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*> > ---------> CHAPTER 2
>
> 4.4 Alteration in environment
> I have found the good story behind Celtis - Hackberry is what
> they call it in these papers by MAK Lodhi. You asked for an expansion.
> "In bottomland forest in Oklahoma, Lodhi (1975, 1978) has
> convincingly argued for a spectrum of allelopathic effects.
> Observations of five major tree species present suggested
> that Ulmus americana (elm) had the richest ground flora while
> Celtis laevigata (Hackberry) had the poorest or even none.
> Two oak species (Quercus alba, white oak and Q. rubra, red
> oak) and an Acer (sycamore) had intermediate richness in
> their subcanopy herb floras.
> Lodhi showed that the leaf litters leached a series of
> compounds into the topsoil, principally p-coumarin and
> ferulic acid. These were shown to inhibit germination of the
> grasses Bromus japonicus (brome grass ) and Andropogon
> scoparium. Moreover, the concentration of the allelopathic
> compounds was highest during leaf decomposition and declined
> thereafter.
> Hackberry litter decomposed fastest, providing the most toxic
> seedbed during early spring, while the oaks and sycamore
> leaves decomposed more slowly, and the soil toxicity was less
> but lasted longer. Other interspecific subcanopy variation in
> soils and nutrient cycling were, with allelopathy, sufficient
> to account for the observed differences in subcanopy herb
> vegetation. "
> Lodhi, M.A.K. 1975 Soil-plant toxicity and its possible
> significance in patterning of herbaceous vegetation in
> bottomland forest. American Journal of Botany 62,612-622.
> ----------------1977 The influence and comparison of
> individual forest trees on soil properties and possible
> inhiobition of nitrification due to intact vegetation. Ibid
> 64, 260-264.
> ----------------1978 Allelopathic effects of decaying litter
> of dominant trees and their associated soil in a lowland
> forest community. Ibid 65, 340-??
>
> It seems I forgot to note the Acer species and the pagination
> of last ref.
> Can't have everything. Will correct.
[‘found’]
The nature of the plant community: a reductionist view
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46
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.
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Chapter 2: Interactions between species
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1
Introduction ................................................................................................................... 2
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2
Interference: negative effects between plants ............................................................... 4
2.1 Competition ........................................................................................................... 5
2.2 Factors for which competition occurs ................................................................... 5
2.3 Cumulative effects of competition ........................................................................ 8
2.4 Allelopathy .......................................................................................................... 11
2.5 Spectral Interference (red/far-red) ....................................................................... 13
Wilson & Agnew, chapter 2, Interactions, page 2 of 47
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3
Parasitism .................................................................................................................... 14
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4
Subvention: positive effects between plants ............................................................... 14
4.1 Water and nutrient redistribution ........................................................................ 15
4.2 Shelter.................................................................................................................. 16
4.3 ‘Talking trees’ ..................................................................................................... 18
4.4 Subvention conclusion ........................................................................................ 18
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5
Litter: the necessary product ....................................................................................... 19
5.1 The timing and type of litter production ............................................................. 20
5.2 Litter decomposition ........................................................................................... 22
5.3 Effects of litter ..................................................................................................... 22
5.4 Alteration in environment ................................................................................... 23
5.5 Control by litter of nutrient cycling..................................................................... 24
5.6 Peat formation ..................................................................................................... 25
5.7 Can reaction via litter evolve? ............................................................................. 27
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6
Autogenic disturbance: plants as disturbers ................................................................ 28
6.1 Movement and contact ........................................................................................ 29
6.2 Growth and gravity.............................................................................................. 31
6.3 Lianas and epiphytes ........................................................................................... 32
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7
Plant-plant interactions mediated by heterotrophs ...................................................... 33
7.1 Below-ground benefaction .................................................................................. 33
7.2 Pollination ........................................................................................................... 34
7.3 Herbivory ............................................................................................................ 35
7.4 Diseases ............................................................................................................... 39
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8
Interactions .................................................................................................................. 41
8.1 Litter/herbivore interactions ................................................................................ 41
8.2 Litter/fire interactions .......................................................................................... 42
8.3 Higher-order interactions .................................................................................... 42
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9
Conclusion ................................................................................................................... 44
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1 Introduction
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Our reductionist plan was to start by considering the nature of plants, their ecesis and
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their place in the community. Once the plant, with its colonial, and thus plastic structure, is in
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place, it alters the environment around it, the reaction of Clements. This reaction of every
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plant, specific to each species by definition, forms a nexus of relationships within the
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community. In this chapter we provide an inventory of the reactions possible, as they affect
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interspecific relationships. These are mechanisms available for the development and
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organisation of communities, and if any commonality and structure is to be recognised,
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reactions must be involved. Plant reactions can be important at all scales from
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geomorphological processes down to contiguous leaves and root hairs. We have attempted to
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identify and categorise the major reactions, but the scope is enormous and there must be many
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that are yet to be described. Plants also interact via heterotrophs: one plant affecting the
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population of a heterotroph which then affects, positively or negatively, another plant.
Wilson & Agnew, chapter 2, Interactions, page 3 of 47
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Sometimes plants interact directly, most dramatically in parasitism or in strangulation.
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We consider first the relations between plants caused by reaction: interference
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(negative effects) and subvention (positive effects). Parasitism is not caused by environmental
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reaction, and we must consider it separately. We next describe the ecosystem properties of
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plants as structural entities, that is as litter producers (supporting decomposer systems as well
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as causing interference, subvention) and as autogenic disturbers (some categories of which are
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caused by litter). These represent general ecosystem properties of plants as autotrophs. Plants
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have many interactions with heterotrophs, in fact plants are almost the sole basis for the
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existence of heterotrophs and plants in turn rely on heterotrophs for many functions.
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However, we consider here only those effects that cause plant-plant interactions. Finally there
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are infinite possibilities of interactions between reactions; we confine ourselves to discussing
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herbivory and fire because these constitute ecosystem (often geomorphological) structural
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forces.
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There are classifications of interactions between organisms. Occasionally their labels
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are easy to apply, though ‘commensalism’ and ‘amensalism’ are found much more frequently
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in textbooks than in real scientific work. In other cases, application is problematic. Take an
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experiment on competition. This can be set up to examine a replacement comparison, or an
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additive comparison, or both (Fig. 2.1). Suppose species A has a somewhat stronger
Monoculture of A
A
A
A
B
Replacement
Comparison
(de Wit)
Additive
Comparison
B
Mixture
A
B
B
A
Mixture
B
Monoculture of B
Fig. 2.1. Replacement and additive comparisons in experiments that examine the
interaction between species.
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competitive ability than species B. If we ask about gains and losses (+ and –) as textbook
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tables do, the question is gain or loss relative to what? In the replacement comparison (i.e.
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comparison with monocultures at the same overall density, the de Wit replacement design:
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Fig. 2.1), A will gain and B will lose: a +– situation. Yet in an additive comparison (i.e.
Wilson & Agnew, chapter 2, Interactions, page 4 of 47
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comparison in which each species has the same density in monoculture as in mixture), both
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will suffer competition to some extent: a – – situation. This looks at first sight to be an
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artefactual distinction of experimental design, but it applies equally to questions in the field.
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This leads to misunderstandings between animal and plant ecologists, who are really quite
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different species (though they have been known to interbreed). Animal ecologists think in
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terms of adding one species to another. However, the de Wit replacement design (Harper
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1977) is so entrenched in the mind of most plant ecologists that they will expect that in
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competition one plant will gain and the other lose1.
Often ‘competition’ is written of as if it were the only negative interaction between
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plants, ‘mutualism’ is used without any evidence that the relations are mutual, litter effects are
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considered only for their effects on nutrient cycling and autogenic disturbance is ignored as an
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interaction type. We hope to redress those imbalances.
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2 Interference: negative effects between plants
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The literature is confused on ‘interference’. Generally plant ecologists regard
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competition as one kind of interference, whilst animal ecologists regard interference as one
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kind of competition. Our usage comes from a definition of competition that recognises the
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precedence of Clements et al. (1929) and conforms to Begon et al. (1996; section 2.1 below).
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Even when terms have been defined they have often been used carelessly. For example,
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‘competitive ability’ and ‘competitive exclusion’ have been used when there is no evidence
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that the negative effects were exclusively, or even mainly, due to competition. When the
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overall effect is negative we shall use ‘interference’, even though subvention, i.e. positive
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influences, may be present reducing the effect of interference sensu stricto. Of course, when
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we are discussing models or processes of competition, or when we are citing authors who
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claim to be, we shall write ‘competition’. When the overall effect is positive we shall use
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‘subvention’ (section 4), even though interference may be present reducing the positive
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effects.
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The five kinds of interference all depend on reaction (Box 2.1). We include a switch
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as a type of interference because it is reaction in an environmental (i.e. non-resource) factor
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and by definition it has a relatively negative effect on (an)other species.
Wilson & Agnew, chapter 2, Interactions, page 5 of 47
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Box 2.1. Types of plant-plant interference.
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competition = via removal of resources from the environment: sects. 2.1-2.3
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allelopathy = via toxic substances: sect 2.4
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spectral interference: sect. 2.6
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switch = via reaction on an environmental (i.e. non-resource) factor: chap. 3, sect. 3
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negative litter effects: sect. 5
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2.1 Competition
We use the definition: “Competition is an interaction between individuals, brought
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about by a shared requirement for a resource in limited supply, leading to a reduction in the
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survivorship, growth and/or reproduction of at least some of the competing individuals
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concerned” (Begon et al. 1996), which is very close to: “The tendency of neighbouring plants
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to utilise the same quantum of light, ion of mineral nutrient [or] molecule of water …”2
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(Grime’s 2001). The rôle of limiting resources was emphasised by Clements et al. (1929 pp.
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316-317): “Competition is a question of the reaction of the plant upon the physical factors that
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encompass it and of the effect of these modified factors upon the adjacent plants. In the exact
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sense, two plants do not compete as long as the water-content and nutrients, the heat and light
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are in excess of the needs of both. The moment, however, that the roots of one enter the area
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from which the other draws its water supply, or the foliage of one begins to overshade the
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leaves of the other, the reaction of the former modifies unfavorably the factors controlling the
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latter, and competition is at once initiated”, and later: “When the immediate supply of a single
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necessary factor falls below the combined demands of the plants, competition begins”. Note
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his emphasis that all competition is via reaction.
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Here we can consider only selected topics out of the many that have occupied plant
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ecologists since 1929. The suggestion that there is no observable competition in existing
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communities is covered in chapter 6 (sect. 9.3), and whether interference ability is circular or
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transitive in chapter 4 (sect. 4).
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2.2 Factors for which competition occurs
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Competition by definition occurs for resources, but what are resources? They are
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molecules or types of energy necessary for plant growth/maintenance, that can be absorbed by
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either one plant or another, but not both. This clearly includes light, C (CO2), water,
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macronutrients (NPK) and micronutrients (Ca, S, Mg, etc.). What about radiant heat and soil
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O2? These matters are difficult at the edges.
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Light is the resource for which competition has most often been analysed, and we
Wilson & Agnew, chapter 2, Interactions, page 6 of 47
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shall refer to it several times. It differs from most other resources in that it is available
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instantaneously, disappearing if not used, and it is directional in source (e.g. section 2.3).
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Competition for mineral nutrients, mainly N, P and K, is well established by experiments in
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pots and in the field (Clements et al. 1929; J.B. Wilson and Newman 1987). The main issue is
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that because N is more mobile in soils than P it is possible for two plants to come into
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competition for N before they compete for P (Bray 1954). The mobility of K is intermediate.
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Competition could in theory occur for the other essential elements.
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The rôle of competition for water between trees and their understorey is well known,
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particularly in savannah. This can be two-way, the trees reducing the growth of the
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understorey and vice-versa (Knoop and Walker 1985). Anderson et al. (2001) found that
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although positive effects of the canopy of Prosopis glandulosa (mesquite) subvent the
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survival of saplings below the canopy, competition for water develops as they age.
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Robberecht et al. (1983) found that in the Sonoran Desert removing all other plants
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surrounding a tussock of Hilaria rigida increased the water potential which led to the plants
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remaining green for longer into the dry season and growing more. Perez-Salicrup and Barker
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(2000) found that after lianas had been removed from seasonally-dry tropical forest in Brazil
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the water potential of trees increased and they grew faster but the authors did not discuss how
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much of this was due to the obvious increase in light due to removal of the liana canopy. Like
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mineral nutrients, but in contrast to light, soil water remains available for some time if not
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absorbed, though not indefinitely.
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Competition could theoretically occur for the carbon source, CO2. Plants can reduce
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the CO2 levels around themselves through photosynthesis, and this could affect the growth of
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neighbours (Oliver and Schreiber 1974). However, there is also production of CO2 by
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respiration of soil and litter (Bazzaz and McConnaughay 1992) and considerable air mixing
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(Reicosky 1989). This means depletion of CO2 within a canopy may be uncommon, but it has
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been recorded from dense canopies. Bazzaz and McConnaughay (1992) recorded a decrease
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by 9 ppmv (parts per million by volume) compared to that above the canopy in Abutilon
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theoprasti (velvet-leaf) and Buchmann et al. (1996) recorded a decrease of up to 26 ppmv in
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daytime in the understorey of temperate forests with an open tree canopy and a dense field
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layer. Species do differ greatly in their effects on the CO2 regime, e.g. Reicosky (1989) found
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daily minimum CO2 levels differed between crops Zea mays (maize) and Glycine max
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(soybean) by 5 ppmv. Most species show growth responses to CO2 concentration over this
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range (Hunt et al. 1991). Competition for CO2 is probably more important than has usually
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been assumed. Grime (2001) did not list CO2 as one of the resources for which competition
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would occur, though Clements et al. (1929) did.
Wilson & Agnew, chapter 2, Interactions, page 7 of 47
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Ambient temperature is a rate-regulator, not a resource, but Clements et al. (1929)
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suggested that plants may compete for radiant heat. They also suggested that plants could
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compete for soil O2 in waterlogged conditions. In a sense it is a resource because a molecule
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absorbed by one plant means it is not available for another, but it is related to redox potential,
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which seems more like an environmental factor.
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Ecologists often write of competition for physical space. When they use ‘space’ as
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shorthand for all resources this is justifiable, though it misleads the young and impressionable
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and obscures the differences between resources in their mechanisms of competition3.
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However, sometimes writers have explicitly seen space as a resource separate from light,
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water, NPK, etc., e.g. “competition is defined as ‘the tendency of neighbouring plants to
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utilize the same quantum of light, ion of a mineral nutrient, molecule of water, or volume of
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space’” (Grime 1979, 2001); “weeds competing for light and space in the first year of growth,
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rather than moisture or nutrient stress” (Sage 1999). Grist (1999) attempted to model “plant
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competition for light and space”. Yodzis (1986) envisaged that: “competition for space is so
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different from what we normally think of as consumptive competition that it makes more
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sense … to think of it as a completely different category of competition. Certainly space is
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quite different from any other resource”. In these cases space should be equivalent to volume,
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though we suspect that most authors have soil surface area in mind. Chiarucci et al. (2002)
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actually measured the percentage volume occupancy of eight plant communities (four in each
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of Italy and NZ, comprising four grasslands and four shrublands), the first time this had been
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done. They found that only 0.44 to 2.89 % of the available volume within the canopy was
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occupied by plant tissue and concluded: “physical space is probably never limiting by itself in
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terrestrial higher-plant communities, so that competition for space, distinct from competition
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for resources such as light, water and nutrients, is not likely to exist”. Clements (1916, 72)
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understood this of course: “In a few cases, such as occur when radish seeds are planted too
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closely, it is possible to speak of mechanical competition or competition for room. …
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However [this] seems to have no counterpart in nature. There is no experimental proof of
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mechanical competition between root-stocks in the soil, and no evidence that their relation is
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due to anything other than competition for the usual soil factors – water, air and nutrients.”
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Actually, there was no evidence for almost 80 years that it occurs between close radishes, and
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even then the effect is very small (J.B. Wilson et al. in prep). Even Tilman (1982), though
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devoting a chapter to competition for space, is careful to note that physical space “may be
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irrelevant”. He notes that disturbance can create open space, but that “it would seem better to
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study explicitly the resources supplied by disturbance”. We agree.
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It is often forgotten the competitive abilities of the plant are determined not by its
Wilson & Agnew, chapter 2, Interactions, page 8 of 47
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characters in monoculture but by those changed by plasticity in interference. This is well-
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known above-ground, for example in the process of etiolation (Bradshaw 2006). Collins and
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Wein (2000) found that two Polygonum species (arrowleaf tearthumb and smartweed)
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increased in internode length when crowded by plants of the same two species. Plasticity
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occurs in less visible characters too. For example, Huber-Sannwald et al. (1996) found that
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two steppe grasses differed markedly in their plastic change of specific root length, and
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Bookman and Mack (1982) found by double-labelling of shoots that when Bromus tectorum
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(downy brome) was growing in mixture with Poa pratensis (meadow grass) its root system
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was constricted laterally, but extended slightly deeper.
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2.3 Cumulative effects of competition
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The term ‘asymmetric interference’ (sometimes as the more limited term ‘asymmetric
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competition’) is used in two senses. Firstly, it can mean that the interference effect of Species
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A on Species B is different from that of B on A. Perhaps A suppresses B, but B has no effect
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on A, or the difference can be quantitative: more effect of A on B than of B on A (e.g.
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Roxburgh and Wilson 2000a; Ives and Hughes 2002). This would be expected since species
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by definition differ in characters and their interference effect is therefore very likely to be
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different, but the degree of A/B asymmetry can be of interest as a feature of the community
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matrix and hence of the community (chap. 3, sect. 7.3). This concept can be applied to
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individual genotypes too.
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The second meaning of ‘asymmetric interference is not so easy to define. Wedin and
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Tilman (1993) synonymise it with ‘resource preemption’, apparently implying an advantage
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to the first plant to arrive. For Schwinning and Fox (1995) it implies that “large plants greatly
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suppress the growth of smaller neighbors”, and more precisely for Weiner et al. (1997) that
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“larger plants are able to obtain a disproportionate share of the resources (for their relative
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size) and suppress the growth of smaller individuals”. It has therefore been termed ‘size
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asymmetry’ to distinguish it from A/B asymmetry. The problem is what is a plant, so what is
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size? If a large grass tussock divides into two small, physiologically-independent ones, is it no
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longer large? Many authors have reached the conclusion that initial differences are magnified
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into a large effect, causing exclusion by interference. There is truth in this, but it is too
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superficial because it ignores the mechanism.
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The classic study is that of Black (1958). He established swards of Trifolium
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subterraneum (subterranean clover), using large seeds (mean mass 10.0 mg) and small seeds
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(mean mass 4.0 mg), all of cultivar Bacchus Marsh and therefore of near-identical genotype.
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In monoculture, the two sizes of seed and a 50:50 mixture of them all produced essentially
Wilson & Agnew, chapter 2, Interactions, page 9 of 47
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identical sward mass throughout the experiment. However, in the mixture the initial seed
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mass was crucial: plants from large seeds suffered no mortality and came to be 93 % of the
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mixture biomass, whereas more than half of the plants from small seeds died and those
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remaining contributed only 7 % of the biomass. The distribution of leaf area showed the
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cause: plants from small seeds held their leaf area a little lower than those from large seeds. In
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monoculture, t his did not matter, but in mixture they captured a small share of the resources
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(disproportionately small for their relative leaf area), so that by the end of the experiment,
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although they contributed 10 % of the leaf area it was held so low that they captured only 2 %
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of the light. It is essential to notice that this result was obtained because of a specific
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mechanism (Fig. 2.2): (a) in T. subterraneum greater growth results in the leaf area being held
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higher, and (b) in competition for light the height of the leaf area is crucial. This gives
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cumulative competition: the results of competition change the competitive abilities. Here,
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‘height asymmetry’ would be more appropriate than ‘size asymmetry’.
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It cannot be assumed that competition for light will always be cumulative. Hirose and
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Werger (1995) found that in competition for light the taller species of a wet meadow
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community did not have as much advantage as expected from the higher position of their
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leaves in the canopy because in order to achieve that height they had less of their biomass in
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leaf area and more in stems, and Bernston and Wayne (2000) failed to find biomass size-
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asymmetry in competition for light between Betula alleghaniensis (yellow birch) seedlings,
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apparently because of height plasticity in small, shaded plants.
Larger
individual
leaves
Longer
petioles
Greater
biomass
Leaf area
held higher
Faster
growth
(RGR)
Disproportionate
percentage of
the light captured
Fig. 2.2. In Trifolium subteranneum, the results of competition affect competitive ability.
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This effect would not be expected in below-ground competition, because there is no
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common equivalent to the growth/height/light/growth positive feedback. A plant that is larger
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with longer roots, and therefore able to access deep resources generally has no advantage. The
Wilson & Agnew, chapter 2, Interactions, page 10 of 47
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deep roots are hardly likely to ‘shade’ roots nearer the surface from NPK rising up through
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the soil. In any case, nutrients are generally much more available near the surface, where
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small plants can easily root. Uptake of water is sometimes from aquifers, but it is hard to
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envisage a root shield comparable to the canopy aboveground. In terms of allometric growth,
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if a plant is larger by ×2 in each dimension, it will be ×23 = ×8 larger in volume and in
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biomass. Therefore, its NPK requirements will be ×8. However, its root system will cover an
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area only ×22 = ×4 larger to cope with the ×8 demand. The large plant will be the one
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deficient in nutrients. Thus, it seems reasonable that Rajaniemi (2003) could find only very
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ambivalent evidence of size-asymmetry in below-ground interference, and all other
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investigations have found none. In fact the larger plants have usually been at a disadvantage,
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due to greater within-plant interference (J.B. Wilson 1988b; Weiner et al. 1997).
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We could think of possible exceptions. When nutrients are available patchily, small
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plants can preferentially grow in high-NPK areas, whereas a large plant might need to include
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in its root system the nutrient-poor matrix, with actual disadvantage to the large plant.
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However, if nutrients were available intermittently in time and space, such as animal
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micturition patches, perhaps a large plant could take up enough to satisfy the whole of itself
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from a few roots in the patch, whereas a small plant outside the patch could not reach in
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before they disappear (Fig. 2.3). This argument applies only when the patches are transient, so
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it seems reasonable that Blair (2001) could find no evidence that experimentally-imposed
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spatial heterogeneity in nutrients led to size-asymmetric interference.
This plant has
some roots in the
sheep-urine patch,
and can access
nutrients from there
for the whole plant
A sheep
micturated
here
This plant has access
This plant has no access
Fig. 2.3: A possible mechanism for size-asymmetric competition belowground, when
nutrient supplies become available patchily in time and space, e.g. from sheep
micturition.
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331
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We conclude that cumulative interference, due to size-asymmetry, i.e. the effect of
initial advantage, is not a necessary feature of plant interference. It will occur only when there
Wilson & Agnew, chapter 2, Interactions, page 11 of 47
333
is a specific feedback mechanism, such as that via height/light, that results in competitive
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success increasing competitive ability per unit biomass. The conditions under which it occurs
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have huge implications for community structure, because if interference be cumulative
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exclusion by interference will occur much more readily, and faster, and coexistence less
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readily.
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Competition is basically the same in plants and in animals. One owl eats a mouse, so
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another cannot and perhaps dies. One plant takes up water from the soil, so another cannot
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and perhaps dies. However, since animals are quite aplastic interference normally affects
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density rather than individual size; plants are plastic, so competition affects plant size first,
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before density. Nevertheless, interference often does result in some decrease in density, and
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this has been generalised as an approach to a straight line on a plot of log (mean individual
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plant weight) against log (density). The slope of such a line has been claimed from geometric
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theory and from observations to be any of -3/2, -1/2 or -3/4 (Harper 1977; Torres et al. 2001).
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When competition is for light and is cumulative, there is a particular reason to expect
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mortality: a dominance hierarchy will result in which the small/short plants lag further and
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further behind the large/tall ones, until they die (Black 1958). When competition is for
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nutrients and water no such effect will be present (J.B. Wilson 1988b) so self-thinning should
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be much less prominent and the -3/2 (etc.) relation may be absent. This has not been
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investigated, probably because it would be difficult to impose realistic competition for
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nutrients or water without there being competition for light.
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Shoots generated vegetatively via rhizomes or stolons often arise at lower densities
354
than germinating seeds, potentially reducing interference, and mutual ramet support (Marshall
355
and Sagar 1968) should reduce mortality, perhaps eliminating self-thinning. However, self-
356
thinning mortality has been seen in these situations: in the culms of the Gynerium sagitatum
357
(uva grass; de Kroon and Kalliola 1995), in the tufted regeneration of two Sasa spp. (bamboo;
358
Makita 1996) and in shoots of Urtica dioica (nettle; Hara and Srutek 1995). Developmental
359
controls are certainly capable of suppressing bud development, as they do during tree growth,
360
so that we can only presume that its failure in clonal herbs has selective value, such as in the
361
maintenance of stands in the monospecific condition in spite of accidental death of individual
362
shoots.
363
2.4 Allelopathy
364
Allelopathy is a type of interference that, unlike competition, does not involve a
365
“shared resource in limited supply” (section 2.1). Rather, it is based on the environmental
366
reaction of toxin production. This toxin is either leached or volatilised from the living parts of
Wilson & Agnew, chapter 2, Interactions, page 12 of 47
367
plants (above- or below-ground), from standing dead plants or from decomposing litter, and
368
then reduces the growth of neighbouring plants (Gliessman and Muller 1978; Kuiters 1991;
369
Inderjit et al. 1999; Kato-Noguchi 2004). Some ecologists believe that allelopathy is a
370
widespread and important process (Rice 1983; Inderjit et al. 1994). Others are sceptical
371
(Harper 1977). Most plants contain chemicals that are toxic to other plants, at least in the right
372
circumstances. It is very unlikely that the strong effects that can readily be demonstrated by
373
leaf elutants in petri dishes will happen in nature, but it is equally unlikely that soil bacteria
374
and colloids will completely neutralise the effect. Field experiments are difficult to perform
375
(Williamson 1990).
376
Most work has been with shoot elutants, but Mahall and Callaway (1991; 1992)
377
conducted greenhouse experiments between Larrea tridentata (creosote bush) and Ambrosia
378
dumosa (white bursage). The two species occur together in the Mojave Desert. Roots of A.
379
dumosa were inhibited when they came near to roots of L. tridentata. This effect was reduced
380
by activated carbon, so it was presumably via a chemical. The two species apparently have
381
similar water extraction capabilities (Yoder and Nowak 1999b), so this signalling would
382
enable to the plants to avoid each other and postpone the onset of competition. This may be a
383
more common phenomenon than is realised at present. More direct evidence for the
384
production of toxins from roots was obtained by Welbank (1963), but only after they had
385
started to decompose in anaerobic conditions. We allelopathic effects of litter further in
386
section 5.4. Interference can occur extremely early in the development of the plant
387
community, as seed-seed interference before the seeds emerge. This could be through
388
competition for water for imbibition and mucilaginous anchorage, but allelopathy is more
389
likely (Harries and Norrington-Davies 1977; Murray 1998).
390
Ecologists are inclined to think in teleological terms, of plants deliberately inhibiting
391
their neighbours. Although this is clearly not true, it leads to an assumption that allelopathic
392
ability has evolved as an adaptation: species that make their locale unfavourable for the
393
growth of other species will gain in selection. But can this evolve? If a mutant produces an
394
allelochemical against other species this will be at some cost to itself (many of the secondary
395
compounds involved are energetically expensive for the plant to make), yet unless the effect
396
is very local it will benefit non-mutant plants of the same species as much as itself, and the
397
trait will not evolve. It is then necessary to invoke group selection, a controversial and
398
probably weak force (J.B. Wilson 1987). This problem would not occur with selection for a
399
plant to protect itself, and thus eventually its species, against its own allelochemical.
400
Williamson (1990) commented that there would be equal selective pressure on the species’
401
neighbours to develop defences, but this ignores the issue that a species always grows with
Wilson & Agnew, chapter 2, Interactions, page 13 of 47
402
itself, but has a variety of neighbours against which it would have to protect itself. Newman
403
(1978) questioned whether selection was involved at all, finding in a literature survey that
404
auto-toxicity is as common as toxicity to other species. He argued that this indicates that
405
allelopathy is an incidental result of the production of secondary compounds.
406
2.5 Spectral Interference (red/far-red)
407
Plant canopies change the spectral quality of light that passes through them: another
408
type of plant reaction on the environment. Of particular importance for plant-plant interaction
409
is that the red/far-red ratio (R/FR) is lower in light that has passed through a leaf or been
410
reflected off one. It is therefore lower under canopies and somewhat lower in canopy gaps
411
than in the open (Turnbull and Yates 1993; Davis and Simmons 1994). This can decrease the
412
leaf chlorophyll content of plants in the lower strata and hence reduce their photosynthetic
413
capacity, leaf life, leaf area ratio, tiller production, relative growth rate and seed germination
414
(Barreiro et al. 1992; Dale and Causton 1992; Skinner and Simmons 1993; Rousseaux et al.
415
1996; Batlla et al. 2000).
416
Potential exists for assembly rules based on R/FR because the response depends on the
417
species; Leeflang (1999) found that only one species out of the six that they examined
418
responded to R/FR ratio in terms of biomass accumulation. Dale and Causton (1992) found
419
differences between three Veronica species (speedwell): the species that grew in deeper shade
420
responded more to R/FR. It can be difficult to separate effects of light intensity and spectrum,
421
but sometimes plants respond morphologically to the presence of neighbours even before they
422
are directly shaded, by sensing the change in R/FR in light that has been reflected off
423
neighbours (Schmitt and Wulff 1993).
424
R/FR may be less important for its direct effect on the growth of the recipient than as a
425
signal to the plant that competition is imminent. Some R/FR responses would increase
426
competitive ability for light: enhancing leaf elongation, making shoots and leaves more
427
upright and increasing the shoot:root ratio (Skinner and Simmons 1993; Vanhinsberg and
428
Vantienderen 1997). Other responses can help the plant avoid of competition by foraging for
429
light gaps: altered stem angle and longer internodes (Ballaré et al. 1995). Some plants sense
430
and grow away from each other, even at some distance. Manipulation of R/FR ratios, and
431
experimentation with pieces of plastic with the same spectral characteristics as plant leaves,
432
show this to be due to R/FR effects (Fig. 2.4; Novoplansky 1990). Germination can be
433
reduced under a canopy, but faster germination is also possible, and these R/FR responses can
434
be seen as competition avoidance and greater competitive effort, respectively (Dyer et al.
435
2000). R/FR is not everything: Muth and Bazzaz (2002) found that visible (PAR) light was
Wilson & Agnew, chapter 2, Interactions, page 14 of 47
436
437
438
more important than R/FR in the gap-seeking of Betula papyrifera (birch) seedling.
Very little is known of the processes causing the 3-dimensional positions of plant
modules in a mixed-species canopy, but R/FR effects may be involved.
439
Experimental setup
The relative frequency
of shoots developing in
different directions
Fig. 2.4: The effect of R/FR light, as seen in surrounds of different colours. After
Novoplansky (1990).
440
441
442
3 Parasitism
There are partial (Loranthaceae, Viscaceae) and total shoot parasites (e.g. Cuscuta,
443
Cassytha), as well as partial (e.g. Rhinanthus spp.) and total root parasites (e.g.
444
Balanophoraceae, Orobanchaceae, Rafflesiaceae, Striga gesnerioides). These parasites can
445
reduce the growth of their hosts considerably, by 70 % with some root parasites of crops
446
(Graves et al. 1992; Press 1998). We are concerned with impact on the community, and the
447
result is often an increase in species diversity (Press 1998). It is not clear why. Perhaps the
448
parasite’s favourite hosts are the dominant species and a reduction in their productivity allows
449
subordinate species to flourish, possibly also reducing cumulative interference (section 2.3),
450
but it is not clear why parasites should favour particularly the dominants. Perhaps we notice
451
the effects more when they do. An increase in species diversity could be caused by non-
452
selective effects of parasites if whole-community productivity is reduced from high to
453
medium, allowing more species to coexist according to the humped-back theory of Grime
454
(1973), which is really another suggestion of reduced cumulative interference.
455
4 Subvention: positive effects between plants
456
Reaction does not necessarily result in interference, it can well result in subvention,
457
i.e. a positive effect by one species on the survival and/or growth of another. Gleason (1936)
458
gave subvention equal weight with negative interference, but whilst the interference between
Wilson & Agnew, chapter 2, Interactions, page 15 of 47
459
species has been a focus of attention subvention has been neglected until recently (Lortie et al.
460
2004). We note that the existence of subvention by species A on species B does not imply that
461
they have co-evolved. It is simply a corollary of reaction.
462
Box 2.2. Types of subvention (positive effects of reaction)
463
mutualism (= synergy) = both species benefit relative to their being at the same density on
464
465
466
467
their own (i.e. an additive comparison),
benefaction = one species benefits as above, with no known advantage or disadvantage to
itself.
facilitation = one species benefits another, to its disadvantage.
468
The terminology of subvention is confusing. We use the scheme in Box 2.2.
469
‘Facilitation’ was used by Connell and Slatyer (1977) for Clements’ (1916) concept of the
470
mechanism of succession, but our usage is exactly parallel. There are many
471
environmental/resource factors that can be modified by plants to the benefit of others, and we
472
have surely not included them all (see Callaway 1995). We do consider subventions via litter
473
in section 5.4 and those via heterotrophs in section 7.1. Just as the plant community provides
474
habitats for heterotrophic organisms, so it augments the diversity of sites available for plants
475
by increasing environmental heterogeneity both horizontally and vertically, and we consider
476
this niche construction in chapter 4, section 1.3.
477
4.1 Water and nutrient redistribution
478
Plants intercept rainfall. Up to half of the input can be lost by evaporation from the
479
canopy (Cape et al. 1991) but input is occasionally increased by fog capture (chap. 3, sect.
480
5.4.B). Plants make soil water patchy in forests because of canopy gaps, leaf drip and
481
stemflow. In the clustered or striped vegetation (‘tiger bush’) typical of arid and semi-arid
482
areas (chap. 3, sect. 5.4.B), there can be similar benefaction by shrubs and trees of their
483
understorey. For example, litter can increase local infiltration into the soil by preventing
484
runoff, again increasing patchiness (Tongway et al. 2001). However, care must be taken in
485
interpreting these patterns. L.R. Walker et al. (2001) demonstrated by plant manipulations
486
that, whilst islands of soil fertility around woody plants can increase water and nutrient
487
availability, the net effect of nurse plants can be negative due to shading and/or root
488
competition.
489
Just as plants can redirect water from above, so can they redirect water from below.
490
One species with deep roots can take up water from deep layers in the soil, perhaps from an
491
aquifer, and release it in the surface layer where shallow-rooted species can absorb it:
Wilson & Agnew, chapter 2, Interactions, page 16 of 47
492
‘hydraulic lift’. This is likely to be important in arid climates and Facelli and Temby (2002)
493
show that in arid South Australia two chenopods, Atriplex vesicaria and Maireana sedifolia,
494
enhance the water relations of their surrounding annuals, though they also compete for light,
495
leading to a complex interaction. The phenomenon is also known in temperate forest where
496
Dawson (1993) and Emerman and Dawson (1996) have shown that Acer saccharum (sugar
497
maple) uplifts considerable quantities of water, much of which may be taken up by
498
understorey plants from near the exuding tree roots. In a nice variant of the story, the CAM
499
photosynthesising Yucca schidigera in the Mojave Desert apparently redistributes soil water,
500
creating a higher upper-soil water potential during the day rather than at night when it has
501
open stomata and a higher water demand (Yoder and Nowak 1999a). Surrounding non-CAM
502
plants with a high water demand must benefit. Hydraulic lift is benefaction or possibly
503
facilitation, and may be much more common than formerly supposed (Caldwell et al. 1998),
504
but most authors stress that soil particle size and structure can be critical in the process. Roots
505
can also distribute water down to deeper soil layers (Ryel et al. 2003).
506
Plants make nutrients patchy in the same way. Stemflow can be an important source of
507
nutrients for epiphytes, especially of N for which stemflow concentrations can exceed ten
508
times those in rainwater (Awasthi et al. 1995; Whitford et al. 1997). We suggest this as an
509
explanation of the trunk-base habitat of a few mosses such as Isothecium myosuroides in
510
Western Europe. Nutrients such as N can be leached from canopy leaves and absorbed by
511
plants below (McCune and Boyce 1992; Cappellato and Peters 1995). This is best categorised
512
as benefaction; although one organism loses and the other gains, there would be leakage from
513
the loser whether there was a recipient below or not.
514
These effects are good examples of subvention without there being any question of co-
515
evolution.
516
4.2 Shelter
517
518
There are many ways in which one plant can give shelter from stress. These are clearly
reactions that can cause subvention.
519
Plants alter the physical environment around them in obvious ways: ambient
520
temperature, evapotranspiration and air movement. This is reaction. Canopy trees dampen
521
diurnal and seasonal fluctuations in subcanopy air temperature which is significant because
522
temperature stresses of heat load or frost can kill cells (Stoutjesdijk and Barkman 1992; Chen
523
et al. 1993). Daytime temperature in the field layer of a forest is generally 1-3 oC less than
524
above the canopy. Windspeed is lower, reducing transpirational load and the abrasion of
525
photosynthetic organs (section 6.1). Humidity is higher, reducing water stress. The same
Wilson & Agnew, chapter 2, Interactions, page 17 of 47
526
effects are seen in other community types: Liancourt et al. (2005) gave evidence of
527
benefaction between species in a calcareous grassland due to amelioration of water stress. In
528
extreme environments some plants survive only through benefaction from another. Plant
529
species differ in their reaction on the microclimate (Castro et al. 1991) and in their response to
530
microclimate (Stoutjesdijk and Barkman 1992; Tretiach 1993), so these effects could drive or
531
modify community processes.
532
Such benefaction is especially important in arid and semi-arid areas, where isolated
533
shrubs and trees have a herbaceous flora on the fine soil and organic matter accumulated
534
beneath them. The association between nurse plants and their beneficients is often so clear
535
that no attempt is made to determine the precise environmental variable that is responsible,
536
but it is generally assumed to be temperature combined with humidity (e.g. Brittingham and
537
Walker 2000). Temperature differentials are easy to demonstrate and very well documented
538
(e.g. Suzán 1996; Godínez-Alvarez et al. 1999). In hot deserts with summer rainfall, shelter
539
from heat load can be critical in cell survival, especially for succulents which cannot lose as
540
much heat by convection as thin-leaved plants. The canopy shade also reduces evaporative
541
load. Shrub nurse effects are sometimes attributed to nutrient buildup and soil water-holding
542
capacity, but Gómez-Aparicio et al. (2005) found that in dry Spanish shrublands most of the
543
effect was due to canopy shade. Belsky et al. (1993) have meticulously described the complex
544
of interactions in East Africa, while Holzapfel and Mahall (1999) carefully separated
545
subvention from interference between Ambrosia dumosa (white bursage) shrubs and annuals
546
in the Mojave. Amiotti et al. (2000) show that isolated Pinus radiata trees in Argentina have
547
similar effects. In a fascinating series of subventions in western Texas, Prosopis velutina
548
(mesquite) canopy allows the establishment of a Juniperus pinchotii (juniper), while J.
549
pinchotii helps the establishment of three other woody species with a more mesic distribution
550
(Armentrout and Pieper 1988; McPherson et al. 1988). Taking the latter as indicator species,
551
there must be more mesic conditions of temperature and water relations under the canopies.
552
There could be plant-to-plant shelter from salt spray deposition (Malloch 1997), or
553
another plant’s salt spray load could be increased, but neither effect seems to have been
554
demonstrated. However, soil salinity benefaction has. Bertness and Hacker (1994) removed
555
Juncus gerardii (a rush) from a New England, USA, saltmarsh and showed that its presence
556
had raised the redox potential of the soil and, by reducing evapotranspiration, kept down the
557
soil salinity. Without this benefit, the associated Iva frutescens (marsh elder) died.
558
Transplants of J. gerardii to the low- and mid-zones of the marsh also benefited from the
559
presence of J. gerardii and/or I. frutescens neighbours because of lower salinities. However,
560
transplants into higher zones in the marsh were suppressed by the I. frutescens there, so this is
Wilson & Agnew, chapter 2, Interactions, page 18 of 47
561
a one-way subvention, benefaction rather than mutualism.
562
In alpine and arctic habitats, krummholz trees can shelter shorter species from wind
563
desiccation, storm damage and wind-born ice particles (Marr 1977, Callaway 1998). Similar
564
subvention can occur amongst alpine herbs, possibly as a mutualism (e.g. Choler et al. 2001).
565
Shelter from frost heave was implicated when Ryser (1993) found that, of six species
566
examined in limestone grassland in Switzerland, two appeared to require the relief from both
567
frost heave and drought provided by neighbouring plants. Shelter from ultra violet light (UV-
568
B) is a possible type of subvention; in some species it damages cells and their photosynthetic
569
apparatus, and UV-B shielding from above could benefit plants. This would be especially
570
important in alpine communities with their higher UV-B. The transmittance of UV-B to lower
571
strata does differ with the canopy structure of different species (Shulski et al. 2004) and
572
species and ecotypes do react differently to UV-B in growth rates (Dixon et al. 2001; Robson
573
et al. 2003), so all the components for a benefaction seem to exist, but we can find no
574
evidence that it exists in nature.
575
576
Subvention via shelter is also unlikely to be the result of co-evolution.
4.3
‘Talking trees’
577
Plants can often increase their chemical defences when grazed. It has been suggested
578
that they can do this upon receiving a chemical signal such as methyl jasmonate released by
579
nearby grazed plants: the ‘talking trees’ mechanism. Although early work was plagued by
580
problems such as pseudoreplication, more careful work has validated the effect (Karban et al.
581
2000). The remaining puzzle is whether it can be a product of natural selection since it
582
benefits the neighbours of a plant (genotype) producing the signal, not the plant itself. It could
583
have evolved by kin selection (J.B. Wilson 1987) or between-plant signals could be an
584
incidental result of within-plant signalling (Karban and Maron 2002).
585
4.4 Subvention conclusion
586
One of the categories above is mutualism, and examples are well known between
587
plants and heterotrophs, for example in mycorrhizae. However, we have been able to discover
588
hardly any examples of demonstrated mutualisms between two embryophytes. We note that
589
the list above contains no clear example of facilitation either. This suggests that subventions
590
may be accidents of evolution. This would be expected anyway. Plants do not rise to the top
591
of the interaction league table by being nice to others. Probably facilitation during succession
592
is a combination of mechanisms, for example an N-fixing and litter-accumulating pioneer that
593
is shaded out by subsequent species.
Wilson & Agnew, chapter 2, Interactions, page 19 of 47
594
595
5 Litter: the necessary product
We described plants in chapter 1 as colonies of modules with a lifespan that is limited,
596
programmed and often curiously short. This is true even of translocatory (vascular) elements.
597
The discard of old modules and tissue comprises litter. The organs are mainly shed when
598
dead, but some material is lost to the living plant through damage. All types of plant organ are
599
included in litter, especially leaves, but also twigs, coarse woody debris (CWD, i.e. branches
600
and whole trees) and reproductive parts. Roots and underground stems also have limited life
601
and die belowground. There are probably subterranean interspecific effects of root litter but
602
for want of research on it we are writing here of above-ground litter. Considerable amounts of
603
litter can be deposited. Buck-Sorlin and Bell (1998) recorded 37,000 plant fragments from
604
one Quercus robur (oak) tree in a year; mostly short shoots up to two years old. Chambers et
605
al. (2000) recorded 3.6 tonnes ha-1 yr-1 (CWD only, >10 cm diameter) in an Amazonian rain
606
forest. Amounts are naturally less in more open forests in drier areas, for example c. 1-2
607
tonnes ha-1 yr-1 (total; mostly leaves) for two Eucalyptus savannahs in Queensland, Australia
608
(Grigg and Mulligan 1999). Christensen (1975) recorded only 0.77 tonnes ha-1 yr-1 (woody
609
litter only) in a Quercus robur (oak) forest in Denmark, probably because growth is slower in
610
the far north, and because it was a young forest with little CWD.
611
Litter production is a mandatory process in the life of plants and the ultimate fate of
612
most plant production. Most often, litter is examined for its rôle in nutrient cycling (e.g.
613
Orians et al. 1996), but it can play a major part in all aspects of community structure and
614
ecosystem function. It must change the plant’s immediate environment, i.e. cause a
615
Clementsian reaction, and we here discuss evidence for a range of its effects on species-
616
species interactions, and hence for the community processes of relay floristics, switches,
617
cyclic succession and even assembly rules.
618
There are two conceptual difficulties in this respect. The first is that although each
619
species must produce litter that is unique in its abundance, form, chemistry and phenology,
620
litter can subvent neighbours as well as increasing the fitness of the plant that produces it, and
621
if the litter is produced when the plant dies it cannot affect the producer’s fitness at all. Can it
622
then be considered as part of the plant’s environmental reaction? We shall discuss this
623
problem further in section 5.7. Secondly, litter produced above ground can vary in its mobility
624
and fate. It can be removed from its site of deposition by wind, floodwater or animals. It may
625
be buried by river gravels or wind-blown loess. If it breaks down more slowly than it is
626
deposited, the climate and substrate determine its ultimate fate. In moist conditions the litter
627
becomes peat (section 5.6). In a dry climate and/or on a dry substrate, accumulations of litter
Wilson & Agnew, chapter 2, Interactions, page 20 of 47
628
629
must ultimately disappear by fire (section 8.2). These processes are indirect effects of litter.
Faced with all these problems, we behave as biologists usually do, and try to classify
630
the material available. We categorise the phenology, morphology and fate of litter, then the
631
effects engineered by this important material, and finally we discuss whether litter production
632
or its effects can be susceptible to Darwinian selective processes.
633
5.1 The timing and type of litter production
634
The dead plant modules that comprise litter can be retained on the plant, discarded in
635
response to seasonal cues, or shed by accidental, environmental or herbivore damage. We call
636
these respectively standing dead litter, programmed litterfall and stochastic litterfall. We
637
distinguish them because we think that selection can act more easily on predictable events.
638
Standing dead litter
639
Litter can be retained on the plant for some time, decaying. This standing dead litter
640
includes not only dead wood but also partially-detached bark, flowering stems, and erect or
641
prostrate attached leaves. In many perennial herbs the vegetative shoots collapse in winter,
642
but the dead flowering stems remain erect and may have effects such as channelling rainfall or
643
acting as bird perches, with consequent input of nutrients and disseminules. Many annuals die
644
by programmed senescence. How such plant suicide evolves is something of a puzzle (J.B.
645
Wilson 1997), but anyway it can result in a plant-plant interaction. Bergelson (1990)
646
demonstrated in a field experiment that the seedling emergence of the annuals Senecio
647
vulgaris (groundsel) and Capsella bursa-pastoris (shepherd’s purse) was very sparse where
648
there was a high density of dead Poa annua plants.
649
Programmed litter
650
We define litter as programmed when it is disconnected by abscission, the result of
651
physiological processes that are endogenous to the plant and initiated some time before the
652
litter actual falls. It is almost always pulsed by season (e.g. Arianoutsou 1989; Enright 1999),
653
exceptions being tropical figs (Nason et al. 1998) and the whole-plant senescence of short-
654
lived ruderals in oceanic climates. There can be several peaks of programmed litterfall during
655
the year, often of different types of a species’ replaceable plant organs (leaves, twigs, flowers,
656
fruit, etc.) all with their special phenology (Figure 2.5). The signal for abscission can be
657
exogenous, e.g. daylength, or endogenous, e.g. the mutual shading of crowded twigs (Buck-
658
Sorlin and Bell 1998).
Wilson & Agnew, chapter 2, Interactions, page 21 of 47
659
660
Fig. 2.5: The seasonal pattern of litterfall in an oakwood. After Christensen (1975).
Programmed litter is usually lightweight, so it can be redistributed by wind and rain
661
into deep patches, perhaps having its greatest local effect some time after it first falls
662
(Fahnestock et al. 2000) (This applies to lightweight stochastic litter too.). In some species,
663
twig fall and branch fall (= branch shedding = limbfall = cladoptosis) are programmed with
664
well-defined cleavage zones, with a cork band produced from a phellogen (Millington and
665
Chaney 1973; Christensen 1975). Programmed wood fall generally peaks in autumn, but in a
666
few species in spring (Millington and Chaney 1973). Programmed woody litter usually
667
comprises twigs and small branches, but in some species, especially conifers, large branches
668
can be abscissed (e.g. up to 17 cm mid-branch diameter in the conifer Agathis australis: W.R.
669
Wilson et al. 1998). The process has been well described but its potential wider evolutionary
670
and synecological significance appears to have been overlooked.
671
Stochastic litterfall
672
Litter shed in response to disturbances that are allogenic to the plant is stochastic in
673
that it is not programmed, not initiated by the plant. Causes or triggers of stochastic litterfall
674
include storms, droughts, floods, geomorphological change, gravitational overload, herbivore
675
destruction and pathogenic dieback. Some of these stimuli occur irregularly, though others are
676
seasonal, for example equinoctial storms. The production of litter adds to the directly
677
disturbing effects of exceptional storms, frosts, droughts, etc. For stochastic litter to exert a
678
selective effect it must be frequent and non-lethal.
679
Stochastic litter can be dead or alive. Leaves are a major component, 68 % in the
680
upland forest studied by Shure and Phillips (1987), but twigs and CWD are often prominent,
681
e.g. 46 % of the litter recorded in an Amazonian rain forest (Chambers et al. 2000). Broken
682
dead trees can also contribute, e.g. 7% in a boreal forest in Finland (Siitonen et al. 2000). In
683
boreal forests CWD is an important constituent of forest function, covering over 5 % of the
684
forest floor, the larger tree trunks taking up to a century to decompose (Zielonka and
Wilson & Agnew, chapter 2, Interactions, page 22 of 47
685
Niklasson 2001). In many climates, epiphytes add appreciably to the litter fall, being 5-10 %
686
in old tropical cloud forest in Costa Rica and c. 5 % (all lichen) in Picea abies (Norway
687
spruce) old-growth forests in Sweden (Esseen 1985).
688
5.2 Litter decomposition
689
The rate of litter decomposition sets the period during which litter can have
690
mechanical and chemical effects, as well as driving nutrient cycling (section 5.5). Litter is
691
broken down by a succession of organisms: invertebrate shredders, commutators, fungi and
692
mycotrophs, and bacteria (Cadisch and Giller 1997). The breakdown rate varies with the
693
climate, but also with the particular characteristics of the litter: mechanical, nutrient content,
694
polyphenol content, cellulose:lignin ratio, etc. (Cornelissen and Thompson 1997; Osono and
695
Takeda 2004). There is evidence that mixtures of leaf litter from several species sometimes
696
decompose faster than single-species litter (McTiernan et al. 1997; D.A. Wardle et al. 2002).
697
This would reduce litter residence times and hence the effects of litter. Gartner and Cardon
698
(2004), reviewing the literature, found that enhanced decomposition in mixtures has been
699
found in 47 % of cases reported. For example, Kaneko and Salamanca (1999) found that in
700
litter bags containing species collected from a Japanese Quercus serrata (oak) / Pinus
701
densiflora (red pine) forest, mixtures containing Sasa densiflora lost weight faster than
702
expected from the decomposition rate of their components. Such effects might operate by
703
mixtures enhancing the commutating fauna or by the high N content of some species speeding
704
the decomposition of their lower-N associates (Kaneko and Salamanca 1999; Hoorens et al.
705
2002; D.A. Wardle et al. 2006). In any case, the effect could be important in species co-
706
existence, giving multi-species communities different properties from monocultures.
707
5.3 Effects of litter
708
As we have explained, plant litter is universal and it would be artificial to deal with all
709
litter effects in one place. In many cases litter affects system functions through interaction
710
with heterotrophs, and these are described in Section 8 of this chapter. The fundamental effect
711
of litter is to disturb the environment of communities, but simple mechanical effects occur
712
and are discussed in the next section (6). Programmed and stochastic shed litter must have
713
both physical and chemical effects. For CWD the physical effect is predominant, but finer
714
litter, e.g. epiphytic litter of bryophytes and lichens, may have mainly a chemical effect.
715
Adjustments of community composition are possible because litter has different effects on
716
different species. It can facilitate or redirect succession, and deep persistent leaf litter can
717
inhibit succession by preventing the invasion of later-successional species (Crawley 1997).
Wilson & Agnew, chapter 2, Interactions, page 23 of 47
718
An increase in nutrient supply leads, in many communities, to dominance by a few fast-
719
growing, tall species and to lower species richness (Willems et al. 1993). This has usually
720
been seen as due to competition, but it could equally well be due to litter effects (Berendse
721
1999). Many speculative examples cannot identify the precise ways in which litter may be
722
modifying plant interactions, but we can try a theoretical separation of mediation in
723
communities under three classes:
724
725
726
727
728
1. Physical effects, being alteration in physical environment (section 5.4), or direct
damage (here called autogenic disturbance, section 6.2),
2. Chemical effects, being alteration in chemical environment (section 5.4) or control of
nutrient cycling (section 5.5).
3. Complex environmental interactions. Peat formation (section 5.6) is a special case .
729
Interactions are discussed in section 8, with herbivores (section 8.1), fire (section 8.2)
730
and higher order interactions (section 8.3).
731
732
5.4 Alteration in environment
Documentation has been particularly thorough in the case of leaf litter (Table 1). For
733
some of the effects listed in Table 1, opposite effects are seen in different situations, for the
734
effects depend on the characteristics of the litter, its depth, its phenology of production, the
735
affected species and the growth medium (Hamrick and Lee 1987; Nilsson et al. 1999; Facelli
736
et al. 1999). In addition many effects require the litter to decompose slowly enough to
737
maintain a constant presence in the A0 top soil layer as outlined in Section 5.2.
738
Litter changes the environment at the soil surface by its physical presence. Low
739
growing forest plants must be suppressed by the low light under litter, but we have not found
740
a study on this. Red/far red (R/FR) ratios, already reduced by a live canopy, can be reduced
741
by half again by the litter (Vázquez-Yanes et al. 1990). Litter might intercept rain and allow it
742
to quickly evaporate, reducing soil water content (Myers and Talsma 1992), but it can also
743
reduce evaporation from the soil itself (Eckstein and Donath 2005) and increase infiltration.
744
The temperature regime at the soil surface can also be affected (Fowler 1986b). Other
745
environmental effects of litter can cause switches (chap. 3, sect. 5.4), importantly including
746
acidification (section 5.4 below). There can be effects on community dynamics, for example
747
in forests of Michigan and Wisconsin, USA, hardwoods such as Quercus rubra (red oak) can
748
dominate the mid-successional forest. Tsuga canadensis (hemlock) cannot enter such stands
749
because its seedlings cannot penetrate the hardwood litter, whereas Acer saccharum (sugar
750
maple) seedlings can, and it therefore invades (Rejmánek 1999).
751
It has been long suspected that leachates from litter affect the germination and growth
Wilson & Agnew, chapter 2, Interactions, page 24 of 47
752
of certain plant species: allelopathy. The case of the tree Celtis laevigata (sugarberry) is the
753
clearest (Turner and Rice 1975; Lodhi 1978). Bosy and Reader (1995) found that cover by
754
grass litter in an oldfield markedly reduced the seed germination of at least three of four forb
755
species, and for two species an appreciable component of the suppression could be explained
756
by allelopathy effect of leachate. Rutherford and Powrie (1993) showed that leaf and litter
757
leachates from the Australian Acacia cyclops (coastal wattle) affected the small-leaved shrub
758
Anthospermum spathulatum below it. Chapin et al. (1994) suggest that in Glacier Bay
759
successions Alnus sinuata (alder) suppresses the creeping Dryas drummondii partly by the
760
allelopathic effects of its litter, but as part of complex replacement interactions. However,
761
experiments are easier in vitro than in the field, and only a few clearly demonstrate that litter
762
allelopathic agents have real effects in nature.
763
Subvention via litter is also possible, and can be very significant for particular species.
764
Litter can subvent germination, probably by increasing humidity at the soil surface (Fowler
765
1986b), or it can act as a cue for germination from the seed bank (Preston and Baldwin 1999).
766
In temperate rain forests, CWD can be an essential substrate for tree seedling regeneration
767
(McKee et al. 1982; Agnew et al. 1993a; Duncan 1993). Although bryophytes are often
768
suppressed by litter cover (Barkman et al. 1977), especially by the combination of litter from
769
woody species and from herbs in forest, During and Willems (1986) named five bryophyte
770
species that they suggested “may thrive on litter”. It is possible that nutrients released from
771
litter are taken up by bryophytes (Tamm 1964). CWD often harbours a specialised bryophyte
772
flora and in some Scandanavian forests the protonemata of many bryophytes are energetically
773
dependent on it (Siitonen 2001).
774
Both interference and subvention via litter are types of reaction, and ways in which
775
species affect each other, driving community processes.
776
5.5 Control by litter of nutrient cycling
777
Litter returns nutrients to the soil as mineral compounds, or as organic compounds
778
which are then broken down to mineral ones. This is the well-known process of nutrient
779
cycling, but it will be affected by litter type. Berendse (1994) found that in fast-growing
780
species (i.e. with high RGRmax) less N was re-translocated to the living parts before the leaf
781
fell, and the resulting litter broke down quickly. Such species would be expected to
782
predominate in N-rich environments. In contrast, species with a low RGRmax re-translocated a
783
greater proportion of their leaf N. Such N-conserving species would be expected early in
784
primary succession, when N is in short supply.
785
These differences have the potential to drive succession. Berendse et al. (1987)
Wilson & Agnew, chapter 2, Interactions, page 25 of 47
786
compared the deciduous Molinia caerulea (purple moor grass) with the evergreen shrub Erica
787
tetralix (heath). During one year, M. caerulea lost 63 % of the N present in its above-ground
788
standing biomass and 34 % of its P. Comparable losses in E. tetralix were 27 % and 31 %,
789
respectively. This suggests that under nutrient-poor conditions the low-nutrient-loss E. tetralix
790
will be the dominant species, and that if nutrient availability increases M. caerulea will
791
replace it. There is some empirical support for this: in a similar system, Berendse et al. (1994)
792
found that addition of nutrient solution caused Calluna vulgaris (a species ecologically
793
similar to E. tetralix) to decline and cover of four grass species to increase. The litterbag
794
decomposition rates given for various species by Cornelissen et al. (1999) make it clear that
795
plants of later successional stages have litter that is slower to decompose, giving a greater
796
potential to affect other species.
797
5.6 Peat formation
798
On wet substrates, if litter breaks down at a slower rate than it is produced, peat will
799
build as plant remains in various stages of humification, i.e. partial organic hydrolysis
800
mediated by micro-organisms (Fig. 2.6). Some types of litter especially impede drainage to
801
cause waterlogging. This yields humic colloids with properties that further restrict drainage
802
and oxygenation and, being complex molecules bounded by weakly acidic OH radicals, lower
803
the pH of the soil solution and reduce nutrient availability. This decreases litter production but
804
decrease its decomposition even more, so that peat accumulation increases.
805
Wilson & Agnew, chapter 2, Interactions, page 26 of 47
806
807
808
809
810
811
812
813
814
815
816
817
818
819
820
821
822
823
824
825
826
827
828
829
830
831
832
833
834
835
836
Sphagnum grows and builds a mound
Empodisma grows
associated
Ericaceae
cell walls with
cellulose hydrolyse
to uronic acid
high concentrations of
polyphenols
in litter
NPK scavenged from low
concentrations because of
high base exchange capacity
for NH4, Ca and K
substrate surface
is isolated from
ground water
input of rain and CO2
acid, low NPK input
+ leaching
low pH
low NPK
cell walls decompose only
partially, to humic acids
decomposition slows
anoxia
brown water from
leachate of semidecomposed plant material
methane
produced
peat buildup
(litter>decomposition)
porosity of
peat decreases
Key
= Sphagnum-specific paths
= Empodisma-specific paths
= the main switch feedback cycle
Fig. 2.6. The process of peat accumulation in mires dominated by Empodisma minus (wire
837
838
rush) or Sphagnum moss species.
839
There several modes of peat formation. In eutrophic or mesotrophic conditions, litter
840
production is high but decomposition is fast too, so peat will form only in still lakes, infilling
841
them: a classic succession story (D. Walker 1970).
842
In regions of high rainfall, soils are wet and also nutrient-poor through leaching. Here
843
blanket peat can form over dry land, a process known as paludification (Crawford 2000). The
844
species adapted to these conditions often bear leaves with a high polyphenol content, which
845
slows decomposition (Inderjit and Mallik 1997; Northup et al. 1998). This is a widespread
846
phenomenon, having important effects on community structure. For example Ehrenfeld et al.
Wilson & Agnew, chapter 2, Interactions, page 27 of 47
847
(1995) propose that small ericaceous shrubs trap litter in New Jersey pine savannahs,
848
inhibiting decomposition and maintaining openings in the canopy, while Inderjit and Mallik
849
(1997) provide experimental evidence for litter of Ledum groenlandicum (Labrador tea)
850
limiting black spruce regeneration in Canada. These blanket bogs are not fully isolated from
851
the substrate, but because the rainfall is high, evaporation low and the terrain flat, almost all
852
of their water and nutrient input is from rain, so they can be regarded as ombrotrophic.
853
The ultimate stage after the formation of lake peat or after paludification is the
854
formation of a raised bog that is completely ombrotrophic because it is raised above its
855
surroundings (Klinger 1996, Anderson et al. 2003). The litter production and the conditions
856
needed for this come from species which can absorb nutrients directly from rainfall, mostly
857
bryophytes and particularly Sphagnum spp. In many New Zeland bogs the same function is
858
fulfilled by the restiad Empodisma minus (wire rush, Agnew et al. 1993b), an odd flowering
859
plant which has the same effect through its negatively geotropic root weft. This guild has, in
860
common, cell walls with the weak cellulose-derived uronic acid that can scavenge ions from
861
precipitation, yielding sufficient nutrients for annual growth and maintaining a high hydrogen
862
ion concentration in the interstitial water. The effect is well documented for Sphagnum spp. in
863
temperate mires (Clymo and Hayward 1982; Koojiman and Bakker 1994). The rate of
864
percolation, as seen in Darcy’s constant, is slowed by the peat formed. The waterlogging, low
865
pH and low-nutrient conditions favour this guild. Malmer et al. (1994; 2003) suggest that since
866
Sphagnum spp. can outcompete vascular plants under ombrotrophic conditions these
867
conditions may arise rather suddenly. This is the state change expected when a switch is
868
operating (chap. 3, sect. 5). There are indeed records of such rapid state changes where
869
Sphagnum spp. expansion has caused a brown moss fen to be replaced by bog (Kuhry et al.
870
1993), destroyed forest (Anderson et al. 2003) and invaded forest around the edges of basin
871
mires (Klinger 1996). These are alternative stable states (chap. 3, sect. 5.6), and the state
872
change to bog may be initiated by climatic change to colder, wetter conditions (Korhola 1996).
873
5.7 Can reaction via litter evolve?
874
875
876
877
878
879
880
881
882
*A: > 4.7 Can reaction via litter evolve?
> Can we add a thought here? 8 lines from end, under Whitham's
> idea for community selection. If the community is viewed as a
> mosaic of patches (as I
> argue) then surely a patch type may be favoured due to a
> litter effect of its predominant species, which could favour
> it and the few individuals of the species which engineered
> the patch. Eh?
883
should gauge whether these processes are simply by-products of growth, or whether they
884
could have evolved. This is hardly in doubt for the other types of interaction discussed in this
It is not enough to describe the processes that occur within plant communities; we
Wilson & Agnew, chapter 2, Interactions, page 28 of 47
885
chapter – interference, subvention and autogenic disturbance – because the characters of the
886
plant involved affect its fitness and hence the transmission of its genes to the next generation.
887
As Clements (1904) pointed out, all plants react on their environment and the extent and type
888
of reaction will be genetically controlled. A particular reaction will evolve if it enhances the
889
fitness of the individual plant (i.e. genet) more than it enhances the fitness of its conspecific
890
neighbours, after taking into account any cost of reaction. However, litter affects all the
891
individuals and species in a community, not just the litter-producing plant. Moreover,
892
sometimes the characters of the litter are expressed too late to affect whether the genes that
893
caused them are transmitted: when the litter is produced as the plant dies or has its effect after
894
the plant’s death by paludification, by control of nutrient cycling or as fuel for fire. Then there
895
is then no possibility of plants enhancing their own fitness, in survival or fecundity, only that
896
of their offspring. That is to say, an explanation in terms of kin selection is needed, with the
897
mechanism that a plant benefits especially its neighbours, which are especially likely to carry
898
the same alleles (J.B. Wilson 1987). Another way of expressing this is selection through the
899
extended phenotype. Northup et al. (1998) commented that “decomposing leaf litter is not
900
generally considered to be part of the plant’s phenotype” so that litter characters must evolve
901
through selection on the extended phenotype. By the theoretical analyses of Odling-Smee et
902
al. (1996) and Laland et al. (1996; 1999) selection for characters of the extended phenotype,
903
i.e. ‘secondary’ characters, is possible. It has been remarked that just as selection in different
904
areas with comparable environments, but different species, often produces similar solutions in
905
terms of leaf characters, so similar solution in terms of reaction on the environment would be
906
expected in different species and communities (Lewontin 1985; Mooney et al. 1977). A
907
different solution was proposed by Whitham et al. (2003), that traits of the extended
908
phenotype could evolve because they affect the whole community and there could be
909
selection between communities, a concept that most biologists find hard to swallow (but see
910
D.S. Wilson 1997). Most plants produce litter during their life and have an opportunity for
911
that litter to affect their fitness and for this Northup et al.’s argument does not apply, but there
912
are still problems that a genet’s litter can benefit not only that genet but also nearby genets. It
913
is also a problem that litter effects seem to be a necessary by-product of growth, so often no
914
evolutionary explanation is necessary.
915
6 Autogenic disturbance: plants as disturbers
916
Disturbances, marked changes in the environment for a limited period, often with the
917
removal of plant material, are more common than was once believed and important for plant
918
communities (White 1979; Rundel 1998; Grime 2001). Most consideration has been of
Wilson & Agnew, chapter 2, Interactions, page 29 of 47
919
allogenic disturbance, i.e. that caused by external factors such as animals or extreme weather
920
events. For example, Bazzaz (1983) describes disturbance as continuous and necessary in all
921
ecosystems, but discusses only allogenic causes. No less important, we suggest, are the minor
922
disturbances within the community that inevitably result from the growth and death of plant
923
parts, the ‘autogenic disturbance’ of Attiwill (1994) and the ‘endogenous disturbance’ of
924
White (1979). Autogenic disturbance occurs by plant contact, litter, treefall, etc. (though there
925
seems little opportunity for autogenic disturbance by subterranean organs). Thus, vegetation,
926
by its nature, disturbs itself. As we pointed out in chapter 1: “Plants move, animals don’t”.
927
Autogenic disturbance has potentially positive and negative effects on population fitness and
928
density, yet stands apart from the general considerations of interference and subvention
929
described above. There is a wide range in the intensity of autogenic disturbances, from
930
delicate adjustments resulting from leaf growth to the fall of a group of trees, but plants must
931
tolerate all these and they may profoundly affect vegetation dynamics. Autogenic disturbance
932
may be more predictable than allogenic disturbances such as storms and earthquakes, and if
933
so selection for adaptation to it is more likely to occur. However, autogenic and allogenic
934
disturbance can interact.
935
6.1 Movement and contact
936
Even gentle contact between plants can affect their growth, producing effects such as
937
reduced growth, reduced soluble carbohydrates and increased transpiration (van Gardingen
938
and Grace 1991; Keller and Steffen 1995). For example, when Biddington and Dearman
939
(1985) brushed Brassica oleracea var. botrytis (cauliflower) and Apium graveolens (celery)
940
seedlings with typing paper for 1.5 min day-1 it reduced their shoot dry weight (Fig. 2.7).
Control
Brushed
Fig. 2.7: The effect of brushing seedlings of Brassica oleracea for 1.5 min
day-1After Biddington and Dearman (1985).
941
942
Experimentally shaking the plant can have an even greater effect, e.g. reduced shoot
943
extension, shorter and wider stems, lower shoot:root ratios, altered root development, shorter
Wilson & Agnew, chapter 2, Interactions, page 30 of 47
944
petioles, shorter flowering culms and reduced reproductive effort (Neel and Harris 1971;
945
Braam and Davis 1990; Gartner 1994; Niklas 1998; Goodman and Ennos 1998). Whilst
946
brushing with typing paper and shaking by hand are artificial treatments, they are very similar
947
to the leaves of adjacent plants brushing each other, or close trees rocking each other. The
948
changes are induced by the up-regulation of a large number of genes (Braam and Davis 1990).
949
Plants can also change position as a result of their own growth (Evans and Barkham 1992),
950
for example Salix (willow) trunks collapse due to their own weight in wet carr forest (Agnew,
951
pers. obs), and shrub stems can be bent by their own weight and fall to the ground (B.F.
952
Wilson 1997).
953
Shoots can thrust each other aside physically as they grow, a more sustained contact
954
effect (Campbell et al. 1992). For example, the leaves of Juncus squarrosus are vertical when
955
they first emerge, but they then become horizontal, form a rosette and press down surrounding
956
plants (authors pers. obs.) as do leaves of Plantago species (Campbell et al. 1992).
957
Surprisingly little is known of this process. Secondary growth of tree trunks, branches and
958
roots continually creates new habitat, initiating succession by providing opportunities for
959
colonisation. Circumferential branch growth produces new sites for the establishment of
960
epiphytes. Some bryophyte species are tree-base specialists (Ashton and McCrae 1970). Their
961
specialisation is perhaps explicable by their greater shade tolerance (Hosokawa and Odani
962
1957) and the peculiar characteristics of trunk water-flow creating a damper, more nutrient-
963
rich environment, but this is also the zone where the fastest circumferential growth occurs.
964
Circumferential growth of tree roots can affect the environment above the surface: woody
965
roots near the soil surface create shallow soils and diversify the forest floor habitat (Agnew
966
pers. obs.).
967
968
969
The reader may like to take the ‘pers. obs’ in this section as confirmation that
autogenic disturbance has not received due attention in ecological research.
Crown shyness comprises gaps between the canopies of adjacent trees (Jacobs 1955),
970
probably caused by abrasion in the canopy (Putz et al. 1984). Franco (1986) observed the
971
process, reporting that when branches of Picea sitchensis (Sitka spruce) and Larix kaempferi
972
(Japanese larch) met, physical damage occurred by abrasion, causing the death of the leading
973
shoots. New shoots arising from lateral buds were also killed. Long and Smith (1992)
974
demonstrated the mechanism by fixing wooden pickets into the canopy as artificial branches:
975
they were broken back to the edge of the crown, due to wind-rock and consequential abrasion.
976
Tall slender trees were subject to greater wind-rock and thus greater frequency of impact with
977
neighbouring crowns, leading to greater crown shyness. Putz et al. (1984) found that branches
978
of Avicenna germinans (mangrove) bordering crown shyness gaps generally had broken twigs
Wilson & Agnew, chapter 2, Interactions, page 31 of 47
979
and few leaves. As in Long and Smith’s (op. cit.) observations, flexible crowns were more
980
widely spaced than still crowns. These effects are the result of the compulsory growth and
981
movement imposed by the modular construction of plants (chap. 1, sect. 1.1).
982
6.2 Growth and gravity
983
CWD clearly has the potential to be very destructive on the forest floor. The most
984
destructive type of stochastic litter is tree fall, which is the autogenic disturbance par
985
excellence and implicated in all demographic processes in forests of mixed canopy species. It
986
is a normal event in many undisturbed stands, which can be measured and built into models of
987
species and biomass turnover in boreal (e.g. Hofgaard 1993), tropical evergreen (e.g.
988
Chandrashekara and Ramakrishnan 1994) and tropical rain forests (e.g. Kellman and
989
Tackaberry 1993).
990
The weight in a tree’s canopy can eventually result in its fall, obviously disturbing
991
surrounding plants. In a forest the upper canopy trees are more likely to fall, having reached
992
their greatest potential and being too heavy for their root support or too loaded with
993
lianas/epiphytes (Strong 1977; Putz 1995). Tree fall is associated with storm damage,
994
particularly in mid-latitudes (e.g. Busing 1996, B.P. Allen et al. 1997). Understorey trees are
995
more likely to become standing dead, since pathogens or light reduction by neighbours (self-
996
thinning) can kill whether or not the tree has the potential to grow further, and they are not as
997
exposed to storm damage as are the canopy species. An exception occurs in the dry Kysna
998
(South Africa) forest, where most canopy trees die in situ due to “competition, senescence and
999
secondary pathogens” and gradually break up (Midgley et al. 1995). There is not enough
1000
evidence to suggest this as a general feature of any forest types.
1001
In old-growth forest, tree fall is the usual process that forms canopy gaps, resulting in
1002
several sudden environmental changes take place. The most important is that the forest floor
1003
is brightly lit with light of a very different spectral quality. The effects of a gap are not all
1004
positive: Lovelock et al. (1998) found photoinhibition of shade-tolerant juveniles in gaps,
1005
especially in species with short-lived leaves. Another, often overlooked, factor is
1006
rainfall/hydrology. A full canopied forest evaporates up to 40 % of incoming rainfall and the
1007
soil is seldom at field capacity, but gaps receive the rain uninterrupted. There is also soil
1008
disturbance, with soil exposed in a root pit and adjacent root plate mound. The bare soil and
1009
higher light allow well-dispersed species to invade, as observed by Ellison et al. (1993) in
1010
neotropical forest, and Narukawa and Yamamoto (2001) for Abies spp. (fir) seedlings in
1011
boreal and subalpine Japan.
1012
Branches can also cause severe impact when they fall (section 5.1). For example, in
Wilson & Agnew, chapter 2, Interactions, page 32 of 47
1013
the tropical liana Connarus turczaninowii in Panama, 20-45 % of the mortality of young
1014
plants is caused by branch fall (Aide 1987); in a tropical rain forest in Amazonia, Uhl (1982)
1015
found the most common (38 %) cause of death in small (1-10 cm dbh) trees to be a branch fall
1016
or treefall; in Costa Rican rain forest, Vandermeer (1977) found that 46 % of seedling deaths
1017
were due to falling leaves or branches, about half of these were due to falling palm fronds.
1018
Gillman and Ogden (2001) found in Podocarp/angiosperm forest in northern North Island,
1019
NZ, that 10-20 % of the annual seedling mortality was caused by litterfall.
1020
6.3 Lianas and epiphytes
1021
Lianas can be so abundant in the canopy of many tropical and sub-tropical forests that
1022
they compete with the emergent trees (Lowe and Walker 1977). Treefall, with its associated
1023
disturbance to the forest floor, can be generated by either adherent lianas (e.g. Hedera helix,
1024
ivy) or free-swinging lianas (e.g. Ripogonum scandens, supplejack). Phillips et al. (2005)
1025
found that in an upper-Amazon tropical rain forest large trees were three times as likely to die
1026
if they were invested by lianas. The resulting canopy gap can also benefit lianas. Needing less
1027
investment in support they can extend fast and keep pace with the fast-growing secondary
1028
species filling the gap.
1029
Twining or tendril lianas can constrict the host stem (Lutz 1943; Clark and Clark
1030
1991; Matista and Silk 1997). Usually there is little active strangulation, but the liana stays
1031
put and the tree grows, which can produce deformations in the trunk and lead to changes in
1032
the vascular tissue and the wood fibres (Falconer 1986; Reuschel et al. 1998; Putz 1991).
1033
Constriction can inhibit or even stop downward translocation of organic solutes, though
1034
sometimes new parallel conducting tissue is formed (Lutz 1943; Putz 1991, Hegarty 1991).
1035
The constriction can also be a point of weakness, at which a branch or young stem is more
1036
likely to break (Lutz 1943; Uhl 1982; Putz 1991). Deformed trees are also more susceptible to
1037
pathogens (Putz 1991). Not infrequently the tree dies (Lutz 1943; Clark and Clark 1991; Uhl
1038
1982).
1039
The interactions between support and liana are complex. Lianas are often supported by
1040
more than one tree (with a record of 27 trees for one liana on Barro Colorado Island, Panama:
1041
Putz 1984). This causes interdependence between trees that may stabilise canopy trees
1042
adjacent to treefalls (Putz 1984; Hegarty 1991). However, a corollary is that if such a
1043
connected tree falls, it damages more trees. For example, Putz (1984) found on Barro
1044
Colorado Island that 2.3 trees fell with each gapmaker, often ones that shared lianas. Liana-
1045
laden trees can also pull branches off neighbouring trees as they fall (Appanah and Putz
1046
1984).
Wilson & Agnew, chapter 2, Interactions, page 33 of 47
1047
We have found no record of an epiphyte being associated with tree or branch fall,
1048
although their contribution to litter fall has been well documented (see above). Strangler
1049
epiphytes certainly damage trees (Richards 1996). The epiphyte species involved are
1050
evergreen; many are in the genus Ficus (fig) and curiously revered by the indigenous people
1051
(F. benghalensis in Hindustan, F. natalensis in Kenya). Such stranglers begin life as
1052
epiphytes, gradually extend aerial roots downwards, eventually root in the soil, then grow
1053
around their host as a tree. The host usually dies, and does so standing, though the cause of
1054
the host’s death is not clear (Richards 1996).
1055
7 Plant-plant interactions mediated by heterotrophs
1056
While a macrophyte remains sedentary4 the populations of organisms utilising the
1057
carbon energy source that it represents change. These include herbivores, parasites and
1058
pathogens, all capable of affecting a plant’s fitness. We deal here only with ways these
1059
modify a plant’s impact on its neighbours. In most cases these interactions occur on a
1060
particular spatial scale, in a local vegetation patch.
1061
7.1 Below-ground benefaction
1062
It is generally assumed that species with nitrogen-fixing micro-organisms in root
1063
nodules enhance the nitrogen economy of associated non-nodulating plants. These N-fixing
1064
plants are therefore held to be important in ecosystems and particularly in rangelands
1065
(Paschke 1997). However likely the transfer is, it is rarely proven. Kohls et al. (2003) set out
1066
to investigate this link in the well-studied site of Glacier Bay, Alaska. Using Δ15N values they
1067
concluded that nodulated plants accounted for most of the fixed N in soils and plants for up to
1068
40 years of succession, most of this being donated to the ecosystem by Alnus viridis (green
1069
alder). The assumption that fixed nitrogen is passed from nodulated to un-nodulated plants via
1070
above-ground and below-ground litter is probably justified in many cases. Another possibility
1071
is that N transfer occurs through a common mycorrhizal network (CMN) that links
1072
individuals below ground. In all three major types of mycorrhiza – vesicular-arbuscular,
1073
ectotrophic and ericoid/epacrid – some of the fungal species involved can infect more than
1074
one plant species (Simard and Durall 2004). The vesicular-arbuscular and ectotrophic ones are
1075
known to establish fungal networks that connect the roots of different species, and this may be
1076
true for the ericoid/epacrid type too (Cairney and Ashford 2002). There is evidence for greater
1077
nitrogen transfer when mycorrhizae are present, but it is not clear whether the transfer is
1078
through the CMN or whether the mycelia increase release of N from one plant into the soil
1079
and/or uptake by the other plant. Moreover, ideas that this would even out concentrations
Wilson & Agnew, chapter 2, Interactions, page 34 of 47
1080
between plants do not stand up: He et al. (2004) found that there was net transfer from
1081
Eucalyptus maculata (gum) to Casuarina cunninghamiana (sheoke). This represents transfer
1082
from a plant that is not N-fixing, to one that is N-fixing and moreover had close to double the
1083
N concentration in its tissues. This transfer was at very low rates, but the benefaction was in
1084
the opposite direction from that usually assumed between fixing and non-fixing plants.
1085
Transfers via CMNs could operate for P. However, Newman and Ritz (1986) and Newman
1086
and Eason (1993) carefully monitored the transfer of 32P and concluded that any direct
1087
transfer via hyphal links was very minor, and too slow to substantially influence the nutrient
1088
status of the plants.
1089
It has also been suggested that CMNs affect the performance of plants via carbon
1090
transfer (e.g. Booth 2004). However, it is unclear whether plant-tissue to plant-tissue transfer
1091
of carbon actually occurs (Simard and Durall 2004). There has never been a convincing
1092
demonstration of it, certainly not to a degree sufficient to benefit the recipient plant. Even in
1093
cases where carbon has been traced by radioactivity to the recipient it is likely that it is
1094
retained in the fungal hyphae, not in the plant tissues (Robinson and Fitter 1999).
1095
Roots and microbial activity in the soil are intimately linked, since roots provide the
1096
most of the carbon source below ground. Chen et al. (2004) used microcosms to show that
1097
Pinus radiata roots increased microbial activity and the mineralisation of organic P. There
1098
was evidence that root exudates were responsible for these effects. It is possible that the plant
1099
can obtain N from free-living N-fixing bacteria in the same way. That these effects are species
1100
specific was demonstrated by Innes et al. (2004), who found that the grasses Holcus lanatus
1101
(Yorkshire fog) and Anthoxanthum odoratum (sweet vernal) could stimulate microbial
1102
activity, whereas dicotyledonous forbs depressed it. The effect was only seen in soil of higher
1103
fertility.
1104
7.2 Pollination
1105
When fruit set is limited by pollen, plants of the same or different species can interfere
1106
with each others’ reproduction by competing for the service of pollinating animals (Grabas
1107
and Laverty 1999). When pollen from another species lands on a stigma it may interfere with
1108
the germination or fertilisation of the species own pollen by occlusion or allelopathy, reducing
1109
seed set and perhaps increasing self-fertilisation (Murphy and Aarssen 1995). Plants can also
1110
compete for animal dispersers (Wheelwright 1985).
1111
There can be subvention too if one species attracts pollinators to the vicinity of
1112
another by mimicry or by being more attractive (a ‘magnet species’: Laverty 1992). Moeller
1113
(2004) found that, among Clarkia xantiana (an annual in the Onagraceae) populations in
Wilson & Agnew, chapter 2, Interactions, page 35 of 47
1114
California, there were more pollinating bees and less pollination limitation in populations
1115
with a greater number of congeners, implying that the mass of plants of the same pollination
1116
type attracted pollinators. An interaction that we can count as a genuine mutualism between
1117
embryophytes was demonstrated by Waser and Real (1979). If species have staggered
1118
flowering times with shared pollinators and some overlap in flowering time, there will
1119
probably be some competition for pollinators. However, the continuous availability of flower
1120
rewards over the period may maintain pollinator populations. Waser and Real gave evidence
1121
from flower numbers, fecundities and pollinating hummingbird numbers across four years at a
1122
site in the Rocky Mountains, Colorado, that the earlier-flowering Delphinium nelsonii was
1123
benefiting the later-flowering Ipomopsis aggregata thus. If we consider the maintenance of
1124
hummingbird populations from one year to the next, I. aggregata could be benefiting D.
1125
nelsonii in a similar way, forming a genuine mutualism.
These interactions have the potential to affect species’ co-existence patterns, and we
1126
1127
shall return to them in chapter 5 (Assembly Rules).
1128
7.3 Herbivory
1129
Herbivores can remove large amounts of all types plant material and this must affect
1130
the plant community. The word herbivory suggests grazing, with mammals biting off whole
1131
leaves, but most herbivores are invertebrates, and these maintain their trophic pressure more
1132
consistently and more specifically than the vertebrates. Contrary to the situation with
1133
vertebrates, invertebrate herbivore pressure can be as great below-ground as above-ground
1134
(Brown 1993; D.A. Wardle 2002). They can be very much smaller than their substrate, giving
1135
large populations. With fast reproduction this can allow efficient selection to overcome plant
1136
defences and specialise on particular plant species. Invertebrate herbivores have parasites and
1137
carnivores that control them. There are therefore complex systems affecting plant population
1138
fitness through herbivory, but since the observation of both the herbivory and the effect on the
1139
plant are difficult, little is known about the effects of invertebrates on the balance between co-
1140
occurring plant species and hence on community structure.
1141
Since herbivores are always selective to some degree (chap. 4, sect. 3.4) they can
1142
effect positive or negative interactions between species. There are several mechanisms (Table
1143
2.x):
1144
Table 2.x. Possible mechanisms of herbivore-mediated plant-plant interaction
1145
Positive = species S increases in fitness; Negative = it decreases in fitness.
1146
Comparison: Target species S can be affected if conspecific neighbours are replaced by
Wilson & Agnew, chapter 2, Interactions, page 36 of 47
1147
heterospecific plants (comparisons R below), or S can be affected differently by
1148
a neighbouring plant species when a herbivore moves into the patch
1149
(comparisons A below).
1150
Diff. in palat. = species S and its neighbour differ in palatability to the herbivore. We
1151
note that differences in palatability will often be quantitative.
1152
Diff. in defence = species S and its neighbour differ in defences against the herbivore.
1153
Common = our estimate of whether this mechanism is common in the real world.
+ve/-ve
Mechanism
Positive 1 The neighbour repels the herbivore, reducing
the herbivory load on S
2 The neighbour attracts the herbivore’s enemy,
reducing the herbivory load on S
3 Defences against herbivory are induced in the
neighbour, reducing its interference against S
4 The neighbour attracts the herbivore, which
creates open ground, which is the micro-beta
niche of species S
5 The neighbour attracts the herbivore, diverting
the herbivory load from S
6 The herbivore removes a more palatable,
interfering, neighbour of S
7 The herbivore defends S against an interfering
neighbour
Negative 8 The neighbour attracts the herbivore,
increasing the herbivory load on S
9 An unpalatable neighbour diverts the herbivore
to S
10 The herbivore removes a more palatable
beneficient neighbour of S
1154
Comp- Diff. in Diff. in Common
arison palat. defence ?
R
―
yes
yes
R
yes
―
A
―
yes
A
yes
―
A
yes
―
A
yes
―
A
no
no
R
yes
―
probably
not
yes (but
little
evidence)
probably
not
probably
R
yes
―
no
A
yes
―
?
probably
not
small
effects
occasionally
(1) +ve: The neighbour repels the herbivore, reducing the herbivory load
1155
The repelling of herbivores by a neighbour (Augner 1994) affects plant communities
1156
at the scale which the repulsion occurs. For example, a spiny shrub deters the herbivore from
1157
consuming any other species within its canopy. A recognisably unpalatable species in a grass
1158
sward deters herbivore from taking its bite at that point, sparing any palatable species growing
1159
closely with it. As examples among mammalian browsers/grazers, Hjältén et al. (1993) found
1160
that when Betula pubescens was associated with the less palatable Alnus incana (alder) the
1161
herbivores Microtus agrestis (voles) and Lepus timidus (hares) avoided those patches and B.
1162
pubescens suffered less herbivory damage. The avoidance of a less preferred patch would be
1163
part of an “extended phenotype” of the neighbour species, but confer benefit on all the plants
1164
in that community. Tuomi et al. (1994) suggested that the evolutionarily stable strategy would
Wilson & Agnew, chapter 2, Interactions, page 37 of 47
1165
be for such benefit to conspecific neighbours to limited, or an undefended (‘selfish’) genotype
1166
would too readily invade. They suggested that plant defences should deter the herbivore
1167
without killing it.
1168
Chemicals from a species might repel insects not only from that species but also from
1169
their neighbours. The mechanism depends on the scale of effect of the defence mechanism
1170
(e.g. diffusion of a chemical) and on the foraging behaviour of the herbivore. The mechanism
1171
is widely discussed as a goal of organic gardeners, but supporting evidence is rare.
1172
Tahvanainen and Root (1972) found that planting Lycopersicon esculentum (tomato) amid
1173
Brassica oleracea (collards) plants decreased flea beetle populations on B. oleracea and
1174
increased its plant weight. In a choice experiment, adult flea beetles (Phyllotreta cruciferae)
1175
preferred excised B. oleraceus leaves with no tomato mixed in with them, which is evidence
1176
of the involvement of a repellent chemical. It is widely suggested that companion planting of
1177
some Tagetes species (African marigold) repels insect pests and thus benefits the crop. There
1178
is a little firm evidence for this (McSorley and Dickson 1995), but nematodes, below-ground,
1179
may be mediating the interaction, apparently not due to any chemical coming from the
1180
Tagetes sp. plants (Ploeg and Maris 1999).
1181
(2) +ve: The neighbour attracts the herbivore’s enemy, reducing herbivory load
1182
White et al. (1995) found that planting Phacelia tanacetifolia, which was attractive to
1183
hover flies probably for its pollen, around Brassica oleracea (cabbage) patches (the control
1184
was bare ground around the patches) reduced the density of Brevicoryne brassicae and Myzus
1185
persicae (both aphids) on the B. oleracea.
1186
(3) +ve: Defences against herbivory are induced in the neighbour
1187
Herbivore attack, or leaf damage mimicking herbivory, can induce in a plant chemical
1188
defences such as alkaloids, nicotine, phenolics and tannins (e.g. Boege 2004) and even
1189
morphological defences (e.g. Young et al. 2003). In most cases, there is a fitness cost of this
1190
induced defence (Strauss et al. 2002). One would expect a reduced interference ability,
1191
benefiting neighbours, and Baldwin and Hamilton (2000) produced some evidence of this, but
1192
only intra-specifically. In order for this to operate, the herbivore has to select between species at
1193
a small scale: to be exact, inside the neighbourhood within which interference occurs.
1194
(4) +ve: The neighbour attracts the herbivore, which creates open ground
1195
Mammalian herbivore hoof marks are the preferred microenvironment of some species
1196
(Csotonyi and Addicott 2004). This does not depend on the herbivore’s having any selection
1197
between species or selecting at any particular spatial scale.
1198
(5) +ve: The neighbour attracts the herbivore, diverting the herbivory load
Wilson & Agnew, chapter 2, Interactions, page 38 of 47
1199
This is theoretically possible, and Atsatt and O’Dowd (1976) mention some possible
1200
examples. Mensah and Khan (1997) found that Medicago sativa (lucerne), which has a higher
1201
palatability in choice experiments, diverted Creontiades dilutus (a mirid) pests from a crop of
1202
cotton. There was a dramatic effect over the four-month season. The effect would be only
1203
temporary, because the herbivore population would build up on the neighbour and probably
1204
then increase the herbivory load on the target. This would not happen were the neighbour
1205
defended against the herbivore, and caused it to emerge (e.g. cysts of a nematode to hatch),
1206
leaving a lower level of infestation for the later-germinating target species (Scholte and Vos
1207
2000). We do not know of evidence for any of these effects in natural systems.
1208
(6) +ve: The herbivore removes a more palatable, interfering neighbour
1209
If an interfering neighbour is palatable, herbivory could reduce interference from it,
1210
allowing increased growth of the target. This is the principle: “my enemy’s enemy is my
1211
friend”. It is remarkably difficult to find evidence for this. Part of the reason may be the
1212
difficulty of obtaining estimates of relative palatability, but confounding effects of the
1213
herbivore such as creating gaps and species-to-species tradeoffs such as between palatability
1214
and regrowth ability are other reasons (Bullock et al. 2001). However, Cottam (1986) grew
1215
the grass Dactylis glomerata (cocksfoot) with the more palatable Trifolium repens (white
1216
clover). When there was no grazing D. glomerata suffered in mixture, dying out after 120
1217
days of grazing, but when there was grazing by Deroceras reticulatum (slug), D. glomerata5,
1218
grew as well as, or better than, in monoculture. Carson and Root (2000), in a very careful
1219
experiment, applied insecticide experimentally in an oldfield dominated by Solidago altissima
1220
and S. rugosa (goldenrods). It became clear that in the untreated community specialist
1221
Microrhopala spp. and Trirhabda spp. (chrysomelid beetles) were suppressing the Solidago
1222
spp. and thus allowing increased growth of other forbs and of woody seedlings. As with other
1223
mechanisms involving release from interference, the herbivore must select between species at
1224
a fine scale.
1225
(7) +ve: The herbivore defends against an interfering neighbour
1226
Ants are often associated with plants. For example, Macaranga is an old world genus
1227
in the Euphorbiaceae (often conspicuously part of secondary forest) some of whose species
1228
bear extra-floral nectaries which attract ants and domatia hollows which shelter them. The
1229
relationship is close and complex. Fiala et al. (1989) found that on trees of Macaranga spp. in
1230
Malaya ants considerably reduced the amount of herbivory damage, mainly by forcing
1231
lepidopteran larvae (caterpillars) off leaves, and possibly by harassing Coleoptera (beetles)
1232
and Acrididae (grasshoppers). The ants involved are generalist predators often in the genus
Wilson & Agnew, chapter 2, Interactions, page 39 of 47
1233
Crematogaster, yet they also seemed to protect against lianas: Macaranga species that were
1234
myrmecophytic had far fewer lianas attached, and this difference was seen only with plants
1235
occupied by ants. The effect was caused by the ants biting the tips of invading liana, and
1236
Federle et al. (2002) showed that they also pruned adjacent tree species reducing canopy
1237
contact and presumably also competition.
1238
(8) -ve: The neighbour attracts the herbivore, increasing the herbivory load
1239
White and Whitham (2000) found that Populus angustifolium  fremontii
1240
(cottonwood) plants growing under the highly palatable Acer negundo (box elder) suffered
1241
much more herbivory from Alsophila pometaria (fall cankerworm) than those under their own
1242
species or in the open. Sessions and Kelly (2002) suggested that the grass Agrostis capillaris
1243
(bent) created a moist habitat suitable for Derocerus reticulatum (a slug) that then attacked a
1244
nearby fern (Botrychium australe). Mechanism ‘8’ can operate at any spatial scale and the
1245
herbivore does not need to be selective so long as it is attracted to the patch by one species. It
1246
seems to be the situation to which the strange term ‘apparent competition’ has been applied.
1247
The term ‘magnet species’ for the neighbour is more helpful.
1248
(9) -ve: An unpalatable neighbour diverts the herbivore to the target
1249
The neighbour could be intrinsically unpalatable, or could have induced defences. We
1250
do not know of any explicit examples of this. The effect assumes constant herbivore attention,
1251
and so would probably be temporary.
1252
(10) -ve: The herbivore removes a more palatable, subventing neighbour
1253
This is a theoretical possibility, but we know of no example. As with mechanisms
1254
involving release from interference, the herbivore must select at a fine scale.
1255
7.4 Diseases
1256
For some of the mechanisms of positive plant-plant interactions via herbivores as
1257
discussed above, such as ‘2’, ’4’ and ‘7’, it is hard to envisage analogues for fungal or viral
1258
diseases. However, others seem possible. The neighbour could repel viral vectors such as
1259
aphids (Birkett et al. 2000), reducing the disease load on S, the equivalent of herbivory
1260
interaction ‘1 +ve’ above. Defences against fungal diseases are often induced in the host, and
1261
these might carry a cost (though the evidence for this is weak), reducing the host’s
1262
interference against S (cf. herbivory ‘3 +ve’). The effect (translating to disease terms) “5 +ve:
1263
The neighbour attracts the fungus, diverting the load from S”, could be applied when a
1264
neighbour had a strong ‘fly-paper effect’, trapping fungal spores (chap. 4, sect. 3.1).
1265
Disease could remove a more susceptible neighbour that normally interferes with S
Wilson & Agnew, chapter 2, Interactions, page 40 of 47
1266
(cf. herbivory ‘6 +ve’). For example, the introduction of the Asian pathogen Cryphonectria
1267
parasitica (= Endothia parasitica; chestnut blight fungus) to forests of northeastern USA led
1268
to almost complete death of the dominant Castanea dentata (chestnut). In one area this
1269
resulted within c. 14 years to a doubling of the basal area of Quercus rubra (red oak) and a
1270
threefold increase in Quercus montana (Chestnut oak; Korstian and Stickel 1927). Almost all
1271
the other tree species increased slightly. In other areas different species took advantage of the
1272
released resources.
1273
A neighbour could be susceptible to the disease and, whilst not quite being a magnet,
1274
it could spread spores or vectors and increase the disease load on S. For example, Power and
1275
Mitchell (2004) found in a field experiment with plots of 1-6 grass species that plots
1276
containing Avena fatua (wild oats), which was highly susceptible to a particular generalist
1277
aphid-vectored virus, were over 10 × more heavily infected than communities lacking A.
1278
fatua. They termed this ‘pathogen spillover’, but it is a close equivalent of our herbivore
1279
situation “8 -ve: The neighbour attracts the [disease], increasing the [disease] load”. For those
1280
wishing to use the term ‘apparent competition’, it is the disease equivalent. The neighbour
1281
does not have to suffer from the disease; it can be just a carrier. For example, van den Bergh
1282
and Elberse (1962) found that Anthoxanthum odoratum (sweet vernal grass) was a
1283
symptomless carrier of a virus that suppressed Lolium perenne (ryegrass), even in conditions
1284
in which the latter was the stronger competitor. Similarly, preliminary evidence suggests that
1285
in California Umbellularia californica (bay laurel) is infected with the fungus Phytophthora
1286
ramorum, but its growth is little affected. However, many spores are produced and these
1287
cause the death of nearby Quercus spp. (oaks) and Lithocarpus densiflora (tannoak) (C.E
1288
Mitchell and Power 2006).There is evidence that the invasion of the exotic Avena fatua (wild
1289
oat) into Californian grasslands has been due to its increasing the incidence of a virus in the
1290
native tussock grasses, severely reducing their growth, though the effect may be indirect, due
1291
to its increasing the abundance of the aphids that are vectors of the virus (Malmstrom et al.
1292
2005).
1293
An equivalent to herbivory mechanism ’9 -ve’ seems just possible, and possibly the
1294
disease could remove a more susceptible neighbour that is a facilitator of S (herbivory
1295
‘10 -ve’).
1296
The impact of diseases is obvious when they appear suddenly, as in the case of
1297
chestnut blight. Surely diseases in the past have had a major hand in shaping the plant
1298
communities that are around today, and continue to.
Wilson & Agnew, chapter 2, Interactions, page 41 of 47
1299
8 Interactions
1300
8.1 Litter/herbivore interactions
1301
Grazing, especially by large grazers, can, but does not necessarily, result in:
1302
1. less litter production, because plant vigour is reduced by the removal of
1303
photosynthetic organs and leaves have a lower probability of reaching senescence,
1304
2. redistribution of lying litter by trampling and habitat use, speeding decomposition
1305
(Eldridge and Rath 2002);
1306
3. an increase in the production of leaf litter induced by animal movement damage, the
1307
fall of necrotic leaf tissue damaged collaterally in a browser or grazer, etc., and more
1308
woody litter including CWD from collateral damage by tree canopy browsers (notably
1309
by elephants: Plumptre 1994);
1310
4. material shed around the point of damage, e.g. Buck-Sorlin and Bell (2000), found
1311
that spring defoliation in Quercus spp. (oak) trees in Wales led to increased shoot
1312
shedding;
1313
1314
5. opening of the canopy, increased growth of sub-canopy species, giving more of their
litter.
1315
The complexity of such processes and systems are well illustrated by Long et al. (2003), who
1316
examined the interaction between the beetle herbivore Trirhabda virgata and its food plant
1317
Solidago altissima (goldenrod). Beetle populations were highest in the densest S. altissima
1318
patches, leading to reduced plant vigour and lower litter production. Litter, when present in
1319
quantity, increased aboveground biomass and reduced species richness. Thus the net effect of
1320
the beetle and S. altissima abundance was to enhance plant species diversity by reducing litter
1321
disturbance.
1322
In heavily grazed vegetation, litter is reduced and can have little or no effect, so that
1323
more of the system of interspecific interactions must depend on interference, subvention and
1324
autogenic disturbance. This conclusion conflicts with the usual assumption that competition
1325
will be less intense under heavy grazing. If only living plant presence is recorded and litter is
1326
ignored, only growth interactions can be assessed. This may explain why the strongest
1327
evidence for assembly rules has been found in heavily grazed (i.e. mown) lawns (e.g. J.B.
1328
Wilson and Roxburgh 1994), a heavily grazed saltmarsh (J.B. Wilson and Whittaker 1995)
1329
and a sand dune (Stubbs and Wilson 2004), in all of which there is very little accumulation of
1330
litter and interactions due to growth are not obscured by the litter effect. We suggest that
1331
assembly rules should be sought which include the litter as well as the living components, as
1332
implied by Grime (2001) in his interpretation of the productivity-richness humpback curve.
Wilson & Agnew, chapter 2, Interactions, page 42 of 47
1333
CWD can also interact with herbivory. Long et al. (1998) suggest that treefall mounds
1334
provide a refuge from herbivory for Tsuga canadensis (hemlock) regeneration, which is
1335
important in spite of its being a less favourable environment for establishment of that species
1336
than the forest floor.
1337
8.2 Litter/fire interactions
1338
Sometimes the autogenic effect of litter interacts with allogenic disturbance. Fire is
1339
perhaps the best example. If litter accumulates faster than it decomposes, and local conditions
1340
of climate and soil are too dry to allow peat accumulation, its ultimate fate on a landscape
1341
scale is destruction by fire. This is basically an autogenic effect because there can be no fire
1342
without fuel, and the initiating fuel of a fire is usually a buildup of standing-dead,
1343
programmed and stochastic litter. However, an allogenic process has to start the fire. This
1344
process is intrinsic to heathlands and dry forests worldwide.
1345
Various factors affect the type of fire. A flash fire burning mainly volatiles in either
1346
the field layer or the canopy will hardly involve litter, but a fire that consumes litter will burn
1347
for longer. All fire will impact more on the less fire-resistant and more fire-intolerant species
1348
(Whelan 1995). In many vegetation types, branch fall provides the fuel build up because
1349
CWD is long-lived, much of it persisting until burnt. Treefall also provides fuel (Whelan
1350
1995). The spread of fire into the canopy is facilitated by the retention of dead limbs (Johnson
1351
1992), so branch fall will help to confine fire to the ground flora, sparing the canopy stratum.
1352
Lianas can have a similar effect: Putz (1991) observed flames travelling up lianas, with the
1353
result that Pinus spp. (pine) trees with lianas (especially Smilax spp., greenbriar etc.) were
1354
more likely to suffer crown scorch than liana-free trees. Fire is especially prevalent in
1355
communities of conifers (particularly Pinus) and Eucalyptus (gum) apparently because of
1356
their flammable resin/oil content (Whelan 1995; Williams et al. 1999). At the other extreme,
1357
some types of vegetation are very fire resistant. For example, in arid central Australia, where
1358
most vegetation is fire-prone, Acacia harpophylla (a wattle) does not burn because of several
1359
features: the chemistry of leaves makes them barely flammable; the simple leaf shape results
1360
in flat, poorly-aerated litter fuelbeds; leaf fall is keyed to intermittent rains when fire is less
1361
likely; bark is not shed; and finally the microclimate of the forest floor discourages drying and
1362
promotes decomposition (Pyne 1991).
1363
8.3 Higher-order interactions
1364
1365
There are several good examples of higher-order interactions between grazing, litter
and fire. For example, in North American Pseudotsuga menziesii (Douglas fir) / Physocarpus
Wilson & Agnew, chapter 2, Interactions, page 43 of 47
1366
malvaceus (mallow ninebark) forest, grazing by livestock (including cattle, sheep and deer)
1367
reduces the herb layer and hastens the decay of litter by trampling and the unpalatable herbs
1368
left tend to be less flammable (Zimmerman and Neuenschwander 1984). This reduces fire
1369
frequency, but allows the buildup of coarse woody debris so that when fires occur they are
1370
more severe and may reach the canopy. Similarly grazing reduces the fuel load and hence fire
1371
frequency in the African savannah (Fig. 2.8; Roques et al. 2001). In systems with both a grass
1372
and a woody component (savannah or ecotone) a number of processes can occur (Fig. 2.8;
1373
Brown and Sieg 1999; Touchan et al. 1995).
1374
This process includes many complexities. It could converge to an equilibrium, it could
1375
operate as a cyclic succession, or a switch could also operate in the system, giving alternative
1376
stable states (Fig. 2.8; Dublin 1995). In the 1960s and 70s, fire caused a decline in Serengeti
1377
woodland because higher rainfall then led to greater grass growth (Dublin et al. 1990).
1378
Loxodonta africana (African elephant) inhibited the recovery and kept it as grassland, and
1379
because of their grazing the grass crop is not enough to support hot fires. On the other hand,
1380
elephants avoid the fire-resistant thickets, which are therefore stable as an alternative stable
1381
state. There are both negative and positive feedback processes here.
1382
Wilson & Agnew, chapter 2, Interactions, page 44 of 47
1383
1384
Fire repelled
1385
1386
1387
Woody thicket
1388
remains
Elephant browsing
1389
repelled
1390
Woody patch escapes
1391
the fire
1392
Catastrophic fire,
1393
triggered by an
1394
exceptional event1
1395
Trees
Woody plants killed,
re-establish
1396
at least above ground
1397
1398
Fire frequency
Less palatable
1399
reduced
forbs dominate
1400
More light is allowed
1401
into the field layer
1402
Litter buildup
1403
reduced
1404
1405
1406
Invasion of
Grass growth promoted
woody species
Fewer old
1407 Litter decays
suppressed
leaves
1408 faster
1409
1410
1411
Regular
Trampling
Grazing
1412
fires
1413
Low
1414
High rain
rain
The grazing
Low
1415
resource increases
rain
Herbivore density
1416
increases
1417
1418
1
1419
A rainy season giving a heavy crop of grass followed by a dry season; or a dry season
1420
making savannah burnable; or high browser density causing CWD accumulation
1421
= switch
1422
Fig. 2.8: Pathways of community change in dry savannah.
1423
9 Conclusion
1424
We have described the many processes that can be involved in the development of
Wilson & Agnew, chapter 2, Interactions, page 45 of 47
1425
mixed species stands. Most types of interference, subvention, litter effects and autogenic
1426
disturbance are based on the universal principle of reaction, that organisms in general, and
1427
plants in particular, modify their physical environment. All these reactions have effects on
1428
neighbours. The wide variety of modifications and the wide variety of responses by
1429
neighbours are the reasons for the long list of interactions we gave, a list that we tried to make
1430
exhaustive, but surely have not.
1431
Plants must be seen within the framework of the ecosystem. Autotrophs make up most
1432
of the stored living carbon framework of terrestrial ecosystems, i.e. its biomass, and a plant’s
1433
biomass is also a necessary part of its work in foraging for light and soil resources. But
1434
phytomass is never alone. Operators from other trophic levels are always present and can
1435
have profound influences on plant species presence, adding to the complexity. Clements
1436
envisaged reaction as being on the physical environment. We are reluctant to expand this to
1437
the biotic environment because of the ensuing complications, but we have listed interactions
1438
“mediated by other trophic levels”. There are complex interactions amongst heterotrophic
1439
levels too, which will also impact on our dear plants. Paine’s (1969) original usage of
1440
‘keystone species’ (chap. 5, sect. 11) is a clear expression of these.
1441
The plant community comprises continual renewal: disturbance, death, establishment,
1442
growth and both sexual and vegetative reproduction of great numbers of offspring – greater
1443
than the habitat can support. The negative and positive interactions that we have listed
1444
moderate those processes. In the next chapter we consider how those processes operate at the
1445
whole-community level to determine successional changes after allogenic or autogenic
1446
disturbance and to affect the spatial pattern of vegetation.
1447
Wilson & Agnew, chapter 2, Interactions, page 46 of 47
1448
1449
Table 2.1. Effects of litter on the population dynamics of species in the community, as
reported in the literature.
1450
1451
1452
1453
1454
1455
1456
1457
1458
1459
1460
1461
1462
1463
1464
1465
1466
1467
1468
1469
1470
1471
1472
1473
1474
1475
1476
1477
1478
1479
1480
1481
1482
1483
1484
Feature
Change
References
Germination
(or emergence)
reduced or delayed
Hamrick and Lee 1987
Peterson and Facelli 1992
Bosy and Reader 1995
Facelli and Kerrigan 1996
Molofsky et al. 2000
Barrett 1931
Facelli and Kerrigan 1996
Myster and Pickett 1993
Cintra 1997
Hamrick and Lee 1987
Myster 1994
Berendse et al. 1994
Xiong and Nilson 1997
Facelli et al. 1999
Facelli and Kerrigan 1996
Facelli et al. 1999
Barrett 1931
Hamrick and Lee 1987
Facelli and Pickett 1991a
Moore 1917
Facelli and Facelli 1993
Facelli 1994
Nilsson et al. 1999
Facelli et al. 1999
Monk and Gabrielson 1985
Peterson and Facelli 1992
Facelli and Facelli 1993
Molofsky et al. 2000
Peterson and Facelli 1992
Facelli et al. 1999
Beatty and Sholes 1988
Facelli and Pickett 1991b
Beatty and Sholes 1988
Helvey and Patric 1965
1485
ILLUSTRATIONS
1486
Fig. 2.1. Replacement and additive comparisons in experiments that examine the interaction
1487
increased
Seed predation
reduced
Establishment
reduced
increased
Seedling mortality
Biomass
increased
increased
reduced
Shoot:root ratio
increased
Species composition
changed
Species habitat range
Water interception
changed
increased
between species.
1488
Fig. 2.2. In Trifolium subteranneum, the results of competition affect competitive ability.
1489
Fig. 2.3: A possible mechanism for size-asymmetric competition belowground, when nutrient
1490
1491
1492
supplies become available patchily in time and space, e.g. from sheep micturition.
Fig. 2.4: The effect of R/FR light, as seen in surrounds of different colours. After
Novoplansky (1990).
Wilson & Agnew, chapter 2, Interactions, page 47 of 47
1493
Fig. 2.5: The seasonal pattern of litterfall in an oakwood. After Christensen (1975).
1494
Fig. 2.6. The process of peat accumulation in mires dominated by Empodisma (wire rush) or
1495
1496
Sphagnum moss species.
Fig. 2.7: The effect of brushing seedlings of Brassica oleracea for 1.5 min day-1After
1497
1498
Biddington and Dearman (1985).
Fig. 2.8: Pathways of community change in dry savannah.
1499
1
Weed ecologists normally use an additive design because they are interested in the effect of
a weed on crop, compared to its not being present.
2
Grime added competition for space, but see section 2.2 below.
3
The attempt by neighbouring plants to use the same space can result in contact and damage,
but this is not competition, it is autogenic disturbance (section 5).
4
Microscopic algae do move.
5
When planted as 66 % of the mixture.