Download Niche-Based vs. Neutral Models of Ecological Communities

Biology and Philosophy (2005) 20:557–566
DOI 10.1007/s10539-005-5583-7
Ó Springer 2005
Book review
Niche-Based vs. Neutral Models of Ecological
Communities
GREGORY M. MIKKELSON
Department of Philosophy and School of Environment
McGill University
855 Sherbrooke Street West
Montréal, Québec H3A 2T7
Canada
E-mail: [email protected]
A review of Jonathan M. Chase and Mathew A. Leibold, Ecological Niches:
Linking Classical and Contemporary Approaches, University of Chicago
Press, Chicago, IL, 2003, 212 pp., (Hb) ISBN 0-226-10179-7, $50.00, (Pb)
ISBN 0-226-10180-0, $20.00.
“The niche” has served as a conceptual foundation of ecological science for
nearly 100 years. It has played an especially important role in explaining
species coexistence. For example, the “competitive exclusion principle”
states that no two species can occupy the same ecological niche. If they did,
one of them would out-compete the other, i.e., drive it locally extinct. Thus,
only species with sufficiently differentiated niches may coexist within the
same ecological community.
Hubbell (2001) and others have recently bucked this explanatory tradition. Competitive exclusion, they say, often takes so long to occur that
other processes – i.e., speciation, dispersal, and “random ecological drift”
in population size – come to dominate. In Hubbell’s “unified neutral theory
of biodiversity and biogeography”, niche differences are irrelevant for
explaining why certain competitors do, but others do not, coexist. Hubbell
conceived this theory in close analogy with Motoo Kimura’s neutral theory
of evolution by genetic drift. In the latter, functional differences (e.g., leading
to heterozygote advantage) are likewise irrelevant for explaining why certain
alleles coexist in the same gene pool.
In their new book, Jon Chase and Mathew Leibold define, demonstrate,
and defend “contemporary” niche theory. They contrast this contemporary
theory with the older “classical” niche theory based on Lotka-Volterra
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competition equations, and with the newer neutral theory. But they devote
the bulk of their book to unifying empirical knowledge within their preferred
niche-based framework. In this project, they achieve remarkable success.
Anyone interested in the current state of ecological science, and how that
state relates to past developments, would thus do well to read it.
Nevertheless, Chase and Leibold do not confront the neutralist framework
as directly as they might have. Because of this, I shall argue, they overlook what may be the most powerful arguments in favor of niche-based, and
against neutral, models of ecological communities.
Trade-offs, “chance”, and competition
The first conceptual move in the book is to define “niche” in terms of two
components: “the requirements of a species for existence in a given environment and its impacts on that environment” (p. 2; italics added). This way
of analyzing the niche concept sets Chase and Leibold apart from previous
commentators (e.g., Schoener 1989; Colwell 1992; Griesemer 1992). The
latter emphasized other dichotomies, such as whether niches are properties of
species or environments. As we shall see below, the requirements vs. impacts
dichotomy does prove to be enlightening – quite a bit more so, in my opinion,
than previous analyses of the niche concept.1
The rest of “Chapter One: History, Context, and Purpose” traces each
niche component back to the ecologist(s) who first emphasized it, and sets
the stage for considering how requirements and impacts interact to determine
whether a given set of species may coexist in a given ecological community.
In “Chapter Two: Revising the Niche Concept”, Chase and Leibold deliver
the main thesis of the book. A wide variety of ecological phenomena, they
say – ranging from evolutionary changes within single species to ecosystem
functions mediated by large numbers of species – can be explained in terms
of just two niche axes. A niche axis is a particular resource, predator, or
“stress agent” that both affects and is affected by the (possibly many) species
of interest. Exactly which two niche axes dominate, differs from ecological
community to ecological community. But
while there are always a multitude of environmental factors that interact
simultaneously . . . many of these factors can reasonably be considered as
background within a given environment, so that one or two factors are of
primary importance in any given situation. (p. 30)
Chase and Leibold’s two-axis framework proves to be quite versatile.
In Chapter 2, they introduce several of the most commonly-invoked pairs
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of niche axes. They devote most of their attention to “resource competition”, or competition for two different resources; and “keystone predation”,
competition for a single resource while suffering predation by a consumer.
But elsewhere in the book, they discuss many other two-axis combinations.
In Chapter 2 and throughout the book, Chase and Leibold focus on
criteria for the coexistence of two or more particular species at demographic
equilibrium. By “demographic equilibrium”, I mean a hypothetical state in
which the populations of all species remain constant. In other words, within
each population, the number of births (plus immigrants) equals the number of
deaths (plus emigrants). This focus differs crucially from that of the neutral
theory, which denies that communities ever reach demographic equilibrium –
even hypothetically. The neutral theory posits equilibria at three higher levels
instead:
(1) Between the sum, over all species at a given site, of births-plus-immigrants and deaths-plus-emigrants (the “zero-sum” postulate);
(2) Between colonization-plus-speciation and local extinction at a site; and
(3) Between speciation and global extinction among all sites.
The other key point of divergence is that niche theory considers differences between the niches of different species to be essential for explaining
which species coexist – whether actual populations ever reach equilibrium
or not. In particular, “[S]pecies must show trade-offs in order to coexist
. . .” (p. 41). In other words, if one species is better than another species,
at something like procuring a certain resource, then it must be worse at something else, like defending against predators. Otherwise, the first species would
competitively exclude the other.
The neutral theory, on the other hand, considers niche differences to be
irrelevant. In a jiu-jitsu-like move, Hubbell (2001) implies that he would not
disagree with Chase and Leibold’s claim, quoted in the last paragraph. Rather,
he considers trade-offs to be so rampant that any two species (within the
same general trophic category or “guild”) could potentially coexist. Niche
differences cannot explain, then, why only certain species coexist at any given
location. The neutral theory explains coexistence as the result of “chance”,
along with historically-contingent initial population size.
The notion of chance invoked by Hubbell (2001) is the one most famously
associated with Laplace (Gigerenzer et al. 1989; Eble 1999). Laplace was, of
course, an arch determinist. But in situations where causes interact in complex
ways, he countenanced, and even pioneered, the use of indeterministic
mathematical models. Hubbell has done a great service to ecology, by introducing a probabilistic approach that goes far beyond the impoverished “null
models” that previously bogged ecology down in decades of debate (Cooper
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1993; Sloep 1993; Mikkelson 1997). However, as we shall see, he and other
neutralists cannot really have their cake (trade-offs) and eat it too – that is,
treat the organisms of different species as ecological equivalents, each having
an equal probability of survival and reproduction.
Chase and Leibold do not acknowledge the above argument of Hubbell’s
(2001). However, they do suggest one reason why it won’t work. Niche theory
predicts that if two species trade off in their performance relative to two niche
axes, then each species should tend to increase when rare. In other words, if
one species is reduced below its equilibrium abundance, it should enjoy a
per-capita competitive advantage over the other species, until both populations re-equilibrate to their previous levels. This ecological phenomenon is
analogous to the maintenance of genetic diversity by frequency-dependent
selection. Despite Hubbell’s professed belief in trade-offs, his neutral theory
rules out any per-capita competitive advantage for rare species – just as
neutral evolutionary theory does not allow for frequency-dependent (or any
other kind of) selection.
A tendency for species to increase when rare, then, would constitute
evidence for niche theory and against neutral theory. Such a tendency would
also lengthen the expected time over which competing species coexist,
relative to the time predicted by the neutral theory. Thus, the presence or
absence of trade-offs would seem to constitute a crucial test after all, for
deciding between niche and neutral theory.
Another potentially crucial test involves a difference in scale. While the
neutral theory denies niche differences an important role at any density
or scale, Chase and Leibold posit an intriguing contrast between the local
and regional scales. According to their theory, differences between both
the requirement- and impact-components of the niche play critical roles in
determining who can coexist with whom in local communities. However,
differences in requirements alone govern coexistence across entire regional
landscapes. Evidence for such a contrast between scales, then, would again
tell in favor of niche, and against neutral, theory.
To sum up, Chapter 2 sets out the main claim of Chase and Leibold’s
version of contemporary niche theory, and suggests two ways of testing it
against neutral theory – though not as explicitly as might have been hoped.
One other problem with this chapter is that there appear to be same typographical errors in its discussion of the technical criteria for coexistence.
On a more positive note, Chase and Leibold rely heavily, and explicitly, on
graphical representations of algebraic models. This emphasis on graphical
tools contributes greatly to the lucidity of their presentation.
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Mechanisms: What are they good for?
“Chapter Three: Comparing Classical and Contemporary Niche Theory”
does exactly what its title asserts. Contemporary niche theory is more
“mechanistic” than “classical” niche theory based on the relatively more
“phenomenological” Lotka-Volterra (LV) equations. To wit, contemporary
niche theory gives more detail about how species compete, rather than simply
indicating the strength of competition via LV “competition coefficients”.
Tilman (1982) pointed out that contemporary niche theory achieves this
increased level of detail, without incurring any greater complexity than the
LV equations.2
Chase and Leibold imply that this increased level of detail about
mechanisms somehow makes the results of contemporary niche theory more
generalizable than those of classical niche theory. This belief seems to be
widespread among ecologists (see, e.g., Tilman 1987). However, I have never
seen a decent argument on its behalf. Since competition between species
can be realized by indefinitely many different mechanisms, why would the
most generalizable approach not be to study the causes and consequences of
competition in general, rather than to worry about the particular niche axes
that underlie specific instances of it?
However, mechanisms may have other advantages. Sterelny and Griffiths
(1999) and Mikkelson (2004) suggest that discovering a plausible mechanism
for a given phenomenon helps to confirm the existence of that phenomenon.
Plate-tectonic mechanisms of continental drift are perhaps the most obvious
example. The discovery of mechanisms can also help to unify our understanding of different levels of organization – especially since the mechanism
for a phenomenon at a given level can just as easily involve higher as lower
levels of organization (Darden 2000; Mikkelson 2004).
In “Chapter Four: Designs and Limitations of Empirical Approaches to
the Niche”, Chase and Leibold demonstrate a third advantage of mechanistic
niche theory: its ability to bring fascinating aspects of natural history to light.
For example, it turns out that among “damselflies . . . [s]pecies of the genus
Ischnura are uniformly superior resource competitors to those of the genus
Enallagma, whereas those of the genus Enallagma are better at avoiding
predators by having lower activity rates.” However, “within the genus
Enallagma (the genus less susceptible to predators), some species are better
at living in lakes where dragonflies are the top predators, while other species
are better at living in lakes where fish are the top predators . . .” (p. 67).
Chase and Leibold’s discussion of this example also hints at the eventual
integration of niche and neutral theory. As Hubbell (2001) points out, such
an integration would recall the reconciliation of genetic drift and selection in
contemporary population genetics.
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McPeek and Brown (2000) have still found there to be more species
per habitat type than this scenario would predict. Thus, there may be
still finer-scaled differences among these species, such as their abilities
to deal with stochastic variance, habitat selection, or complexities due
to their stage-structured life histories . . . Alternatively, regional-scale
patterns of metacommunity interactions could also affect the observed
local-scale diversity . . . Finally, McPeek (personal communication) has
argued that these species may be ecological equivalents whose coexistence may persist for long periods of time by a slow random walk to
extinction (sensu Hubbell 2001). (p. 68)
Chapters 5 and 6 extend the niche-theoretic analysis to cover both
biotic and abiotic “complexities”. “Chapter Five: Incorporating Biological Complexities” applies niche theory to such ecologically important
phenomena as long-distance migration (e.g., by birds and wildebeest), and
individual plants’ allocation of biomass to roots vs. leaves. “Chapter Six:
Environmental Variability in Time and Space” makes good on the claim that
“models that assume that there is an equilibrium are still relevant to systems
that are in disequilibrium” (p. 95). For example, one strategy for dealing with
environmental variability is to treat it as a separate niche axis. Often, species
that are better at competing for a given resource, when it is supplied at a
steady rate, are worse at competing for it when levels of that resource undergo
marked fluctuations.
In “Chapter Seven: Species Sorting in Communities”, Chase and Leibold
shed light on various aspects of a venerable topic in ecology: how species
are distributed across environmental gradients. However, they also admit that
many of the relevant phenomena are “likely to be influenced not only by
local conditions . . . but also by patterns of dispersal limitation and other
biogeographical processes. Thus, the theories we have discussed above are
inadequate to fully explore this situation” (pp. 116–117).
This problem raises the following question: why not treat dispersal ability
as yet another niche axis? In general, the dispersal of a species into a new
community has more of an effect on that community, than on the community
from which it came. To include dispersal ability as a niche axis would therefore deviate from niche theory’s traditional focus on species’ local impacts.
However, it does seem like a natural extension of contemporary niche theory,
to also treat the regional impacts of species in this way.
Biodiversity: Causes vs. consequences
“Chapter Eight: Community Succession, Assembly, and Biodiversity” brings
still more topics into the purview of contemporary niche theory, such as the
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“intermediate disturbance hypothesis” and the effects of productivity – the
sheer amount of living material, or biomass, produced per unit time and area
– on diversity, or number of species.
“Chapter Nine: Niche Relations within Ecosystems” reverses the causal
arrow, addressing, among other things, the influence of diversity on community biomass and stability. Charles Darwin (1859) asserted that communities
with more species tend to produce a greater stock of biomass. This
phenomenon is called “over-yielding”. Darwin’s contemporary, Herbert
Spencer, declared that more species-rich communities tend to be more stable
(van Emden and Williams 1974). However, only in the mid-1990s did
ecological experiments and theories come into close enough contact to firmly
establish, and to delve into the causes of, both these patterns. One result of this
recent activity is that, in order to make stability more empirically tractable,
it has been redefined as the mean, divided by the standard deviation, of total
community biomass in a given place over time (Lehman and Tilman 2000).
What Chase and Leibold should have pointed out is that the neutral theory
is incapable of explaining either consequence of diversity. For one thing,
the neutral theory tracks only the number, and not the total biomass, of
organisms. For another, it assumes that each community contains a fixed
total number of organisms – no matter how many species those organisms
represent. (This is the “zero-sum” postulate mentioned in the above section
on “Trade-Offs, ‘Chance’, and Competition”.) It is thus axiomatic that overyielding can never occur. Even more absurd, the neutral theory assumes that
communities never undergo any fluctuations in either the total number of
organisms, or their total biomass. Since all communities are thus maximally
stable, there cannot be any relationship – positive or negative – between
diversity and stability.
In contrast, niche theorists have come up with compelling explanations
for these relationships between diversity and “ecosystem function” (Kinzig
et al. 2002). Such relationships thus constitute a third crucial test of niche vs.
neutral theory. This test, unlike the two mentioned above in the section on
“Trade-Offs, ’Chance’, and Competition”, has already been performed, and
it refutes neutralism. However, the probabilistic framework developed by the
neutralists is too valuable to simply throw away. Rather, as I suggest below,
niche theorists should seek to improve it by incorporating niche differences
into it.3
“Chapter Ten: The Evolutionary Niche” further illustrates the remarkably
wide scope of contemporary niche theory. For example, Chase and Leibold
predict that species sharing both a key resource and an important predator
should diverge in order to avoid competing too closely. As they do, natural
selection will “act so that the consumer-prey phenotype that has greatest
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conversion efficiency for the basal resource . . . also provides the best food
for the predator . . .” (p. 167).
In the final chapter of the book, “Eleven: Conclusions”, Chase and Leibold
urge their fellow ecologists to learn more about the history of their discipline. They also face up to a limitation of contemporary niche theory, when
they admit that “the relative abundance of species . . . we have mostly
ignored” (p. 177). Along with its failure to account adequately for dispersal
(noted above), this may be the main weakness of contemporary niche theory,
compared to the neutral theory. Since explaining relative abundance is the
leading goal of the neutral theory, it is not surprising that it does better in this
respect.
Neutral theory, on the other hand, is powerless to explain such manifest
patterns as diversity-biomass and diversity-stability relations, and the distribution of mayfly species. It would be equally unable to account for some of
the other patterns predicted by Chase and Leibold, should those predictions
turn out to be true. Above, I mentioned a general tendency for species to
increase when rare, and the contrast between the importance of requirements
vs. impacts for local vs. regional coexistence.
The fact that niche and neutral theory have complementary strengths and
weaknesses could elicit either of two contrasting responses. One option would
be to limit each theory to the phenomena that it does best at predicting and
explaining. Another would be to aim at synthesis. The analogy with drift
and selection, along with comments by both Hubbell (2001) and Chase and
Leibold, strongly recommend the latter.
In the final chapter of his book, Hubbell (2001) discusses a few steps
toward synthesis that have already occurred. However, these efforts deal only
with the causes of diversity and relative abundance. More work is needed in
order to achieve a synthetic theory that accounts for not only these causes, but
also the consequences of diversity, such as increased biomass and stability.
The rich menu of conceptual tools and empirical insights, provided in Chase
and Leibold’s book, offers many prime candidates for inclusion in any such
theory.
Notes
1 Naeem (2003) concurs, calling the requirements vs. impacts dichotomy the true “genius”
of Chase and Leibold’s approach.
2 By “complexity”, I mean the standard statistical definition: the number of adjustable parameters. Forster and Sober (1994) and Mikkelson (2001) discuss philosophical issues involving
this kind of complexity.
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3 Lehman and Tilman (2000) illustrate just how easy it can be to turn a neutral theory into
a niche theory. They do so by simply adding one more “breakage” point along the “stick”
invoked in MacArthur’s (1960) neutral model of relative abundance.
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