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1 The nature of the plant community: a reductionist view 2 3 J. Bastow Wilson Botany Department, University of Otago, P.O. Box 56, Dunedin, New Zealand. 4 5 Andrew D.Q. Agnew Institute of Biological Sciences, University of Wales Aberystwyth, SY23 3DA, U.K. 6 Chapter 3: Community-level processes 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 1 2 3 38 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 39 40 41 42 43 44 45 4 5 6 7 8 Introduction 2 Allogenic change: including secular change ....................................................................................... 4 Relay floristics 7 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 ........................................................................................ 14 5.1 The concept of the switch ......................................................................................................... 14 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 ............................................................................................ 17 5.4.C Mechanisms involving other aspects of microclimate ...................................................... 18 5.4.D Mechanisms involving physical substrate......................................................................... 19 5.4.E Mechanisms involving substrate chemistry ...................................................................... 20 5.4.F Mechanisms involving disturbance ................................................................................... 23 5.4.G Mechanisms involving heterotrophs ................................................................................. 23 5.5 Switch evolution ....................................................................................................................... 25 5.6 Alternative stable states ............................................................................................................ 26 5.7 Negative feedback ..................................................................................................................... 32 Diversity → productivity 32 Stability 35 7.1 Concept ..................................................................................................................................... 35 7.2 Reliability (constancy) .............................................................................................................. 36 7.3 Stability sensu stricto (Liapunov stability) ............................................................................... 37 7.4 Resistance to abiotic perturbation ............................................................................................. 40 7.5 Resistance to invasion ............................................................................................................... 41 7.6 Resilience .................................................................................................................................. 44 Conclusion 46 Wilson & Agnew, chapter 3, Community processes, page 2 of 50 47 ‘switches’. This was not a familiar concept for me, and I enjoyed reading about it. 48 1 Introduction 46 49 In the previous chapter we discussed positive and negative interactions between plants. These 50 are the currency of community processes, and we now examine the implications of their effects at the 51 whole-community level. All plants and animals must alter their immediate surroundings by reaction, 52 which Clements (1916) defined as: “The effect which a plant or a community exerts on its 53 habitat”(chapter 2 above). Whilst admitting that classification of types of reaction was difficult, 54 Clements listed about 20. Plants especially cause reaction, because of their bulk and their necessity to 55 produce litter, leading to modifications of local light availability, climatic regimes, environmental 56 chemistry and geomorphological processes. This affects the populations of herbivores and thus the 57 system as a whole. 58 Community processes can have only two outcomes: stability or change. Change should be the 59 expectation, firstly because the environment is never without temporal variation and secondly because 60 the plants alter, by reaction, their own environment. However, stabilising forces do exist, and aspects of 61 stability can certainly be seen, even if strict stability has never been proved. A contrast can be made 62 (Box 3.1) between a species/community changing the environment to its disbenefit (facilitation, the 63 concept though not the term of Clements 1916) or benefit (switch: Odum 1971; J.B. Wilson and Agnew 64 1992). We therefore link most vegetation change to facilitation and switches in this chapter. In either 65 case, eventually there can be negative feedback, a stabilising process. We also consider the cyclic 66 succession of Watt (1947). 67 Box 3.1: Types of community interaction. 68 species/guild X gives a relative disadvantage to itself: 69 the effect is density-independent: facilitation and/or autointerference = relay floristics 70 the effect disappears at low density of X (negative feedback) = stability 71 72 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 73 caused by underlying environmental variation and caused the unique reaction of each species and its 74 spatial pattern. Peter Greig-Smith (1957) used sampling and analysis to show that the ramets of all 75 species had a non-random pattern. One cause for this is the demographic (dispersal) behaviour and 76 morphology of each species. For example, Kershaw (1964) examined North Wales pastures where 77 Agrostis capillaris (= A. tenuis, bent) showed no clumping to the naked eye, but the tillers proved on 78 sampling to be clumped because disparate rhizomes upturned when nearing each other, forming patches Wilson & Agnew, chapter 3, Community processes, page 3 of 50 79 of denser culms. Patterns resulting from vegetative demography are clearly seen at the level of 80 individual clones in Harberd (1962) (chap. 1, sect. 1.1) and in his similar results for Festuca rubra, 81 Trifolium repens (white clover) and Holcus mollis (creeping velvetgrass). Using Mark Hill’s (1973) 82 algebraic clarification, Agnew & Gitay (1990) found that species and soil nutrients were similarly 83 patterned in visually uniform dune slacks, and that this pattern became more pronounced as species 84 number increased. 85 Resources can be patchy in apparently uniform natural communities (eg Robertson et al 1988). Is the pl 86 comm a force for coarsening the grain of resources in patches or evening them? The differing 87 requirements and acquisition efficiencies in acquiring nutrients as well as differing economies during 88 their life histories (i.e. phenologies of production and litter deposition = reaction) should coarsen the 89 grain of resources, so long as the indiv spp show a definite pattern. We found the most spp pattern 90 (clumps or holes in the distrib) at 20cm diam. But Ca & P did not show this pattern of clumping. 91 However, at 20 cm sample size soil Ca & P variance increased with spp richness. At the same time the 92 phytomass P became less variable at 20cm sample size. So while richness increased P patchiness, it 93 also increased evenness in the plant content. That means that each sp has just enough, from a patchy 94 soil that it has created. Can we make anything of this? 95 96 Patterning is a general quality of all plant communities and has implications for community function. The basic patterns of change are (Fig. 3.1): 97 Allogenic change 98 Directional autogenic change (succession sensu stricto) 99 Watt’s cyclic succession 100 Switches Community X1 Community Y1 Community X2 Community X Community Y2 Time Community Z Clements’ relay floristics Community Y Watt’s cyclic succession Fig. 3.1: Three types of autogenic vegetation change through time. 101 Time Community Y1 Time Community Z Community X Community Z1 Community Y2 Community Z2 A switch, giving alternative stable states Wilson & Agnew, chapter 3, Community processes, page 4 of 50 102 2 Allogenic change: including secular change 103 Vegetation changes on long timescales can be seen via the pollen record of lakes and mires, 104 especially over the past 15,000 yr. In the northern Atlantic and Pacific areas, the most abrupt, non- 105 anthropogenic alteration was a reversion from birch scrub (Betula spp) to tundra herbs in the Younger 106 Dryas period (13,000 – 11,600 yr BP). When historical vegetation change is sudden, it may be that the 107 vegetation is tracking a sudden climate change, or the vegetation change may be abrupt because there is 108 a geographic-scale switch (sect. 5.4.A below). In the case of the Younger Dryas, there does seem to 109 have been a closely-correlated sudden temperature depression (Hu et al. 2002). Such changes are most 110 likely to be seen at the geographical boundary of a vegetation type, for example the pollen profile of 111 Kremenetsky et al. (1999) indicated that the steppe-forest boundary in the Ukraine has moved at least 112 twice since 6000 yr BP. 113 Soils can change on a similar timescale. Soil leaching needs thousands of undisturbed years to 114 take place. It results in plant communities which are slow growing, often evergreen and high in 115 phenolics, on soils that are low in all nutrients, particularly phosphate. Northup et al. (1998) describe a 116 chronosequence of such soils in northern California formed over an estimated 500,000 yr. Recent soil 117 there has pH (in CaCl2) over 6, while in the oldest soil it is less than 4. This environmental change has 118 been tracked not only ecologically but perhaps evolutionarily, since there are endemic species and 119 varieties of conifer particularly adapted to the soil conditions and contributing to them. 120 Fluctuations in the species composition of plant communities from year to year were described 121 by Clements (1934 pp. 41–42) as ‘annuation’, by Penfould (1964) as the ‘pulse phenomenon’ and by 122 Collins et al. (1987) as ‘pulse-phase’. Investigations on this timescale, and the decade-long changes that 123 often accompany it, have been hindered by the paucity of datasets with continuous and long records of 124 approximately equilibrium vegetation. Notable exceptions are the Park Grass experiment in lowland 125 England (since 1856; Silvertown et al. 2006) and plots on Barro Colorado Island (since 1985; Chave 126 2003). 127 When the environment changes, it would not be surprising for the plant community to do 128 likewise, but often the correlations are hard to see. R.B. Allen et al. (1995) found correlation with the 129 rainfall at one of the dry grassland sites examined, but not at four other, nearby sites. Collins et al. 130 (1987) similarly failed to find correlations between individual species and the climate. 131 Dunnett et al. (1998) correlated vegetation changes over 38 years in the roadside vegetation at 132 Bibury, southern England, with climatic fluctuations. Warm dry summers increased species favoured by 133 environmental stress or disturbance (S or R of C-S-R theory), whereas wet growing seasons favoured 134 more productive species (C). Dunnett and Grime (1999) found by experiment that the differential 135 response of species to temperature was based on their physiological response, but the differences 136 between the species were amplified in competition. If we compare these responses with the species’ Wilson & Agnew, chapter 3, Community processes, page 5 of 50 137 distributions in Britain (Preston et al. 2002), we see that species that were notably more abundant in 138 unusually warm summers included Achillea millefolium (yarrow) (Grime et al. 1994) which is 139 distributed almost throughout the British Isles, being absent only in a very few cold/wet parts. However, 140 Ranunculus repens (buttercup) and Trifolium repens (white clover), with almost identical geographical 141 distributions to A. millefolium, were less abundant in those years. Similarly, Brachypodium pinnatum 142 (tor grass) was more abundant in warm summers, and is a species very frequent in chalk/limestone areas 143 with warm summers (July mean > 15 ˚C), but another grass with a very similar distribution, Bromopsis 144 erecta, was less abundant. This is puzzling. 145 One of the most fascinating sets of observations in ecology is Watt’s (1981) 38-year record from 146 Breckland in eastern England. Calcareous ‘Grassland A’ exhibited a sequential dominance, from 1936 147 to 1950 by the small-tussock grass Festuca ovina (sheep’s fescue), from 1950 to 1958 by the creeping 148 herb Hieracium pilosella (hawkweed), from 1959 to 1964 co-dominance of the latter two with the 149 procumbent shrub Thymus polytrichus (= T. drucei, thyme), and from 1965 to the end of recordings in 150 1973 by T. polytrichus on its own. These three species all showed a steady increase to a peak and a 151 steady reduction from it, though when H. pilosella decreased it held on to some microsites rather 152 tenaciously. Watt explains these dramatic changes by very subtle changes in the weather, but as at 153 Bibury the correlations are not convincing, and we have to conclude that these fascinating changes have 154 never been explained. Like Dunnett and Grime (1999), Watt saw competition as important, which it is 155 probably is, but disease may have played a rôle too. 156 Usher (1987) re-analysed Watt's (1960) 22 years of observation in acid grassland.(using 157 Markovian models?) The transition probabilities indicated that change in cover state could occur in 158 either direction between almost any pair of states. However, the predictions of the two Markovian 159 models are difficult to believe, e.g. that the ‘Festuca’ cover type, which had been increasing rather 160 steadily over the period up to 37 % at the end of the 22 years, would somehow decrease to 20 or 28 % in 161 a steady state. Markovian models have a tendency to make conservative predictions for future change, 162 probably because recording errors (but of course not in Watt’s case!) and minor fluctuations give 163 reverse transitions (Mark and Wilson 2005). The other problem is that such models assume constant 164 transition probabilities which almost inevitably lead to a steady state, which is quite at variance with the 165 general observation of annuation / breakouts, i.e. sudden increases in abundance followed by a sudden 166 decrease within a few years, seen dramatically in this grassland (Fig. 3.2). Neither Watt nor Usher had 167 any ecological explanation for these changes. Wilson & Agnew, chapter 3, Community processes, page 6 of 50 Percent cover of Galium type 90 80 70 60 50 40 30 20 10 0 1935 1940 1945 1950 1955 Year 168 Fig. 3.2: Changes in the percentage of the ‘Galium’ cover type in Watt’s acid Breckland grassland. Data from Usher (1987). 169 Shorter-term changes can be seen too. Peco (1989) was able to show that low rainfall produced a 170 single-year retreat in an ordination axis that was correlated with successional time. This represents a 171 whole-community shift in a single year. Some species have been observed to show outbreaks. In the Park 172 Grass Experiment, Dodd et al. (1995) found that of 43 species recorded on non-acidified plots, 10 173 showed outbreaks. These species tended to be ruderals: self-fertilised and suppressed by competition. 174 Outbreaks are seen at Bibury too (Dunnett and Willis 2004) in species such as Urtica dioica (stinging 175 nettle) and Chamerion angustifolium (rosebay willowherb), and on shorter timescales in species such as 176 Galium aparine (goosegrass) and Rumex obtusifolius (dock); Dunnett and Willis say many in the later 177 group have ruderal traits, confirming the conclusion of Dodd et al. The decade-long changes in Watt’s 178 (1981) Breckland site could be compared to such outbreaks, but happening on a longer timescale 179 because of the inertia of the shrubs (Thymus polytrichus), tussocks (Festuca ovina) and clones 180 (Hieracium pilosella). 181 At a fine scale, the elusive Carousel Theory (van der Maarel and Sykes 1997) appears to say that 182 even if a community remains in equilibrium on a large scale, species presence on a small scale changes 183 from year to year, such that within a community most species are capable of occupying most microsites, 184 but in any year each species will leave some potential sites unoccupied, at random. This begs the 185 question of why a species sometimes chooses to be absent. The logical implication is that there is niche 186 limitation to the number of species that can co-exist locally, and there is evidence for this (J.B. Wilson 187 et al. 1995a). Baba (2005), also working in calcareous grassland, emphasised differences in mobility 188 between species: a ‘complex carousel’ rather than a single carousel. Van der Maael and Sykes’ 189 observations of turnover were made on a fine scale, e.g. 3 × 3 cm, which is less than the size of most of 190 the plants, and certainly less than their sphere of influence. The apparent turnover may represent that 191 one year a leaf of a plant overhangs the quadrat, and next year the same plant is present in the same Wilson & Agnew, chapter 3, Community processes, page 7 of 50 192 place, but its leaves are in a different direction. The first priority in understanding communities at this 193 scale is to solve the Paradox of the Plankton (chapter 4), and then to find how these mechanisms of 194 coexistence and those of exclusion by interference interact to produce very fine coexistence. Self- 195 allelopathy for Hypochaeris radicata (cat’s ear; Newman and Rovira 1975) is one example, still not 196 fully established for the field, of the thousands of interactions that must be causal. The Carousel Theory 197 is purely descriptive, and thus a distraction from progress towards understanding the processes. 198 Allogenic, non-directional changes in plant communities are difficult to deal with. It is clear that 199 they are surprisingly common in vegetation that we tend to assume is constant. So far all attempts to 200 explain them have been inadequate. This is probably because the changes are driven by many 201 environmental factors, but also partly through interference and subvention between species, and 202 interactions with other trophic levels: pathogens, insect herbivores, pollinators and many others. There 203 will also be inertia and switches operating. Attempts to understand the cause of allogenic change at any 204 particular site have basically failed. They will continue to fail until there is a complete model of all the 205 species – plant, animal and microbe – with their response to the environment and interactions with each 206 other and their reactions on the environment. This is a tall order for finding why species composition 207 varies on Bibury roadsides, but it is part of the movement away from considering communities as static 208 entities to accepting that change is normal. 209 3 Relay floristics 210 3.1 Concepts 211 A linear gradient from pioneer stage to climax was the norm for Clements (1916). This was 212 characterised by Egler (1954) as “relay floristics” and by others as “facilitation succession” and 213 “succession to climax”. As always, Clements saw much, and synthesised his observations into a general 214 pattern. Like all generalisations, there are exceptions. Clements saw these as well as anyone, and 215 reported them. However, the general pattern that he emphasised is a true one. Communities change 216 through time for three reasons: (1) the environment changes allogenically making invasion possible 217 from the species pool, (2) new species arrive in the regional pool, (3) the reaction of species on the 218 environment (especially the soil) facilitates the establishment of others. It is only the last that can be 219 called succession, either directional or cyclic. 220 If the initiation of succession is geomorphological, i.e. the natural creation of a new land 221 surface, the succession is said to be primary succession; if environmental modifications remain from 222 previous succession it is said to be secondary. A classic description of a primary succession is that of 223 Crocker and Major (1955) on deglaciated terrain in Glacier Bay, Alaska. We observe that this is a 224 space-for-time substitution, and as always with such comparisons the physical location and therefore the 225 physical environment are not identical between stages, neither were the weather and the propagule flux Wilson & Agnew, chapter 3, Community processes, page 8 of 50 226 at each stage of succession. A classic secondary succession is that in Buell-Small oldfields in New 227 Jersey, USA (Bartha et al. 2003), where a genuine temporal record was possible. Earlier workers 228 (Clements 1916) envisaged a single end point of a "climax community" in successions, but it has 229 become clear that there are many potential pathways through vegetation types. Thus in Glacier Bay the 230 initial vegetation was of Dryas drummondii then Alnus sinuata and A. rubra (alders), but the course of 231 soil development in glacial til resulted in flats and hollows where drainage became impeded and mire 232 vegetation developed (‘muskeg’ with Pinus contorta, lodgepole pine) while slopes became Picea 233 sitchensis (sitka spruce) forest. Landform is not the only determinant of successional sequences: E.B. 234 Allen (1988) suggested that the causes of differing trajectories of secondary succession in Wyoming 235 sagebrush rangeland included anthropogenic topsoil alteration, mycorrhizae and alien invaders. There 236 may also be alternative stable states (sect. 5.6 below). 237 Pioneers are said to be mainly short-lived ruderals with high seed output. They have low 238 competitive ability, and are replaced by long-lived species producing fewer but larger seeds and often 239 with vegetative reproduction. These are often termed ‘r’ and ‘K’ selected respectively, by analogy with 240 the Lotka Volterra logistic equations (Krebs 1978). An alternative classification of species is C-S-R 241 theory. It is tempting to equate ‘r’ pioneers with the ‘R’ of C-S-R theory but whilst under Grime’s 242 theory secondary succession starts in the R corner, primary succession starts in the S corner and, after a 243 trip towards the C-S-R centre, ends up also back in the S corner (Grime 2001; Fig. 3.x). Grubb (1987) 244 agrees, pointing out that in primary successions with limited water and nutrients the pioneers are often S 245 species. C Secondary succession Primary succession R S Fig. 3.x. The pathways of succession under Grime’s C-S-R theory. 246 247 248 3.2 Environmental change The reaction that every plant has on its environment operates both above- and below-ground 249 (chapt 2., sect. 2). An above-ground example is the mutual shelter offered by alpine shrubs (Choler et al. 250 2001). However, the principal reactions in mesic successions are below-ground. Wilson & Agnew, chapter 3, Community processes, page 9 of 50 251 Nutrient pools and soil structure change as roots exploit and die in the soil, while the soil fauna 252 uses these resources and incidentally forces nutrient cycling. There is a trend towards soil stratification 253 imposed by surface litter deposition and water movement. Soil systems, like aerial systems in their 254 different ways, consist of a continuum of biota, all of which are leaky, so all components can affect all 255 others through diffusion and by mass flow of solute. However, organisms are typically more closely 256 intermixed below-ground than above-ground. For example, fungi play a vital rôle in vascular plant 257 nutrition and performance, and have the potential to provide intimate connections between roots. Koske 258 and Gemma (1997) found that invasion of the sand dune binding grass Ammophila breviligulata 259 (beachgrass) into bare sand was slow without vascular-arbuscular mycorrhizae (VAM). 260 However, the process of reaction causing facilitation has rarely been documented. For example, 261 L.R. Walker et al. (1986) ,interpreting the zonation away from an Alaskan river as a chronosequence, 262 concluded that there was no evidence of facilitation. , Nitrogen fixers are clear examples of species that 263 might facilitate. L.R. Walker et al. (2003) gave experimental evidence that the net effect of the N-fixing 264 shrub Coriaria arborea (tutu) on the succeeding dominant tree Griselinia littoralis (broadleaf) was 265 positive during succession after a volcanic eruption in North Island, New Zealand,because considerable 266 soil enrichment outweighed the effect of shade. 267 For all the discussion of succession, remarkably little is known about the processes involved. 268 Before Egler (1977) pointed out the fraud of space-for-time substitution there were few attempts to 269 obtain real evidence on succession. Realisation of this problem has led to a search for long-term records 270 that can be used to answer the questions, and to the setting-up of permanent plots. This is highly 271 commendable, though it will need to be combined with field and greenhouse experiments to give a full 272 picture. 273 3.3 Trends 274 The new species entering later in succession are usually more diverse, larger and longer-lived 275 than their predecessors and therefore biodiversity and biomass increase with time (Clements 1916). In 276 chapter 1, section 1, we listed the necessary parts of ecosystems: an energy input apparatus, the capital 277 of energy, the cycling of elements and rate regulation (Reichle et al. 1975). In succession, the increase 278 in biomass, usually through storage of carbon in wood, provides the capital of energy; succession is a 279 process of filling available niches with biomass, and of the creation of new niches (chap. 4, sect. 1.3). 280 The biodiversity of heterotrophs facilitates nutrient cycling (the resource economy). Nutrient capital in 281 the system is part of the rate regulation, other rates being set by the physiology (autecology) of the 282 species. 283 284 Monotonic increases in these values are not inevitable. Allogenic disturbances can trigger decreases in all of them. There can also be an autogenic decrease in biomass due to a switch process Wilson & Agnew, chapter 3, Community processes, page 10 of 50 285 such as paludification (sect . 5.4.E, below). Rather similarly, the litter produced by some species, 286 especially gymnosperms, is low in bases and acidifies the soil, resulting in the leaching of nutrients. 287 This is podsolisation. Such litter is often slow to break down, and therefore retains nutrients. These 288 processes could theoretically lead to reduced biomass. D.A. Wardle et al. (2004) compare sequences 289 from six ‘chronosequences’, in different parts of the world and on different substrates, all showing a 290 decrease in biomass. The timescale on which this process would occur makes it difficult to support with 291 evidence, but they say that “For all the sequences, the decline in basal area became noticeable within 292 thousands to tens of thousands of years after the start”. The sequences vary in the trends of litter N and 293 P, litter decomposition, etc., but most conform to podsolisation. However, succession towards forest 294 should have a special dynamic since the system is storing nutrients (and carbon as biomass), potentially 295 depleting soil resources. Thus Simard and Sachs (2004) found that in young stands taller individuals 296 were most affected by neighbours, while in older stands shorter individuals were more sensitive. This 297 suggests that the resource under competitive demand changed from light to nutrients, the opposite of 298 Tilman’s(1982) interpretation for Cedar Creek. 299 Another biomass-decreasing process which could occur late in a succession is salinisation, caused by 300 deep-rooted plants drawing on a sub-saline groundwater. Climate change and soil salinisation were 301 probably the cause of loss of casuarinid forest and an accompanying increase in salt-tolerant chenopods 302 in south-western New South Wales, Australia after 4500 yrs BP (Cupper et al. 2000). The salinization 303 could have been caused by the transpiration of the forest, in which case the process seems to be 304 autogenic. However, biomass loss caused by autogenic succession seems to be rare. 305 4 Cyclic succession: in fact or fiction 306 A quite different concept is Watt’s (1947) idea of autogenic cycles of change through 307 communities with different species composition and often different biomass and biodiversity. He 308 concluded that such cycles were widespread and the usual cause of vegetation mosaics. The idea fired 309 field ecologists worldwide to look for examples. The mechanism is the opposite to that in a switch: a 310 patch of a major species (usually only one) becomes unable to sustain its own presence or abundance 311 and dies ("moving" laterally), its place being taken often by members of a different guild, e.g. shrubs 312 replaced by bare ground with lichens. The latter eventually form an environment suitable for 313 recolonisation by the former, and so the cycle continues. The effect could be via any kind of reaction 314 such as pH or litter. Similar effects could be caused by plant pathogen increase at high densities; this 315 would not be cyclic succession because no reaction on the environment is involved but it can be difficult 316 to distinguish between these effects in field studies. 317 318 Autoallelopathy is a possible cause. It has been shown many times that leachates from a species’ shoot or occasionally roots can inhibit that same species’ seed germination or growth (Singh et al. Wilson & Agnew, chapter 3, Community processes, page 11 of 50 319 1999). Newman and Rovira (1975) tested a set of British meadow herbs and found that Hypochaeris 320 radicata (cat’s ear) and Plantago lanceolata (ribwort plantain) were significantly inhibited by their own 321 leachate, while Lolium perenne (ryegrass) was not. They argued that this could explain why the former 322 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, 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. 352 353 In arid lands environmental extremes lead easily to subvention and hence perhaps to facilitation, driving a cycle. Sadek and Eldarier (1995) describe how the succulent Arthrocnemum macrostachyum in Wilson & Agnew, chapter 3, Community processes, page 12 of 50 354 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 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. 370 371 None of Watt's (1947) examples were based on solid evidence, and most have been proved wrong on inspection over long time scales. The hummock-hollow alternation in bogs cycle had been Wilson & Agnew, chapter 3, Community processes, page 13 of 50 372 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 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. Wilson & Agnew, chapter 3, Community processes, page 14 of 50 406 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 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- Wilson & Agnew, chapter 3, Community processes, page 15 of 50 440 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. 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. Wilson & Agnew, chapter 3, Community processes, page 16 of 50 466 467 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 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 Wilson & Agnew, chapter 3, Community processes, page 17 of 50 485 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. 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 Higher water status allows taller vegetation 501 502 503 Fig. 3.5: A vegetation pattern caused by a fog-interception switch. Wilson & Agnew, chapter 3, Community processes, page 18 of 50 504 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. 511 Positive feedback between vegetation and water infiltration in arid conditions can give ‘tiger 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 Wilson & Agnew, chapter 3, Community processes, page 19 of 50 528 (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. 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). Wilson & Agnew, chapter 3, Community processes, page 20 of 50 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 21 of 50 569 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 Wilson & Agnew, chapter 3, Community processes, page 22 of 50 604 suppress the algae (van Donk and van de Bund 2002). In the turbid state, fish movement causes 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 Wilson & Agnew, chapter 3, Community processes, page 23 of 50 639 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. 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 Wilson & Agnew, chapter 3, Community processes, page 24 of 50 672 unravelled, some of which may constitute switch mechanisms, maintaining boundaries or changing 673 community structure. 674 Animal invasion can markedly alter plant communities, but this cannot comprise a switch unless 675 the community type both attracts and benefits from the animal exploitation. Much of the material is 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 Wilson & Agnew, chapter 3, Community processes, page 25 of 50 707 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 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. 739 740 Odling-Smee et al. (2003) also conclude that ‘niche construction’ [i.e. reaction] “is a fact of life”. They do not seem so concerned with a population’s affecting its own fitness, but with the causal Wilson & Agnew, chapter 3, Community processes, page 26 of 50 741 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 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 Wilson & Agnew, chapter 3, Community processes, page 27 of 50 775 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. 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 28 of 50 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’. Wilson & Agnew, chapter 3, Community processes, page 29 of 50 826 Platt and Connell (2003) argued that secondary successions might be more liable to the initiation of 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 30 of 50 861 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 31 of 50 896 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 32 of 50 931 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 33 of 50 (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 Wilson & Agnew, chapter 3, Community processes, page 34 of 50 965 species could outyield the highest-yielding monocultures, especially several years after establishment. 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. Wilson & Agnew, chapter 3, Community processes, page 35 of 50 995 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: 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: Wilson & Agnew, chapter 3, Community processes, page 36 of 50 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. 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 Wilson & Agnew, chapter 3, Community processes, page 37 of 50 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). 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 Wilson & Agnew, chapter 3, Community processes, page 38 of 50 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. 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). Wilson & Agnew, chapter 3, Community processes, page 39 of 50 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 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 Wilson & Agnew, chapter 3, Community processes, page 40 of 50 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 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- Wilson & Agnew, chapter 3, Community processes, page 41 of 50 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. 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 Wilson & Agnew, chapter 3, Community processes, page 42 of 50 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. 1242 Evidence 1243 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 1267 Evidence for the effects of diversity on invasion comes from a 4-year old experiment at Cedar Creek. Tilman (1997) sowed seeds of up to 54 species in to patches of native grassland. The proportion Wilson & Agnew, chapter 3, Community processes, page 43 of 50 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 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. Wilson & Agnew, chapter 3, Community processes, page 44 of 50 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 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 Wilson & Agnew, chapter 3, Community processes, page 45 of 50 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. 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 Wilson & Agnew, chapter 3, Community processes, page 46 of 50 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 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. Wilson & Agnew, chapter 3, Community processes, page 47 of 50 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. 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 48 of 50 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 49 of 50 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. Wilson & Agnew, chapter 3, Community processes, page 50 of 50 1471 1472 1473 Fig. 3.8. Maintenance of alternative stable states in space by a Zero-sum switch, comprising spatial resource accumulation and depletion. 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, = total biomass of the mixture. 1479 Fig. 3.10: Pathways of vegetation change. 1480 Fig. 3.11: The background of vegetation change. 1481 General Comments: Section 2 on Allogenic change seems to lack cohesion, it presents very scattered 1482 sum of previous experiments but which you doubt the validity of, but there is no synthesis of 1483 critique,.. 1484