisms become so abundant that byproducts become life-threatening, evolution produces organisms for whom the byproducts or the producing organisms themselves become resources. If natural selection has enough genotypic variation to work with, such checks are always likely. This ‘old idea … could explain the likelihood of regulation at livable levels as a side-effect of evolution in a sufficiently diverse biota’ (Lenton and van Oijen, 2002: 689). Kirchner (2002), one of the most highprofile critics of Gaia theory, proposes a mechanistic alternative to Gaia: because natural selection favours those organisms that can best exploit their environment, organisms will often be dependent on environmental services their ecosystem provides.

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Traits that confer differential advantage will become more common via natural selection, but traits that confer general benefit will undergo genetic drift. This allows for the possibility of coevolution for the mutual benefit of all biota present, but does not predict such an outcome. Dagg (2002) also argues that where Gaia-type phenomena emerge they will be byproducts of naturally selected traits. The strong influences of life on the environment, tight coupling of the biosphere and abiotic components of the earth system, and the coevolution (in at least the sense of contemporaneous and interacting development over time) of the biosphere and other aspects of the earth system are widely accepted. With respect to evolution, however, the implicit or explicit invocation of ‘directed evolution’ of the biosphere is problematic. Smil (2002) asks what Gaia is supposed to accomplish (maximize standing biomass, diversity, primary productivity, or all of the above?). While accepting, and even embracing, the notion that cooperation and mutualism is even more important than competition in evolution, Smil (2002: 231) notes that ‘geneticists refuse to be converted to the idea that evolution can select for environmental altering traits that benefit not just individuals, but the entire biosphere’. However, results from model experiments indicate that Darwinian selection does not rule out Gaia (Sugimoto, 2002), and that ‘selfish gene’ selection combined with the ability of organisms to modify the environment leads to Gaian evolution (Dagg, 2002; Staley, 2002). Kleidon (2004) also showed that a maximum entropy production principle applied to biosphere-atmosphere interactions indicates a high probability of an earth system predicted by Gaia theory. Many of the basic underlying themes of the Gaia hypothesis were arrived at independently by Vernadsky (1926). Vernadsky saw the biosphere as a web of biogeochemical feedback mechanisms that connects organisms and environment in a single


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system. In his view, life has a natural tendency for expansion through intensification of biogeochemical cycles, and natural selection is directed toward species capable of increasing cycling of elements. Lapenis (2002), drawing on Vernadsky and several other Russians writing in the late nineteenth and early twentieth centuries (Rizpolozhensky, 1892; 1897; Kropotkin, 1902; Kostitzin, 1935; 1939), presents an updated version based on a principle of biogeochemical selection. The overall direction of evolution is directed by the universal criterion of natural selection. Because biogeochemical selection promotes species with better recycling skills, the biosphere has a natural tendency to evolve toward a state of greater productivity, diversity, and sociability (Lapenis, 2002). According to Lapenis’s (2002) synthesis of the Russian originals, Kropotkin (1902) held that mutual aid (rather than competition) was the most energetically efficient mechanism of survival. As organisms can be changed in the course of their interactions with the environment, evolution is directed toward the most energetically efficient state. Rizpolozhensky (1892; 1897) also focused on mutualism as a driving force in evolution – a radical view at the time which has since been bolstered by abundant biological support (Margulis, 1998; Smil, 2002). According to Rizpolozhensky (via Lapenis, 2002), mutual aid arises for the purpose of joint preparation of food. Organisms change the environment through the formation of ‘soil’ (Rizpolozhensky’s concept of soil was apparently much broader than the conventional notion), and organisms change the environment (‘soil’) in a direction favourable for life in general. Kostitzin’s (1935; 1939) theoretical models show that the probability of any species surviving through mutual aid is a function of the complexity of the food web, and depict evolution as a chain of very unlikely events directed against the increase of thermodynamic entropy, and driven by selective accumulation of small, random genetic mutations. If food web complexity

is roughly equated with biogeochemical cycling intensity, Kostitzin’s work implies a link between biogeochemical selection and evolution via accumulation of random genetic mutations. 2 Ecosystem assembly and evolution In a discussion of links between conservation philosophies and ecological thought, Callicott et al. (1999) proposed a useful dichotomy between compositionalism and functionalism in ecology. The former is based on evolutionary ecology, with a focus on forms and morphologies of organisms and the composition of communities and ecosystems. The latter is based on ecosystem ecology, with a focus on the flux and cycles of energy and matter. One may speculate that evolutionary theories based on biogeochemical selection, mutual aid in resource preparation, and Gaian principles occupy a conceptual ‘no man’s land’ between these schools of thought (although more overlap and less conflict exists than the dichotomy implies). Indeed, Free and Barton (2007: 611) suggest that Gaian theories remain ‘on the fringes of mainstream biological science’, although it could be argued that Gaian evolutionary theory occupies a more central place in earth system science (cf. Lapenis, 2002; Kleidon, 2004; 2007; Volk, 2007). Vernadsky (1926) essentially viewed the biosphere as a planetary membrane for capturing and processing solar radiation energy. A number of contemporary theories of ecosystem structure, function, and development are based on thermodynamic principles (eg, Patten, 1995; Jorgensen, 1997). Therefore, unsurprisingly, theoretical notions have arisen linking evolution to energetics principles, an idea going back at least to Kropotkin (1902). Although Budyko (1986) viewed evolution primarily as a biotic response to abiotic forcings, his work on the coevolution of climate and the biosphere is based on energetics principles. Eagleson (2002) took a similar approach focused on application of biophysical prin-


Jonathan D. Phillips: Goal functions in ecosystem and biosphere evolution ciples to the problem of the interactions between vegetation, solar energy fluxes, and moisture fluxes. Biology is seen as expression of optimality whereby natural selection seeks to maximize energy fluxes, leading to plants with the optimum form and function for a given environment. Some properties, such as canopy cover, appear to be optimized but cannot be maximized by ‘selfish genes’. Eagleson (2002) identifies opportunities for natural selection to maximize production (assumed to be directly linked to reproductive success) via variations in plant morphology and physiology. Levchenko (1999) holds that evolution of the biosphere is governed by increasing energy flux – for example, that selection pressures favour more rapid energy capture and conversion. Ackland’s (2004) modelling results indicate evolution toward maximizing planetary life. While acknowledging problems of defining the amount of life, Ackland’s (2004) analysis is based on thermodynamic principles. Strong evidence exists that, in many cases, ecosystem development along some optimal pathway does occur, but whether this is a rule, a tendency, or merely a possibility is not clear. Among the proposed rules for ecosystem assembly suggested by Reynolds (2002) are that the most prominent species will be those storing the most exergy (= high-quality energy), and that system growth raises the aggregate ability to harvest and store exergy. Patten (1995) and Fath et al. (2004) argue that ecosystems organize to maximize the storage and throughflow of energy, arising from the microscopic flows and dynamics of ecosystem networks. Patten also shows that maximizing energy flux and storage requires maximizing indirect effects, thus formally linking energy and biogeochemical cycling optima. Fath et al. (2001) summarize the complementarity of ecological goal functions expressed in terms of energy fluxes, storage, and dissipation, and cycling, and shows that they are mutually consistent and indicate similar patterns of ecosystem development. The ‘fourth law of thermodynamics’ governs ecosystems in Jorgensen’s (1997)

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theory: a system that receives a throughflow of exergy has a propensity to move away from thermodynamic equilibrium, and to select the organization that gives the system as much exergy as possible. Jorgensen (1997) explicitly links ecosystem assembly and evolution. A combination of the fourth law, advantageous environmental characteristics and exergy flow led to the formation of highly organized organic molecules, Jorgensen argues. With the emergence of the ‘selfish gene’, evolution was initiated. Long periods of time and a high degree of spatial and temporal heterogeneity ensured the development of diverse and complex ecosystems. The emergence of ‘Gaia effects’ is attributed to a long period of selection pressure under the influence of all the other biological components responsible for the development of a high degree of symbiosis and network mutualism. Some argue (eg, Brooks and Wiley, 1988; Kauffman, 1993) that natural selection alone is not sufficient to result in the evolution of a complex biosphere, that self-organization must also occur. Self-organization principles can explain how optimal pathways might be followed without any guiding hand or without invoking any particular exernally imposed goal functions. For example, Kostitzin (1934) showed that variations in initial conditions, history, and chance produce a variety of potential evolutionary equilibria for a given set of environmental constraints. Unstable communities tend to disappear; stable ones tend to persist. In Kostitzin’s theoretical models stability is linked to food web complexity. To the extent this is tied to biogeochemical cycling, Kostitzin’s (1934) model provides a plausible mechanism for evolution in the direction of increasing energy and elemental cycling. More recent evolutionary modelling and ‘artifical life’ experiments (cf. Staley, 2002; Standish, 2002; Sugimoto, 2002; Ackland, 2004) have shown that a few simple rules can result in evolutionary dynamics which result in increasing diversity, complexity, and energy efficiency. Similar results have been obtained in ecosystem assembly models (cf. Hubbell, 2001).


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3 Energy and resource constraints One of the most comprehensive theories of evolution of the biosphere is that of Levchenko and Starobogatov (1997), which incorporates abiotic environmental constraints, the role of biota in expanding the sphere of life, historical contingency, energetics principles, and evolution/selection at scales ranging from cellular to the biosphere. The concept of licence (from the authors’ Russian-to-English translation) is introduced, defined as unfilled (or contestable) ecological niches. Microevolution is seen as essentially putting realized niches in accordance with licences. Speciation requires a new licence or appropriation of (at least a portion of) an existing one. Levchenko and Starobogatov (1997) emphasize the ability of the biosphere to expand its own boundaries and to create new licences, as well as the constraints placed on subsequent evolution by preceding evolution. They describe this autoregulated evolution as autocanalization; the channelling of evolution based on a combination of environmental constraints and biological evolution. As licences are filled, and new ones created, energy flow through the biosphere is increased and biotic organization and complexity also rises. Biodiversity is seen as necessary (given the historical contingency of evolution) to provide the number of potential adaptations and interactions necessary to respond to the variability of the planet (Levchenko and Starobogatov, 1997). Levchenko (1999) expanded the arguments in the context of information theory, emphasizing optimal evolution and behaviours to maximize energy capture. Natural selection produces algorithms for energy optimality that are ‘remembered’ by the biosphere. The biotic/abiotic sector model was developed by Smith (1986), who argued that evolution may operate at the biosphere, macroevolutionary and community levels. The model is based on the evolution of both biota and environment. Smith places more emphasis on exogenous controls on evolution than in Gaian theories; the biotic sector as a

whole evolves in response to constraints set by the abiotic sector (p. 233). Smith’s (1986) model is also based on energetics principles. The necessity of energy/negentropy import requires suitably adapted organisms at the right place and time. Evolution is seen as a function of biotic contributions to development of more efficient resource turnover (p. 234). Thermodynamic and chemical equilibrium between the abiotic and biotic sectors cannot be reached, at least partly due to biotic adaptations which lead to a net reduction in the amount of energy required to return vital resources to the same stage in a given cycle type. Selective forces are greatest where resource cycling is most suboptimal – habitats demanding the most selection will be occupied most slowly and depopulated from most rapidly. According to Smith (1986: 249): ‘When evolution is understood as the disequilibrium inherent in biotic sector/abiotic sector spatial interaction (and not “the process of adaptation”), the homeostatic, “ecological,” role of adaptation can be accepted as a “result” to provide a straightforward causal picture devoid of circularity and attending logical difficulties. In this view, adaptations are regarded simply as the structural attributes that mediate energy dissipation … it is the properties of spatial interaction that evolve, not the organisms themselves.’ Recursive change (responses to and influences on the abiotic environment) within the biotic sector ‘is most fundamentally guided by selection producing more efficient means of turning over material resources (spatial interaction), as opposed to “fit” individuals and population’ (p. 250). Smith’s concepts (further elaborated in Smith, 1989; 2005) are perhaps the most robust theory of evolution at the ecosystem and biospheric scale, encompassing thermodynamic and energetics arguments, and specifically leading to maximization of the rates of both energy flux and biogeochemical cycling. Beyond linking the evolutionary/ compositional and ecosystem/functional


Jonathan D. Phillips: Goal functions in ecosystem and biosphere evolution perspectives, Smith (1986; 1989) explicitly links biogeography and evolutionary change through his emphasis on the role of spatial interaction. Evolutionary divergence is seen as (usually) a return toward, rather than away from, equilibrium. The main feedbacks are associated with changes in geographical ranges which drive adaptations. Divergence is significant as a way adaptive suites can be refocused to react to local conditions of environmental constraints on resource turnover. The more efficient the turnover, the less constraining the environment becomes (Smith, 1989). Finally, the model is explicitly linked to the issue of directedness in Gaian evolution: ‘We do not need teleology to support a “Gaiac hypothesis” interpretation of world ecosystem change: probabilistic interaction (i.e., spatial interaction) within a limited spatial domain naturally leads to both increasing order and increasing diversity’ (Smith, 1989: 783–84). III Resource space allocation 1 Resource space concept It appears that a tendency in ecosystem or biosphere development toward some maximum rate of productivity requires only the following: The likelihood of successful establishment and reproduction of any individual or population is related to the ability to acquire and process resources (energy, water, nutrients, geographical space). This is either explicitly stated or implied in many of the evolution theories reviewed above. Resource procurement may involve cooperative relationships and the use of ecological byproducts in addition to competition and abiotic resources. While this principle does not necessarily dictate such a trend, it does make productivity maximization likely. Hutchinson (1957) defined an ecological niche as a n-dimensional hypervolume, where n is the number of environmental factors needed for survival and reproduction of a species. Fundamental, or potential, niches define the potential locations of a species, whereas realized niches (a subset of the

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fundamental niche) are where the species actually exists. The resource space concept is introduced here as a broadly similar idea, but applied at a much broader scale, and intended as a heuristic device. Thus, niches are defined relative to a particular species or organism, while resource spaces are defined based on potential resources which may be exploited by multiple species that may be defined at the ecosystem or biosphere scale. Resource space (RS) is thus an n-dimensional space defined by geographical space, time, energy, water, nutrients, and minerals. RS is strongly constrained by abiotic factors, and could be increased or reduced by geophysical phe-nomena, but is also strongly influenced by biota, via byproducts, ecological engineering, etc. Thus, in addition to abiotic forcings, RS may be increased by the introduction of new resources as biological byproducts (increase in n, where x i , x w , x 3 , … , x n are the axes of the resource space) or by production of greater quantities of a given resource (increase of xi). Resource space may be decreased by the loss of species or due to degradation from harmful byproducts. Let S denote an n-dimensional RS, where the x = 1, 2, … , n resources or dimensions define the resource space. These represent the coordinates of geographical space and the supply of energy, water, nutrients, minerals, and any other necessary resources. S i indicates the resource space occupied by taxon i, and S o , S u , respectively, are the occupied and unoccupied portions of the resource space, with So + Su = S. At biological saturation, Su = 0. N is number of species or taxa (hereafter simply species, although the concept may apply to other taxonomic levels). Applying an exclusion principle: N = So /S¯ i

(1)

This resource exclusion principle does not necessarily have implications with respect to stable coexistence; it implies only that two individuals cannot consume or occupy exactly the same resources at the same time.


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The resource exclusion principle therefore does not imply that no two species can utilize the same kind of resources and is not the same as the well-known but debatable competitive exclusion principle. Productivity (P) is conceived, broadly, as the rate of energy and mass fluxes and conversions. Productivity of a given species is Pi, and P = !Pi, i = 1, 2, … , N. Defining " as the rate of resource use in converting mass and energy per unit of resource space: Pi = Si "i

(2)

Theories of the evolution of the biosphere and development of ecosystems are most often concerned with some measure of productivity (P) such as net primary productivity, net ecosystem productivity, evapotranspiration, rates of biogeochemical cycling, etc. Relationships between P, N, and S can be expressed as follows based on the definitions and identities above: ¯ )S " N P = !(S¯ i " i i i

(3)

N = So /S¯ i

(4)

#

So = NS¯ i = !Si

(5)

Relations (3)–(5) provide a means to assess the qualitative changes (eg, increase, decrease, or no change) associated with various external and internal changes in the ecosystem or biosphere. These are summarized in Table 1 and discussed in more detail below. 2 New species When new species are introduced by speciation or invasion, they must claim some portion of resource space to survive. If they use an unoccupied portion of the RS, then So is increased, and both species richness and productivity must be increased. If the newcomers are obliged to use an occupied portion of resource space, then competition occurs with existing species. The resource exclusion principle forbids simultaneous

utilization of the same territory within the RS. In a case where pure competition is at work and neither species is able to adapt to use a different portion of RS, one must go locally extinct via die-offs or outmigration. In this case productivity may increase, decrease, or remain constant depending on the relative productivity of the ‘winner’ and ‘loser’. If one or both competitors is able to adapt by migrating to another, not fully occupied, portion of RS, or via development of mutual cooperation, productivity increases with S o . The establishment of a new species may effect the RS itself, if new resources are produced as byproducts, potentially increasing productivity. 3 Chance extinction Loss of a species to chance extinction (local or global) leaves an area of resource space unoccupied. If this space remains unexploited productivity declines with N. If it is occupied by an existing or new species, changes in productivity will depend on the efficiency (") relative to that of the lost species. A new occupant which produces resources which expand S provides the possibility for a productivity increase. 4 Changes in resource space In additions to changes associated with biological byproducts, S can be enlarged or reduced at all timescales by a variety of geophysical and climatic phenomena. An expansion can only result in increases or constancy of N and P, depending on occupation of the new space. If the RS is not biologically saturated (S > So), some or all of a contraction may be accommodated by utilizing previously unoccupied portions of S. If S is saturated (Su = 0), or if So is reduced, contraction is likely to result in decreasing P. Changes in resource space (or, for than matter, invasions or extinctions) could trigger behavioural or evolutionary adaptation adaptations which modify resource use efficiency. The overall change in productivity


Jonathan D. Phillips: Goal functions in ecosystem and biosphere evolution

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Table 1 Summary of responses in resource space (S), productivity (P), and richness (N) to changes in species, externally controlled resources, and resource use and allocation (see text for more complete explanation) A. New species (invasion or speciation) 1. Uses unoccupied S So, P, N increase 2. Uses occupied S Competition with existing species Neither species able to adapt or migrate N, So constant; P contingent on "i One competitor adapts to new region of S N, So, P increase 3. S increase if new species produces new resources; see C1 B. Chance extinction 1. Vacated resource space not exploited So, P, N decrease 2. Vacated space exploited By existing species So, N constant; P contingent on "i of expanding versus extinct species By new species So, constant; P contingent on "i of new versus extinct species; N increased See also A C. Changes in resource space 1. Increased S P, N increased or constant (see also A1) 2. Decreased S S > So changes may be partially offset by use of previously unoccupied S N, P constant or decreased S = So P decreased (unless increases in " stimulated) Niches reduced but not eliminated N constant Niches eliminated N decreased (see also B) D. Increased resource use efficiency 1. Increased efficiency (") S increased; P increased or constant; N constant or increased; see C1 E. Resource imperialism 1. Newly occupied space previously unoccupied P, So increased; N constant 2. Expansion into occupied space Niche(s) for previous occupants reduced but not eliminated P contingent on " of new occupant relative to previous; So constant; N constant Niche(s) eliminated P contingent on " of new occupant relative to previous; So constant; N decreased


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would then depend on the extent to which the changes in efficiency offset the decline in So. Changes in resource use efficiency are dealt with separately below. 5 Changes in resource use Genetic evolutionary changes at long timescales, and life-cycle or successional changes at ecological timescales, can result in changes in resource procurement and processing. Although the possibility exists that these might in some cases result in less efficient use of resources or the relinquishing of resource space, the weight of evidence favours increased resource use efficiency and the acquisition of new space. Increased efficiency – that is, achieving the same function with less energy, water, area, or whatever – essentially frees up resource space. Thus increased productivity is the most likely outcome, although another possibility is that the vacated space

Figure 1

would not be exploited, keeping productivity constant. Resource imperialism involves a species occupying an increasingly large portion of the resource space (increasing S i with S con-stant). If the new space was previously unoccupied, productivity increases. If imperialism with constant So eliminates niches for other species (thus reducing N), changes in productivity will depend on the relative productivity of the increaser compared to the decreaser, but, under the assumption that an imperialist is a more efficient processor, P will increase (Figure 1). IV Evolutionary pathways The RSA as represented above allows the identification of potential pathways which could result in increases or decreases in diversity and productivity. In general, either increases or decreases in richness and

Potential effects of resource imperialism on productivity


Jonathan D. Phillips: Goal functions in ecosystem and biosphere evolution productivity could result from both intrinsic and extrinsic, and from both biotic and abiotic, changes or forcings. The arrival or new species, the expansion of RS, and increased resource use efficiency cannot, by themselves, decrease productivity, and all may well increase it (for example, see Figure 2). Resource imperialism will increase productivity if the productivity of the imperialist species exceeds that of the species displaced from the resource space. To the extent that productivity is related to competitive ability or selective advantages, this seems likely. Even chance extinctions and decreases in resource space might increase productivity under certain circumstances, depending on the productivity of replacement species and adaptations to shrinking RS. Productivity declines could be associated with extinctions where the vacated space is not exploited, or with

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imperialism where the productivity of the new species is less than that of the displaced one (this seems unlikely; see above). Contractions of RS are also likely to decrease productivity under many circumstances. Many biogeographical models assume biotic saturation; eg, that all niches are filled and in essence, that resource space is completely occupied (eg, Hubbell, 2001). If this assumption is applied to the RS, all that is necessary to dictate a path toward increasing productivity (ie, all the types of changes considered in the preceding section can only increase productivity or leave it unchanged) are the assumptions that productivity is a competitive advantage (imperialists and competitive ‘winners’ are more productive than the species they displace), and that resource space is not decreasing. The analysis above indicates that in a stable or expanding resource space, if biotic

Figure 2 Possible productivity responses to an expansion of resource space due to external forcings or biological byproducts


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saturation occurs and productivity is directly related to competitive or selective advantages and fitness, productivity must increase over time. Assuming that increased productivity is associated with more rapid and efficient elemental cycling, then the latter should increase over time as well. By viewing species in a dynamic resource space that may be expanded, shared, and contested, the basic postulates of goal functions related to productvity emerge without any necessity of invoking selection pressure at any level beyond the individual, and without specifying a goal function a priori. V Discussion The resource space allocation model is a heuristic device, not a predictive or simulation model. Beyond being quite broadbrush, it can accommodate any observed changes in productivity and is therefore not falsifiable, although its underlying assumptions are subject to empirical testing. The utility of the RS framework is that it shows that ecosystems may exhibit systematic changes in productivity without invoking natural selection operating at any level beyond that of the individual, without postulating any particular goals, targets, or optima other than survival, growth, and reproduction of individuals. The RS model is chorographic in the sense that it considers a lumped, aggregate space, albeit at scales up to global. It is complementary to the spatial variability and interaction framework laid out by Smith (2005). He argues that if the environment presents geographically anistropic survival probabilities then there will be a tendency to disperse more rapidly in some locations or directions than others. Survival probabilities are set by the level of optimality of resource delivery (consistent with O’Brien, 2006, Smith suggests this is likely to be water in most instances) relative to the organisms. This optimality includes consideration of how efficiently the biota turns over or recycles resources in the local ecosystem. As populations

grow, they should find it easier to disperse in directions of lower stress and higher resource availability, so that the negative feedbacks of selection will not be as severe as in areas of higher stress. ‘Thus, the suggestion is that all populations will tend to disperse in the same preferred directions, in so doing non-randomly perpetuating genetic flexibility – and, importantly, contributing to the shaping of ever-more stable and resilient biogeochemical pathways. This is evolution – environmentally mediated (or even directed) evolution, to be sure, but not environmentally determined evolution’ (Smith, 2005: 1512). The resource space can be interpreted via Smith (2005) as a statespace in which organisms find themselves, but ‘not in such a fashion as to subvert the “individuality” of any given evolutionary line’. The ecological state-space (resource space) produces change in a way that need not be viewed as ecological determinism (Smith, 2005: 1513). Observations of increases (decreases) in productivity in the context of the RS allocation point to several possible developmental pathways which, alone or in combination, could account for the observations. Place, problem, or system-specific evidence can allow further elaboration of how the observed changes came about. Importantly, however, these examples reveal only what did happen, and do not necessarily point to any generalizations applicable in other situations or to any laws governing evolution of biospheres or ecosystems. Smith (1989) and Kleidon (2004), among others, have previously argued that Gaian evolution does not require teleology or biological goal functions, although both authors focused on principles or tendencies of thermodynamics and energy flux. This review suggests that no assumptions with respect to maximization or optimization of any thermodynamic quantity are necessary; only the (empirically testable) notion that increase resource procurement confers, or is associated with, selective advantages.


Jonathan D. Phillips: Goal functions in ecosystem and biosphere evolution VI Conclusions Increases, decreases, or constancy in productivity can occur following introductions of new species, chance extinctions, changes in the size of the resource space, or changes in resource utilization patterns. However, all that is needed to dictate a general path toward increased productivity are three conditions: (1) biotic saturation (all resources are fully utilized); (2) selective advantages are conferred on or associated with increased productivity; and (3) resource space is not decreasing or contracting. Natural selection mechanisms operating at the levels of individuals, populations, and species can have evolutionary or developmental phenomenologies manifested at broader levels of communities, ecosystems, and biospheres. Evolutionary phenomenologies at the broader levels postulated by many theorists are clearly possible without any teleological appeals, and that a few conditions are all that is required to move a biological system toward increasing productivity and resource cycling. Acknowledgements John Waldron and Charlies Smith made useful comments on an earlier draft. More importantly, without their encouragement I probably would not have attempted to put these ideas into the ‘marketplace’. Several of my biogeography classes at the University of Kentucky have also helped me refine my ideas and exposition thereof. References

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