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The Balance between Positive and Negative Plant Interactions and Its Relationship to Environmental Gradients: A Model Author(s): Rob W. Brooker and Terry V. Callaghan Reviewed work(s): Source: Oikos, Vol. 81, No. 1 (Feb., 1998), pp. 196-207 Published by: Blackwell Publishing on behalf of Nordic Society Oikos Stable URL: http://www.jstor.org/stable/3546481 . Accessed: 18/05/2012 11:35
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FORUM FORUM FORUM

FORUM is intendedfor new ideas or new ways of interpreting existinginformation.It provides a chance for suggestinghypotheses and for challengingcurrent thinking on ecologicalissues. A lighter prose, designedto attract readers,will be permitted.Formal should be concise research reports,albeit short, will not be accepted,and all contributions with a relativelyshort list of references. summary not required. A is

The balance betweenpositive and negativeplant interactionsand its gradients:a model relationshipto environmental
Rob W. Brooker and Terry V. Callaghan, Sheffield Centrefor Arctic Ecology, Dept of Animal and Plant Sciences, Univ. of Sheffield, 26 Taptonville Road, Sheffield, UK S10 5BR (bop95rwb@sheffield.ac.uk).

ongoing and apparently insoluble debates surrounding certain aspects of competition, and its relationship to productivity and diversity, have made researchers more willing to examine what may originally have seemed unorthodox hypotheses. However, regardless of the emergence of new evidence to support the call for increased recognition of positive plant interactions within ecology, "the general importance of positive of interactions betweenmembers a plant commu- interactions to community diversity, structure and procompetitive) It nity, and the severity of the external environment. also ductivity is rarely acknowledged" (Bertness and provides an explanation for the past and current neglect of and they "are largely ignored in curpositive plant interactions, and for the conflicting results from Callaway 1995), suchphe- rent models of natural community organisation" (Bertplantcommunity manipulation experiments examining nomena.Potentialdirectionsfor futureresearchinto positive ness and Hacker 1994). are plantinteractions proposed. In this article we discuss certain unifying aspects of the evidence produced for the occurrence of positive plant interactions. Secondly we suggest a novel link between positive plant interactions and existing ecologiThe existence and importance of positive and beneficial cal theory. Finally we suggest potential directions for interactions within certain plant communities have re- research into positive interactions within plant commucently been highlighted by a number of authors nities. (Callaghan and Emanuelsson 1985, Fowler 1986, Before proceeding it is necessary to set limitations Hunter and Aarssen 1988, Bertness and Hacker 1994, upon the scope of this article. "Positive plant interacBertness and Callaway 1995). They state that this sub- tions" as it is used here, relates (unless otherwise stated) ject, a basic tenet of plant ecological theory during its only to those interactions occurring between physiologinitial development at the start of this century, has ically separate unitary plants. They can be either intersuffered neglect during the last 20 to 30 years. Recently or intraspecific interactions and in all cases at least one the study of ecological interactions between plants has of the interacting individuals benefits, this benefit being been dominated by competition, a bias which possibly reflected in an increase in a recognised measure of plant stems in part from the concentration of ecological performance, for example biomass or reproductive outresearch in competition-rich temperate ecosystems put. The other individual either remains unaltered by, within easy reach of most experimenters (Callaghan or benefits from, the interaction. The interaction can be and Emanuelsson 1985, Bertness and Callaway 1995), defined as either a mutualism (the interaction being coupled with strong arguments concerning the primacy obligatory) or a commensalism (the interaction being of competition as a driving force in ecological processes beneficial to one individual, the other remaining unaf(e.g. Connell and Slatyer 1977). fected) (sensu Odum 1968). A number of positive interDespite this apparent neglect, positive plant interac- actions between plants can occur through physiological tions are again starting to be addressed with the same connections, for example via the connections between quantitative approach that competition has already the ramets of clonal plants, root grafts between trees or been afforded (Aarssen and Epp 1990). Perhaps the mycorrhizal connections between grassland species
Positive, beneficial interactions between individuals within plant communitieshave been observedin nature and recordedin a wide variety of ecological experiments. However, the existence of such interactions has been, and continues to be, largely ignored by most ecological researchers. We present here a new model that combines current ecological theory on plant competition, and its relationshipto environmentalseverity, with evidence from a range of studies that show positive plant interactions in the field. The model describes a hypothetical relationship between the intensity of positive (e.g. mutualistic) and negative (e.g.

196

OIKOS 81:1 (1998)

0 0

Table 1. Evidence for positive interactions taken from ecological literature. The table shows the author(s) of the work, the environm disturbance variable impacting upon plants within those environments, the species involved in the positive plant interaction i.e. spe density-dependent survival these can be the same species), and the form and mechanism of their positive interaction. Authors Bertness and Hacker (1994) Environment High salt marsh intertidal zone Stress/disturbance variable High soil salinity due to evaporative salt concentration High soil salinity due to evaporative salt concentration Extreme cold, and nutrient impoverished soil Species 1 Juncus gerardi Species 2 Iva frutescens (marsh . I I elder)

Bertness and Shumway (1993)

Low salt marsh intertidal zone

Spartina patens

Juncus gerardi

Carlsson and Callaghan (1991)

Arctic mountain fellfield

Cassiope tetragona and Empetrum hermaphroditum

Carex bigelowii

Fowler (1986)

Arid desert

Extremes of temperature, low water supply and grazing Low soil nutrient and moisture availability

Desert shrubs Carnegia gigantea (species unspecified) (sagauro cactus)

Grindey (1975)

Limestone scree

Bryophyte species (unspecified)

Hieracium pilosella

Heilbronn and Walton (1984)

Subantarctic fellfield scree slopes

Frost-heaving scree slope movement

Phleum alpinum

Deschampsia antarctica, Festuca contracta and Acaena tenera Vaccinium myrtilus

Jonasson (1992)

Arctic shrub tundra

Low temperatures and limited soil nutrient availability Herbivory, disease, low temperatures, and low soil nutrient availability

Betula nana

Mailette (1988)

Arctic shrub tundra

Vaccinium uliginosum, V. angustifolium and V. myrtilloides

Vacccinium uliginosum V. angustifolium and V. myrtilloides

Okland and 0kland (1996)

Arctic boreal spruce forest understorey

Low light and water availability

Hylocomium splendens

Hylocomium splendens

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and Aarssen 1988). Although these interactions are not the primary focus of this article, their occurrence should be acknowledged.

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Evidence and mechanisms

The formulation of widely applicable rules of ecology depends upon the existence and observation of widespread reoccurring patterns within ecosystems and ecological interactions. We have tried to identify such patterns from some of the recent evidence demonstrating the occurrence of positive plant interactions (Table 1). There appear to be two common features linking these studies.

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1) The interacting species occur within relatively environments such as polar tundra (Heiland Walton 1984, Carlsson and Callaghan v E ? ,, 1991, Shevtsova et al. 1995), saline marshes (Bertand Shumway 1993, Bertness and Hacker c~.s~ ~ness <,~-^ Bertness and Callaway 1995) or arid desert i1994, |4t ~ 1-b4"~ F?^ ~ c?;q~ (Fowler 1986). >ecosystems ^~ 2) The environmental factor constraining plant growth or survival is one that can be alleviated by ~ the physical presence of another plant. The posiP,, tive interaction does not occur through the ex? ' i E e .1 change of resources but through an amelioration the conditions of the external environment ~*_?~t ^,3tof and Aarsson 1988). As a result of this the >(Hunter og^ ~ gQ~a~ -?~ strength of the interaction is often density depen3 dent (Callaghan and Emanuelsson 1985), for ex'o O ,-o ample increased plant density can lead to cl et ct >, ct increased litter accumulation (Wilson and Keddy f <l 1986), improved water status (Okland and 0kland |t ^e e' .E 1996), increased soil stability (Heilbronn and Wal8<' ton 1984) or decreased evaporative water loss . 5 |) and Hacker 1994). They are therefore c^ ;(Bertness O~ sol^~ eg~E o . ., not dependent upon physical connections between . ~ m ,; = the interacting individuals, but rather act through feedbacks on the external environment. The influence of this second factor may be important in why positive interactions are not ct~~^~~~=~understanding in all plant-plant interactions in severe Xr^~~ eg~~~~ |evident + environments, i.e. in some situations the con:< Ocl ES straining factor is not one that can be alleviated yle< * *through the physical presence of another plant. 0|? ||
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Environmental severity is taken here as being a combination of both stress and disturbance (sensu Grime 1979). Stress includes those phenomena restricting phoproduction, for example limited supply of resources such as light, water and soil nutrients, but can also include environmental factors such as extremes of temperature that can directly limit photosynthesis. Disphenomena, for example grazing or soil erosion, cause partial or total destruction of the plant biomass. The occurrence of stress is often a continuous process whereas disturbance is mainly episodic.
OIKOS 81:1 (1998)

198

Sincemuch of the evidencefor positiveplant interactions (Table 1) comes from extremeenvironments, does this mean that as communityorganising processesthey do not occurin less stressful,more productive environments?This is unlikely;we can easily conceivethat in any ecosystemtherewill be situationswherethe physical presenceof one plant will be beneficialto another plant within its vicinity. For example,increasedstand densitymay provideprotectionagainstwind damagein (Foster 1988)or leguminous forestryplantations species may cause nitrogen enrichmentof soils (Barnes and Archer1996),leadingto increased foliage densitiesand decreasingevaporativewater loss from the soil. Why not then are positive interactions commonlyobserved? We propose that experimentsundertaken in less severeenvironments have found little evidenceof positive plant interactionsbecause,although such interactions occur, they are masked by the relativelygreater impact of competitionfor resourceswithin such environments.In addition there appears to be an active relationshipbetweenthe severityof the externalenvironment and the overall direction, either positive (beneficial)or negative (detrimental),of plant-plant interactions. We have definedenvironmental severityas a combination of both stress and disturbance. Although there seems to be a consensus concerningthe relationship betweenthe level of competitionand disturbance, that betweencompetition stressis still contentious(Tayand lor et al. 1990). The aim of this paper is not to this summarise debate or attemptto find a solution to it. Therefore the followingdiscussionwe will primarin ily examine the relationshipsbetween positive and and gradientsof disnegativeplant-plant interactions turbance.Once we have outlinedour model using disturbanceas our independent environmental factor, we shall brieflyexaminethe relationship betweencompetiand stress. tion (and positiveinteractions)

and Positive and negativeinteractions, of disturbance gradients

When examining the relationshipof competition or positive interactionsto any factor such as stress or disturbance, possibleconfusionmay ensueas a resultof not specifyingwhetherone is dealingwith the intensity or importanceof competition (Welden and Slauson
1986). Competition intensity is the absolute degree of

reductionof a plant's success via the presenceof its

neighbour. Competition importance is "the relative de-

gree to which competitioncontributesto the overall decrease in growth rate, metabolism,fecundity, survival or fitness of that organism below its optimal of condition".The intensityand the importance competition "need not be correlated"(Weldenand Slauson 1986).
OIKOS 81:1 (1998)

Competitionintensitywill affect growth parameters such as biomass. However, the only measure of the of is importance competition its impactupon the fitness of a plant,whichwill be measurable its reproductive as when we discussthe outcomeof the Therefore, output. interactionbetween two individualsand the relative in importanceof competitionand positive interactions causing that outcome, we would measureit as some function of the fitness and reproductive output of the individuals. As mentioned,there currentlyappearsto be a consensus in plant ecology that with increasinglevels of disturbance both the intensityand importance comof petition as a communitystructuring processand selective force are reduced(Taylor et al. 1990). Evidence from experimentation (Table 1) suggests that, just as the importanceand intensity of competitionseem to decreasewith increased so disturbance, positiveinteractions seemto becomemoreimportant intense.Why and should this relationshipoccur? A number of factors may interactto producethis relationship: 1) As stated, the importanceof competitionis reduced by increasedenvironmental severity. within 2) In certainextremeconditionsdisturbance the environment the primaryfactorlimitingthe is growth, development and fitness of vegetation (Porsild 1951, Billings 1978, 1987, Callaghan 1987, Callaghanand Jonasson 1995).Positiveinteractions can act through the ameliorationof disturbance(although it should be pointed out that they might also act throughthe amelioration of stress, Table 1). Thereforethey may have a greaterimpact in harshconditions,since the factor which they alleviate also has an enhanced impact on plant developmentand survival.For example facilitation,a well-knownexample of a positive plant interaction,"appearsto be important only in severeenvironments and primarily ... in the stagesof colonisationand earlycommunity development" and, as the productivity and biomassof the communityincreases,with a concomitant decrease in disturbancelevels through the ameliatoryeffect of the physicalpresenceof plants(e.g. in stabilisingscreeslopes or providing increasedprotectionagainst herbivory)competitive interactions"becomeprogressively more important"(Walkerand Chapin 1987). 3) The results of species interactionsobserved by researchers conductingcommunitymanipulations are the final outcome of a balancebetweenposiand negative (mutualisticor protocooperative) tive (e.g. competitive)interactions. Any plants in close proximity are likely to use the same resources to a certain extent, and may inflict resourcelimitations upon one another(Grime1987) so that, since ameliorationof physical severity seems to depend upon close proximity, "plants
199

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of and betweenthe importance P (positiveplant interactions) N (negativeplant interactions), relationship Fig. 1. Hypothetical disturbance through outcomeof community and the observable (D) (O), to a gradientof decreasing manipulation experiments of surfaces(Figs 2 and 4). All valuesare in arbitrary units, spaceor time (x-axis)used in the production plant-plantinteraction showingthe relativesize of each factor as used in the model (see Appendix1).

that benefit from their neighbors ... are likely also to compete with them" (Hunter and Aarssen 1988). We can combine these points in an attempt to explain the apparent relationship of positive plant interactions, competition and severity of disturbance. The resulting hypothesis holds that under conditions of high disturbance the importance of positive interactions is greatly enhanced. At the same time the importance of competition as a force is greatly diminished due to the relatively greater impact of disturbance on plant survival and reproduction, as outlined above. Since the outcome of any plant-plant interaction is the sum total of the impact of these two opposing forces, the outcome of plant-plant interactions under extremely disturbed environmental conditions is more likely to be a positive relationship. We propose that community manipulation experiments are more likely to reveal positive plant-plant interactions in highly disturbed environments, manifesting as positive density-dependent effects on the fitness of individuals. As disturbance within the environment is reduced, either through time or space, competition becomes more important and in parallel positive interactions become less important, so that competition becomes the dominant selective force in plant-plant interactions. Because we observe only the final outcome of this balance, in temperate ecosystems competition may be the only force apparent within plant communities. Also, because certain abiotic environmental disturbances are episodic, the chance of detecting positive interactions depends to some extent on the duration of observations. 200

A simple model
It is possible to construct an extremely simple model to illustrate this hypothesis. Let us consider the observable outcome of an hypothetical plant community manipulation experiment within a monoculture stand of constant density. Since the observable outcome of any community manipulation is the result of a number of positive and negative interactions we can express it as: O=P+N where O is the observable outcome in terms of the net direction of the interaction, P the importance of positive plant-plant interactions (e.g. mutualism and facilitation) and N the importance of negative plant-plant interactions (e.g. competition or allelopathy). Values of P are given a positive sign, and values of N are given a negative sign, reflecting their opposing actions. P and N, for simplicity, are considered as being directly proportional to the level of disturbance, P being positively correlated with disturbance, and N negatively correlated with disturbance. Let us first examine the relationship between 0, P and N within this monoculture along a gradient of decreasing disturbance (Fig. 1). As proposed by our model, as environmental severity decreases the value of O tends to decrease, the outcome of the relationship between individuals becoming progressively more negative. When O is above the x-axis (i.e. O > 0), the net observable interaction between individuals is positive, and when it is below the x-axis (i.e. 0 < 0) the net
OIKOS 81:1 (1998)

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outcome(O) againstgradients disturbance of Fig. 2. Three-dimensional of observable plot plant-plant interaction throughtime in All (t) and space(s) as illustrated Fig. 1. All areaswhereO > 0 indicatezones of net positiveplant-plant interaction. areas where O < 0 indicatezones of net negativeplant-plant interaction units. (e.g. competition).All values are in arbitrary observable interaction between individuals is a negative one. Levels of disturbance may vary either through time or space. Through time they may vary either cyclically (e.g. in a seasonally variable pattern, as in the case of periglacial soil movement processes in alpine or arctic regions), episodically at random (e.g. as a result of chaotic weather features such as extreme storms), or with a monodirectional trend (e.g. decreasing in intensity during the course of succession). Examples of spatial gradients of disturbance exist in a multitude of situations, for example from the edge to the centre of a scree slope. So the gradient of disturbance severity described above (Fig. 1) could be either a spatial or temporal one (hence the x-axis is defined as distance through either space or time). It is possible that the two types of gradient may interact. For example what may be a beneficially high density of individuals on a moving alpine solifluction lobe during the winter may be the cause of competition for water during a dry summer period. We can combine these gradients of disturbance to show the interactions of space and time in altering the balance of positive and negative interactions within our hypothetical plant community. Now the observable outcome (O) of the interactions within our monoculture stand is expressed as:
OIKOS 81:1 (1998)

o = N,+ P + N,+ P,
where N and P are the importance of negative or positive interactions at a particular point in time (t) or space (s). Using hypothetical data sets (Appendix 1) that illustrate the relative levels of N and P under different levels of disturbance (D) as proposed by the model, this equation will produce plant-plant interaction surfaces, the three axes of each graph being the position in space, the position in time and the observable outcome of the interaction. The position of a point upon this surface relative to the x-axis indicates whether the observable outcome (O) will tend to be a positive or negative interaction. Using this equation we will now examine two hypothetical interactions between patterns of disturbance within space and time. In both examples the relationship of P and N to the gradient of disturbance through space will be that indicated in Fig. 1. Example 1: Successional progression The relationship of P and N to changes in disturbance through time in this example is also that shown in Fig. 1. As disturbance levels decrease with successional progression through time, so the importance of P also decreases, but the importance of N increases (i.e. N

201

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betweenthe importance P (positiveplant interactions) N (negativeplant interactions) of and Fig. 3. Hypothetical relationship to cyclicallyfluctuating levels of disturbance throughtime (x-axis) used in the productionof the plant-plant interaction (D) surfaceshown in Fig. 4. The relationship betweenN, P and D, althoughbased upon the predictions the model, is purely of All illustrative. values are in arbitrary units (see Appendix1 for data set). becomes progressively more negative). The subsequent interaction surface (Fig. 2) indicates the trend from positive to negative interactions through time, a relationship that would perhaps be expected during succession. Once the conditions of the environment are sufficiently ameliorated, for example through the action of facilitatory mechanisms or geological processes such as weathering, then plant-plant interactions tend to become more competitive. The shape of the interaction surface also indicates that in stable environments, even at the initiation of succession, competition may occur. Example 2: Cyclical patterns In this example P and N have a cyclical relationship to disturbance through time (Fig. 3). At either end of the time axis there are high levels of disturbance. This pattern of disturbance could be caused by a seasonally active disturbance factor such as winter-time ice crystal abrasion of exposed plant tissue, or solifluction activity in alpine or arctic environments. In the middle of the time axis the conditions are less severe, as would perhaps be the case during the summer period. The interaction surface (Fig. 4) illustrates the subsequent trend of plant-plant interactions toward competition during the mild period, and the increased importance of positive interactions, perhaps through the provision of shelter and protection from ice-crystal abrasion, during more disturbed periods. In a harsher environment the interactions cycle between positive and negative observable outcomes, whereas in the more clement environ202 ment the interactions are always competitive, although the force of this negative interaction varies. This model, as stated previously, is extremely crude, a number of factors having been excluded from it in the quest for simplicity. For example, it assumes that the relationship of disturbance through space is constant through time, and that the relationships of N and P to disturbance run in parallel. However, this need not necessarily be the case. A more complex relationship of N and P to disturbance in space and time can be introduced by altering the data sets, possibly using data from field experimentation, and will simply produce a more complex interaction surface. One interesting feature of this model is that the observable outcome of a manipulation is variable through time, and the net outcome will be the sum of O for the entire period of a plant's life. Short-term studies of plant-plant interactions may fail to find positive plant interactions either because they are being masked by competitive interactions, or because they are not occurring during the period of the manipulation. This latter explanation may result from the periodic nature of the disturbance factor and the associated periodicity of the positive interactions. For example the benefits of high stand density in forestry plantations are only obvious during occasional short periods of intense wind (Everham and Brokaw 1996). When these factors are combined with the tendency for research to be focused within temperate, easily accessible, productive ecosysOIKOS 81:1 (1998)

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Fig. 4. Three-dimensional of observableplant-plant interactionoutcome(O) againstgradientsof environmental plot severity All throughtime (t) (Fig. 3) and space(s) (Fig. 1). All areas O > 0 indicatezones of net positiveplant-plant interaction. areas units. O < 0 indicatezones of net negativeplant-plant interaction(e.g. competition).All values are in arbitrary tems, the bias toward the study of competition is perhaps not surprising, and could lead to the subsequent neglect of positive interactions as discussed in the introduction. 1) The Taylor et al. hypothesis The first of the two main hypotheses is that put forward by Taylor et al. (1990). They propose that the level of competition within a community is not directly related to the productivity of that community, or the level of stress within the environment. For example, plant species within extremely unproductive, stressful environments will not consistently be subject to lower levels of competition than those in more productive environments. Rather the levels of competition within a particular environment are related to the distance of the actual productivity of that environment from its theoretical maximum carrying capacity, K (MacArthur and Wilson 1967), which is itself a consequence of the intensity and frequency of disturbance events. The closer a community of plants is to its carrying capacity, the more intense the competition for a given level of limiting resource, irrespective of the level of stress within that environment. From this model one can predict that in stressed environments, competition between individuals can be as intense as in more productive environments and possibly "the main organising force in the scanty vegetation" (Oksanen 1982). 2) The Grime et al. hypothesis The opposing view is that put forward by Grime and co-workers (Grime 1974, 1977, 1979, 1987). It states 203

Competition and stress

Although we have so far limited our discussion to an examination of the impact of disturbance on the balance between positive and negative interactions, it is important to consider at some point the effect of stress. From experimental evidence (Table 1) we can see that positive plant interactions can occur through the amelioration of factors that are classified as stress variables, for example water or nutrient shortage. In addition stress, when combined with disturbance (often as "environmental severity"), can have severe impacts on plant growth, development and reproduction (Walker and Chapin 1987). The inclusion of a stress variable in this model, or indeed any variable influencing the importance of competition or positive plant interactions, presents no problems. However, there is some debate as to the exact nature of the relationship between the level of stress and the intensity and importance of competition. The opposing opinions of two of the debate's main protagonists are outlined below.
OIKOS 81:1 (1998)

that the relative importance of competition as a community structuring process is inversely proportional to the levels of stress (or disturbance) within an environment. Therefore as the levels of stress increase, selective forces within the environment are more strongly related to survival within the severe conditions than they are to "winning" competitive interactions with other plants. Both hypotheses are supported by a variety of empirical, experimental data (Wijk 1986, Campbell and Grime 1992, Goldberg and Barton 1992, Wilson and Tilman 1993, Bonser and Reader 1995). The aim here is not to attempt a reconciliation of these two theories. It seems reasonable to predict that for a given level of resource supply and demand the intensity of competition should remain constant. However, resource supply is not the only component of stress. Other factors, not directly related to competitive interactions for resources, may limit growth and competition, and thus also reproductive output and fitness. For the most part along a gradient of increasing stress, although the absolute intensity of competition will follow the pattern outlined by Taylor et al. (1990), the importance of competition is probably reduced, as predicted by Grime, since in very stressed environments the abiotic conditions have a much greater selective impact. As stated by Welden and Slauson (1986) "members of two species living together in a very stressful habitat may require many of the same resource items, and thus compete intensely. At the same time their growth rates, survival or reproductive success may be determined almost entirely by their abilities to cope with or escape abiotic stress, defoliation by herbivores, [or] other forms of disturbance,... thus rendering competition unimportant". In addition, increased stress may act to alter the intensity of competition by reducing resource demand. In particularly severe environments it is doubtful that competition can play much of a role either as a community-structuring force altering plant biomass or growth rate (competition intensity) or its reproductive success (competition importance). It is also worth considering the position of vegetative proliferation in this scheme, since the intensity of competition will impact upon growth rates, which will have a direct influence on the fitness of clonal species. Separation of competition intensity and importance may therefore not be as straightforward as is suggested by the scheme of Welden and Slauson.

of plant community ecology (and possibly other areas of ecology). The model emphasises the need to consider the balance between opposing forces in producing observable experimental outcomes. DiTommaso and Aarssen (1991) have suggested a similar counter-balancing relationship of competition and "beneficence" between plants in determining the overall outcome of plantplant interactions. However, ecological research may often oversimplify interactions by ignoring such balances, and also their long-term nature. It is only through long-term studies that we will be able to get a true indication of the outcome of the interactions between plant species. This may explain certain paradoxical results such as the apparent coexistence of species that would at first appear to be strongly competitive. If there is a sufficiently severe period then this may make the overall balance of interactions between the two species positive, and thus promote coexistence, or at least prevent the competitive dominance of one species. An inherent aspect of this model is the ability of plants to modify their environments. Wilson and Agnew (1992) also considered such environmental feedbacks acting as the basis of positive feedback switches, possibly leading to the divergence of the form of neighbouring communities in a way that could either not be explained by an external, environmental phenomenon, or that enhanced the divergence of community compositions initiated by such phenomena. However, they did not consider the interactions between species in the communities where these feedbacks were operating. Many of the switches that they discuss could be the basis for positive plant interactions, for example the entrapment of soil by roots, or the increased supply of water from occult precipitation collected by vegetation. Both of these interactions may benefit the individuals involved, with increased densities of plants being beneficial either by accumulating more soil within the root system or by capturing more air-borne moisture. Positive interactions, especially in the initial stages of community development, could have important consequences not only for the speed or mechanism of succession (Connell and Slatyer 1977), but also for its direction.

The selectiveimpactof positiveplant interactions

Our model predicts that positive plant interactions occur in the majority of ecosystems, and may be involved in many ecosystem processes. Therefore, further research on the mechanisms and effects of positive plant interactions may be essential for a thorough understanding of the factors involved in the structuring of plant communities. One potential direction for research into positive plant interactions is that of investigating
OIKOS 81:1 (1998)

Positiveplantinteractions current and research

It is important to reiterate that, irrespective of the debate concerning the links between competition, stress and disturbance, our model still illustrates a number of important points, and can provide us with some interesting explanatory hypotheses concerning certain ecological conundra, having ramifications in several fields

204

their evolutionary impact. If they are of consequence in effecting the mortality or fecundity of plants in extreme conditions, then we can infer that they will have some selective impact on plant traits. Can we hypothesise in what way this force will have selected for plant characteristics? A number of possible traits that could enhance positive plant interactions are outlined below. I) Decreased dispersal distance of seeds Increased offspring density near to parent plants may bring density-dependent advantages such as increased seedling survival (Walton 1922, Table 1). Vivipary may be one adaptation to this selective force, since not only will it increase the survival probabilities of offspring through increased maternal investment in large propagules (Billings and Mooney 1968, Callaghan and Emanuelsson 1985), but it will also act to increase the density of conspecifics around the parent plant by limiting propagule dispersal distances. 2) Compact morphology of plants This adaptation could increase the density of plant foliage or biomass within a given space and so enhance positive density-dependent effects. Such a situation may be the cause of the compact form of moss cushions (Callaghan and Emanuelsson 1985). 3) Limited response to improved environmental conditions A large response to improved environmental conditions would perhaps indicate competitive tendencies and plastic morphology. Plants that had undergone selection for reduced competition would less readily respond to improved growing conditions. This would produce extremely determinate growth in plant species from extreme environments, as has been shown to be the case for certain species of cushion plant (Spomer 1964, 1979). 4) Increased tendencyfor mycorrhizal associations between plants within a community Seedlings can utilise mycorrhizal connections with mature plants as a means of obtaining resources from parent plants within a community (Hunter and Aarssen 1988). Increased susceptibility to mycorrhizal infection would increase the chances of this positive interaction occurring. Many of the dominant species from arctic tundra ecosystems, such as dwarf shrubs, have been shown to be mycorrhizal (Michelsen et al. 1995), and the potential enhancement of positive interactions may be one subsequent benefit. 5) Increased tendencyfor clonality Clonality can be viewed as a more advanced form of positive plant interaction. Ramets within a clone are analogous to individuals within a population (Callaghan 1988). The benefits of the physiological
OIKOS 81:1 (1998)

connections that can exist between these individuals are numerous. The connections enable resource exchange between individual ramets (Salzmann and Parker 1985, Stuefer et al. 1994), and tighter regulation of the ramet populations' growth pattern in order to make optimum use of heterogenous environments (J6nsd6ttir and Callaghan 1988). The positive interactions occurring between the units of clonal plants can improve the conditions of both their internal and external environments, and so they may be considered as more advanced than those that occur between unitary plants and alter only the external environment. Enhanced ability for positive interactions may be related to the increased occurrence of clonal species within extreme environments (Callaghan and Collins 1981). Many of these traits are characteristic of species from arctic ecosystems. As well as the occurrence of species with such traits, the Arctic is particularly suited to research into positive plant interactions for a number of reasons. Arctic environments contain a wide variety of stress or disturbance factors such as low temperature, limited nutrient supply, intense ice-crystal abrasion and destructive soil movement processes such as frost heaving. The severity of the physical environment produces the primary limitation on plant growth (Porsild 1951, Billings and Mooney 1968, Savile 1972, Billings 1978, 1987, Callaghan 1987, Callaghan and Jonasson 1995), thus increasing the potential for positive interactions to occur, and to be significantly beneficial to those species involved. According to our hypothesis, the combination of these factors within arctic environments would also increase the probability of positive interactions being observed, and thus being possibly subjected to experimentation. Arctic ecosystems could therefore prove extremely fruitful in any future experimentation on positive plant interactions, such as the examination of possible adaptations. However, in any extreme environment a primary problem with the search for adaptations that enhance positive plant interactions is that of separating this form of adaptation from that designed to exploit the very localised areas of improved microclimate and resource availability that can occur in extreme environments. Localised improvement of conditions, for example increased temperature or nutrient availability, can be caused either by the beneficial impact of plants upon the environment (Table 1), or by the features of small scale landscape topography (Crawford and Abbott 1994). The impact of both factors, biotic and geographic, will be similar, with similar adaptations producing aggregations of individuals. It may be the case that we already have evidence of the evolutionary impact of positive plant-plant interactions, but have never examined it in the light of this possible interpretation. 205

Conclusions
Consideration of positive plant-plant interactions may be a key step in obtaining a firm understanding of the dynamics of plant communities. Without further research to establish the importance of such interactions for ecosystem function, under a range of environmental conditions and over prolonged periods of time, we will never truly be able to say that we understand how plant communities operate. We should at least be certain that positive plant interactions are unimportant in a particular ecosystem or environment before we banish them from our interpretation of experimental results. We believe that the simple model that we have presented here may act as a focal point for future research into positive plant interactions, and may help to integrate this developing branch of plant ecology with existing ecological theory. We also hope that it will further stimulate interest in this neglected branch of plant ecology. Acknowledgements The authors would like to thank Phil Grimefor his discussions encouragement and duringthe devel-

Sven Jonassonand LonnieAarssenfor theirusefulcomments the concerning manuscript.

opment of many of the ideas within this paper, and Phil Grime,

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Appendix 1
All figures were produced using Microsoft Excel (ver. 5.0). Data sets have no scale, the values being purely arbitrary and illustrative, indicating the relative importance of the different factors. Data set for Fig. 1 Distancethrough time or space 0 10 20 30 40 50 60 70 80
90

P 50 45 40 35 30 25 20 15 10
5

N 0 -10 -20 -30 -40 -50 -60 -70 -80

-90

D 100 90 80 70 60 50 40 30 20
10

100 Data set for Fig. 3 Distancethroughtime 0 10 20 30 40 50 60 70 80 90 100

-100

P 50 45 30 15 5 0 5 15 30 45 50

N 0 -10 -30 -70 -90 -100 -90 -70 -30 -10 0

D 100 90 70 30 10 0 10 30 70 90 100

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