Download 1 Introduction

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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 3: Community-level processes
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OVERALL IMPRESSIONS: The second half of the chapter was much easier
to read than the first. I think what is lacking in the first half is basic review of
succession theory and a solid foundation for the conclusions drawn at the end
of the chapter (relay-floristics is the null model). The figures were better than
previous chapters. I liked the conceptual diagrams presented at the end of the
chapter. Several figures could benefit from more descriptive captions. The
idea of resilience was oversimplified which was perhaps a result of the
emphasis of the chapter on the climax condition (?). I liked the section on
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Introduction
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Allogenic change: including secular change ....................................................................................... 4
Relay floristics
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3.1
Concepts ...................................................................................................................................... 7
3.2
Environmental change................................................................................................................. 8
3.3
Trends.......................................................................................................................................... 9
Cyclic succession: in fact or fiction .................................................................................................. 10
Switches: the positive feedback processes ........................................................................................ 13
5.1
The concept of the switch ......................................................................................................... 13
5.2
Types of switch ......................................................................................................................... 14
5.3
Outcomes of switches ............................................................................................................... 15
5.4
Mediating agents ....................................................................................................................... 16
5.4.A
Mechanisms involving regional climate ........................................................................... 16
5.4.B
Mechanisms involving water ............................................................................................ 16
5.4.C
Mechanisms involving other aspects of microclimate ...................................................... 18
5.4.D
Mechanisms involving physical substrate......................................................................... 18
5.4.E
Mechanisms involving substrate chemistry ...................................................................... 19
5.4.F
Mechanisms involving disturbance ................................................................................... 22
5.4.G
Mechanisms involving heterotrophs ................................................................................. 22
5.5
Switch evolution ....................................................................................................................... 24
5.6
Alternative stable states ............................................................................................................ 25
5.7
Negative feedback ..................................................................................................................... 31
Diversity → productivity
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Stability
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7.1
Concept ..................................................................................................................................... 33
7.2
Reliability (constancy) .............................................................................................................. 35
7.3
Stability sensu stricto (Liapunov stability) ............................................................................... 36
7.4
Resistance to abiotic perturbation ............................................................................................. 38
7.5
Resistance to invasion ............................................................................................................... 40
7.6
Resilience .................................................................................................................................. 43
Conclusion
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Wilson & Agnew, chapter 3, Community processes, page 2 of 49
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‘switches’. This was not a familiar concept for me, and I enjoyed reading
about it.
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1 Introduction
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In the previous chapter we discussed positive and negative interactions between plants. These
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are the currency of community processes, and we now examine the implications of their effects at the
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whole-community level. All plants and animals must alter their immediate surroundings by reaction,
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which Clements (1916) defined as: “The effect which a plant or a community exerts on its
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habitat”(chapter 2 above). Whilst admitting that classification of types of reaction was difficult,
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Clements listed about 20. Plants especially cause reaction, because of their bulk and their necessity to
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produce litter, leading to modifications of local light availability, climatic regimes, environmental
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chemistry and geomorphological processes. This affects the populations of herbivores and thus the
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system as a whole.
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Community processes can have only two outcomes: stability or change. Change should be the
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expectation, firstly because the environment is never without temporal variation and secondly because
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the plants alter, by reaction, their own environment. However, stabilising forces do exist, and aspects of
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stability can certainly be seen, even if strict stability has never been proved. A contrast can be made
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(Box 3.1) between a species/community changing the environment to its disbenefit (facilitation, the
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concept though not the term of Clements 1916) or benefit (switch: Odum 1971; J.B. Wilson and Agnew
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1992). We therefore link most vegetation change to facilitation and switches in this chapter. In either
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case, eventually there can be negative feedback, a stabilising process. We also consider the cyclic
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succession of Watt (1947).
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Box 3.1: Types of community interaction.
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species/guild X gives a relative disadvantage to itself:
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the effect is density-independent: facilitation and/or autointerference = relay floristics
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the effect disappears at low density of X (negative feedback) = stability
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species/guild X gives an absolute or relative advantage to itself = switch
None of these processes can take place on a uniform stage because there is both heterogeneity
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caused by underlying environmental variation and caused the unique reaction of each species and its
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spatial pattern. Peter Greig-Smith (1957) used sampling and analysis to show that the ramets of all
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species had a non-random pattern. One cause for this is the demographic (dispersal) behaviour and
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morphology of each species. For example, Kershaw (1964) examined North Wales pastures where
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Agrostis capillaris (= A. tenuis, bent) showed no clumping to the naked eye, but the tillers proved on
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sampling to be clumped because disparate rhizomes upturned when nearing each other, forming patches
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of denser culms. Patterns resulting from vegetative demography are clearly seen at the level of
Wilson & Agnew, chapter 3, Community processes, page 3 of 49
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individual clones in Harberd (1962) (chap. 1, sect. 1.1) and in his similar results for Festuca rubra,
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Trifolium repens (white clover) and Holcus mollis (creeping velvetgrass). Using Mark Hill’s (1973)
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algebraic clarification, Agnew & Gitay (1990) found that species and soil nutrients were similarly
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patterned in visually uniform dune slacks, and that this pattern became more pronounced as species
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number increased.
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Resources can be patchy in apparently uniform natural communities (eg Robertson et al 1988). Is the pl
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comm a force for coarsening the grain of resources in patches or evening them? The differing
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requirements and acquisition efficiencies in acquiring nutrients as well as differing economies during
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their life histories (i.e. phenologies of production and litter deposition = reaction) should coarsen the
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grain of resources, so long as the indiv spp show a definite pattern. We found the most spp pattern
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(clumps or holes in the distrib) at 20cm diam. But Ca & P did not show this pattern of clumping.
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However, at 20 cm sample size soil Ca & P variance increased with spp richness. At the same time the
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phytomass P became less variable at 20cm sample size. So while richness increased P patchiness, it
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also increased evenness in the plant content. That means that each sp has just enough, from a patchy
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soil that it has created. Can we make anything of this?
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Patterning is a general quality of all plant communities and has implications for community
function. The basic patterns of change are (Fig. 3.1):
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Allogenic change
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Directional autogenic change (succession sensu stricto)
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Watt’s cyclic succession
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Switches
Community
X1
Community
Y1
Community
X2
Community
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Community
Y2
Time
Community
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Clements’ relay
floristics
Community
Y
Watt’s cyclic
succession
Fig. 3.1: Three types of autogenic vegetation change through time.
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Time
Community
Y1
Time
Community
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Community
X
Community
Z1
Community
Y2
Community
Z2
A switch, giving
alternative stable states
Wilson & Agnew, chapter 3, Community processes, page 4 of 49
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2 Allogenic change: including secular change
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Vegetation changes on long timescales can be seen via the pollen record of lakes and mires,
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especially over the past 15,000 yr. In the northern Atlantic and Pacific areas, the most abrupt, non-
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anthropogenic alteration was a reversion from birch scrub (Betula spp) to tundra herbs in the Younger
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Dryas period (13,000 – 11,600 yr BP). When historical vegetation change is sudden, it may be that the
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vegetation is tracking a sudden climate change, or the vegetation change may be abrupt because there is
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a geographic-scale switch (sect. 5.4.A below). In the case of the Younger Dryas, there does seem to
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have been a closely-correlated sudden temperature depression (Hu et al. 2002). Such changes are most
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likely to be seen at the geographical boundary of a vegetation type, for example the pollen profile of
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Kremenetsky et al. (1999) indicated that the steppe-forest boundary in the Ukraine has moved at least
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twice since 6000 yr BP.
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Soils can change on a similar timescale. Soil leaching needs thousands of undisturbed years to
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take place. It results in plant communities which are slow growing, often evergreen and high in
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phenolics, on soils that are low in all nutrients, particularly phosphate. Northup et al. (1998) describe a
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chronosequence of such soils in northern California formed over an estimated 500,000 yr. Recent soil
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there has pH (in CaCl2) over 6, while in the oldest soil it is less than 4. This environmental change has
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been tracked not only ecologically but perhaps evolutionarily, since there are endemic species and
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varieties of conifer particularly adapted to the soil conditions and contributing to them.
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Fluctuations in the species composition of plant communities from year to year were described
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by Clements (1934 pp. 41–42) as ‘annuation’, by Penfould (1964) as the ‘pulse phenomenon’ and by
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Collins et al. (1987) as ‘pulse-phase’. Investigations on this timescale, and the decade-long changes that
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often accompany it, have been hindered by the paucity of datasets with continuous and long records of
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approximately equilibrium vegetation. Notable exceptions are the Park Grass experiment in lowland
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England (since 1856; Silvertown et al. 2006) and plots on Barro Colorado Island (since 1985; Chave
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2003).
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When the environment changes, it would not be surprising for the plant community to do
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likewise, but often the correlations are hard to see. R.B. Allen et al. (1995) found correlation with the
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rainfall at one of the dry grassland sites examined, but not at four other, nearby sites. Collins et al.
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(1987) similarly failed to find correlations between individual species and the climate.
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Dunnett et al. (1998) correlated vegetation changes over 38 years in the roadside vegetation at
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Bibury, southern England, with climatic fluctuations. Warm dry summers increased species favoured by
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environmental stress or disturbance (S or R of C-S-R theory), whereas wet growing seasons favoured
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more productive species (C). Dunnett and Grime (1999) found by experiment that the differential
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response of species to temperature was based on their physiological response, but the differences
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between the species were amplified in competition. If we compare these responses with the species’
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distributions in Britain (Preston et al. 2002), we see that species that were notably more abundant in
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unusually warm summers included Achillea millefolium (yarrow) (Grime et al. 1994) which is
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distributed almost throughout the British Isles, being absent only in a very few cold/wet parts. However,
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Ranunculus repens (buttercup) and Trifolium repens (white clover), with almost identical geographical
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distributions to A. millefolium, were less abundant in those years. Similarly, Brachypodium pinnatum
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(tor grass) was more abundant in warm summers, and is a species very frequent in chalk/limestone areas
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with warm summers (July mean > 15 ˚C), but another grass with a very similar distribution, Bromopsis
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erecta, was less abundant. This is puzzling.
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One of the most fascinating sets of observations in ecology is Watt’s (1981) 38-year record from
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Breckland in eastern England. Calcareous ‘Grassland A’ exhibited a sequential dominance, from 1936
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to 1950 by the small-tussock grass Festuca ovina (sheep’s fescue), from 1950 to 1958 by the creeping
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herb Hieracium pilosella (hawkweed), from 1959 to 1964 co-dominance of the latter two with the
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procumbent shrub Thymus polytrichus (= T. drucei, thyme), and from 1965 to the end of recordings in
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1973 by T. polytrichus on its own. These three species all showed a steady increase to a peak and a
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steady reduction from it, though when H. pilosella decreased it held on to some microsites rather
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tenaciously. Watt explains these dramatic changes by very subtle changes in the weather, but as at
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Bibury the correlations are not convincing, and we have to conclude that these fascinating changes have
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never been explained. Like Dunnett and Grime (1999), Watt saw competition as important, which it is
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probably is, but disease may have played a rôle too.
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Usher (1987) re-analysed Watt's (1960) 22 years of observation in acid grassland.(using
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Markovian models?) The transition probabilities indicated that change in cover state could occur in
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either direction between almost any pair of states. However, the predictions of the two Markovian
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models are difficult to believe, e.g. that the ‘Festuca’ cover type, which had been increasing rather
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steadily over the period up to 37 % at the end of the 22 years, would somehow decrease to 20 or 28 % in
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a steady state. Markovian models have a tendency to make conservative predictions for future change,
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probably because recording errors (but of course not in Watt’s case!) and minor fluctuations give
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reverse transitions (Mark and Wilson 2005). The other problem is that such models assume constant
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transition probabilities which almost inevitably lead to a steady state, which is quite at variance with the
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general observation of annuation / breakouts, i.e. sudden increases in abundance followed by a sudden
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decrease within a few years, seen dramatically in this grassland (Fig. 3.2). Neither Watt nor Usher had
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any ecological explanation for these changes.
Wilson & Agnew, chapter 3, Community processes, page 6 of 49
Percent cover of Galium type
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1945
1950
1955
Year
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Fig. 3.2: Changes in the percentage of the ‘Galium’ cover type in Watt’s acid Breckland grassland.
Data from Usher (1987).
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Shorter-term changes can be seen too. Peco (1989) was able to show that low rainfall produced a
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single-year retreat in an ordination axis that was correlated with successional time. This represents a
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whole-community shift in a single year. Some species have been observed to show outbreaks. In the Park
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Grass Experiment, Dodd et al. (1995) found that of 43 species recorded on non-acidified plots, 10
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showed outbreaks. These species tended to be ruderals: self-fertilised and suppressed by competition.
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Outbreaks are seen at Bibury too (Dunnett and Willis 2004) in species such as Urtica dioica (stinging
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nettle) and Chamerion angustifolium (rosebay willowherb), and on shorter timescales in species such as
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Galium aparine (goosegrass) and Rumex obtusifolius (dock); Dunnett and Willis say many in the later
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group have ruderal traits, confirming the conclusion of Dodd et al. The decade-long changes in Watt’s
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(1981) Breckland site could be compared to such outbreaks, but happening on a longer timescale
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because of the inertia of the shrubs (Thymus polytrichus), tussocks (Festuca ovina) and clones
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(Hieracium pilosella).
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At a fine scale, the elusive Carousel Theory (van der Maarel and Sykes 1997) appears to say that
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even if a community remains in equilibrium on a large scale, species presence on a small scale changes
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from year to year, such that within a community most species are capable of occupying most microsites,
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but in any year each species will leave some potential sites unoccupied, at random. This begs the
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question of why a species sometimes chooses to be absent. The logical implication is that there is niche
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limitation to the number of species that can co-exist locally, and there is evidence for this (J.B. Wilson
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et al. 1995a). Baba (2005), also working in calcareous grassland, emphasised differences in mobility
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between species: a ‘complex carousel’ rather than a single carousel. Van der Maael and Sykes’
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observations of turnover were made on a fine scale, e.g. 3 × 3 cm, which is less than the size of most of
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the plants, and certainly less than their sphere of influence. The apparent turnover may represent that
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one year a leaf of a plant overhangs the quadrat, and next year the same plant is present in the same
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place, but its leaves are in a different direction. The first priority in understanding communities at this
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scale is to solve the Paradox of the Plankton (chapter 4), and then to find how these mechanisms of
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coexistence and those of exclusion by interference interact to produce very fine coexistence. Self-
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allelopathy for Hypochaeris radicata (cat’s ear; Newman and Rovira 1975) is one example, still not
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fully established for the field, of the thousands of interactions that must be causal. The Carousel Theory
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is purely descriptive, and thus a distraction from progress towards understanding the processes.
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Allogenic, non-directional changes in plant communities are difficult to deal with. It is clear that
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they are surprisingly common in vegetation that we tend to assume is constant. So far all attempts to
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explain them have been inadequate. This is probably because the changes are driven by many
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environmental factors, but also partly through interference and subvention between species, and
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interactions with other trophic levels: pathogens, insect herbivores, pollinators and many others. There
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will also be inertia and switches operating. Attempts to understand the cause of allogenic change at any
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particular site have basically failed. They will continue to fail until there is a complete model of all the
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species – plant, animal and microbe – with their response to the environment and interactions with each
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other and their reactions on the environment. This is a tall order for finding why species composition
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varies on Bibury roadsides, but it is part of the movement away from considering communities as static
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entities to accepting that change is normal.
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3 Relay floristics
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3.1 Concepts
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A linear gradient from pioneer stage to climax was the norm for Clements (1916). This was
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characterised by Egler (1954) as “relay floristics” and by others as “facilitation succession” and
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“succession to climax”. As always, Clements saw much, and synthesised his observations into a general
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pattern. Like all generalisations, there are exceptions. Clements saw these as well as anyone, and
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reported them. However, the general pattern that he emphasised is a true one. Communities change
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through time for three reasons: (1) the environment changes allogenically making invasion possible
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from the species pool, (2) new species arrive in the regional pool, (3) the reaction of species on the
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environment (especially the soil) facilitates the establishment of others. It is only the last that can be
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called succession, either directional or cyclic.
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If the initiation of succession is geomorphological, i.e. the natural creation of a new land
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surface, the succession is said to be primary succession; if environmental modifications remain from
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previous succession it is said to be secondary. A classic description of a primary succession is that of
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Crocker and Major (1955) on deglaciated terrain in Glacier Bay, Alaska. We observe that this is a
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space-for-time substitution, and as always with such comparisons the physical location and therefore the
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physical environment are not identical between stages, neither were the weather and the propagule flux
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at each stage of succession. A classic secondary succession is that in Buell-Small oldfields in New
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Jersey, USA (Bartha et al. 2003), where a genuine temporal record was possible. Earlier workers
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(Clements 1916) envisaged a single end point of a "climax community" in successions, but it has
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become clear that there are many potential pathways through vegetation types. Thus in Glacier Bay the
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initial vegetation was of Dryas drummondii then Alnus sinuata and A. rubra (alders), but the course of
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soil development in glacial til resulted in flats and hollows where drainage became impeded and mire
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vegetation developed (‘muskeg’ with Pinus contorta, lodgepole pine) while slopes became Picea
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sitchensis (sitka spruce) forest. Landform is not the only determinant of successional sequences: E.B.
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Allen (1988) suggested that the causes of differing trajectories of secondary succession in Wyoming
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sagebrush rangeland included anthropogenic topsoil alteration, mycorrhizae and alien invaders. There
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may also be alternative stable states (sect. 5.6 below).
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Pioneers are said to be mainly short-lived ruderals with high seed output. They have low
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competitive ability, and are replaced by long-lived species producing fewer but larger seeds and often
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with vegetative reproduction. These are often termed ‘r’ and ‘K’ selected respectively, by analogy with
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the Lotka Volterra logistic equations (Krebs 1978). An alternative classification of species is C-S-R
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theory. It is tempting to equate ‘r’ pioneers with the ‘R’ of C-S-R theory but whilst under Grime’s
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theory secondary succession starts in the R corner, primary succession starts in the S corner and, after a
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trip towards the C-S-R centre, ends up also back in the S corner (Grime 2001; Fig. 3.x). Grubb (1987)
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agrees, pointing out that in primary successions with limited water and nutrients the pioneers are often S
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species.
C
Secondary
succession
Primary
succession
R
S
Fig. 3.x. The pathways of succession under Grime’s C-S-R theory.
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3.2 Environmental change
The reaction that every plant has on its environment operates both above- and below-ground
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(chapt 2., sect. 2). An above-ground example is the mutual shelter offered by alpine shrubs (Choler et al.
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2001). However, the principal reactions in mesic successions are below-ground.
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Nutrient pools and soil structure change as roots exploit and die in the soil, while the soil fauna
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uses these resources and incidentally forces nutrient cycling. There is a trend towards soil stratification
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imposed by surface litter deposition and water movement. Soil systems, like aerial systems in their
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different ways, consist of a continuum of biota, all of which are leaky, so all components can affect all
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others through diffusion and by mass flow of solute. However, organisms are typically more closely
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intermixed below-ground than above-ground. For example, fungi play a vital rôle in vascular plant
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nutrition and performance, and have the potential to provide intimate connections between roots. Koske
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and Gemma (1997) found that invasion of the sand dune binding grass Ammophila breviligulata
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(beachgrass) into bare sand was slow without vascular-arbuscular mycorrhizae (VAM).
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However, the process of reaction causing facilitation has rarely been documented. For example,
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L.R. Walker et al. (1986) ,interpreting the zonation away from an Alaskan river as a chronosequence,
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concluded that there was no evidence of facilitation. , Nitrogen fixers are clear examples of species that
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might facilitate. L.R. Walker et al. (2003) gave experimental evidence that the net effect of the N-fixing
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shrub Coriaria arborea (tutu) on the succeeding dominant tree Griselinia littoralis (broadleaf) was
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positive during succession after a volcanic eruption in North Island, New Zealand,because considerable
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soil enrichment outweighed the effect of shade.
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For all the discussion of succession, remarkably little is known about the processes involved.
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Before Egler (1977) pointed out the fraud of space-for-time substitution there were few attempts to
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obtain real evidence on succession. Realisation of this problem has led to a search for long-term records
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that can be used to answer the questions, and to the setting-up of permanent plots. This is highly
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commendable, though it will need to be combined with field and greenhouse experiments to give a full
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picture.
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3.3 Trends
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The new species entering later in succession are usually more diverse, larger and longer-lived
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than their predecessors and therefore biodiversity and biomass increase with time (Clements 1916). In
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chapter 1, section 1, we listed the necessary parts of ecosystems: an energy input apparatus, the capital
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of energy, the cycling of elements and rate regulation (Reichle et al. 1975). In succession, the increase
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in biomass, usually through storage of carbon in wood, provides the capital of energy; succession is a
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process of filling available niches with biomass, and of the creation of new niches (chap. 4, sect. 1.3).
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The biodiversity of heterotrophs facilitates nutrient cycling (the resource economy). Nutrient capital in
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the system is part of the rate regulation, other rates being set by the physiology (autecology) of the
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species.
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Monotonic increases in these values are not inevitable. Allogenic disturbances can trigger
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decreases in all of them. There can also be an autogenic decrease in biomass due to a switch process
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such as paludification (sect . 5.4.E, below). Rather similarly, the litter produced by some species,
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especially gymnosperms, is low in bases and acidifies the soil, resulting in the leaching of nutrients.
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This is podsolisation. Such litter is often slow to break down, and therefore retains nutrients. These
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processes could theoretically lead to reduced biomass. D.A. Wardle et al. (2004) compare sequences
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from six ‘chronosequences’, in different parts of the world and on different substrates, all showing a
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decrease in biomass. The timescale on which this process would occur makes it difficult to support with
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evidence, but they say that “For all the sequences, the decline in basal area became noticeable within
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thousands to tens of thousands of years after the start”. The sequences vary in the trends of litter N and
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P, litter decomposition, etc., but most conform to podsolisation. However, succession towards forest
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should have a special dynamic since the system is storing nutrients (and carbon as biomass), potentially
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depleting soil resources. Thus Simard and Sachs (2004) found that in young stands taller individuals
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were most affected by neighbours, while in older stands shorter individuals were more sensitive. This
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suggests that the resource under competitive demand changed from light to nutrients, the opposite of
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Tilman’s(1982) interpretation for Cedar Creek.
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Another biomass-decreasing process which could occur late in a succession is salinisation, caused by
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deep-rooted plants drawing on a sub-saline groundwater. Climate change and soil salinisation were
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probably the cause of loss of casuarinid forest and an accompanying increase in salt-tolerant chenopods
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in south-western New South Wales, Australia after 4500 yrs BP (Cupper et al. 2000). The salinization
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could have been caused by the transpiration of the forest, in which case the process seems to be
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autogenic. However, biomass loss caused by autogenic succession seems to be rare.
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4 Cyclic succession: in fact or fiction
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A quite different concept is Watt’s (1947) idea of autogenic cycles of change through
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communities with different species composition and often different biomass and biodiversity. He
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concluded that such cycles were widespread and the usual cause of vegetation mosaics. The idea fired
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field ecologists worldwide to look for examples. The mechanism is the opposite to that in a switch: a
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patch of a major species (usually only one) becomes unable to sustain its own presence or abundance
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and dies ("moving" laterally), its place being taken often by members of a different guild, e.g. shrubs
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replaced by bare ground with lichens. The latter eventually form an environment suitable for
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recolonisation by the former, and so the cycle continues. The effect could be via any kind of reaction
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such as pH or litter. Similar effects could be caused by plant pathogen increase at high densities; this
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would not be cyclic succession because no reaction on the environment is involved but it can be difficult
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to distinguish between these effects in field studies.
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Autoallelopathy is a possible cause. It has been shown many times that leachates from a species’
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shoot or occasionally roots can inhibit that same species’ seed germination or growth (Singh et al.
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1999). Newman and Rovira (1975) tested a set of British meadow herbs and found that Hypochaeris
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radicata (cat’s ear) and Plantago lanceolata (ribwort plantain) were significantly inhibited by their own
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leachate, while Lolium perenne (ryegrass) was not. They argued that this could explain why the former
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two species never formed pure stands and individuals of them were short-lived in the meadow
323
community. It could give a two-phase cycle. A related issue is the horticultural/forestry replant problem,
Wilson & Agnew, chapter 3, Community processes, page 11 of 49
324
in which a crop fails to grow satisfactorily when replanted on land from which it has just been
325
harvested/removed. Zhang and Yu (2001) suggested that the replant problem in Cunninghamia
326
lanceolata (China fir) was caused by allelopathy, but Westphal et al. (2002) concluded that in an old
327
Californian vineyard the replant problem was caused by pathogens. Autoallelopathy may be widespread
328
in natural stands.
329
Patchiness in vegetation consisting of shrubby and herbaceous phases has often been interpreted
330
as cyclic (e.g. Agnew 1985). However, solid evidence has been hard to find. Miles (1987) stated that
331
Calluna vulgaris (heather) alternates with Betula pendula and B. pubescens (birch) in Scotland, but his
332
evidence was from current observation, not from historical records that the cycle actually happened. At
333
a smaller scale, Turkington and Harper (1979a) suggested that there was cyclic succession between
334
patches of grasses and clover in a pasture, but they provided only very sketchy evidence. Herben (1990)
335
in a mountain grassland in Czechoslovakia carefully tracked species movement at a small scale, but the
336
pattern of transitions revealed no networks. There have been a few reports of replacement cycles
337
between two dominants, e.g. Rychnovska and Jakrlova (1990) describe almost yearly alternating
338
biomass dominance by Sanguisorba officinalis (burnet) and the grass Nardus stricta in a meadow in
339
Bohemian Sudeten.
340
Seven suggestions have been made for cyclic successions in New Zealand forests, but none has
341
more than the slightest supporting evidence (J.B. Wilson 1990). For example, Mirams (1957) and
342
Blakemore and Miller (1968) suggested that stands of the valuable timber tree, Agathis australis (Kauri,
343
Araucariaceae) in North Island, New Zealand, are one phase of a cycle with broad leaf trees because A.
344
australis is unable to regenerate under its own canopy due to the amount and pH of its litter. A. australis
345
litter is indeed slow to decay (Enright and Ogden 1987), but there is also evidence that seedlings are
346
outcompeted by broad leaf tree canopy and roots (Bieleski 1959). The other part of the proposed cycle is
347
that under the succeeding angiosperm trees the soil changes are reversed, the A. australis can then
348
reinvade, overtopping the angiosperm trees and suppressing their growth (Bieleski 1975), but no
349
evidence is offered and Ogden (1985) has questioned the basic assumption of these suggestions, a lack
350
of direct regeneration of A. australis, reporting that many A. australis stands contain abundant seedlings
351
of different sizes.
352
In arid lands environmental extremes lead easily to subvention and hence perhaps to facilitation,
353
driving a cycle. Sadek and Eldarier (1995) describe how the succulent Arthrocnemum macrostachyum in
354
Mediterranean Egypt traps sediment and builds mounds in saline flats. When A. macrostachyum starts to
355
die back the mounds are colonised by Cynodon dactylon (Bermuda grass), and finally the mound breaks
356
down. Therefore it is clear that vegetation cycles can be driven by one species and that this constitutes a
357
method of maintaining a population by means of growth movement. Perhaps the closest to a
358
demonstration of cyclic succession was provided by Yeaton (1978) in a Texas desert (Fig. 3.3). He
359
examined plant densities, the remains of dead plants below others, the vigour of associated plants, the
Wilson & Agnew, chapter 3, Community processes, page 12 of 49
360
incidence of rodent burrows and soil erosion. The evidence suggests that Larrea tridentata (creosote
361
bush), a prolific seeder, can establish in bare ground. Birds perch in its branches and drop seeds of that
362
species and of a cactus, Opuntia leptocaulis. The O. leptocaulis establishes and grows well under L.
363
tridentata, perhaps because of fine wind-blown soil that accumulates there. The L. tridentata bush later
364
dies partly because of competition for soil water by the cactus, with its mat of shallow roots.
365
O. leptocaulis dies partly because rodents burrow below it and also because soil erosion is liable to
366
occur below its shallow root system, without the stabilisation that the deeper roots of L. tridentata had
Fig. 3.3: The Larrea tridentata
(creosote bush) / Opuntia
leptocaulis cyclic
succession proposed by
Yeaton (1978).
367
provided. This returns the patch to open ground. The data are observations at one time, rather than a
368
temporally observed cycle, but they build a convincing story. The mechanisms are speculation, but
369
believable.
370
None of Watt's (1947) examples were based on solid evidence, and most have been proved
371
wrong on inspection over long time scales. The hummock-hollow alternation in bogs cycle had been
372
proposed long before Watt’s paper, and it has appeared in textbooks, but the weight of evidence is now
373
for the opposite process: a switch, stasis rather that alternation (J.B. Wilson and Agnew 1992; Belyea
374
and Clymo 1998). Watt (1947) described cycling driven by the growth phases of Pteridium aquilinum
375
(bracken) where a vigorous front of P. aquilinum can invade Calluna vulgaris (heather) but the C.
376
vulgaris can invade an older P. aquilinum stand (Watt 1955). However, Marrs and Hicks (1986) found
377
that after several decades the changes that Watt predicted had not happened. It would be possible to see
378
cycles in some of the species in Watt’s (1960) own record from the control plot of acidic grass-heath in
Wilson & Agnew, chapter 3, Community processes, page 13 of 49
379
Breckland, eastern England, or are they breakouts? In this grass-heath, Watt (1947) had proposed that
380
patches of A. capillaris (= tenuis) and A. canina (bent) spread, die out in the middle to form a ring, and
381
the patch is eventually re-colonised making a cycle. In Watt’s (1960) records, those species do indeed
382
appear and then disappear within 10 years in two places in the plot, but they persist for 20 years
383
elsewhere in the plot.
384
Cyclic succession is difficult to detect. Evidence obtained from one moment in time is
385
confounded by the nexus of temporal and spatial interactions present, it is essentially the discredited
386
space-for-time substitution. Many apparent examples of cyclic succession vanish on close examination,
387
and no cycle has ever been confirmed by observation over time. We also have to ask why the systems
388
with proposed cycles do not settle down to an equilibrium. In Watt’s (1947) Pteridium aquilinum /
389
Calluna vulgaris example, why is the equilibrium scattered C. vulgaris with P. aquilinum of moderate
390
vigour? In the bog hummock-hollow alternation, the hollow species are supposed to draw level with the
391
hummock ones, and then forge on up until they become hummocks. Why do they not stop when they
392
draw level and the surface is no longer moist enough for fast growth or for hollow species to persist?
393
Cyclic succession is an appealing idea, but most of the proposed mechanisms have been illogical. It may
394
exist, but we have no evidence of it yet.
395
A quite different kind of cycle of which there is irrefutable evidence is that driven by
396
monocarpic (semelparous) self-replacing dominants. This is triggered when all individuals of a
397
dominant species flower and then die over an appreciable area and within a short timescale.
398
Successional communities with shorter-term dynamics then take over the newly opened soil, starting
399
with ruderals and then often lianas, until the monocarpic species re-establishes its dominance. Examples
400
are some tropical forest understorey acanthacean scrambling shrubs such as Mimulopsis solmsii
401
(Tweedie 1965) and Strobilanthes spp. (van Steenis 1972) and many bamboos (Janzen 1976; Agnew
402
1985). Fire appears to be part of the bamboo cycle in Asia (Keeley and Bond 1999) but not in Africa (in
403
our experience) or Australia (Franklin and Bowman 2003). These cycles are not switches since no plant
404
changes the environment in its favour, and are not stable states because the ruderal phase is not stable.
405
They are cycles caused by endogenous processes, notably plant suicide, but not those of facilitation.
406
5 Switches: the positive feedback processes
407
5.1 The concept of the switch
408
The great majority of the effects that plants have on each other (chapter 2) are via the
409
environment, the ‘Reaction’ concept of Clements (1916), rediscovered by Jones et al. (1994) as
410
‘ecological engineering’ and by Odling-Smee (1988) as ‘niche construction’, cute but redundant terms.
411
However, these concepts seem too general because at the community level, there are two opposite
412
possibilities: (1) The community makes the conditions relatively less favourable for itself. This is the
Wilson & Agnew, chapter 3, Community processes, page 14 of 49
413
basis of Clements' theory of relay floristics, based on facilitation. (2) The community or a key species
414
makes the conditions more favourable for itself, relative to other species. The reaction reinforces the
415
species’ hold on a site, i.e. there is community reinforcement by positive environmental feedback, the
416
process known as a switch (J.B. Wilson and Agnew 1992). The term ‘switch’ was coined by Howard
417
Odum (1971) for the positive-feedback process between biota and environment. We see the vegetation-
418
environment switch as the key to plant community ecology. The switch process has been known by a
419
variety of terms such as "constructiveness" (Braun-Blanquet 1932), "positive feedback", "self-
420
intensifying effect", "self-reinforcing trend" and "bootstrapping" (see J.B. Wilson and Agnew 1992).
421
Switches have been under-studied and under-emphasised, probably because the opposite process,
422
Clements' theory of facilitation, succession, still has a strong hold in the ecological psyche. The two
423
elements of a switch are:
424
Element i. Community X changes the environment,
425
Element ii. This change is relatively more favourable for community X than for community Y.
426
It is very difficult to find hard evidence for both elements ‘i’ and ‘ii’ for any single situation (J.B.
427
Wilson and Agnew 1992), though convincing evidence is emerging for a few cases. In most cases the
428
‘environment’ involved is the physical one, changed by reaction, and that terminology will be used
429
below. However, some switches operate via the biotic environment, i.e. using the ‘Plant-to-plant
430
interactions mediated by heterotrophs’ of chapter 2, section 6; these are discussed in section 5.4.G
431
below. It would be theoretically possible for a switch to operate via autogenic disturbance (chap. 2, sect.
432
6), for example via strangler vines, though we know of no example002E
433
5.2 Types of switch
434
J.B. Wilson and Agnew (1992) identified four types of switch:
435
436
1. One-sided switch: Community X changes the environment (e.g. increases the nutrient status or
lowers the soil pH) in patches where it is present.
437
Zero-sum switch: Community X changes the environment in its patches, and in the process changes
438
the same environmental factor, in the opposite direction, in the patches where it is not present
439
(community Y), for example by channelling water or wind into those patches. We call this ‘zero-
440
sum’ here because it is caused by there being a limited amount of water or air. In J.B. Wilson and
441
Angew (1992) we called these ‘reaction’ switches, but we eschew that term to avoid a clash with
442
Clements’ prior use of it.
443
Symmetric switch: Community X changes an environmental factor in its patches, and Community Y
444
simultaneously changes the same environmental factor in its patches, but in the opposite direction,
445
for example one community raises the soil pH and the other lowers it.
Wilson & Agnew, chapter 3, Community processes, page 15 of 49
446
Two-factor switch: Community X changes an environmental factor in its patches, and Community Y
447
changes a different environmental factor in its patches, for example one community promotes fire
448
and the other casts shade.
449
450
5.3 Outcomes of switches
An indication that a switch is operating is often a sharp spatial boundary without an obvious
451
abiotic cause; types ‘2’, ‘3’ and ‘4’ can provide this. However, there are four possible ecological
452
outcomes of the operation of switches (Fig. 3.4):
453
1. Stable mosaic outcome: In a previously uniform environment a switch of types 2-4 can create a
454
stable mosaic of communities, separated by sharp boundaries. Community X establishes at some
455
sites by chance (whatever chance is), and its modification of the environment ensures it holds the
456
sites. Elsewhere, Community Y establishes, and by the mechanism implied in that switch type also
457
holds its sites. These are alternative stable states. A one-sided switch cannot give a stable mosaic
458
because community X can further invade the unmodified environment.
459
2. Sharpening situation: Where there was originally a gradual environmental boundary, a switch (of
460
any of the four types) can produce a sharp vegetation boundary on a gradient or in a less well-
461
defined mosaic.
462
3. Acceleration situation: If a switch (of any of the four types) be operated by invading
463
species/community, their invasion can be accelerated. The invading species/community Y changes
464
the environment to make it more suitable for community Y, and less suitable for the previous
465
community, X.
466
467
4. Delay situation: Existing species could delay vegetation change via a switch (of any of the four
types). For example, a switch could delay succession, prolong the effect of initial patch
(a) Stable mosaic situation
(b) Sharpening situation
Fig. 3.4: Four
possible
outcomes of
vegetation
switches.
(c) Acceleration situation
(d) Delay situation
Wilson & Agnew, chapter 3, Community processes, page 16 of 49
468
composition, or delay the response to climate change. This operates by community X changing the
469
environment to keep it more suitable for community (e.g. seral stage) X, and less suitable for the
470
succeeding community, Y. The delaying effect of switches has been called ‘inertia’ (Von Holle et
471
al. 2003).
472
If a switch results in alternative stable states, they are technically stable in the Liapunov sense, so that
473
the state will be restored after a small perturbation. However, a large perturbation may cause a change to
474
another of the stable states. We refer to these as ‘state changes’ (cf. Brooks et al. 2004).
475
5.4 Mediating agents
476
We may generalize that there are seven types of agent that can cause a switch. We outline
477
examples briefly here, especially those reported in more recent literature, to complement the fuller
478
review in J.B. Wilson and Agnew (1992).
479
5.4.A Mechanisms involving regional climate
480
G. Miller et al. (2005) proposed that early holocene human firing of the vegetation in the centre
481
of Australia so modified the climatic regime there that the vegetation changed from one with
482
considerable forest/shrub cover to a more open desert-scrub, that was both more fire-promoting and
483
more fire-tolerant, keeping the fire frequency high. They demonstrated through a general circulation
484
model that the resultant increase in the surface albedo and decrease in its roughness would change the
485
climate, increasing the fire frequency and reduce the extent to which monsoonal precipitation penetrated
486
into the area. Both these processes would hold the vegetation cover in its changed state.
487
In general, the different light reflectance, wind resistance (roughness length), energy flow and
488
evapotranspiration of forest vegetation (O’Brien 1996) results, according to models, in a regionally
489
warmer climate. In northern areas at least, this will favour the growth of forest and give a regional- or
490
global-scale switch (Bonan et al. 1992; Otto-Bliesner and Upchurch 1997; Bergengren et al. 2001).
491
According to Gaia theory, this is the reason Earth is habitable at all unlike Venus or Mars (Lovelock
492
1979). We list global-level climate switches as a separate category since they would occur on a spatial
493
scale orders of magnitude greater than our other examples. They are necessarily more speculative, being
494
based on word or simulation models.
495
5.4.B Mechanisms involving water
496
Water is an obvious mediating agent in switches. Occult precipitation is that trapped from
497
fog/clouds by tree branches, and to a lesser extent by stiff, erect tussock grasses and even soft flag-form
498
tussocks and short grassland. The vegetation types that increase their own precipitation are thereby able
499
to grow faster, are less affected by drought, and therefore expand (Figs. 3.5, 3.6). Naturally this is a
500
feature of arid climates.
Wilson & Agnew, chapter 3, Community processes, page 17 of 49
Higher precipitation
and reduced
evapotranspiration
higher up the hill allows
taller vegetation
The taller vegetation
traps fog precipitation,
and further increases
water status higher up
the hill
Fig. 3.5: A vegetation pattern
caused by a
fog-interception switch.
Higher water
status allows taller
vegetation
501
502
503
504
tundra where (isolated) young trees trap snow, which ameliorates low moisture and temperature. They
Precipitation
505
Scott and Hansell (2002) describe Picea glauca (white spruce) islands in Manitoba (Canada)
With occult
precipitation
switch
Without
switch
Grassland
Fog forest
Altitude
Fig. 3.6: Change in precipitation caused by a fog-interception switch.
506
grow well, and peripheral branches root to form woody islands. However, as they age more branches
507
droop, needles abrade and the canopy thins, allowing lichen heath to establish, and permafrost to enter
508
the island. So the young trees operate the switch, but old trees do not. It is unclear how the young trees
509
establish. This is a one-sided switch, but unusually for a one-sided switch it leads to a mosaic because
510
the processes driving the switch no longer operate as the trees age.
Wilson & Agnew, chapter 3, Community processes, page 18 of 49
Positive feedback between vegetation and water infiltration in arid conditions can give ‘tiger
511
512
bush’ alternative stable states (section 5.6). In mesic and wet climates ombrotrophic bogs can form by
513
paludification, a nutrient/pH/waterlogging switch (chap. 2, sect. 5.6). J.B. Wilson and Agnew (1992)
514
discuss water switches in saltmarsh pans.
515
5.4.C Mechanisms involving other aspects of microclimate
516
Montane closed canopy forest usually ends abruptly at the uppermost altitudes at which tree
517
growth is maintained. A tree cover has a lower albedo, which tends to give a lower mean temperature in
518
the plant cover and in the soil (Körner 2003a) and whilst radiation is more readily absorbed (Grace
519
1983) it is also more readily lost. However, the crucial factor is frost. Most tree species are less tolerant
520
of frost for regeneration than as adults. They can therefore regenerate under their own canopy where
521
frost is ameliorated but only with difficulty beyond: a switch. Switches driven by amelioration of frost
522
are common amongst shrubs and trees in alpine and arctic areas.
523
Light can also be the mediating agent, mainly where a species, by its canopy, produces low light
524
levels that allow that species to regenerate but prevent regeneration by others. This could be the
525
explanation for the rare cases of monodominant tropical forests; for example, Torti et al. (2001) suggest
526
monodominance of the legume tree Gilbertiodendron dewevrei (limbali) in the Congo is due in part to
527
low light below it, caused by its dense canopy and deep litter layer. Similarly, Pteridium aquilinum
528
(bracken) often forms very dense and impenetrable litter, suppressing other species and occurring in
529
monospecific stands. Such light switches seem to be very common.
530
5.4.D Mechanisms involving physical substrate
531
Plants can have long-term effects on soil particle size and porosity, and hence stability (Angers
532
and Caron 1998). Hellström and Lubke (1993) describe a moving dune system in South Africa which
533
has been colonized by the Australian shrub/small-tree Acacia cyclops (‘rooikrans’ in South Africa). It
534
has stabilised the sand and increased soil nitrogen to the extent that the dune cannot be returned to its
535
original state by the removal of A. cyclops. This is a switch caused by A. cyclops in physical substrate
536
and in substrate chemistry that will presumably result in a different vegetation type. Another sediment
537
entrapment switch occurs in estuarine salt marshes (De Leeuw et al. 1993; Castellanos et al. 1994), often
538
resulting in single-species stands, e.g. of Spartina anglica (cordgrass) or Puccinellia maritima (a saltmarsh
539
grass). If the entrapment is continuous this can start a succession, but sometimes a stable vegetation type
540
results.
541
Probably the best-documented case of a sediment switch is for algal growth on estuarine bottoms
542
(Fig. 3.7). Diatoms (Baccilariophyceae) and bluegreen algae (Cyanophyta, cyanobacteria) produce
543
extracellular polymeric substances (EPS), largely carbohydrates. These bind the sediment together,
544
leading to lower erosion of the silt component. This encourages diatom growth. If there were a limited
545
amount of silt in the estuary the switch would be zero-sum, resulting in a permanent, if shifting, mosaic.
Wilson & Agnew, chapter 3, Community processes, page 19 of 49
546
That would give bimodality in the frequency of two alternative states, one of the signs of a switch, and
547
this has been observed (van de Koppel 2001).
Higher EPS →
sediment erosion ↓
(Paterson 1989)
Lower sediment erosion →
silt content ↑
algae -> EPS produced
(de Brouwer and Stal 2002)
(Underwood and Paterson 1993)
Higher silt content →
algal growth ↑
(van de Koppel et al. 2001)
Fig. 3.7. A sediment-mediated switch. EPS = extracellular polymeric substances.
548
Plants could also affect soil fauna which can again change soil textures. These processes may
549
well comprise switches and form patchy landscapes but we have found no evidence of this. The nearest
550
we have is the influence of termites in tropical savannahs. For example, West African termite mounds
551
support better vegetation than the surroundings, and have better soil qualities: more clay, better porosity
552
and available moisture (Konate et al. 1998). Yet this cannot be regarded as a switch unless the termites
553
harvest the better vegetation so produced and most termites harvest grasses, not the shrubby vegetation
554
of termite mounds.
555
5.4.E Mechanisms involving substrate chemistry
556
Patches of more mesic conditions in a nutritionally poor arid environment have been called
557
‘resource islands’ and ‘islands of fertility’. A tree or shrub enhances its nutrient regime through trapping
558
wind- or water-borne material around its base, encountering mycorrhizae during soil exploration by its
559
roots or facilitating the presence of other species (both plants and animals) that enhance nutrient cycles
560
in its favour and even provide nutrient rich sites for its seedlings. But they also represent wind switches.
561
Such processes have often been described for isolated trees and shrubs in dry grasslands. In a series of
562
papers Belsky (e.g. 1994) has shown how the shade zone of Acacia tortilis trees in Kenya is an
563
enhanced soil environment with lower evapotranspiration, dampened temperature fluctuations and a
564
more adequate population of soil micro-organisms than the open inter-tree grassland. This in turn
565
attracts large mammals whose defecations add to the effect. When seedling establishment takes place
566
around an isolated tree to form a copse, a switch is occurring. (J.B. Wilson and Agnew 1992). They are
567
a classical cause of vegetation patchiness in a landscape. At the other extreme of rainfall, Agnew et al.
568
(1993a) described a switch mechanism of gymnospermous primal rain forest in western New Zealand,
Wilson & Agnew, chapter 3, Community processes, page 20 of 49
569
where the nutritionally rich seedling sites were on fallen tree trunks. Trees were prevented from falling
570
into an adjacent heathy mire by a fringe of tall myrtaceous shrubs.
571
The preceding examples act through nutrient enhancement. In other switches, nutrients are
572
depleted. In pygmy forest in northern California, Northup et al. (1998) found that the leaves and
573
therefore the litter are high in polyphenols and condensed tannins. The decomposition of this litter is
574
slow, and the soil is therefore low in mineral nutrients, especially N. These conditions are tolerated by
575
the species that grow there but not by possible invaders. In Picea sitchensis (sikta spruce) forests in
576
northern Sweden, the low shrub Empetrum hermaphroditum (crowberry), already present as
577
understorey, can switch nutrient regimes in its favour after cooler forest fires (Mallik 2003). Its litter has
578
a high phenolic content, lowering the pH, sequestering available nitrogen and leaching out metallic ions.
579
These are conditions that it can tolerate. The phenolics also inhibit the development of conifer
580
mycorrhizae. Lowering of the pH and toleration of that low pH seems a common switch, e.g. in many
581
Ericaceae (heather/heath) and Pinus species. The acidification can be effected by either their living or
582
dead parts. In Britain Calluna vulgaris (heather) litter is acid, peat-forming and maintains the acid,
583
oligotrophic nature of the C. vulgaris habitat. Many switches combine a lowering of the pH with a
584
lowering of nutrient availability, as in the Empetrum hermaphroditum example. Low pH, low nutrients
585
and waterlogging are part of a similar switch in paludification and bog growth (chap. 2, sect. 5.6 above;
586
J.B. Wilson and Agnew 1992).
587
Species that interfere with their neighbours by allelopathy, and thereby benefit and are able to
588
further their allelopathic activity, also operate a switch (Odling-Smee et al. 2003). So can heavy-metal
589
hyperaccumulators, species that are resistant to the high levels of Zn, Cd, Cr, Ni, etc. on metaliferous
590
soils and accumulate those metals to very high concentrations (J.B. Wilson and Agnew 1992; Boyd and
591
Jaffré 2001). Concentrations in the shoot have been recorded in the order of 10,000 times that in the soil
592
solution for Zn and 600 times for Cd (Knight et al. 1997). The litter of these plants might raise the
593
available concentrations of such elements in the surface soil to levels that they can tolerate but other
594
species cannot (Boyd and Jaffré 2001), reinforcing their abundance in the site. An analogous salt-
595
mediated switch operates for species which absorb saline water from the lower layers of the soil,
596
increases the salinity of the surface soil by its litter, and is able to tolerate this better than its
597
competitors.
598
A much studied, though complicated, switch occurs in some shallow lakes that can have two
599
alternative stable states: clear and turbid (Scheffer et al. 1993). In the clear state, submerged aquatic
600
vegetation is abundant. Conditions are oligotrophic, low especially in P, allowing little phytoplankton
601
growth and few fish. Macrophytes such as members of the Nymphaeaceae (water lilies) can shelter algal
602
herbivores such as Cladocera species (water fleas), which then keep the algal populations low and
603
hence the water clear (Stansfield et al. 1997). Allelochemicals produced by Chara spp. may also
604
suppress the algae (van Donk and van de Bund 2002). In the turbid state, fish movement causes
Wilson & Agnew, chapter 3, Community processes, page 21 of 49
605
turbidity, which stirs up sediment giving eutrophy and therefore phytoplankton growth, but the sediment
606
reduces light penetration and therefore suppresses submerged macrophyte growth. Food chains are
607
critical. Jones and Sayer (2003) suggest that, in eastern England, fish control the epiphytic grazers,
608
which control the periphyton (algae attached to macrophytes) which controls the macrophytes. That is to
609
say, with too many fish, the periphyton kills the macrophytes, and with no fish the macrophytes are
610
dominant. The switch mediating agents are nutrients, light and fish. Although there are variants, this is
611
an exceptionally well-documented switch.
612
van Nes et al. (2002) modelled the proposed clear/turbid mechanisms, and were able to produce
613
alternative stable states (ASS; sect. 5.6 below). The most critical parameter in their model was the
614
degree to which plants lowered the local turbidity. ASS developed most readily in shallow lakes with
615
uniform depth, or where there was little mixing, or to a lesser extent where there was little mixing of
616
water between areas of different depth. Evidence that alternative stable states exist alongside each other
617
in the real world can be seen in similar lakes, some in one state and some in the other, in natural state
618
changes, and in state changes effected by experimental manipulations (e.g. S.F. Mitchell et al. 1989;
619
Scheffer et al. 1993). Lakes naturally accumulate nutrients from inwash, and trap them through
620
sedimentation and in macrophytic vegetation. The critical point at which a change from one ASS to
621
another occurs appears to depend on initial state and the sedimentation rate (Janse 1997) which must
622
have to do with nutrients. Reversal may or may not occur readily (Körner 2001). For example, Blindow
623
et al. (1993) described two moderately eutrophic, shallow lakes in southern Sweden that have during the
624
past few decades changed several times between the two states. In both lakes, water level fluctuations
625
were the most common factor causing shifts. Blindow et al. (2002) examined one of these lakes in
626
detail, and found that the chlorophyll : total-phosphorus (dissolved, suspended + plankton) ratio
627
declined from April to September, strongly suggesting that some other factor, such as carbon limitation
628
and/or allelopathy by the submerged charophytes, might be controlling the phytoplankton. Hargeby et
629
al. (2004) recorded a change to the turbid state after there had been 30 years of the clear-water state. It
630
occurred over two years with mild winters which increased fish populations, thus increasing
631
bioturbation and nutrient cycling, combined with cool springs which hindered the establishment of
632
macrophytes.
633
Experiments are the key to understanding the workings of communities. Schrage and Downing
634
(2004) removed 75 % of the benthivorous fish from a lake. One immediate effect was a decrease in
635
suspended sediment (probably due to reduced fish movement), and reduced phosphate and ammonia
636
(probably due to both the reduced sediment load and reduced fish excretion). There was an increase in
637
zooplankton, which seemed to lead to a reduction in phytoplankton. These two led to an increase in
638
water clarity, which may have been the cause in an increase in macrophyte frequency. Thus all the
639
elements of a turbidity switch are present. However the lake reverted after two months to its previous
640
state, so an alternative stable state was not induced.
Wilson & Agnew, chapter 3, Community processes, page 22 of 49
641
5.4.F Mechanisms involving disturbance
642
There are many ways by which a switch can operate through disturbance. We dealt with
643
autogenic disturbance in the last chapter. If lianas can facilitate gap formation (chap. 2, sect. 6.3) they
644
would favour regrowth of their own life form in forest gaps, possibly constituting a switch by which
645
lianas maintain themselves. Where tidally inundated marsh vegetation occurs, ecesis is unlikely because
646
of disturbance, but Bertness and Yeh (1994) describe how the erect stems of marsh elder (Iva
647
frutescens) can trap so much water-borne litter that the underlying marsh vegetation dies, allowing its
648
own seedlings to survive. These plant canopies also reduce evapotranspiration and thus surface
649
salinities. This switch maintains marsh elder thickets and is dependent on litter for initiation.
650
Disturbance through fire is a major factor in creating vegetation edges because certain vegetation
651
types are fire resistant and fire promoting, whilst other types are susceptible to fire but do not readily
652
carry it. The South African fynbos shrubland is fire-prone and depends on fire for its persistence, while
653
adjacent closed forest is fire resistant (Manders and Richardson 1992). Both vegetation types benefit
654
from increased water availability (Manders and Smith 1992) but only during wet years can tree
655
seedlings establish in the shrubland. They can then grow to become fruiting nuclei of forest. The fire
656
regime maintains the balance between the two types.
657
Disturbance by humans can also be noted here. Humans follow paths and behaviour patterns in
658
vegetation which are repeated and predictable. The effect on vegetation is to reduce plant height and
659
production which in turn invite foot passage, so that this is a switch between vegetation types (J.B.
660
Wilson and King 1995).
661
5.4.G Mechanisms involving heterotrophs
662
Mycorrhizae present a somewhat different case, since they enhance nutrient uptake and need no
663
external driver, although they can be dependent on litter for long term survival (Vogt et al. 1995). They
664
are essential to nutrient uptake in many nutrient stressed situations. Although we have no examples
665
showing that mycorrhizae are solely responsible for the spread of a species or vegetation type, the
666
dominance of a vegetation type in an oligotrophic habitat and its abrupt edge can be due to this
667
association. The natural history of mycorrhizae is so complex and important that it is still difficult to
668
assess their rôle, whether imperative or facilitative, in plant community dynamics. There are many
669
examples of these interactions: Meadows resulting from abandoned beaver dams in northern Minnesota
670
resist invasion by the surrounding Picea mariana demonstrably through a lack of ectotrophic
671
mycorrhizal fungi (Terwilliger and Pastor 1999). It is clear that there is still much complexity to be
672
unravelled, some of which may constitute switch mechanisms, maintaining boundaries or changing
673
community structure.
674
675
Animal invasion can markedly alter plant communities, but this cannot comprise a switch unless
the community type both attracts and benefits from the animal exploitation. Much of the material is
Wilson & Agnew, chapter 3, Community processes, page 23 of 49
676
speculative. We shall consider two major mechanisms: the effect of browsing and grazing and the effect
677
of frugivores on seed dispersal.
678
Grazers can be switch mediating agents if they are encouraged by a particular type of vegetation
679
cover, and promote it. For example, in grass openings in woodland, large mammal grazers crowd the
680
woodland/grassland ecotone for predator escape (Lamprey 1964). They sharpen the ecotone by
681
removing or trampling any outlying tree seedlings and prevent the woodland from spreading. Much of
682
the speculation on this situation has concerned East Africa, in explanation of the apparent ASS of
683
grassland and Acacia spp. woodland (van de Koppel and Prins 1998). On abandoned agricultural land
684
and range in western Europe, Equus caballus and E. assinus (horses and asses) defecate in preferred
685
sites which they fastidiously avoid for grazing, creating within the meadow thorny patches of Prunus
686
spinosus (blackthorn) and Rubus spp. (brambles) that protect regenerating trees, leading to a mosaic of
687
forest with grassland openings (Bakker et al. 2004; Kuiters and Slim 2003). This seems to be a zero-sum
688
switch, because the thorny patches divert the equines onto the grassy areas, but the area of those limits
689
the animal population numbers.
690
Again, Augustine et al. (1998) describe how ASS can arise when high numbers of white-tailed
691
deer (Odocoileus virginianus) trample Laportea canadensis (Urticaceae) populations. At high
692
L. canadensis plant densities, the plant population survives because O. virginianus avoid the area, while
693
at initially low densities, L. canadensis is trampled as O. virginianus pass and it disappears. This also
694
seems to be a zero-sum switch. Futuyma and Wasseman (1980) described a situation in which Alsophila
695
pometaria (fall cankerworm) adults emerge from pupae in spring. They lay their eggs, the first larvae
696
emerge at about the time Quercus coccinea (scarlet oak) comes into leaf and larval emergence
697
continuess Q. alba (white oak) leafs out. The larvae need young leaves to survive. Therefore, in stands
698
where Q. coccinea is in the minority it suffers more herbivory, presumably reducing its fitness and
699
maintaining the dominance of Q. alba. The converse process would, in stands dominated by Q.
700
coccinea, maintain its dominance. This process could result in ASS in the field, but this has not been
701
demonstrated.
702
Dispersal can mediate switches. We described resource islands above with regards to nutrients,
703
but patches of seedlings around foci can also be produced by perching frugivores. If the plant species is
704
a preferred food of the frugivore, this benefits the frugivore population, constituting a switch.
705
Germinable seeds can be dropped during eating, defecated by the bird around the tree, or carried by/in
706
the bird to establish a new focus (Herrera et al. 1994). In this way, patches of forest can arise around
707
isolated trees (Archer et al. 1988). Dispersers/consumers of nuts could operate a switch when they are
708
dependent on the fruit for food, but benefit the plant by protecting the fruit from other predators, bury
709
them in sites that are probably favourable for establishment, and disperse them away from the tree and
710
perhaps into new areas (Vanderwall 2001). A suite of Fabaceae (legumes) in African savannahs have
711
indehiscent, carbohydrate-loaded pods which are eaten by browsers. The seeds within are refractory and
Wilson & Agnew, chapter 3, Community processes, page 24 of 49
712
they germinate faster after scarification, which can occur during their passage through the gut.
713
Deposition in dung is clearly helpful in seedling establishment. Many browsers concentrate their dry
714
season feeding on such legumes. Many of these are woodland trees (Baikiaea spp., Cassia spp.,
715
Pterocarpus spp. in Miombo woodland; Stokke 1999), and the process maintains the vegetation type.
716
Acacia tortilis (umbrella thorn) and A. erioloba (camel thorn) often grow as isolated trees in rangeland,
717
and can develop into thickets. M.F. Miller (1995) and Dudley (1999) have shown that the pod resource
718
is indeed heavily utilized by browsers and ungulates, and that there is an enhanced germination effect,
719
but other suites of rodents, birds and beetles are also involved in a complex system. Pollinators could
720
mediate a switch in a similar way.
721
A similar switch could operate in which increase in the population of a host-specific pollinator
722
(perhaps an orchid) increased the seed set of species A, leading to greater abundance or a greater spread
723
of species A, leading to there being more nectar/pollen for the pollinator, increasing the population of
724
the pollinator: positive feedback.
725
5.5 Switch evolution
726
J.B. Wilson and Agnew (1992) suggested that switches would be more common than facilitation,
727
because there would be selection for genotypes with reactions that favoured the species producing them
728
over those with reactions that disfavoured them. This is a Gaia-type idea (Lenton and van Oijen 2002),
729
be it a rather mild one. At first sight, the argument seems logical. All plants, like other organisms, effect
730
reaction (Clements 1916; Miles 1985, van Breemen and Finzi 1988; Odling-Smee 1988). For example a
731
plant is bound to shade another plant below it. A switch could arise by chance: characters which were the
732
result of selection for other reasons could happen to give the plant an ability to change its environment in a
733
way that gave it benefits relative to its neighbours. If reaction arose at random, we would expect 50 % of
734
cases to be negative feedback (i.e. facilitation), and 50 % positive feedback (i.e. switches). However, the
735
genotype of each plant will determine the direction and extent of its reaction, and natural selection must
736
operate on that genetic variation. There are hints of the evolution of switches in the endemic varieties that
737
Northup et al. (1998) found on old soils in northern California (section 2 above), where it is possible
738
that the ecotypes evolve towards soil modification, which leads to further ecotype differentiation, etc.
739
Odling-Smee et al. (2003) also conclude that ‘niche construction’ [i.e. reaction] “is a fact of
740
life”. They do not seem so concerned with a population’s affecting its own fitness, but with the causal
741
change: current population → environment modification → next-generation population. Applying this
742
to switch evolution, they say: “We define ecological inheritance as any case in which organisms
743
encounter a modified feature-factor relationship between themselves and their environment where the
744
change in the selective pressures is a consequence of the prior niche construction by parents or other
745
ancestral organisms”. They use the term ‘positive niche construction’ for a switch, giving the examples
746
of allelopathy and fire, and conclude that selection will occur for adaptations that allow organisms to
Wilson & Agnew, chapter 3, Community processes, page 25 of 49
747
carry out their [presumably positive] niche construction with greater efficiency. Laland et al. (1996;
748
1999) also analysed the effect of reaction on the selection process, and concluded there could be strong
749
selection for switches, perhaps leading to the fixation of otherwise deleterious genes.
750
We have to be careful here, almost to the point of disagreeing with ourselves (J.B. Wilson and
751
Agnew 1992). Darwinian selection operates at the level of the individual genotype. A mutant that
752
produces a reaction favourable to that individual plant (genet, technically) could lead to the evolution of
753
a switch. However, this supposes an unlikely degree of independence between coexisting genotypes in
754
their reaction and response – that the mutation benefits only that one individual. We must be careful if
755
we apply this logic to a mutant that produces a reaction that benefits a whole population of the species,
756
because that mutation will have no selective advantage over the ‘wild type’. Selection cannot operate if
757
everyone benefits. Moreover, many of the plant features causing a switch will have a cost. For example,
758
fire, allelopathy and herbivory defence switches can involve the production of secondary compounds,
759
which are expensive energetically. If a character has a cost and benefits a plant’s neighbours, it must be
760
characterised as altruistic, and can evolve only by a group selection mechanism (Wade 1978). The most
761
likely mechanism for plants is local kin selection, in which a plant benefits its neighbours who are likely
762
to be somewhat related to it. However, such selection operates only within a limited range of
763
parameters, and is a weak force (J.B. Wilson 1987).
764
We conclude that Darwinian selection would be possible if the reaction were so local that the
765
plant benefits only itself (e.g. produces litter just under itself), or at least with little benefit to neighbours
766
of the same species. If the effect were a little more widespread, but local enough for most of the plants
767
benefiting to be related to the mutant, the trait could possibly evolve by kin selection. The situation is
768
not as clear-cut as J.B. Wilson and Agnew (1992) supposed. Perhaps most switches arise by accident,
769
not by adaptation.
770
5.6 Alternative stable states
771
In regions of apparently uniform terrain and climatic regime, such as grassland on alluvial
772
plains, there may be vegetation states that are persistent and different, but impossible to relate to
773
variations in the substrate or ambient conditions. The different states could coexist side-by-side in a
774
mosaic, or they could exist in the same site at different times. Such communities are known as
775
alternative stable states (ASS). It is assumed that either state could exist there, but that each is stable, so
776
there is a vegetation-dynamics barrier to be crossed moving from one to another. There are three criteria
777
for ASS (Connell and Sousa 1983):
778
1. The states, differing in species composition, occur in the same environment.
779
The perturbation causing the original change in species composition in space or time appeared as a
780
781
pulse, or by “chance”.
The states are stable.
Wilson & Agnew, chapter 3, Community processes, page 26 of 49
782
These criteria are difficult. For ‘1’, the states must be held by interactions caused by the different
783
species compositions, but then almost all species interactions are via reaction: i.e. a change in the
784
environment. Thus, criterion ‘1’ is impossible to meet literally. Some types of reaction such as light are
785
instantaneous but some such as soil characters have persistence. A realistic criterion would be that the
786
differences in environment are small and of a type probably caused by the plants themselves. For ‘2’,
787
we can rarely see the origin of the states in nature. A perturbation is normally taken to be an
788
environmental or biotic condition outside the normal range, appearing stochastically in time. We have to
789
distinguish between: (a) ‘press’ perturbations, where the difference between treatments is continued, e.g.
790
where there is continued grazing versus none, versus (b) pulse perturbations, where the change in
791
environment is temporary. Some pulse perturbations (shocks, instantaneous perturbations) really are
792
instantaneous, e.g. the removal of plants. Other types of ‘pulse’ perturbation can be applied
793
instantaneously but the environmental change persists for some time, such as a single fertiliser
794
application. However, in the context of ASS the origin of the different states should be historical factors
795
such as management or transient environmental differences that disappeared long ago, random dispersal,
796
the season of establishment by the community founders, or environmental patchiness subtle enough to
797
have been overwhelmed without the establishment of ASS. The critical item is that no continuing
798
environmental pressure is applied that is different between the states. For ‘3’ we theoretically have to
799
apply an infinitely small perturbation and show that the system regains its original state, at least after
800
infinite time (sect 7.3 below). Persistence in the face of natural perturbations is often used as a
801
substitute. We see three processes for maintaining an ASS state, that is a mosaic in space and/or time:
802
1. Spatial resource accumulation and depletion: A switch might result in spatial patches of better-
803
resourced systems in a depleted hinterland. Since accumulation causes depletion this is a Zero-
804
sum (Type 2) switch (Fig. 3.8).
Wilson & Agnew, chapter 3, Community processes, page 27 of 49
Depleted
matrix
Depleted
matrix
Higher
resouce
system
Higher
resouce
system
patch
patch
Depleted
matrix
Higher
resouce
system
patch
Fig. 3.8. Maintenance of alternative stable states in space by a Zero-sum switch, comprising
spatial resource accumulation and depletion. [with fuzzy edges]
805
806
2. Boundary sharpening: Patchiness in the physical environment such as a difference in soil water
807
flow, or variation in a biotic effect such as mycorrhizae – any of the initial differences that we
808
discussed above – could be converted to a spatial mosaic of ASS by boundary sharpening
809
through a switch of any of the types, 1-4.
810
3. Reinforcement. Once a state is established in an area, it can be held against a state change by a
811
one-sided switch (Type 1).
812
The maintenance of alternative stable states is almost inevitably due to a switch. As in the ball-and-cup
813
analogy, although there is stability a sufficiently large pulse perturbation can overcome the resistance
814
and cause a state change (sect. 7.4 below). The ASS concept is close to the theoretical concepts of
815
"Several stable points" (Lewontin 1969) or "Multiple stable points from one initial condition"
816
(Sutherland 1974), though in such papers the crucial involvement of reaction has not generally been
817
elaborated. We should probably examine which type of switch is operating and through which
818
mediating agent before we draw curves of hysteresis or do matrix algebra on “multiple domains of
819
attraction” (Gilpin and Case 1976).
820
Theory
821
Contrary to our wish to examine ecological mechanisms before generating theory, much of the
822
consideration of ASS has been by mathematics or simulation. Luh and Pimm (1993) and Samuels and
823
Drake (1997) have proposed the Humpty-Dumpty principle: that it might not be possible for
824
communities to re-assemble from their constituent species after a perturbation. This might be because
825
the original species composition was based on a switch, originated by the elusive process of ‘chance’.
826
Platt and Connell (2003) argued that secondary successions might be more liable to the initiation of
Wilson & Agnew, chapter 3, Community processes, page 28 of 49
827
ASS, since where there is stochastic establishment by survivors, alternative paths of vegetation
828
development may exist. Another possible cause of a Humpty-Dumpty effect is that succession fails
829
because intermediate species in the assembly process are missing (cf. Samuels and Drake 1997), though
830
this seems a very rigorous interpretation of succession. Law and Morton (1996) modelled the formation
831
of a mosaic of ASS by this process. Van Nes and Scheffer (2004) used a relatively simple Lotka Volterra
832
model and a community matrix to show that alternative stable states can arise in rich mixtures where intra-
833
is less than inter-specific competition, a process driven by negative feedback in contrast to the positive
834
feedback of switches but which seems unlikely in the real world (chap. 4, sect. 7 below). Chase (2003)
835
suggested that alternative stable states were more likely to exist when the regional species pool (if we
836
can ever define that) is large. He argued that with more species there will be more redundancy (i.e.
837
species similar in alpha niche). The trouble with this is that if the species are so similar as to be
838
redundant, the states will not be alternative in reaction. If they are somewhat different, one species will
839
replace another on a path that approaches equilibrium convergence, so the states will not be ASS.
840
Similar reasoning can be applied to his suggestion that less dispersal will increase the likelihood of
841
alternative stable states: a state is not stable just because species find it hard to disperse to the site.
842
Examples
843
It is much harder to find evidence that ASS actually exist. Most investigations cited in reviews
844
as having good evidence of ASS are of freshwater lab microcosms, a few of mesocosms (Schröder et al.
845
2005). Even with those studies, a major problem has been lack of time for it to be clear that the
846
communities are not converging. For example, an experiment by Robinson and Dickerson (1987)
847
introduced species in two orders and at two slightly different rates, and found differences in species
848
frequencies, but the results were analysed on weeks 13-23 of the experiment when first-introductions of
849
a species occurred up to week 8, and re-introductions occurred right up to week 13. Drake (1991)
850
performed similar experiments, again finding that the order of introduction of the autotrophs
851
significantly affected their relative abundance, but the last introduction of an autotroph was on day 180
852
and the final census only 15 days later. Chlamydomonas reinhardtii was the species most likely to end
853
up as a minor component, but this happened most notably in the two treatments where it was the first
854
autotroph to be introduced, i.e. where there had been most time for it to have been excluded by
855
interference. This gives the impression of a competitive hierarchy more than alternative stable states.
856
Coming to the field, Vandermeer et al. (2004) tracked regeneration in Nicaraguan tropical forest
857
over nine years after destruction by a hurricane, and found floristic divergence, especially initially. This
858
would be an illustration of "multiple basins of attraction": ASS. Yet it is questionable whether their time
859
span was long enough, because four out of the six stand comparisons became more similar in the last two
860
years of observation reported.
Wilson & Agnew, chapter 3, Community processes, page 29 of 49
861
So many switches have to do with water stress that it is not surprising that most claims of ASS
862
have been reported from arid lands. Moreover, the frequently patchy nature of vegetation in deserts
863
suggests the possibility of ASS. Rainfall in arid lands is erratic with much coming in storm events.
864
Infiltration is often impeded if the bare soil surface is static with a stone armour or with a cryptogamic
865
crust (Verrecchia et al. 1995). Litter reduces the impact of raindrops on the soil surface, and roots
866
provide soil channels for infiltration. Infiltration can be increased by rodent burrows, soil caches and ant
867
nests, which also increase nutrient capital. This can give an autogenic pattern, with shrubs/trees causing
868
and being supported by infiltration, and the droughted gaps between being bare or covered with grasses
869
and their associates (Tongway et al. 2001). Such patterns can be seen in savannahs, shrublands and
870
grassland, on gravelly soil and in arid/semi-arid areas. The most notable example is ‘tiger bush’, lines of
871
dense woody plant growth at right angles to the direction of gently sloping land under low and variable
872
rainfall regimes. The phenomenon is certainly caused by surface run-off in the inter-stripe zone, onto
873
the vegetation stripe, which has been shown to have much higher soil infiltration rates (Berg and
874
Dunkerley 2004). Van de Koppel et al. (2002) and Shnerb et al. (2003) modelled the process, showing
875
that the formation of tiger bush occurs in a specific range of precipitation. J.B. Wilson and Agnew
876
(1992) interpreted this as a zero-sum switch, because the increase in water by one phase (by infiltration)
877
reduced the water available to the other phase (by reduced runoff), though there can be evaporation
878
from inter-stripe areas in minor rainfall events (*Hierniaux and Gerard 1999). Naturally it is difficult to
879
confirm that these are ASS due to the long timescales involved.
880
Schröder et al. (2005) could find only two examples of ASS that they believed were
881
convincingly demonstrated in the field. One is the situation examined in several studies by R.L. Jefferies
882
and co-workers, and summarised by J.B. Wilson and Agnew (1992) as a switch in “Grazing and nitrogen
883
cycling”. Schröder et al. cite a more recent paper (Handa et al. 2002) where the bare patches at the top of
884
the marsh were hardly being re-colonised, and vegetation could not be re-established. The soil had
885
become hyper-saline due to greater evaporation rates there (Srivastava and Jefferies 1995). This is akin
886
to a switch of the saltmarsh pan type (J.B. Wilson and Agnew 1992), except that Srivastava and
887
Jefferies suggest the salt is coming from buried sediments. N.A. Walker et al. (2003) showed by
888
modelling that nitrogen dynamics, with input from N-fixing bluegreen algae and N export in goose
889
emigration could also explain the alternative stable states in this system. Thus, the mosaic on the ground
890
is a clear hint that a switch is operating, though state changes between the two ASS do not seem to have
891
been reported and it is not clear through which factor the switch is primarily mediated. Schröder et al.’s
892
other example was an experiment by Schmitz (2004) removing a predator spider Pisaurina mira,
893
therefore releasing grasshopper Melanoplus femurrubrum herbivores, which hid in and ate Poa
894
pratensis (meadow grass), releasing Solidago rugosa (goldenrod) which suppressed other forbs. Got it?
895
When predators were allowed back after 2 or 3 yr, the cover of S. rugosa remained high for 3 or 2 yr
Wilson & Agnew, chapter 3, Community processes, page 30 of 49
896
respectively. Schmitz offers no explanation beyond “loss of top predator control”. It seems that,
897
unfortunately, the cover values were guessed.
898
Possibly the situation where the switch mechanism behind ASS has been most clearly
899
demonstrated is in dune slacks on Texel, The Netherlands. Adema et al. (2002) found two seral stages
900
side by side, with a boundary that had been static through 62 years of observation. Having investigated
901
and dismissed all possible environmental reasons for this stasis they surmise that it must be due to some
902
“positive feedback mechanism” (i.e. a switch) involving nutrient cycling or sulphide toxicity. Two early
903
successional species Littorella uniflora (shoreweed) and Schoenus nigricans (bog-rush), release oxygen
904
into the soil allowing greater oxidation of ammonium to nitrate (cf. Adema and Grootjans 2003), and
905
then denitrification to gaseous nitrogen (Adema et al. 2005) . This could hold up succession. To
906
complete the story we would need to know that early successional species are more tolerant of low N,
907
and there is some experimental evidence that both L. uniflora and S. nigricans grow better at low N
908
availability and grow more slowly at high N availability compared to Carex nigra and Calamagrostis
909
epigejos (E.B. Adema pers. comm.).
910
If ASS exist in an area we should be able to see what type of perturbation can cause a state
911
change between them. There are many state-and-change flow diagrams in the literature, for example
912
comprising a whole issue of Tropical Grasslands, indicating the conditions under which each state
913
change occurs, but unfortunately they are all speculation. Oliva et al. (1998) was experimentally unable
914
to confirm a state-and-change system proposed from open grasslands to dwarf shrublands in Patagonia
915
in a 10-year trial, and Valone et al. (2002), who were interested in the grassland/shrubland mosaic,
916
found that after 20 years without grazing there was little change in the shrubland. They suggested that
917
there may be considerable lag times before any changes could be seen. The experience of land managers
918
is that intermediate states are much shorter-lived and state changes can be predicted from management
919
changes. We are not doubting that state changes occur, we are just calling for attempts to document
920
them.
921
Chase (2003) used examples to conclude that “… evidence suggests that community assembly
922
can lead to multiple stable equilibria”, and then goes on to start with an assumption: “Sometimes history
923
matters, creating multiple stable equilibria …”. We believe switches are common and important in
924
vegetation, and switches should often lead to ASS, but there is very little evidence yet to support their
925
existence. It may be that ASS are the explanation for much of the patchiness that we see in vegetation,
926
due to alternative trajectories of change (divergence) in vegetation in response to the same disturbance,
927
but at different times with different biotic and/or physical environment (B.H. Walker 1993; Whisenant
928
and Wagstaff 1995; Lockwood and Lockwood 1993), or different vegetation conditions at the time
929
(Watson et al. 1996). This possibility has rarely been investigated, S. Walker and Wilson (2002) did so
930
in dry grassland in southern NZ, and found no evidence for it. Nevertheless, so far as our present
Wilson & Agnew, chapter 3, Community processes, page 31 of 49
931
knowledge goes, to adapt Frank Egler’s phrase, ASS are “one of the more nauseating but delightful
932
idiocies that stem from the heart, not the mind, of otherwise respectable scientists”.
933
5.7 Negative feedback
934
Positive feedback means that a process P produces a condition/product C and that change in C
935
increases the rate of process P as a switch. Negative feedback means that a process P produces a
936
condition/product C and that change in C decreases the rate of process P. Negative feedback at the
937
whole-community level occur at the end of a succession (the climax) or in one of several alternative
938
stable states. The result is stability and the speed at which the negative feedback occurs is resilience. We
939
discuss these concepts below. However, we note that the negative feedback occurs primarily at the level
940
of individual species, be they interacting ones.
941
6 Diversity → productivity
942
943
There are two major possible outcomes of niche differentiation between species: overyield and
stability.
Wilson & Agnew, chapter 3, Community processes, page 32 of 49
(b) RYT relative
(c) Transgressive
overyielding
overyielding
100% A
50:50 100%B
mixture
Biomass of A
Biomass of A
Biomass of B
50:50 100%B
mixture
Biomass of B
Biomass of B
100% A
Biomass of A
(a) RYM arithmetic
overyielding
100% A
50:50 100%B
mixture
Fig. 3.9. In ‘a’ there is arithmetic overyielding: the absolute gain by A in mixture is greater than the
loss by B so RYM > 1.0. In ‘b’ the relative gain by B is greater than the loss by A so RYT >
1.0, in ‘c’ some mixtures yield more than either monoculture. For definitions of RYM and
RYT see Wilson (1988c).
interaction,
= theoretical biomass of each species with no
= actual biomass of each species,
= total biomass of the mixture.
944
Overyield is the situation in which higher species richness leads to higher total biomass, perhaps as a
945
result of niche differentiation (Fig. 3.9). Investigation of this topic had been fraught with problems, the
946
most important being the ‘selection effect’. If a mixture of species is sown/planted in an experiment, the
947
more competitive species will come to dominate. The more species are planted in the mixture, the
948
greater the probability that one or more of these highly-competitive species will be included in the mix
949
and will take over. If species with high competitive ability also have high production (and note this ‘if’),
950
the result will be higher production for the mixture: the selection effect. In terms of seeking the results
951
of niche differentiation this is an artefact. There is no easy way of looking at the biomass results to
952
know whether simple overyielding (Fig. 3.9a) has been caused by niche differentiation or by the
953
selection effect. However, if the production of the mixture is greater than that of any of the
954
monocultures (‘transgressive overyielding’: Fig. 3.9 c) the selection effect can be ruled out. Niche
955
differentiation is the obvious cause, though explanations in terms of subvention or interactions with
956
heterotrophs are possible. Loreau and Hector (2001) introduced a mathematical separation of the
957
selection and niche differentiation effects. They found that there was significant evidence of a positive
958
selection effect in only two BioDepth experimental localities out of nine, and a negative effect in one
959
(suggesting that the stronger competitor was of lower yield). In contrast, there was significant evidence
960
for niche complementarity in four localities. However, we suggest that if transgressive overyielding is
961
not seen, the results are not of great ecological significance.
962
Experiments to detect overyielding have been fashionable of late, but with mixed results. Tilman
963
et al. (2001) planted field plots at Cedar Creek in a range of species richnesses up to 16, from a pool of
964
18 species in 1994, and analysed in 1999 and 2000. There was evidence that some mixtures of grassland
965
species could outyield the highest-yielding monocultures, especially several years after establishment.
Wilson & Agnew, chapter 3, Community processes, page 33 of 49
966
Lambers et al. (2004) examined the same plots, analysed up to 2002. Over/underyielding spp were
967
determined by regression of yield on diversity. Compared to the -1 slope on log-log basis expected
968
under a null model, six species significantly overyielded and four underyielded. There was no time trend
969
for overyielders to replace underyielders, which is strange. Whittington and O’Brien (1968) planted
970
field plots with Lolium perenne (ryegrass), Festuca pratensis (meadow fescue) and their triploid hybrid.
971
Transgressive yielding was seen in the ‘grazing’ (i.e. low-cut) treatment only sporadically in the first
972
two years, but almost constantly in the third. In two of the mixtures, the two components had diverged
973
in their proportional contribution to the sward. The overyield can be attributed to niche differentiation in
974
the depth of nutrient uptake. L. perenne and F. pratensis grown in monoculture took up very similar
975
percentages of their P from 10, 30 and 60 cm (35/40/25 versus 38/35/27) (O’Brien et al. 1967). Yet
976
when they were grown together L. perenne took up its P from deeper (33/22/45) and F. pratensis from
977
nearer the surface (41/34/25). In contrast, when grown with the deeper-rooted hybrid (monoculture
978
uptake 18/36/47) L. perenne utilised the surface P (56/26/18).
979
There is a tendency in such experiments to find that if overyield is reached, then it is after
980
several years’ growth. One explanation for this is that time is required for the species to sort themselves
981
into their respective niches, e.g. in the canopy or in rooting depth. Another possibility is that overyield is
982
attained only with a certain optimum proportion of each species (as can be seen in many of the results of
983
de Wit’s group) and time is needed for the species to reach these proportions. Possibly, as in
984
Whittaker’s (1965) Niche-preemption concept, the dominant species takes all the resources it can and
985
subordinate species remain in minor amounts to pick up the crumbs that fall from the strong man’s
986
table.
987
Overyielding does not necessarily develop. Hooper and Dukes (2004) planted field plots with
988
local grassland species and followed them for an impressive eight years, giving the species time to reach
989
their optimal niches and their optimal proportions (as discussed above), but no significant transgressive
990
overyielding was seen. On the other hand, Roscher et al. (2005) ran a field experiment in Germany for
991
only one year, sowing nine species characteristic of grasslands of the site. Two-thirds of the plots
992
showed transgressive overyielding, though the effect was highest in 2-species mixtures. Analyses to
993
separate the selection effect from niche complementarity using the method of Loreau and Hector (2001)
994
showed that complementarity reached its peak at 4-species.
995
7 Stability
996
7.1
997
Concept
The question is raised several times in this book of whether any plant community we see is an
998
arbitrary assemblage of species, such that another assemblage might well have existed at that time and
999
place, or whether determinism is involved. There are three possible answers:
Wilson & Agnew, chapter 3, Community processes, page 34 of 49
1000
1001
1002
1003
1. Global stability, with one state: There is only one possible state, at least after there has been
sufficient time for succession to have done its work. This is deterministic community structure.
ASS, with a few states: There is a limited number of possible states. This is the Alternative Stable
States concept discussed above.
1004
A continuous range of states. There is a large number of possible species assemblages, in terms of
1005
species presence and abundance, with all intermediates. The present assemblage exists for
1006
historical or even stochastic reasons, and after a perturbation or even as a result of drift another
1007
state might take its place.
1008
The critical test here is recovery from pulse perturbation (sects. 5.6 above, 7.3 below). If the community
1009
always recovers to the same state, it is globally stable, situation ‘1’ above. If the system is stable to
1010
small perturbations, but not to large ones, situation ‘2’ obtains. If the community does not recover to its
1011
original state after a perturbation, we assume situation ‘3’. We can doubt ‘3’ from our common
1012
observation as ecologists: if it were true we would have no predictive view of landscape. In fact we
1013
generally know what species to expect in a set of environmental conditions. We may sometimes be
1014
surprised, which is a prima facie case for ‘2’, alternative stable states.
1015
Seeing long-term continuance of a range of plant communities – forests, heaths, bogs and arctic
1016
alpines – we intuitively envisage the continuance as stability. However, the difficulty of defining this
1017
kind of stability, plus a little mathematics envy, has led ecology into accepting Liapunov stability as the
1018
true stability. We therefore have various features of the ‘stability’ (sensu lato) of a community:
1019
1. Reliability: Constancy, lack of change probably in spite of minor perturbation.
1020
2. Stability sensu stricto, i.e. Liapunov stability: whether the community ever recovers from a small
1021
1022
1023
1024
pulse perturbation.
3. Resistance: Lack of change upon a pulse (i.e. temporary) perturbation. We separate it here into
resistance to abiotic perturbation and resistance to invasion.
4. Resilience: Rate of recovery from perturbation.
1025
All these concepts assume that the ecological system is at equilibrium, and probably in the real world
1026
none ever is, but the concepts are real. All this leaves open the questions: change in what?, recovery in
1027
what? Here at least we are free from the mathematicians to ask whatever ecologically meaningful
1028
question we feel pressing. The change/recovery can be:
1029
1. Functional: This can be production (best defined, as we discussed in chapter 1, as energy passed
1030
on to the next trophic levels), nutrient cycling, water output, or any other result of whole-
1031
community processes.
1032
2. Guilds: The proportions of certain guilds, i.e. the guild structure.
1033
3. Species composition: Change/recovery in species presence and/or abundance, i.e. floristic
1034
structure.
Wilson & Agnew, chapter 3, Community processes, page 35 of 49
1035
Most general discussions of stability refer to species-composition change/recovery, which is easier to
1036
measure. The categories are asymmetrically related – e.g. there can be functional constancy without
1037
constancy in species composition if species change but the productivity (e.g.) does not, and without
1038
constancy in guild representation. Species composition stability encompasses the other two types of
1039
stability, for if the species in the vegetation do not change, qualitatively and quantitatively, then guild
1040
structure and function of the vegetation are also preserved. A constant question in considering these
1041
concepts will be the effect of species richness: are communities with more species more ‘stable’ (sensu
1042
lato).
1043
7.2 Reliability (constancy)
1044
Reliability is the reciprocal of variation in the ecosystem (e.g. Naeem and Li 1997; Rastetter et
1045
al. 1999). The concept was behind ideas on ‘stability’ up to about 1975. For example, Orians (1975)
1046
wrote of ‘constancy’ as a type of stability. Species richness could increase reliability through the
1047
portfolio effect or through the covariance effect. In the portfolio effect, named after a portfolio of shares
1048
that varies less than individual shares, the community response is dampened because it is an average of
1049
the different responses of different species (Ives and Hughes 2002). It will always operate unless the
1050
species are identical in their environmental responses. Since averaging over minor species has little
1051
effect, the portfolio effect increases with species evenness. The covariance effect is based on
1052
competition: when the environment disfavours one species others will increase by taking up the unused
1053
resources. This seems to be Whittaker’s (1975b) concept of population ‘buffering’: the absorption of
1054
environmental fluctuations through compensation between different species or genotypes. However, we
1055
cannot assume that these effects will be stronger when species richness is higher. Hughes and
1056
Roughgarden (2000) modelled a community with density-dependent Lotka-Volterra competition
1057
equations, and found that with diffuse competition the reliability of biomass decreased with richness,
1058
except in systems with few species and very low interaction strengths. With each species competing
1059
with only its two nearest neighbours, as in MacArthur and Levins (1967) model, the richness/reliability
1060
relation was the reverse. DeWoody et al. (2003) used community models based on variations of
1061
MacArthur’s ‘broken stick’ and found that whilst reliability increased with richness it was, surprisingly,
1062
higher with more difference in competitive ability between the species. Hughes and Roughgarden
1063
(1998) found in a 2-species community-matrix model based on Lotka-Volterra equations that with the
1064
two species equal in competitive ability biomass reliability was not affected by the strength of
1065
competition. As the competitive abilities of the two species became more unequal, reliability decreased.
1066
We shall have to descend to reality.
1067
Boreal forest is reliable in species composition in the short term of centuries. In the longer term
1068
of millenia it is functionally reliable but variable in species composition: even now the trees of Europe
1069
have not re-occupied their potential range after the last glacial retreat (Svenning and Skov 2004).
Wilson & Agnew, chapter 3, Community processes, page 36 of 49
1070
Tropical forests appear to be observationally reliable in the short term and this is impressive considering
1071
their fast growth rates (Manokaran and Swaine 1994 in Malaysia; Sheil et al. 2000 in Uganda). Real
1072
examples of long-term stasis are found amongst stressed communities where the available flora is
1073
limited. The dwarf pitch pine shrubland on Mt Everett, Massachusetts (Motzkin et al. 2000), the Carex
1074
curvula zone in the European Alps (Steinger et al. 1996) and the ombrotrophic mires of Quebec
1075
(Klinger 1996) fit this syndrome. In contrast, O’Connor et al. (2001) found that whilst less common
1076
species increased biomass reliability in African grassland in a fluctuating rainfall this effect was evident
1077
only in rangelands of poor condition.
1078
Experimentally, McGrady-Steed and Morin (2000) found in microcosms of bacteria, micro-
1079
algae, micro-herbivores and bacteriovores and micro-predators that there was a U-shaped relation
1080
between species richness and the reliability of algal density, measured as variation in 3-day steps over
1081
42 days. Tilman (1996), in 207 plots with various nutrient treatments in four fields at Cedar Creek,
1082
found that species-rich plots had greater reliability (lower CV in biomass), though the plots differed in
1083
fertiliser application presumably confounding species richness with species composition. The
1084
experiment of Tilman et al. (2006) overcomes this problem by using plots sown at a range of species
1085
richnesses and maintained thus by weeding. The same increase in reliability was seen. This is the
1086
nearest we have so far to an answer.
1087
7.3 Stability sensu stricto (Liapunov stability)
1088
Defining stability
1089
May (1972) initiated the modern approach to stability with his community matrix analysis, based
1090
on the mathematical procedure of local stability analysis (= ‘Liapunov stability analysis’ =
1091
‘neighbourhood stability analysis’). Stability sensu stricto is defined as the ability to recover completely
1092
from an infinitely small perturbation after an infinitely long time. Though we have phrased this to make
1093
it sound a little ecologically unrealistic, some approach to the concept is essential if we are to discuss
1094
stability. Defined thus, stability is like pregnancy: either one is or one isn’t. The ‘infinitely small’ is
1095
necessary to make the definition one of local stability, perhaps among alternative stable states. Global
1096
stability is a much more difficult idea conceptually and operationally. The phrase ‘after an infinitely
1097
long time’ is necessary to avoid arbitrary cutoffs, as well as to distinguish it from resilience. Stability
1098
can be predicted mathematically from the community matrix – a summary of all possible pairwise
1099
species interactions in an equilibrium community. The community matrix introduces three important
1100
aspects of community structure. The number of species involved, S, is simple. Another aspect is what
1101
proportion of the S×(S-1) off-diagonal matrix elements are non-zero (i.e. the species in that column does
1102
affect the species in that row). This is the connectance. Thirdly, the interaction strength is the mean
1103
absolute value of these non-zero elements.
Wilson & Agnew, chapter 3, Community processes, page 37 of 49
1104
Is stability likely to occur? (simulations)
1105
Since May (1972), the community matrix has been used extensively in theoretical studies to
1106
predict what type of community would be stable (Hall and Raffaelli 1993). It turns out that, given a
1107
matrix comprising random values, communities with many species and/or with many or strong
1108
interspecific interactions are less likely to be stable. In fact, it is very unlikely that a community of
1109
randomly-assembled species will be stable at all. This represents an obvious conflict with our
1110
observation that multi-species communities commonly persist in nature. One explanation is that the
1111
species in natural communities have co-evolved to be able to co-exist. However, it has been found that
1112
the introduction of some basic ecological processes, especially simulating the assembly of a community
1113
by the immigration and extinction of species, or simply with a realistic pattern of extinction, allows
1114
complex multispecies communities to develop relatively easily without any assumption of coevolution
1115
(Tregonning and Roberts 1979; Taylor 1988). In the simplest assembly models of Tokita and Yasutomi
1116
(2003) the community stabilized at about five species. When the introduced species were formed as
1117
minor mutants of a species already in the community, the number of species reached about 10. However
1118
when, in their ‘local’ model, the characters of new species arriving were based on one species already
1119
present, except for its interactions with one other (abundant) species, the size of the community
1120
approached 50 and was still rising after 10 000 periods. Moreover, such communities were resistant to
1121
invasion. They interpreted this as the temporary persistence of species only marginally inferior in
1122
competitive ability, that were able to exist stably once mutualistic partners appeared. This is stability by
1123
very simple coevolution.
1124
Tests for stability (the real world)
1125
Despite all the theoretical work on the community matrix, tests of stability in natural systems
1126
have been surprisingly sparse. The only valid method for estimating the community matrix for a given
1127
community is by the experimental manipulation of the organisms, quantifying the effect that each
1128
species has upon the growth rate of each other species. We are aware of only a few such studies
1129
(Thomas and Pomerantz 1981; Seifert and Seifert 1976; and those below).
1130
Schmitz (1997) used data from field and laboratory experiments to quantify the interaction
1131
strengths between grasshoppers, four old-field plants, and nitrogen supply. He used these values to
1132
parameterize the community matrix and thence to predict the response of each species to nitrogen and
1133
herbivore press perturbation. The predictions carried a high degree of uncertainty, but the observed
1134
results of the field press perturbations was close to, or within, that range in six out of eight cases.
1135
The most direct test of stability in a community has been on the University of Otago Botany
1136
Lawn (Roxburgh and Wilson 2000a; b). A pre-requisite for the concept of stability is that the
1137
community should be at equilibrium, and this seemed to be true. Roxburgh and Wilson (2000a) grew
1138
seven species from a lawn, including the six most abundant species, experimentally in soil from the
Wilson & Agnew, chapter 3, Community processes, page 38 of 49
1139
lawn kept in two strata and placed in deep boxes only metres from the lawn. The species were grown in
1140
monocultures and in 2-species and other mixtures. A community matrix calculated from competition
1141
coefficients predicted the mixture of species to be unstable, but very close to the stability/instability
1142
boundary. It was certainly closer to the stability/instability boundary than matrices constructed under a
1143
range of null models. To test for the actual stability of the community, Roxburgh and Wilson (2000b)
1144
applied three types of pulse perturbation. After shading for 6 weeks and after mechanical perturbation
1145
(removal of vegetation), species composition recovered towards the original equilibrium state, although
1146
full recovery was not seen. Recovery from a herbicide specific to grasses was still quite incomplete after
1147
2.5 years, apparently because the compensatory growth of dicots made it difficult for the grasses to
1148
reinvade. The pattern of recovery of the lawn from the perturbations was consistent with the prediction
1149
of marginal stability/instability given by the community matrix analysis.
1150
Simulations (Roxburgh & Wilson 2000a) showed that the stability of the community matrix,
1151
marginal though it was, could be attributed to the transitive competitive hierarchy found between the
1152
species (chapter 5). A simplistic extrapolation from competitive abilities would be that species with a
1153
greater competitive ability in 2-species experiments would be more abundant in the community. Several
1154
authors have found such a correlation (e.g. Mitchley and Grubb 1986; T.E. Miller and Werner 1987).
1155
However, the strict hierarchy in competitive ability found in the pairwise box experiments, from Holcus
1156
lanatus (Yorkshire fog) as the most competitive species, to the herb Hydrocotyle heteromeria as the
1157
least, had no clear relation to abundances in the Botany Lawn (Roxburgh and Wilson 2000b). Such a
1158
lack of correlation has been found elsewhere (Aarssen 1988). Roxburgh and Wilson (2000b) suggested
1159
that it was due to apparent mutualism in a multi-species mixture: the “My enemy’s enemy is my friend”
1160
effect. This effect will be more prominent the more species there are in the community. Apparent
1161
mutualism is implicitly included in the community matrix model, therefore the model should be able to
1162
predict abundances in the actual community (given that only seven species were included in the model).
1163
It could. For example, the model predicted that Trifolium repens (white clover), Holcus lanatus and
1164
Agrostis capillaris (bent) would be the three dominants, and these three are indeed among the four most
1165
abundant species in the lawn. From the pairwise experiments, H. lanatus headed the competitive
1166
hierarchy. However, it was only the second most abundant species in an experimental 7-species
1167
experimental mixture and in the lawn (Roxburgh and Wilson 2000a), an outcome correctly predicted by
1168
the community matrix model.
1169
7.4 Resistance to abiotic perturbation
1170
Resistance is a difficult concept. It is the response of a system to a natural or anthropogenic
1171
pulse perturbation, or to be more exact the lack of response. But what is a perturbation? Suppose a light
1172
wind blows over grassland, with no effect on community composition. Obviously the change was too
1173
small to be called a perturbation. The trouble is that if a perturbation is applied and the community does
Wilson & Agnew, chapter 3, Community processes, page 39 of 49
1174
not react, it is impossible to say whether that was because it was a very resistant community, or because
1175
the treatment applied was not a real perturbation in the first place. We cannot even compare
1176
communities. If salt is applied to most communities, it will be a perturbation and plants may die.
1177
However, with a saltmarsh community any obligate halophytes there will jump for joy; it was no
1178
perturbation at all. This is analogous to the problems that Körner (2003b) saw in defining ‘stress’. The
1179
concept of resistance can apply at the level of the whole community or of individual species, and again
1180
in terms of function, guilds or species. We could expect some theory at the community level, but there is
1181
little. In Loreau and Behera’s (1999) model, with plants limited by nutrients, the biomass resistance
1182
generally decreased with increased ecological difference between the species.
1183
For evidence, we take two examples: drought and trampling. Drought can be basically a pulse
1184
perturbation. Pfisterer and Schmid (2002), in mesocosms of grassland species, found that species-rich
1185
plots were less resistant to drought in biomass, i.e. function. The same trend can be seen for species
1186
composition in the Cantabrian (Spain) mountain meadows that Gómezal-Sal (1994) examined. Other
1187
field comparisons and those with experimental plots that differ in fertiliser application have yielded the
1188
opposite result, though such comparisons confound species diversity with composition. Vegetation is
1189
complicated, so is its relation to soil, and the behaviour of each species is predicated by its evolutionary
1190
history, so it is little wonder that it is difficult to find generalisations.
1191
There is an extensive literature on the effects of human trampling. For example, Page et al.
1192
(1985) studied the above-ground production resistance of many species in Welsh coastal dune
1193
vegetation over two years after press perturbations of quantified trampling, and compared the results to
1194
controls. They found that species could be assigned to three behavioural classes, partly depending on
1195
their morphology, i.e. their guild / functional-type. In the closed-canopy vegetation of the fixed dunes,
1196
graminoid production was the most resistant, and forb production the least. Forbs and bryophytes of
1197
unstable habitats, counter intuitively, recovered only slowly. However, they have specialised reactions
1198
to particular environmental events. In Bellis perennis (lawn daisy) trampling triggers the swollen corm-
1199
like base, filled with starch, to produce stolons; in fact the species needs open ground for these stolons
1200
to be produced (A.D.Q. Agnew, pers. obs.). The moss Tortula ruralis ssp. ruraliformis (= Tortula
1201
ruraliformis) has fast erect growth under sand burial, probably because it is peculiarly efficient in its
1202
ability to dry and re-hydrate fast with minimal respiratory cost (Willis 1964). The golden moss
1203
Homalothecium lutescens forms a weft with erect shoots which grow up after sand burial. Other authors
1204
using greenhouse and field experiments (e.g. Andersen 1995; Cole 1995) have found that resistance to
1205
human foot and wheel pressure differs between plant guilds in similar ways, the geophytes and tussocky
1206
graminoids being consistently more resistant, upright forbs less resistant. Resistance seems to be
1207
individualistic to the species.
Wilson & Agnew, chapter 3, Community processes, page 40 of 49
1208
7.5 Resistance to invasion
1209
Another type of resistance is that to invasion. The process of invasion can comprise: (1) the
1210
occupancy of an empty niche, (2) splitting an existing niche, (3) ousting an existing species from a
1211
niche, or (4) the invader’s constructing a new niche by reaction. Often, invasion is taken to mean by
1212
species exotic to the region (usually exotic to the continent). This confuses the ability of incomers to
1213
establish in a closed community with whether communities contain empty niches and with whether
1214
exotic species are somehow different from native ones. At other times, the topic means the invasion of
1215
local species that were not present at that spot before, which involves questions of community structure.
1216
The issues here are:
1217
1. Whether disturbance is required before invasion can occur.
1218
2. Whether continual disturbance is required for the invader to persist.
1219
3. The biotic diversity of the target community, and whether it is species-saturated. Behind this is
1220
whether there are empty niches, leaving resources available to the invader.
1221
4. Missing guilds (plant functional types).
1222
5. Community structure, for example whether communities with low interaction strength and/or
1223
1224
low connectance are more invasible, or possibly less so.
6. The existence of an alternative stable state which could keep an invader out, though it could
1225
form a stable state once admitted.
1226
7. Subvention available to the invader, e.g. protection from grazing offered by a thorny shrub.
1227
8. Whether exotic species differ in some way from native ones.
1228
Exotic species will be discussed in chapter 5, but all the aspects above apply to them. Empty niches (‘3’,
1229
‘4’) are especially relevant for exotics. So is ‘1’ because it is possible that the absence of an exotic
1230
species in a community is due to inertia, and lack of disturbance is only delaying the inevitable invasion.
1231
Aspect ‘2’ will be relevant if many of the exotics are ruderal species.
1232
Theory
1233
Case (1991) found that in randomly-constructed Lotka-Volterra based communities resistance to
1234
an invader was higher when species richness was higher and there were strong interspecific interactions.
1235
Shea and Chesson (2002) concluded that theory is indeed now clear that, all other factors being equal,
1236
invasion resistance increases with species diversity. Intuitively, the explanation is that with high
1237
richness there are no resources left for an invader, with appeals, at least implied, to MacArthur and
1238
Levins’ species packing. But then why, except for inertia, do the residents get the resources, not the
1239
invader? In partial refutation of Shea and Chesson (2002), the careful plant-community simulations of
1240
Moore et al. (2001) indicated that there is no simple relation between resistance and richness: it depends
1241
on the model and what caused the richness to vary.
Wilson & Agnew, chapter 3, Community processes, page 41 of 49
1242
1243
Evidence
There have been many studies correlating species diversity and invasion across sites, and also
1244
studies experimentally adding invaders to a range of natural systems. We can draw no conclusions from
1245
these because there are always environmental/historical differences between sites that confound
1246
differences in species diversity. We like the idea that real communities can tell us more, but in this case
1247
experiments are needed in artificial communities.
1248
Dukes (2002) established small field microcosms on a soil/sand mix using grass and forb species
1249
found in a particular grassland in California. When Centaurea solstitialis was added as an invading
1250
species in the form of seeds, mixtures of two or more species reduced its biomass more than the average
1251
monoculture, but no mixture of up to 16 species inhibited invasion more than the most resistant single
1252
species: the annual forb Hemizonia congesta (it is a member of the same guild as C. solstitialis: hints of
1253
niche filling). No increase in resistance was seen beyond four species, though Dukes (2001) attributed
1254
this to a guild effect, an artefact of the experimental design. This raises a complication. We are seeking
1255
a niche complementarity effect, in which with more species there will be a higher probability of
1256
including a species to fill each niche, in this case perhaps the annual forb niche, leaving few resources
1257
for an invader (leaving aside the question we raised above of why the residents should get them). As
1258
with overyield there is the possible artefact of the ‘selection effect’ (D.A. Wardle 2001): when more
1259
species are sown there is more chance that a species with high interference ability is included, and that
1260
species will take over. This mimics complementarity if the species with the highest interference ability
1261
in the resident mixture also has high interference ability against the invader, but that is quite likely, for
1262
example a species with high cover or LAI reducing light intensity below itself. A counter to this artefact
1263
is finding that a mixture is more resistant to invasion, not just compared to an average mixture with
1264
fewer species, but than any mixture with fewer species or any monoculture. The experiment of Dukes
1265
(2001; 2002) did not achieve this.
1266
Evidence for the effects of diversity on invasion comes from a 4-year old experiment at Cedar
1267
Creek. Tilman (1997) sowed seeds of up to 54 species in to patches of native grassland. The proportion
1268
of the 54 added species that became established was negatively correlated with initial species richness
1269
of plots, suggesting that species-rich sites were more resistant to invasion. A problem is that some of the
1270
species added as seeds were already present in some of the plots, when such a species established it
1271
would not count as an invader, and there would be more chance of this happening at higher richnesses.
1272
This does not seem to be the complete explanation because the richness/resistance relation remains
1273
qualitatively the same if only species not already present are counted among those sown (D. Tilman,
1274
pers. comm.). However, the variation between plots was natural, and species composition may have
1275
covaried with richness. These problems were overcome in another experiment at Cedar Creek, when
1276
Fargione and Tilman (2005a) planted and weeded 169 plots to species richnesses from 1, through 2 to
1277
16 for 6 years, then opened them to colonisation for two years. In higher-richness plots there was
Wilson & Agnew, chapter 3, Community processes, page 42 of 49
1278
significantly lower invader richness (R2 = 0.31) and biomass (R2 = 0.18). As usual, most of this effect
1279
on invader richness occurred at low resident richness, between one and two species. The effect seemed
1280
to be largely due to suppression of invaders by C4 grasses, and the authors suggest their effect is via
1281
reduction in soil nitrate. They admit this is most easily seen as a selection effect. However, the invasion
1282
resistance of some mixtures was greater than that of the most resistant monoculture (Schizachyrium
1283
scoparium, bluestem, a C4 grass), and this effect increased up to an 8-species mixture. Specifically, the
1284
percentage of plots that had lower invader biomass than did the best resident monoculture increased
1285
across the species richness gradient. This is all quite impressive evidence of the complementarity effect.
1286
Wilsey and Polley (2002) attempted to outwit the sampling effect by experimentally varying the
1287
evenness of four grassland species (three grasses and one forb), not the diversity. Reducing evenness led
1288
to a greater number of dicot invaders, but had less of an effect on monocot invaders. Opportunity for
1289
testing comes also from guild-removal experiments; we discuss these chapter 5, section 7.4, coming to
1290
the conclusion that they offer little support for guild-based assembly rules.
1291
Resources, disturbance and species
1292
It is very frequently suggested that invasion is greater after disturbance (Davis et al. 2000). This
1293
is true, but misleading. Of course, there must be sufficient resources for an invader to establish.
1294
Autogenic and allogenic disturbances are more likely in habitats with more nutrient resources, due to
1295
greater growth rates and herbivore munchiness respectively, and disturbance often releases resources.
1296
For example Burke and Grime (1996) and Thompson et al. (2001) report an experiment in a limestone
1297
grassland at Buxton, northern England, where they added seed of 54 species, all widespread native herbs
1298
that are commonly found in climates and soils like those at the experimental site but which were not
1299
originally present there. There was greater establishment of the 54 species when the soil was disturbed
1300
and fertiliser added, though the combination of disturbance and fertility levels in which invasion was
1301
maximal was unique for each invading species.
1302
Davis et al. (2000) generalised from experiments such as these to suggest that invasion requires
1303
resource enrichment or release, including that caused by disturbance. There have been many similar
1304
statements, but we must be careful. If the invaders are native then either: (a) they are better suited to the
1305
conditions than the residents, probably because the conditions have changed, in which case disturbance
1306
is simply overcoming inertia, or (b) they are not better suited, in which case they are probably ruderals
1307
taking advantage of the temporary gaps. Neither result is remarkable. If the invaders are exotics, the
1308
same argument applies; the only difference is that the possibility of their being better suited is greater,
1309
because: (a ii) there is the additional possibility that they are a worldwide super-species in those
1310
conditions, and (b ii) there is a greater probability of their being ruderals too, because many exotics are.
1311
With higher nutrients the argument is much the same. There are some careful and ingenious experiments
Wilson & Agnew, chapter 3, Community processes, page 43 of 49
1312
here, but the conclusions usually reached are misleading, and when examined more carefully the results
1313
are trivial.
1314
We should be careful of over-simplification. Species identity matters. For example, Van Ruijven
1315
et al. (2003) sowed plots with 1 to 8 species. They found an effect of species richness on invasibility, but
1316
it could be attributed to just two species, and mainly Leucanthemum vulgare (ox-eye daisy). However
1317
this was not a selection effect: L. vulgare was a low yielder in monoculture. Van Ruijven et al. suggested
1318
it may have suppressed invaders by harbouring root-feeding nematodes, and perhaps also transmitting
1319
viruses through them. Again, Crawley et al. (1999) found little overall effect of species richness in
1320
decreasing volunteer invasion, but there was consistently lower invader richness and biomass in plots
1321
containing Alopecurus pratensis (foxtail).
1322
7.6 Resilience
1323
Resilience is a simple concept: the speed of recovery after a pulse perturbation. Again, recovery
1324
can be measured in an ecosystem function such as production, in guild structure or in species
1325
composition. If structure is described by the guilds present, then the guild proportions (i.e. the
1326
physiognomy and phenology of the vegetation) must be regained, which will restore community
1327
function.
1328
B.H. Walker (1992) argues that maintaining function after a perturbation should be easier if
1329
there are several members of each guild, a situation he calls species/ecological/functional redundancy. If
1330
a perturbation affects the dominant species in a guild, a subsidiary species will then be available to
1331
assume its rôle. Richness could lead to resilience this way. B.H. Walker et al. (1999) suggested that an
1332
Australian rangeland community was rather precisely organised this way: the most abundant species
1333
differed from each other functionally, the most functionally-similar species differed in abundance, and
1334
when a species decreased under heavy grazing another species increased that was functionally similar
1335
but had previously been sparse. For example, using his functional characters, when a large perennial
1336
grass with soft, thin leaves is reduced by grazing, another species with those characters should increase.
1337
This is not easy to imagine. In so far as those characters affect palatability and grazing tolerance, all the
1338
functionally-similar species should decrease together. The relevant theory is that environmental changes
1339
(here, grazing) lead to dominance by species of different beta niches but with the same alpha niches still
1340
mostly represented. The characters that Walker et al. used – height, width, life history, SLW and leaf
1341
‘coarseness’ – do not fit easily into this model. Similarly, Cowling et al. (1994) suggested that in Cape
1342
Fynbos, South Africa, the high species diversity leads to considerable redundancy within guilds. After
1343
the massive fires and droughts which are endemic to the region some members of each guild could
1344
survive, so that the original guild structure is recovered. The concept of redundancy as espoused by
1345
Walker falls all too easily into teleology: “Why do the majority of species occur in low abundance?
1346
They … confer resilience on the community with respect to ecosystem function” (B.H. Walker et al.
Wilson & Agnew, chapter 3, Community processes, page 44 of 49
1347
1999). The real answers to their question come from the mechanisms of coexistence that we shall
1348
discuss in chapter 4, but we note that an alternative answer is that insurance could come not from
1349
redundancy but from migration (Loreau et al.’s 2003).
1350
There have been many studies of the relation between productivity (usually above-ground
1351
biomass) and resilience. Nearly all deal with grasslands, and we therefore expect that generalisations
1352
may emerge about the effects involved. Sadly this is not the case. Moore et al. (1993), in a short review,
1353
state that productivity and resilience are inextricably linked, but Stone et al. (1996), using a range of
1354
mathematical models, suggest it is far from simple, and depends on the model used. Rietkerk et al.
1355
(1997) indicated similar complication using a more mechanistic model, concluding that if plant growth
1356
is water-limited the vegetation on sandy soils is more resilient, but if plant growth is nutrient-limited the
1357
vegetation on clayey soils is more resilient. However, they find that this depends on the extent of the
1358
plant’s reaction on the soil. Sometimes, it is not easy to see a deep meaning in differences in resilience.
1359
For example, Herbert et al. (1999) examined resilience in aboveground net primary productivity in
1360
Hawai’ian tropical rainforest after a hurricane. Plots that had been fertilised with P were less resistant
1361
but more resilient. Both seem a rather simple result of lush growth and high growth rates with
1362
fertilisation.
1363
High species richness would tend to imply high redundancy. Pfisterer and Schmid (2002) sowed
1364
BioDepth plots with a range of grass species richness, perturbed them with simulated drought, and
1365
found that the low-richness plots were more resilient in aboveground net primary productivity.
1366
Mathematical theory on resilience is sparse, but Haydon (1994) used community-matrix models which,
1367
after excluding unfeasible and unstable communities, indicated that resilience should increase with
1368
connectance and interaction strength, and decrease with species richness. The latter prediction matches
1369
Pfistrer and Schmid’s finding, be it that Haydon’s prediction was for species-composition resilience. In
1370
contrast, when Engelhardt and Kadlec (2001) set up aquatic mesocosms with 1-5 aquatic species and
1371
applied the perturbation of clipping off the above-substrate shoots, there was no relation between
1372
species richness on biomass and respiration resilience. The answer is probably that species’ types differ,
1373
and we can expect no simple conclusions. For example, in the trampling experiments of Cole and Trull
1374
(1992) and Cole (1995)’s experimental trampling, resilience in cover (which was measured in the latter
1375
work!) was lower in communities containing more shrubs and chamaephytes.
1376
Correlation of resistance and resilience
1377
An inverse relationship between resistance and resilience has been repeatedly demonstrated,
1378
both across communities and across individual species. We saw this with Herbert et al. (1999) above.
1379
Taking our case study of trampling, Cole and Spildie (1998) found that when montane understorey
1380
communities were subjected to hiker, horse and llama traffic at two intensities, forb-dominated
1381
vegetation was highly vulnerable to vegetation impact but recovered rapidly, whilst shrub-dominated
Wilson & Agnew, chapter 3, Community processes, page 45 of 49
1382
vegetation was more resistant but lacked resilience. At the between-species level, again with trampling,
1383
Cole (1995) found a negative correlation in mountain vegetation; the correlation was seen especially
1384
within the chamaephyte and graminoid guilds. In contrast, Pfisterer and Schmid (2002) found that
1385
species-poor plots of their plots were both more resistant to drought and more resilient. Again, simple
1386
generalisations are premature and probably wrong.
1387
8 Conclusion
1388
Many have tried to make generalisations about plant community change. Unfortunately, none are
1389
generally applicable. Even general phrases such as “Succession as a gradient in time” (Pickett 1976) can
1390
be misleading when a switch is resulting in stasis or a mosaic, or when there is cyclic succession (Fig.
1391
3.10). There have been fashions. Before Egler (1954), and for some time afterwards since most
1392
ecologists dismissed Egler as a crank (which he was), most ecologists held to Clements’ (1916)
1393
concepts of relay floristics in a much more simplistic way than Clements himself had. The reaction (no
1394
pun intended) began in earnest with Connell and Slatyer (1977), and progressed until some ecologists
1395
declared that the very word ‘climax’ should be avoided. Many have declared that the views of Gleason
1396
were “strongly opposing” the successional concepts of Clements, but in fact his concept of the process
1397
of succession (Gleason 1917; 1927) was almost identical.
1398
The geological background is included in Fig. 3.11, with the processes of speciation,
1399
biogeographic distribution, dispersal and environmental filtering / ecesis (steps A-D). In chapter 2 we
1400
discussed the interactions between species that follow (E and F). It is clear that given an area initially
1401
without plants, certain species will predominate first. Whether they do this through dispersal, fecundity
1402
or stress tolerance will depend on the environment. The later species will come in partly because,
1403
though not having those characteristics, they have greater competitive ability. The extent to which they
1404
rely on facilitation by the pioneer species will again depend on the environment and on the species (L.R.
1405
Walker et al. 1986; 2003). A single, stable endpoint is present in one of the three possible pathways
1406
(Fig. 3.1). The ‘climax’ concept should not be thrown out with the bathwater. On the contrary, Relay
1407
floristics should be the null model, not because Clements was almost always right (though he was), but
1408
because it happens often, and it is more profitable to concentrate on the exceptions. The situations that
1409
Clements termed sub-climaxes are one exception to relay floristics, but his use of them was much more
1410
restrained than that of those peddling a simplified version of his theory. He saw fire and grazing
1411
subclimaxes as man-induced, but these days we are more likely to see fire suppression as man-induced.
1412
The only environmental factor that Clements (1916) saw as retarding succession to give a subclimax
1413
was saline/alkaline soils. The replacement of communities (sensu lato) in a cycle is an obvious
1414
exception from the null model, but evidence for it is so hard to find that can be fairly sure it is less
1415
common than Watt supposed.
Wilson & Agnew, chapter 3, Community processes, page 46 of 49
1416
Reaction is clearly important, and reaction in the facilitative direction is part of the relay
1417
floristics. However, there is every reason to expect it to be commonly in the opposite direction, giving a
1418
switch, and this appears to be the case. Although we have emphasised that most putative switches are
1419
unproven, this is quite as true for relay floristics. Moreover, switches are probably often part of relay-
1420
floristics succession, either speeding it up in which case they will hardly be noticed, or slowing it. It is
1421
when switches sharpen a gradient or magnify small initial differences to give a mosaic of alternative
1422
stable states in space or time that they produce patterns that are hard to miss. Clements did eschew the
1423
idea of alternative pathways of succession (Clements 1916, 167), but he allowed two types of reaction
1424
that retarded succession: what we have described as the Sphagnum bog pH switch and the Ericaceae
1425
(e.g. Calluna vulgaris) switch which Clements ascribed to “acids and other harmful substances”
1426
(Clements 1916, 107).
1427
Throughout relay floristics, cyclic succession, the operation of a switch or for that matter
1428
inducing a state change there may be an allogenic environmental change (this chapter, sect. 2) or
1429
allogenic pulse perturbation (i.e. disturbance), changing the rules of the game. Response to and recovery
1430
from pulse perturbation were the subjects of sections 7.4 and 7.6 of this chapter, but for both we
1431
concluded that it is hard to see generalisations, and probably always will be because of individual
1432
responses by species. Resistance to invasion involves questions of alternative stable states (sect. 5.6 of
1433
this chapter), which are still better known in theory than in reality, and also questions of the nature of
1434
exotic species, which we shall deal with in chapter 5, section 12.
1435
Wilson & Agnew, chapter 3, Community processes, page 47 of 49
1436
1437
Bare,
stressful
environment
Bare, benign
environment
(probably
secondary
succession)
(probably
primary
succession)
Dispersal,
ecesis,
Dispersal,
ecesis,
facilitationtype
reaction
perhaps
facilitation-type
reaction
Switchtype
reaction
Delaying or
accelerating
switch
Switchtype
reaction
Mosaic/
sharpening
switch
Alternative
stable state
Climax
Perturbation
Regime
change
Cyclic
autogenic
facilitation
Cyclic
phase
Cataclasm
Fig. 3.10: Pathways of vegetation change
Cyclic
phase
Wilson & Agnew, chapter 3, Community processes, page 48 of 49
1438
1439
1440
1441
1442
1443
1444
1445
A Speciation
B Biogeography: the species pool
C Dispersal
D Environmental filtering / ecesis
E Interference filtering
Geological
processes
1446
Resources
Biota
1447
1448
Resource use by biota
1449
1450
Growth, production
assembly rules
1451
1452
1453
1454
Vegetation change
Autogenic factors
Interference, including:
switch
autogenic disturbance
subvention
effects via heterotrophs
litter effects
1455
Climax
Cyclic
phase
Cyclic
phase
ASS
1456
Allogenic factors
short
timescale
Annual climate fluctuations
(local)
Millenial climatic shifts
(regional)
Geomorphological changes
(local & regional)
Geological changes
(transcendent)
1457
long
timescale
1458
1459
Fig. 3.11: The background of vegetation change.
1460
ILLUSTRATIONS
1461
Fig. 3.1: Vegetation change through time by (a) Clements’ facilitation succession, (b) Watt’s cyclic
1462
1463
1464
1465
1466
succession, (c) a switch.
Fig. 3.2: Changes in the percentage of the ‘Galium’ cover type in Watt’s acid Breckland grassland. Data
from Usher (1987).
Fig. 3.3: The Larrea tridentata (creosote bush) / Opuntia leptocaulis cyclic succession proposed by
Yeaton (1978).
1467
Fig. 3.4: Four possible outcomes of vegetation switches.
1468
Fig. 3.5: A vegetation pattern caused by a fog-interception switch.
1469
Fig. 3.6: Change in precipitation caused by a fog-interception switch.
1470
Fig. 3.7. A sediment-mediated switch. EPS = extracellular polymeric substances.
1471
Fig. 3.8. Maintenance of alternative stable states in space by a Zero-sum switch, comprising spatial
1472
resource accumulation and depletion.
Wilson & Agnew, chapter 3, Community processes, page 49 of 49
1473
Fig. 3.9. In ‘a’ arithmetic overyielding the absolute gain by A in mixture is greater than the loss by B so
1474
RTM > 1.0; in ‘b’ the relative gain by B is greater than the loss by A so RYT > 1.0, in ‘c’ some
1475
mixtures yield more than either monoculture. For definitions of RYM and RYT see J.B. Wilson
1476
(1988c).
1477
1478
= theoretical biomass of each species with no interaction,
= actual biomass of each species,
1479
Fig. 3.10: Pathways of vegetation change.
1480
Fig. 3.11: The background of vegetation change.
= total biomass of the mixture.