Neutral theory in community ecology and the hypothesis of functional equivalence

Abstract

Probably no ecologist in the world with even a modicum of field experience would seriously question the existence of niche differences among competing species on the same trophic level. The real question, however, is how did these niche differences evolve, how are they maintained ecologically, and what niche differences, if any, matter to the assembly of ecological communities? By ecological community I refer to co-occurring assemblages of trophically similar species. By assembly I mean which species, having which niche traits, and how many species, co-occur in a given community. In my judgement, despite a long and rich tradition of research on these questions in community ecology (Chase & Leibold 2003), we are still far from having definitive answers. Several years ago, in an attempt to provide a fresh approach for tackling these questions, I introduced a formal neutral theory for ecology (Hubbell 1997, 2001). The traditional strategy has been to assume that ecological communities are inherently high-dimensional sensuHutchinson's (1957) niche hypervolume for each species, and then to build rather complex models from the outset, incorporating as many of the details of the growth and interactions of each and every species and with their physical environment as possible. Neutral theory, however, adopts a fundamentally different strategy, taking virtually the opposite tack. It begins with the simplest possible hypothesis one can think of – for example, the functional equivalence of species – and then adds complexity back into the theory only as absolutely required to obtain satisfactory agreement with the data. In this approach, one does not assume from the start that ecological communities are high-dimensional. Indeed, the fundamental question now becomes: What is the minimum necessary dimensionality of the theory required to characterize a given ecological community to a desired level of realism and precision? The hypothesis of functional equivalence is the cornerstone of neutral theory. It states that trophically similar species are, at least to a first approximation, demographically identical on a per capita basis in terms of their vital rates, of birth, death, dispersal – and even speciation. Elsewhere I have also used the term symmetry to describe such species (Hubbell 2005). Under the hypothesis of functional equivalence, species can still differ in a great many ways – including characters that enable taxonomists to recognize them as good species – so long as species do not differ in their per capita vital rates. All species in all trophically defined communities violate this assumption to some degree, but the question is, how good an approximation is it? In ecology, there are often multiple, sufficient explanations for the same phenomenon (Chave, Muller-Landau & Levin 2002; Purves & Pacala 2005), and this is especially true of approximate explanations. The strategy of neutral theory relies heavily on Occam's Razor; but whether the assembly rules of ecological communities in nature obey this maxim – to always choose the most parsimonious explanation – is not yet clear. However, as Harte (2003) pointed out, one doesn't necessarily discard theories just because they are just approximations. Physicists still use Boyle's Law, PV = nRT (pressure P times volume V is a linear function of absolute temperature T), even though there are no perfect gases that follow this relationship exactly. Similarly, we continue to teach the Lotka–Volterra equations in ecology, even though no ecologist today would defend them as precise or mechanistic descriptions of nature. Much has been written about the unified neutral theory (UNT) since my book appeared (Hubbell 2001), some of it critical, and there have been several major technical and conceptual advances in the theory since then (e.g. Volkov et al. 2003; Vallade & Houchmandzadeh 2003; Houchmandzadeh & Vallade 2003; McKane, Alonso & Sole 2004; Etienne & Olff 2004). However, my main focus for this forum on neutral theory will not be on the new developments in the theory or on the criticisms. Rather, I wish to highlight the empirical observations that led me to question my own long-held beliefs about the assembly rules for ecological communities in the first place, particularly in plant communities. Before discussing these observations, however, I should sketch out a few of the major milestones in the intellectual history of the classical paradigm of competitive niche assembly theory. Since Grinnell (1917), and more formally since Hutchinson (1957, 1959), ecologists have sought a theoretical framework for the ecological niche concept that would be both necessary and sufficient to explain the coexistence of species having particular suites of traits in ecological communities. Early on, Gause (1934) put forth the central tenet of niche theory in his competitive exclusion principle, which states, paraphrased, that no two species with identical niches can coexist indefinitely. Gause tested this idea by fitting the celebrated Lotka–Volterra equations of two-species competition to the dynamics of competitive exclusion in laboratory populations of Paramecium. From Gause's day onward, the discussion of coexistence and community assembly rules has been framed almost exclusively in terms of competition, despite numerous but largely unsuccessful attempts to broaden the discussion to include additional mechanisms. Gause's principle implied that there must be a maximum tolerable overlap in the use of shared resources for two species to coexist or, in other words, there should be some limiting similarity between the niches of coexisting species (Hutchinson 1959; MacArthur & Levins 1967; MacArthur 1970). The principle also implied that competitive exclusion should be a commonplace observation in nature, or at the very least, that there should be widespread evidence of character displacement in resource use when very similar species co-occur. The empirical evidence, in general, has not borne out these predictions (Grant 1972, 1975), particularly in plant communities. There are only a few well documented examples of character displacement, all of which are in animals; for example, the evolution of beak size in competing Darwin's finches (Grant 1986), similar niche separation in seed-eating sparrows (Pulliam 1975) or in body size in desert rodents (Brown 1975). Most of these cases involve low-dimensional resource competition. However, I know of few examples of proven character displacement in plants, and the list of species whose actual disappearance from a community can be attributed to competitive exclusion is vanishingly short. Hutchinson's (1957) niche hypervolume was a more general concept of niche than one defined solely by limiting resources, and included, for example, the tolerance ranges for physical variables of the environment. His ideas about the fundamental and realized niches invoked competition to explain why species only occupy a subset of the niche space that would be suitable for them in the absence of competitors. However, if niches evolve, and if species are always restricted to smaller, realized niches in equilibrium communities, then how do we explain the persistence of adaptations for parts of fundamental niche space that are never occupied? I will return to this question shortly. The theory for community assembly based on the competitive niche paradigm became highly developed, first with multispecies community matrix theory (Levins 1968), which was developed on the foundation of the Lotka–Volterra equations, and then with more mechanistic theory, which explicitly incorporated the dynamics of resource supply and consumption along with the dynamics of the resource-dependent consumer species (Tilman 1982, 1987). This resource-based theory gave new impetus to testing community assembly rules through direct experimental manipulations of resource availability, most notably in plant community ecology. Perhaps the most significant conceptual spin-off of resource-based theory, however, was broader recognition of the fundamental importance of physiological and life history trade-offs (e.g. Tilman 1982, 1988; Kneitel & Chase 2004). In resource-based, or so-called R* theory, trade-offs occur everywhere because they are essential for coexistence. For example, in two-species competition for two limiting resources, stable coexistence happens only when each species has a higher break-even (R*) requirement for that resource which most limits its own growth, which represents a trade-off in the ability to exploit the two resources. The importance of trade-offs in resource use led Tilman (1994) to consider trade-offs in other life-history characteristics besides those involving resource exploitation, and here additional problems with the classical paradigm began to surface. In particular, Tilman revisited the old fugitive species concept of Hutchinson, and showed theoretically that if there was a strict transitive trade-off between competitive ability (site tenacity) and dispersal ability then, in principle, any arbitrary number of species could coexist. However, soon thereafter, Hurtt & Pacala (1995) showed that Tilman's trade-off assumption could be relaxed and that species of arbitrary competitive and dispersal abilities could coexist if dispersal and recruitment limitation were sufficiently strong. Hurtt and Pacala defined dispersal and recruitment limitation as the failure of species to reach and/or establish in all sites favourable for their growth and survival. When dispersal was infinite, such that all species reached all sites, then the best competitor won each site for which it was superior, the equilibrium solution expected from the classical theory. However, when dispersal and recruitment limitation were strong, many sites were won by default by competitively inferior species because the best competitor for the sites failed to reach them. Although the coexistence produced by this mechanism is non-equilibrium, Hurtt and Pacala showed that competitive exclusion could be essentially infinitely delayed. This result meant that Gause's competitive exclusion principle was not generally true in spatial ecology. The slowness to reach equilibrium also depended on species richness. The more species there were in the community, the stronger dispersal limitation became, and the slower the approach to equilibrium. The elimination of species by competitive exclusion is so slow, in fact, that all it takes to balance species loss and achieve a true long-term equilibrium in species richness and relative species abundance is to incorporate a very slow rate of introduction of new species (i.e. speciation) (Hubbell 2001). The idea of assuming functional equivalence as a theoretical point of departure in community ecology is not particularly new, particularly in plant ecology (Hubbell 1979; Goldberg & Werner 1983; Shmida & Ellner 1984). Neutral theory assumes functional equivalence at the entire community level, but this is much broader than is typically assumed by ecophysiologists and ecosystem ecologists when they aggregate similar species into functional groups (e.g. Reich, Walters & Ellsworth 1997). Recognizing functional groups implies that niche differences among these groups are believed to matter to the assembly, stability and resilience of communities to disturbance (e.g. Loreau, Naeem & Inchausti 2002), although their quantitative importance remains controversial (Hubbell 2005). However, the literature on functional groups has been remarkably silent about the assumption of species equivalence within functional groups, which flies squarely in the face of classical niche theory. Perhaps this silence is because the idea of functional groups largely emerged from the ecosystem perspective, which traditionally has not been focused on species-level questions. There has also been very little discussion about the selective regimes that would lead to the evolution of functional equivalence within functional groups (Hubbell & Foster 1986b; Hubbell 2005). As a result, there is not much development of theory in community ecology for the assembly of functional groups. Does a limiting niche similarity for species in functional groups exist? How many coexisting species can be packed into a functional group? I believe that the answer to the first question is no (at least in plants), and the answer to the second question is essentially arbitrary (again, at least in plants). Loreau (2004) has recently argued that functional equivalence does not really exist. However, in a companion paper (Hubbell 2005), I demonstrate that functional equivalence can evolve easily and often, under selective circumstances that should be commonplace in nature, especially in species-rich communities. My ideas on functional equivalence have developed slowly over the past quarter century. Since 1980 my colleagues and I have been studying the dynamics of a large (50 ha) mapped plot of old-growth tropical forest on Barro Colorado Island (BCI), Panama, attempting to understand the assembly rules of the BCI tree community (Hubbell & Foster 1983). The BCI Forest Dynamics plot contains a little over 300 tree and shrub species and 230–240 thousand stems, depending on the census, with a stem diameter of at least 1 cm at breast height (d.b.h). Details of the BCI plot and the dataset are now well known, and the research design has now been replicated in a pantropical network of plots (Condit 1998). However, I will confine my discussion to the BCI findings because the BCI dataset is the oldest, having now been censused five times. The first observation about the BCI tree community is that there appears to be single dominating axis of niche differentiation, organized by variation in light and its distribution in the forest, that can be well characterized by a trade-off between under and maximum growth rate in (Hubbell & Foster The of this or life history are on one by species that have in but growth rate in and on the other by species that have in the but have very relative growth in only at species at the of the life history one can different functional of some of one of the is the functional and the other is by the competitive functional the generally have good dispersal are and but also have life and to and the competitive on the other typically have dispersal and are of light but are generally slower in and they have life with and with generally higher to and axis of life history among BCI tree species is in to light represents the mean of a single species. at the are species with in but relative growth rate in as a of stem at the are species that mean relative growth in but mean in the of species at the of the such as this are as evidence for a trade-off between and growth However, these mean significant variation in and growth Hubbell & Foster this however, we that the of species these are very There are very many more species in the BCI forest than species. also that that there is no life history these two into functional groups. In fact, there is a of species between the There is also a in the characteristics of BCI tree species in terms of of stem size and et al. In general, the mean abundance of species also with an in the of be with niche theory, but it is not to do of in the of the life history there are many species that are virtually in their tolerance and relative growth rates. this of species at the is to be by niche theory, then one must with a for why niches are more under than under there is a limiting niche similarity in these functional traits, then it is not at all my of these are more by an I believe that species are to the of traits that them for growth and under the of how many other species are the same This has the of species to on similar given are by their different et al. one possible mechanism to explain the hypothesis of & which that species with similar niche are into similar to this the of species in such as BCI is a of the of over relative to From this perspective, what really the species richness of and species in a particular tree community is the richness of the species and the abundance of and in the over long of This then has a on in a community such as of this is that in the disturbance a in the abundance of species, but it will have a on the number of species that are history of this in classical niche theory is expected to lead to a loss of species through competitive but there is no evidence to that this is among BCI species. I believe that two major are at that competitive The most is the of dispersal and recruitment There is evidence of dispersal and recruitment limitation in the BCI tree community (Hubbell et al. et al. and it is even in the best with few et al. The evidence for dispersal and recruitment limitation from a long-term of into a network of the BCI with of a now in its consider dispersal the first of the only of species to at least one to or more of the and more than of the tree species were in five or in years (Hubbell et al. The only species in the BCI forest with a are the but even these species have only dispersal in space and Most within of the and of most species for only The one be an species to a of its long et al. for dispersal limitation among species in the BCI forest, over a which were and from the BCI species to over of the in a and of all species into five or this Hubbell et al. there is recruitment which is also very strong. et al. in the plots to each and in the to in all species that sufficient to et al. the of by the of the of the number of on the number of of the same species into the of would All of the were and many were so that the were absolutely for recruitment represents the of the of number of number of of the same species in the over all in the BCI of would no However, the for all species were in the was so in a of the species that the of the relationship between in to out were these species absolutely more in sites more were et al. The importance of these findings for the discussion is that dispersal and recruitment limitation are sufficiently to competitive exclusion among species whose life history traits the same or very similar adaptations for the most in the have not yet developed a forest for BCI that the but models incorporating dispersal and recruitment limitation are of arbitrary of species of & Pacala Hubbell 2005). this niche point out if is in the of species this is a broader of niche competition that interactions with Indeed, Chase & Leibold (2003) that is a of I have no with but this of niche is not the classical it is not how could character The is by such as the of competition shared In the of BCI species, most of the in the is et al. However, in of to is not required in for recruitment limitation to be in species coexistence. which limits recruitment – even a – will the of species to sites by of species The second competitive exclusion of species is the of the and by of each species. years ago, we the hypothesis that in species-rich communities, the for character displacement among a large number of competing species would be of many competing species would lead to on the of and (Hubbell & Foster in the BCI tree community on there were species in the of each and that on only of the species in their This is to the about life-history on the most then, the concept of dispersal and recruitment limitation was not in the theoretical but such limitation is one of the main why are not this hypothesis is then the long-term and growth of should be of the species of their with the of tested this hypothesis on years of growth and on BCI species. few the species of the was or significant (Hubbell et al. et al. 2004; et al. 2005). This result that the of by competition at the level of virtually every There is little or no in the of at the species level to character displacement in one or the for beak in Darwin's I that this is a major that tropical such of variation and & would that most BCI species are and this does to be the (Hubbell & Foster et al. 2001). the species of For example, consider the variation in growth among of the The variation in growth in this single species virtually the entire of growth of both the and the functional this we how much of this variation is but it does that there be problems with species-level trade-off between and growth rate that we ecologists have argued that such and implies that ecological communities are very (e.g. et al. 2001). However, if species overlap because the is far than the then such as neutral theory, not be such a approximation to of the in growth of the species, represents a of that were cm in that the The of years was from cm a tree that at all to a of cm This in just the entire of variation in growth the entire BCI tree community, including species. This is not and that BCI overlap in the distribution of their vital rates. It that the concept of limiting similarity has little to traits of BCI also the trade-off to The hypothesis of functional equivalence can only be so but the main point of this paper is that there are both empirical and theoretical for taking the hypothesis at least in the tropical tree communities I have It is almost the that the hypothesis will to some communities and functional groups than I it will be often true in communities of but this question will be for the on those communities to What to however, is how far one can with a neutral theory based on the assumption of functional Although have that theories can also many of the same to me this is not the main point of neutral theory. – but also more complex – theories to the if the what or is me the most and question of all is why neutral theory as well as it given the it For neutral theory has been a conceptual because it is a theory of that from fundamental in For example, it is both and that one can the most of species et al. very and from the theory et al. 2003), and that this number out to be to the It is this that my that neutral theory is fundamentally true about the aggregate of on will if my is