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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, P.O. 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.
Chapter 4. Mechanisms of coexistence and stability
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Alpha-niche differentiation ................................................................................................................... 4
1.1 Resources: type of resource and time of availability ............................................................ 5
1.2 Heterotroph-imposed niches ................................................................................................. 6
1.3 The niche extended by reaction ............................................................................................. 7
Environmental fluctuation: seasonal, annual and decadal change ........................................................ 8
Pest pressure: heterotroph challenges ................................................................................................. 10
3.1 Pathogens ............................................................................................................................ 12
3.2 Herbivory, general ............................................................................................................... 13
3.3 Herbivory of disseminules and seedlings ............................................................................ 13
3.4 Vegetative herbivory ........................................................................................................... 14
Circular competitive networks ............................................................................................................ 15
Allogenic disturbance: disrupting growth, mainly mechanically ....................................................... 15
Competition/dispersal tradeoff ........................................................................................................... 17
Initial patch composition .................................................................................................................... 18
Cyclic succession: movement of community phases .......................................................................... 18
Equal chance: neutrality...................................................................................................................... 18
Inertia .................................................................................................................................................. 20
10.1 Temporal inertia .................................................................................................................. 20
10.2 Spatial intertia: aggregation ................................................................................................ 21
Coevolution of similar competitive ability ......................................................................................... 22
Spatial mass effect: vicinism .............................................................................................................. 22
Conclusion .......................................................................................................................................... 23
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Were there no species coexistence, there would be no need for this book. However, most plant
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communities comprise persisting populations of several species. Populations may increase or decrease
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through neutral drift or weather fluctuations, and species can immigrate or disappear from the local
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community. However, long-term studies such as the Park Grass experiment (Silvertown 1987) and
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Bibury (Dunnett et al. 1998) show that the basic tendency is persistence, for example outbreaks are
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often followed by a decrease back to the original abundance. This coexistence is the fundamental
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statement to be made about plant communities, and how it is achieved is the fundamental problem.
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Resources (e.g. light and nutrients) are almost always limiting and competition between
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individuals and species is demonstrable in all types of habitat, except very soon after disturbance (this
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vol., chapt. 2, sect. 2.5 and chapt. 6, sect. 9.2; Clements et al. 1929). Competitive abilities can never be
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exactly equal, so the result should be the competitive exclusion of all but one species (Gause 1934).
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Therefore, the amazing thing is not that the species in plant communities show any particular patterns of
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coexistence, but that they coexist at all. Hutchinson (1941; 1961) asked: "How [is it] possible for a
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number of species to coexist in a relatively isotrophic or unstructured environment, all competing for the
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same sorts of materials?". He called it the “Paradox of the Plankton”.
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Monospecific stands do exist, by which we mean with only one vascular plant species (Plate 1).
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Table 1 lists those that we have seen ourselves, and there are certainly more. They are often at
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land/water ecotones, in wet places and especially in open water or extreme saline environments. In arid
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countries, a monotonous vegetation of one halophytic species can dominate the landscape (Zohary
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1973). We could generalise that these are habitats where only one species is capable of growth due to a
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harsh environment, or where the exuberance of one species excludes others by competition, but in some
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cases it is hard to know whether to credit the extreme habitat or the high competition, e.g. Phragmites
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communis reedswamps.
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At the other extreme is high species richness. Values depend on the size of the area censused, the
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life form guild being considered (e.g. often trees alone are censused in tropical forests) and the
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recording convention used (rooted or shoot presence, perennially or seasonally visible). Whatever the
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sampling regime, extraordinarily high diversities can exist. Tropical rain forest is always quoted as an
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example. Valencia et al. (1994) found 473 species of tree (individuals >5 cm dbh) in 1 ha of Ecuadorian
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tropical rain forest, while Richards (1996) tabulates other examples with over 100 species in 1 ha in
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New World and Malesian (not African!) tropical forests, Naveh and Whittaker (1979) recorded 179
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vascular species in 0.1 ha of a dry shrub/grass community in Israel. Mean species richness of 18.3 per
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0.01 m2 has been found in bryophyte carpets in the per-humid West Cape in New Zealand (Steel et al.
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2004) and 12.2 species at that scale in limestone grassland on Oeland, Sweden (van der Maarel and
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Sykes 1993).
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When we talk of coexistence, the question must be asked at a particular spatial scale. Rainforest
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trees such as Swietenia mahogoni (mahogany) occur in the tropics, and three flowering plant species are
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native to Antarctica, e.g. Colobanthus quitensis. We never wonder how they coexist: they do it by
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growing in quite different places and environmental conditions, that is to say in different beta-niches. In
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fact, to use ‘coexist’ for them is stretching the word. Saltmarsh species (e.g. Salicornia spp., glasswort)
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occur at low altitudes, and alpines (such as Androsace spp.) at high altitudes. Again, we do not ask
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about coexistence. The Paradox of the Plankton as defined by Hutchinson refers to how coexistence can
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occur in a “relatively isotrophic or unstructured environment”. This scale is difficult to define, because
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environmental heterogeneity occurs down to the very finest scales, so all species in a mixture exist as a
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pattern of abundance (this vol., chapt. 3, sect. 1). The species’ patterns will create further patchiness in
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resources since species differ in their resource economies, their reaction on the environment. Numerous
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studies have shown that each species’ individuals affect its soils (sect. 1.3 below). Also, each individual
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by extending over space must sample a spectrum of resource and environmental qualities. Therefore,
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rather than specify a particular scale, we state here that we are concerned with mechanisms that allow
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species to coexist locally, i.e. mechanisms that are not due to imposed habitat heterogeneity within the
Stabilising mechanisms
Niche-differentiation
1. Alpha-niche differentiation (type of resource and time of availability)
2. Environmental fluctuation – season, decadal and gradual change
Balances
3. Heterotroph challenges: pest pressure
4. Circular competitive networks
Escape through movement
5. Allogenic disturbance – disrupting growth mainly mechanically
6. Competition/dispersal tradeoff
7. Initial patch composition
8. Cyclic succession: movement of community phases:
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Equalising mechanisms
9. Equal chance (neutrality)
10. Inertia
Temporal inertia
Spatial inertia: aggregation
12. Coevolution of similar competitive ability
13. Spatial mass effect (vicinism)
area considered.
Wilson (1992) found 12 distinct mechanisms by which coexistence could be maintained:
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(1) Alpha niche differentiation, (2) Environmental fluctuation, (3) Pest pressure, (4) Circular
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competitive networks, (5) Allogenic disturbance, (6) Competition/dispersal tradeoff, (7) Initial patch
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composition, (8) Cyclic succession, (9) Equal chance, (10) Inertia (temporal and spatial),
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(11) Coevolution of similar competitive ability and (12) Spatial mass effect. We believe them to be
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distinct, and we know of no new ones, though we have adopted a different arrangement that we hope
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brings some new insights.
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There is a basic distinction between stabilising mechanisms and equalising mechanisms (Table
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4.2; Chesson 2000). Of the stabilising mechanisms (1 to 8 in Table 4.2), some are due to alpha niche
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differentiation, some involve environmental fluctuation, some are due to balances unrelated to niches
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and some can be categorised as escape through movement (Table 4.2). Species abundances are bound to
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fluctuate, and stabilising mechanisms must include negative abundance-dependence to counter this. [For
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animals, ‘density-dependence’ is often used, but since the concepts of ‘individual’ and ‘density’ are
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difficult in most plants (chapt. 1, sect. # above) the more general ‘abundance-dependence’ should be
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used.] This means that the plants of a species must have higher fitness, and thus biomass should
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increase, when the species is at lower biomass in the community (Chesson in press). Simply, the one
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necessary and sufficient phenomenon for maintaining a species in a mixture is ‘increase-when-rare’1.
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The corollary of this is population limitation, i.e. reduced fitness as biomass increases. Either way, a
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species’ fitness should be inversely related to its abundance. In the short term and in species that
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reproduce only vegetatively we should consider vegetative RGR. In the longer term, population growth
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is the critical question. However, if a species decreases to zero abundance, the long term will never
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arrive for it. The increase-when-rare feature is incorporated into the Lotka-Volterra logistic function, as
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every schoolboy knows. A feature that interferes with this in the real world is the Allee effect, whereby
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populations cannot recover from very low numbers due to low success in mating. We believe that it is
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rare in plants because, as we outlined in chapter1, each individual is effectively a colony and perennials
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have an indefinite life span. Nevertheless there are examples of the effect in Banksia goodii, a shrub of
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dry woodland (Lamont 1993), and in the outpollinated annual Clarkia concinna in California (Groom
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1998). Species with obligate outcrossing and/or scattered distributions and/or monocarpic reproduction
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and/or specialised pollen vectors would be more liable to it.
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True coexistence must be through a stabilising mechanism. Equalising processes do not contain
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an increase-when-rare mechanism, but are ways in which species may persist for a time in unstable local
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coexistence, slowing competitive exclusion. Moreover, if the difference between the competitive
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abilities of species is large, even the presence of a stabilising mechanism may not prevent competitive
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exclusion, and in this situation an equalising mechanism might reduce the difference in competitive
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ability between two species so that the stabilising mechanism is able to cause coexistence (Chesson
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2000 %343). Ultimately every plant has established itself by a process that can be explained by its
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tolerances (its niche) and the environmental conditions prevailing during its ecesis, but the reasons for a
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species' presence in a particular spot are usually obscure. For example a tree may persist for so long that
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the local soil/geomorphological conditions that allowed it to establish have changed. It is therefore
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tempting to suggest that each individual's presence owes as much to chance as to ecological
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differentiation and a theory of equal chance has been proposed to explain species mixtures, as we
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discuss below. Again, species may persist temporarily through inertia of individuals or populations in
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time or aggregation in space. Any process causing similarity in competitive ability is equalising too.
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Lastly, and rather hesitantly, we include the spatial mass effect as an equalising mechanism.
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1 Alpha-niche differentiation
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We discussed alpha niches in chapter 1 (sect. 4.1). It has been pointed out that coexistence by
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alpha-niche differentiation is impossible to disprove. Each species must by definition occupy a different
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niche (chapt. 1, sect. 1.2 above). Moreover, by reaction it uniquely constructs part of its niche. The other
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side of the coin is that if redundancy really occurs, i.e. there are coexisting species that do not differ in
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alpha niche, they will not coexist by this mechanism and some of the 11 other mechanisms mentioned
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below must account for their presence. The ‘increase when rare’ element occurs here because when a
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species is rare the resource that it particularly takes up and requires will be present in greater abundance,
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that is, the niche is not fully occupied, though interference with this process could come through luxury
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uptake of nutrients (Lipson et al. 1996). The population limitation on the other hand is due to full niche
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occupancy, i.e. full use of its resource. The degree of niche separation required will increase with the
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difference in competitive ability between the species; if one species is a very strong competitor another
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species will be able to coexist only if it is occupying a completely different niche. However, in contrast
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to some stabilising mechanisms of coexistence, if the niche differentiation between two species is strong
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enough, they can always coexist.
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1.1 Resources (type of resource and time of availability)
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Tilman (Titman 1976) demonstrated that coexistence was possible between two algae limited by
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different nutrients P and Si, and concluded that the number of species able to coexist is the number of
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resources, and then only if each species is limited by a different resource. He confirmed this in
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modelling (Tilman 1977). *[JBW will see] Huston and DeAngelis (1994) produced a model that
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purported to give coexistence between many species on a single limiting resource if it was patchy and
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resource transport was slow. However, no increase-when-rare mechanism is apparent, and it seems
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likely that the effect was due to immigration of propagules to a system where the advantages of the
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species were similar. *[JBW will see] Vance (1984) produced a model that claimed to show that two
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species can coexist on one limiting resource. However, it depended on “if each species interferes less
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with resource acquisition by the other than with resource acquisition by itself”, which if the only
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interaction is competition must mean niche differentiation (e.g. the one resource is water, but it is taken
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up from different soil strata). The "steady state" that these authors specify will not be realised, but
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environmental variation will bring other mechanisms (sect. 2 below) into play.
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The primary resource requirements of most embryophytes are similar (light, water, CO2, N, P, K,
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minor elements, sometimes pollination and dispersal). The concept of a resource gradient as niche
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differentiation is simple for seed sizes as a resource for birds, but it applies less readily to plants, for
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which most of the resources are discrete requirements. For example one species cannot require a low-
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concentration type of P and another a high-concentration type, and the two cannot occur simultaneously
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anyway. However, in other cases such as soil resources at different depths and pollinator service during
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the season (sect. 2 below), the separation and specialisation of species along gradients are an important
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mechanisms of coexistence (Fig. 5.x; MacArthur and Levins 1967). We should ask how much
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separation is needed, but in spite of the calculations of MacArthur and Levins this question remains
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unanswered for the real world. Even the existence of such niche limitation has been controversial and
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difficult to prove (this vol., chapt. 5).
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Fig. 4.x. The MacArthur and Levins (1967) concept of niche separation along a gradient
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The whole of the above-ground structure of a plant is a light-capture mechanism. Therefore
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gross characteristics of plant form have great relevance. Consider tree size and shape in rain forest,
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where light is the prime resource; Kohyama (1992) and Akashi et al. (2003) concluded from modelling
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that short species, with high seedling recruitment but with height-limited growth, could coexist with
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taller species with lower recruitment rates. This is basically niche differentiation based on canopy strata.
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Kohyama (1993) used the model to show that stable coexistence resulted without requiring a stand
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mosaic and Kubota (1996) showed how just two canopy shapes, conical and spheroidal, interacted with
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speed of recruitment to give situations that allowed a diverse canopy flora. These are subtle and devious
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ways in which resource differentiation takes place in this famous biome. Stratification below ground,
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i.e. in rooting depth, is another important niche gradient (this vol., chapt. 1, sect. 4.3), especially when
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there is both precipitation and an accessible water table.
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Two types of temporal gradient can be seen: (1) If growth is triggered by the resource itself,
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species can differ in their speed of reaction to resource availability, their opportunism. Opportunistic
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species react fast to resource availability, for example production of surface roots of succulents,
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ephemeral leaves like Grewia spp. (cross berry) that have a leaf flush after every rain in African summer
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deciduous bushland, and seasonally produced leaves that must survive periods of resource starvation.
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(2) More commonly seasonal separation of species' growth patterns is controlled not by the resource
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itself but by signals such as daylength and temperature. This causes regular seasonal phenological
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separation of species’ activity. Here, the mechanism overlaps with the Storage effect (sect. 2 below).
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1.2 Heterotroph-imposed niches
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Pollination and dispersal can be switch mediators (this vol., chapt. 3, sect. 5.4.G), but also means of
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niche differentiation. Pollinators come in many sizes and specializations: insects, birds, mammals and
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even reptiles. Among insect pollinators there is huge variation in characteristics, and their interplay with
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plants can be rich and complex. There are robbers, mimics, rewards, guides and warnings. The
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pollination niche is liable to the Allee effect, both for self-incompatible plants when there is no mate in
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the neighbourhood and for those specialised to particular pollinating insects when the plant population is
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not large enough to attract the pollinator. Dispersal tends to be less specialised, without an equivalent to
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the close relation between flower morphology and pollinator morphology seen with some insects and
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birds, but differences in fruiting times could reduce competition for dispersers. An Allee effect is
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possible in dispersal if the population is too small to attract more specialised dispersers. Allee effects
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can neutralise an increase-when-rare mechanism.
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Vascular plants could occupy different niches by associating with different mycorrhizal fungi.
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However, specificity within the two main groups of fungi (VAM, ecto, ericoid/epacrid, etc.) is
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quantitative, in terms of efficacy rather than in absolute ability to colonise the roots. Moreover, the
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effect on the higher plant with all types is on availability of soil nutrients (especially P) and water, and
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the loss is in carbon. We conclude that niche diversification through mycorrhizae unlikely.
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1.3 The niche extended by reaction
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The alpha niche is not a pre-existing box into which a species has to fit. We have emphasised
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that the individuals of a species react on their environment, changing it and to a lesser or greater extent
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constructing their own niche. Ramets of a species always show some sort of pattern of densities (this
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vol., chapt. 3, sect. 1) and this pattern must cause patchiness in the micro-environment of the habitat.
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Litter production is often the basis for nutrient heterogeneity, but plant morphology and root growth can
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also be the cause (Vogt et al. 1995). Habitats, therefore, must always be patchy in resource availability
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and physical environmental actors and the size of the patches depends on the pattern of densities of each
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species. There is much evidence of this, particularly from forests where the sheer size of the trees makes
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their patches large and easy to sample. From many examples we cite Pelletier et al. (1999) who analysed
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the basal soils of more than seven species of North American forest trees and found that each species’
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subcanopy had a characteristic soil, presumably due to root and litter effects. Presumably plants can
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have the same effects, but there are few published studies. This argument is that every plant community
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must show pattern associated with each of its constituent species, but there are other biotic forces
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making habitats more heterogeneous. Litter is not only a significant niche factor, but one especially
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liable to cause change by reaction.
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The necessary presence of patches in a community is important to every species’ foraging
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strategy. Large patches are best exploited by stoloniferous herbs (Wijesinghe and Hutchings 1997).
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Jackson and Caldwell (1996) modelled the effect of root plasticity on the uptake of nutrients from small
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patches versus homogenous environments and found that plasticity was theoretically highly
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advantageous in sagebrush steppe conditions. In the same habitat, patchy soils differentially affected
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Agropyron desertorum (wheatgrass) and Artemisia tridentata (big sagebrush) under shady conditions,
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the former failing in root plasticity, *[JBW will look up] the latter species in root physiology
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compared with uniform nutrient treatments (Cui and Caldwell 1997).
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Of course, the above-ground environment is altered too. Canopy trees create a
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shade/temperature/humidity niche for understorey plants, that might not be able to survive without those
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modifications. Many manifestly cannot do so in competition, since they are restricted to forest
Wilson & Agnew, chapter 4, Species coexistence, page 8 of 25
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understories. Trees also create the niche for climbers and epiphytes via their support, and for many
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epiphytes water and nutrients via stemflow. Parasite plants obviously occupy a niche that would not
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exist without other plants; the term ‘niche construction’ is very appropriate here.
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2 Environmental fluctuation (seasonal, annual and decadal change)
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Species can separate along annual and other changes in the environment, predictable and
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unpredictable. We cannot talk of coexistence caused by millenial-scale fluctuation unless the plants are
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very long-lived (say 500+ yr), because competitive exclusion may happen before the environmental-
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fluctuation coexistence mechanism can operate. We discuss flowering and fruiting niche gradients,
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mediated by pollinators and dispersers, in chapter 5 (sect. 6.2) and species can also separate along niche
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axes of vegetative phenology. An excellent example is the vernal ground flora of deciduous forest.
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Fargione and Tilman (2005 %598) found evidence that vegetative phenological niche differentiation
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added to rooting-depth differences in facilitating the coexistence of species at Cedar Creek with the
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dominant grass Schizachyrium scoparium (bluestem). Separation in flowering times will reduce
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competition for pollinators, giving coexistence based on niche differentiation.
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Environmental fluctuation can cause coexistence if it be on scales shorter than this but long
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enough for there to be feedback on resources. The fluctuation can be one that affects vegetative growth,
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for example the vernal flora of forests and spring ephemerals of semi-arid areas, though there is often an
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accompanying fluctuation in reproduction.
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As will be clear below, there has to be an interaction between growth and resource supply. There
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has been confusion about this. Many authors have claimed that simple variation in the environment and
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therefore in demographic parameters would allow long-term coexistence. For example, Gigon (1997)
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wrote: “The fluctuations and their interferences mean that no species encounters optimal growth
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conditions for a prolonged period of time. Therefore no species can outcompete the others. Fluctuations
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are thus decisive for the coexistence of species”. Coexistence cannot happen this way. For coexistence,
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the long-term growth rate of each species has to be RGR = 0.0 (r = 0.0, λ = 1.0). The long-term growth
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rate for a species is the arithmetic average of RGR (the geometric average of λ) in each period.
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Variation in growth rate will not make it more likely that long-term r is 0.0, in fact a value of exactly 0.0
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due to such averaging is infinitely unlikely. There are only two ways in which temporal variation can
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lead to the coexistence of two species: Relative non-linearity and Sub-additivity. These can cause
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coexistence only if the competitive unbalance between the two species is not too great, and equalising
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mechanisms can contribute to this.
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Relative non-linearity means that two species respond differently to levels of a resource for
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which they are competing, and moreover that they respond by differently-shaped relations. For example,
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the three scenarios in Fig. 4.1 count as different shapes. The way to test for Relative non-linearity of
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shapes is to plot the values of RGR of one species at each level of resource R against the values of the
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other: if the result is a anything but a straight line, the species are relatively non-linear.
C
D
RGR
A
F
B
Rmean
Resource level [R]
Rmean
Resource level [R]
Rmean
Resource level [R]
E
Fig. 4.1: Pairs of two species showing relative non-linearity
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Take the third graph. If [R], the level of resource R, is constant at the mean value (Rmean), species E has
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a higher RGR than F. However, if there be environmental fluctuation around the mean, the mean growth
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rate of F would be higher. Thus, low fluctuation in [R] advantages E, high fluctuation advantages F.
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The reason this matters is that at low [R] species E grows faster than F and therefore depletes the
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resources, at high [R] it grows little more than at Rmean, and leaves much of the R unutilised. Both ways,
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when species E is in the majority it exacerbates the fluctuations in [R]. Conversely when it is in the
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minority, fluctuation in [R] is lower, which favours it: increase when rare is achieved.
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In contrast, species F grows little at low [R], and will hardly deplete R. At high [R] it grows
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disproportionately fast, absorbing R and therefore reducing [R]. Both ways, when species F is in the
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majority it damps down the fluctuations in [R]. Conversely when it is in the minority, fluctuation in [R]
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is higher, which favours it: increase when rare is achieved.
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The second way that environmental fluctuations can cause coexistence is the Storage effect.
There are four requirements for the Storage effect to operate:
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1. The species must be competing for a resource.
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2. They must be affected by an environmental (i.e. non-resource) factor, and respond differently
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to it.
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3. There must be covariance between the environmental factor and the intensity of competition.
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We would expect this, because when the plants are denser or larger competition will be
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more intense. That is, in ‘favourable’ conditions competition will be greater.
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4. There must be subadditivity (= buffering, = an interaction between environment and
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competition). That is to say, the effect of competition on the population of a species
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depends on the environment. So, whilst ‘3’ refers to the intensity of competition, ‘4’
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refers to the effect of competition.
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In years (or other periods) when the environment is favourable for a species, if it is in the majority and
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therefore competing against itself it cannot take much advantage of the favourable conditions because it
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is competing against itself at high biomass: X in Fig. 4.2.
Wilson & Agnew, chapter 4, Species coexistence, page 10 of 25
Competitive intensity
X
Low RGR
High RGR
Environmental favourability
Fig. 4.2: The effect of competitive intensity and environmental favourability on RGR. For ‘X’,
see the text.
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Chesson’s (1994) calculations indicate that the Storage effect is a considerably stronger force than
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Relative non-linearity.
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These mechanisms clarify that the timescale on which environmental fluctuation can cause
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coexistence is set by the timescale on which resource depletion can occur. Light intensity can change
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instantaneously, it cannot be stored from one second to another, and its effects in producing
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photosynthate are quite short-term, so within-day fluctuation could suffice. Water depletion could occur
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over a few days, and nutrient depletion over a few months. Soil nutrients often become more available
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in the spring due to mineralisation but slow uptake over winter, and are depleted during the period of
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active growth, so the Storage effect can operate on within-season or between year variation in nutrient
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use. Seasonal niche differentiation can also be seen as alpha niche differentiation, so long as different
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resource bases are being utilised.
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3 Pest pressure (heterotroph challenges)
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Both pathogens and herbivores (from insects to megaherbivores) have the potential to give an
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increase-when-rare process (we use ‘pest’ to cover both pathogens and herbivores). For this, three
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conditions are required.
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1. Impact: the pests involved must have a significant impact on the growth and/or survival of the
plant species, i.e. their fitness must be reduced.
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2. Specificity: The pests involved must be at least partially specific to the plant species. It could be
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sufficient for the least competitive species to have no specific pests/diseases, but to benefit when
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the others are suppressed by pests/diseases.
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3. Abundance-dependence: The challenge from pests must be less on a sparse than on an abundant
species. This represents an abundance-dependent effect. The requirement is for a lower impact
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on the growth and reproduction of sparse species, but this will presumably be through reduced
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infection.
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If these three conditions all obtain, when any one of the plant species in the mixture becomes more
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abundant, the host-specific pest (Condition 2) will move more rapidly amongst its host population and
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the degree of infestation will increase (Condition 3). This will reduce its fitness (Condition 1). This will
319
not impact other species, or will do so only to a lesser extent (Condition 2). Conversely, when a species
320
becomes sparse, infestation by its specific pests will decrease and its fitness increase relative to its
321
fitness when more abundant, giving the increase-when-rare effect. Again, the strength of conditions 1-3
322
necessary for coexistence depends on the degree of difference in competitive ability, and equalising
323
mechanisms of coexistence can allow Pest pressure to result in coexistence when it otherwise would not.
324
Condition ‘1’ can often be met, since pests have various effects on plant production. Basically,
325
the pest organism must have a carbon requirement, which is almost bound to result in lower production
326
and fitness for the plant. Many pests are quite specific to a species or group of species, meeting
327
Condition 2. Ecologists tend more to question Condition ‘3’ because it is less obvious how abundance-
328
dependence could operate. Possible mechanisms (Boudreau and Mundt 1997) are via: (a) a decreased
329
abundance of palatable / susceptible plants, which inhibits the dispersal of herbivores, disease-spores or
330
disease-vectors, (b) the flypaper effect for disease spores and possibly for insect pests, virus vectors and
331
hence for the viruses they carry, in which the pest is caught by a passive surface, (c) alteration in the air
332
flow and microclimate, (d) chemicals from associated species that repel herbivorous insects, and (e)
333
promotion by an associated species of natural enemies of the herbivorous insects, i.e. their predators.
334
We shall discuss diseases and herbivory separately since they act in different ways with different
335
dynamics. However, there is sometimes evidence for abundance-dependent mortality or a reduction in
336
growth that is circumstantial evidence for the process and therefore for the Pest pressure mechanism,
337
that cannot be pinned down to a particular pest. For example, Packer and Clay (2000) examined the
338
distribution of seedlings of Prunus serotina (black cherry). The greatest number of seeds germinated
339
quite close to their parent tree, 5-10 m. However, 4 months later and thereafter up to 28 months,
340
seedling survival was higher the greater the distance from the parent tree, up to the furthest distance
341
monitored (30 m). This is not always the pattern. Dalling et al. (1998) in tropical rainforest on Barro
342
Colorado Island found that seedlings tended to be denser nearer to an adult of the same species. For
343
temperate forests Houle (1992) found the seedling mortality of Acer saccharum (sugar maple) in an
344
Eastern American forest was not abundance-dependent; there was no particular spatial relation between
345
trees and seedlings. Hyatt et al. (2003), in a thorough review of the literature, found no evidence for an
346
effect of distance from conspecifics on seed survival in either temperate or tropical communities, but
347
there was a tendency for seedlings to show higher survival at distance, with hints that this occurred
348
especially in the tropical forests. This matches the conclusions of Wright (2002 %1) who, with a rather
Wilson & Agnew, chapter 4, Species coexistence, page 12 of 25
349
different review approach, found considerable evidence of low growth performance of saplings near
350
conspecific adults. When effects like this are found, they are assumed to be because of Pest pressure,
351
though Wright discusses other explanations. This kind of pattern recalls the ‘Janzen-Connell’ hypothesis
352
that whilst the greatest density of fruit will be dispersed to near the parent plant, pests will have the
353
greatest impact there, so the maximal regeneration will occur at an intermediate distance from the
354
parent. We would expect this to be an important abundance-dependent method of species' maintenance
355
in diverse, stable communities of trees, specifically tropical rain forest. But it seems that it is far from
356
universal.
357
3.1 Pathogens
358
Pathogens act in the soil, in the plant systemically and in the plant’s photosynthetic and
359
reproductive systems. The impact of fungal pathogens can be considerable. Mihail et al. (1998) found
360
that in a greenhouse experiment with the annual legume Kummerowia stipulacea (Korean clover) the
361
fungus Rhizoctonia solani caused mortality that reduced plant density by 40 % whilst the fungus
362
Pythium irregulare reduced density by 80 %. Mitchell (2003 %147) found that in an oldfield grassland
363
at Cedar Creek 8.9 % of the leaf area was infected by fungal pathogens, which decreased root
364
production by 25% by decreasing leaf life, while herbivores had no effect.
365
366
367
The species-specificity requirement is less easy to meet. Gilbert (2000) concludes that the
evidence so far indicates that in natural communities that most fungi infect a large number of hosts.
The abundance-dependence criterion can often be met. Most ephemeral pathogens are
368
transmitted aerially including rusts and smuts which affect leaves, stems and floral parts. Abundance of
369
the host plant affects the pathogen's population and its persistence, and the transmission of specialist
370
pathogens can be highly sensitive to the identity of other host species in the community (Boudreau and
371
Mundt 1997). An example is the Ustilago violacea smut on Silene alba (≡ S. latifolia; white campion),
372
for which Thrall and Jarosz (1994) experimentally compared the behaviour of the host and pathogen
373
populations to theoretical models. The match was good and showed that both density dependence and
374
frequency dependence occurred. An excellent study by Burdon et al. (1992) described the mortality of
375
Pinus sylvestris (Scots pine) caused by the snow blight fungus Phacidium infestans as being mostly
376
abundance-dependent, with greater mortality in subsites where the host had been denser the previous
377
year. This abundance-dependence has sometimes been shown to lead to a lower pathogen load in
378
mixtures, which must imply some host specificity. Mitchell et al. (2002 %1713) examined 147 plots in
379
an experiment at Cedar Creek established by Tilman and co-workers, sown and weeded to species
380
richness from 1 to 24 species. The percentage of each leaf visibly infected was guessed, using calibrated
381
cards as a guide. Infection dropped as species richness increased, the 24-species plots having only 37%
382
the foliar fungal pathogen load of the mean monoculture (though more than the least-infected
383
monoculture). Similarly, Mitchell et al. (2003 %438) analysed another Cedar Creek experiment sown
Wilson & Agnew, chapter 4, Species coexistence, page 13 of 25
384
and weeded to 1 to 16 species, and the pathogen load in the 16-species plots was only 34% of that in the
385
mean of monocultures. In chapter 3, sections 6 and 7.5 we described the ‘selection’ artefact in overyield
386
and invasion-resistance experiments. A similar artefact would be possible here if the species less
387
susceptible to disease had thereby a competitive advantage and increased its proportion in the mixture,
388
so that the mixture had a lower mean pathogen susceptibility and thus a lower pathogen load. However,
389
Mitchell et al. (2002; 2003) present evidence that this is not the cause of the effect they found. Mitchell
390
and Power (Collinge %58) conclude that “the transmission of specialist pathogens can be highly
391
sensitive to the identity of other host species in the community”.
392
Similar effects could be caused by below-ground pathogens. Bever (2003) modelled this, but
393
concluded that there is no evidence for it yet.
394
3.2 Herbivory, general
395
Herbivores come in all sizes, specialisations and guilds. On vegetative parts there are leaf eaters,
396
stem borers and root eaters. On reproductive systems there are flower exploiters, frugivores and
397
granivores. Plant species are variously adapted to herbivory, with chemical and physical defences, life
398
histories and growth patterns that have evolved seemingly to deal with the challenges. The potential
399
mechanism for coexistence via herbivory is similar to that for pathogens. However, whilst pathogens
400
often reduce the functional efficiency of plant parts, most herbivores simply remove plant material so
401
that the plant needs to regrow to replace tissue and thus its resource base (cf. chapt. 2, sect. #).
402
Obviously we can expect a great variety of relationships between plant species and their herbivores,
403
including symbiotic ones, such as the Yucca moth (James et al. 1993). In many of these systems
404
herbivores exploit plant populations in an abundance-dependent way. Grover (1994) modelled this and
405
used the keystone concept (this vol., chapt. 5, sect. 11) to suggest that a controlling herbivore is one that
406
destroys a plant species that could become a dominant competitor. We may distinguish between
407
abundance-dependent culling of seeds and seedlings and wholesale removal of plant material, i.e.
408
vegetative herbivory.
409
3.3 Herbivory of disseminules and seedlings
410
Seeds and seedlings are a rich nutritional resource and are heavily predated. Maron and Gardner
411
(2000) showed by modelling that herbivores can control adult population abundance by limiting the
412
seed input to the seedbank. Such limitation seems to be widespread. It occurs also via vegetative
413
disseminules. Thus, the ‘impact’ requirement can be met.
414
Disseminule herbivory can often be abundance-dependent. Cygnus bewickii (swans) eat the
415
turions (disseminules, fleshy buds) of Potamogeton pectinatus (pondweed) in the autumn. Jonsen et al.
416
(2002) demonstrated clear abundance-dependent control of the P. pectinatus in which the denser patches
417
of turions were exploited, reducing their density, while areas of low turion densities were unexploited
Wilson & Agnew, chapter 4, Species coexistence, page 14 of 25
418
and here the plant density subsequently increased. Edwards and Crawley (1999) examined four species
419
of British meadows and found that granivory by rodents was abundance-dependent, but its effects on
420
adult densities differed. Densities of species with bigger seeds (Arrhenatherum elatius, oat grass; and
421
Centaurea nigra, knapweed) appeared to be reduced, but in the smaller seeded Rumex acetosa (sorrel)
422
and Festuca rubra survival increased to compensate for seed predation, with no overall effect on plant
423
density. Again, Ehrlen (1996) found that in Lathyrus vernus (spring pea), although seed predation by a
424
Bruchidae beetle was correlated with seed density in small plots and with inflorescence size, this had no
425
consistent effect on plant population recruitment. Thus, even the occurrence of abundance-dependent
426
seed predation is no guarantee that it will control the population and hence contribute to species
427
coexistence.
428
Another limitation of disseminule/seedling herbivory as a mechanism of coexistence may be that
429
most mammal granivores are not specific to one species. There is huge literature assuming that bird
430
granivores are restricted by beak size to a particular range of fruit/seed sizes, but not to one species.
431
However, species of Bruchid beetle are generally restricted to the seeds of one or a few species of
432
Fabaceae (legumes). Seedlings are presumably eaten by invertebrates, but they are likely to be quite
433
generalist.
434
3.4 Vegetative herbivory
435
The impact of herbivory on vegetative parts can be considerable, both by vertebrate herbivores
436
(Jones 1933) and by insects above and below-ground (Brown and Gange 1989). The selectivity of
437
herbivores varies widely from megaherbivores that take large mouthfuls rather indiscriminately such as
438
horses and elephants, through more selective ungulates, to tiny flower gall wasps specific on one or a
439
few plant species and Lepidopterans feeding on one species (this vol., chapt. 2, sect 4.3), such Tyria
440
jacobaeae as (cinnabar moth) on Senecio jacobaea (ragwort): Plate 4.2. *(ref. from Andrew).
441
There are cases when coexistence can be attributed rather clearly to insect vegetative herbivory,
442
for example Carson and Root (2000) found that periodic plagues of folivorous chrysomelid beetles
443
checked populations of the dominant Solidago altissima (goldenrod) in an oldfield in New York state,
444
USA, and were responsible for the diversity and successional rates. The effect of vertebrate grazing in
445
increasing species diversity is well known, as shown by the rabbit exclosures erected by Tansley and
446
Adamson (1925). However, the effect there is surely that when the sward is higher, light competition is
447
more important, and especially there is more opportunity for the feedback between the outcome of
448
competition and competitive ability to occur (this vol., chapt. 3, sect. 1.5), allowing competitive
449
exclusion. This has nothing to do with the any mechanism of coexistence.
Wilson & Agnew, chapter 4, Species coexistence, page 15 of 25
450
451
3.5 Pest pressure conclusions
The Pest pressure effect seems most likely to operate via diseases. However, there can be
452
complex interactions. An example is seen on Netherlands sand dunes, on which there are relatively
453
uniform soils and clear successional sequences. The growth of the pioneer Ammophila arenaria
454
(marram grass) is impacted by nematodes and pathogens (Van der Stoel et al. 2002). The nematodes
455
reduce growth only early in succession and early in the season, and are not significant in the marked
456
decline in vigour commonly seen in older stands of A. arenaria. However, there is apparently a
457
synergistic effect between fungi, and between fungi and nematodes, which reduces A. arenaria’s
458
growth, and this is important in competition with Festuca rubra, the next dominant in the succession
459
(Derooijvandergroes 1995; Van der Putten and Peters 1997). Later in the succession, in nutrient poor
460
grassland, there is often a mosaic of Festuca rubra and Carex arenaria (sand sedge). Here Olff et al.
461
(2000) discovered that each species had phases of increased and decreased vigour, replacing each other,
462
and that this process was associated with pest phases, particularly the plant-feeding nematodes. Each
463
species seems to be affected by different groups of pests, leading to the changing mosaic aspect of the
464
vegetation, which might look superficially like cyclic succession (this vol., chapt. 3, sect. 4).
465
4 Circular competitive networks
466
Interference relations between a set of species are said to be transitive if the species can be
467
arranged in a pecking order, such that a species higher in the order can outcompete any species lower
468
down (this vol., chapt. 5, sect. 4.3). The opposite situation is the existence of circular competitive
469
networks (Fig. 4.3). If such networks exist, they would contain an increase-when-rare mechanism: as
470
species A starts to displace species B, species C increases because it has high competitive ability against
471
A, but then it in turn is replaced by B, completing the cycle. However, it is hard to see how circular
472
competitive abilities could exist, and they seem to be rare or non-existent (this vol., chapt. 5, sect. 4.3).
473
They are almost certainly not an important mechanism of coexistence.
species A
species C
species B
Fig. 4.3. A circular competitive network between three species.
474
475
476
5 Allogenic disturbance (disrupting growth, mainly mechanically)
Disturbance can have the same effect as climate variation (Roxburgh et al. 2004), but the true
Intermediate-timescale disturbance mechanism is a patch mechanism: within an area there are patches
Wilson & Agnew, chapter 4, Species coexistence, page 16 of 25
477
of different time since disturbance, with different suites of species (Wilson 1994 %176). This gives a
478
successional mosaic. Whether this comprises coexistence depends on the scale at which the system is
479
viewed. Coexistence is seen only when considering a scale that is larger than the size of a disturbance
480
patch, so that it includes patches of differing time since disturbance – newly-disturbed versus recovered.
481
The different patch types are different beta niches but on a small scale, and a species specialising in a
482
particular patch type will increase when rare because it will have more of its specific resources
483
available. In a sense, we should therefore not count Allogenic disturbance as a mechanism of
484
coexistence; we do so here because it is so frequently seen as one, because of the impossibility of
485
defining the target scale, and because disturbances occur on all scales so that however small a scale we
486
examine there will still be disturbances within it. The disturbance does need to be sufficiently frequent
487
that each patch will usually include patches at various stages of recovery, or the mechanism will not
488
operate.
489
All sorts of allogenic disturbances happen and it is not always easy to separate disturbance from
490
climatic stress, i.e. the environmental fluctuation discussed above (sect. 2 above). The characteristics of
491
disturbance are: (1) Plants not only fail to reproduce but are killed, at least above ground. (2) Most
492
species are killed, not just those that cannot tolerate a particular stress. (3) The event is sudden. (4) The
493
environmental effect is temporary, i.e. it is a pulse perturbation, so the original species can re-establish
494
the composition of the patch. However, the real difference is that Allogenic disturbance is a between-
495
patch mechanism. Disturbance is common, creating gaps over the landscape at a range of scales from
496
meteor hits (many km2) to worm casts (about 0.03 m). Fossorial rodents, ants and termites act at scales
497
which can be important for individual plants. A good example is that of McGinley et al.’s (1994)
498
description of enriched harvester ant mounds in western Texas. It is possible that much the variation that
499
we see in communities is due to old disturbances, where vegetation cover has been regained, and
500
obvious pioneers have been eliminated, but the species composition is different. Perhaps we do not
501
realise this because we fail to recognise mid-succession species as being such (Veblen and Stewart 1982
502
%413).
503
The Allogenic disturbance mechanism assumes that there are distinct pioneer and climax
504
species, i.e. r and K, R and C-S. However, we are talking of secondary succession, and cannot assume
505
this. Peterson and Pickett (1995) found that after windthrow disturbance in a North American conifer /
506
deciduous forest some species regenerated by the germination of seed and some from already-present
507
seedlings, but pioneer shade-intolerant species were sparse, apparently due to a lack of propagule input.
508
Autosuccession, in which the climax species immediately re-establishes after a disturbance, is known
509
from mesic areas such as after windthrow in temperate Nothofagus rainforest in New Zealand
510
(Cockayne 1926), but it is specially found under environmental stress, as predicted by C-S-R theory
511
(this vol., chapt. 6, sect. 6.7; Wilson and Lee 2000). We might expect that the greater species richness in
Wilson & Agnew, chapter 4, Species coexistence, page 17 of 25
512
tropical rain forests would include a good number of gap specialists. Indeed, Hubbell (2005 %166)
513
demonstrated for Barro Colorado Island tropical rainforest a close negative correlation among species
514
between survival rate in shade and growth rate in full light (in gaps), though admitting there were rather
515
few gap species and their abundance was low. Wright et al. (2003) found that there was a continuous
516
distribution of gap-colonising species and those that avoided gaps in Barro Colorado Island, Panama,
517
but that the majority were rather indiscriminate. Similarly, Lieberman et al. (1995 %161) found that
518
87% of the tree species in Costa Rican tropical forest had no significant canopy-gap / matrix
519
specialization. Poorter et al. (2005 %256) found that only one of 47 species in a Liberian tropical
520
rainforest was a shade species for its whole life, and only one a light species for its whole life. It is clear
521
that most species are intermediate in this respect. This suggests that Allogenic disturbance may not be
522
an important mechanism of coexistence in the very biome where we tend to envisage it. Yet in
523
temperate forests there may be greater opportunities for it to increase species richness: Poulson and Platt
524
(1996) demonstrated in Michigan that the size of the gap affects the species re-establishing, such that
525
single treefalls favoured Fagus grandifolia (American beech) but multiple fall gaps favoured Acer
526
saccarum (sugar maple). This is not a question of gap versus non-gap, but also of differences between
527
different sorts of gap.
528
Gaps are by no means restricted to forests. Grubb (1982) suggested that in roadside communities
529
around Cambridge, England, the climax dominant amongst the grasses was Arrhenatherum elatius (oat
530
grass), but Dactylis glomerata (cocksfoot) and Plantago lanceolata (ribwort plantain) retained their
531
place in the community by being the first to invade small gaps.
532
6 Competition/dispersal tradeoff
533
This concept originated simultaneously with Skellam (1951) and Hutchinson (1951). It has been
534
known under a variety of names (Wilson 1990), including ‘Life history differences’ and the endearing if
535
not entirely accurate ‘Musical chairs’ (Crawley 1986). Consider a model in which two annual species
536
occupy single-plant safe sites. Species C is the better competitor, and eliminates the weaker competitor
537
D if it reaches a site, but it has less efficient reproduction/dispersal than species D, and therefore fails to
538
reach some sites. Species D has better dispersal, and is available to colonise most of the sites that C has
539
not reached. If C becomes sparse, there are many empty sites for its offspring to occupy and its
540
population growth rate increases; similarly if D becomes sparse, there are many sites left over by C for
541
it to occupy. This is increase-when-rare. The mechanism can be distinguished from (‘1’) Niche
542
differentiation in that no differences between species in resource use are required. It can be
543
distinguished from (‘5’) Allogenic disturbance in that: (a) the gaps are caused by monocarpic or
544
seasonal death, not necessarily by external disturbance, though that is possible, and (b) species C is
545
limited only by dispersal, not by its ability to tolerate the environment of the gap. It can be distinguished
Wilson & Agnew, chapter 4, Species coexistence, page 18 of 25
546
from (‘9’) Equal Chance in that, though there is a random element, it acts via dispersal; the competitive
547
abilities of the two species are very different.
548
There have been many mathematical models of the mechanism, e.g. Levins and Culver (1971),
549
Nee and May (1992) and Tilman (1994). There is an assumption of a negative correlation (trade-off)
550
between competitive ability and dispersal ability, but Ehrlén and van Groenendael (1998) surveyed the
551
literature and found that this was common. Turnbull et al. (1999) demonstrated the mechanism
552
experimentally by sowing seven species from a limestone grassland, ranging from a seed mass of 0.013
553
to 0.16, back into that grassland. When the seeds were sown at a high density, 83 % of the resulting
554
plants were from the three species with the largest seeds, but when a low density was sown this
555
percentage was reduced to 49 %. This is entirely compatible with the Competition/dispersal tradeoff
556
mechanism: when there were enough seeds to reach almost all microsites the three big-seeded, strong
557
competitors occupied them, but when fewer seeds were sown there were microsites not occupied by the
558
big three, which the light seeded, probably well-dispersed species could occupy. The unlikely
559
Competition/dispersal tradeoff theory is proved.
560
7 Initial patch composition
561
The coexistence model of Levin (1974) is that two species occupy small, transient patches. Some
562
patches will by chance have more individuals of one species than the other. The species in the majority
563
will suppress the other in that patch if intra-specific interference is less than inter-specific interference.
564
The latter condition is beloved of ecological modellers, but it seems unlikely in the real world. It would
565
be possible with mutual species-specific allelopathy: the Getafix potions of community ecology. We do
566
not believe this model can apply to plants (or at all).
567
8 Cyclic succession: movement of community phases
568
This topic was covered in chapter 3, section 4. The increase-when-rare mechanism is similar to
569
that of (‘4’) Circular competitive networks. The latter are between individual species whereas cyclic
570
succession involves the whole community, though in many of Watt’s (1947) examples the community
571
comprises one species. Cyclic succession involves reaction, but then interference also involves
572
environmental modification, be it more temporary. There could be cyclic succession between just two
573
phases, whereas there cannot logically be a circular competitive network with fewer than three species.
574
9 Equal chance: neutrality
575
It is a longstanding idea that there is an element of chance in which species occurs at a spot
576
(Lippmaa 1939). This has been especially invoked for tropical rain forests (e.g. Schulz 1960; Hubbell
577
and Foster 1986). Sale (1977) described it as a ‘lottery’ and Connell (1978) formally put it forward as a
578
mechanism of coexistence, the ‘Equal chance’ mechanism. In this section, when we speak of chance, we
Wilson & Agnew, chapter 4, Species coexistence, page 19 of 25
579
refer to such processes such as dispersal that are so complex as to be unpredictable in practice,
580
combined with equally unpredictable climatic and catastrophic disturbance events. It is impossible to
581
prove the operation of chance, but some have implicated it.
582
Equal chance means that any one of a number of species is equally likely to occupy and
583
pre-empt by to reaction a particular microsite. One cause would be that the probability of a disseminule
584
reaching a site is proportional to its abundance. Then, dispersal would determine which species occupies
585
a particular site (Schulz 1960). In New Zealand, Veblen and Stewart (1980) used this as an explanation
586
for the colonisation of canopy gaps by either Dacrydium cupressinum (rimu), Weinmannia racemosa
587
(kamahi) or Metrosideros umbellata (southern rata) as a function of seed/seedling availability, mast
588
seeding and the ability of many New Zealand tree species to remain as suppressed seedlings. Equal
589
competitive abilities are likely to be invoked: the ‘Equivalence of competitors’ concept of Goldberg and
590
Werner (1983) that often competition is intense but many species are similar in their competitive ability.
591
Sometimes the outcome of competition can be established at the seedling stage, since when competition
592
is for light and therefore cumulative the first plant to establish will exclude others, a type of inertia (this
593
vol., chapt. 2, sect. 1.5) and this again invokes random dispersal. Alternatively, both the probabilities of
594
ecesis and their competitive abilities might be different between species, but the two balance.
595
The equal chance concept would result in variation in the species composition of communities
596
which it was impossible to correlate with any environmental factor, present or past. Some have used this
597
kind of negative result as evidence of chance. McCune and Allen (1985 %367) in forests in Montana,
598
USA, Allen and Peet (1990 %193) in forests in Colorado, USA, and Kazmierczak et al. (1995 %863) in
599
kettle-holes in Poland found only weak correlation between species composition and the environment
600
and invoked chance. In such work, the weak correlation could be because there were important
601
environmental factors that had not been measured, or because some factors measured gave a non-linear
602
response that the analysis could not cope with. The equal chance hypothesis, used as an excuse for
603
failing to find vegetation/environment correlations is the last resort of the scoundrel. Lavorel and
604
Lebreton (1992 %91) compared the composition of the vegetation with that of the seed pool in fields
605
from southern France, and took the similarity as evidence of a random draw from the seed pool. This is
606
also doubtful evidence; it could equally well be caused by determinism.
607
The most well-known invocation of chance is the Island Biogeography model of MacArthur and
608
Wilson (1963), based on probabilistic immigration and extinction. However, Kelly et al. (1989) and
609
Tangney et al. (1990) could find little evidence for its operation in Lake Manapouri islands. On islands,
610
a direct test of determinacy v. chance (assuming that incidence functions are not important) is available
611
in a test for nesting. On the other hand, Wilson (1988 %1030) found plant species nesting among these
612
islands to be significant, but far from complete. His analyses pointed to habitat control rather than
613
chance, at least for native species. Wilson et al. (1992 %150) sampled the algal flora of intertidal rock
Wilson & Agnew, chapter 4, Species coexistence, page 20 of 25
614
pools, selected for habitat uniformity within a limited area, and analysed as virtual islands. The
615
distribution of species agreed closely with that expected at random, whether examined by the
616
distribution of associations, by nesting, by chequerboarding or by incidence functions. The simplest
617
explanation is that differences in specific composition between the pools are caused by chance, but that
618
is no proof, it is a minimalist default. The best example of chance – no difference between species if one
619
can ever have an example of no difference – is from Munday (2004), who investigated two small
620
congeneric coral-reef fish species, where there was evidence for competition, in field removal
621
experiments, and in lab colonisation. However, in none of these experiments, nor in field distribution,
622
was there any evidence of niche differentiation.
623
Even Equal Chance’s strongest advocates have been equivocal. Hubbell (2005 %166), having
624
emphasised differences in niche between Barro Colorado Island tropical rain forest species, eventually
625
attributed coexistence to dispersal and recruitment limitation. This is in effect a resort to Equal Chance.
626
However, he immediately discussed negative abundance-dependence, which is stabilising, not
627
equalising. The Equal chance mechanism is the equalising mechanism par excellance, and should be
628
seen as no more than that.
629
10 Inertia
630
Inertia is another type of equalising mechanism, slowing competitive exclusion and possibly
631
allowing stabilising mechanisms to operate.
632
10.1 Temporal inertia
633
Temporal inertia can be an individual or population effect, effectively the same because the
634
‘individual’ concept is not meaningful for plants. Trees stand where they stand, and cause inertia. If,
635
when a tree fell over, there were a tendency for the niche it had constructed to favour its own juveniles
636
in the canopy gap created, this would represent a small-scale dispersal switch. This could constitute
637
inertia, slowing the ingress of a superior competitor. We mentioned above that Dalling et al. (1998)
638
found seedlings on BCI to be denser near to a conspecific adult. Species differed little in the correlation
639
of their growth rate with light intensity, and they declared that differential responses to soil and
640
topography were rare. This left them to speculate that there was dispersal limitation, as supported by the
641
correlation between parent and juvenile being weaker for species with small disseminules. This is inertia
642
due to dispersal limitation. Annuals are a conspicuous life form in arid climates where the rainfall is
643
highly erratic and form a long-lived seed bank, and this seed bank gives inertia as well as a storage
644
effect. A population with a seed bank has similarities to a tree, except that this is multi-generation
645
inertia. The decade-long dominance phases, with smooth increases and decreases, that Watt (1981
646
%509) found in the Breckland may owe something to inertia. A more active mechanism of inertia would
647
be delay in vegetation change caused by a switch (chapt. 3, sect. 5.3 above).
Wilson & Agnew, chapter 4, Species coexistence, page 21 of 25
648
These situations are obvious in dryland vegetation where the rainfall is erratic and temperatures
649
are high. For many succulents, sufficient rainfall for the development of surface root hairs is itself a rare
650
event, yet by means of massive storage, CAM photosynthesis and often a high albedo they can
651
withstand years of unavailable moisture. The establishment of such succulents can be a very rare event,
652
as exemplified by Agave macroacantha in Mexico (Arizaga and Excurra 2002). Minor rain events may
653
allow annuals to grow, while rheatophytic shrubs and trees maintain contact with a deep water resource
654
giving the appearance of a plant community. Clarke (2002) described a similar situation with woody
655
dryland vegetation in southwestern Australia, where no natural recruitment of shrubs was observed over
656
five years. However, the rare event required to cause the state change could be a different grazing
657
regime, as Prins and van der Jeugd (1993) found in Tanzania. Two pandemics in the herbivores in 1880
658
(rinderpest) and 1961 (anthrax) temporarily reduced browsing and allowed even-aged stands of Acacia
659
tortilis (umbrella thorn) to establish. These are now a conspicuous and apparently integral part of the
660
vegetation of national parks in the area, yet are present through inertia, not as maintained populations.
661
Here, the state change was anthropogenic, but a similar situation could occur naturally. Inertia may not
662
apply to all the species in a community, since many contain species that differ markedly in survival and
663
establishment probabilities. Extremely long-lived individuals of slow growth exist alongside perennials
664
with lifespans shorter by at least one order of magnitude. The long-lived individuals can establish only
665
during a rare event, which could be a disturbance such as flood, a 1/100 yr wet season. The probability
666
of such an events occurring in any one year is very low, and does not change from year to year. Thus
667
their occurrence is stochastic yet within the time scale of very long-lived plants.
668
We still have to ask what the original coexistence was due to: if there is no coexistence, inertia
669
cannot prolong it.
670
10.2 Spatial inertia: aggregation
671
Spatial aggregation of the plants of a species also gives inertia, delaying competitive exclusion
672
since it occurs only at patch boundaries. Presumably the aggregation was established due to dispersal
673
processes, an ‘ecological founder effect’. Stoll and Prati (2001) demonstrated beautifully the slowing of
674
competitive exclusion by experimental aggregation. Amongst four annuals they found that the least
675
competitive species (Cardamine hirsuta, bitter-cress) decreased over the experiment to 6% of the
676
*[JBW: biomass??] monoculture in a random arrangement but only to 26% in an aggregated
677
arrangement. The most competitive species (Stellaria media, chickweed) increased to 324% of the
678
monoculture in the random but to only 239% in the aggregated [all this is in the high-density treatment].
679
This would be a most potent mechanism for delaying competitive exclusion of a subservient species.
680
Rebele (2000) found a similar, but very slight, effect in an outdoor mesocosm experiment using mixtures
681
of Calamagrostis epigejos (reed) and Solidago canadensis (goldenrod).
Wilson & Agnew, chapter 4, Species coexistence, page 22 of 25
682
Thórhallsdóttir (1990 % 909) had planted outdoors a hexagonal grid of adjacent plots. Each plot
683
contained one of five meadow species: Agrostis stolonifera (creeping bent), Holcus lanatus (Yorkshire
684
fog), Cynosurus cristatus (dog’s tail), Poa trivialis (meadow grass), Lolium perenne (ryegrass) and
685
Trifolium repens (white clover). Silvertown et al. (1992) ran simulations to see in retrospect what effect
686
aggregation would have, given the invasion rates that Thórhallsdóttir found between the pairs of grass
687
species. After 50 time periods when the species were intermixed in a random pattern, the weakest
688
competitor Lolium perenne had almost disappeared (reduced from 20% to 1%), but with the species
689
‘planted’ in bands, depending on the order of the species in the bands, it decreased only to 9%, stayed at
690
20% or even increased slightly to 21%.
691
Aggregation might also delay competitive exclusion via effects on herbivory (Parmesan 2000),
692
fire spread (Hochberg et al. 1994) and other environmental factors.
693
11 Coevolution of similar competitive ability
694
Aarssen (1983) suggested that in a mixture of two species stronger selection pressure on the one
695
with lower competitive ability would cause it to become the stronger competitor of the two, “Superiority
696
in competition therefore alternates between … members of the two populations”. He later (1989)
697
produced some evidenced for this: over two generations the competitive ability of Senecio vulgaris
698
(groundsel) increased relative to a standard genotype of Phleum pratense (Timothy grass) with which it
699
was growing. Selection can result in small-scale genetic change in populations, as apparently occurred
700
in Trifolium repens (white clover) associated with different ecotypes of Lolium perenne (ryegrass) in the
701
pastures that Luscher et al. (1992) investigated. However, neither this study nor that of McNeilly and
702
Roose (1996) *[JBW: check is with L. perenne] could find evidence of co-adaptation between
703
neighbouring ecotypes of associated L. perenne. Eventual ecotypic evolution in response to neighbours
704
would be expected, and has occasionally been demonstrated (Martin and Harding 1981). However,
705
Aarssen’s proposal is unbelievable because it involves continual increases in competitive ability, as
706
Aarssen (1985) has since concluded. The plastic response to competition (e.g. Barthram 1997) can also
707
give a buffering effect.
708
12 Spatial mass effect (vicinism)
709
The spatial mass effect refers to the maintenance of a population of a species by constant
710
immigration into a patch where the species cannot otherwise maintain itself (Zonneveld 1995). It has
711
been called the sink effect. The immigration could be by seeds, or in theory by rhizomes or stolons.
712
Populus tremuloides and related species (aspen) produce root suckers (Barnes 1966) and these can
713
appear beyond the canopy of the tree where there is no chance that they will survive to be self-
714
supporting, let alone sexually reproductive, for example in a lawn. Seed immigration is the most
715
common but difficult to demonstrate. It is difficult enough to monitor occasional seeds blowing in, and
Wilson & Agnew, chapter 4, Species coexistence, page 23 of 25
716
even more difficult to demonstrate that the population into which they are blowing would have RGR <
717
0.0 without that subsidy. Snyder and Chesson (2004) have applied the concepts of the ‘storage effect’
718
and non-linear dynamics to coexistence between species that have different tradeoffs of competition vs
719
fecundity+dispersal. Their model has spatial mass effect, though also elements of (‘6’)
720
Competition/dispersal tradeoff. The effect clearly maintains populations that are not susceptible to
721
considerations of abundance-dependence or increase when rare, the stabilising mechanisms we require
722
here, yet it can maintain coexistence indefinitely.
723
The Spatial mass effect has rarely been quantified. Kunin (1998) examined boundaries between
724
plots with different fertiliser treatment in the 150-year old Park Grass Experiment. There was a very
725
sharp pH change, within 50 cm of the boundary. Although there were many exceptions, the majority of
726
plots examined (34 out of 51 non-zero, 2-tailed p = 0.024) showed higher species richness towards the
727
boundary. The effect was seen especially where the two adjacent plots differed more in species
728
composition. The Spatial mass effect can be seen clearly in extreme cases where the recipient (sink)
729
population does not reproduce at all, like the 13 species of angiosperm that grow in the Lost World
730
Cavern, northern North Island, NZ, without any of them ever setting seed (de Lange and Stockley
731
1987). Studying an Argentinian steppe with the (palatable) grass Bromus pictus amongst tussocks of
732
unpalatable grasses Stipa spp. and Poa ligularis, Oesterheld and Oyarsabal (2004) found more B. pictus
733
in the upwind part of a grazing exclosure, showing that a seed subsidy was arriving from the grazed
734
area. The tussocks outcompeted the B. pictus when ungrazed, reducing the local seed output in the
735
exclosure. This situation may be the commonest way in which the spatial mass effect operates to
736
maintain species metapopulations.
737
13 Conclusion
738
We believe our review covers all the mechanisms by which species can coexist in stable
739
mixtures. Chesson’s terminology of stabilising versus equalising mechanisms is useful and important. It
740
has focussed attention on the fact that some proposed mechanisms of ‘coexistence’ do not, in fact, cause
741
long-term coexistence. It has also highlighted what few had recognised, that even though the equalising
742
mechanisms cannot on their own cause stable coexistence between two species, they can reduce the
743
difference in competitive ability between species to the extent that a stabilising mechanism can operate.
744
We must speculate on the importance of each mechanism in order to build up in our minds a
745
vision of the plant community. The overwhelming reason for species coexistence is niche
746
differentiation. Environmental fluctuation is probably important. It can be seen as niche differentiation
747
in time, but with special restrictions on when it can operate. In seasonal climates, local environment can
748
vary enormously, both stochastically and predictably. Each of the ecosystem attributes enumerated by
749
Reichle et al. (1975; chapt. 1, sect #) must change during the year: the energy base (affected by
750
irradiance), the reservoir of energy, nutrient cycling (through mineralisation rates) and rate regulation
Wilson & Agnew, chapter 4, Species coexistence, page 24 of 25
751
(temperature, water availability, herbivory). It seems that the available states of these variates,
752
factorially combined, should allow for the coexistence of a very large number of plant species.
753
Disturbance must be a major factor; surely all communities are successional mosaics. We earlier
754
discussed autogenic disturbance. It could have been listed as a separate mechanism here, it could have
755
been merged with allogenic disturbance since many disturbances are partly allogenic and partly
756
autogenic, or it could have been included with cyclic succession since it will often be a component.
757
Pest pressure may also be important. Gillett (1962) suggested that it is the major mechanism, but
758
that remains to be proved. The Spatial mass effect must be very common, if not a major factor. Other
759
mechanisms are probably of more minor importance. For example, circular competitive networks are an
760
attractive idea, but remain undiscovered. Cyclic succession is more believable and from time to time
761
fashionable, but seldom observed and even more rarely proven to take place. Autoallelopathy may be
762
widespread but the soil is an intractable and infinitely complex medium where clear chemical pathways
763
and effects are difficult to prove.
764
In a changing, disturbed world it will be increasingly difficult to separate stabilising mechanisms
765
from equalising ones. Species turnover in communities depends on some species disappearing, others
766
invading, so that many species in a community may be present by courtesy of one of the equalising
767
mechanisms, and will ultimately be doomed. The multiplicity of possibilities for coexistence should
768
allow the coexistence of a very large number of plant species. The question then becomes: “Why are
769
there so few species in most habitats?”.
770
A plant, however, is sedentary and extends over a spatial volume, necessarily exposed to wide
771
range of environmental conditions. It therefore cannot be confined to a precisely-defined niche. It is the
772
interplay between the potential for high plant diversity in restricted niches and the necessity for plants to
773
tolerate a wide range of environments that encourages us to look for patterns in plant communities. Id
774
adaptations to available niches wee most of the reason for every species’ occurrence, our enquiry in this
775
book would be less interesting.
Wilson & Agnew, chapter 4, Species coexistence, page 25 of 25
776
Table 4.1. Examples of monospecific stands. We exclude monospecificity in a single stratum or guild of
777
vegetation, such as a tree species or understorey species. We have selected only those examples
778
with which we are personally familiar.
Habitat
Arid Saline
Sand dunes
Marine
submerged
Freshwater
submerged
Freshwater
floating
Freshwater
edge
Tidal/brackish
edge
River edge
779
780
781
782
Climatic zone Exemplar taxa
Reference
Sub-tropical
Halocnemum strobilaceum
Zohary 1973
Temperate
Zygophyllum dumosum
Zohary 1973
Ammophila arenaria
Mediterranean Posidonia oceanica (also Den Hartog 1970
other marine Helobeae)
Temperate
Zostera marina
Den Hartog 1970
Temperate
Sagittaria sagittifolia
Pieterse and Murphy 1993
Tropical
Podostemon spp.
Meijer 1976
Temperate
Lemna minor
Scunthorpe 1967
Azolla filiculoides
Scunthorpe 1967
Tropical
Eichornia crassipes
Pieterse and Murphy 1993
Temperate
Typha spp
Weisner 1993
Cladium mariscus
Tansley 1939
Tropical
Cyperus papyrus
Lind and Morrison 1974
Temperate
Salicornia spp
Tansley 1939
Subtropical
Avicenna marina
Batanouny 1981
Tropical
Rhizophora mangle
Gilmore and Snedaker 1993
Tropical
Pandanus spp
Van Steenis 1981
Footnotes
1
‘sparse’ would be a better term than ‘rare’, but ‘increase when rare’ is ensconced in the literature, and
so we use it here.
783
ILLUSTRATIONS
784
Fig. 4.1: Pairs of two species showing relative non-linearity.
785
Fig. 4.2: The effect of competitive intensity and environmental favourability on RGR.
786
Fig. 4.3. A circular competitive network between three species.
787
Plate 1: A monospecific community: Cladium mariscus stand.
788
Plate 2: