Download 1 Theories

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The nature of the plant community: a reductionist view
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J. Bastow Wilson
Botany Department, University of Otago, Box 56, Dunedin, New Zealand.
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Andrew D.Q. Agnew
Institute of Biological Sciences, University of Wales Aberystwyth, SY23 3DA, U.K.
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Chapter 6: Theories
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Theories .......................................................................................................................................... 1
Clements and the integrated concept ............................................................................................. 3
Gleason........................................................................................................................................... 6
Whittaker and Austin ..................................................................................................................... 8
Hubbell and chance ........................................................................................................................ 9
Grime’s C-S-R theory .................................................................................................................. 10
6.1 The triangle ...................................................................................................................... 10
6.2 Stress ................................................................................................................................ 11
6.3 Disturbance ...................................................................................................................... 14
6.4 Species/character tests...................................................................................................... 14
6.5 Competition...................................................................................................................... 15
6.6 Community-level tests ..................................................................................................... 16
6.7 Does succession provide a test of C-S-R? ....................................................................... 16
6.8 Conclusions ...................................................................................................................... 19
7 Centrifugal theory (Keddy) .......................................................................................................... 20
8 Tilman’s theory ............................................................................................................................ 20
8.1 Co-existence ..................................................................................................................... 20
8.2 Species diversity .............................................................................................................. 20
8.3 Succession ........................................................................................................................ 20
8.4 Intensity of competition ................................................................................................... 22
8.5 The competitive process: R* ............................................................................................ 22
9 Grime versus Titman/Tilman ....................................................................................................... 25
9.1 Strategy ............................................................................................................................ 25
9.2 Competition...................................................................................................................... 26
10 Synthesis: we are like blind dogs ................................................................................................. 32
1 Theories
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In this chapter we consider theories that aim to generalise over all plant communities. Some
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are aimed at terrestrial communities but we would hope for a theory that is general enough to cover
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aquatic communities too. Often the models are aimed at embryophytes, but we would be happy if
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the theories could be applied to fungi and algae. The theories can be seen in the light of Diamond’s
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(1975) challenge: are there assembly rules for communities? The theories concern how species
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assemble from a defined species pool; they are not intended to consider the biogeographic processes
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by which those pools arose. The first distinction is between models that are:
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Deterministic: Environmental filters and the constraints of plant interactions wholly and
predictably control species composition. Composition does not have to be deterministic at
Wilson and Agnew, chapter 6, Theories, page 2 of 38
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the level of particular species, e.g. it the number of species in a particular guild could be
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determined, or the total number of species in the community.
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Stochastic: The community-determining processes are governed, or at least initiated, by
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chance. Perhaps many of the species in the species pool are ecological equivalents, so
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which arrive and establish at a site is partly due to chance. Species composition is therefore
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unpredictable, just one event of a number of similar possibilities.
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The other distinction is between communities that are:
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Discrete: separated by clear boundaries; vegetation may change suddenly along an
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environmental gradient, as one discrete community gives way to another at a boundary,
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versus
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Continuous: gradual change, without clear boundaries; a continuum of vegetation along an
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environmental gradient, with gradual, species-by-species change between the limits.
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These two distinctions have often been confused. However, they can be seen in the three concepts
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listed by Gleason (1939), plus one other, giving the four logical combinations:
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(a)
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(b)
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Fig. 6.1: The distribution of species along an environmental gradient: (a) a simplistic version
of Clements, (b) a simplistic version of Gleason, and (c) Whittaker (who needs no
simplification).
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Deterministic and discrete, i.e. the species composition is predictable from the environment
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and there are distinct communities (‘associations’) with sharp boundaries and no/few
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intermediates (Fig. 6.1a). This concept has been attributed to Clements. Coevolution is a
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likely explanation of such structure, so this includes the coevolution-structured model of
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Rummel and Roughgarden (1983). However, it is possible that there is no coevolution, that
Wilson and Agnew, chapter 6, Theories, page 3 of 38
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there is assembly of pre-adapted species (Bazzaz 1987), only certain combinations of
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species being stable. Gleason (1939) described this as Theory 1: "The association is a quasi-
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organism".
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Deterministic but continuous, i.e. the composition is predictable, but with continuous change
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as along an environmental gradient, and no boundaries. It might correspond to Gleason’s
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type 2: "The association is a series of separate similar units ..., repeated in numerous
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examples". This model probably includes the Invasion-structured communities of Rummel
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and Roughgarden (1983), since the latter involves no coevolution, but involves rigid control
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on the ability of species to coexist. However, it is possible that coevolution may be involved
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in this type of model. Whittaker distinguished between such a model without coevolution
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(6.1b) and with (Fig. 6.1c).
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Stochastic, continuous: Gleason at times identified this with his Individualistic theory "3:
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The vegetation-unit is a temporary and fluctuating phenomenon". Whittaker (e.g. 1967)
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interpreted this as “communities which occur continuous environmental gradients usually
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intergrade continuously, with gradual changes …”, but this was not Gleason’s view (1917,
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and see below). It is quite difficult to draw a gradient under this theory (Fig. 61.b) because
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random scattering of bell-shaped curves gives considerable variation in total abundance,
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which is surely not intended.
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Stochastic and discrete: This seems almost a contradiction. If the community structure is not
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deterministic, how can there be discrete boundaries? Such structure could arise by a switch
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(Wilson and Agnew 1992). If a propagule lands, and its offspring appear near it, it might
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modify the local environment in its favour, resulting in a sharp boundary from the
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surrounding vegetation. However, as we have described it this would be a one-sided switch;
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it would require another species operating another switch, or possibly a reaction switch, to
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give a stable mosaic.
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2 Clements and the integrated concept
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Frederick E. Clements saw communities as integrated: "an organic entity exhibiting
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cooperation and division of labor" (Clements et al. 1929; see also Clements 1905) and thus
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"something more than the mere sum of its parts" (Clements 1931). Clements produced wide-ranging
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ideas, omitting to give his theory a name because he thought it was The Truth. Phillips (1935),
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whom Clements and Shelford (1939) cited with the greatest approval, elaborated on this: "With
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properties definitely unpredictable from a knowledge of the individual organisms", i.e. emergent
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properties (Wilson 2002 %47). This implies deterministic structure: "The bond of association is so
Wilson and Agnew, chapter 6, Theories, page 4 of 38
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strict ... that the same seral stage may recur around the globe ... with the same dominants and
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subdominants" (Clements et al. 1929). “An association is similar throughout its extent in … general
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floristic compositions” (Weaver and Clements 1938). These communities were therefore nameable.
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Of course, Clements was too good a field ecologist to take these communities literally, writing that
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that they had "more or less definite limits" forming a "mosaic, in which the various pieces now
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stand out sharply, and are now obscure”, “[A formation] can rarely have definite limits” (Pound and
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Clements 1900), the "ecotones are rarely sharply defined" (Clements 1905). This concept has been
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called the "Integrated" community view (Goodall 1963), and the "Community-unit" view
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(Whittaker 1967).
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Others expanded on Clements’ theme: "All the species which are members of a given
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association ... are adjusted more or less perfectly to one another" (Dice 1952). Tansley, another
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ecologist with great field experience, wrote: “the complex of interactions between plants and their
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environment does lead to a certain degree of order … The same species are constantly present in the
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same kind of place and show the same groupings”. At equilibrium, he said, the association becomes
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“the mature, integrated, self-maintaining quasi-organism” (Tansley 1920 %118). One might think
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that Braun-Blanquet (1932), who described the association as having concrete reality, would have a
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similar view, but he could not accept the degree of integration that Clements proposed: "the
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organismic character, the centralized organisation and the division of labour etc. is lacking in it". In
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spite of the strength of opinions for and against these concepts – "more than the mere sum of its
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parts", "complex organism", etc. – it is difficult to pin them down to testable features.
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Whether communities are ‘complex organisms’ or not, the naming of them implies
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recurrence: that we shall find the same community in several different locations. This has rarely
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been tested, but Wilson et al. (1996 %471) did so for roadside communities in the continental-
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climate Ebro Basin of Spain and across a wide range of climates in southern New Zealand. The
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problem is defining “the same” community. It would be unrealistic to expect exactly the same
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species complement, so we need a baseline of how similar two remote quadrats should be to be
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regarded as the same. Wilson et al. answered this in two ways. The quadrats had been placed in
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adjacent pairs. One baseline was therefore the mean similarity between the two quadrats of a pair,
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making the question: “does one ever come across another patch of vegetation as similar to this one
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as the patch next door is?”. Some next-door quadrats would happen to be quite different, e.g. in
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disturbance, so Wilson et al. omitted the 10 % of least similar pairs before taking the mean. The
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answer was basically No; for only 41 % of sites was there another in the survey similar to it by this
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criterion (Fig. x) *[This number looks wrong against the figure. JBW will check.]. For the more
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heterogeneous NZ data the figure was only 19 %. However, another comparison was available,
Wilson and Agnew, chapter 6, Theories, page 5 of 38
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since the pairs of quadrats at a site had themselves been placed in subsites 50 m apart. Using those
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subsites as the baseline, the percentage of sites with vegetation that occurred elsewhere in the
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survey increased to 98% in Spain and 83% in NZ. Allowing for the likelihood that vegetation
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similar to any site could have been found outwith the quadrats sampled, we have to conclude that
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communities do recur, and in this Clements was right.
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Fig. 6.2. Spain
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One would imagine that Clementsian structure would arise from coevolution. Clements does
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not seem to have used the term, but he considered that the evolution of species was part of the
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process of community evolution (Clements 1929), and later workers made it more explicit, e.g. the
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"interco-ordinated evolution" of Dice (1952). The most explicit development of such views is that
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of Dunbar (1960) who suggested that selection could operate at the level of the whole ecosystem:
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just as an individual can die and be replaced by one of genotype with higher fitness, so an
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ecosystem can be unstable, collapse to leave “empty environmental space”, and be replaced by a
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community from nearby with genetic differences in some of its species, giving it a higher stability
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(i.e. fitness). Collapse to empty space is not realistic, and the idea reeks of group selection. Darnell
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(1970) had similar ideas, writing that “the ecosystem … is … the basic selectional unit of evolution.
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He suggested that species-level selection led to evolutionary adaptation, which led to stability. The
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major difficulty with such co-evolution is that species normally occur in several communities, and
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the characters of a whole species cannot coevolve to be optimal in each (Goodall 1966). Anyway,
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how do such ecosystems arise?
Wilson and Agnew, chapter 6, Theories, page 6 of 38
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Although many are ready these days to ridicule Clements' views, many contemporary
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ecologists are producing models in which the control of species composition is every bit as tight:
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mainly theoretical ecologists (e.g. Drake 1990), but also field ecologists such as Cody (1989).
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3 Gleason
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Gleason’s concepts are hard to pin down. Probably he saw all the same complications of
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plant communities that Clements had, but instead of presenting one strong line then mentioning
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exceptions, he simply put down what he saw. He did from the beginning (Gleason 1917) state that
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contra Clements exact repetition of the same vegetation never occurs, and that abrupt vegetation
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transitions occur only with abrupt variation in the environment (Gleason 1939). Vegetation was
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"merely the resultant of the development ... of ... individuals" (Gleason 1917), the vegetation
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depending on the environment, competition, and accidents of immigration (Gleason 1917). He
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named these ideas the Individualistic concept of the plant community.
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Yet behind the invective most of his views were identical to Clements’. Clements et al.
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(1929) emphasised the importance of competition. So did Gleason (1936), writing that that with any
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two plants growing together “each interferes with the environment of the other”, and that this
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interference “may act either favourably or unfavourably” so that “the vegetation … is the result of
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the interference”. The latter statement is as strong as any ecologist has ever made, and the very
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opposite of the no-interaction caricature of him that we often read. In the process, he was among the
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first to suggest that subvention is widespread. His views on the mechanism of succession, with
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reaction as the basic process (Gleason 1927) were identical to Clements’ (1916). Gleason also
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accepted the concept of the association with “limits … fixed by space and time” with “tension
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zones” (i.e. ecotones) between them (Gleason 1927) and that every community must have extent,
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boundary and uniformity (Gleason 1936). Clements could not have put this better. Cements’
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concept of the landscape was of different formations/associations, repeated in a mosaic (Pound and
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Clements 1900), with “the same species or formation in similar but separate situations” (Clements
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1907; see also 1904), a situation he called alternation. Gleason’s (1936) concept was identical: “a
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vegetational mosaic, composed of numerous types of vegetation, each repeated numberless times,
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but all united intro a harmonious and extensive whole”. Clements believed that narrow transition
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zones (ecotones) between associations could occur along gradual environmental gradients because
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of reaction (environmental control). Gleason (1917) thought that at least in regions of “genial
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environment and dense vegetation” there is reaction (which he used interchangeably with
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‘environmental control’) with the result that “species of one association are then excluded from the
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margin of the other by environmental control, when the nature of the physical factors alone would
Wilson and Agnew, chapter 6, Theories, page 7 of 38
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permit their immigration. The adjacent associations meet with a narrow transition zone, even
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though the variation in physical environment from one to the other is gradual.” Gleason’s statement
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is a precise summary of Clements’ view. Both are saying that there are very often switch ecotones
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between associations, because of reaction.
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In terms of our seven steps in community assembly (this vol., chapt. 1, sect. 2) both
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Clements and Gleason would have accepted A-E. It is hard to discern views on assembly rules from
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their writings, but it seems likely Gleason would not have accepted them, and we can see assembly
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rules when Clements (1907) writes on alternation: “owing to the accidents of migration and
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competition, similar areas within a habitat are not always occupied by the same species or group of
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species. A species found in one area may be replaced in another by a different one … Such genera
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and species … must be essentially alike in … response to the habitat, though they may be entirely
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unrelated systematically”. Here there is a niche in a community into which one species or another
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can fit, an assembly rule as strong as any.
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“Clements versus Gleason” is a useful straw man in questions in seminars and in
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introductions to papers, e.g. “the now well-known dispute between Clements (1916) and Gleason
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(1926) … pitting the idea of ‘discrete communities’ against that of a ‘continuum’ (Leibold and
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Mikkelson 2002). However, there was no real difference in their concepts. There were probably
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personalities involved, at least in their approach to science. Gleason could not stomach Clements’
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community-as-an-organism concept and the classifications that flowed from it. Perhaps this was
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because Gleason was a plant taxonomist, and saw that communities are not the clear objects that
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most taxonomic species are.
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Wilson and Agnew, chapter 6, Theories, page 8 of 38
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4 Whittaker and Austin
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Whittaker clearly adhered to theory 2, deterministic but continuous. Deterministic in that the
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community is "a distinctive living system with its own composition, structure, ... development and
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function" (Whittaker 1970 *[see]) and structured by competitive exclusion: "The unique
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identification of niche with species within a particular community ... is not a matter of chance, but
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as the result of competitive exclusion" (Whittaker and Levin 1975, p30). No one has believed more
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strongly in coevolution as a cause of community structure: "Other species evolve toward close
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association with the dominants and towards adaptations for living with one another" (Whittaker
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1975) and "The community is an assemblage of interacting and coevolving species" (Whittaker and
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Woodwell 1969). There was also coevolution in the opposite direction, towards mutual avoidance:
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"toward scattering of their population centers along environmental gradients" (Whittaker and
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Woodwell 1969, see also Whittaker 1967). All this is far from the view of Gleason. From his
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'Gradient Analysis' results (Whittaker 1967) concluded that spatial vegetational change was a
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continuum, though it has to be said that flaws in his methods leave those results somewhat in doubt
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(Wilson et al. 2004 %245).
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From this, a ‘Continuum theory’ was developed by Austin and co-workers, defined as: “the
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organisation of vegetation structure and composition in terms of continuous change in properties
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along environmental gradients” (Austin and Gaywood 1994). This begs the question of what the
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environmental gradients are, and how they are measured. If, as usual, the environment is calculated
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from geographical trends (e.g. Leathwick and Austin 2001) there will certainly be sudden change
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where switches locally modify the environment to produce a sharp boundary: rainforest/savannah,
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treeline, fog-catching boundaries, etc. (Wilson and Agnew 1992). It is not clear what Continuum
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theory is beyond the existence of gradual change, for example it is not clear how deterministic it is.
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Analysing distribution of species along gradients, Oksanen and Minchin (2002) defined a
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simplistic Continuum theory as “species have symmetric, unimodal responses to ecological
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gradients” (perhaps a normal curve), and a more sophisticated version as “response shapes should
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differ among gradient types or gradient locations”. Austin and Gaywood (1994) are more explicit,
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saying that species response curves are skewed with the longer tail being towards the middle of
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mesic position, though the latter must be hard to define. Austin et al. (1994 %215) did find that all
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nine SE Australia Eucalyptus species that they examined showed significant skewing along a
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gradient of mean annual temperature, in the expected direction if ‘mesic’ is defined as 11.5 °C.
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However, Oksanen and Minchin (2002) found for an altitudinal gradient in Tasmania (930-1380 m
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asl) that only 21% of the responses were skewed. The conclusion will depend on the type of curve
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fitted, and how skewed is skewed (significance is not the best guide to effect size). Moreover,
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skewness can be reliably determined only when there is good evidence that the whole
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environmental range of the species has been sampled (M.P. Austin pers. comm.). A conclusion of
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skewness also depends on the way the X-axis is expressed, for example a simple gradient assumes
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that the difference between 0 mm and 300 mm rainfall is equivalent to that between 2000 and 2300
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mm, which seems unlikely. The occurrence of bimodal curves would be interesting. Bimodality on
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a proxy gradient such as altitude would be boring, because it could be due to frost above treeline
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and similar frost in the valleys due to cold air drainage. Austin (1985 %39) commented: “The
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occurrence of bimodal curves … seems well established”. However, he cites Whittaker whose
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evidence for bimodality was very weak (Wilson et al. 2004 %245). We have not been able to find
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any good example of bimodality.
5 Hubbell and chance
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Chance (Lippmaa 1939), or random effect, does not really exist. Seeds are sometimes said to
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disperse randomly, but in fact they disperse under the laws of physics. It is just that eddy diffusion
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is very complicated. Everything happens under the law of physics (except arguably the resurrection
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of the Our Lord Jesus Christ: Wilson 2002 %47), and above the scale of the atom chance plays no
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rôle. Nevertheless, many have suggested a rôle for it in the species composition of plant communities,
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assuming that many species are ecological equivalents1 of each other (e.g. Lippmaa 1939; Richards
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1963; Sykes et al. 1994). Fowler (1990) used the term ‘disorderliness’.
Hubbell and Foster (1986 %314) make this concept explicit, with saying that “biotic
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interactions … are not very effective in stabilizing particular taxonomic assemblages, in causing
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competitive exclusion, or in preventing invasion of additional species” because there are
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“ecologically equivalent species”. Therefore “chance and biological uncertainty may play a major
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role in shaping the population biology and community ecology of tropical tree communities”.
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Hubbell (2001) developed these concepts into a full ‘Neutral’ model in which species are equivalent
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in their demography and dispersal, i.e. in which niche differences play no rôle. He discovered, to his
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surprise almost as much as anyone else’s, that many of the features of ecological communities that
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ecologists have long been discussing, such as relative abundance distributions, species-area
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relations and island biogeography can be predicted on this basis. Hubbell’s (2001) theory does not
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imply that even on one tropic level all species have the same niche: “No ecologist in the world with
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This can be distinguished from the redundancy concept, where the species are equivalent in alpha
niche but not in beta niche.
Wilson and Agnew, chapter 6, Theories, page 10 of 38
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even a modicum of field experience would seriously question the existence of niche differences
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among competing species” (Hubbell 2005 %166). Hubbell’s (2001) approach is to start with the
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simplest null model, which in this case comprises the functional (niche) equivalence of species, and
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then to add to the theory only when necessary to explain observations in the real world. Hubbell’s
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earlier work had described niche differences in the tropical rainforest that he often takes as his
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example: “Some tree species are largely restricted to slopes, whereas others are predominant on flat
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ground or in the seasonal swamp”, “Shade-tolerant shrubs and understorey trees are also
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recognizable guilds. Finally, there are gap-edge regeneration specialists” (Hubbell and Foster 1986
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%314). These effects would tend to cause aggregation within species, but the same workers
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demonstrated “pervasive” negative effects of plants on neighbours that were of the same species.
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Such effects were confirmed when Uriarte et al. (2004) estimated the effect of neighbouring
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saplings on the diameter growth of other saplings on BCI, work in which Hubbell has been
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involved; for almost half of the species species-specific effects could be found, including more
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competition if the neighbours were conspecific, or confamilial, or in the same gap/shade-tolerant
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guild. All this emphasises that Hubbell’s (2001) thesis is intended as a null model, not a best-fit
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model.
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Wootton (2005) tested the theory using a 12-year record of transitions in an intertidal
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community (sessile animals and algae) to parameterise a Hubbell (2001)-type model. Model
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predictions matched the observed relative abundance distribution (RAD), but there was no
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alternative model (and RAD curves tend all to look rather similar because they monotonically
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decrease), and the confidence limits for the model prediction were wide. Many observed curves
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could have fitted. However, observed species abundance in mussel-removal plots bore no relation to
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the model’s predictions. This confirms the conclusion of Chave (2004) that many ecological models
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can result in the same patterns, especially of the relative abundance distribution (which was already
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known, see Wilson 1991 %35), but that does not prove that any one of them is correct.
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If the chance theory were correct, there would be no reason to expect community re-
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assembly except by chance, and hence no predictability. However, the reverse argument cannot be
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made: a failure to predict species composition well from the measured environmental factors is no
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evidence for chance, as we discussed in chapter 4, section 9.
6 Grime’s C-S-R theory
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6.1 The triangle
Grime’s C-S-R theory (1974; 2001) theory is based on a contrast between types of habitat
and adaptation to them:
Wilson and Agnew, chapter 6, Theories, page 11 of 38
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─ high-productivity / high-competition habitats (C),
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─ high environmental-stress habitats (S) and
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─ high-disturbance (i.e. ruderal, open) habitats (R).
C (competition)
Disturban
ce
Productivity
C-S-R
S (stress)
(ruderal) R
(disturbance)
Productivit
Untenable
triangle
Disturbanc
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Heathrow
airport, main
runway
Fig. 6.3: The dreaded C-S-R triangle.
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In the original 1974 formulation of C-S-R theory one axis was RGRmax, i.e. relative growth rate in
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the first few weeks after germination and in optimal conditions. Now, a method is available for
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placing a species within the triangle by weighting its characters (Hodgson et al. 1999). Even a few
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simply-obtained characters such as canopy height, flowering period and SLW can give good
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prediction of C-S-R category for most species (Bogaard et al. 1998; Hodgson et al. 1999), but a
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wider, and perhaps more meaningful, range of characters is desirable (Caccianiga et al. 2006).
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These species * C-S-D equilibrium of sites (Grime 1988 %371).
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Grime’s ideas were supported by the analytical models of Bolker and Pacala (1999),
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showing that three, and only three spatial strategies are possible. The ‘Exploitation’ strategy can be
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matched with C, the ‘Colonisation’ strategy with ‘R’ and the ‘Tolerance’ strategy with S.
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6.2 Stress
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Stress is clearly defined in C-S-R theory as "The external constraints which limit the rate of
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dry matter production of all or part of the vegetation". The disturbance axis (R–C) recalls the r-K
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spectrum of MacArthur and Wilson (1967), but the S (stress tolerators) axis is new to C-S-R theory.
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Grime (2001) assumes that plants cannot grow where disturbance and stress are both high (the grey
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area in Fig. 6.2), such as the middle of Heathrow Airport’s main runway where the soil is too dry
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and low in nutrients (i.e. non-existent) and is disturbed every two minutes (Fig. 6.2). This leaves
Wilson and Agnew, chapter 6, Theories, page 12 of 38
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which leaves the C-S-R triangle (Fig. 6.2). C, S and R (or D for disturbance) were originally
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categories of habitats, but they are also categories of the species that occur in those habitats.
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There remains the problem of stress to which species. Take an alpine herbfield, where
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temperatures are low (Koerner, 2003). Humans would consider this a stress, and so would most
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plants. Yet under climate warming, the heat-lovers would be able to establish, and probably
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competitively exclude the alpines. How can we say that the alpines were under a stress before, when
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they were growing to their heart’s content, but they are not under stress now that they are dead?
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Some alpine species grow poorly in ‘low-stress’ sea level conditions, probably because they lose
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carbohydrate in the warmer winter temperatures there (Stewart and Bannister 1973). One would
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think that the phytometer approach of Clements and Goldsmith (1924) would be ideal: planting the
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same species into a range of communities and measuring its growth. However, Grime has chosen to
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define stress on a whole-community basis and on the basis of the plants presently occurring, and is
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consistent in that.
356
Perhaps the most difficult habitat for C-S-R theory is forests. We might think that the
357
dominant trees of tropical rainforests are the ultimate competitors, but Hubbell (2005 %166)
358
described them as the “competitive (stress tolerator) functional group”, with characteristics typical
359
of S species: tolerance of low light levels, long life spans, high resistance to pests and herbivores.
360
This rather depends on how they regenerate. If they grow fast from seed/oskars after disturbance,
361
they could be C species, almost R. Others have seen the dominants as species that are shade tolerant
362
and growth slowly up through the canopy, or sit still “conservatively” in the shade and make bursts
363
of growth during mini-gaps, they are S species. Then again, Grime (2001) points out that trenching
364
experiments have shown that nutrients are often more limiting than light to herbs and seedlings on
365
the forest floor. For many types of stress, as resources become limiting they will also become more
366
patchily limited. *[Andrew is working on this]
367
Since the r-K spectrum is widely accepted, the controversial aspect of C-S-R theory is that
368
different kinds of stress have much in common, resulting in a consistent S-species type. Such
369
species grow slowly, at least in their natural habitat. Leaves can therefore be produced only
370
infrequently, and must be evergreen, 'tough' both mechanically and in herbivore defence, so that it
371
can function for more than a year. The energy constraints affect a whole suite of characters (Reich
372
et al. 1991; 1992), e.g. slow relative growth rate, evergreen habit, low maximum photosynthetic
373
rate, low leaf percentage nitrogen, abundant defence compounds, leaves that are small, often stiff,
374
needle-like and with high specific leaf weight. This suite of characters is also part of Leaf
375
Amortization theory (Wilson and Lee 2000). Thus, the S axis of C-S-R theory is an adumbration of
Wilson and Agnew, chapter 6, Theories, page 13 of 38
376
the theory of leaf costs and amortisation of Orians and Solbrig (1977). The coincidence is so great
377
that we can see the relation: C-S-R = r/K theory + Leaf Amortization theory.
378
It has sometimes been suggested that low RGRmax is adaptive in stress environments (e.g.
379
Hunt and Hope-Simpson 1990). However, adaptation to stress environments is by relatively high
380
RGR in those environments, not by low RGR in a hypothetical optimal environment. Low RGRmax
381
is adaptive to stress environments only via a strategic trade-off: "It is possible that genetic
382
characteristics conducive to rapid growth in productive conditions become disadvantageous when
383
the same plants are subjected to environmental extremes" (Grime and Hunt 1975).
384
Grime (1988 %371, 2001) has more recently emphasised that the common underlying stress
385
is a deficit of major mineral nutrients either directly or as a result of other stresses. This view is
386
comparable to that of some physiologists, who have proposed a unifying stress mechanism (see
387
Wilson and Lee 2000). Craine (2005) considers this at least unproven.
388
A limitation to the generalisation of C-S-R is that different types of stress favour different
389
types of species (Grime 1988 %371). For example, species of nutrient-poor habitats have a high
390
allocation to roots, but species of low-light habitats have low allocation to roots (Tilman 1987). One
391
problem with this example is that Grime (1979) considered biotic shade to be competition rather
392
than stress (though there is abiotic shade, e.g. in caves)
393
It is very difficult to characterise a site as low/high stress in terms of light, since in a
394
productive environment there will always be some species low in the canopy that have to tolerate
395
the stress of shade from taller plants (Pigott 1980). Grime had envisaged that any community would
396
comprise a mixture of species with different C-S-R status, but this is not just a case of the overlap of
397
species' ecological ranges, or of micro-habitat variation, because, as Pigott notes, the species "grow
398
together in vegetation ... because they possess different strategies" [italics ours]. Athyrium filix-
399
femina (lady fern) and the grass Bromus erectus occupy very similar areas on the Triangular
400
Ordination of Grime et al. (1988), but differ in life form and population dynamics (Austin and
401
Gaywood 1994). The succulent habit is found on saltmarshes and deserts but not in habitats where
402
the stress is water-mediated.
403
Moreover, not all species are adapted to one particular stress in the same way. A dramatic
404
example of this is seen in adaptation to water stress in deserts. The extreme variability within and
405
between years in deserts is responsible for the wide range of life forms that are found in these
406
regions. By this we mean the predictability of climate itself differs between deserts such that some,
407
e.g. Namibia, with predictable rain in summer, supports relatively few extant life forms whereas
408
others such as the North American deserts, with rainfall less predictable from year to year, support a
409
very wide range. Some species are adapted by being avoiders, including stem succulents such as
Wilson and Agnew, chapter 6, Theories, page 14 of 38
410
cacti and leaf succulents as in members of the Crassulaceae), but also annuals/ephemerals which
411
avoid water stress as adults by dying, but survive water stress as dormant seeds. Others, like the
412
shrubs, are tolerators, where water potentials in the tissues are very low in dry periods, shedding
413
leaves and even branches, but which can tolerate this without death. Again, this emphasises C-S-R
414
as a simplification.
415
6.3 Disturbance
416
Grime’s definition of disturbance is unambiguous: "The mechanisms which limit the plant
417
biomass by causing its partial or total destruction". This refers to the whole community, but this
418
brings the problem that what is a disturbance to one species might not be to another (paralleling one
419
of the criticisms relating to stress). For example, the mowing disturbance of Burke and Grime
420
(1996) will have disturbed the tall species, but increased resource (light) availability to short ones.
421
Selective grazing is another example. Short or unpalatable species might be described as
422
‘disturbance avoiders’ in contrast to ‘disturbance tolerators’, but it is not clear how to fit this
423
distinction into C-S-R theory. We argued in chapter 2 that autogenic disturbance is important in
424
plant communities; it is not clear how C-S-R theory incorporates this.
425
6.4 Species/character tests
426
A basic assumption of C-S-R theory is that there are “design constraints" (Grime 1988,
427
Grime et al. 1988) that limit viable character combinations. Reich et al. (2003) found a compelling
428
negative correlation between leaf lifespan and net photosynthetic capacity, though of course with
429
scatter, and a slightly weaker one via leaf N. Grime et al. (1987) made a more general test by
430
classifying species by cluster analysis on a range of characters, and then looking for correlation
431
between the resulting groups and the three C-S-R 'strategies'. They found, in one analysis, a group
432
of low-stature, evergreen species with 'tough' foliage, comparable to the S group. Grime et al.
433
(1997) used 67 characters, including experimental responses, to ordinate 43 species. They could
434
informally overlay a C-S-R triangle on the ordination diagram. There was also a good fit between
435
this ordination and that derived in Grime et al. (1988) from field distributions: e.g. the three species
436
in the C corner of the character ordination are in that corner in the distribution ordination, with
437
comparable fits for the S and R corners. This gives some support to C-S-R theory. A more direct
438
test of these trade-offs would be to find unoccupied character space.
439
Other tests can be made by determining whether species of the right type occur in the right
440
habitats. For example, Madon and Médail (1997) examined the distribution of species in a
441
Mediterranean grassland. Sites with a high cover of S species (how they were designated as S
442
species is unclear) also contained a higher cover of annuals (which would normally be R species in
Wilson and Agnew, chapter 6, Theories, page 15 of 38
443
C-S-R theory). It is true that such semi-arid grasslands often contain many annuals. So do deserts;
444
in fact deserts commonly comprise a mixture of species with quite different characters (see above).
445
This emphasises that C-S-R theory is a simplification, not a law of the type that physicists can have.
446
Caccianiga et al. (2006) attempted to test C-S-R theory on succession on glacial moraines in
447
Italy. The concept is valid, and it was a brave attempt, but there are problems: (1) They use
448
“percentage ground cover”, without saying how it was measured. (2) They conclude that there is a
449
successional trend from R species to S ones, and their Fig. 3 confirms this, yet their Fig. 4
450
contradicts it. (3) Although an R→S change is predicted by C-S-R theory, it is generally with an
451
intermediate increase in C and with the S stage not being reached for a long time (more than the
452
<200 yr of their dataset). Moreover this R→S change applies in C-S-R theory to a secondary
453
succession; for a primary succession, which theirs certainly is, the initial trend should be S→C-S-R
454
(Grime 2001 %bok).
455
An experimental approach is perhaps better, since one can be sure what the habitat
456
differences are. Moog et al. (2005) applied four basic treatments – sheep grazing, mulching with
457
hay, burning in winter and control (‘succession’) – at 14 sites in SW Germany. The vegetation
458
resulting 25 years later was classified in terms of C-S-R composition, using guessed cover and
459
species’ C-S-R rankings by the method of Hodgson et al. (1999). There were some changes in
460
community C-S-R status that agreed with C-S-R theory. For example, grazing and twice-yearly
461
mulching, presumably both disturbances, led to a C-ness c. 0.35 below the control. Grazing and
462
burning increased S-ness by c. 0.2 above the control. Moog et al. explained the grazing effect due to
463
the herbivory defence of S-strategists, or due to nutrient removal though it is not clear whether how
464
grazing will reduce nutrient availability or whether it may increase it though nutrient recycling.
465
They explained the increase in S-ness with burning as an indirect effect, that burning favoured
466
species with rhizomes, which happened to be S-strategists, though severe burning can lower
467
nutrients (Certini 2005). Grazing and mulching increased R-ness by 0.4-0.5 above the control, as
468
predicted by C-S-R theory. However large differences in C-S-R status were found between the
469
same treatment at different sites, up to 1.0 difference. Not clear-cut.
470
6.5 Competition
471
Some have rejected the concept of competitiveness as an overall plant attribute, i.e. the
472
concept that a species that is a superior competitor for one resource is also a superior competitor for
473
all other resources (e.g. Grubb 1985). This is one prediction of C-S-R theory that can be tested quite
474
clearly. Contrasting shoot competitive ability (for light) with root competitive ability (for water and
475
the major nutrients), for the same species in the same conditions, the data assembled by Wilson
476
(1988 %279) indicate 13 (22%) cases where the relative competitive abilities of two species were
Wilson and Agnew, chapter 6, Theories, page 16 of 38
477
different between shoot and root competition, and 46 (78%) where they were in the same direction
478
– a significant difference. Non-transitivity of competitive ability (Chapter 7) would make a
479
nonsense of the idea of overall competitive ability, but it seems to be rare, and has arguably never
480
been demonstrated in plants. Another prediction of C-S-R theory is that competition intensity will
481
be lower in stress sites (Grime 2001). Grime (op. cit.) writes: “Some ecologists are extremely
482
reluctant to recognise the declining importance of competition for resources in unproductive
483
habitats”. We agree. We are amongst those who are extremely reluctant, and we discuss this issue
484
below.
485
6.6 Community-level tests
486
It is difficult to make testable predictions in the middle of the triangle, because all such
487
predictions are merely questions of degree. Testable predictions come from the rare, most-extreme
488
habitats in the corners of the triangle. Therefore, although most habitats and species apparently
489
occur in the central parts of the triangle, to obtain critical tests we here emphasise the extreme
490
corners. The position of the R corner is well defined in concept, i.e. 100% disturbance, but this is
491
hard to apply operationally. No plant can exist exactly in the corner, and it is hard to know how
492
disturbance should be quantified when degree, frequency and even type have to be taken into
493
account. Similarly, it is impossible for a plant to exist exactly in the S corner because by the
494
definition of stress biomass is reduced to zero there. It is possible to define the C corner in terms of
495
zero disturbance, but zero stress is zero reduction in biomass: from what? In the triangular
496
ordinations of Grime et al. (1988) the great majority of habitats and species cluster towards the
497
middle of the triangle, but this seems largely an artefact of the method of construction of the figure
498
(Wilson and Lee 2000). Caccianiga et al. (2006 % 10) do manage, by using a good
499
species/character dataset and the method of Hodgson et al. (1999 %282) to get a good spread of
500
species along the bottom half of the triangle, which is reasonable for their field site.
501
Grime's (1979) assumed that in high-disturbance, high-stress sites no plants would grow.
502
This implies that all high-disturbance sites occupied by plants must be relatively low-stress and all
503
high-stress sites occupied by plants must be relatively low-disturbance. Tests have not so far been
504
attempted, they would be difficult to perform and there would be logical problems (Wilson and Lee
505
2000).
506
6.7 Does succession provide a test of C-S-R?
507
The early stages of primary succession often involve stressful habitats. Colonisation of bare
508
rock is a good example. Some of the species of such habitats are clearly S species, such as lichens.
Wilson and Agnew, chapter 6, Theories, page 17 of 38
509
Thus, it seems that R species occur mainly in secondary succession (Grime 1988), and we shall
510
consider only secondary successions in our examples.
511
Lack of C-S differentiation in the R corner
512
Grime's (1979) interpretation of secondary succession was that for sites of differing
513
productivity there would be separate successional pathways, all starting from the R corner, and all
514
ending (eventually) in the S corner (Fig. 3a,b). At the start in the R corner, the succession
515
trajectories are very close (Fig. a), indicating that the difference between stressful (S) and
516
productive (C) sites is negligible, giving the opportunity for the same species to occur, i.e. the same
517
ruderal species in stressful as in benign habitats (Fig. b,c).
(c)
518
519
520
521
522
523
Fig. 6.4. C-S-R theory and specialist pioneers.
(a) Grime suggested that sites with differing degrees of stress would follow different
pathways. - - - indicates the part of the succession which will probably be slow.
(b) Since there is little difference between C and S in the R corner, the same species will
occur along different pathways.
524
(c) Towards the R corner of the triangle, there is little or no difference between C and S.
525
Considering the three S habitat types discussed by Wilson and Lee (2000), the main pioneer of
526
degraded land in Naiman Banner County, Inner Mongolia, is Agriophyllum squarrosum, a specialist
527
pioneer of dunes in semi-arid areas (Zhang et al. 2005). In Sonoran Desert oldfields, pioneers
528
include the very widespread weed Taraxacum officinale (dandelion), but also species such as
529
Salsola kali, a ruderal annual of dry, often alkaline areas (Castellanos et al. 2005). These recent
530
examples confirm the previous conclusion that in arid habitats the majority of secondary pioneers
531
are not species restricted to deserts, though a few are. The secondary pioneers of saltmarsh gaps are
532
generally species of the lower saltmarsh, as we would expect since all species that occur on salt
533
marshes have to be quite salt tolerant, ruderal or not. Colonists at 950+ m elevation in the
534
Cairngorms (Scotland) are species absent from mesic habitats, but not specialist pioneers (Bayfield
Wilson and Agnew, chapter 6, Theories, page 18 of 38
535
et al. 1984). The species present in mid succession in southern New Zealand alpine grassland
536
included Anisotome aromatica, Plantago novae-zelandiae Colobanthus strictus and Epilobium
537
alsinoides (Lloyd et al. 2003), the latter extends down to the lowlands, but the others are basically
538
montane / subalpine in range. However, pioneers in the Andean alpine oldfields include the very
539
widespread ruderals Erodium cicutarium, Poa annua and Rumex acetosella (Sarmiento et al. 2003).
540
We have to conclude that in some S sites, secondary pioneers (R species) are present that are
541
restricted to that habitat, but in other cases more general ruderals are the colonists.
542
Autosuccession
543
Another way to apply C-S-R theory to succession is to argue that the R corner represents
544
habitats with a high frequency/intensity of disturbance. In S habitats, there will be no variation
545
along the R–C axis, because the triangle narrows towards the S corner (as a triangle must: Fig. X).
546
Therefore, one can predict from C-S-R theory that secondary succession in high-stress habitats will
547
occur entirely within the S corner (Grime 1987; Fig. x). This is autosuccession: the first colonists
548
are also the climax species *[jbw: cf initial floristics]. [This is similar to Grime's (1988) depiction of
549
primary succession for S habitats, indeed no absolute distinction is possible between primary and
550
secondary succession.] This leads to the conclusion that autosuccession will be the norm in extreme
551
S habitats (Figs. 3c, 4b), i.e. the first species to colonise after disturbance will be the same species
552
as are found in the undisturbed ('climax') vegetation, there being no specialised secondary pioneer
553
species [contrast this with Egler’s (1954) ‘Initial floristic composition’ concept in which some
554
species are pioneers]. Again, C-S-R theory strictly predicts the same type of species, but if there is
555
space for fewer niches the species themselves are likely to be the same (Fig. x). There is some
556
apparent conflict here with the prediction above that the secondary pioneers of S habitats will not be
557
specific to those habitats, but this is due to our operating near the corners of the C-S-R triangle, not
558
in them, so that the predictions are not absolute. Autosuccession will tend to occur, but when there
559
are pioneers they will be general ones. *[jbw will coord with Grime’s figures]
560
561
Wilson and Agnew, chapter 6, Theories, page 19 of 38
562
Fig. 6.5. C-S-R theory and autosuccession. *[JBW: To be rationalised with the on-figure caption]
563
(c) In areas of high stress, which by C-S-R theory can never be high-disturbance, succession
564
will follow a full pathway; in areas of high stress, which by C-S-R theory can never be
565
high-disturbance, succession will follow a shortened pathway (cf Fig 20.3l of Grime 1987
566
*[JBW: to check, box strat grime ATR]).
567
568
(b) Towards the S corner of the triangle, there is little or no difference between C and R.
*[JBW: QDA says he needs to read this again; he is confused] Wilson and Lee (2000) tested
569
the prediction in relation to four types of stress, taking care to restrict consideration to secondary
570
succession to minimise problems of confounding disturbance with stress, and we summarise rather
571
than repeat their conclusions. Grime (1979) gave alpine habitats as a further example of a high-
572
stress (S) habitat. Wilson and Lee (2000) cited an example of a Himalayan alpine meadow where
573
there were specialist alpine pioneers, and another from New Zealand high-alpine cushionfield
574
where there were not. Sarmiento et al. (2003) found, in high-Andean oldfield succession, that of the
575
eight most abundant species in the undisturbed community four were absent the first year after
576
abandonment, three others were present in traces, and the remaining one made up less than 1 % of
577
the cover – no autosuccession here. Thus, the evidence is equivocal. In arctic tundra, another habitat
578
cited by Grime (1979) as high-stress, there are usually pioneers, but autosuccession is occasionally
579
seen (Wilson and Lee 2000). Autosuccession is often seen on saltmarsh, especially on the more S
580
lower saltmarsh. For desert, Allen’s (1991) suggestion that autosuccession is common is not
581
supported by the literature (Wilson and Lee 2000) or by Castellanos (2005) in the Sonoran Desert,
582
though the evidence of Zhang (2005) from China is mixed. It is necessary to remember that
583
autosuccession can also occur in mesic habitats (Wilson and Lee 2000). Overall, there is a weak
584
trend for autosuccession to occur in the most extreme S habitats, but it occurs also in some mesic
585
habitats..
586
6.8 Conclusions
587
Several of the predictions of C-S-R theory are very difficult to test, reducing *[Grime says it
588
is a problem for us how to deal with lags in equilibration, spatial and temporal variation in C, S and
589
R within the community] the value of the theory as an explanatory model for the structure of plant
590
communities. Even for predictions that are more easily tested, there has been little quality evidence.
591
The evidence so far is that predictions from C-S-R fail as often as they succeed (Wilson and Lee
592
2000). There have been many more criticisms, but most of them have missed the point of C-S-R
593
theory (Wilson and Lee).
Wilson and Agnew, chapter 6, Theories, page 20 of 38
7 Centrifugal theory (Keddy)
594
595
The ‘Centrifugal’ theory of Wisheu and Keddy (1992) is in some ways the opposite of C-S-
596
R. Whereas C-S-R sees all stresses as in some sense equivalent and arranges them on a single axis,
597
Centrifugal theory emphasises their differences, placing them on multiple axes diverging from the
598
productive sites in the centre of a diagram. This is a display rather than a theory. As Austin and
599
Gaywood (1994) point out, it does not make testable predictions, so it is difficult to see how it could
600
be falsified.
8 Tilman’s theory
601
602
Tilman (Titman 1976 %463; Tilman 1982 %bok; 1988 %bok etc.) has produced a number
603
of ideas. Here we emphasise those that have made a particular contribution to the topic of our book.
604
The concept have been described as having “a hard centre but woolly edges”: that is, there is a solid
605
core of irrefutable mathematics, but it is not always clear how to apply this to the real world.
606
8.1 Co-existence
607
Tilman (1976 %463) concluded from his first experiments: “long-term coexistence of
608
competing species was observed only when the growth rate of each species was limited by a
609
different nutrient”. This is standard Gaussian competitive exclusion. He later developed a concept
610
of spatial niches (1988), and then embraced the fugitive model (Tilman 1994; see Chapter 4).
611
8.2 Species diversity
612
Tilman (1982, book) reached a similar conclusion to Grime (1973 %Nature), that there
613
would be a humped-back relation between productivity and species richness. Like Grime, Tilman’s
614
argument for low richness under low productivity / resource-availability seems to have been that
615
there are few species capable of growing in conditions of high stress. However, part of his
616
explanation for low richness at high productivity / resource-availability was that the effect of spatial
617
heterogeneity on richness would be reduced. Yet he later, finding that nitrogen application led to a
618
reduction in species richness in the Cedar Creek oldfields, converged with Grime’s conclusion that
619
this effect was due to shading suppression by live plant material and litter *[jbw will get reference
620
from Craine]. *[jbw will put this in the Grime/Tilman comparison section]
621
8.3 Succession
622
Tilman (1982 %bok) also generated a resource-ratio theory of succession, starting from the
623
observation that at his Cedar Creek experimental site soil nitrogen (N) increased during secondary
Wilson and Agnew, chapter 6, Theories, page 21 of 38
624
succession. This is often the case, though it is difficult to know what fraction of soil N is available
625
to plants. This led him to theorise that the early-successional species would be more tolerant of low
626
N and therefore better competitors at low N, but late-successional species would require high N but
627
be better competitors, probably for light, in those conditions. Yet his experiments showed that later
628
successional species at Cedar Creek do not necessarily have a higher N requirement or response
629
(Tilman 1986 %555; Tilman 1987 %189; Tilman and Cowan 1989).
630
Actually, although modal nitrogen content of the soil in which various species grow at
631
Cedar Creek is not significantly related to their experimental growth (Tilman and Cowan 1989) at
632
low N (Spearman’s rank correlation rs = -0.45, with RGR taken from the graphs of Tilman and
633
Cowan at 150 mg N / kg of soil), nor their growth at high N (rs = -0.24, RGR at 1500 mg N), their
634
response to N (RGR at high N / RGR at low N) is clearly related (rs = +0.84, p < 0.05). What is not
635
so well related is their successional position. Agrostis scabra does indeed appear early on and peak
636
at c. 5 five years (Tilman and Wedin 1991 %685), but the high-requiring and high-responding Poa
637
pratensis peaks at c. 15 years, whereas Schizachyrium scoparium is hardly present then, and peaks
638
at c. 45 years.
RGR response to X10 nitrogen increase
1.35
Poa
pratensis
1.3
Schizachyrium
scoparium
1.25
1.2
`
1.15
Agrostis
scabra
1.1
0
2
4
6
8
10
N status in field: rank
Fig. 6.6: The experimental response to N compared to the rank of species in a
successional/N field gradient.
639
Harpole and Tilman (2006) produced similar partial support by correlating previously-
640
determined nitrogen R* values with relative abundance in three semi-natural or experimental areas.
641
In the real world of the Community matrix competitive ability and abundance in a mixture will not
642
necessarily be correlated, but in the world of R* they are. The correlations were highly significant
643
but highly far from impessive. There was considerable respect for Tilman that he had published
644
these results with frank admission of their conflict with this theory. However, this leaves his theory
645
hanging. It is also difficult to generalise his ideas. Tilman emphasises the increase in soil nutrient
Wilson and Agnew, chapter 6, Theories, page 22 of 38
646
status, especially of nitrogen, during both primary and secondary succession (Tilman 1988 %bok).
647
[Grime (2001 book), in contrast, sees the initial stages of primary succession as being accompanied
648
by an increase in soil nutrients.] There are a few successions that do not have a monotonic N
649
increase (e.g. Crews et al. 1995 %140 examining a 4100000 yr chronosequence in Hawai’i), and
650
often phosphate limitation is a major determinant of plant growth during succession (Chapin et al.
651
1994 %149; Richardson et al. 2004 %267).
652
8.4 Intensity of competition
Tilman’s (1988) view is that competition will be equally important in productive and
653
654
unproductive environments. This is in direct conflict with the views of Grime, and we address it
655
below.
656
8.5 The competitive process: R*
657
Tilman’s (1982) R* theory is that a species has an R* value for any resource R and set of
658
conditions, which is the lowest [R] (i.e. concentration of R) at which it can grow in monoculture
659
Above its R* the species can grow, absorb R, and will therefore lower R towards R*. In mixture,
660
where R is limiting, as [R] becomes lower each species will drop out as [R] drops below its R*.
661
Apparently no species will enter in this process. The one species left will be the one that can
662
tolerate that the lowest [R], and the concentration of R will be its R*. To summarise, the species
663
capable of sustaining itself at the lowest [R] in monoculture will be the superior competitor. There
664
is a problem here, that the multi-species communities that we normally see have been eliminated in
665
the process, so there must be some other mechanism of coexistence for them.
666
[jbw says: Rate of M supply is in 2 phases, minerfal of organic and de novo entering
667
sysgtfem, rainfall and hydolysis of esp of feldspars and apatite, all dependent on water for rain or
668
soil soln, hydrolysis depons acidity from orgianic and rocks, therfeorfe climatic. Has anyone taken
669
this up? *A says try Vitousek? Air particulates, n-fix, perhaps SO2 from air. ]
670
The model is deceptively simple. Of course if one species reduces the level of a resource to
671
one where only it can use the resource, it must drive out all other species. But application is a
672
different matter: the brave work of Tilman and Wedin (1991 %685, %1038) shows that it is very
673
difficult to obtain conclusive evidence in real experiments with embryophytes.
674
Major soil nutrients (NPK)
675
Tilman (1981) found that the R* model explained which species of alga won in a microcosm
676
experiment with inorganic nutrient limitation. T.E. Miller et al. (2005) surveyed the literature and
677
found 11 experiments with microalgae or zooplankton that had tested R* in laboratory microcosms,
678
and arguably all supported the theory. *[jbw algal cultures the env can be held stable, unlike real
Wilson and Agnew, chapter 6, Theories, page 23 of 38
679
conditions; B thinks it is more a question of uniform mixing; cut down the env variance, diff bet
680
field and expt]
681
The situation is not so clearcut in soil, things are different. Tilman and Wedin (1991 %685,
682
%1038) in field plots at their Cedar Creek experimental site found the outcome of competition on
683
low N soil was predicted by R* in some cases. Comparing Agrostis scabra with Schizachyrium
684
scoparium, the two performed approximately equally in monoculture, but in competition S.
685
scoparium was the clear winner. By R* theory, it should have reduced N in the soil (both nitrate and
686
ammonium) to a lower level than A. scabra, and indeed available N as measured by KCl extraction
687
was lower. It should also have been able to grow at a lower N level, but the experimental results do
688
not tell us one way or the other. A. scabra suffered in competition at the low N levels that S.
689
scoparium produced, but not necessarily because of them. Indeed it suffered almost as much in
690
competition in the two higher N levels. Very similar effects were seen in competition between the
691
A. scabra and Andropogon gerardi, and in a less clear-cut way in competition between A. scabra
692
and Agropyron repens. These results are ambiguous: perhaps A. scabra is more efficient at N
693
uptake but suffers in light competition. Indeed, it grew shorter than other species, including S.
694
scoparium in the experiments of Tilman (1986 %555).
695
Actually, it is difficult to apply R* to soil NPK competition even conceptually. Plants will
696
lower [N/P/K] to some extent, though it is always being produced from by decomposers, so it is
697
patchily available in space but especially in time, resulting from the processes such as
698
mineralization, nitrification, immobilisation, volatilisation, denitrification, fixation and leaching.
699
Nitrogen will normally be most abundant in spring, when maximum growth occurs, and Tilman and
700
Wedin (1991) measured soil N in summer. Plant roots will hardly lower total [P] since most is
701
insoluble. Unlike fast-diffusing NH3 or NO2, and available P is almost immobile. Therefore, unlike N,
702
plants do not take up P from the soil as a whole but the plant roots have to explore the soil, taking up
703
P from a cylinder around the root as they grow, the cylinder being some few mm around the root,
704
perhaps just 1 mm (Kraus et al. 1987). This basic difference between competition for N and that for P
705
was pointed out by Bray (1954). How do we apply R* theory in these circumstances?
706
Water
707
Water is available intermittently in time, a complication for R* theory, but often at different
708
depths. Most water lands on the surface, and perhaps moves down, but water can also be available
709
from deep aquifers, and by hydraulic lift plants can raise it. Plants are not using the same pool of
710
water in time (ephemeral annuals versus perennials) or space (deep-rooted shrubs and perennial
711
grasses versus shallow-rooted cacti). How does R* apply then?
Wilson and Agnew, chapter 6, Theories, page 24 of 38
712
Light
713
In light competition, canopy species reduce the resource availability below them, but not
714
above them, introducing a complication. By R* theory, the climax canopy species would reduce
715
lower-stratum light to low levels, and be able to tolerate these low levels and hence regenerate. But
716
this depends on whether there is continuous regeneration, large-gap regeneration or single-tree
717
replacement, and in the latter two cases whether the next generation is from dispersal, the seed pool,
718
oskars (*jbw will define) [*jbw will comment, I can find no survey on this.] or advanced
719
regeneration: all these modes occur, often with different species regenerating by different modes,
720
within the same community (e.g. Lusk and Ogden 1992; Thomas and Bazzaz 1999).
721
Assuming continuous below-the-canopy regeneration, R* predicts that shade-tolerant plants
722
would achieve tolerance by having a lower light-compensation point. Kitajima (1994 %419)
723
compared 13 tree species of Barro Colorado Island rainforest. Shade tolerance was determined as
724
the survival (i.e. non-mortality) rate of seedlings under shade cloth that gave light intensity very
725
similar to that of the forest understorey, supported by field observations of mortality in the
726
understorey and the tendency of the species to occur in light gaps. Survival was uncorrelated with
727
the light compensation point (r = +0.27) and with dark respiration (r = +0.25 on a mass basis).
728
Eschenbach et al. (1998, %356) examined tree species of North Borneo lowland dipterocarp forests
729
in the field. Light compensation points were attained mainly between 6 and 9 mu mol photons m-2 s-
730
1
731
regeneration, but the presence of pioneer species reminds us that gap regeneration is occurring.
732
Cenzato and Ganf (2001 %53) compared two aquatic species, the one that normally grew with
733
wholly-submerged leaves had a light-compensation point almost half that of another spp which
734
grew with floating emergent leaves. This conflicts with R* theory if we use the analogy with
735
forests. *[JBW: A says: “How so, I would have thought it agreed”]
736
but were higher for pioneering species. This supports an R* interpretation in continuous
The truth is that regeneration in forests, and probably in some other communities, is too
737
complex to fit R* theory.
738
Conclusion
739
None of these complications occur in homogenous, nutrient-limited habitats such as a lab
740
tank with planktonic algae. Tilman had such experiments of his in mind when he formed R* theory.
741
In real habitats, R* theory is not only very complex to test, it is often impossible to see how to
742
apply it or test it. There are many, obvious simplifications in this model. So long as the model is
743
still predictive, and can be seen by Occam’s Razor as being provisional true, that is no problem. A
744
statement of some simple truth is the aim of Science, and difficult in Ecology.
Wilson and Agnew, chapter 6, Theories, page 25 of 38
9 Grime versus Tilman
745
746
The ideas of Titman/Tilman (1988) have often been compared with C-S-R theory. However,
747
C-S-R theory is a coherent body of ideas, summarising habitats and species, including the
748
characters of the species, the characteristics of the habitats, their relation, succession, and in the
749
humped-back relation of species richness to productivity. These ideas are all interconnected into
750
one theory. It has remained essentially unchanged since 1979, the only major addition being that all
751
stresses are basically unavailability of mineral nutrients. Love it or lump it, it is the only
752
comprehensive, coherent theory we have in community ecology. Titman/Tilman’s theory, in
753
contrast, includes a number of ideas that are rather separate, covering the mechanism of
754
competition, where competition will be most intense, how resources will change during succession,
755
whether and how species will co-exist, species diversity, etc. Some of these theories have been
756
effectively disproved, even by Tilman himself, but others remain alive. To some extent this reflects
757
that the theories are put in a more testable form than Grime’s. Grime does have one undisputed
758
advantage over Titman/Tilman: he did not change his name part way through.
759
9.1 Strategy
760
The concept of strategy is old, and intuitive to every child, that the effort a plant or animal
761
puts into one organ or activity is at the expense of another. Plant ecologists generally think of effort
762
as biomass, though calorific content might be more appropriate. Cody (1966) stated the concept of
763
strategy eloquently: “It is possible to think of organisms as having a limited amount of … energy
764
available for expenditure, and of natural selection as that force which operates in the allocation of
765
this … energy in the way that maximises the contribution of the genotype to following generations”
766
(the ‘…’s refer to time, which is easier to see as a resource for animals than for plants). Harper and
767
Ogden (1970) applied this concept to plants by examining the proportion of energy allocated to
768
reproductive structures. Much consideration has been given to the conditions under which particular
769
reproductive strategies should be optimal, formalising it in terms of optimal strategy and then later
770
correcting this to the evolutionarily stable strategy (ESS: Smith 1982). The concept applies to a
771
whole species, to ecotypes and to plastic responses. The principle applies to vegetative allocation
772
too, for example shoot versus root allocation: "the plant makes every endeavour to supply itself
773
with adequate nutriment, and as if, when the food supply is low, it strives to make as much root
774
growth as possible” (Brenchley 1916). This principle is implicit in C-S-R theory: it explains why no
775
species can be a perfect competitor, a perfect stress-tolerator and a perfect ruderal all at the same
776
time. Indeed, Grime commonly refers to C-S-R as ‘Strategy Theory’, as though it were the only
777
one. Tilman has also moved to an emphasis on strategy with his ALLOCATE model of plant
Wilson and Agnew, chapter 6, Theories, page 26 of 38
778
growth and competition (Tilman 1988 %bok), emphasising shoot versus root strategy, a field with a
779
long history of theory and observation (Wilson 1988 %433) but usefully put into the context of the
780
community.
781
9.2 Competition
782
Grime’s and Tilman’s hypotheses
783
*[JBW will integrate]
784
However, mortality that happens to exactly balance the juvenile:adult ratio, i.e. that exactly
785
balances recruitment, is infinitely unlikely. Yet, even a slight excess of mortality over recruitment
786
would give λ (population growth rate) less than 1.0 and a population that declined to zero, and
787
even a slight deficit of mortality would give λ greater than 1.0, and a population that climbed
788
towards infinity. We never see either of these in existing populations. The logical conclusion is that
789
in all persistent populations of a species, (i.e. excepting transient situations), recruitment and/or
790
mortality must be density-dependent and the most likely cause of this is competition. The
791
population will grow until its individuals run out of resources, even if we outsiders cannot easily see
792
what the critical resource is. This is the answer to the not very fruitful argument between Grime
793
(1979; 2001) and Tilman (1988) to which we turn in chapter 6. Or herbivory holds abundance too
794
low for competition to occur. But perhaps with such low levels of plant productivity herbivore
795
populations cannot exist. *[JBW will ask William Bond. And try Rietkerk paper on “Multiple stable
796
states”]
797
Grime (1979, 2001) stated that competition is less intense in stressful environments,
798
apparently because the plants there are limited by abiotic stress, not by competition. Tilman
799
states that competition is equally present in all environments. There are complications. If we
800
put plants in a pot, or if colonisation occurs in the wild, the plants will grow faster in the less
801
stressful environments, and thus come into competition sooner. On the other hand, resources
802
will be exhausted sooner in a more stressful environment. But then the mobility of some soil
803
nutrients will be higher when they are present at higher concentrations (e.g. Vaidyanathan et
804
al. 1968), and this can result in greater below-ground competition (Wilson and Newman 1987).
805
There is also no generally-agreed index of competition (Weigelt and Jolliffe 2003). All this
806
makes the question very difficult to answer (Wilson and Lee 2000 %77). However, basically,
807
in all environments plants will increase in density and/or size until they are limited by the
808
resources, i.e. competition is 100% (what about isolated plants?). Ecologists often see what
809
they think are exceptions in arid and semi-arid areas, where the plants are spaced above-
810
ground. However, the logic used above indicates there must be 100% competition below
Wilson and Agnew, chapter 6, Theories, page 27 of 38
811
ground, and experiments confirm the existence of such competition. Grime’s argument has
812
the obvious flaw that, although competition for water and for mineral nutrients can actually
813
increase as resource supply increases, at some point there will be plentiful supply of these
814
resources and thus no competition for them. At this point, competition shifts to competition
815
for light. The environmental conditions are then so different that it is difficult to say
816
whether competition is less, the same or greater, and anyway competition for light is
817
different in being asymmetric/cumulative (see *).
818
Grime (1974) made it clear that in the S corner of the C-S-R Triangle there is no
819
competition because neighbours are too constrained by the unfavourable environment to interact.
820
This is an aspect of the C versus S versus R trade-off, i.e. of his application of the principle of
821
strategy. Grime’s concept conflicts with our common observation and common sense. We see
822
almost everywhere that plants fill the whole area – why is this, unless through competition (sensu
823
lato: we shall have to include allelopathy here too)? Tilman’s (1988) view is that competition will
824
be equally important in productive and unproductive environments. The logic seems to be that if
825
resource availability is too high for there to be competition, the plants will grow until availability
826
has been reduced so that it is. Moreover, in any environment there will be competition for either
827
mineral nutrients (especially N) or light, competition for which is inversely related (Tilman 1988).
828
These viewpoints are connected to the right-hand part of the humped-back model of species
829
richness. For Grime, at high productivity / standing-crop, i.e. low S and high C, competition and
830
therefore competitive exclusion will be maximal. Wardle (2002) uses this argument to comment that
831
Tilman’s R* model is “difficult to reconcile with the frequently observed humped-back relationship
832
between diversity and productivity”, because according to Tilman competition, and hence competitive
833
exclusion, will be no greater at high biomass. Wardle’s statement is misleading for several reasons:
834
(a) the relation is far from universal, especially with statistical significance from an appropriate test,
835
(b) the usual relation has been with richness, not diversity, (c) productivity has hardly ever been
836
measured, only above-ground standing crop, and (d) the logic is based on the downturn in richness at
837
high standing-crop being due to competitive exclusion, which even Wardle admits is only “a likely
838
reason”.
839
Grace (1991 %583) made another important point: “both Grime and Tilman discuss
840
gradients in habitat productivity as if it makes no difference whether they are gradients in
841
[resources] or non-resource factors”. However, there is more complication. Many studies in the
842
literature examine the effect of a mineral nutrient such as N in a system where competition is
843
probably for light, or even necessarily for light by the experimental design. For example, Stern and
844
Donald (1962) added N to a grass and a clover growing with their roots separated. In this example
Wilson and Agnew, chapter 6, Theories, page 28 of 38
845
the gradient is a resource, N, but the competition is not for N, but for a different resource – light.
846
The true distinction is between a gradient in a factor for which there is competition and in a factor
847
for which there is no competition.
848
The growth-rate artefact
849
A huge complication in experiments to test the Grime versus Tilman ideas on competition is
850
that, by definition, in conditions favourable for growth the plants will grow faster and hence be
851
larger and come into competition sooner. Therefore, if competition is measured at a fixed time after
852
planting, it will appear to be greater in more productive conditions. This situation mirrors that after
853
natural disturbance. Competition will eventually be 100% right along the gradient because the
854
plants will grow until carrying capacity is reached and competition is complete in the community-
855
matrix sense, that if x grams of plant material are removed growth will resume until there are x
856
grams more. Therefore competitive intensity cannot be measured as the final outcome either.
857
Competition is like death: it’s not a question of if but of when. This problem of the growth-rate
858
artefact is removed when the conclusion is one of lower competition at higher nutrients, but it is
859
difficult to accept only results in one direction.
860
Our own hypothesis
861
Our own view, from first principles, is that along a beta-niche gradient (i.e. a gradient of
862
conditions, of non-resources, or of resources for which competition is not occurring), competition
863
will be of constant intensity, but will appear to be greater in more favourable conditions because of
864
the growth-rate artefact. Along a gradient of a resource for which there is competition, competition
865
will be strongest when the resource is in shortest supply. There can be exceptions, e.g. sometimes at
866
low concentrations of a mineral nutrient it is so immobile that there can be little competition for it
867
(Wilson and Newman 1987). The same could apply to water. An additional complication is that as
868
the availability of resource X increases along a gradient, the plants may change from competing for
869
X to competing for resource Y.
870
Deserts
871
The clearest case of competition under low resources is deserts. It cannot be denied that the
872
desert habitat is stressful, and if there be competition it is likely to be for the same factor that causes
873
the stress: water supply. Many, from Shreve (1942) through Went (1955) to Mirkin (1994) have
874
denied that desert plants compete. This idea was fuelled by studies that failed to find a regular
875
spatial pattern of individual plant in deserts, and sometimes found clumping instead (e.g. Gulmon et
876
al. 1979). The idea was often that plant populations in deserts were kept below 100% occupancy by
877
unfavourable probabilities of colonisation and death. This is intrinsically unlikely, since
Wilson and Agnew, chapter 6, Theories, page 29 of 38
878
colonisation and death would have to balance exactly to prevent the population going to zero or to
879
infinity. Anyway, the existence of intense competition for water has been demonstrated by finding
880
negative correlations between plant sizes and distance apart (Yeaton and Cody 1976 %689) and by
881
relief of plant water stress and increase in plant growth upon removing neighbours (Fonteyn and
882
Mahal 1978; Robberecht, et al. 1983; Fowler 1986 %89; Kadmon and Shmida 1990). In fact, the
883
effect of competition on plant spatial pattern has been best demonstrated in desert communities.
884
Ecologists have trended to underestimate the intensity of competition in these environments because
885
of the slow growth of perennial plants, and the apparent unvegetated gaps between plants. The cacti
886
and shrubs may be spaced out, but their root systems are not (Woodell et al. 1969). Clements knew
887
this, of course: “The open spacing of desert shrubs in particular suggests some indirect influence in
888
explanation, but studies of the root systems demonstrate that this is a result of competition for water
889
where the deficit is great” (Clements et al. 1929, p. 317). However, population regulation could
890
occur via herbivory or the spatial mass effect.
Wilson and Agnew, chapter 6, Theories, page 30 of 38
10000
1000
Biomass (g m-2)
Arrhenatherum
Bromus
Dactylis
100
Desmazeria
Festuca
Lolium
Poa
10
1
0.001
0.01
0.1
1
10
Relative nutrient concentration
120
Competive suppression
100
Arrhenatherum
80
Bromus
Dactylis
60
Desmazeria
Festuca
Lolium
40
Poa
20
0
0.001
0.01
0.1
1
10
Relative nutrient concentration
Fig. 6.7: The effect of nutrient concentration on competitive ability
891
What else would limit plant growth in unproductive sites under C-S-R theory if competition
892
does not? Disturbance? But it is the basis of the C-S-R triangle that stress sites cannot have much
893
disturbance, or no plants can grow. Herbivores and defences? But it is a tenet of C-S-R theory that
894
plants of unproductive sites have more defences Grime (2001). The intensity of competition is likely
895
to be approximately 100% in all communities, supporting Tilman’s conclusion, perhaps for different
896
reasons.
897
Tests
898
The complete absence of competition would be testable. However, we argue above that this
899
is not tenable. Anyway, no habitat can fall exactly in the S corner so the question does not arise. We
900
have to test degrees of competition along an S–C gradient, which is possible but difficult. The very
901
concept of intensity of competition has proved difficult and controversial, with arguments about
902
indices. We shall try to judge the effect of competition on a species by it percentage reduction from
903
monoculture, ideally in RGR but sometimes in biomass.
Wilson and Agnew, chapter 6, Theories, page 31 of 38
904
An interesting experiment is that of Campbell and Grime (1992), growing seven species in
905
outdoor plots with a range of nutrient levels and disturbance regimes. Nutrients promoted growth
906
considerably (Fig. x). Campbell and Grime declare that Arrhenatherum elatius is a plant of fertile
907
soils, and Festuca ovina, Bromus erectus and Desmazeria rigida are plants of infertile soils, but
908
actually the nutrient response does not differ between species (test for heterogeneity of slopes on a
909
log-log basis, p = 0.989). The results are directly relevant to our question (Fig. y), because it turns
910
out that although the species differ in the effect of competition on them (p < 0.001 by analysis of
911
covariance, with log of nutrient concentration as the independent variate), there is no overall effect
912
of nutrient supply on the effect of competition on biomass (p = 0.072 for a joint residual
913
regression). Goldberg et al. (1999 %1118) found in a meta-analysis that there was a tendency for
914
competitive intensity to decrease more often than increase with productivity, in conformity with our
915
theory and Peltzer and Wilson (2001) found no significant trend with standing crop, used as in
916
inverse proxy for stress. However, the experiment of Campbell and Grime, as many of those
917
surveyed by Goldberg, has the restriction that we cannot tell whether competition was for the
918
resource (NPK) that varied along the gradient. This restricts the range of investigations very
919
considerably.
920
The experiments of Peltzer et al. (1998 %465) in Saskatchewan, Canada, and Cahill (1999
921
%466) in Pennsylvania, USA, were both in oldfields, planting seeds or seedlings into plots where
922
shoot competition was prevented by tying back the vegetation, root competition was either
923
prevented or allowed by using plastic tubes, and fertiliser (N in the case of Pelzer et al. and NPK in
924
the case of Cahill) was added or nor. Both studies showed somewhat greater belowground
925
competitive effects when soil resources were in shorter supply. Cahill recorded soil moisture with
926
gypsum blocks, and found no significant difference between treatments, implying so far as one can
927
from non-significance that the competition was not for water. This confirms the conclusion of
928
Wilson (1988 %279), surveying experiments on root competition, that the limited evidence
929
available indicates that competitive intensity is highest when soil resources are in shortest supply. In
930
those experiments we know that the gradient is one of soil nutrients, and we know that competition
931
is for soil nutrients or water, but generally we do not know just which resource. The study that
932
comes closest to answering the question is that of Wilson and Tilman (1991 %1050) at Cedar
933
Creek, an experiment similar in most respects to those of Peltzer et al. and Cahill. It is known from
934
other work that nitrogen is the limiting mineral nutrient in the oldfield at Cedar Creek, other
935
nutrients were applied to all treatments to ensure this was true in the experiment (right down to Cu,
936
Co, Mn and Mo), and only N (ammonium nitrate) differed between treatments. It therefore seems
937
likely that we are looking at competition for N along a gradient of N supply. Moreover, RGR is
Wilson and Agnew, chapter 6, Theories, page 32 of 38
938
available to judge the result. In all three species used the belowground competitive effect was
939
greater at low soil N supply. An experiment with one of the same species confirmed this (Wilson
940
and Tilman 1991 %599). The evidence is not perfect, but it overwhelmingly supports our contention
941
that competition for resource X will generally be most severe when X is in shorter supply. It is
942
surprising that anyone thought otherwise. However, we have to expect nutrients to be patchy (this
943
vol., chapt. 4, sect. #), Fitter and students, jbw will ask] [JBW will think about ecotones]
944
Coming to the effect of conditions, La Peyre et al. (2001) grew three species of
945
salt/freshwater marshes in monoculture and competition along a salinity gradient. A measure of the
946
overall importance of competition was almost constant along a gradient, and once allowance is
947
made for dead material the competitive response of the individual species varies remarkably little.
948
Similarly, Cahill (1999 %466) found no consistent change in aboveground competition in his
949
oldfield experiment between the two NPK levels. Although N, P and K are resources, in the latter
950
comparison there is competition only for light, so they are conditions. These two pieces of work
951
support our thesis that along a gradient of conditions, competition will be of constant intensity.
952
10 Synthesis
953
Theories and switches
954
None of the models yet produced for plant communities have high synthetic or predictive
955
value. We deeply respect Frederick E. Clements’ knowledge of vegetation in the field, as well as his
956
powers of observation and generalisation. His experimental studies on competition (Clements et al.
957
1929) were a huge advance and still most of what we know about competition can be found in his
958
writings. His ideas on succession, whilst a simplification, contain a good deal of truth. His tendency
959
to name communities is being continued today. Since the same community does not generally recur
960
(Wilson et al. 1996 %471) such classification is a simplification, but it does little harm when the
961
‘associations’ are not taken too seriously and it is admitted that the main purpose is to identify
962
conservation targets to the public and to government. His concept of the plant community as a
963
organism is mainly harmless, because it is hard to see what it means. We dedicate this book to him.
964
We can accept that variation is sometimes continuous along environmental gradients but at
965
other times discontinuous because of the operation of a switches, as both Clements and Gleason
966
noted. Gleason spent considerable time in the field, and if that was primarily as a taxonomist he
967
clearly looked at the vegetation patterns. Mike Austin and co-workers have done excellent work
968
characterising the shape of variation along environmental gradients. Austin’s curves are continuous.
969
This is partly a result of his methods, but also because he was working with a larger spatial extent
970
than that on which most switches occur. Nevertheless, there is increasing interest in geographic-
Wilson and Agnew, chapter 6, Theories, page 33 of 38
971
scale switches (this vol., chapt. 3, sect. 5.4.A). What Gleason saw as one aspect of plant
972
distributions, Bob Whittaker simplified and took as the whole, adding his idea that that species co-
973
evolve to separate their positions on that gradient. There is no evidence of this, and the observation
974
that the species assemblages we see today are quite different from those in earlier post-glacial times
975
(this vol., chapt. 5, sect. 9), and probably from those in earlier interglacials, make such precision
976
intrinsically unlikely. We argue below that coevolution between plant species is unlikely anywhere.
977
However, Clements saw, Gleason saw, and we can all see that there are many sharp
978
boundaries in nature due to reaction / environmental modification / switches. This is true even of
979
many boundaries that we see as ‘environmental’ such as between a saltmeadow and a saltpan, and
980
such as a riverbank. The rôle of switches in generating the spatial patterns that we see has been
981
considerably underestimated.
982
Philip Grime’s C-S-R theory is the only overall theory of plant communities. Our
983
conclusion is that it is very much a generalisation, with many exceptions, but we accept that this can
984
be useful. It has also spurred the collection of an excellent database of plant ecological characters,
985
and set the example for other datasets, which because of current funding models have been of
986
considerably lower quality. Tilman’s concept that competition will be equal along a productivity
987
gradient is close to the truth, but his R* approach seems to be much too simplistic for
988
embryophytes.
989
Wilson and Agnew, chapter 6, Theories, page 34 of 38
990
The features of plants
991
Anna Bio entitled her Ph.D. thesis (2000): “Does vegetation suit our models?”: a neat
992
criticism of our tendency as plant community ecologists to produce models and then try to make the
993
vegetation fit.
994
995
The nature of the community depends on the nature of its parts, and although there has been
996
useful introgression of ideas into plant ecology from animal and bacterial ecology, we need to start
997
from the particular and often unique characteristics of plants. We attempted to describe these in
998
chapter 1, section 1.1. In vegetatively-reproducing or apomictic plants it is often arbitrary when one
999
individual becomes two, and anyway plants are hugely plastic. There is therefore no basic
1000
demographic or genetic difference between growth, vegetative reproduction and apomictic
1001
reproduction, and in demographic terms between them and sexual reproduction. The basic unit is
1002
the module, often the leaf. All types of growth are an increase in the number of modules. However,
1003
even modules can be plastic in size and the best measure of growth and abundance is biomass, or
1004
better still calorific value. Since the individual plant is not a real entity, the species plays the part of
1005
an individual in the community. The rôle of a species in a community depends on its shape and
1006
secondarily its physiology and chemistry. Its reaction on the environment and on associated biota
1007
flow from these. Plants cannot move around freely, but they can move by vegetative reproduction
1008
and apomictic seeds. Moreover, most have disposable photosynthetic modules, and must move in
1009
space as they produce new ones. They also move through their litter production. Animals, in
1010
contrast, generally stay within a rather fixed body once they reach adulthood, replacing molecules
1011
within that body. As we said “Plants move, animals don’t”.
1012
Community assembly
1013
These characteristics of plants produce a range of interactions within and between species
1014
(Box 6.1). Some, such as competition and some types of mutualism, have been widely discussed.
1015
Other types of interactions have rarely been considered in a community context. Litter effects are
1016
part of a plant’s extended phenotype, which can affect its offspring and have lasting effects,
1017
especially if there is a switch operating. The reaction of plants does not stop when they die. It will
1018
be difficult for vegetation to suit our simple models when the plants can interact in so many ways,
1019
and when their effects often live on.
Wilson and Agnew, chapter 6, Theories, page 35 of 38
Box 6.1: Types of interaction between X species Y
Interference (negative effects)
competition: X removes resources from the environment, which are then unavailable to Y
allelopathy: X produces a substance toxic to Y
parasitism: X removes resources directly from plants of Y
spectral interference: X changes the R/FR balance, disadvantaging Y
pest carriers: X is a ± symptomless carrier of a pest to which Y is susceptible
[other negative interactions]
Subvention (positive effects)
mutualism = X and Y both benefit relative to their being at the same density on their own
1020
benefaction = X benefits Yas above, with no known advantage/disadvantage to itself
1021
facilitation
= X benefits
Y, to itsdirectly
disadvantage
Actually, plants
rarely interact
with each other. Parasitism and strangling lianes are
1022
examples, and the fascinating and understudied case of physical abrasion. Interactions via
1023
herbivores, fungi and microbes are probably more important. The third type of interaction is via the
1024
environment. In the short term this includes interference and subvention. In the longer term it
1025
comprises reaction – plants changing their own environment. Most kinds of interference and
1026
benefaction are based on reaction too, but with lesser and more temporary change. Long-term
1027
reaction can result in either change via relay floristics / facilitation / autogenic succession, or
1028
reinforcement of the current state via a switch (Box 6.2). The “or” is a simplification since a
1029
accelerating or delaying switch can operate during autogenic succession. Cyclic succession is surely
1030
less common than Watt (1947) supposed, but it seems to occur. There is very rarely good evidence
1031
for it, but there is only marginally more for relay floristics or switches. All three patterns are based
1032
on reaction. Reaction is the plant community. The combination of these processes do not give a neat
1033
pattern (Fig. 3.10) nor does it make it easy to use neat labels. However, it is clear that whenever we
1034
see a sharp boundary in nature without an obvious environmental or historical cause, we should
1035
suspect that a switch is operating.
1036
Coevolution between plant species is unlikely. Communities change. The environment and
1037
the species pool both change, and equilibrium is rare. This would not matter so much if groups of
1038
species moved around the landscape together, but the pollen record tells us clearly that they often
Box 6.2: Types of interaction between plants
species/guild X gives a relative advantage to itself = switch
species/guild X gives a relative disadvantage to itself:
the effect disappears at low density of X (negative feedback) = stability
the effect is density-independent: facilitation and/or autointerference = succession
Wilson and Agnew, chapter 6, Theories, page 36 of 38
1039
associate in different ways (this vol., chapt. 5, sect 9). Even at the present time the vast majority of
1040
species live with different associates in different places (Gleason 1926). Within one community
1041
adjacent species are not predictable in a multi-species mix, since environmental heterogeneity exists
1042
right down to the smallest scales. The major reactions affecting the modules of one ramet/individual
1043
are often those caused by other modules of the same ramet, not by a neighbouring species. For all
1044
these reasons, whole species cannot coevolve to match all these different assemblages. Moreover,
1045
we argued in chapter 1 that evolutionary change in plants is often slow. All this makes coevolution
1046
of species traits impossible in heterogeneous communities, and hardly likely even within
1047
homogenous ones. Therefore, when we find assembly rules they must be due to the assembly of
1048
preadapted species, ones that happen from their evolutionary history in a variety of contexts to have
1049
the right characters for the job. Preadaptation is the key to community ecology.
1050
There are three things we can say about plant communities: (1) almost all comprise many
1051
species, as we discussed in chapter 4, (2) they are heterogenous and (3) we hope there are some
1052
rules governing the assembly of species in them: assembly rules.
1053
Assembly rules
1054
All of our discussion would be little more than natural history were there not some
1055
regularities, or rules, that could be seen in how species assembled into communities. We have to be
1056
very careful in examining apparent evidence, because there are many traps for the unwary null
1057
modeller. The best evidence for assembly rules so far is from character-based rules. There is a trend
1058
in plant community ecology towards analysing plant communities not by the names of their species
1059
but by the characters of the plants. We can see the beginnings of this awareness of characters at the
1060
community level in Jan Barkman’s concept of vegetation texture. In general, distributional evidence
1061
supports guild proportionality, as does the successional study of Fukami et al. (2005). There is little
1062
support from removal experiments, probably because of high experimental error. The use of a priori
1063
guilds has severe limitations, and we strongly advocate seeking intrinsic guilds. The use of texture
1064
instead of discrete guilds avoids classification, but does not avoid the problem of character choice.
1065
The evidence so far comes mainly from herbaceous communities, and the only
1066
comprehensive body of evidence is from the University of Otago Botany Lawn. The coherent
1067
conclusions from that site are compelling, even though we would be cautious about the
1068
demonstration of an assembly rule in a single study. The evidence suggests that canopy relations are
1069
important, even in the shortest grassland communities such as lawns, saltmarshes and sand dunes.
1070
This may be partly because of the types of communities that have been examined so far, and
1071
because of the characters easily measured, since the work of Stubbs and Wilson (2005) on a sand
1072
dune implicates structuring by acquisition of water and soil nutrients there. There is enough
Wilson and Agnew, chapter 6, Theories, page 37 of 38
1073
evidence on even spacing of flowering that allows us to believe that phenological niche
1074
differentiation is important in restricting species assembly too, though we have to be very careful in
1075
examining that evidence. However, the failure of roadside communities to re-assemble in NZ
1076
(Wilson et al. 2000 %757) indicates that the assembly rules are weak. Such assembly rules have
1077
been demonstrated in relatively homogenous communities, often homogenous by imposition of
1078
uniform disruption: mowing, tidal submergence, annual drought. Examples are the Otago Lawn
1079
(locus classicus!), the Ynyslas slack and the saltmarsh.Assembly rules may be invisible in
1080
heterogeneous communities because: (1) they are ephemeral, applying only to a transient stage in
1081
ecesis and/or (b) they are dimensionless, applying only at point locations.
1082
Heterogeneity
1083
1084
1085
Interpretation of heterogeneity is deceptively simple. Our model for judging community
processes can start with environmental heterogeneity or homogeneity.
Heterogeneity in the underlying environment has been the usual assumption. It is very hard
1086
to get away from heterogeneity. Deserts appear uniform, but have damper depressions and even
1087
dunes. Alluvial flood plains do not receive uniform deposits because rivers meander and even
1088
split/rejoin; the deposits are reworked by the original river, and then by smaller streams as the river
1089
is lost. The same is true on saltmarshes, which are particularly liable to sharpening into a mosaic by
1090
a switch. There is then the truism that species differ in their environmental tolerances which we can
1091
assume from their environmental distributions: the “easy task” of Warming (1909). So, we assume
1092
environmental heterogeneity and different species tolerances.
1093
Alternatively we can start explaining this pesky heterogeneity in vegetation by starting with
1094
a uniform underlying environment. We then have to assume ‘random’ dispersal of species to give
1095
some pattern. Too little inward dispersal would leave gaps and too much would give uniform cover,
1096
so we have to assume infiltration invasion (chapt. 1, sect. #), which conveniently seems to be the
1097
norm. Then we have to assume that those colonists react on their environment, and we gave plenty
1098
evidence for this when discussing switches (chapt. 3, sect. #). Further, we must assume that species
1099
differ in their reaction is often in the direction that favours their good selves, and we have switches
1100
sharpening the differences into a mosaic. Without switches the tendency would be relay floristics,
1101
with a homogenous endpoint. The assumptions here are infiltration invasion and switches.
1102
Almost certainly, both processes occur, and do so simultaneously. The greatest gap in our
1103
knowledge is the degree to which the species of one community differ in their reaction. Effects can
1104
be seen readily in the light regime beneath different species. Soil reactions occur much more
1105
slowly. It is clear that a few species, such as Calluna vulgaris (heather) and Sphagnum spp., differ
1106
strongly from their neighbours in their reactions. Whether this is general, for example whether the
Wilson and Agnew, chapter 6, Theories, page 38 of 38
1107
canopy trees in a forest generally differ, is basically unknown. We can see local soil/species
1108
correlations, but distinguishing cause from effect is difficult. Experiments with soil litter bags
1109
normally last 2-5 years, rather than 50 years, and usually examine the litter, not the nearby soil. We
1110
believe that reaction on the environment has been bigtime underestimated as the cause of
1111
heterogeneity, and we call for people to investigate it, but not us because soil is messy.
1112
“I can’t see who’s in the lead, it’s either Oxford or Cambridge”
1113
This is the state of community ecology. We are sometimes asked how assembly rules should
1114
be applied to practical problems. This should be one of the eventual aims for scientific theories.
1115
Unfortunately, ecological theories are sometimes applied when there is too little support for their
1116
truth. Theories of community structure are at a very early phase. Perhaps we have good evidence
1117
that they operate for one site, but we do not know how, and we have very little knowledge of how to
1118
extrapolate to the world: whether such rules exist in all communities and if so whether they are the
1119
same in all communities. Actually, we don’t even know what causes heterogeneith. As Mao Zee
1120
Tzung is claimed to have said when asked what the effect of the French Revolution had been on
1121
subsequent history: “It is too soon to tell”.
1122
Plants are simple to physiological ecologists, operating not so far above the level of physics.
1123
Even so, they have found it hard to produce general theories, except that of adaptation which is
1124
dangerous if applied uncritically (Gould and Lewontin 1979). Population ecologists, working at the
1125
level below community ecology, can see clear patterns such as a logarithmic decline when death
1126
rates are constant (Harper 1967), but the main principle seems to be density-dependence, which we
1127
argued above is logically an almost necessary feature of a persisting population. In ecosystem
1128
ecology, at the level above community ecology, it is possible to see some patterns imposed by the
1129
laws of conservation of matter and of energy. We community ecologists are in the worst situation.
1130
Theories fail. When we try to generalise from first principles and from hard evidence, as we have
1131
here, the best evidence we have is for the Botany Lawn. In that one community it is clear that
1132
assembly rules are operating, but we do not know whether they are based on aboveground or
1133
belowground plant interactions. As in John Snagge’s famous declaration during an Oxford versus
1134
Cambridge University Boat Race: “I can’t see who’s in the lead, it’s either Oxford or Cambridge”.
1135
What we do know is that plant communities are affected by exogenous heterogeneity,
1136
reaction affecting other species and causing autogenic heterogeneity, and preadaptation. All these
1137
lead to assembly rules.