Download Chapter 2

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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 ........................................................................ 9
2.6 Rarity and competitive ability ............................................................................. 12
2.7 Allelopathy .......................................................................................................... 13
2.8 Parasitism ............................................................................................................ 14
2.9 Spectral Interference (red/far-red) ....................................................................... 15
2.10 Pest carriers ......................................................................................................... 16
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Subvention: positive effects between plants ............................................................... 18
3.1 Water flow and nutrient redistribution ................................................................ 18
3.2 Ambient conditions (temperature, evapotranspiration and wind) ....................... 19
3.3 Aerial leakage of nutrients .................................................................................. 20
3.4 Salt ....................................................................................................................... 20
3.5 Shelter from ultra-violet ...................................................................................... 21
3.6 Protection from soil frost-heave .......................................................................... 21
3.7 Hydraulic lift ....................................................................................................... 21
3.8 ‘Talking trees’ ..................................................................................................... 22
3.9 Subvention conclusion ........................................................................................ 22
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Litter: the necessary product ....................................................................................... 22
4.1 The timing and type of litter production ............................................................. 23
4.2 Litter decomposition ........................................................................................... 27
4.3 Effects of litter ..................................................................................................... 28
4.4 The direct mechanical effect of litter .................................................................. 29
4.5 Alteration in environment by litter ...................................................................... 29
4.6 Leachates from litter............................................................................................ 30
4.7 Control of nutrient cycling .................................................................................. 30
4.8 Peat formation ..................................................................................................... 31
4.9 Can reaction via litter evolve? ............................................................................. 33
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Autogenic disturbance: plants as disturbers ................................................................ 34
5.1 Movement and contact ........................................................................................ 35
5.2 Growth thrust....................................................................................................... 36
5.3 Crown shyness..................................................................................................... 37
5.4 Growth and gravity.............................................................................................. 37
5.5 Lianas .................................................................................................................. 38
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Plant-plant interactions mediated by other trophic levels ........................................... 39
6.1 Below-ground benefaction .................................................................................. 40
Wilson & Agnew, chapter 2, Interactions, page 2 of 54
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6.2 Pollination ........................................................................................................... 41
6.3 Herbivory ............................................................................................................ 42
6.4 Indirect impacts of diseases................................................................................. 46
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Interactions .................................................................................................................. 47
7.1 Litter-herbivore interactions ................................................................................ 47
7.2 Litter-fire interactions ......................................................................................... 49
7.3 Litter-herbivore-fire interactions ......................................................................... 49
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Conclusion ................................................................................................................... 51
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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
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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 54
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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 54
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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
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.)
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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Why not? Isn’t space a resource, independent of other resources that plants compete
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for?
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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
Wilson & Agnew, chapter 2, Interactions, page 5 of 54
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that he emphasises that all competition is via reaction. No intrinsic competitive
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characteristics?
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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.
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Transitivity? Definitions of terms not yet dealt with would be helpful
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. What
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happened here? There has been a change in gears with minimal transition
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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
Wilson & Agnew, chapter 2, Interactions, page 6 of 54
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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
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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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I’m not seeing the hierarchical arrangement of interference versus competition. It
seems that they could easily be flip flopped, according to the earlier definition of each.
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
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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
Wilson & Agnew, chapter 2, Interactions, page 8 of 54
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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
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volume occupancy of eight plant communities (four in each in each of Italy and NZ,
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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). Isn’t it true that plants REACT to each other in competition for
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space? The example of vines keeps coming to mind, where different species wrap around each
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other, indirectly searching for resources. However, the growth itself is a competitive activity,
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in search of space.
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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
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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. I’d like to see more on plasticity (phenotypes being expressed or
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repressed, mechanisms of plasticity, etc.)
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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’.
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
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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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Size asymmetry seems very subjective.
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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
353
large plant could take up enough to satisfy the whole of itself from a few roots in the patch,
354
whereas a small plant outside the patch could not reach in (Fig. 2.3). This argument applies
355
only when the patches are transient, so it seems reasonable that Blair (2001 %199) could find
356
no evidence that spatial heterogeneity in nutrients led to size-asymmetric competition.
357
If nutrients are patchy, then all plants have a roughly – chance of landing
358
(germinating) in a high nutrient patch. Larger plants though have an increased chance of
359
capturing a high nutrient patch within their root-soil-volume. Therefore the large plant will
360
be more likely to have access to a high nutrient area than a small plant. The large plant does
361
have to support roots in low nutrient areas, but once a high nutrient area has been
362
encountered, the plant can allocated increased root growth into that soil volume.
Wilson & Agnew, chapter 2, Interactions, page 12 of 54
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.
363
364
We conclude that cumulative competition, due to size-asymmetry, i.e. the effect of
365
initial advantage, is not a necessary feature of plant competition. It will occur only when there
366
is a specific feedback mechanism, such as that via height/light, that results in competitive
367
success increasing competitive ability per unit biomass. The conditions under which it occurs
368
have huge implications for community structure, because if competition be cumulative
369
competitive exclusion will occur much more readily, and faster, and coexistence less readily.
370
2.6
Rarity and competitive ability
371
It is often suggested that plant species become rare because they are poor competitors,
372
but the evidence here is mixed. Walck et al. (1999) found that low competitive ability may be
373
one factor contributing to the narrow endemism of the dryland species Solidago shortii
374
(goldenrod) in comparison with the widespread S. altissima, which can overtop S. shortii in
375
more mesic sites but it is simplistic to interpret a two-species comparison in terms of general
376
trends in rarity. Lloyd et al. (2002) working in New Zealand found that there was no general
377
relation between competitive ability and rarity at either high or low levels of soil fertility for
378
ten species in the rosaceous genus Acaena (biddy bid), but in the grass genus Chionochloa
379
(snow tussock) common species tended to be stronger competitors than rare species, and this
380
was significant at the low level of fertility—in some sense, either via initial
381
advantage/competition or through some sort of competitive mechanism, isn’t it inevitable that
382
common species have competed their way to their place?. Several of the common
383
Chionochloa species have expanded their geographic ranges since anthropogenic forest
384
removal, consistent with their greater competitive ability. Conversely, rare Chionochloa
Wilson & Agnew, chapter 2, Interactions, page 13 of 54
385
species occupy specialized habitats that may be interpreted as refuges from competition—is
386
this the competition v. ruderal v. disturbance idea?. However, it is too simplistic to speak of a
387
plant being a generally strong or weak competitor. Apart from ruderals, every species is a
388
good competitor in the sites that it inhabits, at least a good enough one to persist. Hubbell et
389
al. (2001 %759) reported a curious relationship between rarity and neighbourhood effects in
390
neotropical forest, such that the survival by rare trees was more adversely affected by
391
conspecific neighbours than that of common species. One explanation is that the rare species
392
are using rare resources, or that they are limited by specific pests (chapt. 4, sect. 3 below)
393
This subject was covered to quickly. It would be useful to explain how rarity could increase
394
the fitness of those individuals left, and why this is useful in defining a plant community.
395
2.7
396
Allelopathy
Allelopathy is another type of interference. Unlike competition, it does not involve a
397
“shared resource in limited supply” (sect. 2.1 above). Rather, a toxin produced by plants is
398
either leached or volatilised from their living parts, above- (Inderjit et al. 1999) or below-
399
ground (Kato-Nogudi 2004), from standing dead plants (Gliessman and Muller 1978), or from
400
the breakdown of their litter (e.g. Kuiters 1991; Sharma et al. 2000), and then reduces the
401
growth of neighbouring plants. Some ecologists believe that allelopathy is a widespread and
402
important process (Rice 1983; Inderjit et al. 1994). Others are sceptical (Harper 1977). Most
403
plants contain chemicals that are toxic to other plants, at least in the right circumstances. It is
404
very unlikely that the strong effects that can readily be demonstrated by leaf elutants in petri
405
dishes will happen in nature, but it is equally unlikely that soil bacteria and colloids will
406
completely neutralise the effect, and field experiments are difficult to perform (Williamson
407
1990).
408
Most work has been with shoot elutants, but Mahall and Callaway (1991 %2145; 1992
409
%874) conducted greenhouse experiments between Larrea tridentata (creosote bush) and
410
Ambrosia dumosa (white bursage). The two species occur together in the Mojave Desert.
411
Roots of A. dumosa were inhibited when they came near to roots of L. tridentata. This effect
412
was reduced by activated carbon, so it was presumably via some chemical. The two species
413
apparently have similar water extraction capabilities (Yoder and Nowak 1999b), so this
414
signalling would enable to the plants to avoid each other and postpone the onset of
415
competition. This may be a more common phenomenon than we have knowledge of at
416
present. More direct evidence for the production of toxins from roots was obtained by
417
Welbank (1963), but only after they had started to decompose in anaerobic conditions. But
418
there are always decomposing roots around a living plant and they may indeed create
Wilson & Agnew, chapter 2, Interactions, page 14 of 54
419
anaerobic conditions in the immediate vicinity of the decomposing root through their own
420
decomposition or the uptake of O2 by neighbouring roots. Perhaps then it isn’t unreasonable
421
to look at this as a source of these compounds.
422
We are inclined to think in teleological terms, of plants deliberately inhibiting their
423
neighbours. Although we know this is not true, it leads to an assumption that allelopathic
424
ability has evolved as an adaptation: species that make their locale unfavourable for the
425
growth of other species will gain in selection. But can this evolve? If a mutant produces an
426
allelochemical against other species this will be at some cost to itself (many of the secondary
427
compounds involved are expensive for the plant to make), yet unless the effect is very local it
428
will benefit non-mutant plants of the same species as much as itself—but isn’t it often very
429
local? Especially in ecosystems where, e.g. the Janzen scatter hypothesis holds, species’
430
individuals tend to spread out anyway?, and the trait will not evolve. Why shouldn’t the
431
allelopathic chemical affect non-mutants of the same species?
432
We then have to invoke group selection, is a controversial and probably weak force
433
(Wilson 1987 %493). This problem would not occur with selection for a plant to protect itself,
434
and thus eventually its species, against its own allelochemical. Williamson (1990) commented
435
that there would be equal selective pressure on the species’ neighbours to develop defences,
436
but this ignores the issue that a species always grows with itself, but has a variety of
437
neighbours against which it would have to protect itself. Newman (1978) questioned whether
438
selection was involved at all, finding in a literature survey that auto-toxicity is as common as
439
toxicity to other species. He argued that this indicates that allelopathy is an accidental result
440
of the production of secondary compounds.
441
442
We discuss the particularly complex allelopathic interactions with litter in section 3.5
443
below. Allelopathy seems more of a competitive trait than simply an interfering trait .
444
Allelopathy contributes to the competitive ability of an organism, right? So, how are
445
interference and allelopathy not functions of competition?
446
447
448
2.8
Parasitism
Plant parasites are commoner in the dry tropics than in temperate climates. There are
449
partial shoot parasites (Loranthaceae, Viscaceae) and total shoot parasites (e.g. Cuscuta,
450
Cassytha) as well as partial (e.g. Rhinanthus spp.) and total root parasites (e.g.
451
Balanophoraceae, Orobanchaceae, Rafflesiaceae, Striga gesnerioides). The immediate effect
452
of a parasite is to depress the growth of the hosts. Infestation by some root parasites can
Wilson & Agnew, chapter 2, Interactions, page 15 of 54
453
reduce crops by up to 70% (Graves et al. 1992; Press 1998). There is often an increase in
454
species diversity (Press 1998). This may be because the parasite’s favourite hosts are the
455
dominant species, and a reduction in their productivity allows subordinate species to flourish,
456
possibly also reducing cumulative competition (sect. 1.1.4 above). It is not clear why parasites
457
should favour the dominants, but perhaps we see the effect more when they do. On the other
458
hand, the parasite could reduce the productivity of the whole community from high to
459
medium, allowing more species to coexist if the humped-back theory of Grime (1973; 2001)
460
is correct. Situations, however, can be very complex when plant hosts, their parasites and their
461
herbivores are examined. Marvier (1996; 1998) compared aphid performance on the parasite
462
Castilleja wightii (paintbrush) in host plants differing in N content, which was highest in a
463
legume (Fabaceae) and lowest in a composite (Asteraceae). Aphid populations did best on the
464
parasite when it depended on the legume host and worst when the host was the composite,
465
leaving the C. wightii worse off on the legume, in spite of the latter’s higher nitrogen content.
466
These interactions differentially affect the host plant species and their parasite, modifying
467
competitive ability, but are complicated by the parasite’s ability to better its performance by
468
mixing its hosts.
469
2.9
Spectral Interference (red/far-red)
470
Plant canopies change the spectral quality of light that passes through them. Of
471
particular importance for plant-plant interaction is that the red/far-red ratio (R/FR) is lower in
472
light that has passed through a leaf or been reflected off one. It is therefore lower under
473
canopies and somewhat lower in canopy gaps than in the open (Turnbull and Yates 1993;
474
Davis and Simmons 1994). This can decrease the leaf chlorophyll content of plants in the
475
lower strata and hence reduce their photosynthetic capacity, leaf life, leaf area ratio, tiller
476
production and relativeh growth rate (Barreiro et al. 1992; Dale and Causton 1992; Skinner
477
and Simmons 1993; Rousseaux et al. 1996), and decrease seed germination (Batlla et al.
478
2000, Kasperbauer 2000).
479
These responses are mediated by phytochrome (Gilbert et al. 1995). However, the
480
response depends on the species. Leeflang (1999) found that only one species out of the six
481
that they examined responded to R/FR ratio in terms of biomass accumulation. Dale and
482
Causton (1992) found differences between three Veronica species (speedwell): the species
483
that grew in deeper shade responded more to R/FR. It can be difficult to separate effects of
484
light intensity and spectrum, but sometimes plants respond morphologically to the presence of
485
neighbours even before they are directly shaded, by sensing the change in R/FR in light that
486
has been reflected off neighbours (Schmitt and Wulff 1993).
Wilson & Agnew, chapter 2, Interactions, page 16 of 54
487
R/FR may be less important for its direct effect on the growth of the recipient than as a
488
signal to the plant that competition is imminent, allowing it to respond by either competition
489
tolerance or competition avoidance. (Murphy and Briske 1994; Stuefer and Huber 1998). For
490
avoidance, R/FR can induce plastic changes which would allow the plant to reduce shading
491
by its neighbours, e.g. enhancing leaf elongation, making shoots and leaves more upright, and
492
increasing shoot:root ratio (Skinner and Simmons 1993; Vanhinsberg and Vantienderen
493
1997). The R/FR signal can also promote plant foraging for light gaps away from competitors,
494
through altered stem angle and longer internodes (Ballaré et al. 1995). Some plants sense and
495
grow away from each other, even at some distance. Manipulation of R/FR ratios, and
496
experimentation with pieces of plastic with the same spectral characteristics as plant leaves,
497
show this to be due to R/FR effects (Fig. 2.4; Novoplansky 1991). Germination can be
498
reduced under a canopy, but faster germination is also possible, and these R/FR responses can
499
be seen as competition avoidance and greater competitive effort, respectively (Dyer et al.
500
2000). R/FR is not everything: Muth and Bazzaz (2002) found that visible (PAR) light was
501
more important than R/FR in the gap-seeking of Betula papyrifera (birch) seedling.
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).
502
503
504
2.10 Pest carriers
Plants can interact at a local scale using pests as weapons. Van den Bergh and Elberse
505
(1962) found that under a high nutrient regime Lolium perenne at first outcompeted
506
Anthoxanthum odoratum, but eventually A. odoratum transmitted a virus to L. perenne and
507
suppressed it. There is evidence that the invasion of the exotic Avena fatua (wild oat) into
508
Californian grasslands has been due to its increasing the incidence of a virus in the native
509
tussock grasses, severely reducing their growth, though the effect may be indirect, due to its
510
increasing the abundance of the aphids that are vectors of the virus (Malmstrom et al. 2005).
Wilson & Agnew, chapter 2, Interactions, page 17 of 54
511
A similar situation may exist in California where preliminary evidence suggests that
512
Umbellularia californica (Bay laurel) is infected with the fungus Phytophthora ramorum, but
513
is little affected. However, many spores are produced and these cause the death of nearby
514
Quercus spp. (oaks) and Lithocafvrpus densiflora (tannoak) (Mitchell and Power %Collinge
515
58). We list these examples of species as pest carriers separately, though they grade into
516
plant-plant interactions moderated by diseases (sect. 4.4, below).
517
Wilson & Agnew, chapter 2, Interactions, page 18 of 54
518
519
3 Subvention: positive effects between plants
520
Just as the plant community provides a diversity of habitats for heterotrophic
521
organisms, so it augments the diversity of sites available for plant species by increasing
522
environmental heterogeneity both horizontally and vertically. One logical result of this
523
reaction (sensu Clements) should be subvention: positive effects by some species on the
524
survival and/or growth of others. Gleason (1936) gave subvention equal weight with negative
525
interference, but whilst the interference between species has been a focus of attention
526
subvention has been neglected until recently (Lortie et al. 2004). Subvention changes during
527
ecesis as plants grow and change shape, so that repeatable patterns of interaction are difficult
528
to find. Usually two species are not absolutely dependent on each other for survival.
529
Moreover, the existence of a subvention by species A on species B does not imply that they
530
have co-evolved. It is simply a corollary of reaction. The terminology of subvention is
531
confusing. We use the scheme:
532
subvention
533
mutualism (= synergy) = both species benefit relative to their being at the same
534
density on their own (i.e. an additive comparison).
535
benefaction = one species benefits as above, with no known advantage or
536
disadvantage to itself
537
facilitation = one species benefits another, to its disadvantage
538
The term ‘facilitation’ was used thus by Connell and Slatyer (1977) for Clements’ (1916)
539
concept of the mechanism of succession, but it is appropriate here since the mechanisms are
540
the same. We consider here the various environmental features which are modified by plants
541
to the benefit of their own, or other species. The list is a long one, and we are aware that many
542
potential effects have been left out. The review by Callaway (1995) discusses more examples
543
than are cited here.
544
3.1
Water flow and nutrient redistribution
545
Plants intercept rainfall. Up to half of the input can be lost by evaporation from the
546
canopy (Cape et al. 1991), but input is occasionally increased due to fog capture (chapt. 3,
547
sect. 5.4.B below). The distribution of soil water input is made far more patchy, for example
548
through stemflow amongst many interactions. Nutrients can be made even more patchy
549
because of leaf leaching. Stemflow can be an important source of nutrients for epiphytes,
550
especially of nitrogen for which stemflow concentrations can be more than ten times those in
Wilson & Agnew, chapter 2, Interactions, page 19 of 54
551
rainwater (Awasthi et al. 1995; Whitford et al. 1997). This may explain the trunk-base habitat
552
of a few mosses such as Isothecium myosuroides in Western Europe. This induced patchiness
553
in nutrients is a good example of benefaction without there being any question of co-
554
evolution. Benefaction, by its nature, would not seem to involve co-evolution. It is confusing
555
to bring up the possibility of co-evolution in this way when talking about benefaction.
556
It might be better to leave it out or firm up the statement. In the clustered or striped vegetation
557
(‘tiger bush’) typical of arid and semi-arid areas (chapt. 3, sect. 5.4.B below), there can be
558
similar benefaction by shrubs and trees of their understorey. For example, litter can increase
559
infiltration into the soil by preventing runoff in semiarid areas (Tongway et al. 2001).
560
However care must be taken in interpreting these patterns. Walker et al. (2001) demonstrated
561
by plant manipulations that whilst islands of soil fertility around woody plants can increase
562
water and nutrient availability, the net effect of nurse plants can be negative due to shading
563
and/or root competition.
564
3.2
565
Ambient conditions (temperature, evapotranspiration and wind)
Plants alter the physical environment around and below them in obvious ways:
566
ambient temperature, evapotranspiration and air movement. This is reaction. Canopy trees
567
dampen diurnal and seasonal fluctuations in subcanopy air temperature (Stoutjesdijk and
568
Barkman 1992; Chen et al. 1993) and this is significant because temperature stresses of heat
569
load or frost can kill cells. Daytime temperature in the field layer of a forest is generally 1-
570
3 oC less than above the canopy. Windspeed is lower, reducing transpirational load and the
571
abrasion of photosynehetic organs (sect. 3.3 below). Humidity is higher, reducing water
572
stress. Within one grass stratum, Liancourt et al. (2005) gave evidence of benefaction between
573
species in a calcareous grassland due to amelioration of water stress. Plant species differ in
574
their reaction on the microclimate (Castro et al. 1991) and in their response to microclimate
575
(Stoutjesdijk and Barkman 1992; Tretiach 1993). In extreme environments the presence of
576
one plant can allow another to survive.
577
In alpine and arctic habitats krummholz trees can shelter a shorter species from wind
578
desiccation, storm damage and wind-born ice particles (Marr 1977, Callaway 1998). Similar
579
subvention can occur amongst alpine herbs, possibly as a mutualism (e.g. Choler et al. 2001).
580
In arid and semi-arid areas tree shade has an obvious associated flora. Extensive
581
woody vegetation with isolated canopies can be an essential part of system function in warm
582
semi-arid climates, and often fine soil and organic matter accumulate below the canopy,
583
bearing a herbaceous flora. The association between nurse plants and their beneficients is
584
often so clear that no attempt is made to determine the precise environmental variable that is
Wilson & Agnew, chapter 2, Interactions, page 20 of 54
585
responsible, but it is generally assumed to be temperature combined with humidity (e.g.
586
Brittingham and Walker 2000). Temperature differentials are easy to demonstrate and very
587
well documented (e.g. Suzán 1996; Godínez-Alvarez et al. 1999), and in hot deserts with
588
summer rainfall cell death by high temperatures can be a critical factor in survival. This is
589
particularly important for succulents, which can suffer from heat load in full sun, being unable
590
to lose as much heat by convection as thin-leaved plants. Water loss is also a problem for
591
plants. Under shrub canopies, the litter ameliorates soil processes, increasing water-holding
592
capacity. Shrub nurse effects are sometimes attributed to nutrient buildup but Gómez-
593
Aparicio et al. (2005) found that in dry Spanish shrublands most of the effect was due to
594
canopy shade. Belsky et al. (1993 %143) have meticulously described the complex of
595
interactions in East Africa, while Holzapfel and Mahall (1999) carefully separated subvention
596
from interference between Ambrosia dumosa (white bursage) shrubs and annuals in the
597
Mojave. Amiotti et al. (2000) show that isolated Pinus radiata trees in Argentina have similar
598
effects. In a fascinating series of subventions in western Texas, Prosopis velutina (mesquite)
599
canopy allows the establishment of a Juniperus pinchotii (juniper), while J. pinchotii helps
600
the establishment of three other woody species with a more mesic distribution (Armentrout
601
and Pieper 1988; McPherson et al. 1988). Presumably there are more mesic conditions of
602
temperature and water relations under these canopies.
603
These are good examples of subvention that do not seem to be the result of co-
604
evolution.
605
3.3
Aerial leakage of nutrients
606
Nutrients such as nitrogen can be leached from canopy leaves and absorbed by the
607
leaves of other plants below (McCune and Boyce 1992; Cappellato and Peters 1995). This
608
interaction is difficult to categorise. Presumably one organism loses and the other gains,
609
almost by definition, as in predator/prey and parasite/host relations, except that there would
610
be leakage from the loser whether there was a recipient below or not. It seems best
611
categorised as benefaction.
612
3.4
613
614
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.
615
Bertness and Hacker (1994 %363) showed, by removing Juncus gerardii (a rush) from
616
a New England, USA, saltmarsh showed that its presence had raised the redox potential of the
617
soil and, by reducing evapotranspiration, kept down the soil salinity. Without this benefit, the
Wilson & Agnew, chapter 2, Interactions, page 21 of 54
618
associated Iva frutescens (marsh elder) died. Transplants of J. gerardii to the low and mid
619
zones of the marsh also benefited from the presence of J. gerardii and/or I. frutescens
620
neighbours because of lower salinities. However, transplants into higher zones in the marsh
621
were suppressed by the I. frutescens there, so this is a one-way subvention, benefaction rather
622
than mutualism.
623
3.5
624
Shelter from ultra-violet
In some species, ultra violet light (UV-B) damages cells and their photosynthetic
625
apparatus, so we might expect that plants could exhibit benefaction by UV-B shielding. This
626
could be stronger in alpine communities, with higher UV-B. The transmittance of UV-B to
627
lower strata differs with the canopy structure of different species (Shulski et al. 2004). Species
628
and ecotypes react differently to UV-B in growth rates (Dixon et al. 2001; Robson et al.
629
2003). All the components for a benefaction seem to exist, but we cannot find any evidence
630
that it exists in nature.
631
3.6
632
Protection from soil frost-heave
Ryser (1993) found that, of six species examined in limestone grassland in
633
Switzerland, two appeared to require shelter from neighbouring plants against frost heave as
634
well as drought.
635
3.7
636
Hydraulic lift
This is the process by which one species takes up water from deep layers in the soil
637
and releases it in the surface layer. In arid climates, woody rheatophytes with deep roots in an
638
aquifer could benefit species with shallow roots by this mechanism. Indeed, Facelli and
639
Temby (2002) show that Atriplex vesicaria and Maireana sedifolia (both Chenopodiaceae)
640
enhance the water relations of their surrounding annuals. However, they can also compete for
641
light, leading to a complex interaction. In a nice variant of the story, Yucca schidigera in the
642
Mojave Desert, with CAM photosynthesis, apparently redistributes soil water by creating a
643
higher upper-soil water potential during the day, rather than at night when it has open stomata
644
and a higher water demand (Yoder and Nowak 1999 %093). Surrounding non-CAM plants
645
with a high water demand must benefit. The phenomenon is also known in temperate forest
646
where Dawson (1993) and Emerman and Dawson (1996) have shown that Acer saccharum
647
(sugar maple) uplifts considerable quantities of water, much of which may be taken up by
648
understory plants from near the exuding tree roots. This phenomenon is benefaction or
649
possibly facilitation, and may be much more common that formerly supposed (Caldwell et al.
650
1998), but most authors stress that soil particle size and structure can be critical in the process.
Wilson & Agnew, chapter 2, Interactions, page 22 of 54
651
Roots can also distribute water to deeper soil layers (Ryel et al. 2003).
652
3.8
653
‘Talking trees’
Plants can often increase their content of defence compounds when grazed (see
654
below). It has been suggested that they can do this upon receiving a chemical signal such as
655
methyl jasmonate released by nearby grazed plants: the ‘talking trees’ mechanism. Although
656
early work was plagued by problems such as pseudoreplication, careful work has since
657
validated the effect (Karban et al. 2000). The remaining puzzle is whether it can be a product
658
of natural selection since it benefits the neighbours of a plant (genotype) producing the signal,
659
not the plant itself (Strauss et al. 2002). It could have evolved by kin selection (Wilson 1987
660
%493) or between-plant signals could be an accidental result of within-plant signalling
661
(Karbon and Maron 2002).
662
3.9
663
Subvention conclusion
One of the categories above is mutualism, and examples are well known between
664
plants and heterotrophs, for example in mycorrhizae. However, we have been able to discover
665
any examples of demonstrated mutualisms between two embryophytes. Awk sentence We
666
also note that the list above contains no clear example of facilitation. This suggests that
667
subventions may be accidents of evolution. We would expect this anyway. Plants do not rise
668
to the top of the interaction league table by being nice to others. Probably facilitation during
669
succession is a combination of mechanisms, for example an N-fixing and litter-accumulating
670
pioneer that is shaded out by subsequent species.
671
4 Litter: the necessary product
672
As we described in chapter 1 (sect. 1.1) the fundamental pattern in the natural history
673
of plants is that growth comprises the production of modules. The functional lifespan of these
674
organs, such as leaves and translocatory (vascular) tissue, is programmed and curiously short.
675
New organs and tissue must be produced, and discard of the old ones results in the production
676
of litter. The organs are mainly shed when dead, but some material is lost to the living plant
677
through damage while it is still living. All types of plant organ are included in litter,
678
especially leaves but also twigs, coarse woody debris (CWD, i.e. branches and whole trees)
679
and reproductive parts. Litter from roots and underground stems is deposited below ground
680
but remains in position and there is little evidence of its mediating plant interactions. The
681
proportion of total litterfall that is from reproductive parts varies, e.g. 16-24% in an NZ
682
podocarp/angiosperm forest (Enright 1999), 23% in a Mediterranean shrubland (Arianoutsou
Wilson & Agnew, chapter 2, Interactions, page 23 of 54
683
1989), versus a much smaller proportion in a tropical forest in India (Sundarapandian and
684
Swamy 1999).
685
686
687
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
688
689
or loess is being deposited,
690
 transport in surface floodwater, carried into rivers,
691
 fire. Even in the desert decomposition eventually happens
692
The two former fates are allogenic and do not impact on the plant communities that
693
delivered the litter. However, fire does so and is discussed below.
694
 When the climate and substrate are moist enough, litter can become peat. We deal with
695
this below. What about the range of conditions between these 2 extremes which would
696
include the majority ecosystems on the planet?
697
Litter plays a major part in the functioning of most ecosystems. We start with a description of
698
litter production and then deal with its effect on its neighbours. Litter production is most often
699
examined in ecological studies for its rôle in nutrient cycling (e.g. Orians et al. 1996). Here,
700
we focus on its other impacts on plant communities.
701
4.1
702
Litter can be of three kinds: Seems unnecessarily simple for the intended audience
703

704
705
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.
706
Such litter is almost always produced in pulses at predictable seasons. It comprises
707
mainly leaves, reproductive parts and root hairs (Larcher 1980; Osborne 1989).
708

Stochastic litter is shed by an allogenic disturbance (i.e. accidental damage) or by
709
pathogenic dieback, not initiated by the plant. Some types are produced irregularly,
710
though others are seasonal.
711
These types may differ in the ability that selection has to lead to adaptations in both the litter-
712
producing species, and the species on which the litter falls.
713
Standing dead litter
714
715
Exemplifying the effects of this type of litter, Bergelson (1990) demonstrated in a field
experiment that the seedling emergence of the annuals Senecio vulgaris (groundsel) and
Wilson & Agnew, chapter 2, Interactions, page 24 of 54
716
Capsella bursa-pastoris (shepherd’s purse) was very sparse where there was a high density of
717
dead Poa annua plants. Gleissman and Muller (1972) reported evidence that the dead fronds
718
of at least some ecotypes of Pteridium aquilinum (bracken) have suppressive effects on
719
underlying vegetation. On the acid forest floor in the uplands of northern Britain the grass
720
Deschampsia flexuosa is often dominant, with the litter consisting largely of D. flexuosa
721
remains (Ovington 1953). Regeneration of Quercus petraea (sessile oak) can be almost absent
722
in a wood with a developed D. flexuosa leaf-and-litter mat, in comparison to good
723
regeneration in other, nearby woods (Scurfield 1953). In this case the litter is mostly of dead
724
D. flexuousa leaves still attached to the plant, and these leaves form a thatch over the grass
725
tufts, shedding the oak leaf litter should this read “shading the oak seedlings and decreasing
726
regeneration”? Other litter effects on these acid forest floors are described below. However,
727
little has been published on the importance of abscission versus retention of dead material in
728
the functional ecology of plant communities. In many perennial herbs the vegetative shoots
729
collapse in winter but the dead flowering stems remain erect. The latter may have effects such
730
as channelling rainfall or acting as bird perches, with consequent input of nutrients and
731
disseminules.
732
Programmed litter
733
In this type, the organ being shed is usually disconnected by abscission, the result of
734
physiological processes endogenous to the plant and initiated some time before actual litter
735
fall occurs. Programmed litter is almost always pulsed by season (e.g. Arianoutsou 1989;
736
Enright 1999), exceptions being tropical figs (Nason et al. 1998) and ruderals in oceanic
737
climates. There can be several peaks of programmed litterfall during the year, often of
738
different types of a species’ replaceable plant organs (leaves, twigs, flowers, fruit, etc.) all
739
with their special phenology. Reproductive litter is always programmed. In masting species it
740
can be pulsed by year (Buck-Sorlin and Bell 1998) though not necessarily in a simple way:
741
the latter workers found that copious shoot shedding correlated with masting the following
742
year. As well as being temporally patchy, reproductive litter is also spatially patchy, for
743
example in some New Zealand forests it is greater near trees of Agathis australis (kauri;
744
Enright 1999).
745
The fall of leaf litter and other organs of photosynthesis such as cladodes and
746
phyllodes enough vocab already. Use the appropriate words, but there are places (like here)
747
where “big” words seemed be used to show that they can be. What is wrong with the words
748
leaves and petioles. is a pulse in almost all forests whether dominated by deciduous or
749
evergreen species. The number and amplitude of pulses each year depend on the phenology of
Wilson & Agnew, chapter 2, Interactions, page 25 of 54
750
the vegetation and its response to the environment. The pulse of falling leaves disturbs the
751
environment of the ground flora, and each species’ leaf litter has a characteristic pH, phenolic
752
content, breakdown rate and pattern of fall, depending upon its chemistry, specific leaf area,
753
leaf size and geometry. The effects of a litter pulse can be to change light and humidity at the
754
soil surface or to start nutrient cycling.
755
Programmed litter is usually lightweight and therefore easily dispersed. Sometimes it
756
is redistributed by wind and rain into deep patches, having a great local effect (Fahnestock et
757
al. 2000). This means that its time of impact at a point does not necessarily coincide with the
758
time of it falls (this applies to lightweight stochastic litter too). It can also be redistributed by
759
animals (Theimer and Gehring 1999), for example bird scratching can remove the litter load
760
locally, and permit germination of surface seeds. Branch fall (= branch shedding = limbfall =
761
cladoptosis) is programmed in some species. The process has been well described (Millington
762
and Chaney 1973) but its potential wider evolutionary and synecological significance appears
763
to have been overlooked. It involves well-defined cleavage zones, for example with a cork
764
band produced from a phellogen, usually in twigs and small branches but also in large (e.g. up
765
to 6 cm in diameter) branches of several years of growth. Branch fall can be seasonal, usually
766
in autumn but in a few species in spring (Millington and Chaney 1973). The fall of heavy
767
litter such as palm leaves and the branches of some conifers (Agathis australis: W.R. Wilson
768
et al. 1998) can be programmed to occur at a particular season and there can be in
769
considerable amounts (e.g. c. 800 kg ha-1 yr-1: Christensen 1975; Buck-Sorlin and Bell 1998).
770
Stochastic litterfall
771
Stochastic litterfall is that which is not programmed. Rather, it is caused or triggered
772
by storm damage, droughts, floods, geomorphological change, gravitational overload,
773
herbivore destruction etc.
774
Stochastic litter can be dead or alive. It includes leaves: 68% in the upland forest
775
studied by Shure and Phillips (1987). However, the lignified plant parts (twigs and CWD) are
776
often prominent, e.g. 46% of the litter recorded in an Amazonian rain forest (Chambers et al.
777
2000). Wardle (1984), in evergreen Nothofagus in New Zealand, found that twig fall
778
comprised about 30% of the litter. It can be very sizable in total: Buck-Sorlin and Bell (1998)
779
recorded 37,000 plant fragments from one oak tree in a year; the shoots were generally short
780
shoots not older than two years. Chambers et al. (2000) recorded 3.6 tonnes ha-1 yr-1 of CWD
781
(>10 cm diameter) in an Amazonian rain forest. Amounts are somewhat less in more open
782
forests in drier areas, for example in the order of 1-2 tonnes ha-1 yr-1, mostly leaves, for two
783
Eucalyptus savannahs in Queensland, Australia (Grigg and Mulligan 1999). Trees are
Wilson & Agnew, chapter 2, Interactions, page 26 of 54
784
continually shedding overtopped branches (Buck-Sorlin and Bell 1998). Broken dead trees
785
can also make a contribution, e.g. 7% in a boreal forest in Finland (Siitonen et al. 2000). In
786
many climates, epiphytes add appreciably to the litter fall, being 5-10% in old tropical cloud
787
forest in Costa Rica, where epiphyte fall is temporally sporadic (Nadkarni and Matelson
788
1992), and c. 5 % in Picea abies (Norway spruce) old-growth forests in Sweden, consisting of
789
lichens (Esseen 1985).
Fig. 2.5: The seasonal pattern of litterfall in an oakwood. After Christensen (1975).
790
791
By definition stochastic litterfall occurs less predictably than programmed litter, especially in
792
the case of CWD which falls mostly during storms. However, stochastic litterfall can be
793
pulsed by phenology, falling especially at the end of the life of a modular organ. It can also be
794
pulsed by a pest epidemic or short-term weather conditions. Such pulses occur sporadically
795
between years (Harmon et al. 1986) but sometimes with seasonal peaks related to storm
796
frequency (Fig. 2.5; Gentry and Whitford 1982; Brokaw 1982; Buck-Sorlin and Bell 1998).
797
Wardle (1984) found that in NZ Nothofagus it was seasonal, though less consistently so than
798
leaf fall. The time of the peak differed between Nothofagus species and also between sites,
799
usually but not always coinciding with the peak of litter fall. In Nothofagus menziesii (silver
800
beech) there was a double peak. Both Nadkarni and Matelson (1992) and Esseen (1985) found
801
the epiphyte fall to occur mainly in storms. There is a gradation from seasonal events to those
802
separated by decades or centuries. Even programmed branch fall can be partly stochastic, i.e.
803
influenced by the environment, such as that resulting from dieback after drought-induced
804
cavitation (Rood et al. 2000).
805
806
807
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%
808
of the forest floor (Zielonka and Niklasson 2001), the larger tree trunks taking up to a century
809
to decompose.
Wilson & Agnew, chapter 2, Interactions, page 27 of 54
810
811
4.2
Litter decomposition
The litter decomposition rate is obviously important because it sets the period during
812
which litter can have a mechanical and chemical effect, as well as driving nutrient cycling
813
(sect. 3.13 below). Decomposition depends on moisture, temperature, and the litter’s nutrient
814
and phenolic content. These are influenced by climate, soils and the identity of the littering
815
species. On a global scale climate affects decomposition rates more than do the characteristics
816
of the litter, with the fastest decomposition in warm, wet climates (Meentemeyer 1978), but
817
on a local scale litter nutrient and polyphenol content, and to some extent morphology, control
818
breakdown rates in conjunction with the water regime in each habitat (Osono and Takeda
819
2004). For example, the frequent occurrence of tannin-rich litter in heavily leached soils is
820
correlated with an increase in its polyphenol content which controls the release of nitrogen, so
821
important for decomposers (Northup et al. 1995). Further, Moorhead et al. (1998)
822
experimented with mycorrhizal nutrition in grassland of Bouteloua gracilis (grama grass) /
823
Schizachyrium scoparium (bluestem), and interestingly concluded that this community could
824
retard litter decay by reducing decomposer action in a nutrient-limited soil, since the grasses
825
could outcompete the decomposers for scarce nutrients.
826
Litter is broken down by a succession of microbial communities, involving
827
invertebrate shredders, commutators, fungi and mycotrophs, and bacteria (Cadisch and Giller
828
1997). If the litter is large and woody the process involves macrofauna. However, the
829
suberised exfoliating bark of Eucalyptus spp. trees in Australia is slow to break down, and
830
often needs destruction by fire (Canhoto and Graca 1999). Breakdown rates differ between
831
species and taxonomic groups, for example Cornelissen (1996) found within British regional
832
flora a rough correlation between “evolutionary advancement” and leaf decomposition rate,
833
But the slow breakdown of grasses (Poaceae) was anomalous, explained by their low base
834
status compared with the dicotyledons (except the Ericaceae) from that region. However, in
835
the study of Preston and Trofymow (2000) comparing species within one vegetation type
836
rather than an entire flora, grass litter decomposed the fastest and Fagus grandifolia
837
(American beech) the slowest. The rate is undoubtedly correlated with cellulose:lignin ratios
838
and mechanical characteristics of the leaves (Cornelissen and Thompson 1997).
839
There is some evidence that leaf litter combined from several species tend to
840
decompose faster than single-species litter (McTiernan et al. 1997; Wardle et al. 2002 %585),
841
reducing litter residence times and hence the disturbing effect of litter. Gartner and Cardon
842
(2004), reviewing the literature, found that enhanced decomposition in mixtures has been
843
found in 47% of cases reported. For example, Kaneko and Salamanca (1999) found that in
844
litter bags of species collected from a Quercus serrata (oak) / Pinus densiflora (red pine)
Wilson & Agnew, chapter 2, Interactions, page 28 of 54
845
forest in Japan, mixtures containing Sasa densiflora lost weight faster than expected from the
846
decomposition rate of their components. They suggested the effect may operate via the faunal
847
commutators. However, Wardle et al. (2006 %1052) conclude that effects of litter mixing on
848
decomposition and on fauna are not related. Perhaps this synergy holds only for certain types
849
of litter: Hoorens et al. (2002) suggested that the effect was due to the high N content of some
850
species which would speed the decomposition of their lower-N associates. However, they
851
found that while broad-leaved herb litter mixes (of legumes) decayed faster, there was no
852
effect when Sphagnum recurvum (=S. fallax) was mixed with Carex rostrata (beaked sedge).
853
4.3
854
Effects of litter
Litter must have a chemical effect as well as its physical one. In the case of CWD, the
855
physical effect overwhelms the chemical, but finer reproductive parts may have mainly a
856
chemical effect. Decomposition and leaching are both central to the nutrient cycling regime in
857
the plant community. Litter fall can affect community succession, facilitating it or redirecting
858
it. Deep persistent leaf litter can inhibit the invasion of later-successional species (Crawley
859
1997). In many communities, an increase in nutrient supply leads to dominance by a few fast-
860
growing tall species, and lower species richness (Willems et al. 1993). This has usually been
861
seen as due to competition, but it could equally well be due to the effect of litter (Berendse
862
1999). Litter can have differential effects on particular species and thus on their populations
863
within a plant community. Documentation has been particularly thorough in the case of leaf
864
litter (Table 1). For some of the effects listed in Table 1, opposite effects are seen in different
865
situations, depending on the depth of the litter, the affected species and the growth medium
866
(Hamrick and Lee 1987; Nilsson et al. 1999; Facelli et al. 1999). The effects of litter can be
867
classified as:
868
1. Direct mechanical effects
869
a. physical damage,
870
b. alteration in environment.
871
2. Chemical effects
872
a. leachates from litter,
873
c. control of nutrient cycling.
874
3. Complex environmental interactions
875
a. peat formation,
876
b. litter-herbivore interactions (sect. 6.5 below),
877
c. litter-fire interactions (sect. 6.5 below),
878
d. higher order interactions (sect. 6.5 below).
Wilson & Agnew, chapter 2, Interactions, page 29 of 54
879
All of these depend on the characteristics of the litter material and its phenology of production
880
as described above. In addition many of them require the litter to decompose slowly enough
881
to maintain a constant presence in the A0 top soil layer.
882
4.4
883
The direct mechanical effect of litter
The physical impact of litter, particularly on the forest floor, is very conspicuous, and
884
we discuss it below (sect. 5.4 below) as an autogenic disturbance.
885
4.5
886
Alteration in environment by litter
Litter also causes general environmental changes at the soil surface. Plant growth,
887
especially of herbaceous plants, must be suppressed by the low light under litter, but we have
888
not found any study on this. Red/far red (R/FR) ratios are reduced by a live canopy, then
889
sometimes by half again by the litter. This can suppress germination (Vazquez-Yanes et al.
890
1990) or increase it (Fowler 1986 %131). Litter might intercept and shortly evaporate rain,
891
reducing soil water content (Myers and Talsma 1992), but it can also reduce evaporation from
892
the soil itself (Eckstein and Donath 2005). The temperature regime at the soil surface can also
893
be affected (Fowler 1986 %131).
894
Whenever species of stiff, erect form, such as the grass Holcus mollis and Vaccinium
895
myrtillus, trap and accumulate tree leaves (e.g. of Quercus spp., oaks; or Fagus sylvatica,
896
beech), other plants including Deschampsia flexuosa are killed, as demonstrated by dead D.
897
flexuosa seen below such litter (Watt 1931; Ovington 1953). Watt (op. cit.) mimicked this by
898
laying a layer of beech leaves 5 cm thick; the D. flexuosa was killed. Watt suggested this
899
could not be due to allelopathy, because where taller D. flexuosa leaves occasionally projected
900
above the litter layer they grew well, and moreover Holcus mollis growth was much improved
901
by similar treatment. This can allow H. mollis to invade areas that had been dominated by D.
902
flexuosa (Ovington 1953; Scurfield 1953). No litter is built up by H. mollis, as its dead organs
903
rot too fast (Ovington 1953), so Quercus can establish in the tree litter, or amongst H. mollis,
904
once the D. flexuosa litter mat is removed (Watt 1931; Ovington 1953). Chapin et al. (1994)
905
suggest that in Glacier Bay successions Alnus sinuata (alder) suppresses Dryas drummondii
906
partly by the allelopathic effects of its litter, but as part of complex replacement interactions.
907
In forests in the mid west USA (Michigan and Wisconsin), hardwoods (e.g. Quercus rubra,
908
red oak) can dominate the mid-successional forest. In these stands, Tsuga canadensis
909
(hemlock) cannot invade, because its seedlings are unable to penetrate the hardwood litter,
910
whereas Acer saccharum (sugar maple) seedlings can, and it therefore invades (Rejmanek
911
1999).
Wilson & Agnew, chapter 2, Interactions, page 30 of 54
912
Subvention via litter can be very significant for particular species and, in some
913
temperate rain forests the seedlings of many trees depend on fallen trunks and CWD for their
914
establishment and hence regeneration (McKee et al. 1982; Agnew et al. 1993; Duncan 1993).
915
CWD has a characteristic development in old growth stands, and harbours a specialized, often
916
endangered, invertebrate fauna and bryophyte flora. Bryophytes are particularly vulnerable to
917
litter cover (Barkman et al. 1977; Oechel and Van Cleve 1986), especially in forest, where
918
litter is deposited by the herbaceous field layer as well as by woody vegetation. However,
919
During and Willems (1986) named five bryophyte species that they suggested “may thrive on
920
litter”. One possibility is that nutrients released from litter is taken up by bryophytes (Tamm
921
1964). In Scandanavian forests many species are dependent CWD for regeneration or growth,
922
including many bryophytes (Siitonen 2001).
923
4.6
924
Leachates from litter
It has been long suspected that leachates from litter affected germination and growth
925
of certain plant species. Early reports of this were concerned with crop residues (Kimber
926
1973) but then evidence came from natural plant assemblages. The case of the tree Celtis
927
laevigata (sugarberry) is the clearest (Turner and Rice 1975; Lodhi 1978). Bosy and Reader
928
(1995) investigated suppression of germination of four forbs by grass litter in an oldfield.
929
Germination of seeds of at least three of the species was markedly reduced under litter, and
930
for two species an appreciable component of the suppression could be explained by the
931
inhibitory effect of leachate. However, it is also possible for litter to subvent germination
932
(Xiong and Nilsson 1999), or to act as part of a cue for germination from the seed bank
933
(Preston and Baldwin 1999).
934
Allelopathy was discussed above. The allelopathic effect of litter leachates has long
935
been suspected and repeatedly tested. For example, Rutherford and Powrie (1993) showed
936
that leaf and litter leachates from the Australian Acacia cyclops (coastal wattle) affected the
937
small-leaved shrub Anthospermum spathulatum below it. Apparently leachates from both the
938
canopy and litter are implicated in many allelopathic effects. However, experiments are easier
939
in vitro than in the field, and only a few clearly demonstrate that litter allelopathic agents have
940
real effects in nature.
941
4.7
942
Control of nutrient cycling
Litter returns nutrients to the soil as mineral compounds or as organic compounds
943
which are then broken down to mineral ones. This is the well-known process of nutrient
944
cycling, but different litter types will differ. Berendse (1994a) found that in fast-growing
Wilson & Agnew, chapter 2, Interactions, page 31 of 54
945
species (i.e. with high RGRmax) less N was re-translocated to the living parts before the leaf
946
fell, and the resulting litter broke down quickly. Such species would be expected to
947
predominate in N-rich environments. In contrast, species with a low RGRmax re-translocated a
948
greater proportion of their leaf N before it fell. Such N-conserving species, with a low carbon
949
turnover, would be expected early in primary succession, when N is in short supply.
950
Berendse et al. (1987) later compared the deciduous Molinia caerulea (purple moor
951
grass) with the evergreen microphyllous woody shrub Erica tetralix (heath). M. caerulea lost,
952
during one year, 63% of the N present in the above-ground biomass standing at the end of the
953
growing season and 34% of its P. Comparable losses in E. tetralix were 27% and 31%,
954
respectively. This suggests that under nutrient-poor conditions the low-nutrient-loss E. tetralix
955
will be the dominant species, and that if nutrient availability increases M. caerulea will
956
replace it. There is some empirical support for this: in a similar system, Berendse et al.
957
(1994b) found that addition of nutrient solution caused Calluna vulgaris (a species
958
ecologically similar to Erica tetralix) to decline and cover of four grass species to increase.
959
The litterbag decomposition rates given for various species by Cornelisson et al. (1999) make
960
it clear that plants of later successional stages will have litter that is slower to decompose and
961
thus with a greater potential disturbance effect. These authors report from a wide ranging
962
survey an almost universal negative correlation between decomposition rate and herbivore
963
defence.
964
4.8
965
Peat formation
On wet substrates, if litter breaks down at a slower rate than it is produced peat will
966
build up. Peat is composed of plant remains in various stages of humification by a partial
967
organic hydrolysis of plant material mediated by micro-organisms (Fig. 2.6). Some types of
968
litter especially impede drainage to cause waterlogging. This yields humic colloids with
969
properties that restrict drainage and oxygenation and, being complex molecules bounded by
970
weakly acidic OH radicals, lower the pH of the soil solution. Nutrient availability and
971
oxygenation are reduced, which decrease litter production but decrease its decomposition
972
even more, so that peat accumulation increases yet more.
973
974
975
Wilson & Agnew, chapter 2, Interactions, page 32 of 54
976
977
978
979
980
981
982
983
984
985
986
987
988
989
990
991
992
993
994
995
996
997
998
999
1000
1001
1002
1003
1004
1005
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)
1006
or Sphagnum moss species.
1007
There are three routes to peat formation. In eutrophic or mesotrophic conditions litter
1008
production is high but decomposition is fast too, so peat will form only in still lakes, infilling
1009
them. This is a classic succession story (Walker 1970). Paludification often follows from this
1010
point. Peat can also form on the wet, nutrient-poor soils often caused by the leaching effect of
1011
high rainfall (Crawford 2000), a process known as paludification. There are two ways in
1012
which paludification can happen. Firstly, the species adapted to these conditions often bear
1013
leaves with a high polyphenol content, which slows decomposition and thus potential for
1014
paludification (Inderjit and Mallik 1997; Northup et al. 1998). This is a widespread
1015
phenomenon, having important effects on community structure. For example Ehrenfeld et al.
Wilson & Agnew, chapter 2, Interactions, page 33 of 54
1016
(1995) propose that small ericaceous shrubs trap litter in New Jersey pine savannahs,
1017
inhibiting decomposition and maintaining openings in the canopy, while Inderjit and Mallik
1018
(1997) provide experimental evidence for litter of Ledum groenlandicum (Labrador tea)
1019
limiting black spruce regeneration in Canada.
1020
The ultimate peat-forming process is the formation of an ombrogenous bog by
1021
isolation of the peat surface from its surroundings in water and nutrient supply (Klinger 1996,
1022
Anderson et al. 2003). This is effected by a guild of species which can absorb nutrients
1023
directly from rainfall, mostly bryophytes and particularly Sphagnum spp. and the restiad
1024
Empodisma minus (wire rush, Agnew et al. 1993), an odd flowering plant which has the same
1025
effect though its negatively geotropic root weft. This guild has, in common, cell walls with a
1026
cellulose-derived weak acid (uronic) that can scavenge ions from precipitation, yielding
1027
sufficient nutrients for annual growth and maintaining a high hydrogen ion concentration in
1028
the interstitial water. The effect is very well documented for Sphagnum spp. in temperate
1029
mires (Clymo 1963; Clymo and Hayward 1982; Koojiman and Bakker 1994). The rate of
1030
percolation, as seen in Darcy’s constant, is slowed by the peat formed. The waterlogging, low
1031
pH and low-nutrient conditions favour this guild. Malmer et al. (1994; 2003) suggest that since
1032
Sphagnum spp. can outcompete vascular plants under ombrotrophic conditions these
1033
conditions may arise rather suddenly. This is the state change expected when a switch is
1034
operating (chapt. 3, sect. 5 below). There are indeed records of such rapid state changes where
1035
Sphagnum spp. expansion has caused a brown moss fen to be replaced by bog (Kuhry et al.
1036
1993), destroyed forest (Anderson et al. 2003) and invaded forest around the edges of basin
1037
mires (Klinger 1996). The process may be initiated by climatic change to colder, wetter
1038
conditions (Korhola 1996).
1039
4.9
1040
Can reaction via litter evolve?
It is not enough to describe the processes that occur within plant communities; we
1041
should gauge whether these processes are accidental, or whether they could be the result of
1042
evolution. This is hardly in doubt for the other types of interaction discussed in this chapter –
1043
interference, subvention and autogenic disturbance—wasn’t it in question just a little before?
1044
– because the characters of the plant involved affect its fitness and hence the transmission of
1045
its genes to the next generation. The problem with litter is that it is by definition deceased
1046
plant tissue. As Clements (1904) pointed out, all plants react on their environment, but the
1047
extent and type of reaction will be genetically controlled. A particular reaction will evolve if it
1048
enhances the fitness of the individual plant (i.e. genet) more than it enhances the fitness of its
1049
conspecific neighbours, after taking into account any cost of reaction. However, litter affects
Wilson & Agnew, chapter 2, Interactions, page 34 of 54
1050
all the individuals and species in a community. In some cases it is produced when the whole
1051
plant dies, so the characters are expressed too late to affect whether the genes that caused
1052
them will increase or decrease. This is clearest in cases when the litter is produced when the
1053
plant dies or has its effect after the plant’s death, for example by paludification, by control of
1054
nutrient cycling, and as fuel for fire. There is then no possibility of plants enhancing their own
1055
fitness, in survival or fecundity, only that of their offspring (which will carry their genes. I
1056
don’t see why evolution can’t therefore act on litter).
1057
For effects that occur after the death of the plant we need to call on kin selection, with
1058
the mechanism that a plant benefits especially its neighbours, which are especially likely to
1059
carry the same alleles (Wilson 1987 %493). Another way of expressing this is selection
1060
through the extended phenotype. Northrup et al. (1998) commented that “decomposing leaf
1061
litter is not generally considered to be part of the plant’s phenotype” so that litter characters
1062
must evolve through selection on the extended phenotype. It has been remarked that just as
1063
selection in different areas with comparable environments but different species often produces
1064
similar solutions in terms of leaf characters, so similar solution in terms of reaction on the
1065
environment would be expected in different species and communities (Lewontin 1985;
1066
Mooney et al. 1977). The concept is that this reaction can lead to the evolution of secondary
1067
characters if an organism modifies its own environment, and the same induced environmental
1068
change is reimposed for sufficient generations to serve as a significant source of selection
1069
(Olding-Smee et al. 1996; Laland et al. 1996 1999)-community selection?. A different
1070
solution was proposed by Whitham et al. (2003), that traits of the extended phenotype could
1071
evolve because they affect the whole community and there could be selection between
1072
communities, a concept that most biologists find hard to swallow (but see D.S. Wilson 1997).
1073
However, most plants produce litter during their life and have an opportunity for that litter to
1074
affect their fitness, in which case Northup et al.’s argument does not apply. Still, there are
1075
problems with the idea that reaction via litter can evolve; litter effects seem to be a necessary
1076
by-product of growth.
1077
5 Autogenic disturbance: plants as disturbers
1078
Disturbances, marked changes in the environment for a limited period, often with the
1079
removal of plant material, are more common than was once believed and important for plant
1080
communities (White 1979; Rundel 1998; Grime 2001). The concept ‘autogenic disturbance’
1081
was coined by Attiwill (1994), though it is close to the ‘endogenous disturbance’ of White
1082
(1979). Most consideration has been of allogenic disturbance, i.e. that caused by external
1083
factors such as animals or extreme weather events. For example, Bazzaz (1983) describes
Wilson & Agnew, chapter 2, Interactions, page 35 of 54
1084
disturbance as continuous and necessary in all ecosystems, but discusses only allogenic
1085
causes. No less important, we suggest, are the minor disturbances within the community that
1086
inevitably result from the growth and death of plant parts, for example by plant contact and by
1087
litter (there seems little opportunity for autogenic disturbance by subterranean organs). Thus,
1088
vegetation, by its nature, disturbs itself. As we pointed out in chapter 1: “Plants move,
1089
animals don’t”. Autogenic disturbance has potentially positive and negative effects on
1090
population fitness and density, yet stands apart from the general considerations of interference
1091
and subvention described above. There is a wide range in the intensity of autogenic
1092
disturbances, from delicate adjustments resulting from leaf growth to the fall of a group of
1093
trees, but plants must tolerate all these effects. It may have profound bearing on vegetation
1094
dynamics. Autogenic disturbance may be more predictable than allogenic disturbances such
1095
as storms and earthquakes perhaps they are more predictable on a day to day basis, but over
1096
the course of an organism’s life, the probability of experiencing many allogenic disturbances
1097
is very predictable. I might not know whether or not I’m going to be hit be a storm tomorrow,
1098
but I do know that I will be hit by a storm in the course of my life. As the damage sustained
1099
by a storm or other allogenic dist can be much more severe shouldn’t all this (when combined
1100
with the plasticity issue commented on below) lead to a high level of selection on allogenic
1101
dist. related traits?, and if so selection for adaptation to it is more likely to occur. If plants can
1102
respond with plasticity to autogenic disturbance (as you suggest below) but not with allogenic
1103
disturbances, wouldn’t selective pressure be greater on allogenic dist. adaptations? However,
1104
autogenic and allogenic disturbance can interact.
1105
5.1
1106
Movement and contact
Even gentle contact between plants can affect their growth, producing effects such as
1107
reduced growth, reduced soluble carbohydrates and increased transpiration (van Gardingen
1108
and Grace 1991; Keller and Steffen 1995). For example, when Biddington and Dearman
1109
(1985) brushed Brassica oleracea var. botrytis (cauliflower) and Apium graveolens (celery)
1110
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 36 of 54
Control
Brushed
Fig. 2.5: The effect of brushing seedlings of Brassica oleracea for 1.5 min
day-1After Biddington and Dearman (1985).
1111
1112
Experimentally shaking the plant can have an even greater effect, e.g. reduced shoot
1113
extension, shorter and wider stems, lower shoot:root ratios, altered root development, shorter
1114
petioles, shorter flowering culms and reduced reproductive effort (Neel and Harris 1971;
1115
Braam and Davis 1990; Gartner 1994; Niklas 1998; Goodman and Ennos 1998). Whilst
1116
brushing with typing paper and shaking by hand are artificial treatments, they are very close
1117
to the leaves of adjacent plants brushing each other, or close trees rocking each other. The
1118
changes are mediated by the up-regulation of a large number of genes (Braam and Davis
1119
1990). Plants can also change position as a result of their own growth (Evans and Barkham
1120
1992), for example Salix (willow) trunks collapse due to their own weight in wet carr forest
1121
(Agnew, pers. obs), and shrub stems can be bent by their own weight and fall to the ground
1122
(B.F. Wilson 1997).
1123
5.2
1124
Growth thrust
Shoots can thrust each other aside physically as they grow (Campbell et al. 1992). For
1125
example, the leaves of Juncus squarrosus are vertical when they first emerge, but they then
1126
become horizontal, form a rosette and press down surrounding plants (authors pers. obs.) as
1127
do leaves of Plantago species (Campbell et al. 1992). Surprisingly little is known of this
1128
process.
1129
Secondary growth of tree trunks, branches and roots continually creates new habitat,
1130
initiating succession by providing opportunities for colonisation. Circumferential branch
1131
growth produces new sites for the establishment of epiphytes. Some bryophyte species are
1132
tree-base specialists (Ashton and McCrae 1970). Their specialisation is perhaps explicable by
1133
their greater shade tolerance (Hosokawa and Odani 1957) and the peculiar characteristics of
1134
trunk water flow creating a damper, more nutrient-rich environment, but this is also the zone
1135
where the fastest circumferential growth occurs. Circumferential growth of tree roots can
Wilson & Agnew, chapter 2, Interactions, page 37 of 54
1136
affect the environment above the surface: woody roots near the soil surface create shallow
1137
soils and diversify the forest floor habitat (Agnew pers. obs.). The reader may like to take the
1138
‘pers. obs’ in this section as confirmation that autogenic disturbance has not received due
1139
attention in ecological research.
1140
5.3
Crown shyness
1141
Crown shyness comprises gaps between the canopies of adjacent trees (Jacobs 1955),
1142
probably caused by abrasion in the canopy (Putz et al. 1984 %24). Franco (1986) observed
1143
the process, reporting that when branches of Picea sitchensis (Sitka spruce) and Larix
1144
kaempferi (Japanese larch) met physical damage occurred by abrasion, causing the death of
1145
the leading shoots. New shoots arising from lateral buds and were also killed. Sounds like
1146
competition for space to meLong and Smith (1992) demonstrated the mechanism by fixing
1147
wooden pickets into the canopy as artificial branches: they were broken back to the edge of
1148
the crown, due to wind-rock and consequential abrasion. Tall slender trees were subject to
1149
greater wind-rock, and thus greater frequency of impact with neighbouring crowns, leading to
1150
greater crown shyness. Putz et al. (1984 %24) measured swaying of Avicenna germinans
1151
(mangrove) and found that branches bordering crown shyness gaps generally had broken
1152
twigs and few leaves. Flexible crowns were more widely spaced than still crowns, confirming
1153
the observation of Long and Smith (op. cit.). These effects are the result of the compulsory
1154
growth and movement imposed by the modular construction of plants (chapt. 1, sect. 1.1
1155
above).
1156
5.4
1157
Growth and gravity
CWD clearly has the potential to be very destructive on the forest floor. The most
1158
destructive type of stochastic litter is tree fall, which is the autogenic disturbance par
1159
excellance and implicated in all demographic processes in forests of mixed canopy species. It
1160
appears to be a normal, predictable event in many undisturbed stands, which can be measured
1161
and built into models of species and biomass turnover in boreal (e.g. Hofgaard 1993), tropical
1162
evergreen (e.g. Chandrashekara and Ramakrishnan 1994) and tropical rain forests (e.g.
1163
Kellman and Tackaberry 1993).
1164
The weight in a tree’s canopy can eventually result in its fall, obviously disturbing
1165
surrounding plants. In a forest the upper canopy trees are more likely to fall, having reached
1166
their greatest potential and being too heavy for their root support or too loaded with
1167
lianas/epiphytes (Strong 1977; Putz 1995). Tree fall is associated with storm damage,
1168
particularly in mid-latitudes (e.g. Busing 1996, Allen et al. 1997). Understorey trees are more
Wilson & Agnew, chapter 2, Interactions, page 38 of 54
1169
likely to become standing dead, since pathogens or light reduction by neighbours (self-
1170
thinning) can kill, whether or not the tree still has the potential to grow further, and they are
1171
not as exposed to storm damage as are the canopy species. An exception occurs in the dry
1172
Kysna (South Africa) forest, where most canopy trees die in situ due to “competition,
1173
senescence and secondary pathogens” and gradually break up (Midgley et al. 1995). There is
1174
not enough evidence to suggest this as a general feature of any forest types.
1175
In old-growth forest, tree fall is the usual process that forms canopy gaps. In gap
1176
formation, several sudden environmental changes take place. The most important is that the
1177
forest floor is brightly lit with light of a very different spectral quality. The effects of a gap
1178
are not all positive: Lovelock et al. (1998) found photoinhibition of shade-tolerant juveniles in
1179
gaps, especially in species with short-lived leaves. Another, often overlooked, factor is
1180
rainfall/hydrology. A full canopied forest evaporates up to 40% of incoming rainfall and the
1181
soil is seldom at field capacity, but gaps receive the rain uninterrupted. There is also soil
1182
disturbance, with soil exposed in a root pit and adjacent root plate mound. The bare soil and
1183
higher light allow secondary species to invade, as observed by Ellison et al. (1993) in
1184
neotropical forest, and Narukawa and Yamamoto (2001) for Abies spp. (fir) seedlings in
1185
boreal and subalpine Japan.
1186
Branches can also cause severe impact when they fall (sect. 3.9 above). For example,
1187
in the tropical liana Connarus turczaninowii in Panama, 20-45% of the mortality of young
1188
plants is caused by branch fall (Aide 1987); in a tropical rain forest in Amazonia, Uhl (1982)
1189
found the most common (38%) cause of death in small (1-10 cm dbh) trees to be a branch fall
1190
or treefall; in Costa Rican rain forest, Vandermeer (1977) found that 46% of seedling deaths
1191
were due to falling leaves or branches, about half of these were due to falling palm fronds.
1192
Gillman and Ogden (2001 %671) found in Podocarp/angiosperm forest in northern North
1193
Island, NZ, that 10-20 % of the annual seedling mortality was caused by litterfall.
1194
5.5
1195
Lianas
Lianas can be so abundant in the canopy of many tropical and sub-tropical forests that
1196
they compete with the emergent trees (Lowe and Walker 1977). Treefall, with its associated
1197
disturbance to the forest floor, can be generated by either adherent lianas (e.g. Hedera helix,
1198
ivy) or free-swinging lianas (e.g. Ripogonum scandens, supplejack). Phillips et al. (2005
1199
%1250) found that in an upper-Amazon tropical rain forest large trees were three times as
1200
likely to die if they were invested by lianas. The resulting canopy gap can also benefit lianas.
1201
Needing less investment in support they can extend fast and keep pace with the fast-growing
1202
secondary species filling the gap.
Wilson & Agnew, chapter 2, Interactions, page 39 of 54
1203
Twining or tendril lianas can constrict the host stem (Lutz 1943; Clark and Clark
1204
1991; Matista and Silk 1997). Usually there is little active strangulation, but the liana stays
1205
put and the tree grows, which can produce deformations in the trunk and lead to changes in
1206
the vascular tissue and the wood fibres ((Falconer 1986; Reuschel et al. 1988; Putz 1991).
1207
Sometimes new conducting tissue is formed parallel to the constriction, but constriction can
1208
inhibit or even stop downward translocation of organic solutes (Lutz 1943; Putz 1991,
1209
Hegarty 1991). The constriction can also be a point of weakness, at which a branch or young
1210
stem is more likely to break (Lutz 1943; Uhl 1982; Putz 1991). Deformed trees are also more
1211
susceptible to pathogens (Putz 1991). Not infrequently the tree dies (Lutz 1943; Clark and
1212
Clark 1991; Uhl 1982).
1213
In the tropics, epiphytes, lianas and trees are often not distinct categories. Many
1214
genera in the Araceae (Monsteroideae) start as lianas but can maintain themselves as
1215
epiphytes without contact with the forest floor. We have found no record of an epiphyte being
1216
associated with tree or branch fall, although their contribution to litter fall has been well
1217
documented (see above). Strangler epiphytes certainly damage trees (Richards 1996). The
1218
epiphyte species involved are evergreen; many are in the genus Ficus (fig) and curiously
1219
revered by the indigenous people (F. benghalensis in Hindustan, F. natalensis in Kenya).
1220
Such stranglers begin life as epiphytes, gradually extend aerial roots downwards, eventually
1221
root in the soil, then grow around their host as a tree. The host usually dies, and does so
1222
standing, though the cause of the host’s death is not clear (Richards 1996).
1223
The interactions between support and liana are complex. Lianas are often supported by
1224
more than one tree (with a record of 27 trees for one liana on Barro Colorado Island, Panama:
1225
Putz 1984 %1713). This causes interdependence between trees that may stabilise canopy trees
1226
adjacent to treefalls (Putz 1984 %1713; Hegarty 1991). However, a corollary is that if such a
1227
connected tree falls, it damages more trees. For example, Putz (1984 %1713) found on Barro
1228
Colorado Island that 2.3 trees fell with each gapmaker, often ones that shared lianas. Liana-
1229
laden trees can also pull branches off neighbouring trees as they fall (Appanah and Putz
1230
1984).
1231
6 Plant-plant interactions mediated by other trophic levels
1232
While a macrophyte remains sedentaryi, its environment is changing, especially with
1233
respect to the various sets of organisms utilising the carbon energy source that it represents.
1234
These include herbivores, parasites and pathogens, all capable of modifying a plant’s fitness
1235
and therefore its competitive ability. There is also the potential for various combinations of
1236
heterotrophs and neighbouring plants to build complex nexus of inter-relationships. In most
Wilson & Agnew, chapter 2, Interactions, page 40 of 54
1237
cases these interactions are associated with a "patch effect", which works only if one species
1238
is sufficiently abundant in a local vegetation patch to change the behaviour of the herbivore or
1239
pollinator.
1240
6.1
1241
Below-ground benefaction
It is generally assumed that species with root nodules that contain nitrogen-fixing
1242
micro-organisms enhance the nitrogen economy of associated non-nodulating plants. These
1243
N-fixing plants are therefore held to be important in ecosystems and particularly in rangelands
1244
(Paschke 1997). However likely the transfer is, it is rarely proven. Kohls et al. (2003) set out
1245
to investigate this link in the well-studied site of Glacier Bay, Alaska. Using Δ15N values they
1246
concluded that nodulated plants accounted for most of the fixed N in soils and plants for up to
1247
40 years of succession; most of this being donated to the ecosystem by Alnus viridis (green
1248
alder). The assumption that fixed nitrogen is indirectly passed from nodulated to un-nodulated
1249
plants is probably justified in many cases.
1250
Common mycorrhizal networks (CMNs) link individuals below ground so that
1251
nutrient and carbon transfers have the potential to enhance or depress plant growth. In all
1252
three major types of mycorrhiza – vesicular-arbuscular, ectotrophic and ericoid/epacrid –
1253
some of the fungal species involved can infect more than one plant species (Simard and
1254
Durall 2004). The vesicular-arbuscular and ectotrophic ones are known to establish fungal
1255
networks that connect the roots of different species, and this may be true for the
1256
ericoid/epacrid type too (Cairney and Ashford 2002). It has been suggested that CMNs affect
1257
the performance of plants (e.g. Booth 2004). However, it is unclear whether plant-tissue to
1258
plant-tissue transfer of carbon actually occurs (Simard and Durall 2004). There has never
1259
been a convincing demonstration of it, certainly not to a degree sufficient to benefit the plant.
1260
In cases where carbon has been traced by radioactivity to the recipient it is likely that it is
1261
retained in the fungal hyphae, not in the plant tissues (Robinson and Fitter 1999).
1262
Similar transfers could operate in mineral nutrients. However, Newman and Ritz
1263
(1986) and Newman and Eason (1993) carefully monitored the transfer of 32P and concluded
1264
that any direct transfer via hyphal links was very minor, and too slow to substantially
1265
influence the nutrient status of the plants. There is evidence for greater nitrogen transfer when
1266
mycorrhizae are present but it is not clear whether the transfer is through the CMN or whether
1267
the mycelia increase release of N from one plant into the soil and/or uptake by the other plant.
1268
Moreover, ideas that this would even out concentrations between plants do not stand up: He et
1269
al. (2005 %897) found that there was net transfer from Eucalyptus maculata (gum) to
1270
Casuarina cunninghamiana (sheoke). This represents transfer from a plant that is not N-
Wilson & Agnew, chapter 2, Interactions, page 41 of 54
1271
fixing, to one that is N-fixing and had close to double the N concentration in its tissues. This
1272
transfer was at very low rates, but the benefaction was in the opposite direction from that
1273
usually assumed between fixing and non-fixing plants.
1274
Roots and microbial activity in the soil are intimately linked, since roots provide the
1275
most of the carbon source below ground. Chen et al. (2004) used microcosms to show that
1276
Pinus radiata roots increased microbial activity and the mineralisation of organic P. There
1277
was evidence that root exudates were responsible for these effects. It is possible that the plant
1278
can obtain N from free-living N-fixing bacteria in the same way. That these effects are species
1279
specific was demonstrated by Innes et al. (2004), who found that the grasses Holcus lanatus
1280
(Yorkshire fog) and Anthoxanthum odoratum (sweet vernal) could stimulate microbial
1281
activity, whereas dicotyledonous forbs depressed it. The effect was only seen in soil of higher
1282
fertility.
1283
6.2
1284
Pollination
When fruit set is limited by pollen, plants of the same or different species can interfere
1285
with each others’ reproduction by competing for the service of pollinating animals (Grabas
1286
and Laverty 1999). When pollen from another species lands on a stigma it may interfere with
1287
the germination or fertilisation of the species own pollen by occlusion or allelopathy (Murphy
1288
and Aarssen 1995a). This can reduce seed set and increase self-fertilisation (Bell et al. 2005).
1289
Plants can also compete for animal dispersers (Wheelwright 1985).
1290
There can be subvention too if one species attracts pollinators to the vicinity of
1291
another by being more attractive (a ‘magnet species’) or by mimicry (Laverty 1992). Moeller
1292
(2004) found that among Clarkia xantiana (an annual in the Onagraceae) populations in
1293
California there were more pollinating bees and less pollination limitation in populations with
1294
a greater number of congeners, implying that the mass of plants of the same pollination type
1295
attracted pollinators. An interaction that we can count as a genuine mutualism between
1296
embryophytes was demonstrated by Waser and Real (1979). If species have staggered
1297
flowering times with shared pollinators and some overlap in flowering time, there will
1298
probably be some competition for pollinators. However, the continuous availability of flower
1299
rewards over the period may maintain pollinator populations. Waser and Real gave evidence
1300
from flower numbers, fecundities and pollinating hummingbird numbers across four years at a
1301
site in the Rocky Mountains, Colorado, that the earlier-flowering Delphinium nelsonii was
1302
benefiting the later-flowering Ipomopsis aggregata thus. If we consider the maintenance of
1303
hummingbird populations from one year to the next, I. aggregata could be benefiting D.
1304
nelsonii in a similar way, forming a genuine mutualism.
Wilson & Agnew, chapter 2, Interactions, page 42 of 54
In an interesting study assessing the decoy function of sterile teratological “flowers”
1305
1306
on Arabis holboellii (rock cress) caused by the rust Puccinia monoica, Roy (1996) showed
1307
that the mass flowering of mixtures of A. holboellii and Anemone patens attracted more bee
1308
visits to the latter. During bee visits the sticky pseudoflowers of A. holboellii removed pollen
1309
derived from the A. patens stamens and replaced it with fungal spermatia which reduced seed
1310
set in the A. patens. This is a complex interactive system that shows the potential for fertility
1311
interference effects, whether via pathogens or pollen vectors.
1312
6.3
1313
Herbivory
Herbivores can remove large amounts of plant material and this must affect the plant
1314
community. The word herbivory suggests grazing, with mammals biting off whole leaves, but
1315
most herbivores are invertebrates, and these maintain their trophic pressure more consistently
1316
and more specifically than the vertebrates. Contrary to the situation with vertebrates,
1317
invertebrate herbivore pressure can be as great below-ground as above-ground (Brown 1993;
1318
Wardle 2002). They can be very much smaller than their substrate, giving large populations.
1319
With fast reproduction this can allow efficient selection to overcome plant defences and
1320
specialise on particular plant species. Invertebrate herbivores have parasites and carnivores
1321
that control them. There are therefore complex systems affecting plant population fitness
1322
through herbivory, but since the observation of both the herbivory and the effect on the plant
1323
are difficult, we know little about the effects of invertebrates on the balance between co-
1324
occurring plant species and hence on community structure.
1325
Herbivores are always selective to some degree. However, the degree of
1326
discrimination varies widely. Many Lepidopteran larvae feed on only one species of plant,
1327
e.g. Tyria jacobaeae (the cinnabar moth) on Sencio jacobaea (ragwort). At the other extreme,
1328
many large non-ruminant animals such as Loxodonta africana (African elephant), even
1329
though they have preferences, will readily eat a wide range of species. More importantly,
1330
some such as Equus spp. (horses) often graze finely-patterned vegetation at a relatively coarse
1331
scale, necessarily taking in species with a range of palatability. We can see the causes of
1332
differential palatability of plants most clearly within species, e.g. cyanogenesis for
1333
Gastropoda (slugs; Jones 1966), smell and visual appearance for Atherigona soccata (a shoot
1334
fly; Nwanze et al. 1998), concentrations of nonstructural carbohydrates, sodium, iron and
1335
mercury for Sciurus aberti (a squirrel; Snyder (1992) and cineole in the leaf terpenoids for
1336
Anoplognathus spp. (Christmas beetles; Edwards et al. 1993). The relative palatability of
1337
species will be affected by a complex of such characters.
1338
Differences in palatability can affect the type of interaction between species. A plant
Wilson & Agnew, chapter 2, Interactions, page 43 of 54
1339
of target species S can be positively or negatively affected if conspecifics are replaced by
1340
plants of another species (analogously to a replacement comparison in interference, R below),
1341
or they can be affected positively or negatively by the presence of a neighbouring plant
1342
species when a herbivore moves into the patch (comparison A below), both by several
1343
mechanisms:
1344
positive:
1345
(1) the neighbour repels the herbivore, reducing the herbivory load on S (R)
1346
(2) the neighbour attracts the herbivore’s enemy, reducing the herbivory load on S
1347
1348
1349
1350
1351
(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)
1352
(5) the neighbour attracts the herbivore, diverting the herbivory load from S (A)
1353
(6) the herbivore removes a more palatable, interfering, neighbour of S (A)
1354
(7) The herbivore defends S against a an interfering neighbour (A)
1355
negative:
1356
(8) the neighbour attracts the herbivore, increasing the herbivory load on S (A or R)
1357
(9) the herbivore removes a more palatable beneficient neighbour of S (A)
1358
(10) induced defences against herbivory in the neighbour divert the herbivore to S (R)
1359
(1) +ve: The neighbour repels the herbivore, reducing the herbivory load
1360
The repelling of herbivores by a neighbour (Augner 1994) affects plant communities
1361
at the scale which the repulsion occurs. For example, a spiny shrub deters the herbivore from
1362
consuming any other species within its canopy. A recognisably unpalatable species in a grass
1363
sward deters herbivore from taking its bite at that point, sparing any palatable species growing
1364
closely with it. As examples among mammalian browsers/grazers, Hjältén et al. (1993 %125)
1365
found that when Betula pubescens was associated with the less palatable Alnus incana (alder)
1366
the herbivores Microtus agrestis (voles) and Lepus timidus (hares) avoided those patches and
1367
B. pubescens suffered less herbivory damage, and Oesterheld and Oyarzábal (2004) found
1368
that plants of the palatable grass Bromus pictus tended to occur within one of the unpalatable
1369
tussocks. The avoidance of a less preferred patch would be part of an “extended phenotype”
1370
of the neighbour species, but confer benefit on all the plants in that community, as we have
1371
discussed above. Tuomi et al. (1994) suggested that the evolutionarily stable strategy would
1372
be for such benefit to conspecific neighbours to limited, or an undefended (‘selfish’) genotype
Wilson & Agnew, chapter 2, Interactions, page 44 of 54
1373
would too readily invade, and they suggested that plant defences should therefore deter the
1374
herbivore without killing it.
1375
Chemicals from a species might repel insects not only from that species but also from
1376
their neighbours. This is widely discussed as a goal of organic gardeners, but good evidence is
1377
hard to find. Tahvanainen and Root (1972) found that planting Lycopersicon esculentum
1378
(tomato) amid Brassica oleracea (collards) plants decreased flea beetle populations on B.
1379
oleracea and increased its plant weight. In a choice experiment, adult flea beetles (Phyllotreta
1380
cruciferae) preferred excised B. oleraceus leaves with no tomato mixed in with them, which
1381
is evidence of the involvement of a repellent chemical. It is widely suggested that some
1382
Tagetes species (African marigold), as companion plants, repel insect pests and thus benefit
1383
other plants in the crop. There is a little firm evidence for this (McSorley and Frederick 1994;
1384
McSorley and Dickson 1995), but nematodes, below-ground, may be mediating the
1385
interaction, apparently not due to any chemical coming from the Tagetes sp. plants (Ploeg and
1386
Maris 1999).
1387
(2) +ve: The neighbour attracts the herbivore’s enemy, reducing herbivory load
1388
White et al. (1995 %1171) found that planting Phacelia tanacetifolia, which was
1389
attractive to hover flies probably for its pollen, around Brassica oleracea (cabbage) patches
1390
(the control was bare ground around the patches) reduced the density of Brevicoryne
1391
brassicae and Myzus persicae (both aphids) on the B. oleracea.
1392
(3) +ve: Defences against herbivory are induced in the neighbour
1393
It is well established that herbivore attack, or leaf damage mimicking herbivory, can
1394
induce in a plant chemical defences such as alkaloids, nicotine, phenolics and tannins (e.g.
1395
Boege 2004, Vandarn et al. 2000), and even morphological defences (e.g. Young et al. 2003).
1396
In most cases, there is a fitness cost of this induced defence, for example in growth rate (Strauss
1397
et al. 2002). One would expect a reduced interference ability this is not the same as inducing
1398
defences in the neighbor, benefiting neighbours, and Baldwin and Hamilton (2000 %915)
1399
produced some evidence of this, but only intra-specifically. In order for this to operate, the
1400
herbivore has to select between species at a small scale: to be exact, inside the neighbourhood
1401
within which interference occurs.
1402
(4) +ve: The neighbour attracts the herbivore, which creates open ground
1403
Hoof marks are the preferred microenvironment of some species (Csotonyi and
1404
Addicott 2004). This does not depend on the herbivore’s having any selection between
1405
species or selecting at any particular spatial scale.
1406
(5) +ve: The neighbour attracts the herbivore, diverting the herbivory load
Wilson & Agnew, chapter 2, Interactions, page 45 of 54
1407
This is theoretically possible, and Atsatt and O’Dowd (1976) mention some possible
1408
examples. Mensah and Khan (1997) found that Medicago sativa (lucerne), which has a higher
1409
palatability in choice experiments to divert Creontiades dilutus (a mirid) pests from a crop of
1410
cotton. There was a dramatic effect over the four-month season. However, we can find no
1411
evidence from natural systems. The effect would be only temporary, because the herbivore
1412
population would build up on the neighbour, and probably then increase the herbivory load on
1413
the target.
1414
(6) +ve: The herbivore removes a more palatable, interfering neighbour
1415
If an interfering neighbour is palatable, herbivory could reduce interference from it,
1416
allowing increased growth of the target. This is the principle: “my enemy’s enemy is my
1417
friend”. It is remarkably difficult to find evidence for this. Part of the reason may be the
1418
difficulty of obtaining estimates of relative palatability, but confounding effects of the
1419
herbivore such as creating gaps and species-to-species tradeoffs such as between palatability
1420
and regrowth ability are other reasons (Bullock et al. 2001 %253). However, Cottam (1986)
1421
grew the grass Dactylis glomerata (cocksfoot) with the more palatable Trifolium repens
1422
(white clover). When there was no grazing D. glomerata suffered in mixture, dying out after
1423
120 days of grazing, but when there was grazing by Deroceras reticulatum (slug),
1424
D. glomerataii, grew as well as, or better than, in monoculture. Carson and Root (2000), in a
1425
very careful experiment, applied insecticide experimentally in an oldfield dominated by
1426
Solidago altissima and S. rugosa (goldenrods). It became clear that in the untreated
1427
community specialist Microrhopala spp and Trirhabda spp (chrysomelid beetles) were
1428
suppressing the Solidago spp and thus allowing increased growth of other forbs and of woody
1429
seedlings. As with other mechanisms involving release from interference, the herbivore must
1430
select between species at a fine scale.
1431
(7) +ve: The herbivore defends against an interfering neighbour
1432
Ants are often associated with plants. For example, Macaranga is an old world genus
1433
in the Euphorbiaceae (often conspicuously part of secondary forest) some of whose species
1434
bear extra-floral nectaries which attract ants and domatia hollows which shelter them. The
1435
relationship is close and complex. Fiala et al. (1989) found that on trees of Macaranga spp. in
1436
Malaya ants considerably reduced the amount of herbivory damage, mainly by forcing
1437
lepidopteran larvae (caterpillars) off leaves, and possibly by harassing Coleoptera (beetles)
1438
and Acrididae (grasshoppers). The ants involved are generalist predators often in the genus
1439
Crematogaster, yet they also seemed to protect against lianas: Macaranga species that were
1440
myrmecophytic had far fewer lianas attached, and this difference was seen only with plants
Wilson & Agnew, chapter 2, Interactions, page 46 of 54
1441
occupied by ants. The effect was caused by the ants biting the tips of invading liana, and
1442
Federle, Maschwitz and Holldobler (2002) showed that they also pruned adjacent tree species
1443
reducing canopy contact and presumably also competition.
1444
(8) -ve: The neighbour attracts the herbivore, increasing the herbivory load
White and Whitham (2000) found that Populus angustifolium  fremontii
1445
1446
(cottonwood) plants growing under the highly palatable Acer negundo (box elder) suffered
1447
much more herbivory from the insect Alsophila pometaria (fall cankerworm) than those under
1448
their own species or in the open. Sessions and Kelly (2002) suggested that the grass Agrostis
1449
capillaris (bent) created a moist habitat suitable for Derocerus reticulatum (a slug) that then
1450
attacked a nearby fern (Botrychium australe). Mechanism ‘8’ can operate at any spatial scale
1451
and the herbivore does not need to be selective so long as it is attracted to the patch by one
1452
species. It seems to be the situation to which the strange term ‘apparent competition’ has been
1453
applied. The term ‘magnet species’ for the neighbour is more helpful.
1454
(9) -ve: The herbivore removes a more palatable, subventing neighbour
1455
This is a theoretical possibility, but we know of no example. As with mechanisms
1456
involving competitive release, the herbivore must select at a fine scale.
1457
(10) -ve: Induced defences in the neighbour divert the herbivore to the target
1458
Induced defences are now known in many species, which could protect that species
1459
but not a neighbour. We do not know of any explicit examples of this.
1460
6.4
1461
Indirect impacts of diseases
For some of the mechanisms of positive plant-plant interactions via herbivores that we
1462
discussed above, such as ‘2’, ’4’ and ‘7’,it is hard to envisage analogues for fungal or viral
1463
diseases. However, others seem possible. The neighbour could repel viral vectors such as
1464
aphids (Birkett et al. 2000), reducing the disease load on S, the equivalent of herbivory
1465
interaction ‘1 +ve’ above. Defences against fungal diseases are often induced in the host, and
1466
these might carry a cost (though the evidence for this is weak), reducing the host’s
1467
competitive ability against S (cf. herbivory ‘3 +ve’). The effect (translating to disease terms)
1468
“5 +ve: The neighbour attracts the fungus, diverting the load from S”, could be applied when
1469
a neighbour had a strong ‘fly-paper effect’, trapping fungal spores (chapt. 4, sect. 4.3, below).
1470
Disease could remove a more susceptible neighbour that normally interferes with S
1471
(cf. herbivory ‘6 +ve’). For example, the introduction of the Asian pathogen Cryphonectria
1472
parasitica (= Endothia parasitica; chestnut blight fungus) to forests of northeastern USA led
1473
to almost complete death of the dominant Castanea dentata (chestnut) trees. In one area this
Wilson & Agnew, chapter 2, Interactions, page 47 of 54
1474
resulted within c. 14 years to a doubling of the basal area of Quercus rubra (red oak) and a
1475
threefold increase in Quercus montana (Chestnut oak) (Korstian and Stickel 1927). Almost all
1476
the other tree species increased slightly. In other areas different species took advantage of the
1477
released resources.
1478
A neighbour could be very susceptible to the disease, and, whilst not quite being a
1479
magnet, it could spread spores or vectors and increase the disease load on S. For example,
1480
Power and Mitchell (2004, %79) found in a field experiment with plots of 1-6 grass species
1481
that plots containing Avena fatua (wild oats), which was highly susceptible to a particular
1482
generalist aphid-vectored virus, were over 10 × more heavily infected than communities
1483
lacking A. fatua. They termed this ‘pathogen spillover’, but it is a close equivalent of our
1484
herbivore situation “8 -ve: The neighbour attracts the [disease], increasing the [disease] load”.
1485
For those wishing to use the term ‘apparent competition’, it is the disease equivalent.
1486
Possibly, the disease could removes a more susceptible neighbour that a facilitator of S
1487
(herbivory ‘9 -ve’). An equivalent to herbivory mechanism ’10 -ve’ seems just possible.
1488
The impact of diseases is seen most obviously when they appear suddenly, as in the
1489
case of chestnut blight. We can be fairly sure that diseases in the past have had a major hand
1490
in shaping the plant communities that we see today and continue to. (Janzen scatter
1491
hypothesis?)
1492
7 Interactions
1493
7.1
1494
1495
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
1496
removal of photosynthetic organs and because leaves have a lower probability of
1497
reaching senescence,
1498
1499
1500
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
1501
tearing of edges of leaves that have been bitten, etc., and more woody litter including
1502
CWD from collateral damage by tree canopy browsers (notably by elephants:
1503
Plumptre 1994),
1504
4. material shed around the point of damage, e.g. Buck-Sorlin and Bell (2000), found
1505
that spring defoliation and shoot tip removal in Quercus spp. (oak) trees in Wales led
1506
to increased shoot shedding;
Wilson & Agnew, chapter 2, Interactions, page 48 of 54
1507
5. reduced suppression of sub-canopy species, potentially adding more of their litter.
1508
The complexity of such processes and systems are well illustrated by Long et al. (2003), who
1509
examined the interaction between the beetle herbivore Trirhabda virgata and its food plant
1510
Solidago altissima (goldenrod). Beetle populations were highest in the densest S. altissima
1511
patches, leading to reduced plant vigour and lower litter production. Litter, when present in
1512
quantity, increased aboveground biomass and reduced species richness. Thus the net effect of
1513
the beetle and S. altissima concentrations was to enhance plant species diversity by reducing
1514
litter disturbance.
1515
In heavily grazed vegetation, litter is reduced and can have little or no effect, so that
1516
more of the system of interspecific interactions must depend on growth disturbance, as well as
1517
interference and subvention. This conclusion conflicts with the usual assumption that
1518
competition will be less intense under heavy grazing. There is nothing in the first sentence
1519
that proves that just because litter has no effect, that interference (neg. interactions., aka
1520
competition) and subvention (pos. interactions) are necessarily the forces that are driving
1521
community structure- it is merely stated as a fact without backing. Heavy grazing might give
1522
rise to a community structured by the ability to survive the grazing or to recolonize areas
1523
opened by disturbance, in other words a community structured not be plant-plant interactions,
1524
but by plant-herbivore interactions. It might favour rare species (escape from grazing) or
1525
unpalatable species. Indeed as you state that both negative and positive plant interactions are
1526
more important in these systems, even that statement doesn’t lead to the conclusion that
1527
negative interactions (competition) will increase or even dominate the system interactions.
1528
If only living plant presence is recorded and litter is ignored, only growth interactions
1529
can be assessed. This may explain why the strongest evidence for assembly rules has been
1530
found in uniformly and heavily grazed (i.e. mown) lawns (Wilson and Roxburgh 1994), in a
1531
heavily grazed saltmarsh (Wilson and Whittaker 1995) and a sand dune (Stubbs and Wilson
1532
2004), in all of which there is very little accumulation of litter and interactions due to growth
1533
are not obscured by the litter effect. This suggests that assembly rules should be sought which
1534
include not only the living components but also the litter, as implied by Grime (2001) in his
1535
interpretation of the productivity-richness humpback curve.
1536
CWD can also interact with herbivory. Long et al. (1998) suggest that treefall mounds
1537
provide a refuge from herbivory for Tsuga canadensis (hemlock) regeneration, which is
1538
important in spite of its being a less favourable environment for establishment of that species
1539
than the forest floor.
Wilson & Agnew, chapter 2, Interactions, page 49 of 54
1540
7.2
1541
Litter-fire interactions
Sometimes the autogenic effect of litter interacts with allogenic disturbance. Fire is
1542
perhaps the best example. If litter accumulates faster than it decomposes, and local conditions
1543
of climate and soil are too dry to allow peat accumulation, its ultimate fate on a landscape
1544
scale is destruction by fire. This is basically an autogenic effect because there can be no fire
1545
without fuel, and the initiating fuel of a fire is usually a buildup of standing dead,
1546
programmed and stochastic litter. However, an allogenic process has to start the fire. After
1547
fire, the litter accumulation cycle restarts. This is a process intrinsic to heathlands and dry
1548
forests over large geographical areas.
1549
Various factors affect the probability and the type of fire. In a flash fire burning
1550
mainly volatiles either in the field layer or the canopy, litter will play little part. However a
1551
fire that consumes the litter will burn for longer. All fire will impact more on the less fire-
1552
resistant and more fire-intolerant species (Whelan 1995). In many vegetation types, branch
1553
fall provides the fuel build up because CWD is long-lived, much of it persisting until burnt.
1554
Treefall also provides fuel (Whelan 1995). The spread of fire into the canopy is facilitated by
1555
the retention of dead limbs (Johnson 1992), so branch fall will help to confine fire to the
1556
ground flora, sparing the canopy stratum. Lianas can have a similar effect: Putz (1991)
1557
observed flames travelling up lianas, with the result that Pinus spp. (pine) trees with lianas
1558
(especially Smilax spp., greenbriar etc.) were more likely to suffer crown scorch than liana-
1559
free trees. Fire is especially prevalent in communities of conifers (particularly Pinus:
1560
Ne’eman and Trabaud 2000) and of Eucalyptus (gum) apparently because of their flammable
1561
resin/oil content (Whelan 1995; Williams et al. 1999). At the other extreme, some types of
1562
vegetation are very fire resistant. For example, in arid central Australia, where most
1563
vegetation is fire-prone, Acacia harpophylla (wattle) does not burn (Pyne 1991) because of
1564
several features: their chemistry makes the leaves barely flammable; the simple leaf shape
1565
results in flat, poorly-aerated litter fuelbeds; leaf fall is keyed to intermittent rains, when fire
1566
is less likely; bark is not shed; and finally the microclimate of the forest floor discourages
1567
drying and promotes decomposition.
1568
7.3
1569
Litter-herbivore-fire interactions
There are several examples of good evidence for higher-order interactions between
1570
grazing, litter and fire. For example, in North American Pseudotsuga menziesii (Douglas fir) /
1571
Physocarpus malvaceus (mallow ninebark) forest, grazing by livestock (including cattle,
1572
sheep and deer) reduces the herb layer and hastens the decay of litter by trampling
1573
(Zimmerman and Neuenschwander 1984), and the unpalatable herbs left tend to be less
Wilson & Agnew, chapter 2, Interactions, page 50 of 54
1574
flammable. This reduces fire frequency, but allow the buildup of coarse woody debris so that
1575
when fires occur they are more severe and may reach the canopy. A similar effect of grazing
1576
reducing the fuel load and hence the frequency of fires occurs in the African savannah (Fig.
1577
2.8; Roques et al. 2001). In habitats with both a grass and a woody component (savannah or
1578
ecotone) a number of processes can occur (Fig. 2.8; Brown and Sieg 1999; Touchan et al.
1579
1995).
1580
This process includes many complexities. It could converge to an equilibrium, it could
1581
operate as a cyclic succession, or a switch could also operate in the system, giving alternative
1582
stable states (Fig. 2.8; Dublin 1995). In the 1960s and 70s, fire caused a decline in Serengeti
1583
woodland, because higher rainfall then led to greater grass growth (Dublin et al. 1990).
1584
Loxodonta africana (African elephant) inhibited the recovery and kept it as grassland, and
1585
because of their grazing the grass crop is not enough to support hot fires. On the other hand,
1586
elephants avoid the fire-resistant thickets, which are therefore stable as an alternative stable
1587
state. There are both negative and positive feedback processes here.
1588
Wilson & Agnew, chapter 2, Interactions, page 51 of 54
1589
1590
Fire repelled
1591
1592
1593
Woody thicket
1594
remains
Elephant browsing
1595
repelled
1596
Woody patch escapes
1597
the fire
1598
Catastrophic fire,
1599
triggered by an
1600
exceptional event1
1601
Trees
Woody plants killed,
re-establish
1602
at least above ground
1603
1604
Fire frequency
Less palatable
1605
reduced
forbs dominate
1606
More light is allowed
1607
into the field layer
1608
Litter buildup
1609
reduced
1610
1611
1612
Invasion of
Grass growth promoted
woody species
Fewer old
1613 Litter decays
suppressed
leaves
1614 faster
1615
1616
1617
Regular
Trampling
Grazing
1618
fires
1619
Low
1620
High rain
rain
The grazing
Low
1621
resource increases
rain
Herbivore density
1622
increases
1623
1624
1
1625
A rainy season giving a heavy crop of grass followed by a dry season; or a dry season
1626
making savannah burnable; or high browser density causing CWD accumulation
1627
= switch
1628
Fig. 2.8: Pathways of community change in dry savannah.
1629
8 Conclusion
1630
We have described the many processes that can be involved in the development of
Wilson & Agnew, chapter 2, Interactions, page 52 of 54
1631
mixed species stands. Most types of interference, subvention, litter effects and autogenic
1632
disturbance are based on the universal principle of reaction, that organisms in general, and
1633
plants in particular, modify their physical environment. All these reactions have effects on
1634
neighbours. The wide variety of modifications and the wide variety of responses by
1635
neighbours are the reasons for the long list of interactions we gave, a list that we tried to make
1636
exhaustive but surely have not.
1637
Plants must be seen within the framework of the ecosystem. Autotrophs make up most
1638
of the stored living carbon framework of terrestrial ecosystems, i.e. its biomass, and a plant’s
1639
biomass is also a necessary part of its work in foraging for light and soil resources. But
1640
phytomass is never alone. Operators from other trophic levels are always present and can
1641
have profound influences on plant species presence, adding to the complexity. Clements
1642
envisaged reaction as being on the physical environment. We are reluctant to expand this to
1643
the biotic environment because of the ensuing complications, but we have listed interactions
1644
“mediated by other trophic levels”. There are complex interactions amongst heterotrophic
1645
levels too, which will also impact on our dear plants. Paine’s original usage of ‘Keystone
1646
species’ (chapt. 5, sect. 11 below) is a clear expression of these.
1647
The plant community comprises continual renewal: disturbance, death, establishment,
1648
growth and both sexual and vegetative reproduction of great numbers of offspring – greater
1649
than the habitat can support. The negative and positive interactions that we have listed
1650
moderate those processes. In the next chapter we consider how those processes operate at the
1651
whole-community level, to determine successional changes after allogenic or autogenic
1652
disturbance, and to affect the spatial pattern of vegetation.
1653
Wilson & Agnew, chapter 2, Interactions, page 53 of 54
1654
1655
Table 1. Effects of litter on the population dynamics of species in the community, as reported
in the literature.
1656
1657
1658
1659
1660
1661
1662
1663
1664
1665
1666
1667
1668
1669
1670
1671
1672
1673
1674
1675
1676
1677
1678
1679
1680
1681
1682
1683
1684
1685
1686
1687
1688
1689
1690
1691
1692
1693
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
1694
ILLUSTRATIONS
1695
Fig. 2.1. Replacement and additive comparisons in experiments that examine the interaction
1696
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.
1697
Fig. 2.2. In Trifolium subteranneum, the results of competition affect competitive ability.
1698
Fig. 2.3: A possible mechanism for size-asymmetric competition belowground, when nutrient
1699
supplies become available patchily in time and space, e.g. from sheep micturition.
Wilson & Agnew, chapter 2, Interactions, page 54 of 54
1700
Fig. 2.4: After Novoplansky et al. (1990).
1701
Fig. 2.5: After Biddington and Dearman (1985).
1702
Fig. 2.6: The seasonal pattern of litterfall in an oakwood. After Christensen (1975).
1703
Fig. 2.7. The process of peat accumulation in mires dominated by Empodisma (wire rush) or
1704
1705
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