Download Individuals, populations and the balance of nature: the question of

Biol Philos (2008) 23:417–438
DOI 10.1007/s10539-007-9106-6
Individuals, populations and the balance of nature:
the question of persistence in ecology
G. H. Walter
Received: 16 October 2006 / Accepted: 16 December 2007 / Published online: 16 January 2008
Springer Science+Business Media B.V. 2007
Abstract Explaining the persistence of populations is an important quest in
ecology, and is a modern manifestation of the balance of nature metaphor.
Increasingly, however, ecologists see populations (and ecological systems generally) as not being in equilibrium or balance. The portrayal of ecological systems as
‘‘non-equilibrium’’ is seen as a strong alternative to deterministic or equilibrium
ecology, but this approach fails to provide much theoretical or practical guidance,
and warrants formalisation at a more fundamental level. This is available in
adaptation theory, which allows population persistence to be explained as an epiphenomenon stemming from the maintenance, survival, movement and
reproduction of individual organisms. These processes take place within a physicochemical and biotic environment that persists through structured annual cycles,
but which is also spatiotemporally dynamic and subject to stochastic variation. The
focus is thus shifted from the overproduction of offspring and the consequent
density dependent population pressure thought to follow, to the adaptations and
ecological circumstances that support those relatively few individuals that do
survive.
Keywords Adaptation Autecology Balance of nature Density dependence Equilibrium Life cycle Pluralism Nomadic pastoralists Turkana Population regulation
‘‘Remember that the life of mankind is like the life of a man, a flutter from
darkness to darkness’’
Robinson Jeffers - The Torch-Bearers’ Race
G. H. Walter (&)
School of Integrative Biology, The University of Queensland, Brisbane, QLD 4072, Australia
e-mail: [email protected]
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Introduction
Although the balance of nature concept is central to a great deal of ecological
investigation and interpretation, it remains surprisingly invisible. And despite its
relevance, much about it has to be inferred (Cooper 2001). The concept may simply
have a low profile, as suggested by Cooper (2001), because it is unconsciously
concealed by the paradigmatic status it carries. Nevertheless, the argument about
ecological systems being balanced is surprisingly complex, and subject to ready
misinterpretation (Cuddington 2001). The issue of balance, or stability, is further
complicated in the diverse and subtle extension and amplification of the idea of
balance as one moves from its simplest application at the population level, to the
more complex communities and ecosystems through which ecological systems are
further conceptualised (see Grimm and Wissel 1997; Sarkar 2005).
Here I expand on recent debate about ecological balance and focus on issues as they
relate to populations in ecology, for resolution at this point will surely have
implications for interpreting the more complex areas of ecological theory. My primary
aim is to consider the basis of the conceptual alternative to the balance of nature
argument. At least two alternative concepts are available, one centred on the concept
of ‘‘non-equilibrium’’ and the other focussing on the adaptations for survival and
reproduction of individual organisms. Neither has yet been fully formulated and it
seems likely that the two are not incompatible with one another and can be unified.
Each of these approaches is outlined, their differences specified, and an approach to
unifying them into a stronger alternative theory to the balance of nature is expanded.
Formalisation—balance of nature and population equilibrium
The precise structure of the balance of nature concept is difficult to find in an explicit
statement. Cooper’s (2001) exposure and formulation of the concept, structured as an
‘‘argument’’, has advanced the debate considerably. Two general schemes that deal
with ecological balance are identifiable in the literature. The original one is more
restrictive, presumes a level of organization in ecological systems that is unlikely to be
there, and few would accept this argument as sound (called Argument I by Cooper
(2001)). It begins with the view that population density is constant relative to the
capacity for reproduction in organisms. Populations are therefore considered to be
rather tightly regulated through the prompt action of density dependent processes.
Populations persist because of such regulation, but population persistence itself is not
emphasised particularly. The problem with Argument I lies in its imprecision. How
much variability in population density would actually contravene the claim of ‘‘tight
regulation’’ (Hengeveld 1989; Cooper 2001; Sarkar 2005)? Nevertheless, this
particular view of populations is still invoked by environmentalists, whether scientists
or not, in justification of their attitudes and actions (as pointed out by Drury (1998),
Botkin (2001) and Cuddington (2001)).
The second Argument differs from Argument I mainly in its foundation
statement, about populations being relatively constant, and is outlined in Table 1.
Argument II asserts that persistence of populations is an ecological fact (e.g., Hixon
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Table 1 Cooper’s (2001) summary statement of the modified balance of nature argument (II in text)
Ideas in inferential progression
Comment
1. Persistence of populations is a fact
Replaces view that populations are constant
relative to the capacity for increase
2. Unregulated populations are destined to
random walk to extinction
Populations must therefore be regulated in the
‘‘stationary probability sense’’
3. Regulated populations must have an
equilibrium
Most populations must therefore be equilibrium
populations
4. Population regulation implies density
dependence must be the regulatory process
Most populations are under the influence of density
dependent processes
5. Biotic processes are the most likely
to impose density dependence
We should expect biotic forces to be important
determinants of population behaviour
et al. 2002). The population is present (i.e. persists) and must be regulated if it is not
destined to random walk its way to extinction (Cooper 2001). These views are more
likely to be representative of what most ecologists would currently accept, at least in
general terms. Cooper does emphasise, though, that the argument tends to be
implicit rather than explicit and it is not an argument in the logician’s sense; it does
not express premises that deductively support conclusions. Rather, it is a
constellation of mutually reinforcing ideas that have something of the character
of an inferential progression. The earlier lines in Table 1 do not guarantee the truth
of the statements that follow them but are considered to boost their plausibility.
Most population ecologists would recognise the views outlined above and would
also agree on how the concept of population equilibrium related to those views. They
are likely to see the equilibrium as the stable, positive value to which populations are
considered to return after disturbance, for that represents the balance or stability in
ecological systems. This, in more general terms, is the balance of nature. Such balance
is perceived also at other levels in the ecological hierarchy, namely the community and
ecosystem, and here the subtlety becomes even more profound, as explained by Sarkar
(2005). The perceptions of ecologists notwithstanding, equilibrium in ecology has also
been defined more strictly, in mathematical terms, and this perception is quite different
from the view of equilibrium outlined above. In population ecology we thus have two
concepts of equilibrium.
Equilibrium, in mathematical terms, is that state at which the net rate of change
in population density is zero (Cuddington 2001). Equilibrium thus encompasses
vastly more than a return to an average value, for equilibria may be stable or
unstable and extinction is a distinct possibility (Cuddington 2001). The mathematical formulation is, therefore, not a formalisation of the original balance of nature
metaphor and nor does it represent the more modern perception of ecological
equilibrium (Argument II). Practising ecologists evidently do not use it as a basis for
their investigations. They are clearly driven primarily by the ecological or
metaphorical views of equilibrium to investigate and interpret ecological systems.
They do so mainly in relation to potential density dependent processes that are
considered responsible for returning populations to a positive average (or
equilibrium) value. Also, ecologists apply the metaphorical balance concept, in
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conservation and pest management for example, to promote the re-establishment of
an orderly and pristine form of self-regulation in ecological systems (see Drury
1998; Botkin 2001; Cuddington 2001). Although the mathematical concept of
population equilibrium embodies a diversity of possible dynamics and outcomes, it
is routinely conflated with the metaphorical concept of balance, perhaps because it
is associated mainly with the models of Lotka and Volterra, in which population
density plays such a central role. Conflation of the mathematical and metaphorical
concepts of equilibrium is evidently obstructive of theory development and seems to
give the mistaken impression that the balance of nature argument in ecology is more
sophisticated than its current development suggests (Cuddington 2001).
Arguments against a balance of nature, and the nature of ecological theory
Many ecologists have questioned the validity of the balance of nature argument. The
debate has been long and often heated. Disagreement has been aimed not only at the
observable fluctuations in natural systems relative to the claims of balance, but also
at the equilibrium models themselves. Most of the heat, though, has been generated
in considerations of the processes postulated to maintain populations at levels that
ensure their persistence. These processes relate to the ways in which populations are
considered to return to equilibrium, whether metaphorical or mathematical. If such
density dependent processes are not effective in regulating populations, both the
mathematical and metaphorical concepts are presumably brought into question.
Although the promulgators of the original equilibrium equations were aware of
their limitations (Scudo 1971, 1991), the ecologists who followed them were far
more liberal in their application of the mathematics to ecological systems and to the
metaphorical impression of the balance of nature. The lack of realism in such
extrapolations has been comprehensively itemised and criticised by Andrewartha
and Birch (1954) and Heck (1976), among others. The logistic equation, for
example, underpins the deterministic predator–prey and competition equations. It
was, however, not the only option, or even the best option, for modelling S-shaped
population growth curves (Pielou 1974). Such a revelation has had far less impact in
ecological theory than one would have imagined, for the logistic equation still
represents the core assumptions of modern population equilibrium theory, including
metapopulation theory (Hanski and Gilpin 1991).
The persistence of the logistic is surprising, considering also that its principal
weakness is that it is not derived explicitly from the biological properties of the
individual members of populations (Lomnicki 1987). Its longevity may be partly
explained, however, by the powerful hold of the regulation argument, for regulation
‘‘… seems to be required for the possibility of general ecological knowledge’’
(Cooper 2003, p. 94). When this perspective is combined with the suggested
replacement theory essentially being a simple denial of the regulation argument (i.e.
non-equilibrium), the hold seems to intensify (see Cooper 2003, pp. 93–94). This
point is expanded next, and the rest of this manuscript is dedicated to converting this
denial into a positive explanation based on the ecological role of adaptive
mechanisms.
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The alternative to the balance of nature concept that is most commonly promoted
embraces the view that ecological systems are in a state of non-equilibrium.
However, ‘‘non-equilibrium’’ does not provide an obvious alternative to the notion
of equilibrium. When ecological systems are defined in this way, in terms of what
they are not, one is implicitly taken back to the point of departure, meaning that
ecological systems are again interpreted only in relation to the equilibrium that is
simultaneously being denied. Furthermore, the mathematical formulation already
encompasses dynamics that are unstable, even to the point of extinction (e.g.,
Cuddington 2001). At this point, though, it is perhaps better to put the mathematical
concept aside in considering ecological systems, for that approach was coopted from
physical chemistry. It is essentially a research tool, being a mode of analysis for
examining complex phenomena (Cuddington 2001) rather than a foundation
statement about the nature of ecological systems. The mathematical concept does,
however, reflect the primary significance given to population density and can be put
aside here also for that reason. Consequently, the concept of non-equilibrium, as
now used widely in ecology, relates primarily to the balance of nature argument
expressed in Table 1.
The debate about the ecological significance of density dependence has been
intense and is likely to continue. Several ecologists have seen nothing in the
evidence available to them to support the view that density-influenced feedback
keeps populations in a regulated state. Such effects seem far too sporadic, localised
and weak to be ecologically influential (e.g., Andrewartha and Birch 1954, 1984;
den Boer 1968, 1982, 1990; White 1969, 1993, 2001, 2004; Strong 1984, 1986,
1989; Cronin and Strong 1994; Wolda et al. 1994; Chitty 1996; den Boer and
Reddingius 1996). Although strong proponents of density dependence persist, nonequilibrium views and interpretations seem to be gaining ground (e.g., Rohde 2005;
Sarkar 2005).
The ideas related to population regulation were originally developed to represent
ecological dynamics at a local level, simply because early demographic ecology was
based on the premise that ecologically significant processes (seen to be mainly
competition, predation and parasitism) acted locally, to the extent that historical,
stochastic and migratory influences could be ignored (e.g., Kingsland 1985). This
view was consistent with Nicholson’s (1954) metaphor of a steam engine governor.
Local population increase was seen to generate local density feedbacks. However,
ecological processes operate at much more extensive spatial scales, even in those
ecological systems that were chosen for research specifically because they seemed
closed off to immigration or emigration (e.g. Forbes’ lake microcosm and the
Whytham wood winter moths (see Walter 2003, pp. 104, 244)). Such ‘‘leakiness’’ in
terms of organismal movement has provided an insurmountable problem to
population regulationists. Admittedly, this problem faces ecologists of all persuasions, and theory must be developed to take account of such circumstances. They
cannot be ignored for convenience.
In some ways the sting has been removed from the density dependence debate by
the weakening of the once strong link between population regulation and density
dependence. Population regulation has simply been redefined rather vaguely, in
Argument II, as the persistence of populations (Cooper 2001), and erratic population
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dynamics have been attributed to the deterministic process (density dependence)
simply being disrupted by chaotic inputs (Hassell et al. 1989). Such a relaxation
opens the way for pluralism in ecological interpretation, a feature that has been
welcomed in many quarters (e.g., Schoener 1986; Aarssen 1997; Paine 2002).
However, pluralism can bring attendant dangers in that the adjusted theory seems, in
practice, to promote as acceptable virtually any claim about the importance of
ecological processes. Any ecological ‘‘factor’’ can now be important, here or there,
and now or later. No yardstick is available for judging the validity of claims, and the
ecological interpretation of research results essentially becomes descriptive and
loses its analytical basis.
More problematic, though, is that this approach seems to remove any focus from
theory and places it on empirical research and context-specific mathematical models,
whereas all of these aspects are required. These various components, as well as the
diverse aims of models, have been disentangled by Cooper (2003, 160ff.), who
emphasises the tool-like utility of the mathematical models that are increasingly used
by ecologists. A diversity of such tools, applied in novel ways, is clearly desirable to
analyse particular problems. So, too, is a diversity of experimental and analytical
approaches. However, the significance of ecological questions, data and interpretation
inevitably requires a context. And a valid context for analysis, interpretation and
synthesis can be provided only by a theoretical underpinning (e.g., Chalmers 1999, p.
207). For such theoretical support, the pluralism advocated by ecologists to date would
almost inevitably fall back, by default, on the theory currently associated with
population regulation and density dependence. The guidance of theory is unavoidable
at times, although it must inevitably be adjusted or replaced, for ‘‘The practising
biologist must keep track of a dynamic inventory of theories, models, and data that run
deep in detail and broad in their interconnectedness’’ (Castle 2005, p. 203). The call for
pluralism therefore needs to be treated with caution.
The nature of general theory in ecology is seldom discussed, but frequently
implied. Most commonly it is hoped, or anticipated, that ecology will be able to
develop generalised statements that encapsulate how organisms of type X will
respond to particular environmental circumstances in Y fashion (e.g., Orians 1962;
Lawton 1999). The expectation of accurate prediction is strong, and the pathway to
prediction clear. General rules, even ‘‘contingency rules’’ (Lawton 1999), are
believed to be intrinsic to ecological systems, and within reach. For example, the
search for global pattern (not just geographical pattern) in macroecology (Ricklefs
1989; Lawton 1999; Blackburn and Gaston 2006) derives from such a premise.
Essentially, the views are deterministic and reflect a belief that ‘‘equilibrium
principles’’ in some form will hold in ecological systems.
Another problem for ecological theory is that species, in ecological terms, behave
‘‘idiosyncratically’’ in relation to the expectations of equilibrium theory, most
noticeably in community ecology. Not only do stochastic influences frequently
impinge on ecological systems and disrupt the expected patterns but, more
significantly, species have idiosyncratic species-specific adaptive mechanisms with
which they confront the world. They are almost invariably adapted to particular
subsets of the features and conditions within any particular environmental setting,
with different species in the area invariably being adapted differentially in this
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regard (Hengeveld 1990; Walter 1995; Hengeveld and Walter 1999; Walter and
Hengeveld 2000). The population consequences of these mechanisms that sustain
organisms within the environment are explored further in the Section ‘‘Individual
organisms, adaptive mechanisms and population persistence’’.
Given that species are ‘‘idiosyncratic’’ as specified, the most effective way to
generalise about their ecology requires broad ecological statements that hold across
species at a basic or relatively deep level. They should inform in general terms as to
how individual organisms of all species interact with their environment at different
stages of their life cycle. This, I believe, is the overarching aim of Andrewartha and
Birch’s (1954) approach to understanding the dynamics of where a species occurs in
nature and its local abundance. They, however, made no comment about the
philosophical nature of their general method, besides specifying a three-stage
research approach (Andrewartha & Birch 1954, p. 10).
Autecology interprets the distribution and abundance of organisms in relation to
the way in which individual organisms of a species interact with key aspects of their
immediate environment (biotic and abiotic in combination) through their speciesspecific adaptations (Hengeveld and Walter 1999; Walter and Hengeveld 2000). The
shifting patterns of organismal abundance across localities is influenced primarily
by the spatiotemporal structure and dynamics of the external environment, which is
mainly under the influence of climate. The resultant survival and reproductive rates
set local patterns of abundance, although this is influenced by predation and other
such influences at times. Autecological theory will clearly not provide the sorts of
generalisations anticipated from equilibrium theory, as described above. No lawlike regularity can be expected in the way in which particular types of organisms
will respond to particular ecological situations, not even at the level of specific
higher taxa (e.g. insects as opposed to birds). Rather, autecological theory is
expected to inform generally as to how organisms respond to the external
environment, and thus generate perceptions, expectations and approaches by which
the ecology of any species of interest may be tackled. The foundation statements are
broad, for they apply to all species, but they are not predictive in the way desired by
most ecologists. They simply steer investigation. In this, they resemble the ways and
strengths of the Recognition Concept of species (Walter 1995). Autecology theory
thus has the significant roles of generalising views and providing a basis for the
development of alternative explanations in specific cases. Furthermore, the general
theory is open to test, because it is based, for example, upon specified premises
about organisms, their adaptive mechanisms and the spatial distributions of those
mechanisms, as reported elsewhere (Hengeveld and Walter 1999; Walter and
Hengeveld 2000).
The ultimate aim of this paper is to expand on this alternative general theory,
explain how it is based on the conceptualisation of adaptive mechanisms relative to
the structure of environmental conditions, and propose how it explains the observed
dynamics of populations. The balance of nature argument, with its emphasis on
density dependence, effectively by-passed the importance of adaptive mechanisms
in sustaining life. It also failed to deal directly with the way in which organisms (and
thus populations) operate relative to environmental circumstances (Walter and
Zalucki 1999). These ideas about the significance of individual organisms have
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languished in relation to the aims of ecology, but have been kept alive by some
(Andrewartha and Birch 1954; Wellington 1977; White 1993). Since autecology is
consistent with recent ideas about the origins of adaptation and speciation (Paterson
1985 1986; Walter 1995), it fills an important gap currently seen to be serviced by
macroecology (see Sterelny 2005) in explaining how external (regional) influences
impact local ecology. How the mathematical tool kit is deployed relative to such
premises remains to be seen, but individual-based models will undoubtedly play a
large part (e.g., Van den Bosch et al. 1992; Hengeveld and van den Bosch 1997;
Grimm and Railsback 2005).
Non-equilibrium, density independence and density vague ecology
A strong alternative to population regulation and density dependence should clearly
appeal to many ecologists, but despite a growing number of ecologists taking up
some version of the density independent or non-equilibrium approach, none have
met with much success. A significant practical problem lies in the various solutions
on offer not necessarily being true equivalents of one another. Some, for example,
have been developed to solve particular issues within the equilibrium framework
(e.g. metapopulation theory and macroecology). Others offer true alternatives but
are not consistent with one another (‘‘spreading of risk’’ is not necessarily
commensurate with non-equilibrium, for example, as explained later). Some
alternatives provide only part of the solution (e.g. ‘‘inadequate environment’’), and
none is comprehensive in its coverage of ecological systems. Despite these nuances,
these offerings are often treated as inclusive or complementary of one another, and
even as synonyms at times, despite their often significant, albeit subtle, differences.
A significant factor in the poor performance of alternative theory in population
ecology seems to lie in the nature of the arguments presented. Although ‘‘nonequilibrium’’ and the associated processes of ‘‘density independence’’ and ‘‘density
vague ecology’’ (Strong 1984) are sometimes seen to represent profound
alternatives to the original balance concept (e.g., Perry 2002), they also seem to
fail as true alternatives. Although non-equilibrium ecology has incorporated such
aspects as contingency, historical influences, pluralism, individual variation, and so
on (see Cooper 2001), no positive and consistent theoretical core to this approach
has been presented. Their basic claim seems to be that, on average, densities will
average out, and this seems to suggest the entire demographic system is
underpinned by randomness. That this is not the general way in which to see
ecological systems is redressed later in this manuscript.
A more fundamental point seems to be at issue here, and this relates to the
paradigmatic difference between the ‘‘balance’’ approach to ecology and an
approach based on the interaction of individuals with their environmental surrounds.
The latter does not see the local ecological ‘‘population’’ as an entity, so ‘‘return
tendency’’ and ‘‘stationary probability distribution’’ are not treated as phenomena.
Numbers of individuals within a local area (in most cases specified arbitrarily by the
observer) rise and fall, through mortality, recruitment of young and movement in
and out of the specified area. The ‘‘population’’ is not seen as an entity with
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properties, although high densities of individuals of a species may, at times, impact
on the environment, change it or reduce food resources, and thus affect conspecific
(and other) organisms.
The lack of a foundation statement is clear in those non-equilibrium treatments
that are focussed on group-related phenomena, such as those associated with the
‘‘spreading of risk’’ (e.g., den Boer 1968; Andrewartha and Birch 1984). The theory
associated with risk spreading is based on a stochastic model. It accepts that the
various populations that make up a species (or ‘‘natural population’’ if physical
barriers separate conspecific organisms in different geographical areas from one
another) are not synchronised in the sense of all not going extinct or overexploiting
their resources simultaneously (Andrewartha and Birch 1984, p. 200; Hengeveld
1989). That the rates of increase, for example, vary asynchronously across the local
populations means that the overall variation is reduced (Andrewartha and Birch
1984). Here, regulation is still central because a large number of stochastic
influences, spread over a broad spatial scale, are considered to reduce the variance
around the population mean (see Hengeveld 1989). These views thus seek density
independent processes that could delay extinction and prevent population outbreaks,
so ultimately they also deal with regulation. Population ‘‘regulation’’ is thus seen to
be a statistical by-product of the complexity of ecological systems. The problem is
that the phrase ‘‘spreading of risk’’ cannot be related to individual organisms, for it
is not they that are ‘‘spreading risk’’ in this particular theoretical treatment.
Somehow the population is doing so, which enters the realm of group selection.
Such proposals also ignore observations demonstrating that relatively few
ecological factors exert disproportionate influence at a particular place and time
and that different primary ecological variables influence the ecology of individuals
(and thus abundance) at different localities (Hengeveld 1989).
A further problem was pointed out early, in Orians’ (1962) criticism of
Andrewartha and Birch’s (1954) thesis, which focussed on individual organisms
within their environmental setting as the basis of an alternative theory (although this
was coupled with an emphasis on density independence that has since been broadened
into ‘‘spreading of risk’’ (Andrewartha and Birch 1984)). Orians pointed out that the
methods of Andrewartha and Birch could not be reconciled with evolutionary theory,
and that they advocated keeping ecology distinct from evolution. At that time selective
pressures were strongly related to density dependent population pressures, and
adaptive local change was seen to be inevitable and ongoing. Orians’ criticism is
therefore not surprising, given that evolutionary ecology was in the ascendant then,
and is based firmly on the premise that selection pressures are strongly demographic
(mainly through competition) and adaptive change is ongoing at a local scale (Collins
1986). We see this manifest today in optimisation theory in which the deterministic
processes of competition and density effects (Ghiselin 1974, pp. 56–57) are considered
to drive the system. Those seeking an alternative to such density dependent processes
as a basis for generalisation in ecology therefore encountered a serious problem. The
ecological processes whose importance they were questioning were seen to be driving
evolutionary change through ongoing local adaptation.
In their approach to ecology, Andrewartha and Birch (1954) implicitly treated the
adaptive mechanisms of organisms, the ones relevant to ecology, as species-specific
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and species-wide in nature, and therefore stable in an evolutionary sense. The
stability of species is increasingly accepted, even in evolutionary ecology (e.g.,
Eldredge et al. 2005), and speciation is increasingly seen as historical and linked to
such external ‘‘drivers’’ as climate change (e.g., van Dam et al. 2006). Andrewartha
and Birch (1954) could be portrayed as prescient in this regard, but they did
subscribe to the view of the day that evolution is an ongoing process (Andrewartha
and Birch 1954, Chap. 15, 16) and here they did outline how ecological
investigation relates to evolutionary processes, and how ecologists could contribute
to evolutionary understanding. The fact, though, that their criticisms of the balance
of nature argument also struck at the heart of evolutionary theory does not seem to
have been noticed by many (but see Cooper (2003, pp. 55–60 and 93–94)), and is an
issue that warrants much closer inspection.
A more positive alternative to the balance of nature argument is required. It must
be independent of the equilibrium model, it must be consistent with evolutionary
processes and it must explain observed dynamics. Does such a construction exist?
The rudiments have undoubtedly been laid, especially through the progress of
Andrewartha and Birch (1954) and White (1993) in developing the autecological
perspective on ecological systems. In the following section I outline how
developments in evolutionary theory and autecology add to their alternative in a
way that overcomes the problems just outlined. Here the main focus in ecology is on
the individual organism, principally to maintain consistency with Darwin’s
individual selection and to focus on the mechanisms by means of which organisms
interact with their environment (Hengeveld and Walter 1999; Walter and Hengeveld
2000). Furthermore, this alternative is consistent with a view of evolution that is
gaining in empirical support, and which is expanded in the following section before
it is related to issues in ecological understanding.
Individual organisms, adaptive mechanisms and population persistence
‘‘Let us imagine that we are descendants of the first organism which lived in
the world. Our structure deviates radically from that of our ancestor. It is even
possible that we do not share a single gene with the hypothetical organism.
Here we instinctively notice change, evolution. The other side of the problem,
what is the entity which changed, is easily pushed into the background; but
this ‘existence of life’ is the basic phenomenon. Evolution would not have
been possible without it.’’
Erkki Haukioja (1982)
Individual organisms have special significance in evolutionary theory. One of the
few interpretations in evolution that is widely accepted is that individual selection is
the basis for the transmission of adaptive characters. Indeed, this is seen as one of
the strongest aspects of Darwin’s work (Lewontin 1974, p. 4), and the reason for the
persistence of his basic evolutionary views. Individual organisms are thus given
special prominence. But what is a living organism? This unlikely question, for an
ecologist at any rate, was sprung by Erkki Haukioja (1982) in a thought provoking
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paper that remains little cited (8 citations on the Web of Science, 22 August 2007).
The question is rather beguiling because its answer probes deep into current theory
in biology. The implications for evolutionary biology were spelled out by Haukioja
(1982, p. 363) in rather understated fashion: ‘‘A set of automata [or living entities]
can be regarded as a population … If we count the proportions of different kinds of
automata at successive intervals, we probably notice that the mean kind of automata
changes. This is evolution. It is not a goal but a by product of POL [the process of
living]. However, it is the main topic of biological research’’. The implications for
ecology were not explored explicitly, but are similarly deep and pervasive, and are
developed next.
The central function of living organisms is to maintain themselves within the
environmental context (Haukioja 1982). If they fail in this task, they simply fail to
survive. If an organism has the appropriate organization to produce other organisms,
and it maintains itself to reproductive maturity, it can produce a lineage that spans
generations. This reproduction mechanism could, in principle, be based upon one of
three alternative mechanisms of transmitting information to offspring (Haukioja
1982). Two of these can be excluded, because arbitrary (or randomised) information
will result in failure and planned information is beyond the capacity of any
organism.
The only real option is information that has been tested, and the test is provided
by natural selection on those organisms that contributed to the lineage of the
organism of interest. Although sexual reproduction yields variation, the raw
material of evolution, the variants produced are mostly coded by information that
has already been subject to test. Individuals must maintain themselves before they
can reproduce, and successful maintenance depends on features that rely on this
tested information. ‘‘Tested information’’, in turn, carries the strong implication of
sameness rather than difference. Although variation is evident among offspring,
evolutionary change is not an inevitable consequence of the appearance of such
variation. The action, frequency and influence of stabilising selection must be
appreciated.
The above analysis from the perspective of individual organisms reveals that
adaptive change is not a goal of organisms. Evolutionary change is a by-product, a
population consequence (Haukioja 1982). The circumstances under which change
does occur are critical, and are examined later. This evolutionary perspective
ultimately provides a positive basis for interpreting what is currently referred to as
non-equilibrium ecology, but which is better characterised as the autecology
promoted by Andrewartha and Birch (1954) (Hengeveld and Walter 1999; Walter
and Hengeveld 2000).
Adaptive mechanisms have profound significance in the life of organisms, for
they mediate the interactions between organism and environment (as expanded in
the following section). Such complex adaptations comprise subsidiary components
whose actions are ultimately integrated to achieve fundamental biological functions
like dealing with temperature and its variation (daily, seasonal and erratic), habitat
and host location, sexual interactions, locomotion and migration, and so on
(Paterson 1985, 1986; Hengeveld and Walter 1999; Walter and Hengeveld 2000).
Integrated mechanisms like this are expected to be under stabilising selection, so
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they have a particular distribution within natural systems. They are distributed
throughout the local population and they have essentially the same structure
throughout the population, with some variation around the mean, even in species
considered to be variable (e.g., Popple et al. 2007) or extreme generalists (e.g.,
Rajapakse and Walter 2007). In population genetics terms, the mechanisms are
‘‘fixed’’ within the population and under stabilising selection. In Mendelian terms,
we also speak of a population of populations. This extended population represents
the species gene pool, or the field for gene recombination (Carson 1957; Ayala
1982; Paterson 1986), and adaptive mechanisms tend to be species-specific relative
to this ‘‘field’’. Subspecies, defined in population genetics terms, must be treated in
the same way, for they are produced by the same processes that lead to the
production of ‘‘full’’ species (Walter 2003; Popple et al. 2007). This sequence of
connections between individuals and species (or subspecies, depending on the
particular case) is critical to understanding evolution and ecology, as well as
specifying the relationship between the two disciplines. This approach does not
deny that changes in allelic frequencies take place, as in the evolution of insecticide
resistance, just that these relatively simple adaptive changes, coded by one (or very
few) alleles, are not representative of the way in which complex adaptations change,
or in the way in which speciation may ensue.
Because the mechanisms that support the survival of individuals and their
reproduction are species-specific and species-wide, they must have been acquired
when their population was small and with a very restricted distribution geographically (Paterson 1985, 1986; Vrba and DeGusta 2004). The mechanisms were
carried to the outer limits of the species’ current broad distribution by movement of
individuals. We see this process around us, for it is a natural aspect of ecology
(Hengeveld 1990; Botkin 2001), and the trans-Atlantic movement and establishment
of the cattle egret in the Americas is a good example (see Botkin 2001, for details).
The argument outlined above provides a basis for interpreting the relationship
between individuals, their species-specific adaptations, seasonal structure of the
environment, and population abundance and persistence. Just as evolutionary
change is a by-product of the existence of organisms, so patterns of population
change and persistence through time are the consequences of the factors just
mentioned, as detailed next.
Survival and reproduction of individuals, environmental structure
and dynamics, and ‘‘Population Stability’’
Individual organisms have a lifeline (Rose 1997). As this runs its course, the
organism must maintain itself within its environmental setting, even as it changes
developmentally. Organisms change morphologically as they develop, sometimes
rather dramatically. Their biochemical, physiological and behavioral mechanisms
also change, and so do their responses to the environment. Their ecology, in other
words, changes through their life. We conceptualize those changes as the life cycle,
the significance of which has not been maintained in modern ecological theory
(Bonner 1993; Arthur 2004). The continued survival of the individual through all
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Individuals, populations and the balance of nature
429
stages of the life cycle requires the appropriate operation of its adaptive mechanisms
of development, motion and resource acquisition in relation to the structured
sequence and extremes of environmental conditions to which it is exposed. These
mechanisms, environmental requirements and environmental tolerances differ from
life stage to life stage and the appropriate sets of ecological conditions for two
different life stages of the same individual may be in different places, and therefore
require the appropriate movement by that individual at the appropriate time, as seen
in benthic marine organisms with a planktonic larval stage (e.g. ascidians and
mollusks (Jackson et al. 2002)), and in ruderal plants whose seeds must usually
reach newly cleared land for successful establishment and growth. Those
individuals whose mechanisms fail in this regard will almost inevitably not survive
or reproduce. Conversely, those individuals in inappropriate environments are
similarly selected out.
The requirements of mating also impose ecologically on individual organisms.
The appropriate physiological and behavioral preparation for sexual reproduction is
fundamental to ensuring the synchronization of the sexes with one another and also
with the particular environmental circumstances they usually inhabit. Achieving
fertilization at the appropriate time of the year ensures the young are produced
during circumstances favorable to their survival. This is as true of mammals (Kiltie
1984) as it is of fish (Sinclair 1988), insects (Butterfield and Coulson 1997) and
plants (Proctor et al. 1996). Indeed, Sinclair (1988, p. 68) even sees mating, or
‘‘closure of the life cycle’’, to be an ‘‘ecological constraint’’ in sexually reproducing
species, to the extent that the complex life histories frequently observed in the
oceans ensure temporal persistence of populations in relatively fixed geographic
space (at least whilst those localities remain suitable for the species in question).
The species persists only in those geographic locations within which continuity of
the life cycle of the constituent individuals is possible. Sinclair’s (1988) chosen
example is the population of Atlantic herrings that spawn at specific offshore
localities associated with the Georges Bank and Nova Scotia. The hatchlings must
remain in their natal area to grow sufficiently before they can migrate inshore to
feed and develop further. Retention of the individuals within their natal area is
maintained behaviorally within the context of local sea floor topography and the
prevailing oceanic currents (Lough et al. 1994; Tremblay et al. 1994). The
‘‘retained’’ individuals can be seen as members of the grouping we refer to in
ecology as the ecological population, and in evolution as the Mendelian population.
The dynamic environment-organism interaction thus generates persistent local
patterns of appearance and abundance in the oceans (Sinclair 1988, p. 71). The same
principle applies to life in terrestrial systems although details, environmental
features and adaptive mechanisms will vary.
The most sensitive stage of the life cycle is almost invariably the newborn young
(Kiltie 1984), newly hatched larvae (Zalucki et al. 2002; Doherty et al. 2004) and
seedling plants (Kitajima and Fenner 2000; Fenner and Thompson 2005). These
individuals have just emerged from an enclosed, protective environment and have to
survive their external exigencies. Consequently, mortality rates at this stage are
often enormous, and these frequently set local abundance levels of the species
(Varley et al. 1973; Zalucki et al. 2002). The issue of synchrony of emergence or
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hatching to coincide with the most appropriate environmental circumstances, all
within a stochastically changing environment, is critical. We see this particularly
clearly with organisms that rely upon bud burst for their survival, such as in the
larvae of winter moth and autumnal moth, but such environmental events are not
predictable with any precision by the individuals concerned (Hunter 1992; Klemola
et al. 2003). Their adaptive mechanisms simply maximize the chances of a good
coincidence.
Organisms thus rely on their various adaptations to support their survival through
the changing environmental circumstances they face. The survival of individuals is
therefore of paramount ecological significance (Wellington 1977; White 1993).
Furthermore, the survival, reproduction and movement of organisms relative to the
persistence, seasonal and spatial dynamics, and vagaries of environmental
conditions can alone account for the observable dynamics, from apparent stability
to local overabundance to local extinction. If environments persist, organisms have
adaptations to persist in their usual habitat, and ‘‘populations’’ are thus seen to
persist. That is, demographic regulation is not necessary, although density-related
impacts may influence numbers locally and sporadically. This perspective accounts
particularly well for the persistence of species at low densities, a situation not really
dealt with particularly well by population equilibrium theory, for in the latter it is
assumed that the lifting of demographic pressure, when population densities drop,
provides adequately for increase to follow. When we consider that most species are
rare (e.g., Walter and Zalucki 1999), it seems clear that the survival and
reproduction of individuals within a spatiotemporally varying environment is more
of an issue than explaining how populations do not overshoot carrying capacity. The
focus in ecology is thus moved from the overproduction of offspring and the
density-dependent population pressure thought to follow, to the species-specific
adaptations and the ecological circumstances that support those relatively few that
do survive to reproductive age.
The point just developed can, moreover, be illustrated further and perhaps more
strikingly with reference to aspects of human ecology. Recourse to humans is made
because the direct influence of the environment is readily appreciated, and because
details of other organisms are well known to ecologists and information about them
can be readily assimilated in the way illustrated. The lifestyle of nomadic
pastoralists may be understood and appreciated by urban people, but is seen as
difficult and hazardous. How do we explain the persistence of the populations
concerned and this way of life? Although we might turn instinctively to density for
inspiration, recent research reveals that the explanation is far richer, and relates to
the specific requirements and capabilities of the individuals concerned, and to the
nature and dynamics of the environment. This is illustrated, below, with reference to
the Turkana people of Kenya. That such an approach is as informative about human
ecology as it is about the ecology of other organisms suggests the approach does
provide a realistic alternative to the equilibrium paradigm. It does not, moreover,
discount density from having sporadic effects. But the true impact of density can be
appreciated in full only in relation to the interpretation of the system as a whole.
Nomadic pastoralism is best represented as a distinct pattern of subsistence in an
environment that is seen as marginal, fragile, and with limited productivity for humans
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431
(Table 2). Besides that, it is variable. Rainfall is limited in amount, space and time,
which leads to drought that is seasonal or even more extended. Ultimately, such arid
environments are heterogeneous and unpredictable across space and through time, but
this is a feature that is common to all environments albeit in various ways (Hengeveld
and Walter 1999; Walter and Hengeveld 2000). To understand how the nomadic
Ngisonyoka pastoralists of the Turkana region of northwest Kenya survive, their
family-based groups were investigated within the context of their environment, its
dynamics, and their socio-economic and political surrounds (Little et al. 1999a, b;
McCabe et al. 1999). To survive, they ‘‘manage their lives’’ by adapting behaviorally
and socially to environmental contingencies (Table 2), and such responses that are
favorable ‘‘enable individuals to survive, be healthy, be an integral part of their
society, and to reproduce within the existing framework’’ (Little et al. 1999b). Such
adjustments do, however, come at a cost to body condition, fertility and opportunity (in
relation to diet and herd building, for example). In brief, there is a cost to maintenance
or persistence (Leslie et al. 1999), so the survival of individuals is a struggle that
cannot be taken for granted (White 1993).
Population density may constitute an ecologically significant part of the
environment of these people, but it is secondary in the sense that it does not
inevitably manifest ecologically important effects and any such effects are likely to
be sporadic. Its occurrence and effects are, in any case, understood only in relation
to the life, behavior and movement of the individuals concerned. And those features
are understood only in relation to the spatiotemporal dynamics and stresses of the
environment, in which no single year or even two-year period is evidently typical in
its rainfall and vegetation cover (Leslie et al. 1999; Little et al. 1999a). The
ecological consequences for the people concerned is that there is no really typical
period for livestock holdings, food production or migration patterns. Neither is the
body weight and health status of the individuals stable (Little et al. 1999a, b), and
all of these implications for the individuals concerned need to be appreciated if their
ecology is to be understood.
Table 2 The life of nomadic pastoralists - nature of the environment and responses of the Turkana
people (from Leslie et al. 1999)
Key environmental characteristics
Semiarid with limited resources
Spatial and temporal variability
Multiple external perturbations—unpredictable
Human responses to environmental features
Complex livestock management system, based on detailed knowledge of environment
Mobility to local areas that are more suitable
Temporal changes to biology and behavior (e.g. distribution of resources, emphases in pastoral
activities)—seasonal and longer term
Opportunistic exploitation of resources when sufficient rain falls
Complex social networks—exchange and reciprocity (e.g. with livestock), resource allocation
High growth rates of herds and families when conditions suitable
High failure rate and loss of people from the pastoral sector
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The uncertainty and risk inherent in such a system manifests itself in the overall
strategy towards livestock husbandry. Herds are diversified for the differential use
of vegetation types by the different livestock species. And there is clear individual
choice, by group leaders, of when to move livestock, which species to move and
which individuals (milking or non-milking) to take. The direction of the migration
and the distance to travel has also to be finalized (McCabe et al. 1999). Besides
movement, individuals and groups respond to changing environmental conditions
by adjusting diet and activity patterns, infant and childcare, and group structure and
distribution across the landscape (Leslie et al. 1999). In particular, resources are
diverted, when limited, to the vulnerable young and to childbearing and nursing
women, so the chances that all persist through periods of adversity are maximised.
These actions all have physiological, social and population structure consequences
(Leslie et al. 1999), and the responses of the decision makers can be seen as
introducing a further stochastic element into the system, for perfect knowledge of
future conditions is not available to them.
The overall goal with respect to livestock is the maintenance of livestock
productivity, and the ongoing herd building strategy could mean the difference
between survival and failure (de Vries et al. 2006). Ultimately, the wellbeing and
survival of family members is a primary consideration, as is the persistence of the
family group (Leslie et al. 1999). The group is important because it is the vehicle
for individual survival. By contrast, the persistence of the population as a whole is
not an issue to the individuals concerned, and maximum productivity is not a goal
(Leslie et al. 1999). Indeed, the population growth recorded for the Turkana has
been a consequence of the growth within domestic units, which is a specific and
active goal (Leslie et al. 1999), and this has presumably been aided to some extent
by modern medicine, and has occurred despite the increased emigration of
individuals during severe drought (Leslie et al. 1999).
In effect, the persistence of the nomadic way of life and the Ngisonyoka population
is entirely a consequence of the life and reproduction of the individuals concerned,
how they have adapted to environmental circumstances and their particular responses
to environmental contingencies. In other words, understanding persistence in this
system does not (and cannot) derive from perceptions and investigation at the level of
populations. ‘‘Through movement of livestock and people the Turkana can live in an
environment unsuitable to many other subsistence strategies. The ability of individual
Ngisonyoka herd owners to respond to variable environmental conditions is one of the
principal factors which has led to a successful adaptation to the stressful and variable
environment in which the Turkana live’’ (McCabe et al. 1999).
Conclusions
Equilibrium theory focuses on high densities and persistence of populations, with
the implicit claim that if populations did not exist in this state (i.e. with upward
pressure from an overproduction of individuals), they would ‘‘random walk’’ their
way to extinction. Autecology, by contrast, suggests that individuals of a species do
not usually achieve such high densities locally (as is increasingly accepted in the
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Individuals, populations and the balance of nature
433
literature, now usually in terms of ecological systems being seen as nonequilibrium) and that persistence relates to organisms embodying mechanisms that
are adapted to particular subsets of the environment. Furthermore, such environmental circumstances persist seasonally, but are spatiotemporally variable and
dynamic. It is this dynamic and ongoing match between the adaptive mechanisms of
organisms and the environment that ensures the persistence of individuals and
lineages and, as a consequence, ensures the persistence of what we see as
populations, despite juvenile production suffering enormous attrition rates through
various agencies (environmental challenges, predation and so on). Local outbreaks
and extinctions are thus readily explained.
Autecology focuses primarily on the mechanisms for maintenance and
reproduction that are carried by individual organisms (e.g., White 1970a, b, 1993,
2004), and relates ecology explicitly to adaptive mechanisms (rather than with the
adaptive process as an ongoing feature of life, as seen with the emphasis on fitness
measures in evolutionary ecology (Walter and Hengeveld 2000)). The successful
completion of the life cycle to reach reproductive stage and then to reproduce
successfully is not seen to be easily or inevitably accomplished (White 1993), as is
assumed in theories that focus on explaining the persistence of populations through
population level processes. The explanation of how the life cycle of a particular
species matches the spatiotemporally dynamic and variable environmental circumstances to which it is adapted is thus the aim in this alternative (Hengeveld and
Walter 1999; Walter and Hengeveld 2000). Such explanation is not straightforward.
These interactions are not explicable simply in terms of average temperatures,
moisture conditions or humidity, for the environment is structured temporally and
spatially with regard to a range of aspects of temperature and other physicochemical
features (Walter and Hengeveld 2000). Furthermore, the adaptive mechanisms have
a diversity of inputs and components that require understanding, including genetic,
developmental, biochemical, physiological, morphological and behavioral features.
Selection pressures have sometimes clearly shifted (or are shifting) the capacity of
organisms to interact with their environment, as in the relatively minor genetic
changes associated with resistance to insecticides and malaria (see below). The
ecological consequences of such changes can be substantial, and cannot be ignored
in ecological investigation.
The environment also has biotic structure, but principally in relation to vegetation
cover and with respect to the other species that may be of relevance to the species of
interest, and often these are host organisms. Clearly, though, predators and parasites
may be relevant in particular circumstances, but here the emphasis should not
necessarily focus on density relationships. For example, the impact of malaria on
human populations in ancient Italy was not strongly related to density, but to
locality and local conditions, for ‘‘... the distribution of malaria is always
discontinuous and highly localised because of its very complicated ecological
requirements’’ (Sallares 2002). Important factors include environmental temperature
(which needs to be high enough for completion of parasite sporogony within the
fly), breeding site availability for mosquito larvae, genetic makeup of the host
population, quality of human nutrition, and human infection rates by other diseases
(for these last two debilitate individuals and increase chances of mortality from
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malarial infection) (Sallares 2002). The severity of malaria in some areas even
precluded agriculture, and villages were sometimes shifted. Again it is the survival
of individuals that is important, and how these people managed their lives in relation
to the local environment (malaria included). Population trends are consequences and
cannot be understood on their own, or in relation to homeostatic mechanisms
postulated to save populations from overexploitation and, somehow, from
extinction. The Italian example illustrates, as well, that the autecological argument
does not hold only for physically severe environments.
Perhaps the most typical term associated with the idea of non-equilibrium in
ecology is ‘‘stochastic’’. Stochastic influences are seen as intrusive events and are
seen to move systems away from equilibrium. Whereas most ecologists acknowledge this, they also generally accept that deterministic density-related forces return
soon enough (e.g., Pimm 1991), and this may be why most non-equilibrium writings
tend back to the regulation camp. Ecological systems, in this latter view, can be
understood only in relation to the regularly invoked population-level demographic
forces, with the stochasticity ultimately represented as an intrusion. Seldom do nonequilibrium writings extend to serious consideration of species-specific adaptations,
and thus the ecological idiosyncrasy or individualism of species (but see Rohde
(2005)). Also bypassed is the idiosyncratic or ecologically unique way in which the
life cycle of species is adapted to ‘‘match’’ with a particular sequence of
environmental features. Where these features are considered, the concept of local
ecological population may re-intrude in reified form, rather than being treated as the
epiphenomenon that it seems to be. This occurs despite ecological systems having
no clear boundaries and thus no objective or purpose, and so being quite unlike
organisms (Grimm 1998). However, the way in which we, as humans, view the
world apparently steers us into visualizing populations as if they were entities, and
consequently we do not readily see the underlying processes that actually account
for what we describe. The balance of nature concept thus maintains a strong hold,
even though it is not explicit.
The view promoted in this paper accepts that stochasticity is a global and
continual influence in the life of all organisms. But it does recommend a refocus on
ecological stochasticity for at least three reasons. One, the assumption that large
numbers of unspecified stochastic factors are operating independently of one
another (as in ‘‘spreading of risk’’ theory) is untenable and untestable, and should be
avoided, as it fails to explain and provides no basis for analysis (Hengeveld 1989).
Two, the simple focus on the large-scale stochastic influences (such as periods of
unusually severe weather) that alter population densities dramatically are undoubtedly important, but they are by no means the only stochastic influences in ecology.
Third, no organism is actually exempt from stochasticity, regardless of how stable
the environment may seem, for such influences are of daily import and can be seen
as individual risks. Indeed, adaptive mechanisms (as opposed to adaptation as the
enhancement of efficiency that is claimed in optimisation studies) are inexplicable
without reference to their role in the amelioration of external environmental
variation, whether this be through damping the variance, as in Claude Bernard’s
maintenance of the milieu inte´rieur, or internal environment of organisms (Rose
1991), or through maximising opportunity when conditions are good and
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435
minimising impacts when bad, as seen in the Turkana nomads (Leslie et al. 1999, p.
367), and even in organisms as different from people as aphids. Theory and models
appropriate to this structured form of individual risk assessment have been
developed and are being extended (Hengeveld 1999; Hengeveld and van den Bosch
1997; Hengeveld and Walter 1999; Van den Bosch et al. 1992; Walter and
Hengeveld 2000).
Acknowledgements I wish to thank Mark Colyvan, Mary Finlay-Doney, Erkki Haukioja, Rob
Hengeveld, Adriana Najar-Rodriguez, Lindsay Popple, Hugh Paterson, Chris Pavey and Andrew Ridley
for their help with the concepts and their expression in the manuscript. The perceptive criticisms of an
anonymous reviewer and the editor, Kim Sterelny, helped clarify several important points in the
manuscript.
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