Download 6 Plant-plant interactions mediated by other trophic levels

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The nature of the plant community: a reductionist view
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J. Bastow Wilson
Botany Department, University of Otago, P.O. Box 56, Dunedin, New Zealand.
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Andrew D.Q. Agnew
Institute of Biological Sciences, University of Wales Aberystwyth, SY23 3DA, U.K.
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Chapter 2: Interactions between species
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Introduction ................................................................................................................... 2
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Interference: negative effects between plants ............................................................... 3
2.1 Competition ........................................................................................................... 4
2.2 Competition and individual ramets ....................................................................... 5
2.3 Factors for which competition occurs ................................................................... 6
2.4 Plasticity and competition ..................................................................................... 8
2.5 Cumulative effects of competition ........................................................................ 8
2.6 Rarity and competitive ability ............................................................................. 12
2.7 Allelopathy .......................................................................................................... 12
2.8 Parasitism ............................................................................................................ 14
2.9 Spectral Interference (red/far-red) ....................................................................... 14
2.10 Pest carriers ......................................................................................................... 16
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Subvention: positive effects between plants ............................................................... 17
3.1 Water flow and nutrient redistribution ................................................................ 17
3.2 Ambient conditions (temperature, evapotranspiration and wind) ....................... 18
3.3 Aerial leakage of nutrients .................................................................................. 19
3.4 Salt ....................................................................................................................... 19
3.5 Shelter from ultra-violet ...................................................................................... 20
3.6 Protection from soil frost-heave .......................................................................... 20
3.7 Hydraulic lift ....................................................................................................... 20
3.8 ‘Talking trees’ ..................................................................................................... 21
3.9 Subvention conclusion ........................................................................................ 21
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Litter: the necessary product ....................................................................................... 21
4.1 The timing and type of litter production ............................................................. 22
4.2 Litter decomposition ........................................................................................... 26
4.3 Effects of litter ..................................................................................................... 27
4.4 The direct mechanical effect of litter .................................................................. 28
4.5 Alteration in environment by litter ...................................................................... 28
4.6 Leachates from litter............................................................................................ 29
4.7 Control of nutrient cycling .................................................................................. 29
4.8 Peat formation ..................................................................................................... 30
4.9 Can reaction via litter evolve? ............................................................................. 32
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Autogenic disturbance: plants as disturbers ................................................................ 33
5.1 Movement and contact ........................................................................................ 34
5.2 Growth thrust....................................................................................................... 35
5.3 Crown shyness..................................................................................................... 36
5.4 Growth and gravity.............................................................................................. 36
5.5 Lianas .................................................................................................................. 37
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Plant-plant interactions mediated by other trophic levels ........................................... 38
6.1 Below-ground benefaction .................................................................................. 39
Wilson & Agnew, chapter 2, Interactions, page 2 of 53
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6.2 Pollination ........................................................................................................... 40
6.3 Herbivory ............................................................................................................ 41
6.4 Indirect impacts of diseases................................................................................. 45
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Interactions .................................................................................................................. 46
7.1 Litter-herbivore interactions ................................................................................ 46
7.2 Litter-fire interactions ......................................................................................... 48
7.3 Litter-herbivore-fire interactions ......................................................................... 48
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Conclusion ................................................................................................................... 50
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1 Introduction
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Plants interact. In chapter 1, we described how plants arrive at a locale and start to
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develop. In later chapters we shall seek assembly rules – generalised patterns that are the
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imprint of restrictions in the community assembly process. In this chapter we follow our
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reductionist approach by considering the plant-plant interactions that lead to those restrictions.
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Such interactions are often via reactions: modifications of the plant’s local environment. We
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must beware of assuming that any or certain interactions necessarily occur, but any set of
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organisms that are in close proximity must affect each other and these interactions can be
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mediated through many processes.
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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 interference. This can be set up to examine a replacement situation, or an
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additive situation, or both (Fig. 2.1).
Monoculture of A
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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.
Wilson & Agnew, chapter 2, Interactions, page 3 of 53
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Suppose species A has a somewhat stronger competitive ability than species B. If we
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ask about gains and losses (+ and –) as textbook tables do, the question is gain or loss relative
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to what? In the replacement comparison (i.e. comparison with monocultures at the same
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overall density, the de Wit replacement design(define): Fig. 2.1), A will gain and B will lose:
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a +– situation. Yet in an additive comparison (i.e. comparison in which each species has the
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same density in monoculture as in mixture), both will suffer competition to some extent: a – –
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situation. This looks at first sight to be an artefactual distinction of experimental design, but it
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applies equally to questions in the field. This leads to misunderstandings between animal and
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plant ecologists, who are really quite different species (though they have been known to
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interbreed). Animal ecologists think in terms of adding one species to another. Weed
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ecologists do normally use an additive design, because they are interested in the effect of a
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weed on a particular density of a crop. 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 lose. So really you are distinguishing between 2
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types of ecologists, animal ecologists and weed ecologists (who use the same additive design)
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and plant ecologists who use a replacement design. Of course these are grand generalizations
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that don’t always hold up, but what bothers me the most is the insinuation that plant
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ecologists see competition as resulting in one plant gaining and one loosing b/c of their
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experimental design. Now that’s a truly grand assumption without any backing.
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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. We follow the precedence of Clements et al. (1929), and the textbook
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definition of Begon et al. (1996) to give:
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interference (negative effects)
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competition = via removal of resources from the environment
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allelopathy = via toxic substances
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parasitism = removal of resources directly from the plant
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spectral interference
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pest carriers.
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[Other negative effects are discussed elsewhere, via: litter (sect. 4), autogenic disturbance
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(sect. 5), other trophic levels (sect. 6) and other types of reaction such as pH modification
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(chapt. 3).] Interference can occur extremely early in the development of the plant
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community, as seed-seed interference before the seeds emerge. This could be through
Wilson & Agnew, chapter 2, Interactions, page 4 of 53
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competition for water for imbibition and anchorage by mucilaginous coat, but allelopathy is
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the more likely cause (Harries and Norrington-Davies 1977; Murray 1998).
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2.1
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Competition
We use the definition of Begon et al. (1996): “Competition is an interaction between
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individuals, brought about by a shared requirement for a resource in limited supply, leading to
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a reduction in the survivorship, growth and/or reproduction of at least some of the competing
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individuals concerned”. Grime’s (2001) definition very close: “The tendency of neighbouring
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plants to utilise the same quantum of light, ion of mineral nutrient [or] molecule of water …”.
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(Grime added competition for space; we have omitted it because we do not believe that it
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occurs.)
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Don’t rooted plants need some soil surface on which to exist? Please provide more
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explanation here, or at least state that the topic will be discussed in more detail later in the
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chapter.
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You need to either give references or say that you will explain later, or both.
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The subject of competition has occupied most plant ecologists from time to time. The
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result is a weighty literature and a plethora of ideas, models and theories. We could not do it
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justice to all this here (though you could cite select references of good synthesis or histories),
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and we deal only with selected topics. In all species of plant there are more seeds and juvenile
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plants than adults, which indicates mortality. Some have proposed that there is no observable
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competition in existing communities, perhaps only the residuum of past competition. We shall
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discuss this in chapter 6 (sect. 9.2).
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Competition must be for some limiting resource, such as light, water, CO2, nutrients,
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radiant heat and, some claim, space. As Clements et al. (1929 pp. 316-317) expressed it:
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“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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that he emphasises that all competition is via reaction.
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Transitivity in interference networks is discussed in chapter 5. Give more here, at least
a definition or leave it out till later.
Wilson & Agnew, chapter 2, Interactions, page 5 of 53
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2.2
Competition and individual ramets
Competition must occur between individuals, even if our interest is in interspecific
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interactions. If we follow the Gausian principle of competitive exclusion, two similar species
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cannot occupy the same niche (Krebs 1972). It follows that the greatest potential for
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competition should be between individuals with the same resource requirements, and there
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can be no greater similarity than between individuals of the same species. There is no
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fundamental difference in the competitive process between motile individual animals and our
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plants. One owl eats a mouse, so another cannot, and perhaps dies. One plant takes up water
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from the soil, so another cannot, and perhaps dies. The competition is sometimes ultimate
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rather than proximate: a lion defends its territory rather than competing directly, but the
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existence of territorial behaviour is set by evolution in order to defend resources, and the size
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of territories are probably adjusted in ecological time to the density of resources. Similarly, a
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plant may not compete so strongly with its neighbours because they are suppressed by its
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allelopathy or by its harbouring pests/s, and these behaviours may be adaptations (or may not:
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Newman 1978). One usual difference is that since animals are quite aplastic, competition
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normally affects densities rather than individual size, but plants are plastic, so that
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competition affects plant size before density. Thus, the effects of plant competition are best
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expressed as total biomass (often above-ground, for practical reasons) per area.
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Often, some decrease in density does result from competition and this has been
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generalised as an approach to a straight line on a plot of log (mean individual plant weight)
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against log (density). The slope of such a line has been justified on theoretical (especially
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geometric) grounds and on the basis of observations as being any of -3/2, -1/2 or -3/4 (Harper
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1977; Torres et al. 2001). When competition is for light and is cumulative (sect. 1.1.6 below),
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there is a particular reason to expect mortality: a dominance hierarchy will result in which the
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small/short plants lag further and further behind the large/tall ones, until they die (Black
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1958). When competition is for nutrients and water no such effect will be present (J.B. Wilson
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1988 %019) so self-thinning should be much less prominent and the -3/2 (etc.) relation may
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be absent. This has not been investigated, probably because it would be difficult to impose
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realistic competition for nutrients or water without there being competition for light. Nutrient
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availability can moderate the relation caused by competition for light, not changing the -3/2
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(etc.) slope but changing the density and mean weight per plant at which self thinning starts to
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take place (Bi 2004, Morris and Myerscough 1991).
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Shoots generated by vegetative reproduction via rhizomes or stolons are produced at
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lower densities than those sometimes seen in seed-established populations. Moreover, mutual
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support through ramets (Marshall and Sagar 1968) should reduce mortality, perhaps
Wilson & Agnew, chapter 2, Interactions, page 6 of 53
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eliminating self-thinning. However, self-thinning mortality has been seen in these situations:
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in the culms of the Gynerium sagitatum (uva grass; Dekroon and Kalliola 1995), in the tufted
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regeneration of two Sasa spp. (bamboo; Makita 1996) and in shoots of Urtica dioica (nettle;
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Hara and Srutek 1995). Developmental controls are certainly capable of suppressing bud
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development, as they do during tree growth, so that we can only presume that its failure in
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clonal herbs has value, such as in the maintenance of stands in the monospecific condition in
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spite of accidental death of individual shoots. The above is an awkward paragraph. It’s intent
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is unclear- what point are you trying to get across.?
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2.3
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Factors for which competition occurs
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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one plant or another. This clearly includes light, C (CO2), water, macronutrients (NPK) and
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micronutrients (Ca, S, Mg, etc.). Even though Clements claimed radiant heat, it seems more
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like pH, an environmental factor, but how is it different from light? Is soil O2 a resource,
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because a molecule absorbed by one plant means it is not available for another? But it is
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related to redox potential, which seems more like an environmental factor. These matters are
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difficult at the edges.
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Light is the resource for which competition has most often been analysed, and we
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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 and disappears if not used; it is also directional in source (e.g. sect. 2.5).
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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; Wilson and Newman 1987). The main issue is that
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because N is more mobile in soils than P it is possible for two plants to come into competition
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for N before they compete for P (Bray 1954). The mobility of K is intermediate
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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 the canopy of Prosopis glandulosa (mesquite) subvents the survival of saplings
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below the canopy, competition for water develops as they age. Robberecht et al. (1983) found
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that in the Sonoran Desert removing all other plants surrounding a tussock of Hilaria rigida
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increased the water potential which led to the plants remaining green for longer into the dry
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reason and growing more. Perez-Salicrup and Barker (2000) found that after lianas had been
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removed from seasonally-dry tropical forest in Brazil the water potential of trees increased
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and they grew faster but the authors did not discuss how much of this was due to the obvious
Wilson & Agnew, chapter 2, Interactions, page 7 of 53
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increase in light due to removal of the liana canopy. Like mineral nutrients but in contrast to
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light soil water remains available for some time if not 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.
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Temperature is a rate-regulator, not a resource, although 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 air in waterlogged conditions.
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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 competition.
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However, sometimes it is made clear that space is seen 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.
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As far as spatial volume is concerned, Chiarucci et al. (2002) measured the percentage
volume occupancy of eight plant communities (four in each in each of Italy and NZ,
Wilson & Agnew, chapter 2, Interactions, page 8 of 53
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comprising four grasslands and four shrublands). In spite of all the assumptions and
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speculation in the literature, this had never before been measured. They found that only
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0.44% to 2.89% of the available volume within the canopy was occupied by plant tissue and
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concluded: “physical space is probably never limiting by itself in terrestrial higher-plant
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communities, so that competition for space, distinct from competition for resources such as
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light, water and nutrients, is not likely to exist”. Clements (1916, 72) understood this: “In a
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few cases, such as occur when radish seeds are planted too closely, it is possible to speak of
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mechanical competition or competition for room. … However [this] seems to have no
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counterpart in nature. There is no experimental proof of mechanical competition between
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root-stocks in the soil, and no evidence that their relation is due to anything other than
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competition for the usual soil factors – water, air and nutrients.” Actually, there is no evidence
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that it occurs between close radishes. Even Tilman (1982), though devoting a chapter to
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competition for space, is careful to note that physical space “may be irrelevant”. He notes that
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disturbance can create open space, but that “it would seem better to study explicitly the
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resources supplied by disturbance”. We agree. The attempt by neighbouring plants to use the
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same space can result in contact and damage, but this is not competition, it is autogenic
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disturbance (sect. 5 below).
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2.4
Plasticity and competition
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We must remember that the competitive abilities of the plant are determined not by its
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characters in monoculture but by those changed by plasticity in competition. This can be seen,
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and is well-known, above ground, for example etiolation, an increase in height as a result of
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shade (Bradshaw 2006). Collins and Wein (2000) found that two Polygonum species
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(arrowleaf tearthumb and smartweed) increased in internode length when crowded by plants
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of the same two species. Plasticity occurs in less visible characters too. For example, Huber-
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Sannwald et al. (1996) found that two steppe grasses differed markedly in their plastic change
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of specific root length. Bookman and Mack (1982) found by double-labelling of shoots that
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when Bromus tectorum (downy brome) was growing in competition with Poa pratensis
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(meadow grass) its root system was constricted laterally, but extended slightly deeper.
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2.5
Cumulative effects of competition
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The term ‘asymmetric competition’ (with the more general ‘asymmetric interference’)
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is used in two senses. Firstly, it can mean that the interference effect of Species A on Species
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B is different from that of B on A. Perhaps A suppresses B, but B has no effect on A, or the
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difference can be quantitative: more effect of A on B than of B on A (e.g. Roxburgh and
Wilson & Agnew, chapter 2, Interactions, page 9 of 53
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Wilson 2000 %395; Ives and Hughes 2002 %388). This would be expected since species by
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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 (chapt. 3, sect. 7.3 below). This concept can be applied to
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individual genotypes too.
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The second meaning of ‘asymmetric competition’ is not so easy to define. Wedin and
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Tilman (1993 %199) synonymise it with ‘resource preemption’, apparently implying an
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advantage to the first plant to arrive. For Schwinning and Fox (1995 %432) it implies that
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“large plants greatly suppress the growth of smaller neighbors”, and more precisely for
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Weiner et al. (1997 %85) that “larger plants are able to obtain a disproportionate share of the
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resources (for their relative size) and suppress the growth of smaller individuals”. It has
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therefore been termed ‘size asymmetry’ to distinguish it from A/B asymmetry. The problem is
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what is a plant, so what is size? If a large grass tiller divides into two small, physiologically-
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independent tillers, is it no longer large? (that depends on the question you are asking) Many
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authors have reached the conclusion that initial differences are magnified into a large effect
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on the long-term outcome of competition, so that the process favours competitive exclusion.
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There is truth in this, but it is too 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
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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 cause:
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plants from small seeds held their leaf area a little lower than those from large seeds. In
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monoculture, this 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. In this
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context, ‘height asymmetry’ would be more appropriate than ‘size asymmetry’.
Wilson & Agnew, chapter 2, Interactions, page 10 of 53
Larger
individual
leaves
Longer
petioles
Greater
biomass
Leaf area
held higher
Faster
growth
(RGR)
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Disproportionate
percentage of
the light captured
Fig. 2.2. In Trifolium subteranneum, the results of competition affect competitive ability.
It cannot be assumed that competition for light will always be cumulative. Hirose and
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Werger (1995 %466) 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 %1072) to failed to find biomass
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size-asymmetry in competition for light between Betula alleghaniensis (yellow birch)
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seedlings, apparently perhaps because of height plasticity in small, shaded plants.
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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?!!.
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The deep roots are hardly likely to ‘shade’ roots nearer the surface from NPK rising up
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through the soil. In any case, nutrients are generally much more available near the surface,
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where small plants can easily root. Uptake of water is sometimes from aquifers, but it is hard
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to envisage a root shield comparable to the canopy aboveground. In terms of allometric
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growth, if a plant is larger by ×2 in each dimension, it will be ×23 = ×8 larger in volume and
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in biomass. Therefore, its NPK requirements will be ×8. However, its root system will cover
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an 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. Why are you looking at the above ground plant as a 3D entity and the
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below ground plant as a 2D entity? Seems inconsistent given that plants occupy a soil volume
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not a soil plane.Thus, it seems reasonable that Rajaniemi (2003) could find only very
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ambivalent evidence of size-asymmetry in below-ground competition, 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 competition (Wilson 1988 %019; Weiner et al. 1997 %085). So if
Wilson & Agnew, chapter 2, Interactions, page 11 of 53
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I were to stop here, I could maybe extrapolate as to how some of these characteristics may
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extend to plant community characteristics…
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We could think of possible exceptions. If nutrients are available patchily, small plants
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can grow in high-NPK areas, whereas a large plant might need to include in its root system
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the nutrient-poor matrix, with actual disadvantage to the large plant. However, if nutrients
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were available intermittently in time and space, such as animal urination patches, perhaps a
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large plant could take up enough to satisfy the whole of itself from a few roots in the patch,
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whereas a small plant outside the patch could not reach in (Fig. 2.3). This argument applies
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only when the patches are transient, so it seems reasonable that Blair (2001 %199) could find
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no evidence that spatial heterogeneity in nutrients led to size-asymmetric competition.
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If nutrients are patchy, then all plants have a roughly – chance of landing
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(germinating) in a high nutrient patch. Larger plants though have an increased chance of
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capturing a high nutrient patch within their root-soil-volume. Therefore the large plant will
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be more likely to have access to a high nutrient area than a small plant. The large plant does
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have to support roots in low nutrient areas, but once a high nutrient area has been
349
encountered, the plant can allocated increased root growth into that soil volume.
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.
350
351
We conclude that cumulative competition, due to size-asymmetry, i.e. the effect of
352
initial advantage, is not a necessary feature of plant competition. It will occur only when there
353
is a specific feedback mechanism, such as that via height/light, that results in competitive
354
success increasing competitive ability per unit biomass. The conditions under which it occurs
355
have huge implications for community structure, because if competition be cumulative
356
competitive exclusion will occur much more readily, and faster, and coexistence less readily.
Wilson & Agnew, chapter 2, Interactions, page 12 of 53
357
2.6
Rarity and competitive ability
358
It is often suggested that plant species become rare because they are poor competitors,
359
but the evidence here is mixed. Walck et al. (1999) found that low competitive ability may be
360
one factor contributing to the narrow endemism of the dryland species Solidago shortii
361
(goldenrod) in comparison with the widespread S. altissima, which can overtop S. shortii in
362
more mesic sites but it is simplistic to interpret a two-species comparison in terms of general
363
trends in rarity. Lloyd et al. (2002) working in New Zealand found that there was no general
364
relation between competitive ability and rarity at either high or low levels of soil fertility for
365
ten species in the rosaceous genus Acaena (biddy bid), but in the grass genus Chionochloa
366
(snow tussock) common species tended to be stronger competitors than rare species, and this
367
was significant at the low level of fertility—in some sense, either via initial
368
advantage/competition or through some sort of competitive mechanism, isn’t it inevitable that
369
common species have competed their way to their place?. Several of the common
370
Chionochloa species have expanded their geographic ranges since anthropogenic forest
371
removal, consistent with their greater competitive ability. Conversely, rare Chionochloa
372
species occupy specialized habitats that may be interpreted as refuges from competition—is
373
this the competition v. ruderal v. disturbance idea?. However, it is too simplistic to speak of a
374
plant being a generally strong or weak competitor. Apart from ruderals, every species is a
375
good competitor in the sites that it inhabits, at least a good enough one to persist. Hubbell et
376
al. (2001 %759) reported a curious relationship between rarity and neighbourhood effects in
377
neotropical forest, such that the survival by rare trees was more adversely affected by
378
conspecific neighbours than that of common species. One explanation is that the rare species
379
are using rare resources, or that they are limited by specific pests (chapt. 4, sect. 3 below)
380
2.7
381
Allelopathy
Allelopathy is another type of interference. Unlike competition, it does not involve a
382
“shared resource in limited supply” (sect. 2.1 above). Rather, a toxin produced by plants is
383
either leached or volatilised from their living parts, above- (Inderjit et al. 1999) or below-
384
ground (Kato-Nogudi 2004), from standing dead plants (Gliessman and Muller 1978), or from
385
the breakdown of their litter (e.g. Kuiters 1991; Sharma et al. 2000), and then reduces the
386
growth of neighbouring plants. Some ecologists believe that allelopathy is a widespread and
387
important process (Rice 1983; Inderjit et al. 1994). Others are sceptical (Harper 1977). Most
388
plants contain chemicals that are toxic to other plants, at least in the right circumstances. It is
389
very unlikely that the strong effects that can readily be demonstrated by leaf elutants in petri
390
dishes will happen in nature, but it is equally unlikely that soil bacteria and colloids will
Wilson & Agnew, chapter 2, Interactions, page 13 of 53
391
completely neutralise the effect, and field experiments are difficult to perform (Williamson
392
1990).
393
Most work has been with shoot elutants, but Mahall and Callaway (1991 %2145; 1992
394
%874) conducted greenhouse experiments between Larrea tridentata (creosote bush) and
395
Ambrosia dumosa (white bursage). The two species occur together in the Mojave Desert.
396
Roots of A. dumosa were inhibited when they came near to roots of L. tridentata. This effect
397
was reduced by activated carbon, so it was presumably via some chemical. The two species
398
apparently have similar water extraction capabilities (Yoder and Nowak 1999b), so this
399
signalling would enable to the plants to avoid each other and postpone the onset of
400
competition. This may be a more common phenomenon than we have knowledge of at
401
present. More direct evidence for the production of toxins from roots was obtained by
402
Welbank (1963), but only after they had started to decompose in anaerobic conditions. But
403
there are always decomposing roots around a living plant and they may indeed create
404
anaerobic conditions in the immediate vicinity of the decomposing root through their own
405
decomposition or the uptake of O2 by neighbouring roots. Perhaps then it isn’t unreasonable
406
to look at this as a source of these compounds.
407
We are inclined to think in teleological terms, of plants deliberately inhibiting their
408
neighbours. Although we know this is not true, it leads to an assumption that allelopathic
409
ability has evolved as an adaptation: species that make their locale unfavourable for the
410
growth of other species will gain in selection. But can this evolve? If a mutant produces an
411
allelochemical against other species this will be at some cost to itself (many of the secondary
412
compounds involved are expensive for the plant to make), yet unless the effect is very local it
413
will benefit non-mutant plants of the same species as much as itself—but isn’t it often very
414
local? Especially in ecosystems where, e.g. the Janzen scatter hypothesis holds, species’
415
individuals tend to spread out anyway?, and the trait will not evolve. Why shouldn’t the
416
allelopathic chemical affect non-mutants of the same species?
417
We then have to invoke group selection, is a controversial and probably weak force
418
(Wilson 1987 %493). This problem would not occur with selection for a plant to protect itself,
419
and thus eventually its species, against its own allelochemical. Williamson (1990) commented
420
that there would be equal selective pressure on the species’ neighbours to develop defences,
421
but this ignores the issue that a species always grows with itself, but has a variety of
422
neighbours against which it would have to protect itself. Newman (1978) questioned whether
423
selection was involved at all, finding in a literature survey that auto-toxicity is as common as
424
toxicity to other species. He argued that this indicates that allelopathy is an accidental result
425
of the production of secondary compounds.
Wilson & Agnew, chapter 2, Interactions, page 14 of 53
426
427
We discuss the particularly complex allelopathic interactions with litter in section 3.5
428
below.
429
2.8
430
Parasitism
Plant parasites are commoner in the dry tropics than in temperate climates. There are
431
partial shoot parasites (Loranthaceae, Viscaceae) and total shoot parasites (e.g. Cuscuta,
432
Cassytha) as well as partial (e.g. Rhinanthus spp.) and total root parasites (e.g.
433
Balanophoraceae, Orobanchaceae, Rafflesiaceae, Striga gesnerioides). The immediate effect
434
of a parasite is to depress the growth of the hosts. Infestation by some root parasites can
435
reduce crops by up to 70% (Graves et al. 1992; Press 1998). There is often an increase in
436
species diversity (Press 1998). This may be because the parasite’s favourite hosts are the
437
dominant species, and a reduction in their productivity allows subordinate species to flourish,
438
possibly also reducing cumulative competition (sect. 1.1.4 above). It is not clear why parasites
439
should favour the dominants, but perhaps we see the effect more when they do. On the other
440
hand, the parasite could reduce the productivity of the whole community from high to
441
medium, allowing more species to coexist if the humped-back theory of Grime (1973; 2001)
442
is correct. Situations, however, can be very complex when plant hosts, their parasites and their
443
herbivores are examined. Marvier (1996; 1998) compared aphid performance on the parasite
444
Castilleja wightii (paintbrush) in host plants differing in N content, which was highest in a
445
legume (Fabaceae) and lowest in a composite (Asteraceae). Aphid populations did best on the
446
parasite when it depended on the legume host and worst when the host was the composite,
447
leaving the C. wightii worse off on the legume, in spite of the latter’s higher nitrogen content.
448
These interactions differentially affect the host plant species and their parasite, modifying
449
competitive ability, but are complicated by the parasite’s ability to better its performance by
450
mixing its hosts.
451
2.9
Spectral Interference (red/far-red)
452
Plant canopies change the spectral quality of light that passes through them. Of
453
particular importance for plant-plant interaction is that the red/far-red ratio (R/FR) is lower in
454
light that has passed through a leaf or been reflected off one. It is therefore lower under
455
canopies and somewhat lower in canopy gaps than in the open (Turnbull and Yates 1993;
456
Davis and Simmons 1994). This can decrease the leaf chlorophyll content of plants in the
457
lower strata and hence reduce their photosynthetic capacity, leaf life, leaf area ratio, tiller
458
production and relativeh growth rate (Barreiro et al. 1992; Dale and Causton 1992; Skinner
Wilson & Agnew, chapter 2, Interactions, page 15 of 53
459
and Simmons 1993; Rousseaux et al. 1996), and decrease seed germination (Batlla et al.
460
2000, Kasperbauer 2000).
461
These responses are mediated by phytochrome (Gilbert et al. 1995). However, the
462
response depends on the species. Leeflang (1999) found that only one species out of the six
463
that they examined responded to R/FR ratio in terms of biomass accumulation. Dale and
464
Causton (1992) found differences between three Veronica species (speedwell): the species
465
that grew in deeper shade responded more to R/FR. It can be difficult to separate effects of
466
light intensity and spectrum, but sometimes plants respond morphologically to the presence of
467
neighbours even before they are directly shaded, by sensing the change in R/FR in light that
468
has been reflected off neighbours (Schmitt and Wulff 1993).
469
R/FR may be less important for its direct effect on the growth of the recipient than as a
470
signal to the plant that competition is imminent, allowing it to respond by either competition
471
tolerance or competition avoidance. (Murphy and Briske 1994; Stuefer and Huber 1998). For
472
avoidance, R/FR can induce plastic changes which would allow the plant to reduce shading
473
by its neighbours, e.g. enhancing leaf elongation, making shoots and leaves more upright, and
474
increasing shoot:root ratio (Skinner and Simmons 1993; Vanhinsberg and Vantienderen
475
1997). The R/FR signal can also promote plant foraging for light gaps away from competitors,
476
through altered stem angle and longer internodes (Ballaré et al. 1995). Some plants sense and
477
grow away from each other, even at some distance. Manipulation of R/FR ratios, and
478
experimentation with pieces of plastic with the same spectral characteristics as plant leaves,
479
show this to be due to R/FR effects (Fig. 2.4; Novoplansky 1991). Germination can be
480
reduced under a canopy, but faster germination is also possible, and these R/FR responses can
481
be seen as competition avoidance and greater competitive effort, respectively (Dyer et al.
482
2000). R/FR is not everything: Muth and Bazzaz (2002) found that visible (PAR) light was
483
more important than R/FR in the gap-seeking of Betula papyrifera (birch) seedling.
Wilson & Agnew, chapter 2, Interactions, page 16 of 53
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 (1991).
484
485
486
2.10 Pest carriers
Plants can interact at a local scale using pests as weapons. Van den Bergh and Elberse
487
(1962) found that under a high nutrient regime Lolium perenne at first outcompeted
488
Anthoxanthum odoratum, but eventually A. odoratum transmitted a virus to L. perenne and
489
suppressed it. There is evidence that the invasion of the exotic Avena fatua (wild oat) into
490
Californian grasslands has been due to its increasing the incidence of a virus in the native
491
tussock grasses, severely reducing their growth, though the effect may be indirect, due to its
492
increasing the abundance of the aphids that are vectors of the virus (Malmstrom et al. 2005).
493
A similar situation may exist in California where preliminary evidence suggests that
494
Umbellularia californica (Bay laurel) is infected with the fungus Phytophthora ramorum, but
495
is little affected. However, many spores are produced and these cause the death of nearby
496
Quercus spp. (oaks) and Lithocafvrpus densiflora (tannoak) (Mitchell and Power %Collinge
497
58). We list these examples of species as pest carriers separately, though they grade into
498
plant-plant interactions moderated by diseases (sect. 4.4, below).
499
Wilson & Agnew, chapter 2, Interactions, page 17 of 53
500
501
3 Subvention: positive effects between plants
502
Just as the plant community provides a diversity of habitats for heterotrophic
503
organisms, so it augments the diversity of sites available for plant species by increasing
504
environmental heterogeneity both horizontally and vertically. One logical result of this
505
reaction (sensu Clements) should be subvention: positive effects by some species on the
506
survival and/or growth of others. Gleason (1936) gave subvention equal weight with negative
507
interference, but whilst the interference between species has been a focus of attention
508
subvention has been neglected until recently (Lortie et al. 2004). Subvention changes during
509
ecesis as plants grow and change shape, so that repeatable patterns of interaction are difficult
510
to find. Usually two species are not absolutely dependent on each other for survival.
511
Moreover, the existence of a subvention by species A on species B does not imply that they
512
have co-evolved. It is simply a corollary of reaction. The terminology of subvention is
513
confusing. We use the scheme:
514
subvention
515
mutualism (= synergy) = both species benefit relative to their being at the same
516
density on their own (i.e. an additive comparison).
517
benefaction = one species benefits as above, with no known advantage or
518
disadvantage to itself
519
facilitation = one species benefits another, to its disadvantage
520
The term ‘facilitation’ was used thus by Connell and Slatyer (1977) for Clements’ (1916)
521
concept of the mechanism of succession, but it is appropriate here since the mechanisms are
522
the same. We consider here the various environmental features which are modified by plants
523
to the benefit of their own, or other species. The list is a long one, and we are aware that many
524
potential effects have been left out. The review by Callaway (1995) discusses more examples
525
than are cited here.
526
3.1
Water flow and nutrient redistribution
527
Plants intercept rainfall. Up to half of the input can be lost by evaporation from the
528
canopy (Cape et al. 1991), but input is occasionally increased due to fog capture (chapt. 3,
529
sect. 5.4.B below). The distribution of soil water input is made far more patchy, for example
530
through stemflow amongst many interactions. Nutrients can be made even more patchy
531
because of leaf leaching. Stemflow can be an important source of nutrients for epiphytes,
532
especially of nitrogen for which stemflow concentrations can be more than ten times those in
Wilson & Agnew, chapter 2, Interactions, page 18 of 53
533
rainwater (Awasthi et al. 1995; Whitford et al. 1997). This may explain the trunk-base habitat
534
of a few mosses such as Isothecium myosuroides in Western Europe. This induced patchiness
535
in nutrients is a good example of benefaction without there being any question of co-
536
evolution. In the clustered or striped vegetation (‘tiger bush’) typical of arid and semi-arid
537
areas (chapt. 3, sect. 5.4.B below), there can be similar benefaction by shrubs and trees of
538
their understorey. For example, litter can increase infiltration into the soil by preventing
539
runoff in semiarid areas (Tongway et al. 2001). However care must be taken in interpreting
540
these patterns. Walker et al. (2001) demonstrated by plant manipulations that whilst islands of
541
soil fertility around woody plants can increase water and nutrient availability, the net effect of
542
nurse plants can be negative due to shading and/or root competition.
543
3.2
544
Ambient conditions (temperature, evapotranspiration and wind)
Plants alter the physical environment around and below them in obvious ways:
545
ambient temperature, evapotranspiration and air movement. This is reaction. Canopy trees
546
dampen diurnal and seasonal fluctuations in subcanopy air temperature (Stoutjesdijk and
547
Barkman 1992; Chen et al. 1993) and this is significant because temperature stresses of heat
548
load or frost can kill cells. Daytime temperature in the field layer of a forest is generally 1-
549
3 oC less than above the canopy. Windspeed is lower, reducing transpirational load and the
550
abrasion of photosynehetic organs (sect. 3.3 below). Humidity is higher, reducing water
551
stress. Within one grass stratum, Liancourt et al. (2005) gave evidence of benefaction between
552
species in a calcareous grassland due to amelioration of water stress. Plant species differ in
553
their reaction on the microclimate (Castro et al. 1991) and in their response to microclimate
554
(Stoutjesdijk and Barkman 1992; Tretiach 1993). In extreme environments the presence of
555
one plant can allow another to survive.
556
In alpine and arctic habitats krummholz trees can shelter a shorter species from wind
557
desiccation, storm damage and wind-born ice particles (Marr 1977, Callaway 1998). Similar
558
subvention can occur amongst alpine herbs, possibly as a mutualism (e.g. Choler et al. 2001).
559
In arid and semi-arid areas tree shade has an obvious associated flora. Extensive
560
woody vegetation with isolated canopies can be an essential part of system function in warm
561
semi-arid climates, and often fine soil and organic matter accumulate below the canopy,
562
bearing a herbaceous flora. The association between nurse plants and their beneficients is
563
often so clear that no attempt is made to determine the precise environmental variable that is
564
responsible, but it is generally assumed to be temperature combined with humidity (e.g.
565
Brittingham and Walker 2000). Temperature differentials are easy to demonstrate and very
566
well documented (e.g. Suzán 1996; Godínez-Alvarez et al. 1999), and in hot deserts with
Wilson & Agnew, chapter 2, Interactions, page 19 of 53
567
summer rainfall cell death by high temperatures can be a critical factor in survival. This is
568
particularly important for succulents, which can suffer from heat load in full sun, being unable
569
to lose as much heat by convection as thin-leaved plants. Water loss is also a problem for
570
plants. Under shrub canopies, the litter ameliorates soil processes, increasing water-holding
571
capacity. Shrub nurse effects are sometimes attributed to nutrient buildup but Gómez-
572
Aparicio et al. (2005) found that in dry Spanish shrublands most of the effect was due to
573
canopy shade. Belsky et al. (1993 %143) have meticulously described the complex of
574
interactions in East Africa, while Holzapfel and Mahall (1999) carefully separated subvention
575
from interference between Ambrosia dumosa (white bursage) shrubs and annuals in the
576
Mojave. Amiotti et al. (2000) show that isolated Pinus radiata trees in Argentina have similar
577
effects. In a fascinating series of subventions in western Texas, Prosopis velutina (mesquite)
578
canopy allows the establishment of a Juniperus pinchotii (juniper), while J. pinchotii helps
579
the establishment of three other woody species with a more mesic distribution (Armentrout
580
and Pieper 1988; McPherson et al. 1988). Presumably there are more mesic conditions of
581
temperature and water relations under these canopies.
582
These are good examples of subvention that do not seem to be the result of co-
583
evolution.
584
3.3
Aerial leakage of nutrients
585
Nutrients such as nitrogen can be leached from canopy leaves and absorbed by the
586
leaves of other plants below (McCune and Boyce 1992; Cappellato and Peters 1995). This
587
interaction is difficult to categorise. Presumably one organism loses and the other gains,
588
almost by definition, as in predator/prey and parasite/host relations, except that there would
589
be leakage from the loser whether there was a recipient below or not. It seems best
590
categorised as benefaction.
591
3.4
592
593
Salt
A plant could shelter another from salt spray deposition (Malloch 1997). It could also
increase its salt spray load. Neither effect seems to have been demonstrated.
594
Bertness and Hacker (1994 %363) showed, by removing Juncus gerardii (a rush) from
595
a New England, USA, saltmarsh showed that its presence had raised the redox potential of the
596
soil and, by reducing evapotranspiration, kept down the soil salinity. Without this benefit, the
597
associated Iva frutescens (marsh elder) died. Transplants of J. gerardii to the low and mid
598
zones of the marsh also benefited from the presence of J. gerardii and/or I. frutescens
599
neighbours because of lower salinities. However, transplants into higher zones in the marsh
Wilson & Agnew, chapter 2, Interactions, page 20 of 53
600
were suppressed by the I. frutescens there, so this is a one-way subvention, benefaction rather
601
than mutualism.
602
3.5
603
Shelter from ultra-violet
In some species, ultra violet light (UV-B) damages cells and their photosynthetic
604
apparatus, so we might expect that plants could exhibit benefaction by UV-B shielding. This
605
could be stronger in alpine communities, with higher UV-B. The transmittance of UV-B to
606
lower strata differs with the canopy structure of different species (Shulski et al. 2004). Species
607
and ecotypes react differently to UV-B in growth rates (Dixon et al. 2001; Robson et al.
608
2003). All the components for a benefaction seem to exist, but we cannot find any evidence
609
that it exists in nature.
610
3.6
611
Protection from soil frost-heave
Ryser (1993) found that, of six species examined in limestone grassland in
612
Switzerland, two appeared to require shelter from neighbouring plants against frost heave as
613
well as drought.
614
3.7
615
Hydraulic lift
This is the process by which one species takes up water from deep layers in the soil
616
and releases it in the surface layer. In arid climates, woody rheatophytes with deep roots in an
617
aquifer could benefit species with shallow roots by this mechanism. Indeed, Facelli and
618
Temby (2002) show that Atriplex vesicaria and Maireana sedifolia (both Chenopodiaceae)
619
enhance the water relations of their surrounding annuals. However, they can also compete for
620
light, leading to a complex interaction. In a nice variant of the story, Yucca schidigera in the
621
Mojave Desert, with CAM photosynthesis, apparently redistributes soil water by creating a
622
higher upper-soil water potential during the day, rather than at night when it has open stomata
623
and a higher water demand (Yoder and Nowak 1999 %093). Surrounding non-CAM plants
624
with a high water demand must benefit. The phenomenon is also known in temperate forest
625
where Dawson (1993) and Emerman and Dawson (1996) have shown that Acer saccharum
626
(sugar maple) uplifts considerable quantities of water, much of which may be taken up by
627
understory plants from near the exuding tree roots. This phenomenon is benefaction or
628
possibly facilitation, and may be much more common that formerly supposed (Caldwell et al.
629
1998), but most authors stress that soil particle size and structure can be critical in the process.
630
Roots can also distribute water to deeper soil layers (Ryel et al. 2003).
Wilson & Agnew, chapter 2, Interactions, page 21 of 53
631
3.8
632
‘Talking trees’
Plants can often increase their content of defence compounds when grazed (see
633
below). It has been suggested that they can do this upon receiving a chemical signal such as
634
methyl jasmonate released by nearby grazed plants: the ‘talking trees’ mechanism. Although
635
early work was plagued by problems such as pseudoreplication, careful work has since
636
validated the effect (Karban et al. 2000). The remaining puzzle is whether it can be a product
637
of natural selection since it benefits the neighbours of a plant (genotype) producing the signal,
638
not the plant itself (Strauss et al. 2002). It could have evolved by kin selection (Wilson 1987
639
%493) or between-plant signals could be an accidental result of within-plant signalling
640
(Karbon and Maron 2002).
641
3.9
642
Subvention conclusion
One of the categories above is mutualism, and examples are well known between
643
plants and heterotrophs, for example in mycorrhizae. However, we have been able to discover
644
any examples of demonstrated mutualisms between two embryophytes. Awk sentence We
645
also note that the list above contains no clear example of facilitation. This suggests that
646
subventions may be accidents of evolution. We would expect this anyway. Plants do not rise
647
to the top of the interaction league table by being nice to others. Probably facilitation during
648
succession is a combination of mechanisms, for example an N-fixing and litter-accumulating
649
pioneer that is shaded out by subsequent species.
650
4 Litter: the necessary product
651
As we described in chapter 1 (sect. 1.1) the fundamental pattern in the natural history
652
of plants is that growth comprises the production of modules. The functional lifespan of these
653
organs, such as leaves and translocatory (vascular) tissue, is programmed and curiously short.
654
New organs and tissue must be produced, and discard of the old ones results in the production
655
of litter. The organs are mainly shed when dead, but some material is lost to the living plant
656
through damage while it is still living. All types of plant organ are included in litter,
657
especially leaves but also twigs, coarse woody debris (CWD, i.e. branches and whole trees)
658
and reproductive parts. Litter from roots and underground stems is deposited below ground
659
but remains in position and there is little evidence of its mediating plant interactions. The
660
proportion of total litterfall that is from reproductive parts varies, e.g. 16-24% in an NZ
661
podocarp/angiosperm forest (Enright 1999), 23% in a Mediterranean shrubland (Arianoutsou
662
1989), versus a much smaller proportion in a tropical forest in India (Sundarapandian and
663
Swamy 1999).
Wilson & Agnew, chapter 2, Interactions, page 22 of 53
664
665
666
If litter breaks down more slowly than it is deposited and is not redistributed within
the area by wind, animals, etc., climatic and local regimes determine its ultimate fate:
 In a dry climate and/or on a dry substrate, litter can disappear by:
 burial in habitats on which material such as gravel (in braided river systems), sand
667
668
or loess is being deposited,
669
 transport in surface floodwater, carried into rivers,
670
 fire. Even in the desert decomposition eventually happens
671
The two former fates are allogenic and do not impact on the plant communities that
672
delivered the litter. However, fire does so and is discussed below.
673
 When the climate and substrate are moist enough, litter can become peat. We deal with
674
this below. What about the range of conditions between these 2 extremes which would
675
include the majority ecosystems on the planet?
676
Litter plays a major part in the functioning of most ecosystems. We start with a description of
677
litter production and then deal with its effect on its neighbours. Litter production is most often
678
examined in ecological studies for its rôle in nutrient cycling (e.g. Orians et al. 1996). Here,
679
we focus on its other impacts on plant communities.
680
4.1
681
Litter can be of three kinds: Seems unnecessarily simple for the intended audience
682

683
684
The timing and type of litter production
Standing dead litter is retained for some time on the plant, decaying. It comprises leaves
and stems in many herbs and grasses as well as branches and trunks from shrubs/trees.

Programmed litter shed via the physiological process of senescence and abscission.
685
Such litter is almost always produced in pulses at predictable seasons. It comprises
686
mainly leaves, reproductive parts and root hairs (Larcher 1980; Osborne 1989).
687

Stochastic litter is shed by an allogenic disturbance (i.e. accidental damage) or by
688
pathogenic dieback, not initiated by the plant. Some types are produced irregularly,
689
though others are seasonal.
690
These types may differ in the ability that selection has to lead to adaptations in both the litter-
691
producing species, and the species on which the litter falls.
692
Standing dead litter
693
Exemplifying the effects of this type of litter, Bergelson (1990) demonstrated in a field
694
experiment that the seedling emergence of the annuals Senecio vulgaris (groundsel) and
695
Capsella bursa-pastoris (shepherd’s purse) was very sparse where there was a high density of
696
dead Poa annua plants. Gleissman and Muller (1972) reported evidence that the dead fronds
Wilson & Agnew, chapter 2, Interactions, page 23 of 53
697
of at least some ecotypes of Pteridium aquilinum (bracken) have suppressive effects on
698
underlying vegetation. On the acid forest floor in the uplands of northern Britain the grass
699
Deschampsia flexuosa is often dominant, with the litter consisting largely of D. flexuosa
700
remains (Ovington 1953). Regeneration of Quercus petraea (sessile oak) can be almost absent
701
in a wood with a developed D. flexuosa leaf-and-litter mat, in comparison to good
702
regeneration in other, nearby woods (Scurfield 1953). In this case the litter is mostly of dead
703
D. flexuousa leaves still attached to the plant, and these leaves form a thatch over the grass
704
tufts, shedding the oak leaf litter should this read “shading the oak seedlings and decreasing
705
regeneration”? Other litter effects on these acid forest floors are described below. However,
706
little has been published on the importance of abscission versus retention of dead material in
707
the functional ecology of plant communities. In many perennial herbs the vegetative shoots
708
collapse in winter but the dead flowering stems remain erect. The latter may have effects such
709
as channelling rainfall or acting as bird perches, with consequent input of nutrients and
710
disseminules.
711
Programmed litter
712
In this type, the organ being shed is usually disconnected by abscission, the result of
713
physiological processes endogenous to the plant and initiated some time before actual litter
714
fall occurs. Programmed litter is almost always pulsed by season (e.g. Arianoutsou 1989;
715
Enright 1999), exceptions being tropical figs (Nason et al. 1998) and ruderals in oceanic
716
climates. There can be several peaks of programmed litterfall during the year, often of
717
different types of a species’ replaceable plant organs (leaves, twigs, flowers, fruit, etc.) all
718
with their special phenology. Reproductive litter is always programmed. In masting species it
719
can be pulsed by year (Buck-Sorlin and Bell 1998) though not necessarily in a simple way:
720
the latter workers found that copious shoot shedding correlated with masting the following
721
year. As well as being temporally patchy, reproductive litter is also spatially patchy, for
722
example in some New Zealand forests it is greater near trees of Agathis australis (kauri;
723
Enright 1999).
724
The fall of leaf litter and other organs of photosynthesis such as cladodes and
725
phyllodes enough vocab already. Use the appropriate words, but there are places (like here)
726
where “big” words seemed be used to show that they can be. What is wrong with the words
727
leaves and petioles. is a pulse in almost all forests whether dominated by deciduous or
728
evergreen species. The number and amplitude of pulses each year depend on the phenology of
729
the vegetation and its response to the environment. The pulse of falling leaves disturbs the
730
environment of the ground flora, and each species’ leaf litter has a characteristic pH, phenolic
Wilson & Agnew, chapter 2, Interactions, page 24 of 53
731
content, breakdown rate and pattern of fall, depending upon its chemistry, specific leaf area,
732
leaf size and geometry. The effects of a litter pulse can be to change light and humidity at the
733
soil surface or to start nutrient cycling.
734
Programmed litter is usually lightweight and therefore easily dispersed. Sometimes it
735
is redistributed by wind and rain into deep patches, having a great local effect (Fahnestock et
736
al. 2000). This means that its time of impact at a point does not necessarily coincide with the
737
time of it falls (this applies to lightweight stochastic litter too). It can also be redistributed by
738
animals (Theimer and Gehring 1999), for example bird scratching can remove the litter load
739
locally, and permit germination of surface seeds. Branch fall (= branch shedding = limbfall =
740
cladoptosis) is programmed in some species. The process has been well described (Millington
741
and Chaney 1973) but its potential wider evolutionary and synecological significance appears
742
to have been overlooked. It involves well-defined cleavage zones, for example with a cork
743
band produced from a phellogen, usually in twigs and small branches but also in large (e.g. up
744
to 6 cm in diameter) branches of several years of growth. Branch fall can be seasonal, usually
745
in autumn but in a few species in spring (Millington and Chaney 1973). The fall of heavy
746
litter such as palm leaves and the branches of some conifers (Agathis australis: W.R. Wilson
747
et al. 1998) can be programmed to occur at a particular season and there can be in
748
considerable amounts (e.g. c. 800 kg ha-1 yr-1: Christensen 1975; Buck-Sorlin and Bell 1998).
749
Stochastic litterfall
750
Stochastic litterfall is that which is not programmed. Rather, it is caused or triggered
751
by storm damage, droughts, floods, geomorphological change, gravitational overload,
752
herbivore destruction etc.
753
Stochastic litter can be dead or alive. It includes leaves: 68% in the upland forest
754
studied by Shure and Phillips (1987). However, the lignified plant parts (twigs and CWD) are
755
often prominent, e.g. 46% of the litter recorded in an Amazonian rain forest (Chambers et al.
756
2000). Wardle (1984), in evergreen Nothofagus in New Zealand, found that twig fall
757
comprised about 30% of the litter. It can be very sizable in total: Buck-Sorlin and Bell (1998)
758
recorded 37,000 plant fragments from one oak tree in a year; the shoots were generally short
759
shoots not older than two years. Chambers et al. (2000) recorded 3.6 tonnes ha-1 yr-1 of CWD
760
(>10 cm diameter) in an Amazonian rain forest. Amounts are somewhat less in more open
761
forests in drier areas, for example in the order of 1-2 tonnes ha-1 yr-1, mostly leaves, for two
762
Eucalyptus savannahs in Queensland, Australia (Grigg and Mulligan 1999). Trees are
763
continually shedding overtopped branches (Buck-Sorlin and Bell 1998). Broken dead trees
764
can also make a contribution, e.g. 7% in a boreal forest in Finland (Siitonen et al. 2000). In
Wilson & Agnew, chapter 2, Interactions, page 25 of 53
765
many climates, epiphytes add appreciably to the litter fall, being 5-10% in old tropical cloud
766
forest in Costa Rica, where epiphyte fall is temporally sporadic (Nadkarni and Matelson
767
1992), and c. 5 % in Picea abies (Norway spruce) old-growth forests in Sweden, consisting of
768
lichens (Esseen 1985).
Fig. 2.5: The seasonal pattern of litterfall in an oakwood. After Christensen (1975).
769
770
By definition stochastic litterfall occurs less predictably than programmed litter, especially in
771
the case of CWD which falls mostly during storms. However, stochastic litterfall can be
772
pulsed by phenology, falling especially at the end of the life of a modular organ. It can also be
773
pulsed by a pest epidemic or short-term weather conditions. Such pulses occur sporadically
774
between years (Harmon et al. 1986) but sometimes with seasonal peaks related to storm
775
frequency (Fig. 2.5; Gentry and Whitford 1982; Brokaw 1982; Buck-Sorlin and Bell 1998).
776
Wardle (1984) found that in NZ Nothofagus it was seasonal, though less consistently so than
777
leaf fall. The time of the peak differed between Nothofagus species and also between sites,
778
usually but not always coinciding with the peak of litter fall. In Nothofagus menziesii (silver
779
beech) there was a double peak. Both Nadkarni and Matelson (1992) and Esseen (1985) found
780
the epiphyte fall to occur mainly in storms. There is a gradation from seasonal events to those
781
separated by decades or centuries. Even programmed branch fall can be partly stochastic, i.e.
782
influenced by the environment, such as that resulting from dieback after drought-induced
783
cavitation (Rood et al. 2000).
784
785
786
Because it is less phased, stochastic litter is unlikely to disturb as much and certainly
not as predictably as programmed litter.
In boreal forests CWD is an important constituent of forest function, covering over 5%
787
of the forest floor (Zielonka and Niklasson 2001), the larger tree trunks taking up to a century
788
to decompose.
Wilson & Agnew, chapter 2, Interactions, page 26 of 53
789
790
4.2
Litter decomposition
The litter decomposition rate is obviously important because it sets the period during
791
which litter can have a mechanical and chemical effect, as well as driving nutrient cycling
792
(sect. 3.13 below). Decomposition depends on moisture, temperature, and the litter’s nutrient
793
and phenolic content. These are influenced by climate, soils and the identity of the littering
794
species. On a global scale climate affects decomposition rates more than do the characteristics
795
of the litter, with the fastest decomposition in warm, wet climates (Meentemeyer 1978), but
796
on a local scale litter nutrient and polyphenol content, and to some extent morphology, control
797
breakdown rates in conjunction with the water regime in each habitat (Osono and Takeda
798
2004). For example, the frequent occurrence of tannin-rich litter in heavily leached soils is
799
correlated with an increase in its polyphenol content which controls the release of nitrogen, so
800
important for decomposers (Northup et al. 1995). Further, Moorhead et al. (1998)
801
experimented with mycorrhizal nutrition in grassland of Bouteloua gracilis (grama grass) /
802
Schizachyrium scoparium (bluestem), and interestingly concluded that this community could
803
retard litter decay by reducing decomposer action in a nutrient-limited soil, since the grasses
804
could outcompete the decomposers for scarce nutrients.
805
Litter is broken down by a succession of microbial communities, involving
806
invertebrate shredders, commutators, fungi and mycotrophs, and bacteria (Cadisch and Giller
807
1997). If the litter is large and woody the process involves macrofauna. However, the
808
suberised exfoliating bark of Eucalyptus spp. trees in Australia is slow to break down, and
809
often needs destruction by fire (Canhoto and Graca 1999). Breakdown rates differ between
810
species and taxonomic groups, for example Cornelissen (1996) found within British regional
811
flora a rough correlation between “evolutionary advancement” and leaf decomposition rate,
812
But the slow breakdown of grasses (Poaceae) was anomalous, explained by their low base
813
status compared with the dicotyledons (except the Ericaceae) from that region. However, in
814
the study of Preston and Trofymow (2000) comparing species within one vegetation type
815
rather than an entire flora, grass litter decomposed the fastest and Fagus grandifolia
816
(American beech) the slowest. The rate is undoubtedly correlated with cellulose:lignin ratios
817
and mechanical characteristics of the leaves (Cornelissen and Thompson 1997).
818
There is some evidence that leaf litter combined from several species tend to
819
decompose faster than single-species litter (McTiernan et al. 1997; Wardle et al. 2002 %585),
820
reducing litter residence times and hence the disturbing effect of litter. Gartner and Cardon
821
(2004), reviewing the literature, found that enhanced decomposition in mixtures has been
822
found in 47% of cases reported. For example, Kaneko and Salamanca (1999) found that in
823
litter bags of species collected from a Quercus serrata (oak) / Pinus densiflora (red pine)
Wilson & Agnew, chapter 2, Interactions, page 27 of 53
824
forest in Japan, mixtures containing Sasa densiflora lost weight faster than expected from the
825
decomposition rate of their components. They suggested the effect may operate via the faunal
826
commutators. However, Wardle et al. (2006 %1052) conclude that effects of litter mixing on
827
decomposition and on fauna are not related. Perhaps this synergy holds only for certain types
828
of litter: Hoorens et al. (2002) suggested that the effect was due to the high N content of some
829
species which would speed the decomposition of their lower-N associates. However, they
830
found that while broad-leaved herb litter mixes (of legumes) decayed faster, there was no
831
effect when Sphagnum recurvum (=S. fallax) was mixed with Carex rostrata (beaked sedge).
832
4.3
833
Effects of litter
Litter must have a chemical effect as well as its physical one. In the case of CWD, the
834
physical effect overwhelms the chemical, but finer reproductive parts may have mainly a
835
chemical effect. Decomposition and leaching are both central to the nutrient cycling regime in
836
the plant community. Litter fall can affect community succession, facilitating it or redirecting
837
it. Deep persistent leaf litter can inhibit the invasion of later-successional species (Crawley
838
1997). In many communities, an increase in nutrient supply leads to dominance by a few fast-
839
growing tall species, and lower species richness (Willems et al. 1993). This has usually been
840
seen as due to competition, but it could equally well be due to the effect of litter (Berendse
841
1999). Litter can have differential effects on particular species and thus on their populations
842
within a plant community. Documentation has been particularly thorough in the case of leaf
843
litter (Table 1). For some of the effects listed in Table 1, opposite effects are seen in different
844
situations, depending on the depth of the litter, the affected species and the growth medium
845
(Hamrick and Lee 1987; Nilsson et al. 1999; Facelli et al. 1999). The effects of litter can be
846
classified as:
847
1. Direct mechanical effects
848
a. physical damage,
849
b. alteration in environment.
850
2. Chemical effects
851
a. leachates from litter,
852
c. control of nutrient cycling.
853
3. Complex environmental interactions
854
a. peat formation,
855
b. litter-herbivore interactions (sect. 6.5 below),
856
c. litter-fire interactions (sect. 6.5 below),
857
d. higher order interactions (sect. 6.5 below).
Wilson & Agnew, chapter 2, Interactions, page 28 of 53
858
All of these depend on the characteristics of the litter material and its phenology of production
859
as described above. In addition many of them require the litter to decompose slowly enough
860
to maintain a constant presence in the A0 top soil layer.
861
4.4
862
The direct mechanical effect of litter
The physical impact of litter, particularly on the forest floor, is very conspicuous, and
863
we discuss it below (sect. 5.4 below) as an autogenic disturbance.
864
4.5
865
Alteration in environment by litter
Litter also causes general environmental changes at the soil surface. Plant growth,
866
especially of herbaceous plants, must be suppressed by the low light under litter, but we have
867
not found any study on this. Red/far red (R/FR) ratios are reduced by a live canopy, then
868
sometimes by half again by the litter. This can suppress germination (Vazquez-Yanes et al.
869
1990) or increase it (Fowler 1986 %131). Litter might intercept and shortly evaporate rain,
870
reducing soil water content (Myers and Talsma 1992), but it can also reduce evaporation from
871
the soil itself (Eckstein and Donath 2005). The temperature regime at the soil surface can also
872
be affected (Fowler 1986 %131).
873
Whenever species of stiff, erect form, such as the grass Holcus mollis and Vaccinium
874
myrtillus, trap and accumulate tree leaves (e.g. of Quercus spp., oaks; or Fagus sylvatica,
875
beech), other plants including Deschampsia flexuosa are killed, as demonstrated by dead D.
876
flexuosa seen below such litter (Watt 1931; Ovington 1953). Watt (op. cit.) mimicked this by
877
laying a layer of beech leaves 5 cm thick; the D. flexuosa was killed. Watt suggested this
878
could not be due to allelopathy, because where taller D. flexuosa leaves occasionally projected
879
above the litter layer they grew well, and moreover Holcus mollis growth was much improved
880
by similar treatment. This can allow H. mollis to invade areas that had been dominated by D.
881
flexuosa (Ovington 1953; Scurfield 1953). No litter is built up by H. mollis, as its dead organs
882
rot too fast (Ovington 1953), so Quercus can establish in the tree litter, or amongst H. mollis,
883
once the D. flexuosa litter mat is removed (Watt 1931; Ovington 1953). Chapin et al. (1994)
884
suggest that in Glacier Bay successions Alnus sinuata (alder) suppresses Dryas drummondii
885
partly by the allelopathic effects of its litter, but as part of complex replacement interactions.
886
In forests in the mid west USA (Michigan and Wisconsin), hardwoods (e.g. Quercus rubra,
887
red oak) can dominate the mid-successional forest. In these stands, Tsuga canadensis
888
(hemlock) cannot invade, because its seedlings are unable to penetrate the hardwood litter,
889
whereas Acer saccharum (sugar maple) seedlings can, and it therefore invades (Rejmanek
890
1999).
Wilson & Agnew, chapter 2, Interactions, page 29 of 53
891
Subvention via litter can be very significant for particular species and, in some
892
temperate rain forests the seedlings of many trees depend on fallen trunks and CWD for their
893
establishment and hence regeneration (McKee et al. 1982; Agnew et al. 1993; Duncan 1993).
894
CWD has a characteristic development in old growth stands, and harbours a specialized, often
895
endangered, invertebrate fauna and bryophyte flora. Bryophytes are particularly vulnerable to
896
litter cover (Barkman et al. 1977; Oechel and Van Cleve 1986), especially in forest, where
897
litter is deposited by the herbaceous field layer as well as by woody vegetation. However,
898
During and Willems (1986) named five bryophyte species that they suggested “may thrive on
899
litter”. One possibility is that nutrients released from litter is taken up by bryophytes (Tamm
900
1964). In Scandanavian forests many species are dependent CWD for regeneration or growth,
901
including many bryophytes (Siitonen 2001).
902
4.6
903
Leachates from litter
It has been long suspected that leachates from litter affected germination and growth
904
of certain plant species. Early reports of this were concerned with crop residues (Kimber
905
1973) but then evidence came from natural plant assemblages. The case of the tree Celtis
906
laevigata (sugarberry) is the clearest (Turner and Rice 1975; Lodhi 1978). Bosy and Reader
907
(1995) investigated suppression of germination of four forbs by grass litter in an oldfield.
908
Germination of seeds of at least three of the species was markedly reduced under litter, and
909
for two species an appreciable component of the suppression could be explained by the
910
inhibitory effect of leachate. However, it is also possible for litter to subvent germination
911
(Xiong and Nilsson 1999), or to act as part of a cue for germination from the seed bank
912
(Preston and Baldwin 1999).
913
Allelopathy was discussed above. The allelopathic effect of litter leachates has long
914
been suspected and repeatedly tested. For example, Rutherford and Powrie (1993) showed
915
that leaf and litter leachates from the Australian Acacia cyclops (coastal wattle) affected the
916
small-leaved shrub Anthospermum spathulatum below it. Apparently leachates from both the
917
canopy and litter are implicated in many allelopathic effects. However, experiments are easier
918
in vitro than in the field, and only a few clearly demonstrate that litter allelopathic agents have
919
real effects in nature.
920
4.7
921
Control of nutrient cycling
Litter returns nutrients to the soil as mineral compounds or as organic compounds
922
which are then broken down to mineral ones. This is the well-known process of nutrient
923
cycling, but different litter types will differ. Berendse (1994a) found that in fast-growing
Wilson & Agnew, chapter 2, Interactions, page 30 of 53
924
species (i.e. with high RGRmax) less N was re-translocated to the living parts before the leaf
925
fell, and the resulting litter broke down quickly. Such species would be expected to
926
predominate in N-rich environments. In contrast, species with a low RGRmax re-translocated a
927
greater proportion of their leaf N before it fell. Such N-conserving species, with a low carbon
928
turnover, would be expected early in primary succession, when N is in short supply.
929
Berendse et al. (1987) later compared the deciduous Molinia caerulea (purple moor
930
grass) with the evergreen microphyllous woody shrub Erica tetralix (heath). M. caerulea lost,
931
during one year, 63% of the N present in the above-ground biomass standing at the end of the
932
growing season and 34% of its P. Comparable losses in E. tetralix were 27% and 31%,
933
respectively. This suggests that under nutrient-poor conditions the low-nutrient-loss E. tetralix
934
will be the dominant species, and that if nutrient availability increases M. caerulea will
935
replace it. There is some empirical support for this: in a similar system, Berendse et al.
936
(1994b) found that addition of nutrient solution caused Calluna vulgaris (a species
937
ecologically similar to Erica tetralix) to decline and cover of four grass species to increase.
938
The litterbag decomposition rates given for various species by Cornelisson et al. (1999) make
939
it clear that plants of later successional stages will have litter that is slower to decompose and
940
thus with a greater potential disturbance effect. These authors report from a wide ranging
941
survey an almost universal negative correlation between decomposition rate and herbivore
942
defence.
943
4.8
944
Peat formation
On wet substrates, if litter breaks down at a slower rate than it is produced peat will
945
build up. Peat is composed of plant remains in various stages of humification by a partial
946
organic hydrolysis of plant material mediated by micro-organisms (Fig. 2.6). Some types of
947
litter especially impede drainage to cause waterlogging. This yields humic colloids with
948
properties that restrict drainage and oxygenation and, being complex molecules bounded by
949
weakly acidic OH radicals, lower the pH of the soil solution. Nutrient availability and
950
oxygenation are reduced, which decrease litter production but decrease its decomposition
951
even more, so that peat accumulation increases yet more.
952
953
954
Wilson & Agnew, chapter 2, Interactions, page 31 of 53
955
956
957
958
959
960
961
962
963
964
965
966
967
968
969
970
971
972
973
974
975
976
977
978
979
980
981
982
983
984
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
= Empodisma paths
= the main switch feedback cycle
Fig. 2.7. The process of peat accumulation in mires dominated by Empodisma (wire rush)
985
or Sphagnum moss species.
986
There are three routes to peat formation. In eutrophic or mesotrophic conditions litter
987
production is high but decomposition is fast too, so peat will form only in still lakes, infilling
988
them. This is a classic succession story (Walker 1970). Paludification often follows from this
989
point. Peat can also form on the wet, nutrient-poor soils often caused by the leaching effect of
990
high rainfall (Crawford 2000), a process known as paludification. There are two ways in
991
which paludification can happen. Firstly, the species adapted to these conditions often bear
992
leaves with a high polyphenol content, which slows decomposition and thus potential for
993
paludification (Inderjit and Mallik 1997; Northup et al. 1998). This is a widespread
994
phenomenon, having important effects on community structure. For example Ehrenfeld et al.
Wilson & Agnew, chapter 2, Interactions, page 32 of 53
995
(1995) propose that small ericaceous shrubs trap litter in New Jersey pine savannahs,
996
inhibiting decomposition and maintaining openings in the canopy, while Inderjit and Mallik
997
(1997) provide experimental evidence for litter of Ledum groenlandicum (Labrador tea)
998
limiting black spruce regeneration in Canada.
999
The ultimate peat-forming process is the formation of an ombrogenous bog by
1000
isolation of the peat surface from its surroundings in water and nutrient supply (Klinger 1996,
1001
Anderson et al. 2003). This is effected by a guild of species which can absorb nutrients
1002
directly from rainfall, mostly bryophytes and particularly Sphagnum spp. and the restiad
1003
Empodisma minus (wire rush, Agnew et al. 1993), an odd flowering plant which has the same
1004
effect though its negatively geotropic root weft. This guild has, in common, cell walls with a
1005
cellulose-derived weak acid (uronic) that can scavenge ions from precipitation, yielding
1006
sufficient nutrients for annual growth and maintaining a high hydrogen ion concentration in
1007
the interstitial water. The effect is very well documented for Sphagnum spp. in temperate
1008
mires (Clymo 1963; Clymo and Hayward 1982; Koojiman and Bakker 1994). The rate of
1009
percolation, as seen in Darcy’s constant, is slowed by the peat formed. The waterlogging, low
1010
pH and low-nutrient conditions favour this guild. Malmer et al. (1994; 2003) suggest that since
1011
Sphagnum spp. can outcompete vascular plants under ombrotrophic conditions these
1012
conditions may arise rather suddenly. This is the state change expected when a switch is
1013
operating (chapt. 3, sect. 5 below). There are indeed records of such rapid state changes where
1014
Sphagnum spp. expansion has caused a brown moss fen to be replaced by bog (Kuhry et al.
1015
1993), destroyed forest (Anderson et al. 2003) and invaded forest around the edges of basin
1016
mires (Klinger 1996). The process may be initiated by climatic change to colder, wetter
1017
conditions (Korhola 1996).
1018
4.9
1019
Can reaction via litter evolve?
It is not enough to describe the processes that occur within plant communities; we
1020
should gauge whether these processes are accidental, or whether they could be the result of
1021
evolution. This is hardly in doubt for the other types of interaction discussed in this chapter –
1022
interference, subvention and autogenic disturbance—wasn’t it in question just a little before?
1023
– because the characters of the plant involved affect its fitness and hence the transmission of
1024
its genes to the next generation. The problem with litter is that it is by definition deceased
1025
plant tissue. As Clements (1904) pointed out, all plants react on their environment, but the
1026
extent and type of reaction will be genetically controlled. A particular reaction will evolve if it
1027
enhances the fitness of the individual plant (i.e. genet) more than it enhances the fitness of its
1028
conspecific neighbours, after taking into account any cost of reaction. However, litter affects
Wilson & Agnew, chapter 2, Interactions, page 33 of 53
1029
all the individuals and species in a community. In some cases it is produced when the whole
1030
plant dies, so the characters are expressed too late to affect whether the genes that caused
1031
them will increase or decrease. This is clearest in cases when the litter is produced when the
1032
plant dies or has its effect after the plant’s death, for example by paludification, by control of
1033
nutrient cycling, and as fuel for fire. There is then no possibility of plants enhancing their own
1034
fitness, in survival or fecundity, only that of their offspring (which will carry their genes. I
1035
don’t see why evolution can’t therefore act on litter).
1036
For effects that occur after the death of the plant we need to call on kin selection, with
1037
the mechanism that a plant benefits especially its neighbours, which are especially likely to
1038
carry the same alleles (Wilson 1987 %493). Another way of expressing this is selection
1039
through the extended phenotype. Northrup et al. (1998) commented that “decomposing leaf
1040
litter is not generally considered to be part of the plant’s phenotype” so that litter characters
1041
must evolve through selection on the extended phenotype. It has been remarked that just as
1042
selection in different areas with comparable environments but different species often produces
1043
similar solutions in terms of leaf characters, so similar solution in terms of reaction on the
1044
environment would be expected in different species and communities (Lewontin 1985;
1045
Mooney et al. 1977). The concept is that this reaction can lead to the evolution of secondary
1046
characters if an organism modifies its own environment, and the same induced environmental
1047
change is reimposed for sufficient generations to serve as a significant source of selection
1048
(Olding-Smee et al. 1996; Laland et al. 1996 1999)-community selection?. A different
1049
solution was proposed by Whitham et al. (2003), that traits of the extended phenotype could
1050
evolve because they affect the whole community and there could be selection between
1051
communities, a concept that most biologists find hard to swallow (but see D.S. Wilson 1997).
1052
However, most plants produce litter during their life and have an opportunity for that litter to
1053
affect their fitness, in which case Northup et al.’s argument does not apply. Still, there are
1054
problems with the idea that reaction via litter can evolve; litter effects seem to be a necessary
1055
by-product of growth.
1056
5 Autogenic disturbance: plants as disturbers
1057
Disturbances, marked changes in the environment for a limited period, often with the
1058
removal of plant material, are more common than was once believed and important for plant
1059
communities (White 1979; Rundel 1998; Grime 2001). The concept ‘autogenic disturbance’
1060
was coined by Attiwill (1994), though it is close to the ‘endogenous disturbance’ of White
1061
(1979). Most consideration has been of allogenic disturbance, i.e. that caused by external
1062
factors such as animals or extreme weather events. For example, Bazzaz (1983) describes
Wilson & Agnew, chapter 2, Interactions, page 34 of 53
1063
disturbance as continuous and necessary in all ecosystems, but discusses only allogenic
1064
causes. No less important, we suggest, are the minor disturbances within the community that
1065
inevitably result from the growth and death of plant parts, for example by plant contact and by
1066
litter (there seems little opportunity for autogenic disturbance by subterranean organs). Thus,
1067
vegetation, by its nature, disturbs itself. As we pointed out in chapter 1: “Plants move,
1068
animals don’t”. Autogenic disturbance has potentially positive and negative effects on
1069
population fitness and density, yet stands apart from the general considerations of interference
1070
and subvention described above. There is a wide range in the intensity of autogenic
1071
disturbances, from delicate adjustments resulting from leaf growth to the fall of a group of
1072
trees, but plants must tolerate all these effects. It may have profound bearing on vegetation
1073
dynamics. Autogenic disturbance may be more predictable than allogenic disturbances such
1074
as storms and earthquakes perhaps they are more predictable on a day to day basis, but over
1075
the course of an organism’s life, the probability of experiencing many allogenic disturbances
1076
is very predictable. I might not know whether or not I’m going to be hit be a storm tomorrow,
1077
but I do know that I will be hit by a storm in the course of my life. As the damage sustained
1078
by a storm or other allogenic dist can be much more severe shouldn’t all this (when combined
1079
with the plasticity issue commented on below) lead to a high level of selection on allogenic
1080
dist. related traits?, and if so selection for adaptation to it is more likely to occur. If plants can
1081
respond with plasticity to autogenic disturbance (as you suggest below) but not with allogenic
1082
disturbances, wouldn’t selective pressure be greater on allogenic dist. adaptations? However,
1083
autogenic and allogenic disturbance can interact.
1084
5.1
1085
Movement and contact
Even gentle contact between plants can affect their growth, producing effects such as
1086
reduced growth, reduced soluble carbohydrates and increased transpiration (van Gardingen
1087
and Grace 1991; Keller and Steffen 1995). For example, when Biddington and Dearman
1088
(1985) brushed Brassica oleracea var. botrytis (cauliflower) and Apium graveolens (celery)
1089
seedlings with typing paper for 1.5 min day-1 it reduced their shoot dry weight (Fig. 2.7).
Wilson & Agnew, chapter 2, Interactions, page 35 of 53
Control
Brushed
Fig. 2.5: The effect of brushing seedlings of Brassica oleracea for 1.5 min
day-1After Biddington and Dearman (1985).
1090
1091
Experimentally shaking the plant can have an even greater effect, e.g. reduced shoot
1092
extension, shorter and wider stems, lower shoot:root ratios, altered root development, shorter
1093
petioles, shorter flowering culms and reduced reproductive effort (Neel and Harris 1971;
1094
Braam and Davis 1990; Gartner 1994; Niklas 1998; Goodman and Ennos 1998). Whilst
1095
brushing with typing paper and shaking by hand are artificial treatments, they are very close
1096
to the leaves of adjacent plants brushing each other, or close trees rocking each other. The
1097
changes are mediated by the up-regulation of a large number of genes (Braam and Davis
1098
1990). Plants can also change position as a result of their own growth (Evans and Barkham
1099
1992), for example Salix (willow) trunks collapse due to their own weight in wet carr forest
1100
(Agnew, pers. obs), and shrub stems can be bent by their own weight and fall to the ground
1101
(B.F. Wilson 1997).
1102
5.2
1103
Growth thrust
Shoots can thrust each other aside physically as they grow (Campbell et al. 1992). For
1104
example, the leaves of Juncus squarrosus are vertical when they first emerge, but they then
1105
become horizontal, form a rosette and press down surrounding plants (authors pers. obs.) as
1106
do leaves of Plantago species (Campbell et al. 1992). Surprisingly little is known of this
1107
process.
1108
Secondary growth of tree trunks, branches and roots continually creates new habitat,
1109
initiating succession by providing opportunities for colonisation. Circumferential branch
1110
growth produces new sites for the establishment of epiphytes. Some bryophyte species are
1111
tree-base specialists (Ashton and McCrae 1970). Their specialisation is perhaps explicable by
1112
their greater shade tolerance (Hosokawa and Odani 1957) and the peculiar characteristics of
1113
trunk water flow creating a damper, more nutrient-rich environment, but this is also the zone
1114
where the fastest circumferential growth occurs. Circumferential growth of tree roots can
Wilson & Agnew, chapter 2, Interactions, page 36 of 53
1115
affect the environment above the surface: woody roots near the soil surface create shallow
1116
soils and diversify the forest floor habitat (Agnew pers. obs.). The reader may like to take the
1117
‘pers. obs’ in this section as confirmation that autogenic disturbance has not received due
1118
attention in ecological research.
1119
5.3
Crown shyness
1120
Crown shyness comprises gaps between the canopies of adjacent trees (Jacobs 1955),
1121
probably caused by abrasion in the canopy (Putz et al. 1984 %24). Franco (1986) observed
1122
the process, reporting that when branches of Picea sitchensis (Sitka spruce) and Larix
1123
kaempferi (Japanese larch) met physical damage occurred by abrasion, causing the death of
1124
the leading shoots. New shoots arising from lateral buds and were also killed. Sounds like
1125
competition for space to meLong and Smith (1992) demonstrated the mechanism by fixing
1126
wooden pickets into the canopy as artificial branches: they were broken back to the edge of
1127
the crown, due to wind-rock and consequential abrasion. Tall slender trees were subject to
1128
greater wind-rock, and thus greater frequency of impact with neighbouring crowns, leading to
1129
greater crown shyness. Putz et al. (1984 %24) measured swaying of Avicenna germinans
1130
(mangrove) and found that branches bordering crown shyness gaps generally had broken
1131
twigs and few leaves. Flexible crowns were more widely spaced than still crowns, confirming
1132
the observation of Long and Smith (op. cit.). These effects are the result of the compulsory
1133
growth and movement imposed by the modular construction of plants (chapt. 1, sect. 1.1
1134
above).
1135
5.4
1136
Growth and gravity
CWD clearly has the potential to be very destructive on the forest floor. The most
1137
destructive type of stochastic litter is tree fall, which is the autogenic disturbance par
1138
excellance and implicated in all demographic processes in forests of mixed canopy species. It
1139
appears to be a normal, predictable event in many undisturbed stands, which can be measured
1140
and built into models of species and biomass turnover in boreal (e.g. Hofgaard 1993), tropical
1141
evergreen (e.g. Chandrashekara and Ramakrishnan 1994) and tropical rain forests (e.g.
1142
Kellman and Tackaberry 1993).
1143
The weight in a tree’s canopy can eventually result in its fall, obviously disturbing
1144
surrounding plants. In a forest the upper canopy trees are more likely to fall, having reached
1145
their greatest potential and being too heavy for their root support or too loaded with
1146
lianas/epiphytes (Strong 1977; Putz 1995). Tree fall is associated with storm damage,
1147
particularly in mid-latitudes (e.g. Busing 1996, Allen et al. 1997). Understorey trees are more
Wilson & Agnew, chapter 2, Interactions, page 37 of 53
1148
likely to become standing dead, since pathogens or light reduction by neighbours (self-
1149
thinning) can kill, whether or not the tree still has the potential to grow further, and they are
1150
not as exposed to storm damage as are the canopy species. An exception occurs in the dry
1151
Kysna (South Africa) forest, where most canopy trees die in situ due to “competition,
1152
senescence and secondary pathogens” and gradually break up (Midgley et al. 1995). There is
1153
not enough evidence to suggest this as a general feature of any forest types.
1154
In old-growth forest, tree fall is the usual process that forms canopy gaps. In gap
1155
formation, several sudden environmental changes take place. The most important is that the
1156
forest floor is brightly lit with light of a very different spectral quality. The effects of a gap
1157
are not all positive: Lovelock et al. (1998) found photoinhibition of shade-tolerant juveniles in
1158
gaps, especially in species with short-lived leaves. Another, often overlooked, factor is
1159
rainfall/hydrology. A full canopied forest evaporates up to 40% of incoming rainfall and the
1160
soil is seldom at field capacity, but gaps receive the rain uninterrupted. There is also soil
1161
disturbance, with soil exposed in a root pit and adjacent root plate mound. The bare soil and
1162
higher light allow secondary species to invade, as observed by Ellison et al. (1993) in
1163
neotropical forest, and Narukawa and Yamamoto (2001) for Abies spp. (fir) seedlings in
1164
boreal and subalpine Japan.
1165
Branches can also cause severe impact when they fall (sect. 3.9 above). For example,
1166
in the tropical liana Connarus turczaninowii in Panama, 20-45% of the mortality of young
1167
plants is caused by branch fall (Aide 1987); in a tropical rain forest in Amazonia, Uhl (1982)
1168
found the most common (38%) cause of death in small (1-10 cm dbh) trees to be a branch fall
1169
or treefall; in Costa Rican rain forest, Vandermeer (1977) found that 46% of seedling deaths
1170
were due to falling leaves or branches, about half of these were due to falling palm fronds.
1171
Gillman and Ogden (2001 %671) found in Podocarp/angiosperm forest in northern North
1172
Island, NZ, that 10-20 % of the annual seedling mortality was caused by litterfall.
1173
5.5
1174
Lianas
Lianas can be so abundant in the canopy of many tropical and sub-tropical forests that
1175
they compete with the emergent trees (Lowe and Walker 1977). Treefall, with its associated
1176
disturbance to the forest floor, can be generated by either adherent lianas (e.g. Hedera helix,
1177
ivy) or free-swinging lianas (e.g. Ripogonum scandens, supplejack). Phillips et al. (2005
1178
%1250) found that in an upper-Amazon tropical rain forest large trees were three times as
1179
likely to die if they were invested by lianas. The resulting canopy gap can also benefit lianas.
1180
Needing less investment in support they can extend fast and keep pace with the fast-growing
1181
secondary species filling the gap.
Wilson & Agnew, chapter 2, Interactions, page 38 of 53
1182
Twining or tendril lianas can constrict the host stem (Lutz 1943; Clark and Clark
1183
1991; Matista and Silk 1997). Usually there is little active strangulation, but the liana stays
1184
put and the tree grows, which can produce deformations in the trunk and lead to changes in
1185
the vascular tissue and the wood fibres ((Falconer 1986; Reuschel et al. 1988; Putz 1991).
1186
Sometimes new conducting tissue is formed parallel to the constriction, but constriction can
1187
inhibit or even stop downward translocation of organic solutes (Lutz 1943; Putz 1991,
1188
Hegarty 1991). The constriction can also be a point of weakness, at which a branch or young
1189
stem is more likely to break (Lutz 1943; Uhl 1982; Putz 1991). Deformed trees are also more
1190
susceptible to pathogens (Putz 1991). Not infrequently the tree dies (Lutz 1943; Clark and
1191
Clark 1991; Uhl 1982).
1192
In the tropics, epiphytes, lianas and trees are often not distinct categories. Many
1193
genera in the Araceae (Monsteroideae) start as lianas but can maintain themselves as
1194
epiphytes without contact with the forest floor. We have found no record of an epiphyte being
1195
associated with tree or branch fall, although their contribution to litter fall has been well
1196
documented (see above). Strangler epiphytes certainly damage trees (Richards 1996). The
1197
epiphyte species involved are evergreen; many are in the genus Ficus (fig) and curiously
1198
revered by the indigenous people (F. benghalensis in Hindustan, F. natalensis in Kenya).
1199
Such stranglers begin life as epiphytes, gradually extend aerial roots downwards, eventually
1200
root in the soil, then grow around their host as a tree. The host usually dies, and does so
1201
standing, though the cause of the host’s death is not clear (Richards 1996).
1202
The interactions between support and liana are complex. Lianas are often supported by
1203
more than one tree (with a record of 27 trees for one liana on Barro Colorado Island, Panama:
1204
Putz 1984 %1713). This causes interdependence between trees that may stabilise canopy trees
1205
adjacent to treefalls (Putz 1984 %1713; Hegarty 1991). However, a corollary is that if such a
1206
connected tree falls, it damages more trees. For example, Putz (1984 %1713) found on Barro
1207
Colorado Island that 2.3 trees fell with each gapmaker, often ones that shared lianas. Liana-
1208
laden trees can also pull branches off neighbouring trees as they fall (Appanah and Putz
1209
1984).
1210
6 Plant-plant interactions mediated by other trophic levels
1211
While a macrophyte remains sedentaryi, its environment is changing, especially with
1212
respect to the various sets of organisms utilising the carbon energy source that it represents.
1213
These include herbivores, parasites and pathogens, all capable of modifying a plant’s fitness
1214
and therefore its competitive ability. There is also the potential for various combinations of
1215
heterotrophs and neighbouring plants to build complex nexus of inter-relationships. In most
Wilson & Agnew, chapter 2, Interactions, page 39 of 53
1216
cases these interactions are associated with a "patch effect", which works only if one species
1217
is sufficiently abundant in a local vegetation patch to change the behaviour of the herbivore or
1218
pollinator.
1219
6.1
1220
Below-ground benefaction
It is generally assumed that species with root nodules that contain nitrogen-fixing
1221
micro-organisms enhance the nitrogen economy of associated non-nodulating plants. These
1222
N-fixing plants are therefore held to be important in ecosystems and particularly in rangelands
1223
(Paschke 1997). However likely the transfer is, it is rarely proven. Kohls et al. (2003) set out
1224
to investigate this link in the well-studied site of Glacier Bay, Alaska. Using Δ15N values they
1225
concluded that nodulated plants accounted for most of the fixed N in soils and plants for up to
1226
40 years of succession; most of this being donated to the ecosystem by Alnus viridis (green
1227
alder). The assumption that fixed nitrogen is indirectly passed from nodulated to un-nodulated
1228
plants is probably justified in many cases.
1229
Common mycorrhizal networks (CMNs) link individuals below ground so that
1230
nutrient and carbon transfers have the potential to enhance or depress plant growth. In all
1231
three major types of mycorrhiza – vesicular-arbuscular, ectotrophic and ericoid/epacrid –
1232
some of the fungal species involved can infect more than one plant species (Simard and
1233
Durall 2004). The vesicular-arbuscular and ectotrophic ones are known to establish fungal
1234
networks that connect the roots of different species, and this may be true for the
1235
ericoid/epacrid type too (Cairney and Ashford 2002). It has been suggested that CMNs affect
1236
the performance of plants (e.g. Booth 2004). However, it is unclear whether plant-tissue to
1237
plant-tissue transfer of carbon actually occurs (Simard and Durall 2004). There has never
1238
been a convincing demonstration of it, certainly not to a degree sufficient to benefit the plant.
1239
In cases where carbon has been traced by radioactivity to the recipient it is likely that it is
1240
retained in the fungal hyphae, not in the plant tissues (Robinson and Fitter 1999).
1241
Similar transfers could operate in mineral nutrients. However, Newman and Ritz
1242
(1986) and Newman and Eason (1993) carefully monitored the transfer of 32P and concluded
1243
that any direct transfer via hyphal links was very minor, and too slow to substantially
1244
influence the nutrient status of the plants. There is evidence for greater nitrogen transfer when
1245
mycorrhizae are present but it is not clear whether the transfer is through the CMN or whether
1246
the mycelia increase release of N from one plant into the soil and/or uptake by the other plant.
1247
Moreover, ideas that this would even out concentrations between plants do not stand up: He et
1248
al. (2005 %897) found that there was net transfer from Eucalyptus maculata (gum) to
1249
Casuarina cunninghamiana (sheoke). This represents transfer from a plant that is not N-
Wilson & Agnew, chapter 2, Interactions, page 40 of 53
1250
fixing, to one that is N-fixing and had close to double the N concentration in its tissues. This
1251
transfer was at very low rates, but the benefaction was in the opposite direction from that
1252
usually assumed between fixing and non-fixing plants.
1253
Roots and microbial activity in the soil are intimately linked, since roots provide the
1254
most of the carbon source below ground. Chen et al. (2004) used microcosms to show that
1255
Pinus radiata roots increased microbial activity and the mineralisation of organic P. There
1256
was evidence that root exudates were responsible for these effects. It is possible that the plant
1257
can obtain N from free-living N-fixing bacteria in the same way. That these effects are species
1258
specific was demonstrated by Innes et al. (2004), who found that the grasses Holcus lanatus
1259
(Yorkshire fog) and Anthoxanthum odoratum (sweet vernal) could stimulate microbial
1260
activity, whereas dicotyledonous forbs depressed it. The effect was only seen in soil of higher
1261
fertility.
1262
6.2
1263
Pollination
When fruit set is limited by pollen, plants of the same or different species can interfere
1264
with each others’ reproduction by competing for the service of pollinating animals (Grabas
1265
and Laverty 1999). When pollen from another species lands on a stigma it may interfere with
1266
the germination or fertilisation of the species own pollen by occlusion or allelopathy (Murphy
1267
and Aarssen 1995a). This can reduce seed set and increase self-fertilisation (Bell et al. 2005).
1268
Plants can also compete for animal dispersers (Wheelwright 1985).
1269
There can be subvention too if one species attracts pollinators to the vicinity of
1270
another by being more attractive (a ‘magnet species’) or by mimicry (Laverty 1992). Moeller
1271
(2004) found that among Clarkia xantiana (an annual in the Onagraceae) populations in
1272
California there were more pollinating bees and less pollination limitation in populations with
1273
a greater number of congeners, implying that the mass of plants of the same pollination type
1274
attracted pollinators. An interaction that we can count as a genuine mutualism between
1275
embryophytes was demonstrated by Waser and Real (1979). If species have staggered
1276
flowering times with shared pollinators and some overlap in flowering time, there will
1277
probably be some competition for pollinators. However, the continuous availability of flower
1278
rewards over the period may maintain pollinator populations. Waser and Real gave evidence
1279
from flower numbers, fecundities and pollinating hummingbird numbers across four years at a
1280
site in the Rocky Mountains, Colorado, that the earlier-flowering Delphinium nelsonii was
1281
benefiting the later-flowering Ipomopsis aggregata thus. If we consider the maintenance of
1282
hummingbird populations from one year to the next, I. aggregata could be benefiting D.
1283
nelsonii in a similar way, forming a genuine mutualism.
Wilson & Agnew, chapter 2, Interactions, page 41 of 53
In an interesting study assessing the decoy function of sterile teratological “flowers”
1284
1285
on Arabis holboellii (rock cress) caused by the rust Puccinia monoica, Roy (1996) showed
1286
that the mass flowering of mixtures of A. holboellii and Anemone patens attracted more bee
1287
visits to the latter. During bee visits the sticky pseudoflowers of A. holboellii removed pollen
1288
derived from the A. patens stamens and replaced it with fungal spermatia which reduced seed
1289
set in the A. patens. This is a complex interactive system that shows the potential for fertility
1290
interference effects, whether via pathogens or pollen vectors.
1291
6.3
1292
Herbivory
Herbivores can remove large amounts of plant material and this must affect the plant
1293
community. The word herbivory suggests grazing, with mammals biting off whole leaves, but
1294
most herbivores are invertebrates, and these maintain their trophic pressure more consistently
1295
and more specifically than the vertebrates. Contrary to the situation with vertebrates,
1296
invertebrate herbivore pressure can be as great below-ground as above-ground (Brown 1993;
1297
Wardle 2002). They can be very much smaller than their substrate, giving large populations.
1298
With fast reproduction this can allow efficient selection to overcome plant defences and
1299
specialise on particular plant species. Invertebrate herbivores have parasites and carnivores
1300
that control them. There are therefore complex systems affecting plant population fitness
1301
through herbivory, but since the observation of both the herbivory and the effect on the plant
1302
are difficult, we know little about the effects of invertebrates on the balance between co-
1303
occurring plant species and hence on community structure.
1304
Herbivores are always selective to some degree. However, the degree of
1305
discrimination varies widely. Many Lepidopteran larvae feed on only one species of plant,
1306
e.g. Tyria jacobaeae (the cinnabar moth) on Sencio jacobaea (ragwort). At the other extreme,
1307
many large non-ruminant animals such as Loxodonta africana (African elephant), even
1308
though they have preferences, will readily eat a wide range of species. More importantly,
1309
some such as Equus spp. (horses) often graze finely-patterned vegetation at a relatively coarse
1310
scale, necessarily taking in species with a range of palatability. We can see the causes of
1311
differential palatability of plants most clearly within species, e.g. cyanogenesis for
1312
Gastropoda (slugs; Jones 1966), smell and visual appearance for Atherigona soccata (a shoot
1313
fly; Nwanze et al. 1998), concentrations of nonstructural carbohydrates, sodium, iron and
1314
mercury for Sciurus aberti (a squirrel; Snyder (1992) and cineole in the leaf terpenoids for
1315
Anoplognathus spp. (Christmas beetles; Edwards et al. 1993). The relative palatability of
1316
species will be affected by a complex of such characters.
1317
Differences in palatability can affect the type of interaction between species. A plant
Wilson & Agnew, chapter 2, Interactions, page 42 of 53
1318
of target species S can be positively or negatively affected if conspecifics are replaced by
1319
plants of another species (analogously to a replacement comparison in interference, R below),
1320
or they can be affected positively or negatively by the presence of a neighbouring plant
1321
species when a herbivore moves into the patch (comparison A below), both by several
1322
mechanisms:
1323
positive:
1324
(1) the neighbour repels the herbivore, reducing the herbivory load on S (R)
1325
(2) the neighbour attracts the herbivore’s enemy, reducing the herbivory load on S
1326
1327
1328
1329
1330
(R)
(3) defences against herbivory are induced in the neighbour, reducing its interference
against S (A)
(4) the neighbour attracts the herbivore, which creates open ground, which is the
micro-beta niche of species S (R)
1331
(5) the neighbour attracts the herbivore, diverting the herbivory load from S (A)
1332
(6) the herbivore removes a more palatable, interfering, neighbour of S (A)
1333
(7) The herbivore defends S against a an interfering neighbour (A)
1334
negative:
1335
(8) the neighbour attracts the herbivore, increasing the herbivory load on S (A or R)
1336
(9) the herbivore removes a more palatable beneficient neighbour of S (A)
1337
(10) induced defences against herbivory in the neighbour divert the herbivore to S (R)
1338
(1) +ve: The neighbour repels the herbivore, reducing the herbivory load
1339
The repelling of herbivores by a neighbour (Augner 1994) affects plant communities
1340
at the scale which the repulsion occurs. For example, a spiny shrub deters the herbivore from
1341
consuming any other species within its canopy. A recognisably unpalatable species in a grass
1342
sward deters herbivore from taking its bite at that point, sparing any palatable species growing
1343
closely with it. As examples among mammalian browsers/grazers, Hjältén et al. (1993 %125)
1344
found that when Betula pubescens was associated with the less palatable Alnus incana (alder)
1345
the herbivores Microtus agrestis (voles) and Lepus timidus (hares) avoided those patches and
1346
B. pubescens suffered less herbivory damage, and Oesterheld and Oyarzábal (2004) found
1347
that plants of the palatable grass Bromus pictus tended to occur within one of the unpalatable
1348
tussocks. The avoidance of a less preferred patch would be part of an “extended phenotype”
1349
of the neighbour species, but confer benefit on all the plants in that community, as we have
1350
discussed above. Tuomi et al. (1994) suggested that the evolutionarily stable strategy would
1351
be for such benefit to conspecific neighbours to limited, or an undefended (‘selfish’) genotype
Wilson & Agnew, chapter 2, Interactions, page 43 of 53
1352
would too readily invade, and they suggested that plant defences should therefore deter the
1353
herbivore without killing it.
1354
Chemicals from a species might repel insects not only from that species but also from
1355
their neighbours. This is widely discussed as a goal of organic gardeners, but good evidence is
1356
hard to find. Tahvanainen and Root (1972) found that planting Lycopersicon esculentum
1357
(tomato) amid Brassica oleracea (collards) plants decreased flea beetle populations on B.
1358
oleracea and increased its plant weight. In a choice experiment, adult flea beetles (Phyllotreta
1359
cruciferae) preferred excised B. oleraceus leaves with no tomato mixed in with them, which
1360
is evidence of the involvement of a repellent chemical. It is widely suggested that some
1361
Tagetes species (African marigold), as companion plants, repel insect pests and thus benefit
1362
other plants in the crop. There is a little firm evidence for this (McSorley and Frederick 1994;
1363
McSorley and Dickson 1995), but nematodes, below-ground, may be mediating the
1364
interaction, apparently not due to any chemical coming from the Tagetes sp. plants (Ploeg and
1365
Maris 1999).
1366
(2) +ve: The neighbour attracts the herbivore’s enemy, reducing herbivory load
1367
White et al. (1995 %1171) found that planting Phacelia tanacetifolia, which was
1368
attractive to hover flies probably for its pollen, around Brassica oleracea (cabbage) patches
1369
(the control was bare ground around the patches) reduced the density of Brevicoryne
1370
brassicae and Myzus persicae (both aphids) on the B. oleracea.
1371
(3) +ve: Defences against herbivory are induced in the neighbour
1372
It is well established that herbivore attack, or leaf damage mimicking herbivory, can
1373
induce in a plant chemical defences such as alkaloids, nicotine, phenolics and tannins (e.g.
1374
Boege 2004, Vandarn et al. 2000), and even morphological defences (e.g. Young et al. 2003).
1375
In most cases, there is a fitness cost of this induced defence, for example in growth rate (Strauss
1376
et al. 2002). One would expect a reduced interference ability this is not the same as inducing
1377
defences in the neighbor, benefiting neighbours, and Baldwin and Hamilton (2000 %915)
1378
produced some evidence of this, but only intra-specifically. In order for this to operate, the
1379
herbivore has to select between species at a small scale: to be exact, inside the neighbourhood
1380
within which interference occurs.
1381
(4) +ve: The neighbour attracts the herbivore, which creates open ground
1382
Hoof marks are the preferred microenvironment of some species (Csotonyi and
1383
Addicott 2004). This does not depend on the herbivore’s having any selection between
1384
species or selecting at any particular spatial scale.
1385
(5) +ve: The neighbour attracts the herbivore, diverting the herbivory load
Wilson & Agnew, chapter 2, Interactions, page 44 of 53
1386
This is theoretically possible, and Atsatt and O’Dowd (1976) mention some possible
1387
examples. Mensah and Khan (1997) found that Medicago sativa (lucerne), which has a higher
1388
palatability in choice experiments to divert Creontiades dilutus (a mirid) pests from a crop of
1389
cotton. There was a dramatic effect over the four-month season. However, we can find no
1390
evidence from natural systems. The effect would be only temporary, because the herbivore
1391
population would build up on the neighbour, and probably then increase the herbivory load on
1392
the target.
1393
(6) +ve: The herbivore removes a more palatable, interfering neighbour
1394
If an interfering neighbour is palatable, herbivory could reduce interference from it,
1395
allowing increased growth of the target. This is the principle: “my enemy’s enemy is my
1396
friend”. It is remarkably difficult to find evidence for this. Part of the reason may be the
1397
difficulty of obtaining estimates of relative palatability, but confounding effects of the
1398
herbivore such as creating gaps and species-to-species tradeoffs such as between palatability
1399
and regrowth ability are other reasons (Bullock et al. 2001 %253). However, Cottam (1986)
1400
grew the grass Dactylis glomerata (cocksfoot) with the more palatable Trifolium repens
1401
(white clover). When there was no grazing D. glomerata suffered in mixture, dying out after
1402
120 days of grazing, but when there was grazing by Deroceras reticulatum (slug),
1403
D. glomerataii, grew as well as, or better than, in monoculture. Carson and Root (2000), in a
1404
very careful experiment, applied insecticide experimentally in an oldfield dominated by
1405
Solidago altissima and S. rugosa (goldenrods). It became clear that in the untreated
1406
community specialist Microrhopala spp and Trirhabda spp (chrysomelid beetles) were
1407
suppressing the Solidago spp and thus allowing increased growth of other forbs and of woody
1408
seedlings. As with other mechanisms involving release from interference, the herbivore must
1409
select between species at a fine scale.
1410
(7) +ve: The herbivore defends against an interfering neighbour
1411
Ants are often associated with plants. For example, Macaranga is an old world genus
1412
in the Euphorbiaceae (often conspicuously part of secondary forest) some of whose species
1413
bear extra-floral nectaries which attract ants and domatia hollows which shelter them. The
1414
relationship is close and complex. Fiala et al. (1989) found that on trees of Macaranga spp. in
1415
Malaya ants considerably reduced the amount of herbivory damage, mainly by forcing
1416
lepidopteran larvae (caterpillars) off leaves, and possibly by harassing Coleoptera (beetles)
1417
and Acrididae (grasshoppers). The ants involved are generalist predators often in the genus
1418
Crematogaster, yet they also seemed to protect against lianas: Macaranga species that were
1419
myrmecophytic had far fewer lianas attached, and this difference was seen only with plants
Wilson & Agnew, chapter 2, Interactions, page 45 of 53
1420
occupied by ants. The effect was caused by the ants biting the tips of invading liana, and
1421
Federle, Maschwitz and Holldobler (2002) showed that they also pruned adjacent tree species
1422
reducing canopy contact and presumably also competition.
1423
(8) -ve: The neighbour attracts the herbivore, increasing the herbivory load
White and Whitham (2000) found that Populus angustifolium  fremontii
1424
1425
(cottonwood) plants growing under the highly palatable Acer negundo (box elder) suffered
1426
much more herbivory from the insect Alsophila pometaria (fall cankerworm) than those under
1427
their own species or in the open. Sessions and Kelly (2002) suggested that the grass Agrostis
1428
capillaris (bent) created a moist habitat suitable for Derocerus reticulatum (a slug) that then
1429
attacked a nearby fern (Botrychium australe). Mechanism ‘8’ can operate at any spatial scale
1430
and the herbivore does not need to be selective so long as it is attracted to the patch by one
1431
species. It seems to be the situation to which the strange term ‘apparent competition’ has been
1432
applied. The term ‘magnet species’ for the neighbour is more helpful.
1433
(9) -ve: The herbivore removes a more palatable, subventing neighbour
1434
This is a theoretical possibility, but we know of no example. As with mechanisms
1435
involving competitive release, the herbivore must select at a fine scale.
1436
(10) -ve: Induced defences in the neighbour divert the herbivore to the target
1437
Induced defences are now known in many species, which could protect that species
1438
but not a neighbour. We do not know of any explicit examples of this.
1439
6.4
1440
Indirect impacts of diseases
For some of the mechanisms of positive plant-plant interactions via herbivores that we
1441
discussed above, such as ‘2’, ’4’ and ‘7’,it is hard to envisage analogues for fungal or viral
1442
diseases. However, others seem possible. The neighbour could repel viral vectors such as
1443
aphids (Birkett et al. 2000), reducing the disease load on S, the equivalent of herbivory
1444
interaction ‘1 +ve’ above. Defences against fungal diseases are often induced in the host, and
1445
these might carry a cost (though the evidence for this is weak), reducing the host’s
1446
competitive ability against S (cf. herbivory ‘3 +ve’). The effect (translating to disease terms)
1447
“5 +ve: The neighbour attracts the fungus, diverting the load from S”, could be applied when
1448
a neighbour had a strong ‘fly-paper effect’, trapping fungal spores (chapt. 4, sect. 4.3, below).
1449
Disease could remove a more susceptible neighbour that normally interferes with S
1450
(cf. herbivory ‘6 +ve’). For example, the introduction of the Asian pathogen Cryphonectria
1451
parasitica (= Endothia parasitica; chestnut blight fungus) to forests of northeastern USA led
1452
to almost complete death of the dominant Castanea dentata (chestnut) trees. In one area this
Wilson & Agnew, chapter 2, Interactions, page 46 of 53
1453
resulted within c. 14 years to a doubling of the basal area of Quercus rubra (red oak) and a
1454
threefold increase in Quercus montana (Chestnut oak) (Korstian and Stickel 1927). Almost all
1455
the other tree species increased slightly. In other areas different species took advantage of the
1456
released resources.
1457
A neighbour could be very susceptible to the disease, and, whilst not quite being a
1458
magnet, it could spread spores or vectors and increase the disease load on S. For example,
1459
Power and Mitchell (2004, %79) found in a field experiment with plots of 1-6 grass species
1460
that plots containing Avena fatua (wild oats), which was highly susceptible to a particular
1461
generalist aphid-vectored virus, were over 10 × more heavily infected than communities
1462
lacking A. fatua. They termed this ‘pathogen spillover’, but it is a close equivalent of our
1463
herbivore situation “8 -ve: The neighbour attracts the [disease], increasing the [disease] load”.
1464
For those wishing to use the term ‘apparent competition’, it is the disease equivalent.
1465
Possibly, the disease could removes a more susceptible neighbour that a facilitator of S
1466
(herbivory ‘9 -ve’). An equivalent to herbivory mechanism ’10 -ve’ seems just possible.
1467
The impact of diseases is seen most obviously when they appear suddenly, as in the
1468
case of chestnut blight. We can be fairly sure that diseases in the past have had a major hand
1469
in shaping the plant communities that we see today and continue to. (Janzen scatter
1470
hypothesis?)
1471
7 Interactions
1472
7.1
1473
1474
Litter-herbivore interactions
Grazing, especially by large grazers, can result in:
1. less natural litter production, both because plant vigour may be reduced by the
1475
removal of photosynthetic organs and because leaves have a lower probability of
1476
reaching senescence,
1477
1478
1479
2. redistribution of lying litter by trampling and habitat use, often speeding
decomposition (Eldridge and Rath 2002),
3. an increase in the production of leaf litter induced by animal movement damage, the
1480
tearing of edges of leaves that have been bitten, etc., and more woody litter including
1481
CWD from collateral damage by tree canopy browsers (notably by elephants:
1482
Plumptre 1994),
1483
4. material shed around the point of damage, e.g. Buck-Sorlin and Bell (2000), found
1484
that spring defoliation and shoot tip removal in Quercus spp. (oak) trees in Wales led
1485
to increased shoot shedding;
Wilson & Agnew, chapter 2, Interactions, page 47 of 53
1486
5. reduced suppression of sub-canopy species, potentially adding more of their litter.
1487
The complexity of such processes and systems are well illustrated by Long et al. (2003), who
1488
examined the interaction between the beetle herbivore Trirhabda virgata and its food plant
1489
Solidago altissima (goldenrod). Beetle populations were highest in the densest S. altissima
1490
patches, leading to reduced plant vigour and lower litter production. Litter, when present in
1491
quantity, increased aboveground biomass and reduced species richness. Thus the net effect of
1492
the beetle and S. altissima concentrations was to enhance plant species diversity by reducing
1493
litter disturbance.
1494
In heavily grazed vegetation, litter is reduced and can have little or no effect, so that
1495
more of the system of interspecific interactions must depend on growth disturbance, as well as
1496
interference and subvention. This conclusion conflicts with the usual assumption that
1497
competition will be less intense under heavy grazing. There is nothing in the first sentence
1498
that proves that just because litter has no effect, that interference (neg. interactions., aka
1499
competition) and subvention (pos. interactions) are necessarily the forces that are driving
1500
community structure- it is merely stated as a fact without backing. Heavy grazing might give
1501
rise to a community structured by the ability to survive the grazing or to recolonize areas
1502
opened by disturbance, in other words a community structured not be plant-plant interactions,
1503
but by plant-herbivore interactions. It might favour rare species (escape from grazing) or
1504
unpalatable species. Indeed as you state that both negative and positive plant interactions are
1505
more important in these systems, even that statement doesn’t lead to the conclusion that
1506
negative interactions (competition) will increase or even dominate the system interactions.
1507
If only living plant presence is recorded and litter is ignored, only growth interactions
1508
can be assessed. This may explain why the strongest evidence for assembly rules has been
1509
found in uniformly and heavily grazed (i.e. mown) lawns (Wilson and Roxburgh 1994), in a
1510
heavily grazed saltmarsh (Wilson and Whittaker 1995) and a sand dune (Stubbs and Wilson
1511
2004), in all of which there is very little accumulation of litter and interactions due to growth
1512
are not obscured by the litter effect. This suggests that assembly rules should be sought which
1513
include not only the living components but also the litter, as implied by Grime (2001) in his
1514
interpretation of the productivity-richness humpback curve.
1515
CWD can also interact with herbivory. Long et al. (1998) suggest that treefall mounds
1516
provide a refuge from herbivory for Tsuga canadensis (hemlock) regeneration, which is
1517
important in spite of its being a less favourable environment for establishment of that species
1518
than the forest floor.
Wilson & Agnew, chapter 2, Interactions, page 48 of 53
1519
7.2
1520
Litter-fire interactions
Sometimes the autogenic effect of litter interacts with allogenic disturbance. Fire is
1521
perhaps the best example. If litter accumulates faster than it decomposes, and local conditions
1522
of climate and soil are too dry to allow peat accumulation, its ultimate fate on a landscape
1523
scale is destruction by fire. This is basically an autogenic effect because there can be no fire
1524
without fuel, and the initiating fuel of a fire is usually a buildup of standing dead,
1525
programmed and stochastic litter. However, an allogenic process has to start the fire. After
1526
fire, the litter accumulation cycle restarts. This is a process intrinsic to heathlands and dry
1527
forests over large geographical areas.
1528
Various factors affect the probability and the type of fire. In a flash fire burning
1529
mainly volatiles either in the field layer or the canopy, litter will play little part. However a
1530
fire that consumes the litter will burn for longer. All fire will impact more on the less fire-
1531
resistant and more fire-intolerant species (Whelan 1995). In many vegetation types, branch
1532
fall provides the fuel build up because CWD is long-lived, much of it persisting until burnt.
1533
Treefall also provides fuel (Whelan 1995). The spread of fire into the canopy is facilitated by
1534
the retention of dead limbs (Johnson 1992), so branch fall will help to confine fire to the
1535
ground flora, sparing the canopy stratum. Lianas can have a similar effect: Putz (1991)
1536
observed flames travelling up lianas, with the result that Pinus spp. (pine) trees with lianas
1537
(especially Smilax spp., greenbriar etc.) were more likely to suffer crown scorch than liana-
1538
free trees. Fire is especially prevalent in communities of conifers (particularly Pinus:
1539
Ne’eman and Trabaud 2000) and of Eucalyptus (gum) apparently because of their flammable
1540
resin/oil content (Whelan 1995; Williams et al. 1999). At the other extreme, some types of
1541
vegetation are very fire resistant. For example, in arid central Australia, where most
1542
vegetation is fire-prone, Acacia harpophylla (wattle) does not burn (Pyne 1991) because of
1543
several features: their chemistry makes the leaves barely flammable; the simple leaf shape
1544
results in flat, poorly-aerated litter fuelbeds; leaf fall is keyed to intermittent rains, when fire
1545
is less likely; bark is not shed; and finally the microclimate of the forest floor discourages
1546
drying and promotes decomposition.
1547
7.3
1548
Litter-herbivore-fire interactions
There are several examples of good evidence for higher-order interactions between
1549
grazing, litter and fire. For example, in North American Pseudotsuga menziesii (Douglas fir) /
1550
Physocarpus malvaceus (mallow ninebark) forest, grazing by livestock (including cattle,
1551
sheep and deer) reduces the herb layer and hastens the decay of litter by trampling
1552
(Zimmerman and Neuenschwander 1984), and the unpalatable herbs left tend to be less
Wilson & Agnew, chapter 2, Interactions, page 49 of 53
1553
flammable. This reduces fire frequency, but allow the buildup of coarse woody debris so that
1554
when fires occur they are more severe and may reach the canopy. A similar effect of grazing
1555
reducing the fuel load and hence the frequency of fires occurs in the African savannah (Fig.
1556
2.8; Roques et al. 2001). In habitats with both a grass and a woody component (savannah or
1557
ecotone) a number of processes can occur (Fig. 2.8; Brown and Sieg 1999; Touchan et al.
1558
1995).
1559
This process includes many complexities. It could converge to an equilibrium, it could
1560
operate as a cyclic succession, or a switch could also operate in the system, giving alternative
1561
stable states (Fig. 2.8; Dublin 1995). In the 1960s and 70s, fire caused a decline in Serengeti
1562
woodland, because higher rainfall then led to greater grass growth (Dublin et al. 1990).
1563
Loxodonta africana (African elephant) inhibited the recovery and kept it as grassland, and
1564
because of their grazing the grass crop is not enough to support hot fires. On the other hand,
1565
elephants avoid the fire-resistant thickets, which are therefore stable as an alternative stable
1566
state. There are both negative and positive feedback processes here.
1567
Wilson & Agnew, chapter 2, Interactions, page 50 of 53
1568
1569
Fire repelled
1570
1571
1572
Woody thicket
1573
remains
Elephant browsing
1574
repelled
1575
Woody patch escapes
1576
the fire
1577
Catastrophic fire,
1578
triggered by an
1579
exceptional event1
1580
Trees
Woody plants killed,
re-establish
1581
at least above ground
1582
1583
Fire frequency
Less palatable
1584
reduced
forbs dominate
1585
More light is allowed
1586
into the field layer
1587
Litter buildup
1588
reduced
1589
1590
1591
Invasion of
Grass growth promoted
woody species
Fewer old
1592 Litter decays
suppressed
leaves
1593 faster
1594
1595
1596
Regular
Trampling
Grazing
1597
fires
1598
Low
1599
High rain
rain
The grazing
Low
1600
resource increases
rain
Herbivore density
1601
increases
1602
1603
1
1604
A rainy season giving a heavy crop of grass followed by a dry season; or a dry season
1605
making savannah burnable; or high browser density causing CWD accumulation
1606
= switch
1607
Fig. 2.8: Pathways of community change in dry savannah.
1608
8 Conclusion
1609
We have described the many processes that can be involved in the development of
Wilson & Agnew, chapter 2, Interactions, page 51 of 53
1610
mixed species stands. Most types of interference, subvention, litter effects and autogenic
1611
disturbance are based on the universal principle of reaction, that organisms in general, and
1612
plants in particular, modify their physical environment. All these reactions have effects on
1613
neighbours. The wide variety of modifications and the wide variety of responses by
1614
neighbours are the reasons for the long list of interactions we gave, a list that we tried to make
1615
exhaustive but surely have not.
1616
Plants must be seen within the framework of the ecosystem. Autotrophs make up most
1617
of the stored living carbon framework of terrestrial ecosystems, i.e. its biomass, and a plant’s
1618
biomass is also a necessary part of its work in foraging for light and soil resources. But
1619
phytomass is never alone. Operators from other trophic levels are always present and can
1620
have profound influences on plant species presence, adding to the complexity. Clements
1621
envisaged reaction as being on the physical environment. We are reluctant to expand this to
1622
the biotic environment because of the ensuing complications, but we have listed interactions
1623
“mediated by other trophic levels”. There are complex interactions amongst heterotrophic
1624
levels too, which will also impact on our dear plants. Paine’s original usage of ‘Keystone
1625
species’ (chapt. 5, sect. 11 below) is a clear expression of these.
1626
The plant community comprises continual renewal: disturbance, death, establishment,
1627
growth and both sexual and vegetative reproduction of great numbers of offspring – greater
1628
than the habitat can support. The negative and positive interactions that we have listed
1629
moderate those processes. In the next chapter we consider how those processes operate at the
1630
whole-community level, to determine successional changes after allogenic or autogenic
1631
disturbance, and to affect the spatial pattern of vegetation.
1632
Wilson & Agnew, chapter 2, Interactions, page 52 of 53
1633
1634
Table 1. Effects of litter on the population dynamics of species in the community, as reported
in the literature.
1635
1636
1637
1638
1639
1640
1641
1642
1643
1644
1645
1646
1647
1648
1649
1650
1651
1652
1653
1654
1655
1656
1657
1658
1659
1660
1661
1662
1663
1664
1665
1666
1667
1668
1669
1670
1671
1672
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
Theimer and Gehring 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
Watt 1931
Scurfield 1953
Beatty and Sholes
Facelli and Pickett 1991b
Beatty and Sholes 1988
Helvey and Patric 1965
1673
ILLUSTRATIONS
1674
Fig. 2.1. Replacement and additive comparisons in experiments that examine the interaction
1675
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.
1676
Fig. 2.2. In Trifolium subteranneum, the results of competition affect competitive ability.
1677
Fig. 2.3: A possible mechanism for size-asymmetric competition belowground, when nutrient
1678
supplies become available patchily in time and space, e.g. from sheep micturition.
Wilson & Agnew, chapter 2, Interactions, page 53 of 53
1679
Fig. 2.4: After Novoplansky et al. (1990).
1680
Fig. 2.5: After Biddington and Dearman (1985).
1681
Fig. 2.6: The seasonal pattern of litterfall in an oakwood. After Christensen (1975).
1682
Fig. 2.7. The process of peat accumulation in mires dominated by Empodisma (wire rush) or
1683
1684
Sphagnum moss species.
Fig. 2.8: Pathways of community change in dry savannah.
i
ii
Microscopic algae do move.
when planted as 66% of the mixture