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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. Chapter 4. Mechanisms of coexistence 6 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 1 2 3 4 5 6 7 8 9 10 11 12 13 Alpha-niche Differentiation .................................................................................................................. 5 1.1 Resources (type of resource and time of availability) ........................................................... 5 1.2 Heterotroph-imposed niches ................................................................................................. 6 1.3 The niche extended by reaction ............................................................................................. 7 Environmental Fluctuation (seasonal, annual and decadal change) ..................................................... 8 Pest Pressure (heterotroph challenges) ............................................................................................... 11 3.1 Pathogens ............................................................................................................................ 12 3.2 Herbivory, general ............................................................................................................... 13 3.3 Herbivory of disseminules and seedlings ............................................................................ 14 3.4 Vegetative herbivory ........................................................................................................... 15 3.5 Pest Pressure conclusions .................................................................................................... 15 Circular Interference Networks .......................................................................................................... 16 Allogenic Disturbance (disrupting growth, mainly mechanically) ..................................................... 21 Interference/dispersal Tradeoff ........................................................................................................... 22 Initial Patch Composition ................................................................................................................... 23 Cyclic Succession: movement of community phases ......................................................................... 23 Equal Chance: neutrality..................................................................................................................... 24 Inertia .................................................................................................................................................. 25 10.1 Temporal Inertia .................................................................................................................. 25 10.2 Spatial Inertia: aggregation ................................................................................................. 26 Coevolution of Similar Interference Ability ....................................................................................... 27 Spatial Mass Effect (vicinism) ............................................................................................................ 28 Conclusion .......................................................................................................................................... 28 Were there no plant species coexistence, there would be no need for this book. However, most 32 plant communities comprise persisting populations of several species. Populations may increase or 33 decrease through neutral drift or weather fluctuations and species can immigrate or disappear from the 34 local community. However, long-term studies such as the Park Grass experiment (Silvertown 1987) and 35 Bibury (Dunnett et al. 1998) show that the basic tendency is persistence, for example, outbreaks are 36 often followed by a decrease back to the original abundance. This coexistence is the fundamental 37 statement to be made about plant communities, and how it is achieved is the fundamental problem. 38 Resources (e.g. light and nutrients) are almost always limiting. Competition, and thus 39 interference between individuals and species, is demonstrable in all types of habitat, except immediately 40 after disturbance (chap. 6, sect. 9.3 below; Clements et al. 1929). Interference abilities can never be 41 exactly equal, so the result should be the exclusion by interference of all but one species (Gause 1934). 42 Therefore, the amazing thing is not that the species in plant communities show any particular patterns of J.B. Wilson & Agnew, chapter 4, Species coexistence, page 2 of 30 43 coexistence, but that they coexist at all. Hutchinson (1941; 1961) asked: "How [is it] possible for a 44 number of species to coexist in a relatively isotrophic or unstructured environment, all competing for the 45 same sorts of materials?". He called it the “Paradox of the Plankton”. 46 Monospecific stands of vegetation do exist, i.e. with only one vascular plant species (Plate 4.1). 47 Table 4.1 lists those that we have seen ourselves. They are often at land/water ecotones, in wet places 48 and especially in open water or extreme saline environments. In arid countries, a monotonous vegetation 49 of one halophytic species can dominate the landscape (Zohary 1973). We could generalise that these are 50 habitats where only one species is capable of growth due to a harsh environment, or where the 51 exuberance of one species excludes others by interference, but in some cases it is hard to know whether 52 to credit the extreme habitat or the high interference, e.g. Phragmites communis reedswamps. 53 Table 4.1. Some examples of monospecific stands. We exclude monospecificity in a single stratum or 54 guild of vegetation, such as a tree species or understorey species. Habitat Arid Saline Sand dunes Marine submerged Freshwater submerged Freshwater floating Freshwater edge Tidal/brackish edge River edge 55 Climatic zone Exemplar taxa Reference Sub-tropical Halocnemum strobilaceum Zohary 1973 Temperate Zygophyllum dumosum Zohary 1973 Ammophila arenaria Mediterranean Posidonia oceanica (also Den Den Hartog 1970 other marine Helobeae) Temperate Zostera marina Den Den Hartog 1970 Temperate Sagittaria sagittifolia Pieterse and Murphy 1993 Tropical Podostemon spp. Meijer 1976 Temperate Lemna minor Scunthorpe 1967 Azolla filiculoides Scunthorpe 1967 Tropical Eichornia crassipes Pieterse and Murphy 1993 Temperate Typha spp Weisner 1993 Cladium mariscus Tansley 1939 Tropical Cyperus papyrus Lind and Morrison 1974 Temperate Salicornia spp Tansley 1939 Subtropical Avicenna marina Batanouny 1981 Tropical Rhizophora mangle Gilmore and Snedaker 1993 Tropical Pandanus spp van Steenis 1981 At the other extreme is vegetation with high species richness. Values depend on the size of the 56 sample units, the life form guild being considered (e.g. often trees alone are recorded in tropical forests) 57 and the recording convention used (rooted or shoot presence, perennially or seasonally visible). 58 Whatever the sampling regime, extraordinarily high diversities can exist. Tropical rain forest is always 59 quoted as an example. Valencia et al. (1994) found 473 species of tree (individuals >5 cm dbh) in 1 ha 60 of Ecuadorian tropical rain forest, while Richards (1996) tabulates other examples with over 100 species 61 in 1 ha in New World and Malesian (not African!) tropical forests, Naveh and Whittaker (1979) 62 recorded 179 vascular species in 0.1 ha of a dry shrub/grass community in Israel. Mean species richness 63 of 18.3 per 0.01 m2 has been found in bryophyte carpets in the per-humid West Cape in New Zealand J.B. Wilson & Agnew, chapter 4, Species coexistence, page 3 of 30 64 (Steel et al. 2004) and 12.2 species at that scale in limestone grassland on Oeland, Sweden (van der 65 Maarel and Sykes 1993). 66 Box 4.1: Mechanisms of coexistence. 67 68 69 70 Stabilising mechanisms Niche-differentiation 1. Alpha-niche Differentiation (type of resource and time of availability) 2. Environmental Fluctuation – season, decadal and gradual change 71 72 73 Balances 3. Heterotroph challenges: Pest Pressure 4. Circular competitive networks 74 75 76 77 78 Escape through movement 5. Allogenic Disturbance – disrupting growth mainly mechanically 6. Competition/dispersal Tradeoff 7. Initial Patch Composition 8. Cyclic Succession: movement of community phases: 79 80 81 82 83 84 85 86 Equalising mechanisms 9. Equal Chance (neutrality) 10. Inertia Temporal Inertia Spatial Inertia: aggregation 12. Coevolution of Similar Interference Ability 13. Spatial Mass Effect (vicinism) Questions about coexistence must be asked at a particular spatial scale. The rainforest tree 87 Swietenia mahogoni (mahogany) occurs in the tropics and Colobanthus quitensis occurs in Antarctica; 88 they cannot be said to coexist. They grow in quite different places and environmental conditions, i.e. in 89 different beta niches. Similarly, Salicornia spp. (glasswort) occur on low-altitude saltmarshes and 90 Androsace spp. are alpines, again they occupy different beta niches. The Paradox of the Plankton as 91 defined by Hutchinson refers to how coexistence can occur in a “relatively isotrophic or unstructured 92 environment”. This scale is difficult to define, because allogenic environmental heterogeneity occurs 93 down to the very finest scales, so all species in a mixture exist as a pattern of abundance. The species’ 94 patterns will create further patchiness in resources since species differ in their resource economies: their 95 reaction on the environment. Numerous studies have shown that each species’ individuals affect its soils 96 (section 1.3), which can give autogenic heterogeneity. Also, each individual, by extending over space, 97 must sample a spectrum of resource and environmental qualities. Therefore, rather than specify a 98 particular scale, we state here that we are concerned with mechanisms that allow species to coexist 99 locally, i.e. mechanisms that are not due to imposed habitat heterogeneity within the area considered. 100 J.B. Wilson (1990) identified 12 distinct mechanisms by which coexistence could be maintained: 101 (1) Alpha-niche Differentiation, (2) Environmental Fluctuation, (3) Pest Pressure, (4) Circular 102 Interference Networks, (5) Allogenic Disturbance, (6) Interference/dispersal Tradeoff, (7) Initial Patch 103 Composition, (8) Cyclic Succession, (9) Equal Chance, (10) Inertia (temporal and spatial), J.B. Wilson & Agnew, chapter 4, Species coexistence, page 4 of 30 104 (11) Coevolution of Similar Interference Ability and (12) Spatial Mass Effect. We believe them to be 105 distinct and we know of no new ones, though we have adopted a different arrangement that we hope 106 brings some new insights. 107 There is a basic distinction between stabilising mechanisms, which contain an increase-when- 108 rare mechanism, and equalising mechanisms, which make the differences between species in 109 replacement rates smaller (Box 4.1; Chesson 2000). Stabilising mechanisms (1 to 8 in Box 4.1) are 110 driven by Alpha-niche Differentiation, Environmental Fluctuation, balances unrelated to niches or 111 escape through movement (Box 4.1). Species abundances are bound to fluctuate and stabilising 112 mechanisms must include negative abundance-dependence to counter this. [For animals, ‘density- 113 dependence’ is often used, but since the concepts of ‘individual’ and ‘density’ are difficult in most 114 plants (chap. 1, sect. 1.1) the more general ‘abundance-dependence’ should be used.] This means that 115 when a species is at lower biomass in the community its plants must have higher fitness in terms of 116 long-term RGR, and its biomass should increase (Chesson in press). Simply, the one necessary and 117 sufficient phenomenon for maintaining a species in a mixture is ‘increase-when-rare’1. The corollary of 118 this is population limitation, i.e. reduced fitness as biomass increases. Either way, a species’ fitness 119 should be inversely related to its abundance. In the short term and in species that reproduce only 120 vegetatively we should consider vegetative RGR (relative growth rate). In the longer term, population 121 growth is the critical question. The increase-when-rare feature is incorporated into the Lotka-Volterra 122 logistic function, as every schoolboy knows. A feature that interferes with this in the real world is the 123 Allee effect, whereby populations cannot recover from very low numbers due to low success in mating. 124 We believe that it is rare in plants because, as we outlined in chapter 1, each individual is effectively a 125 colony and perennials have an indefinite life span. Nevertheless there are examples of the effect in 126 Banksia goodii, a shrub of dry savannah (Lamont et al. 1993), and in the outpollinated annual Clarkia 127 concinna in California (Groom 1998). Species with obligate outcrossing and/or scattered distributions 128 and/or monocarpic reproduction and/or specialised pollen vectors would be more liable to it. 129 True coexistence must be through a stabilising mechanism. Equalising processes do not contain 130 an increase-when-rare mechanism, but are ways in which species may persist for a time in unstable local 131 coexistence, slowing exclusion by interference. Moreover, if the difference between the interference 132 abilities of species is large, even the presence of a stabilising mechanism may not prevent exclusion by 133 interference and in this situation an equalising mechanism might reduce the difference in interference 134 ability between two species so that the stabilising mechanism is able to cause coexistence (Chesson 135 2000). Ultimately every plant has established itself by a process that can be explained by its tolerances 136 (its niche) and the environmental conditions prevailing during its ecesis, but the reasons for a species' 137 presence in a particular spot are usually obscure. For example, a tree may persist for so long that the 138 local soil/geomorphological conditions that allowed it to establish have since changed. It is therefore J.B. Wilson & Agnew, chapter 4, Species coexistence, page 5 of 30 139 tempting to suggest that each individual's presence owes as much to chance as to ecological 140 differentiation and a theory of equal chance has been proposed to explain species mixtures, as we 141 discuss below. Again, species may persist temporarily through inertia of individuals or populations in 142 time or aggregation in space. Any process causing similarity in interference ability is also equalising. 143 Lastly, and rather hesitantly, we include the Spatial Mass Effect as an equalising mechanism. 144 1 Alpha-niche Differentiation 145 We discussed alpha niches in chapter 1 (sect. 4.1). It has been pointed out that coexistence by 146 Alpha-niche Differentiation is impossible to disprove. Each species must by definition occupy a 147 different niche (chap. 1, sect. 2.1). Moreover, by reaction it uniquely constructs part of its niche. The 148 other side of the coin is that if redundancy really occurs, i.e. there are coexisting species that do not 149 differ in alpha niche, they will not coexist by this mechanism and some of the 11 other mechanisms 150 mentioned below must account for their presence. The ‘increase when rare’ element occurs here because 151 when a species is rare the resource that it particularly takes up and requires will be present in greater 152 abundance, that is, the niche is not fully occupied, though interference with this process could come 153 through luxury uptake of nutrients (Lipson et al. 1996). The population limitation on the other hand is 154 due to full niche occupancy, i.e. full use of its resource. The degree of niche separation required will 155 increase with the difference in interference ability between the species; if one species is a very strong 156 competitor another species will be able to coexist only if it is occupying a completely different niche. 157 However, in contrast to some stabilising mechanisms of coexistence, if the niche differentiation between 158 two species is strong enough, they can always coexist. 159 1.1 Resources (type of resource and time of availability) 160 Tilman (Titman 1976) demonstrated that coexistence was possible between two algae limited by 161 different nutrients, P and Si, and concluded that the number of species able to coexist is equal to the 162 number of resources and then only if each species is limited by a different resource. He confirmed this 163 in modelling (Tilman 1977), and there appears to have been no contradiction. Vance (1984) claimed to 164 show that two species can coexist on one limiting resource, but only “if each species interferes less with 165 resource acquisition by the other than with resource acquisition by itself”, which with pure competition 166 must mean niche differentiation (e.g. the one resource is water, but it is taken up from different soil 167 strata). 168 The primary resource requirements of most embryophytes are similar (light, water, CO2, N, P, K, 169 minor elements, sometimes pollination and dispersal). The concept of a resource gradient as niche 170 differentiation is simple for seed sizes as a resource for birds, but it applies less readily to plants, for 171 which most of the resources are discrete requirements. For example one species cannot require a low- 172 concentration type of P and another a high-concentration type, and the two cannot occur simultaneously J.B. Wilson & Agnew, chapter 4, Species coexistence, page 6 of 30 173 anyway. However, in other cases such as soil resources at different depths and pollinator service during 174 the season (section 2), the separation and specialisation of species along gradients are important 175 mechanisms of coexistence (Fig. 4.1; MacArthur and Levins 1967). An important question is how much 176 separation is needed, but in spite of the calculations of MacArthur and Levins this remains unanswered 177 for the real world. Even the existence of such niche limitation has been controversial and difficult to 178 prove (chapter 5). 179 Fig. 4.1. The MacArthur and Levins (1967) concept of niche separation along a gradient. 180 The above-ground structure of a plant is a light-capture mechanism. Therefore gross 181 characteristics of plant form have great relevance. Consider tree size and shape in rain forest, where 182 light is the prime resource; Kohyama (1992) and Akashi et al. (2003) concluded from modelling that 183 short species, with high seedling recruitment but with height-limited growth, could coexist with taller 184 species with lower recruitment rates. This is basically niche differentiation based on canopy strata. 185 Kohyama (1993) used the model to show that stable coexistence resulted without requiring a stand 186 mosaic and Yokozawa et al. (1996) demonstrated that two canopy shapes, conical and spheroidal, could 187 interact with different speeds of recruitment to give situations that allowed a diverse canopy flora. These 188 are subtle and devious ways in which resource differentiation takes place in this famous biome. 189 Stratification below ground, i.e. in rooting depth, is another important niche gradient (chap. 1, sect. 4.3), 190 especially when there is both precipitation and an accessible water table. 191 Two types of temporal gradient can be seen: (1) If growth is triggered by the resource itself, 192 species can differ in their speed of reaction to resource availability, their opportunism. Opportunistic 193 species react fast to resource availability, for example production of surface roots of succulents, 194 ephemeral leaves like Grewia spp. (cross berry) that have a leaf flush after every rain in African summer 195 deciduous bushland, and seasonally produced leaves that must survive periods of resource starvation. 196 (2) More commonly seasonal separation of species' growth patterns is controlled not by the resource 197 itself, but by signals such as daylength and temperature. This causes regular seasonal phenological 198 separation of species’ activity. Here, the mechanism overlaps with the Storage effect (section 2). 199 1.2 Heterotroph-imposed niches 200 Pollination and dispersal can be switch mediators (chap. 3, sect. 5.4.G), but also means of niche 201 differentiation. Pollinators come in many sizes and specialisations: insects, birds, mammals and even J.B. Wilson & Agnew, chapter 4, Species coexistence, page 7 of 30 202 reptiles. Among insect pollinators there is huge variation in characteristics and their interplay with 203 plants can be rich and complex. There are robbers, mimics, rewards, guides and warnings. The 204 pollination niche is liable to the Allee effect, both for self-incompatible plants when there is no mate in 205 the neighbourhood and for those specialised to particular pollinating insects when the plant population is 206 not large enough to attract the pollinator. Dispersal tends to be less specialised, without an equivalent to 207 the close relation between flower morphology and pollinator morphology seen with some insects and 208 birds, but differences in fruiting times could reduce competition for dispersers. An Allee effect is 209 possible in dispersal if the population is too small to attract more specialised dispersers. Allee effects 210 can neutralise an increase-when-rare mechanism. 211 Vascular plants could occupy different niches by associating with different mycorrhizal fungi. 212 However, specificity within the two main groups of fungi (VAM, ecto, ericoid/epacrid, etc.) is 213 quantitative, in terms of efficacy rather than in absolute ability to colonise the roots. Moreover, the 214 effect on the higher plant with all types is on availability of soil nutrients (especially P) and water, and 215 the loss is in carbon. We conclude that niche diversification through mycorrhizae is unlikely. 216 1.3 The niche extended by reaction 217 The alpha niche is not a pre-existing box into which a species has to fit. We have emphasised 218 that the individuals of a species react on their environment, changing it and to a lesser or greater extent 219 constructing their own niche. Ramets of a species always show some sort of density pattern (chap. 3, 220 sect. 1) and this pattern must cause patchiness in the micro-environment of the habitat. Litter production 221 is often the basis for nutrient heterogeneity, but plant morphology and root growth can also be the cause 222 (Vogt et al. 1995). Habitats, therefore, must always be patchy in resource availability and physical 223 environmental actors and the size of the patches depends on the pattern of densities of each species. 224 There is evidence of this, particularly from forests where the sheer size of the trees makes their patches 225 large and easy to sample. For example, Pelletier et al. (1999) examined a mixed-species forest in 226 Québec, Canada, and found using ordination that forest-floor soil was different beneath different 227 species. For example, soil [Ca] was low below Fagus grandifolia (American beech) and they concluded 228 that it reduced the soil [Ca]. In most such observational studies there is a chicken-and-egg problem, that 229 perhaps the soil differences are determining which species grows at a point, not the reverse. However, 230 Pelletier et al. went two steps further: (a) they used spatial statistics to remove spatial correlations, so 231 that as far as possible they were examining the effects of individual trees, and (b) they offered evidence 232 that F. grandifolia produces litter which, from its Ca, lignin, polyphenol and tannin contents, was likely 233 to reduce soil [Ca]. The study of Ehrenfeld et al. (2001) went that step further in another way. They 234 found higher pH below two exotic species in a deciduous forest in New Jersey, USA, than beneath the 235 native Vaccinium spp., but they also grew the species in the greenhouse on field soil and found pH J.B. Wilson & Agnew, chapter 4, Species coexistence, page 8 of 30 236 differences in the same direction. The main problem for interpretation here is that the two exotics 237 (planted together) may have raised the pH more because of their greater growth. 238 Presumably plants can have the same effects, but there are few published studies. This argument 239 is that every plant community must show pattern associated with each of its constituent species, but 240 there are other biotic forces making habitats more heterogeneous. Litter is not only a significant niche 241 factor, but one especially liable to cause change by reaction. 242 The necessary presence of patches in a community is important to every species’ resource 243 foraging strategy. Large resource patches are best exploited by stoloniferous herbs (Wijesinghe and 244 Hutchings 1997). Jackson and Caldwell (1996) modelled the effect of root plasticity on the uptake of 245 nutrients from heterogenous versus homogenous environments and found that plasticity was 246 theoretically highly advantageous in sagebrush steppe conditions. In the same habitat the effect of 247 patchy soil nutrients differentially affected Agropyron desertorum (wheatgrass) and Artemisia tridentata 248 (big sagebrush), but only under shade conditions where carbon gain was reduced (Cui & Caldwell, 249 1997). Here A. desertorum outcompeted A. tridentata because, although its root proliferation was 250 reduced, its efficiency of P uptake was not and it could exploit rich patches. A. tridentata on the other 251 hand lost efficiency of P uptake and could not make use of patches of higher P availability. 252 Of course, the above-ground environment is altered too. Canopy trees create a 253 shade/temperature/humidity niche for understorey plants, that might not be able to survive without those 254 modifications. Many manifestly cannot do so in mixture with other species, since they are restricted to 255 forest understories. Trees also create the niche for climbers and epiphytes via their support, and they 256 create a niche for many epiphytes by water and nutrient stemflow. Parasite plants obviously occupy a 257 niche that would not exist without other plants; the term ‘niche construction’ is very appropriate here. 258 2 Environmental Fluctuation (seasonal, annual and decadal change) 259 Species can separate along annual and other changes in the environment, predictable and 260 unpredictable. We cannot talk of coexistence caused by millenial-scale fluctuation unless the plants are 261 very long-lived (say 500+ yr), because exclusion by interference may happen before the environmental- 262 fluctuation coexistence mechanism can operate. We discuss flowering and fruiting niche gradients, 263 mediated by pollinators and dispersers, in chapter 5 (sect. 6.2) and species can also separate along niche 264 axes of vegetative phenology. An excellent example is the vernal ground flora of deciduous forest. 265 Fargione and Tilman (2005b) found evidence that vegetative phenological niche differentiation added to 266 rooting-depth differences in facilitating the coexistence of species at Cedar Creek with the dominant 267 grass Schizachyrium scoparium (bluestem). Separation in flowering times will reduce competition for 268 pollinators, giving coexistence based on niche differentiation. 269 270 Environmental fluctuation can cause coexistence if it be on scales shorter than this but long enough for there to be feedback on resources. The fluctuation can be one that affects vegetative growth, J.B. Wilson & Agnew, chapter 4, Species coexistence, page 9 of 30 271 for example the vernal flora of forests and spring ephemerals of semi-arid areas, though there is often an 272 accompanying fluctuation in reproduction. 273 As will be clear below, there has to be an interaction between growth and resource supply for 274 environmental fluctuation to cause coexistence. There has been confusion about this. Many authors have 275 claimed that simple variation in the environment and therefore in demographic parameters would allow 276 long-term coexistence. For example, Gigon (1997) wrote: “The fluctuations and their interferences mean 277 that no species encounters optimal growth conditions for a prolonged period of time. Therefore no species 278 can outcompete the others. Fluctuations are thus decisive for the coexistence of species”. Coexistence 279 cannot happen this way. For coexistence, the long-term growth rate of each species has to be RGR = 0.0 280 (r = 0.0, λ = 1.0). The long-term growth rate for a species is the arithmetic average of RGR (the 281 geometric average of λ) in each period. Variation in growth rate will not make it more likely that long- 282 term r is 0.0, in fact a value of exactly 0.0 due to such averaging is infinitely unlikely. Whilst it is true 283 that environmental variation can cause coexistence it can also promote exclusion by interference or have 284 no effect at all on coexistence/exclusion, depending on the biological response of the species to the 285 environment and to competition (Chesson 1990). There are only two ways in which temporal variation 286 can lead to the coexistence of two species: Relative non-linearity and Sub-additivity. These can cause 287 coexistence only if the interference unbalance between the two species is not too great, and equalising 288 mechanisms can contribute to this. 289 Relative non-linearity means that two species respond differently to levels of a resource for 290 which they are competing, and moreover that they respond by differently-shaped relations (Chesson in 291 press). For example, the three scenarios in Fig. 4.2 count as different shapes. The way to test for 292 Relative non-linearity of shapes is to plot the values of RGR of one species at each level of resource R 293 against the values of the other: if the result is anything but a straight line, the species are relatively non- 294 linear. C D RGR A F B Rmean Resource level [R] Rmean Resource level [R] Rmean Resource level [R] E Fig. 4.2: Pairs of two species showing relative non-linearity. 295 296 Take the third graph. If [R], the level of resource R, is constant at the mean value (Rmean), species E has 297 a higher RGR than F. However, if there be environmental fluctuation around the mean, the mean growth 298 rate of F would be higher. Thus, low fluctuation in [R] advantages E, high fluctuation advantages F. 299 The reason this matters is that at low [R] species E grows faster than F and therefore depletes the J.B. Wilson & Agnew, chapter 4, Species coexistence, page 10 of 30 300 resources, at high [R] it grows little more than at Rmean, and leaves much of the R unutilised. Both ways, 301 when species E is in the majority it exacerbates the fluctuations in [R]. Conversely when it is in the 302 minority, fluctuation in [R] is lower, which favours it: increase when rare is achieved. 303 In contrast, species F grows little at low [R], and will hardly deplete R. At high [R] it grows 304 disproportionately fast, absorbing R and therefore reducing [R]. Both ways, when species F is in the 305 majority it damps down the fluctuations in [R]. Conversely when it is in the minority, fluctuation in [R] 306 is higher, which favours it: increase when rare is achieved. 307 308 The second way that environmental fluctuations can cause coexistence is the Storage effect (Chesson in press. There are four requirements for the Storage effect to operate: 309 1. The species must be competing for a resource. 310 2. They must be affected by an environmental (i.e. non-resource) factor, and respond differently 311 312 to it. 3. There must be covariance between the environmental factor and the intensity of competition. 313 We would expect this, because when the plants are denser and/or larger, competition will 314 be more intense. That is, in ‘favourable’ conditions competition will be greater. 315 4. There must be subadditivity (= buffering, = an interaction between environment and 316 competition). That is to say, when environmental conditions are favourable to growth the 317 effect of competition on RGR is greater. So, whilst ‘3’ refers to the intensity of 318 competition, ‘4’ refers to the effect of competition. 319 In years (or other periods) when the environment is favourable for a species, if it is in the majority and 320 therefore competing against itself it cannot take much advantage of the favourable conditions because it 321 is competing against itself at high biomass: X in Fig. 4.3. Competitive intensity X Low RGR High RGR Environmental favourability Fig. 4.3: The effect of competitive intensity and environmental favourability on RGR. For ‘X’, see the text. 322 323 Chesson’s (1994) calculations indicate that the Storage effect is a considerably stronger force than 324 Relative non-linearity. J.B. Wilson & Agnew, chapter 4, Species coexistence, page 11 of 30 325 These mechanisms clarify that the timescale on which environmental fluctuation can cause 326 coexistence is set by the timescale on which resource depletion can occur. Light intensity can change 327 instantaneously, it cannot be stored from one second to another and its effects in producing 328 photosynthate are quite short-term, so within-day fluctuation could suffice. Water depletion could occur 329 over a few days, and nutrient depletion over a few months. Soil nutrients often become more available 330 in the spring due to mineralisation, but slow uptake over winter, and are depleted during the period of 331 active growth, so the Storage effect can operate on within-season or between year variation in nutrient 332 use. For neither Non-linearity or the Storage effect do the species need to differ in the resources they 333 use. However, they do use them at different times. Seasonal differences in resource use can be seen 334 either as Alpha-niche Differentiation or as the Storage effect. 335 3 Pest Pressure (heterotroph challenges) 336 Both pathogens and herbivores (from insects to large mammal herbivores) have the potential to 337 give an increase-when-rare process (we use ‘pest’ to cover both pathogens and herbivores). For this, 338 three conditions are required. 339 1. Impact: the pests involved must have a significant impact on the growth and/or survival of the 340 plant species, i.e. their fitness must be reduced. 341 2. Specificity: The pests involved must be to some degree specific to the plant species. It could be 342 sufficient for the species with lowest interference ability to have no specific pests/diseases, but 343 to benefit when the others are suppressed by pests/diseases. 344 3. Abundance-dependence: The challenge from pests must be less on a sparse than on an abundant 345 species. This represents an abundance-dependent effect. The requirement is for a lower impact 346 on the growth and reproduction of sparse species, but this will presumably be through reduced 347 infection. 348 If these three conditions obtain, when any one of the plant species in the mixture becomes more 349 abundant, the host-specific pest (Condition 2) will move more rapidly amongst its host population and 350 the degree of infestation will increase (Condition 3). This will reduce its fitness (Condition 1). This will 351 not directly impact other species, or will do so only to a lesser extent (Condition 2). Conversely, when a 352 species becomes sparse, infestation by its specific pests will decrease and its fitness increase relative to 353 its fitness when more abundant, giving the increase-when-rare effect. Again, the strength of conditions 354 1-3 necessary for coexistence depends on the degree of difference in interference ability, and equalising 355 mechanisms of coexistence can allow Pest Pressure to result in coexistence when it otherwise would 356 not. 357 Condition ‘1’ can often be met, since pests have various effects on plant production. Basically, 358 the pest organism must have a carbon requirement, which is almost bound to result in lower production 359 and fitness for the plant. Many pests are quite specific to a species or group of plant species, meeting J.B. Wilson & Agnew, chapter 4, Species coexistence, page 12 of 30 360 condition 2. Ecologists tend more to question condition ‘3’ because it is less obvious how abundance- 361 dependence could operate. Possible mechanisms (Boudreau and Mundt 1997) are via: (a) a decreased 362 abundance of palatable / susceptible plants, which inhibits the dispersal of herbivores, disease-spores or 363 disease-vectors, (b) the flypaper effect for disease spores and possibly for insect pests, virus vectors and 364 hence for the viruses they carry, in which the pest is caught by a passive surface, (c) alteration in the air 365 flow and microclimate, (d) chemicals from associated species that repel herbivorous insects, and (e) 366 promotion by an associated species of natural enemies of the herbivorous insects, i.e. their predators. 367 We shall discuss diseases and herbivory separately since they act in different ways with different 368 dynamics. However, there is sometimes evidence for abundance-dependent mortality or a reduction in 369 growth that is circumstantial evidence for the process and therefore for the Pest Pressure mechanism, 370 that cannot be attributed to a particular pest. For example, Packer and Clay (2000) examined the 371 distribution of seedlings of Prunus serotina (black cherry). The greatest number of seeds germinated 372 quite close to their parent tree, 5-10 m. However, 4 months later and thereafter up to 28 months, 373 seedling survival was higher the greater the distance from the parent tree, up to the furthest distance 374 monitored (30 m). This is not always the pattern. Dalling et al. (1998) in tropical rainforest on Barro 375 Colorado Island found that seedlings tended to be denser nearer to an adult of the same species. For 376 temperate forests Houle (1992) found the seedling mortality of Acer saccharum (sugar maple) in an 377 Eastern American forest was not abundance-dependent; there was no particular spatial relation between 378 trees and seedlings. Hyatt et al. (2003), in a thorough review of the literature, found no evidence for an 379 effect of distance from conspecifics on seed survival in either temperate or tropical communities, but 380 there was a tendency for seedlings to show higher survival at distance, with hints that this occurred 381 especially in the tropical forests. This matches the conclusions of Wright (2002) who, with a rather 382 different review approach, found considerable evidence of low growth performance of saplings near 383 conspecific adults. When effects like this are found, they are assumed to be because of Pest Pressure, 384 though Wright discusses other explanations. This kind of pattern recalls the ‘Janzen-Connell’ hypothesis 385 that whilst the greatest density of fruit will be dispersed to near the parent plant, pests will have the 386 greatest impact there, so the maximal regeneration will occur at an intermediate distance from the 387 parent. This would be expected to be an important abundance-dependent method of species' 388 maintenance in diverse, stable communities of trees, specifically tropical rain forest, but it seems that it 389 is far from universal. 390 3.1 Pathogens 391 Pathogens act in the soil, in the plant systemically and in the plant’s photosynthetic and 392 reproductive systems. The impact of fungal pathogens can be considerable. Mihail et al. (1998) found 393 that in a greenhouse experiment with the annual legume Kummerowia stipulacea (Korean clover) the 394 fungus Rhizoctonia solani caused mortality that reduced plant density by 40 % whilst the fungus J.B. Wilson & Agnew, chapter 4, Species coexistence, page 13 of 30 395 Pythium irregulare reduced density by 80 %. C.E. Mitchell (2003) found that in an oldfield grassland at 396 Cedar Creek 8.9 % of the leaf area was infected by fungal pathogens, which decreased root production 397 by 25 % by decreasing leaf life, while herbivores had no effect. 398 399 The species-specificity requirement is less easy to meet. Gilbert (2002) concludes that the evidence so far indicates that in natural communities that most fungi infect a large number of hosts. 400 However, the abundance-dependence criterion can often be met. Most ephemeral pathogens are 401 transmitted aerially including rusts and smuts which affect leaves, stems and floral parts. Abundance of 402 the host plant affects the pathogen's population and its persistence, and the transmission of specialist 403 pathogens can be highly sensitive to the identity of other host species in the community (Boudreau and 404 Mundt 1997). An example is the Ustilago violacea smut on Silene alba (≡ S. latifolia; white campion), 405 for which Thrall and Jarosz (1994) experimentally compared the behaviour of the host and pathogen 406 populations to theoretical models. The match was good and showed that both density dependence and 407 frequency dependence occurred. An excellent study by Burdon et al. (1992) described the mortality of 408 Pinus sylvestris (Scots pine) caused by the snow blight fungus Phacidium infestans as being mostly 409 abundance-dependent, with greater mortality in subsites where the host had been denser the previous 410 year. This abundance-dependence has sometimes been shown to lead to a lower pathogen load in 411 mixtures, which must imply some host specificity. C.E. Mitchell et al. (2002) examined 147 plots in an 412 experiment at Cedar Creek established by Tilman and co-workers, sown and weeded to species richness 413 from 1 to 24 species. The percentage of each leaf visibly infected was guessed, using calibrated cards as 414 a guide. Infection dropped as species richness increased, the 24-species plots having only 37 % the 415 foliar fungal pathogen load of the mean monoculture (though more than the least-infected monoculture). 416 Similarly, C.E. Mitchell et al. (2003) analysed another Cedar Creek experiment sown and weeded to 1 417 to 16 species, and the pathogen load in the 16-species plots was only 34 % of that in the mean of 418 monocultures. In chapter 3, sections 6 and 7.5 we described the ‘selection’ artefact in overyield and 419 invasion-resistance experiments. A similar artefact would be possible here if the species less susceptible 420 to disease had thereby an interference advantage and increased its proportion in the mixture, so that the 421 mixture had a lower mean pathogen susceptibility and thus a lower pathogen load. However, C.E. 422 Mitchell et al. (2002; 2003) present evidence that this is not the cause of the effect they found. C.E. 423 Mitchell and Power (2006) conclude that “the transmission of specialist pathogens can be highly 424 sensitive to the identity of other host species in the community”. 425 Similar effects could be caused by below-ground pathogens. Bever (2003) modelled this, but 426 concluded that there is no evidence for it yet. 427 3.2 Herbivory, general 428 429 Herbivores come in all sizes, specialisations and guilds. On vegetative parts there are leaf eaters, stem borers and root eaters. On reproductive systems there are flower exploiters, frugivores and J.B. Wilson & Agnew, chapter 4, Species coexistence, page 14 of 30 430 granivores. Plant species are variously adapted to herbivory, with chemical and physical defences, life 431 histories and growth patterns that have evolved seemingly to deal with the challenges. The potential 432 mechanism for coexistence via herbivory is similar to that for pathogens (chap. 2, sects. 7.3, 7.4). 433 However, whilst pathogens often reduce the functional efficiency of plant parts, most herbivores simply 434 remove plant material so that the plant needs to regrow to replace tissue and thus its resource base. 435 Obviously a great variety of relationships can be expected between plant species and their herbivores, 436 including symbiotic ones, such as Tegeticula spp. and Parategeticula spp. (yucca moths; James et al. 437 1993). In many of these systems herbivores exploit plant populations in an abundance-dependent way. 438 Grover (1994) modelled this and used the keystone concept (chap. 5, sect. 11 below) to suggest that a 439 controlling herbivore is one that holds down the abundance of a potentially-dominating plant species 440 and thus allows subordinate species to survive. We may distinguish between abundance-dependent 441 culling of seeds and seedlings and wholesale removal of plant material, i.e. vegetative herbivory. 442 3.3 Herbivory of disseminules and seedlings 443 Seeds and seedlings are a rich nutritional resource and are heavily predated. Maron and Gardner 444 (2000) showed by modelling that herbivores can control adult population abundance by limiting the 445 seed input to the seedbank. Such limitation seems to be widespread. It occurs also via vegetative 446 disseminules. Thus, the ‘impact’ requirement of the Pest Pressure mechanism can be met by 447 disseminule/seedling herbivory. 448 Disseminule herbivory can often be abundance-dependent. Cygnus bewickii (swans) eat the 449 turions (disseminules, fleshy buds) of Potamogeton pectinatus (pondweed) in the autumn. Jonzen et al. 450 (2002) demonstrated clear abundance-dependent control of the P. pectinatus in which the denser patches 451 of turions were exploited, reducing their density, while areas of low turion densities were unexploited 452 and here the plant density subsequently increased. Edwards and Crawley (1999) examined four species 453 of British meadows and found that granivory by rodents was abundance-dependent, but its effects on 454 adult densities differed. Densities of species with bigger seeds (Arrhenatherum elatius, oat grass; and 455 Centaurea nigra, knapweed) appeared to be reduced, but in the smaller seeded Rumex acetosa (sorrel) 456 and Festuca rubra survival increased to compensate for seed predation, with no overall effect on plant 457 density. Again, Ehrlen (1996) found that in Lathyrus vernus (spring pea), although seed predation by a 458 Bruchidae beetle was correlated with seed density in small plots and with inflorescence size, this had no 459 consistent effect on plant population recruitment. Thus, even the occurrence of abundance-dependent 460 seed predation is no guarantee that it will control the population and hence contribute to species 461 coexistence. 462 Another limitation of disseminule/seedling herbivory as a mechanism of coexistence may be that 463 most mammal granivores are not specific to one species. There is huge literature assuming that bird 464 granivores are restricted by beak size to a particular range of fruit/seed sizes, but not to one species. J.B. Wilson & Agnew, chapter 4, Species coexistence, page 15 of 30 465 However, species of Bruchid beetle are generally restricted to the seeds of one or a few species of 466 Fabaceae (legumes). Seedlings are presumably eaten by invertebrates, but they are likely to be quite 467 generalist. 468 3.4 Vegetative herbivory 469 Herbivory on vegetative parts can be considerable. Vertebrate herbivores (Jones 1933) are 470 involved, and insects both above- and below-ground (Brown and Gange 1989). The selectivity of 471 herbivores varies widely. Many large non-ruminant animals such as Loxodonta africana (African 472 elephant), even though they have preferences, will readily eat a wide range of species. More 473 importantly, some such as Equus spp. (horses) often graze finely-patterned vegetation at a relatively 474 coarse scale, necessarily taking in species with a range of palatability. Other ungulates such as sheep 475 and cattle are more selective, some tiny flower gall wasps are confined to one or a few plant species, 476 and some lepidopterans feed on only one species such as Tyria jacobaeae (cinnabar moth) on Senecio 477 jacobaea (ragwort): Plate 4.2. 478 There are cases when coexistence can be attributed rather clearly to insect vegetative herbivory. 479 For example, Carson and Root (2000) found that periodic plagues of folivorous chrysomelid beetles 480 checked populations of the dominant Solidago altissima (goldenrod) in an oldfield in New York state, 481 USA, and were responsible for the diversity and successional rates. The effect of vertebrate grazing in 482 increasing species diversity is well known, as shown by the rabbit exclosures erected by Tansley and 483 Adamson (1925). However, the effect there is surely that when the sward is higher, light competition is 484 more important, and especially there is more opportunity for the feedback between the outcome of 485 competition and interference ability to occur (chap. 2, sect. 2.3), allowing exclusion by interference. 486 This has nothing to do with any mechanism of coexistence between plant species. 487 3.5 Pest Pressure conclusions 488 The Pest Pressure effect seems most likely to operate via diseases. However, there can be 489 complex interactions. An example is seen on Netherlands sand dunes, on which there are relatively 490 uniform soils and clear successional sequences. The growth of the pioneer Ammophila arenaria 491 (marram grass) is impacted by nematodes and pathogens (Van der Stoel et al. 2002). The nematodes 492 reduce growth only early in succession and early in the season, and are not significant in the marked 493 decline in vigour commonly seen in older stands of A. arenaria. However, there is apparently a 494 synergistic effect between fungi, and between fungi and nematodes, which reduces A. arenaria’s 495 growth, and this is important in mixture with Festuca rubra, the next dominant in the succession 496 (de Rooij-van der Groes 1995; Van der Putten and Peters 1997). Later in the succession, in nutrient poor 497 grassland, there is often a mosaic of Festuca rubra and Carex arenaria (sand sedge). Here Olff et al. 498 (2000) discovered that each species had phases of increased and decreased vigour, replacing each other, J.B. Wilson & Agnew, chapter 4, Species coexistence, page 16 of 30 499 and that this process was associated with pest phases, particularly the plant-feeding nematodes. Each 500 species seems to be affected by different groups of pests, leading to the changing mosaic aspect of the 501 vegetation, which might look superficially like cyclic succession (chap. 3, sect. 4). 502 4 Circular Interference Networks 503 Interference relations between a set of species are said to be transitive if the species can be species A species C species B Fig. 4.4. A circular competitive network between three species. 504 arranged in a pecking order, such that a species higher in the order can always competitively exclude 505 one lower down. The opposite situation is the existence of circular interference networks (Fig. 4.4). If 506 such networks exist, they would contain an increase-when-rare mechanism: as species A starts to 507 displace species B, species C increases because it has high interference ability against A, but then it in 508 turn is replaced by B, completing the cycle. 509 Simple questions are not always neatly answerable. First, we note that the question can be asked 510 only in one environment, for competitive abilities will change with the environment (Keddy et al. 2000; 511 Fynn et al. 2005). Clearly they must; that is the main reason there is different vegetation in different 512 places. Second, the species that dominates the mixture will be the one with the higher relative growth 513 rate, but as interference proceeds the proportions of the species will change and as a result the relative 514 RGRs of the two species may change. Therefore, the eventual result must be judged in terms of 515 exclusion by interference (often loosely referred to as ‘competitive exclusion’). Yet we know that for a 516 variety of reasons (Chapter 4) exclusion by interference does not always occur. For these cases, the 517 question of transitivity cannot be asked. 518 Several studies have determined interference ability by comparing of species’ performances in 519 mixture with those in monoculture. Connolly (1997) pointed logical flaws in this. Correction can be 520 made for the “size-bias”, but the basic error has been comparison with a monoculture. We are tempted 521 to conclude that if species A grows more slowly in mixture than in its monoculture whilst species B 522 grows faster in mixture than in its monoculture, B has the higher interference ability. Yet Connolly’s 523 table (4.2), over the undefined period of his artificial data and assuming a starting biomass of 1, gives an 524 example where A does worse in mixture than in monoculture, and B does better in mixture than in 525 monoculture. Yet A has the faster growth rate in mixture (loge 2.77 – loge 1 = 1.02) than Species B (loge J.B. Wilson & Agnew, chapter 4, Species coexistence, page 17 of 30 526 2.71 – loge 1 = 1.00) and will come to exclude its competitor from the mixture (subject to the conditions 527 mentioned above). If B goes extinct it can hardly be said to have had the higher interference ability. Table 4.2. Which species has the higher interference ability? The starting biomass for both species was 1.00 Species Biomass in Biomass monoculture in mixture A 3.00 decrease 2.77 Winner in mixture B 2.64 increase 2.71 528 It turns out that what is essential in designing such an experiment is not the monocultures, as 529 many people had thought, but two harvests so RGR can be calculated. This invalidates almost all the 530 studies of transitivity done so far. All we have to do is to wait, perhaps for close to infinite time, and see 531 which species has the higher growth rate as the mixture approaches one of them. This is coming to be 532 one of those community ecology questions that are impossible to answer. 533 At the moment, it is interesting to look at the imperfect evidence available. Buss and Jackson 534 (1979) claimed several competitive cycles for coral reef sedentary organisms, as seen in static evidence 535 for overtopping. Likewise, Russ (1982) claimed non-transitive relations between species in the 536 overgrowth of sedentary marine organisms observed colonising experimental plastic sheets in the sea in 537 Australia, though no cycle can be made out of his results. 538 Turning to pure plant work, Mouquet et al. (2004) grew eight meadow herbs species in 539 replacement mixture in all possible pairs. Using relative yield (RYi,j = biomass of species i when 540 growing with species j / biomass of i in monoculture), if the species form a transitive hierarchy it should 541 be possible to arrange them so if species i is further up the hierarchy than species j, and RYi,j-RYj,I is 542 always positive. In his experiment, at both low and high density, it almost is, and with a very similar 543 order (Table 4.3). 544 Table 4.3. Competitive hierarchy from Mouquet et al. (2004), strong competitors at the top High density Holcus lanatus Rumex acetosella Cerastium glomeratum Anthoxanthum odoratum Festuca rubra Arabidopsis thaliana Lamium pupureum Veronica arvensis 545 Low density Holcus lanatus Rumex acetosella Cerastium glomeratum Anthoxanthum odoratum Festuca rubra Lamium pupureum Arabidopsis thaliana Veronica arvensis J.B. Wilson & Agnew, chapter 4, Species coexistence, page 18 of 30 546 At each density, there is one negative RY1,2-RY2,1 indicating a conflict with the hierarchy, it is between 547 species not contiguous in the hierarchy, but it is of size -0.05 or -0.06 which is clearly within the 548 experimental error. 549 A study that returned a clear answer to the question of transitivity is that of Roxburgh and 550 Wilson (2000a). It relates to a real community, since the seven species used in the interference 551 experiment were taken from that community, the University of Otago Botany Lawn, grown in lawn soil 552 in boxes placed near the lawn. The use of 10 replicates in careful experimental conditions allowed 553 significance tests. The seven species could be arranged in a hierarchy to which all significant 554 competitive relations conformed, i.e. if species X is higher in the hierarchy and species Y lower, then 555 the suppressive effect of X on Y is greater than that of Y on X (Fig. 4.5). In fact, relations between all 556 pairs of species, significant or not, were compatible with the hierarchy. 557 558 Fig. 4.5: Competitive relations in seven species from the University of Otago Botany Lawn. From 559 Roxburgh and Wilson (2000a). 560 The experimental design of Keddy et al. (1998) comprised planting a number of ‘wetland’ 561 species into a number of swards of wetland species. They report results for 18 species planted into five 562 swards. The 18 species tended to respond similarly to different swards, e.g. Kendal’s coefficient of 563 concordance took a rank of 0.7 (1.0 = complete agreement as to which target suffered more/less), highly 564 significant. Some of the variation in invader/sward combinations could be due to experimental error (no 565 replication was possible), but some results are impressive, e.g. the rank of Carex crinita (sedge) varied 566 only from 14 to 17 across the 5 swards (18=suppressed most), and Lythrum salicaria (purple loosestrife) 567 varied from 4 to 7 (1= suppressed least). J.B. Wilson & Agnew, chapter 4, Species coexistence, page 19 of 30 568 In a different approach, Silvertown et al. (1992) used data from an experiment where several 569 species had been planted in adjacent hexagons, and invasion between hexagons recorded. Examining the 570 difference between the invasion of Species A into Species B and that of Species B into Species A, 571 replacement rates could be calculated. A pecking order can be formed from these results (Fig. 4.6), with 572 no discrepancies (though L. perenne (ryegrass) and C. cristatus (dog’s tail) could equally well exchange 573 positions). There are qualitative discrepancies. Since H. lanatus (Yorkshire fog) can invade P. trivialis 574 (A) and P. trivialis can strongly invade L. perenne (B), the expectation would be that H. lanatus would 575 be able to invade L. perenne even more strongly, but in fact their invasion rates are exactly balanced 576 (C). Moreover, although the species A. stolonifera (creeping bent) at the top of the order can invade C. 577 cristatus at the bottom, the rate of replacement is less than for other pairs (D). Agrostis stolonifera Holcus lanatus A Poa trivialis D B C Lolium perenne Cynosurus cristatus 578 579 Key: Strong (> 0.2) difference in invasion rates 580 Weak-moderate difference in invasion rates 581 Invasion rates equal (i.e. no net invasion) 582 Fig. 4.6. The competitive hierarchy from invasion rates in data of Silvertown et al. (1992). 583 In a similar experiment Silvertown et al. (1994) used only four species, so there was less 584 opportunity for intransitivity, but in any case there was none in any of the four grazing treatments (Table 585 4.4). 586 Table 4.4: Competitive hierarchy of four species in four treatments in Silvertown et al. (1994). 587 Summer sward grazing height Winter and spring Invasion ability: greater → lesser 3 cm Grazed Lolium perenne → Festuca rubra → Schedonorus phoenix → Poa pratensis 3 cm Ungrazed Festuca rubra → Lolium perenne → Poa pratensis → Schedonorus phoenix 9 cm Grazed Festuca rubra → Lolium perenne → Schedonorus phoenix → Poa pratensis 9 cm Ungrazed Lolium perenne → Festuca rubra → Poa pratensis → Schedonorus phoenix J.B. Wilson & Agnew, chapter 4, Species coexistence, page 20 of 30 (1) A is taller than B and shades B out C produces an allelopathic chemical, toxic to A C C is shadetolerant, and scavenges nitrogen A o A Tree A is taller than shrub B and shades B out grass C lowers the temperature, and suppresses seedlings of A B B is taller than C (3) C (2) A B C shrub B shades out grass C, and is not affected by lower temperature (4) A is taller than B and shades B out B is taller than C, and fixes N B A C with A is taller than it, and shades it out C B B with C is taller than it, and shades C out 588 . 589 Fig. 4.7. Possible causes of intransitivity between three species: A, B and C. 590 A is taller than B and shades B out It’s interesting to wonder what ecological processes would give rise to intransitivity (Fig. 4.7). In 591 scenario ‘1’, we use an allelopathic chemical produced only by C and toxic only to A. This works, but 592 species-specific allelopathy is rather like Getafix’s magic potions in the Asterix books: it can 593 perform/explain any wonder. Scenario ‘2’ is similar, except that the third factor is lower temperature 594 (Ball et al. 2002) rather than a toxin. In ‘3’, we have to ask why C can suppress A; presumably the 595 shade-tolerance of C minimises the competition for light, so competition for N becomes important, and 596 C has the lower Tilman R* (chapt. 6, sect. 7.1). Why cannot C suppress B? Perhaps because it is shorter 597 and so cannot compete for light, and its low R* for N does not help because B can fix N. Does this 598 work? Probably. In all three cases, not all pairs are interfering using the same resource/factor. Could we 599 envisage a 3-species solution using competition for light (‘4’)? How can there be heights of A>B, B>C 600 and C>A? Differential plasticity allows such magic: in this case probably by red:far-red effects (chap. 2, 601 sect. 2.6). However, we are again introducing a second factor: light spectrum in addition to light 602 intensity. All this is rather convoluted, which suggests that intransitivity will not be the norm. 603 The evidence is that circular interference networks are uncommon. They have not been observed 604 in plants. In retrospect we should have expected that, because we had not thought what mechanisms 605 would cause them, and such mechanisms are difficult to envisage. This is almost certainly not an 606 important mechanism of coexistence. J.B. Wilson & Agnew, chapter 4, Species coexistence, page 21 of 30 607 5 Allogenic Disturbance (disrupting growth, mainly mechanically) 608 Disturbance can have the same effect as climate variation (Roxburgh et al. 2004), but the true 609 Intermediate-timescale disturbance mechanism is a patch mechanism: within an area there are patches 610 of different time since disturbance, with different suites of species (J.B. Wilson 1994a). This gives a 611 successional mosaic. Whether this comprises coexistence depends on the scale at which the system is 612 viewed. Coexistence is seen only when considering a scale that is larger than the size of a disturbance 613 patch, so that it includes patches of differing time since disturbance – newly-disturbed versus recovered. 614 The different patch types are different beta niches, but on a small scale, and a species specialising in a 615 particular patch type will increase when rare because it will have more of its specific resources 616 available. In a sense, Allogenic Disturbance should not be counted as a mechanism of coexistence; we 617 do so here because it is so frequently seen as one, because of the impossibility of defining the target 618 scale, and because disturbances occur on all scales so that however small a scale we examine there will 619 still be disturbances within it. The disturbance does need to be sufficiently frequent that each patch will 620 usually include patches at various stages of recovery, or the mechanism will not operate. 621 All types of allogenic disturbances happen and it is not always easy to separate disturbance from 622 climatic stress, i.e. the environmental fluctuation discussed above (section 2). The characteristics of 623 disturbance are: (1) Plants not only fail to reproduce but are killed, at least above ground. (2) Most 624 species are killed, not just those that cannot tolerate a particular stress. (3) The event is sudden. (4) The 625 environmental effect is temporary, i.e. it is a pulse perturbation, so the original species can re-establish 626 the composition of the patch. However, the real difference is that Allogenic Disturbance is a between- 627 patch mechanism. Disturbance is common, creating gaps over the landscape at a range of scales from 628 meteor hits (many km2) to worm casts (about 0.03 m). Fossorial rodents, ants and termites act at scales 629 which can be important for individual plants. A good example is that of McGinley et al.’s (1994) 630 description of enriched harvester ant mounds in western Texas. It is possible that much of the variation 631 seen in communities is due to old disturbances, where vegetation cover has been regained, and obvious 632 pioneers have been eliminated, but differences in species composition remain. Perhaps we do not realise 633 this because ecologists fail to recognise mid-succession species as being such (Veblen and Stewart 634 1982). 635 The Allogenic Disturbance mechanism assumes that there are distinct pioneer and climax 636 species, i.e. r and K, R and C-S. However, we are talking of secondary succession, and cannot assume 637 this. Peterson and Pickett (1995) found that after windthrow disturbance in a North American conifer / 638 deciduous forest some species regenerated by the germination of seed and some from already-present 639 seedlings, but pioneer shade-intolerant species were sparse, apparently due to a lack of propagule input. 640 Autosuccession, in which the climax species immediately re-establishes after a disturbance, is known 641 from mesic areas such as after windthrow in temperate Nothofagus rainforest in New Zealand J.B. Wilson & Agnew, chapter 4, Species coexistence, page 22 of 30 642 (Cockayne 1926), but it is specially found under environmental stress, as predicted by C-S-R theory 643 (chap. 6, sect. 6.7 below; J.B. Wilson and Lee 2000). We might expect that the greater species richness 644 in tropical rain forests would include a good number of gap specialists. Indeed, Hubbell (2005) 645 demonstrated for Barro Colorado Island tropical rainforest a close negative correlation among species 646 between survival rate in shade and growth rate in full light (in gaps), though admitting there were rather 647 few gap species and their abundance was low. Wright et al. (2003) found that there was a continuous 648 distribution of gap-colonising species and those that avoided gaps in Barro Colorado Island, Panama, 649 but that the majority were rather indiscriminate. Similarly, Lieberman et al. (1995) found that 87 % of 650 the tree species in Costa Rican tropical forest had no significant canopy-gap / matrix specialization. 651 Poorter et al. (2005) found that only one of 47 species in a Liberian tropical rainforest was a shade 652 species for its whole life, and only one a light species for its whole life. It is clear that most species are 653 intermediate in this respect. This suggests that Allogenic Disturbance may not be an important 654 mechanism of coexistence in the very biome where we tend to envisage it. Yet in temperate forests there 655 may be greater opportunities for it to increase species richness: Poulson and Platt (1996) demonstrated 656 in Michigan that the size of the gap affects the species re-establishing, such that single treefalls favoured 657 Fagus grandifolia (American beech) but multiple fall gaps favoured Acer saccarum (sugar maple). This 658 is not a question of gap versus non-gap, but also of differences between different sorts of gap. 659 Gaps are by no means restricted to forests. Grubb (1982) suggested that in roadside communities 660 around Cambridge, England, the climax dominant amongst the grasses was Arrhenatherum elatius (oat 661 grass), but Dactylis glomerata (cocksfoot) and Plantago lanceolata (ribwort plantain) retained their 662 place in the community by being the first to invade small gaps. 663 6 Interference/dispersal Tradeoff 664 This concept originated simultaneously with Skellam (1951) and Hutchinson (1951). It has been 665 known under a variety of names (J.B. Wilson 1990), including ‘Life History Differences’ and the 666 endearing if not entirely accurate ‘Musical Chairs’ (Crawley 1986). Consider a model in which two 667 annual species occupy single-plant safe sites. Species C is the better competitor, and eliminates the 668 weaker competitor D if it reaches a site, but it has less efficient reproduction/dispersal than species D 669 and therefore fails to reach some sites. Species D has better dispersal and is therefore available to 670 colonise most of the sites that C has not reached. If C becomes sparse, there are many empty sites for its 671 offspring to occupy and its population growth rate increases; similarly if D becomes sparse, there are 672 many sites left over by C for it to occupy. This is increase-when-rare. The mechanism can be 673 distinguished from (‘1’) Niche differentiation in that no differences between species in resource use are 674 required. It can be distinguished from (‘5’) Allogenic Disturbance in that: (a) the gaps are caused by 675 monocarpic or seasonal death, not necessarily by external disturbance, though that is possible, and (b) 676 species C is limited only by dispersal, not by its ability to tolerate the environment of the gap. It can be J.B. Wilson & Agnew, chapter 4, Species coexistence, page 23 of 30 677 distinguished from (‘9’) Equal Chance in that, though there is a random element, it acts via dispersal; 678 the interference abilities of the two species are very different. 679 There have been many mathematical models of the mechanism, e.g. Levins and Culver (1971), 680 Nee and May (1992) and Tilman (1994). There is an assumption of a negative correlation, due to a 681 trade-off, between interference ability and dispersal ability, but Ehrlén and van Groenendael (1998) 682 surveyed the literature and found that this was common. Turnbull et al. (1999) demonstrated the 683 mechanism experimentally by sowing seven species from a limestone grassland, ranging from a seed 684 mass of 0.013 to 0.16, back into that grassland. When the seeds were sown at a high density, 83 % of the 685 resulting plants were from the three species with the largest seeds, but when a low density was sown this 686 percentage was reduced to 49 %. This is entirely compatible with the Interference/dispersal Tradeoff 687 mechanism: when there were enough seeds to reach almost all microsites the three big-seeded, strong 688 competitors occupied them, but when fewer seeds were sown there were microsites not occupied by the 689 big three, which the light seeded, probably well-dispersed species could occupy. The unlikely 690 Interference/dispersal Tradeoff theory is proved. 691 7 Initial Patch Composition 692 The coexistence model of Levin (1974) is that two species occupy small, transient patches. Some 693 patches will by chance have more individuals of one species than the other. The species in the majority 694 will suppress the other in that patch if intra-specific interference is less than inter-specific interference. 695 The latter condition is beloved of ecological modellers, but it seems unlikely in the real world. It would 696 be possible with mutual species-specific allelopathy: the Getafix potions of community ecology. We do 697 not believe this model can apply to plants (or at all). 698 8 Cyclic Succession: movement of community phases 699 This topic was covered in chapter 3, section 4. The increase-when-rare mechanism is similar to 700 that of (‘4’) Circular Interference Networks. The latter are between individual species whereas cyclic 701 succession involves the whole community, though in many of Watt’s (1947) examples the community 702 comprises one species. Cyclic succession involves reaction, but then interference also involves 703 environmental modification, be it more temporary. There could be cyclic succession between just two 704 phases, whereas there cannot logically be a circular interference network with fewer than three species. 705 Autoallelopathy, for example, would satisfy our criterion for increase-when-rare because a 706 species that is sparse finds less of its self-toxin in the soil, but there must be some kind of reaction 707 involved, giving abundance-dependence. A mosaic arises because a phase of the cycle that is replaced at 708 one point appears elsewhere; we therefore count it as a mechanism that uses movement to escape 709 exclusion by interference. This also means that the mechanism is scale-dependent: the scale examined 710 has to be one that includes patches of the mosaic in different phases. J.B. Wilson & Agnew, chapter 4, Species coexistence, page 24 of 30 711 712 9 Equal Chance: neutrality It is a longstanding idea that there is an element of chance in which species occurs at a spot 713 (Lippmaa 1939). This has been especially invoked for tropical rain forests (e.g. Schulz 1960; Hubbell 714 and Foster 1986). Sale (1977) described it as a ‘lottery’ and Connell (1978) formally put it forward as a 715 mechanism of coexistence, the ‘Equal Chance’ mechanism. In this section, when we speak of chance, 716 we refer to processes such as dispersal that are so complex as to be unpredictable in practice, combined 717 with equally unpredictable climatic and catastrophic disturbance events. It is impossible to prove the 718 operation of chance, but some have implicated it. 719 Equal Chance means that any one of a number of species is equally likely to occupy and 720 pre-empt by reaction a particular microsite. One cause would be that the probability of a disseminule 721 reaching a site is proportional to its abundance. Then, dispersal would determine which species occupies 722 a particular site (Schulz 1960). In New Zealand, Veblen and Stewart (1980) used this as an explanation 723 for the colonisation of canopy gaps by either Dacrydium cupressinum (rimu), Weinmannia racemosa 724 (kamahi) or Metrosideros umbellata (southern rata) as a function of seed/seedling availability, mast 725 seeding and the ability of many New Zealand tree species to remain as suppressed seedlings. Equal 726 interference abilities are likely to be invoked: the ‘Equivalence of Competitors’ concept of Goldberg 727 and Werner (1983) that often interference is intense, but many species are similar in their interference 728 ability. Sometimes the outcome of interference can be established at the seedling stage, since when 729 competition is for light and therefore cumulative, the first plant to establish will exclude others, a type 730 of inertia (chap. 2, sect. 2.3). This again invokes random dispersal. Alternatively, both the probabilities 731 of ecesis and their interference abilities might be different between species, but the two balance. 732 The Equal Chance concept would result in variation in the species composition of communities 733 which it was impossible to correlate with any environmental factor, present or past. Some have used this 734 kind of negative result as evidence of chance. McCune and Allen (1985) in forests in Montana, USA, 735 R.B. Allen and Peet (1990) in forests in Colorado, USA, and Kazmierczak et al. (1995) in kettle-holes in 736 Poland found only weak correlation between species composition and the environment and invoked 737 chance. In such work, the weak correlation could be because there were important environmental factors 738 that had not been measured, or because some factors measured gave a non-linear response that the 739 analysis could not cope with. The Equal Chance hypothesis, used as an excuse for failing to find 740 vegetation/environment correlations is the last resort of the scoundrel. Lavorel and Lebreton (1992) 741 compared the composition of the vegetation with that of the seed pool in fields from southern France, 742 and took the similarity as evidence of a random draw from the seed pool. This is also doubtful evidence; 743 it could equally well be caused by determinism. 744 745 The most well-known invocation of chance is the Island Biogeography model of MacArthur and Wilson (1963), based on probabilistic immigration and extinction. However, Kelly et al. (1989) and J.B. Wilson & Agnew, chapter 4, Species coexistence, page 25 of 30 746 Tangney et al. (1990) could find little evidence for its operation in Lake Manapouri islands. On islands, 747 a direct test of determinacy v. chance (assuming that incidence functions are not important) is available 748 in a test for nesting. On the other hand, J.B. Wilson (1988d) found plant species nesting among these 749 islands to be significant, but far from complete. His analyses pointed to habitat control rather than 750 chance, at least for native species. J.B. Wilson et al. (1992a) sampled the algal flora of intertidal rock 751 pools, selected for habitat uniformity within a limited area, and analysed as virtual islands. The 752 distribution of species agreed closely with that expected at random, whether examined by the 753 distribution of associations, by nesting, by chequerboarding or by incidence functions. The simplest 754 explanation is that differences in specific composition between the pools are caused by chance, but that 755 is no proof; it is a minimalist default. The best example of chance – no difference between species if one 756 can ever have an example of no difference – is from Munday (2004), who investigated two small 757 congeneric coral-reef fish species, where there was evidence for interference, in field removal 758 experiments, and in lab colonisation. However, in none of these experiments, nor in field distribution, 759 was there any evidence of niche differentiation. 760 Even Equal Chance’s strongest advocates have been equivocal. Hubbell (2005), having 761 emphasised differences in niche between Barro Colorado Island tropical rain forest species, eventually 762 attributed coexistence to dispersal and recruitment limitation. This is in effect a resort to Equal Chance. 763 However, he immediately discussed negative abundance-dependence, which is stabilising, not 764 equalising. The Equal Chance mechanism is the equalising mechanism par excellence, and should be 765 seen as no more than that. 766 10 Inertia 767 Inertia is another type of equalising mechanism, slowing exclusion by interference and possibly 768 allowing stabilising mechanisms to operate. 769 10.1 Temporal Inertia 770 Temporal Inertia (Cowles 1901) can be an individual or population effect, effectively the same 771 because the ‘individual’ concept is not meaningful for plants. Trees stand where they stand and cause 772 inertia. If, when a tree fell over, there were a tendency for the niche it had constructed to favour its own 773 juveniles in the canopy gap created, this would represent a small-scale dispersal switch. This could 774 constitute inertia, slowing the ingress of a superior competitor. We mentioned above that Dalling et al. 775 (1998) found seedlings on Barro Colorado Island to be denser near to a conspecific adult. Species 776 differed little in the correlation of their growth rate with light intensity and they declared that differential 777 responses to soil and topography were rare. This left them to speculate that there was dispersal 778 limitation, as supported by the correlation between parent and juvenile being weaker for species with 779 small disseminules. This is inertia due to dispersal limitation. Annuals are a conspicuous life form in 780 arid climates where the rainfall is highly erratic and form a long-lived seed bank. This seed bank gives J.B. Wilson & Agnew, chapter 4, Species coexistence, page 26 of 30 781 inertia as well as a storage effect. A population with a seed bank has similarities to a tree, except that 782 this is multi-generation inertia. The decade-long dominance phases, with smooth increases and 783 decreases, that Watt (1981) found in the Breckland may owe something to inertia. A more active 784 mechanism of inertia would be delay in vegetation change caused by a switch (chap. 3, sect. 5.3). Inertia 785 caused by the length of life of trees must be common. Abrams and Scott (1989) describe a situation 786 where, until disturbance occurs, early-successional trees dominate the canopy with young plants of later 787 successional stages beneath them, and their model diagram shows the high species richness resulting at 788 this stage. 789 These situations are obvious in dryland vegetation where the rainfall is erratic and temperatures 790 are high. For many succulents, sufficient rainfall for the development of surface root hairs is itself a rare 791 event, yet by means of massive storage, CAM photosynthesis and often a high albedo, they can 792 withstand years of unavailable moisture. The establishment of such succulents can be a very rare event, 793 as exemplified by Agave macroacantha in Mexico (Arizaga and Ezcurra 2002). Minor rain events may 794 allow annuals to grow, while deep-rooted shrubs and trees maintain contact with a deep water resource 795 giving the appearance of a plant community. Clarke (2002) described a similar situation with woody 796 dryland vegetation in southwestern Australia, where no natural recruitment of shrubs was observed over 797 five years. However, the rare event required to cause the state change could be a different grazing 798 regime, as Prins and van der Jeugd (1993) found in Tanzania. Two pandemics in the herbivores in 1880 799 (rinderpest) and 1961 (anthrax) temporarily reduced browsing and allowed even-aged stands of Acacia 800 tortilis (umbrella thorn) to establish. These are now a conspicuous and apparently integral part of the 801 vegetation of national parks in the area, yet are present through inertia, not as maintained populations. 802 Here, the state change was anthropogenic, but a similar situation could occur naturally. Inertia may not 803 apply to all the species in a community, since many contain species that differ markedly in survival and 804 establishment probabilities. Extremely long-lived individuals of slow growth exist alongside perennials 805 with lifespans shorter by at least one order of magnitude. The long-lived individuals can establish only 806 during a rare event, which could be a disturbance such as flood, a 1/100 yr wet season. The probability 807 of such an event occurring in any one year is very low and does not change from year to year. Thus their 808 occurrence is stochastic yet within the time scale of very long-lived plants. 809 We still ask what the original coexistence was due to: if there is no coexistence, inertia cannot 810 prolong it. 811 10.2 Spatial Inertia: aggregation 812 Spatial aggregation of the plants of a species also gives inertia, delaying exclusion by 813 interference since it occurs only at patch boundaries. Presumably the aggregation was established due to 814 dispersal processes, an ‘ecological founder effect’. Stoll and Prati (2001) demonstrated beautifully the 815 slowing of exclusion by interference by experimental aggregation. Amongst four annuals they found J.B. Wilson & Agnew, chapter 4, Species coexistence, page 27 of 30 816 that the species with least interference ability (Cardamine hirsuta, bitter-cress) decreased over the 817 experiment to 6 % of the monoculture in a random arrangement but only to 26 % in an aggregated 818 arrangement. The species with lowest interference ability (Stellaria media, chickweed) increased its 819 biomass to 324 % of the monoculture in the random but to only 239 % in the aggregated1. This would 820 be a most potent mechanism for delaying exclusion by interference of a subservient species. Rebele 821 (2000) found a similar, but very slight, effect in an outdoor mesocosm experiment using mixtures of 822 Calamagrostis epigejos (reed) and Solidago canadensis (goldenrod). 823 Thórhallsdóttir (1990) had planted outdoors a hexagonal grid of adjacent plots. Each plot 824 contained one of five meadow species: Agrostis stolonifera (creeping bent), Holcus lanatus (Yorkshire 825 fog), Cynosurus cristatus, Poa trivialis (meadow grass), Lolium perenne (ryegrass) and Trifolium 826 repens (white clover). Silvertown et al. (1992) ran simulations to see in retrospect what effect 827 aggregation would have, given the invasion rates that Thórhallsdóttir found between the pairs of grass 828 species. After 50 time periods when the species were intermixed in a random pattern, the weakest 829 competitor Lolium perenne had almost disappeared (reduced from 20 % to 1 %), but with the species 830 ‘planted’ in bands, depending on the order of the species in the bands, it decreased only to 9 %, stayed 831 at 20 % or even increased slightly to 21 %. 832 Aggregation might also delay exclusion by interference via effects on herbivory (Parmesan 833 2000), fire spread (Hochberg et al. 1994) and other environmental factors. 834 11 Coevolution of Similar Interference Ability 835 Aarssen (1983) suggested that in a mixture of two species stronger selection pressure on the one 836 with lower interference ability would cause it to become the stronger competitor of the two, “Superiority 837 in competition therefore alternates between … members of the two populations”. He later (1989) 838 produced some evidenced for this: over two generations the interference ability of Senecio vulgaris 839 (groundsel) increased relative to a standard genotype of Phleum pratense (Timothy grass) with which it 840 was growing. Selection can result in small-scale genetic change in populations, as apparently occurred 841 in Trifolium repens (white clover) associated with different ecotypes of Lolium perenne (ryegrass) in the 842 pastures that Lüscher et al. (1992) investigated. However, neither this study nor that of McNeilly and 843 Roose (1996) could find evidence of co-adaptation between neighbouring ecotypes of associated L. 844 perenne. Eventual ecotypic evolution in response to neighbours would be expected, and has 845 occasionally been demonstrated (Martin and Harding 1981). However, Aarssen’s proposal is 846 unbelievable because it involves continual increases in interference ability, as Aarssen (1985) has since 847 concluded. The plastic response to interference (chap. 2, sect. 2.2) can also give a buffering effect. J.B. Wilson & Agnew, chapter 4, Species coexistence, page 28 of 30 848 849 12 Spatial Mass Effect (vicinism) The Spatial Mass Effect refers to the maintenance of a population of a species by constant 850 immigration into a patch where the species cannot otherwise maintain itself (Zonneveld 1995). It has 851 been called the sink effect. The immigration could be by seeds, or in theory by rhizomes or stolons. 852 Populus tremuloides and related species (aspen) produce root suckers (Barnes 1966) and these can 853 appear beyond the canopy of the tree where there is no chance that they will survive to be self- 854 supporting, let alone sexually reproductive, for example in a lawn. Seed immigration is the most 855 common but difficult to demonstrate. It is difficult enough to monitor occasional seeds blowing in, and 856 even more difficult to demonstrate that the population into which they are blowing would have RGR < 857 0.0 without that subsidy. Snyder and Chesson (2004) have applied the concepts of the ‘storage effect’ 858 and non-linear dynamics to coexistence between species that have different tradeoffs of interference 859 versus fecundity+dispersal. Their model has Spatial Mass Effect, though also elements of (‘6’) 860 Interference/dispersal Tradeoff. The effect clearly maintains populations that are not susceptible to 861 considerations of abundance-dependence or increase when rare, the stabilising mechanisms we require 862 here, yet it can maintain coexistence indefinitely. 863 The Spatial Mass Effect has rarely been quantified. Kunin (1998) examined boundaries between 864 plots with different fertiliser treatment in the 150-year old Park Grass Experiment. There was a very 865 sharp pH change, within 50 cm of the boundary. Although there were many exceptions, the majority of 866 plots examined (34 out of 51 non-zero, 2-tailed p = 0.024) showed higher species richness towards the 867 boundary. The effect was seen especially where the two adjacent plots differed more in species 868 composition. The Spatial Mass Effect can be seen clearly in extreme cases where the recipient (sink) 869 population does not reproduce at all, like the 13 species of angiosperm that grow in the Lost World 870 Cavern, northern North Island, NZ, without any of them ever setting seed (de Lange and Stockley 871 1987). Studying an Argentinian steppe with the (palatable) grass Bromus pictus amongst tussocks of 872 unpalatable grasses Stipa spp. and Poa ligularis, Oesterheld and Oyarzábal (2004) found more B. pictus 873 in the upwind part of a grazing exclosure, showing that a seed subsidy was arriving from the grazed 874 area. The tussocks outcompeted the B. pictus when ungrazed, reducing the local seed output in the 875 exclosure. This situation may be the commonest way in which the spatial mass effect operates to 876 maintain species metapopulations. 877 13 Conclusion 878 We believe our review covers all the mechanisms by which species can coexist in stable 879 mixtures. Chesson’s terminology of stabilising versus equalising mechanisms is useful and important. It 880 has focussed attention on the fact that some proposed mechanisms of ‘coexistence’ do not, in fact, cause 881 long-term coexistence. It has also highlighted what few had recognised, that even though the equalising J.B. Wilson & Agnew, chapter 4, Species coexistence, page 29 of 30 882 mechanisms cannot on their own cause stable coexistence between two species, they can reduce the 883 difference in interference ability between species to the extent that a stabilising mechanism can operate. 884 We must speculate on the importance of each mechanism in order to build up in our minds a 885 vision of the plant community. The overwhelming reason for species coexistence is Alpha-niche 886 Differentiation. Environmental Fluctuation is probably important. It can be seen as niche differentiation 887 in time, but with special restrictions on when it can operate. In seasonal climates, local environment can 888 vary enormously, both stochastically and predictably. Each of the ecosystem attributes enumerated by 889 Reichle et al. (1975; see also chap. 1, sect. 1 above) must change during the year: the energy base 890 (affected by irradiance), the reservoir of energy, nutrient cycling (through mineralisation rates) and rate 891 regulation (temperature, water availability, herbivory). It seems that the available states of these 892 variates, factorially combined, should allow for the coexistence of a very large number of plant species. 893 Pest Pressure may be important; Gillett (1962) suggested that it is the major mechanism, but that 894 remains to be proved. The Spatial Mass Effect must be very common. Disturbance is clearly common, 895 and has potential to allow co-existence; surely all communities are successional mosaics. We earlier 896 discussed autogenic disturbance. It could have been listed as a separate mechanism here, it could have 897 been merged with Allogenic Disturbance since many disturbances are partly allogenic and partly 898 autogenic, or it could have been included with Cyclic Succession since it will often be a component. 899 Other mechanisms are probably of more minor importance. For example, circular interference 900 networks are an attractive idea, but remain undiscovered. Cyclic succession is more believable and from 901 time to time fashionable, but seldom observed and even more rarely proven to take place. 902 Autoallelopathy may be widespread but the soil is an intractable and infinitely complex medium where 903 clear chemical pathways and effects are difficult to prove. 904 905 Based on the evidence derived from the present literature, we list the mechanisms below in increasing order of importance: 906 Initial Patch Composition (7) 907 Co-Evolution of Similar Interference Ability (11) 908 Equal Chance (9) 909 Circular Interference Networks (4) 910 Cyclic Succession (8) 911 Temporal and Spatial Inertia (10) 912 Interference/Dispersal Tradeoffs (6) 913 Allogenic Disturbance (5) 914 Spatial Mass Effect (12) 915 Pest Pressure (3) 916 Environmental Fluctuation (2) J.B. Wilson & Agnew, chapter 4, Species coexistence, page 30 of 30 917 Alpha-niche Differentiation (1) 918 In a changing, disturbed world it will be increasingly difficult to separate stabilising mechanisms from 919 equalising ones. The temporal turnover of species in communities depends on some species 920 disappearing, others invading, so that many species in a community may be present by courtesy of one 921 of the equalising mechanisms and will ultimately be doomed. The multiplicity of possibilities for 922 coexistence should allow the coexistence of a very large number of plant species. The question then 923 becomes: “Why are there so few species in most habitats?”. 924 A plant, however, is sedentary and extends over a spatial volume, necessarily exposed to wide 925 range of environmental conditions. It therefore cannot be confined to a precisely-defined niche. It is the 926 interplay between the potential for high plant diversity in restricted niches and the necessity for plants to 927 tolerate a wide range of environments that encourages us to look for patterns in plant communities. If 928 adaptations to available niches were most of the reason for every species’ occurrence, our enquiry in 929 this book would be less interesting. 930 Footnotes 931 1 932 ‘sparse’ would be a better term than ‘rare’, but ‘increase when rare’ is ensconced in the literature, and so we use it here. 933 TABLES, ILLUSTRATIONS and PLATES 934 Table 4.1: Some Examples of monospecific stands. We exclude monospecificity in a single stratum or 935 936 guild of vegetation, such as a tree species or understorey species. Table 4.2: Which species has the higher interference ability? The starting biomass for both species was 937 1.00 938 Table 4.3: Competitive hierarchy from Mouquet et al. (2004), strong competitors at the top 939 Table 4.4: Competitive hierarchy of four species in four treatments in Silvertown et al. (1994). 940 Fig. 4.1: The MacArthur and Levins (1967) concept of niche separation along a gradient. 941 Fig. 4.2: Pairs of two species showing relative non-linearity. 942 Fig. 4.3: The effect of interference intensity and environmental favourability on RGR. 943 Fig. 4.4: A circular interference network between three species. 944 Fig. 4.5: Competitive relations in seven species from the University of Otago Botany Lawn. From 945 Roxburgh and Wilson (2000a). 946 Fig. 4.6. The competitive hierarchy from invasion rates in data of Silvertown et al. (1992). 947 Fig. 4.7. Possible causes of intransitivity between three species: A, B and C. 948 Plate 4.1: A monospecific community: Cladium mariscus stand. 949 Plate 4.2: Tyria jacobaeae (cinnabar moth) on Senecio jacobaea (ragwort) 1 all this is in the high-density treatment