Forests, Competition and Succession' - Oregon State University

Forests, Competition and Succession'

David A. PerryOregon State University

CompetitionSuccession

Competition, the struggle for limited resources,and succession, the sequence of change in dominantorganisms following colonization, have long beenkey concepts employed by ecologists to understandand organize the patterns of nature. Although com-petition and succession are distinct processes, theyare closely related for at least two reasons. First,successional trajectories are largely driven by inter-actions among organisms, including (but not re-stricted to) competition. Second, both are inti-mately related to the degree of equilibrium ordisequilibrium in ecosystems and landscapes. Ecol-ogists once believed that succession led inexorablyto a stable equilibrium within a given communityof organisms, the composition of which was deter-mined in large part by who won the struggle forlimited resources. Although that view has not beentotally discarded, most ecologists now recognizethat change is the rule rather than the exception innature, with few if any ecological communitiesachieving a long-lasting equilibrium in speciescomposition. Disturbances at many spatial andtemporal scales create "shifting mosaics" of com-munities in different stages of succession, resultingin diverse niches that allow more species to coexist

Portions excerpted from D. A. Perry (1995). "Forest Ecosys-tems. - Copyright Johns Hopkins University Press, with per-mission.

than would be possible if all were competing forthe same set of resources.

This article first discusses competition: why itoccurs, why it does not occur, and how it shapesthe structure of communities. It then turns to thepatterns and mechanisms of succession, many ofwhich turn on the nature of both competitive andcooperative interactions among species.

I. COMPETITION

"The inhabitants of the world at each suc-cessive period in its history have beaten theirpredecessors in the race for life." (CharlesDarwin, "The Origin of Species," 1859)

One of the oldest ideas in ecology is that individ-uals utilizing the same resource will compete ifthat resource is in short supply. For many yearsecologists assumed that the sizes of all populationswithin a given community were ultimately limitedby resources, hence competition was believed tobe an inevitable consequence of making a livingand the major determinant of community structure(i.e., the number of species and size of each popula-tion). Constant struggle is not necessarily implied;over many generations species may evolve waysto avoid competition through allocating resources.Nevertheless, communities are ultimately struc-

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136 FORESTS, COMPETITION AND SUCCESSION

tured by competition, be it ongoing or, as a pop-ular phrase puts it, the "ghost of competitionpast."

Although competition for resources undoubt-edly occurs (at least in some trophic levels), thenotion that it is the major organizing force in natureis overly simplistic. Most ecologists now recognizethat ecological communities are complicated andvariable, with their structure shaped by many inter-acting environmental and biotic factors in additionto resource competition. Species may not competefor resources at all or they may simultaneouslycompete and cooperate. For example, multispeciesflocks of insectivorous birds commonly follow antswarms in the tropics, feeding on insects flushedby the ants. In 1983, F. Bourliere listed two possibleadvantages to such mixed flocking: more efficienthunting in a patchy environment and more eyesand ears for protection against predators. Differentspecies of monkeys also frequently forage together,even when they are quite similar in body size anddiet. Once again, Bourliere (1983, p. 87): ". . .the main advantage for mixed groups (of monkeys)appears to be to make easier the location of patchilydistributed food sources and the detection of preda-tors. A monospecific group of similar size mightwell offer the same benefits to its members, but atthe cost of a stringent social hierarchy which wouldimply a greater energy expenditure for its enforce-ment." A. F. Hunter and L. W. Aarssen list thefollowing ways in which coexisting plant specieshave been demonstrated to help one another: ". . .improving the soil or microclimate, providingphysical support, transferring nutrients, distractingor deterring predators or parasites, reducing theimpact of other competitors, encouraging benefi-cial rhizosphere components or discouraging detri-mental ones, and attracting pollinators or dispersalagents." [See FORAGING STRATEGIES.]

At least three things come into play to modifythe importance of competition within ecologicalcommunities.

1. Species within a given trophic level may belimited by factors other than resources, henceseldom or never have to compete. It has beensuggested that the importance of competition

alternates up the trophic ladder: plants compete;herbivores are held down by predation, hence donot compete; and carnivores compete because theyare at the top of the food chain and therefore haveno predators. Evidence in support of this idea isequivocal. However, there is little doubt that pre-dation, disturbance, or climatic fluctuations can andfrequently do act to maintain populations belowwhat their food supply would permit. This is oftenthe case with herbivorous insects and its can alsooccur in plant communities when herbivores andpathogens increase the species richness of plantcommunities by reducing the ability of any onespecies to competitively dominate others. Higherorder interactions other than predation may comeinto play to reduce competition. Such is the casewith at least some types of mycorrhizal fungi,which by mediating a more equitable distributionof resources among individual plants reduce theability of one or more species to dominate a com-munity.

2. Species may compete for the same resourcesbut also benefit one another in some way that tendsto dilute or negate their negative effects. This un-doubtedly occurs in ecosystems (as exemplified bythe mixed foraging groups discussed earlier), butmay not be readily apparent from casual observa-tion or even from experiments unless conductedover many years (which seldom happens). It hasbeen hypothesized that plant species participate indefense guilds, i.e., either directly or indirectly re-duce herbivory and/or pathogenesis within thecommunity. For example, flowering plants arecommon in young conifer forests, where theyprobably compete with the conifers for variousresources. However, nectar produced by flowersof these plants is important in the diet of at leastsome insects that prey on defoliating insects. It hasbeen documented that 148 species of parasitoids(important predators of defoliating insects) are as-sociated with flowering plants in forests of northernGermany. What is the net effect of these plants onconifers? If they were not in the ecosystem wouldfaster conifer growth eventually be negated bylarger populations of defoliating insects made pos-sible by lower populations of their predators?Questions such as these are seldom entertained in

137FORESTS, COMPETITION AND SUCCESSION

competition studies. Potentially competing specieshave also been hypothesized to form cooperativeguilds based on protecting and stabilizing ecologi-cal commons such as shared mutualists (e.g., polli-nators, mycorrhizal fungi) and soils. "Facilitation,"in which one plant species has some effect thatbenefits others, is commonly observed during suc-cession. It does not follow that a "facilitator" doesnot also compete for resources; however, the neteffect is positive rather than negative. On the otherhand, there are clear instances in which one plantspecies has a net negative effect on others, and othercases in which the net effect of one species on an-other varies with time and environment. Thesepoints are followed in the section on succession.

3. Complexity at scales ranging from landscapesthrough individual trees to soil aggregates createsdiverse niches that allow species to avoid competi-tion through specializing.

One of the primary criticisms leveled against theidea that communities are structured primarily bycompetition is that few experiments have reallytested this. If one wants to know the effect of spe-cies A on species B, then species A must be re-moved in a properly designed study, and the re-sponse of species B must be measured over asufficiently long time to assess the fitness of B.Experiments in which one or more plant speciesare removed are common in forestry and frequentlyshow that removing "competitors" improves thegrowth of those that remain. However, these areseldom followed long enough to tell whether long-term effects tell a different story. While competi-tion is generally an ongoing process that is readilymeasured in short-term experiments, the beneficialeffects of one species on another may be subtle,long term, or manifest only during certain criticalperiods. For example, nodulated nitrogen-fixingplants are common pioneers on disturbed sites,where they play an important ecological role byreplenishing soil nitrogen and carbon. In the shortterm these plants compete with others for resourceswhereas in the longer term they benefit others byincreasing soil fertility. To give another example,some hardwood species that grow intermixed withconifers are relatively resistant to fire. During much

of the lifetime of a stand these may compete withconifers, but during wildfire they protect the coni-fers. Species-diverse grasslands are more stable dur-ing a severe drought than species-simple grass-lands. [See FIRE ECOLOGY.

Interactions among species requiring the sameresources are complex, varying over time and withenvironmental conditions. In contrast, much of thetraditional ecological thinking about the role ofcompetition in structuring communities has beenshaped by mathematical models that treat two in-teracting species as if they were in a constant envi-ronment and isolated from other species in the sys-tem. L. Stone and A. Roberts developed a morerealistic model that evaluates the interactions be-tween any two species ". . . within the frameworkof the community to which they belong." Theirapproach, which they refer to as the "inversemethod," deals strictly with interactions within agiven trophic level. In other words, these are inter-actions in which the participants potentially com-pete for resources. The criterion they use to deter-mine whether a species benefits or suffers ininteraction with another is population growth: inessence, they ask "what happens to numbers ofspecies A if numbers of species B increase?" If Aincreases, it benefits from B (at least within therange of increase of B that is modeled), if A de-creases, it suffers from B. Stone and Roberts con-clude:

"Remarkably, the 'inverse' method findsthat generally a high proportion (20-40%) ofinteractions must be beneficial, or 'advanta-geous,' when not lifted out of the communitycontext in which they actually occur. Thecontrary case, called here 'hypercompetitive,'in which each species suffers from every otherspecies, can occur only if the environment isnearly constant, and the species closely akinto each other, with both of these conditionsholding and persisting to a degree that mustbe considered implausible."

Given the current evidence for major extinctionscaused by meteor impacts, Darwin's "survival ofthe fittest" may be appropriately modified to "sur-


vival of the luckiest." Nevertheless, while variousfactors reduce competition for limited resources,there seems little doubt that important aspects ofcommunity structure reflect the "ghost of com-petition past." Evidence suggests that throughevolutionary time conflicts over food have fre-quently been resolved through specialization; thisis thought by some to have been a significant diver-sifying force in nature. Examples of food-relatedniche diversification within animals are widespreadin nature. In the neotropics, fruits compose theprimary diet of 405 species of birds, 33 species ofprimates, and 96 species of bats. But the diversearray of fruits produced by the numerous plantspecies of these areas permits frugivores to special-ize to some degree and thus reduce competition oravoid it altogether. In the dry tropical forestsaround Monte Verde, Costa Rica, it has been esti-mated that only 13 of the 169 species of fruit eatenby birds are also eaten by bats. Similar studiesthroughout the tropics have found little overlap inthe diets of fruit-eating bats, birds, and primates.[See EVOLUTION AND EXTINCTION. ]

Niche diversification may take numerous forms,including type of food, timing of feeding, place offeeding, and, in some instances, the ability of aspecies to capitalize on food provided by periodicextraordinary events. One of the better known ex-amples is Robert MacArthur's study of five warblerspecies that coexist in conifer forests of New En-gland. All are insect eaters and are about the samesize. These species feed in different positions in thecanopy, move in different directions through thetrees, feed in different manners, and have slightlydifferent nesting dates.

Numerous studies of niche diversification amonganimals have focused on the so-called metric traits,readily measurable attributes such as body size or,in birds, shape and size of the bill, that are assumedto reflect differences in diet. MacArthur discussesbird species diversity on the island of Puercos offthe coast of Panama.

"(T)here are . . four species of interiorforest flycatchers on Puercos. The smallest,the beardless tyrannulet, . . . has an averageweight of 8 gm; the next smallest is the scrubflycatcher . . . with an average weight of

14.6 gm; then follows the short-crested fly-catcher . . . with a mean weight of 33.3 gm.Each of these is about double the weight ofthe previous one. Finally, the largest is thestreaked flycatcher . . . that weighs an aver-age of 44.5 gm. . . . Other families do notseem to sort by size. For instance, there aretwo flower-feeding `honeycreepers,' the ba-nanaquit . . . and the red-legged honey-creeper. They feed together among the flow-ers in the canopy and their mean weights are10.7 and 12.8 gm, respectively. There is aplausible explanation for the (fact that fly-catchers sort by size while honey-creepers donot). Large flycatchers do eat larger foods thansmall ones . . . , whereas there is no simpleway that a large honeycreeper could eat . . .different food than a small one. . . . Ratherthe bills are of different shape, and it is verylikely that these species eat nectar from differ-ent flowers or eat different insects while feed-ing on nectar."

In summary, long-term, diffuse interactions arethe rule in ecological communities instead of theexception. Species certainly compete among them-selves for resources, and it will never be knownhow many are now extinct because they lost astruggle to a superior competitor. However, spe-cies also depend on one another in numerous waysthat are not readily apparent. Those that competemost of the time might benefit one another duringcertain critical periods. When one reflects on themultiplicity of indirect, diffuse, and subtle interac-tions that are possible in ecosystems, it is apparentthat the experiments necessary to truly grasp thepatterns of nature will be formidably difficult atbest, and maybe even impossible (which is notto say that they should not be attempted). Likephysicists (who deal with much simpler systems),ecologists may have to accept an "uncertainty prin-ciple," i.e., we may never completely capture therichness of nature within the framework of scien-tific hypotheses and models.

II. SUCCESSION

"No matter what forms we observe, butparticularly in the organic, we shall find no-


where anything enduring, resting, comp-leted, but rather that everything is in continu-ous motion." (Goethe, 1790)

Envision a landscape of bare rocks exposed by aretreating glacier. This is an inhospitable environ-ment for life. There is no soil, hence no waterand nutrient storage capacity to support plants.Animals find little shelter and no food. Some lifeis adapted to such conditions, however. Lichenscolonize the rocks, obtaining nitrogen directlyfrom the air and other nutrients by releasing acidsthat break down the rock. They scrounge waterfrom cracks in the rock. Lichens provide a foodbase for animals and, mixing their own organicmatter with the products of rock weathering,slowly build a soil, which allows higher plants toestablish. These, along with the set of animals andmicrobes that accompany them, further modifythe environment, casting shade and building litterlayers, resulting in yet another set of plants andanimals—adapted to the new conditions—comingto occupy the site.

This sequence represents what is termed primarysuccession; the term "primary" is applied becausethere was no preexisting community on the site(or if there was all traces were obliterated). It is anidealized picture—some higher plants, includingtrees, are quite capable of colonizing fields of barerock and do not have to wait on lichens—but never-theless illustrates a common pattern in primary suc-cession:

A disturbance (glaciation in the example justgiven, but it could be something else, e.g.,volcanic eruption, lava flows) wipes out lifeand most or all traces of life on a site.A set of organisms adapted to survive andreproduce in these "primary" conditionsbecomes established; the colonizing plants areoften characterized by an ability to extractnitrogen (N) directly from the atmosphere andother nutrient elements directly from rock.Colonizing organisms modify the site,accumulating nutrients and building soil, thuscreating the conditions that permit a secondwave of organisms to establish.

Over many years the site becomes increasinglymodified by the biotic communities thatoccupy it: that combination of minerals, deadorganic matter, complex biochemicalmolecules, and living organisms that is calledsoil continues to be built, litter accumulates,and, particularly in climates capable ofsupporting trees, the accumulation of leaf areaincreasingly shades and buffers the interior ofthe community from environmental extremes.As one set of organisms modifies the site, it isreplaced by another set better adapted to thenew conditions. Barring another disturbance, arelatively persistent community eventuallycomes to occupy the site, in forests often (butnot always) dominated by tree species that areable to reproduce in shade. The qualifyingterm relatively must be taken seriously whenapplied to the persistence of late successionalstages. Trees may live from hundreds tothousands of years, but they are not immortal.If fire, wind, insects, pathogens, chainsaws, orsomething else does not kill them, old ageeventually will. Each death creates space fornew individuals of the same or different speciesto grow, hence forests are dynamic rather thanstatic. A given set of species virtually neverpersists indefinitely on a given piece of ground,although constancy in species composition doesoccur at regional scales (except during majorchanges in climate).

There are many variations on this theme, butone feature is common to all primary successionalsequences: primary succession involves a progres-sive "imprinting" of biological features onto aphysical landscape.

Perhaps the most important biological imprintis soil. Joan Ehrenfeld discusses soil developmentduring primary succession on sand dunes:

"The soil microflora interacts with plantsin promoting soil development in dune eco-systems. Hyphae of both saprophytic and en-domycorrhizal fungi help bind sand grainsinto aggregates through the excretion ofamorphous polysaccharides which in turnserve as substrate for colonization by bacteria,


4

actinomycetes, and algae. The presence of adiverse microflora enhances the process of ag-gregation. The degree of soil aggregation in-creases (as succession proceeds) . . . soil ag-gregates (mg /kg soil) increase from 5 in theforedunes to 40 on the mobile dune slope, 300on the dune crest, and 1260 on young fixeddunes. The aggregates contain a variety offungal species, including mycorrhizal species,and various bacteria . . . thought to be nitro-gen fixing. There is an interactive effect be-tween plant root growth and aggregate for-mation . . . (the) total amount ofaggregation, and concomitantly the abun-dance of all microfloral species . . increasesdramatically in the presence of roots."

Now envision the mature forest that is the "endpoint" of primary succession on that bare rock. Infact, it is not an end point at all, but one stage ina (more or less) cyclical alternation of communitiesthat will dominate that site. At some future date theglaciers will probably return, but in the interveningperiod there will be many more disturbances suchas fire or severe windstorms that will kill the treesand initiate the process called secondary succession,which occurs where disturbance has left biologicalimprints (or legacies) such as soil, surviving indi-viduals, and dead wood. Virtually all ecosystemsexist within a matrix of fluctuating environmentspunctuated by periodic disturbances ranging frommild to severe. The twin processes of disturbanceand succession form the core of natural dynamicsand create much of the variety that is seen in thenatural world. On the other hand, disturbances thatare too frequent, severe, or "foreign" (i.e., havecharacteristics to which the species composing thesystem are not adapted) can throw succession offtrack and lead to persistent changes that frequentlyinclude loss of diversity and productivity, a wide-spread phenomenon in today's world. Hence un-derstanding the mechanisms of community re-sponse to and recovery from disturbance is morethan an academic exercise, it yields insights intohow humans can protect and sustainably utilizenatural systems.

A. Brief Historical Notes

Among American ecologists, two names stand outin the development of successional ideas during theearly years of the 20th century: Frederick Clementsand H. A. Gleason. 2 Clements believed that com-munities were superorganisms and that successionwas a maturation of the community toward itsmost mature state, which he called the "climax:"

"Succession must then be regarded as thedevelopment or life history of the climax for-mation. It is the basic organic process of vege-tation, which results in the adult or final formof this complex organism. All the stages thatprecede the climax are stages of growth. Theyhave the same essential relation to the finalstable structure of the organisms that seedlingand growing plant have to the adult individ-ual." (Clements, 1916)

For Clements, the composition of the climax vege-tation was uniquely determined by climate:

"Such a climax is permanent because of itsentire harmony with a stable habitat. It willpersist just as long as the climate remains un-changed, always providing that migrationdoes not bring a new dominant from anotherregion."

Like Clements, Gleason recognized the impor-tance of environment in determining the composi-tion of plant communities; however, he rejectedClements' idea that a given community was a re-peatable entity that occurred whenever a given setof environmental conditions occurred. In his 1926paper, Gleason argued that two factors came intoplay to make each community distinct from everyother. The first was the independent nature of plantspecies:

2 The same contrasting viewpoints were developed in early 20thcentury Europe. There, the Russian Sukatchew and the FrenchmanBraun-Blanquet argued that plant communities were repeatableentities, whereas the individualistic view was developed by theRussian, Ramensky, and the Frenchman, Lenoble.


. . every species of plant is a law untoitself, the distribution of which in spacedepends upon its individual peculiaritiesof migration and environmental require-ments. . . . The behavior of the plant offersin itself no reason at all for the segregation ofdefinite communities." (Gleason, 1926)

The second factor was randomness, by whichGleason meant that the composition of a givencommunity was not completely predetermined byenvironmental factors. Instead, any number ofplant species might be able to occupy a given site,but may or may not depending on whether theirseeds were dispersed into disturbed areas. Gleasonargued that community composition might be re-peatable in regions with few species, simply be-cause there were few alternative communities thatmight develop. But, as species diversity increasedwithin a region, so did the variety of communitytypes that might develop on a given site during thecourse of succession.

As with most polar issues, the "truth," at leasthow it is perceived today, contains some elementsof both Clements and Gleason, but is adequatelycaptured by neither. Most modern ecologists rejectClements' idea of communities as superorganisms.But, if a community is not an organism in thesame sense as an oak tree or a swallowtail butterfly,neither is an individual plant, as Gleason suggests,a law unto itself. Every organism is part of and ininteraction with a larger community: feeding, be-ing fed upon, competing, cooperating, and coexist-ing. Moreover, although randomness is clearly apowerful force in nature, species evolve strategiesto reduce the uncertainty associated with ran-domness and to retain a presence, or a potentialpresence, on a site. Biological legacies, including(but not restricted to) buried seeds, live roots fromwhich new tops sprout, and mycorrhizal fungi,are passed from the old community to the new,shaping the new in the image of the old, as Clem-ents suggested. Finally, despite the undeniable (andnot surprising) fact that different species differ intheir environmental requirements (as Gleason ar-gued), the Clementsian view of mutual dependenceamong members of a community also has validity.

Through the years there has been a shift in em-phasis among ecologists who study succession.Clements, Gleason, and others who followed themfocused on end points—of which Clements' climaxwas the archetype. Today, ecologists are more con-cerned with the mechanisms and processes thatshape community dynamics. The following twosections explore successional patterns, then con-sider mechanisms behind those patterns. It mustbe kept in mind that what follows are generaliza-tions that may or may not hold in a given situation.As Blaise Pascal observed, "Imagination tires be-fore nature."

B. Stages of Succession

Particularly in severe disturbances, rapidly grow-ing, often short-lived species with widely dispersedseeds are often the most abundant early pioneers.These nomads, as Gomez-Pompa and Vasquez-Yanes call them, are frequently herbs but may alsoinclude some tree species. Nomads seldom domi-nate a site for long periods, generally being quicklyreplaced by shrubs and trees that were present inone form or another in the predisturbance commu-nity. These include plants that grow from buriedseeds, sprout from roots, or that survive the distur-bance unharmed. In many cases, early successionalplants are intolerant of shade, hence their seedlingsdo not survive and grow beneath an establishedcanopy; in the absence of disturbance the early suc-cessional community generally does not perpetuateitself.

Early successional stages are relatively short inboth time and stature of the dominant vegetation,whereas the intermediate stages are increasinglylengthy and taller, culminating in Clements' climaxcommunity, one that, in theory, persists indefi-nitely, but in fact rarely does. (In fact, coniferousforests become highly susceptible to crown fireswhen the mid-successional trees are senescing andlate successional conifers begin to grow taller.)Note that a successional sequence refers to changesin dominance, or the degree to which the site isoccupied by canopies and roots, not to the presenceor absence of a given life form. Shrubs and treesthat sprout from roots or grow from buried seed,


legacies of the old forest, are likely to be presentduring the earliest stages of secondary succession(unless the disturbance is so catastrophic that sur-face soils are lost). Many species that come to domi-nate forests in late successional stages are also ableto pioneer newly disturbed sites. Western hemlock,a shade-tolerant, late seral tree of the Pacific North-west, has light, readily dispersed seed and fre-quently pioneers clear-cuts in relatively moist habi-tats. In New England forests, both early and late-seral tree species establish soon after disturbance,with fast-growing pin cherry dominating early insuccession and slower growing species emergingto dominate later. In general, throughout any givensuccessional sequence, the community at any onepoint in time is likely to contain not only the domi-nants, but seedlings of future dominants. The pe-riod prior to complete canopy closure is a timeof great species richness, containing mixtures ofherbs, shrubs, and tree seedlings, which in turncreate diverse habitats for animals.

Most, if not all, forest communities include spe-cies that are adapted to recover quickly from distur-bances. For example, in the black spruce forestscommon to the interior of Alaska, burned sites arequickly occupied by sprouting grasses, shrubs, andsmall trees (willows, birch) and by numerous blackspruce seedlings originating from seed stored insemiserotinous cones. In the Pacific Northwest,wildfires create a mosaic of species that either sur-vive the fire through heat-resistant bark or regener-ate through sprouting or from buried seed. Theinitial colonizers in areas where the overstory iskilled are generally nomads that persist for a fewmonths to a few years before being succeeded byformer residents growing from sprouts or buriedseed. [See FOREST STAND REGENERATION, NATURALAND ARTIFICIAL.]

Disturbance severity acts as a filter on the avail-able species pool, modifying the composition of theearly successional community. Disturbances thatpreserve soil but destroy aboveground parts favorsprouters or species with seed stored in the soil.Species with serotinous cones are generally an ex-ception, but not always. In the Rocky Mountains,very intense burns may consume the serotinouscones of lodgepole pine, favoring sprouting aspen.

This may also occur in black spruce/aspen standsthat occupy certain habitats in interior Alaska. Onthe other hand, fires that generate excessive heatin the soil either delay recovery by sprouting plantsor kill the roots so no sprouting is possible. Tropi-cal trees, many of which sprout prolifically follow-ing windthrow, are particularly vulnerable to rootsbeing killed in fire. Without the sprouters, the com-position of the early successional community de-pends on seeds stored in the soil or input to the sitefollowing disturbance. Disturbances severe enoughto destroy soil (e.g., landslides) generally initiateprimary succession, and sites must be colonizedby seeds from elsewhere. However, biological leg-acies have a surprising ability to persist and shapeearly successional communities. Foreign distur-bances—those for which species that comprise thesystem have no adaptations (e.g., herbicides, firein some forests)—may eliminate biological legaciesand open the site to colonization by nomads.

Along with disturbance severity, timing of a dis-turbance also filters the available species pool.Composition of the early successional communityoften depends on coincidences between the time atwhich a disturbance occurs and the natural rhythmsof species within the colonizing pool. Three differ-ent time scales are important: time of year, the yearitself, and the interval between disturbances. Thefirst two time scales relate to coincidence betweendisturbance and the availability of propagules(seeds or sprouts) whereas the third relates to lifespan.

Plant species vary in their seasonal rhythms,hence a disturbance occurring at one time of theyear may select for quite a different set of earlysuccessional plants than one occurring at anothertime of year. The ability of some species to sproutfollowing the destruction of aboveground partsvaries seasonally: destroyed at one time of yearthese recover vigorously, at another time of yearnot at all. Seeds of different species mature, henceare available for colonization, at different times ofthe year. For example, in interior Alaska mostwildfires occur during June and July, coincidentwith the ripening and dispersal of aspen and balsampoplar seed, but before seeds of white spruce andpaper birch ripen. In the tropics, where yearly


rhythms of the biota are not constrained by lowtemperature for part of the year, species varywidely in phenology. Trees that produce animal-dispersed seeds tend to fruit year-round, whilethose producing wind-dispersed seeds fruit onlyduring the dry season and, moreover, seeds aredispersed only on days with relatively low humid-ity. Other factors being equal, a disturbance coin-ciding with this dispersal would probably resultin a relatively high proportion of wind-dispersedspecies in the pioneering community, whereas onethat did not coincide would have more animal-dispersed species.

Many trees produce seeds at intervals of severalyears. In Alaska, for example, birch producesheavy seed crops at least once every 4 years, butwhite spruce only once every 10 to 12 years. Hencethe capacity of a given species to deliver seed to anewly disturbed site depends, among other things,on whether the disturbance coincides with a goodseed year. Such a coincidence is not totally random,however, because weather conditions that increasethe probability of wildfire, such as hot, dry springs,also trigger seed production by white spruce.

Finally, the interval between disturbances canalso influence the composition of the pioneeringcommunity. For example, an 80-year-old westernhemlock forest in northern Montana was estab-lished following a fire without being preceded bylodgepole pine, which is the usual early succes-sional tree of that area. In that case the intervalbetween fires had been sufficiently long that shade-intolerant lodgepole pine had dropped out of theforest, leaving only hemlock to colonize. (Unlikemany late-successional trees, hemlock produceslight, widely dispersed seed, enabling them to playthe role of the pioneer.)

The Steady-State Forest

Once the forest becomes dominated by species thatreproduce successfully under their own canopy orin gaps created by the death of old trees, commu-nity composition may become relatively stable.This is Clements' climax, and is also called thesteady-state or equilibrium community. The domi-nant trees are called climax species. The steady-stateforest is not static, but is composed of a dynamic

mosaic of patches created by old trees dying andyoung trees filling the gaps that are left—a condi-tion termed "shifting-mosaic steady state." Speciescomposition may or may not change over time atany one point on the ground, but on the largerscale of the landscape it will remain constant. Theage structure of the forest changes from the rela-tively even-aged condition of earlier successionalstages to the many-aged condition. Biomass accu-mulation levels out to zero and total biomass re-mains relatively constant. When discussing steadystates, it is important to distinguish between forestsand forested landscapes. In theory, all forests attaina steady state as the end point of succession. Infact, however, many do not, or if they do, theydo not stay there long because disturbance is alwayspart of the scene. On the other hand, forested land-scapes may maintain a relatively stable distributionof stands in different successional stages (the shift-ing mosaic), even when disturbances are frequent.The landscape area within such a relative steadystate depends on the average scale of the distur-bance: a regime dominated by small-scale distur-bances, such as minor windthrow or low intensityfire, produces a steady state within relatively smallareas. This seems to be the case in moist tropicalforests that are not on hurricane tracks, mixed coni-fer hardwood forests of eastern and central NorthAmerica, dry ponderosa pine forests of interiorwestern North America, and dry miombo wood-lands of southern Africa. In each of these, the steadystate is characterized by frequent minor distur-bances, such as the death of old trees, minorwindthrow, or ground fires, that create spacewithin which young trees can establish and grow.The steady state of both ponderosa pine forests andmiombo woodland depends on frequent groundfires, in the absence of which new species invadeand the character of the forest changes. When thedisturbance regime is characterized by large events(e.g., high intensity crown fires), a steady-statemay be found only within very large landscapes.Because the disturbance regime of many foresttypes is characterized by relatively frequent small-scale events punctuated by infrequent large-scaleevents, the scale at which constancy is found onthe landscape varies over time. F. G. Hall and col-


leagues used remote imagery (Landsat) to doc-ument the nature of the shifting mosaic in the900-km2 area of the Superior National Forest innortheastern Minnesota, a little less than one-halfof which was in wilderness (no logging allowed).Using spectral characteristics (light reflected fromthe surface) of both visible light and near-infrared,different tree species were distinguished along withthe degree of crown closure. This information wasused to identify five successional stages (from earlyto late) from Landsat photos: clearings, areas ofregeneration (cleared areas covered by low shrubsand young trees), mature stands of deciduous trees,mixed deciduous—conifer stands, and closed can-opy pure conifer stands. Photographs from 1983were then compared to 1973 photos to determinethe rate of change from one type to another. Thelandscapes of both the wilderness and nonwilder-ness were very dynamic. Over the 10-year periodthat was studied, about one-half of the standschanged from one successional stage to another.Despite the dynamism at the stand level, however,the proportion of different successional stagesacross the landscape remained relatively constant.

C. Mechanisms of Succession

In brief, successional trajectories are influenced bytwo primary factors: which species colonize first(the so-called priority effects) and how the initialdominants (and each succeeding wave of domi-nants) influence what follows. Numerous factorscombine to determine which species (or set of spe-cies) initially establish, although biological legaciesprovide threads of continuity that facilitate the re-covery of species with prior history on a site. Ac-cording to J. H. Lawton and V. K. Brown, "Thereis growing evidence for priority effects in commu-nity assembly (either species A or species B canestablish in the habitat; which one actually doesdepends upon which arrives first). Priority effectsmay then lock community development into alter-native pathways, generating different end pointsor alternative states." Through what mechanismsdo the earliest arrivals shape subsequent patternsof community development?

In an influential paper in 1977, J. H. Connell andR. 0. Slatyer proposed three ways in which a plant

might influence a potential successor: facilitation,tolerance, and inhibition. These terms refer to theeffect of environmental modification by early colo-nizers on the subsequent establishment of late suc-cessional species. In the facilitation model, onlyearly successional species are able to colonize dis-turbed sites, and these modify the environment insuch a way that it becomes less suitable for theirown species and more suitable for others. In thetolerance and inhibition models, disturbed sites arepotentially colonized by both early and late succes-sional species (i.e., there is nothing inherent in thenewly disturbed environment to prevent coloniza-tion by late successional species), which then mod-ify the environment in such a way that new individ-uals of early successional species are unable tobecome established, with late successional specieseither unaffected by these modifications (tolerancemodel) or also inhibited (inhibition model).

J. H. Connell and R. 0. Slatyer provided a valu-able framework for thinking about species interac-tions during succession. However, except in a fewcases, successional dynamics rarely fit neatly intoone or another of the categories they proposed.The interaction between individuals of two differ-ent plant species during succession often containselements of both inhibition (e.g., competition forresources) and facilitation, with the net effect vary-ing depending on factors such as soil fertility, cli-mate, and the relative stocking density of each spe-cies. The net effect may also vary over time, arelationship dominated by competition at one stageof stand development becoming predominantly fa-cilitative later on or vice versa. Moreover, succes-sional dynamics can rarely be reduced to interac-tions between two species: the nature of therelationship between any two individuals is condi-tioned by numerous other plants, animals, and mi-crobes.

With this background in mind, the mechanismsof interaction will be explored in more detail, be-ginning with facilitation, then moving to inhibi-tion, and closing with higher-order interactions.

D. Facilitation

Primary successions probably always involve facil-itation of one kind or another, most often related


to soil building and nutrient accumulation. Soils donot develop without plants, and pioneers facilitateestablishment of their successors by weatheringrocks, accumulating nutrients and carbon, and pro-viding the energy base that allows populations ofsoil microbes and animals to establish and grow.Facilitation commonly occurs during secondary aswell as primary succession. For example, largeamounts of nitrogen can be lost from ecosystemsduring fire, and nodulated plants are often amongthe earliest pioneers on burned sites. These plantsare often rapid growers that initially compete withother trees and shrubs for water and nutrients, andforesters have often viewed these as undesirablecompetitors with crop trees. However, in the longrun they facilitate the growth of other plants in theecosystem by restoring soil fertility.

Early successional plants may create certainstructures or habitats that facilitate the establish-ment of later successional species. Providing coveror perches for animals that disperse seeds is oneway in which this happens: fruits are eaten and theseed is defecated and nuts are dispersed throughthe caching behavior of animals. Seeds buried bybirds (particularly nutcrackers and jays) and mam-mals (e.g., squirrels, bears) are a primary avenueof establishment for heavy-seeded species such asoaks, beech, hickories, and some pines (whitebark,limber). It has been estimated that, in a good seedyear, a single Clark's nutcracker may cache 100,000whitebark and limber pine seeds and that jays areable to disperse 150,000 nuts from a beech woodlot.Since animals are exposed to predators when in theopen, they frequently constrain their movements,including seed caching, to areas with cover. Jays,for example, avoid open fields when buryingacorns. Hence the cover provided by early succes-sional trees and shrubs facilitates the seed dispersalof late successional trees.

One of the more common examples of facilita-tion during early succession, at least in some envi-ronments, is the so-called "island effect," in whichtree or shrub seedlings establish most readily in thevicinity of an already established tree or shrub (thenurse plant). (This should not be confused with facil-itation by nodulated plants discussed earlier; nurseplants may or may not be nodulated.) Tree seed-lings invading savannas in Belize, for instance, es-

tablish preferentially near other trees, and the sameis true for tree seedlings establishing in savannasin the Philippines and in abandoned pastures inAmazonia. The island effect has been noted often inboth forests and deserts of western North America.Both ponderosa and pinyon pines require nurseplants to establish on certain droughty and/orfrosty sites. Live oak seedlings are strongly associ-ated with some species of woody shrubs in centralCalifornia, and Douglas fir seedlings establish pref-erentially beneath some species of oaks in northernCalifornia. One study of natural regeneration inOregon found nearly five times more Douglas firseedlings beneath Pacific madrone trees than in theopen. Not all trees and shrubs necessarily act asnurse plants on a given site. For example, whileabundant Douglas fir seedlings establish beneathcanopies of Pacific madrone and some species ofoaks, none establish beneath nearby Oregon whiteoak stands.

Reasons for the island effect are not always clear,but there are at least three plausible mechanisms,any or all of which could be operating in a givensituation. Nurse plants might (a) shelter seedlingsfrom environmental extremes, (b) act as foci forseed inputs, and (c) provide enriched soil micro-sites. Shelter can significantly improve survival indroughty sites as well as in cold environments.For example, in the droughty forests of southernOregon and northern California, shade cast byearly successional hardwood trees and shrubs mayreduce the water use by conifer seedlings growingbeneath them (less transpiration is needed to coolleaves). On high elevation or other frosty sites,nurse plants provide a relatively warm nighttimeenvironment by preventing excessive loss of radi-ant heat. As discussed earlier, established trees andshrubs act as foci for seed inputs because they attractbirds, and birds often leave behind seeds. Overone 6-month period in an abandoned pasture inAmazonia, nearly 400 times more tree seeds weredispersed beneath Solanum crinitum trees colonizingthe pasture than fell in the open. Eighteen differenttree species were represented in the seed rain be-neath Solanum.

Plant islands may also facilitate the establishmentof later-arriving species during secondary succes-sion through soil chemistry, biology, or structure.

146 FORESTS. COMPETITION AND SUCCESSION

This is in some ways similar to, but in other waysquite different than, the facilitation that occursthrough soil building during primary succession.Pioneers during secondary successions may restoresoil carbon, nutrients, and organisms lost duringdisturbance; however, what is probably more com-mon following natural disturbances is that the mostresiliant members of the former community, spe-cies that are able to sprout from roots or growfrom buried seeds, prevent soil degradation in thefirst place by preventing excessive nutrient loss andby maintaining critical elements of soil biology andstructure.

Ecologists have known for some time that earlysuccessional plants prevent excessive nutrient lossafter disturbance. A growing body of evidence sug-gests that islands of pioneering shrubs and trees,especially those that are legacies of the previousforest, also stabilize soil microbes that facilitate thereestablishment of later-arriving plants. The sur-vival and growth of tree seedlings establishing indisturbed areas may depend on their ability toquickly reestablish links with their belowgroundmicrobial partners, especially on infertile soils orin climatically stressful environments. That wouldseem not to be a problem for plants that can sproutfrom roots because they presumably never losecontact with belowground partners. However, itcould be a problem for trees that reestablish slowlybecause their seeds must be dispersed to disturbedsites from elsewhere. What happens to their micro-bial partners during the period the host plant isabsent? One possibility is that the microbe simplygoes dormant until its host plant reestablishes. An-other possibility is that the microbe is flexibleenough to utilize other food sources, perhaps bysoil organic matter or a pioneering plant. The latterseems to be the case in tropical and at least sometemperate forests. The most common mycorrhiza-forming fungal species in tropical forests are widelyshared among different tree species, as are some ofthe fungi that form mycorrhizas with temperatetrees and shrubs. An early successional plant thatsupports microbes needed by later-arriving plantseffectively facilitates the reestablishment of the lat-ter, although it may also compete with the latearrival for light, water, and nutrients. In southwest

Oregon and northwest California, Douglas-fir andvarious hardwood trees and shrubs share someof the same mycorrhizal fungi. The hardwoodssprout from roots following disturbances whereasDouglas-fir must reestablish from seeds. Douglas-fir seedlings tend to survive and grow better inthe proximity of at least some hardwood speciesthan in the open; controlled studies indicate thatthe phenomenon is related to soil biology. TheDouglas-fir arc believed to "plug into" the networkof hyphae extending from the hardwood mycorrhi-zae, which allows seedlings to rapidly develop theirown water- and nutrient-gathering capacity. Butthe phenomenon is complex and appears to involveother factors as well, including nitrogen-fixing bac-teria and perhaps bacteria that stimulate root tipproduction by seedlings. Nutrients also cycle fasterin soils near hardwoods than in the open, a reflec-tion of greater biological activity. The evidenceamassed so far suggests that hardwoods of thisarea act as selective filters of soil biology, retainingbeneficial soil microbes and inhibiting detrimentalones. Studies of unreforested clear-cuts have foundthat the inability of seedlings to establish may berelated to the buildup of certain types of microbesthat inhibit seedlings and their mycorrhizal fungi.In at least one instance, soils near sprouting hard-wood islands within a clear-cut were relatively freeof deleterious microbes. At present, ecologists haveonly a rudimentary understanding of the complexrelationships among plants and soil organisms, andhow these influence successional dynamics.

I. InhibitionSuccession always implies a change in the availabil-ity of resources. The deepening canopy shades andalters the microclimate within a stand, favoringshade-tolerant species over those that need high lightlevels to establish. Nutrients become increasinglytied up in biomass. In what has been called the re-source ratio hypothesis, David Tilman argues thatrelative change in the availability of different re-sources is generally an important mechanism forspecies change during both primary and secondarysuccessions. In many cases early successional speciescreate the conditions that inhibit their own progenyfrom succeeding them. For instance, many sites that


had been clear-cut in the Oregon Cascades duringthe 1960s and early 1970s became dominated bynitrogen-fixing shrubs in the genus Ceanothus. For-esters and some scientists were concerned that cea-nothus might exclude trees for many decades. Even-tually, however, intermixed conifers began to growabove the shrub canopy, and most of those sites arenow dominated by Douglas-fir. Inhibition was notpermanent in these cases because of the inherentlydifferent growth rhythms of the species: ceanothusand alder grow fast and reach maximum heights ata relatively young age, whereas Douglas-fir growsmore slowly but maintains growth, eventually be-coming taller than the others.

On the other hand, inhibition of one species byanother can be relatively long lasting when circum-stances permit an aggressive early successionalplant to form a dense, monospecific cover that ef-fectively excludes other species. The pioneer couldexclude other species by preempting site resourcesso fully and quickly that no other species can estab-lish, or it might allelopathically inhibit other plantsand/or their mycorrhizal fungi. In eastern NorthAmerica, for example, the failure of trees to rees-tablish in old clear-cuts, abandoned agriculturalfields, and areas burned by wildfire has been relatedto the allelopathic inhibition of tree seedlings byherbs, ferns, and grasses. In the Sierra Nevada ofCalifornia, the herbaceous perennial Wyethia mollishas spread widely in old burns and allelopathicallyinhibits tree regeneration. Excluding wildfiresfrom Swedish forests resulted in the spread of adwarf shrub (Empetrum hermaphroditum) that allelo-pathically inhibits tree regeneration. The inhibitoryplants in these examples are often natives that oncehad been present in relatively low numbers and thatwere apparently triggered into a more aggressivemode by some foreign disturbance; in other words,a balance was disrupted. In Pennsylvania, tree seed-lings were originally eliminated from recoveringclear-cuts by forest fires and exceptionally highpopulations of deer. In California, overgrazing al-lowed the unpalatable Wyethia to spread at the ex-pense of more tasty plants. In Sweden and else-where, excluding wildfire has shifted a balance soas to favor the spread of plants previously limitedby fire.

Woody plants can have particular difficulty get-ting a foothold within established grass communi-ties. In western North America, annual grasses areoften deliberately sown in recently burned foreststo stabilize soils. However, the grasses can com-pletely inhibit the recovery of native shrubs, at leastfor several years. In Central and South America,areas cleared of forest are frequently seeded tograsses to provide cattle pasture, then abandonedafter a few years because they decline in productiv-ity. Trees have great difficulty in reinvading aban-doned pastures. According to D. Nepstad et al.(1990):

"Directly or indirectly, grasses present bar-riers to tree seedlings at every step of estab-lishment in abandoned pastures with historiesof intensive use. Seed dispersal into grass-dominated vegetation is low because grassesdo not attract birds and bats that eat fleshyfruits of forest trees. Grasses provide food andshelter for large populations of rodents thatconsume tree seeds and seedlings . . . . Thedense root systems of grasses produce severesoil moisture deficits in the dry season andcompete for available soil nutrients. Finally,grasses favor fire so that tree seedlings thatdo surmount the numerous obstacles to estab-lishment are periodically burned."

If a pioneer successfully excludes other plantsand is also capable of reproducing under its owncanopy, it can, in theory at least, hold a site indefi-nitely. Such is the case with the Pacific coast shrubsalmonberry Rubus spectabilis, which produces purestands of 30,000 or more stems per ha followingdisturbance. By sprouting from basal buds and rhi-zomes, salmonberry quickly replaces old stemswith new ones, thereby creating unevened periods.Once a pure stand (i.e., without intermixed treeseedlings) attains a sufficiently high density, plantssuch as salmonberry are likely to persist until weak-ened by pathogens or insects or until confrontedwith a disturbance to which they are not adapted.Because of their relative simplicity, species mono-cultures may be especially vulnerable to pests andpathogens; however, this remains to be seen.


2. Higher-Order Interactions: ThoseInvolving More Than Two Species

In the past, ecologists thought of succession as aprocess driven primarily by plant-plant interac-tions. Studies have now shown that many otherelements of the ecosystem can either directly orindirectly influence successional trajectories, in-cluding particular microbes, animals, and abioticenvironmental factors. Community interactionsinvariably involve several species, not just two,hence complex relationships may develop duringsuccession. In the North Carolina Piedmont, forexample, early successional pines inhibit the estab-lishment of fast-growing hardwoods such as Liq-uidambar, which, in the long term, facilitates theentry of slower-growing oaks and hickories. Ani-mals often modulate plant-plant interactions dur-ing succession. In the Pacific Northwest, browsingelk and deer prefer hardwood shrubs over coniferseedlings, accelerating succession from shrubs totrees. This was demonstrated by a study that ex-cluded elk and deer from a portion of a clear-cutin western Washington. In areas accessible to elkand deer there were 8.7 woody stems per m2, one-half of which were Douglas-fir, whereas the areawith no animals present had 19 woody stems perm2, 11 of which were salmonberry, a particularlyaggressive competitor with conifer seedlings. Ineastern Oregon, early successional communities inwhich deer, elk, and cattle are excluded are domi-nated by Ceanothus sp. Where those animals arepresent, however, browsing limits the heightgrowth of the shrub, and sites are dominated rela-tively quickly by conifers. On the other hand,where trees are favored food or, as is more oftenthe case, when excessively high animal numbersresult in a shortage of preferred food, animals willdefinitely retard succession and even jeopardize theexistence of trees on a site.

Soil organisms play an important but poorly un-derstood role in shaping the composition of succes-sional plant communities. The belowground food-web is critically important to the nutrient cycle,especially invertebrates and protists that graze mi-crobes. Soils contain microbes such as mycorrhizalfungi and some types of bacteria that directly bene-

fit plants, and microbes that are pathogenic or oth-erwise inhibitory toward plants. Particular micro-bial species within those broad groups seldomaffect all plant species equally, e.g., a given speciesof mycorrhizal fungus may benefit some plants andnot others; the same is true for the detrimentaleffect of pathogens. In some instances, a microbethat stimulates one plant species is pathogenic to-ward another. Because of the selectivity of theiraction, the composition of the microbial commu-nity on a site feeds back to affect the relative successof different plant species. The relationship is recip-rocal because a microbe that depends on livingplants for food—whether it is a mycorrhizal fungusor a pathogen—presumably cannot persist indefi-nitely in the absence of a host plant. As a result,feedback relationships develop between composi-tion of the plant community and composition ofthe soil microbial community.

The availability of beneficial microbes in someinstances determines whether their host plants canestablish on a site or how well they grow onceestablished. Mycorrhiza formation by plants maybe reduced where host plants have been absent toolong, on highly disturbed areas (e. g., where erosionis severe), and in some instances even with rathermild soil disturbance. Inoculating seedlings eitherwith mycorrhizal fungi or with forest soils or litterhas significantly improved the survival of treesplanted in mine spoils, abandoned fields, old clear-cuts, and natural grasslands. Research in Canadaindicates that inoculating with certain types of rhi-zosphere bacteria significantly improves thegrowth of outplanted tree seedlings. In one case,forest soil transfers enhanced tree seedling estab-lishment in clear-cuts through reintroducing inver-tebrates and protists that are keystones in the nutri-ent cycle.

Inhibitory soil microbes include well-knownpathogens, such as root rots and the so-called"damping-off" fungi, and less well-knowngroups, sometimes called "exopathogens," thatcan have sublethal inhibitory effects on plants and/or mycorrhizal fungi. Actinomycetes, a form offilamentous bacteria, have been implicated in refor-estation failures in the Pacific Northwest. Strepto-myces, from which the antibiotic streptomycin is


derived, is a genetically diverse soil actinomycetethat has complex effects on other organisms. De-pending on the isolate, Streptomyces allelopathicallyinhibit plants, bacteria, and/or plant pathogens,and may either inhibit or stimulate mycorrhizalfungi. Streptomyces have been found to be higherin soils of unreforested clear-cuts than in forestsoils and, within clear-cuts, higher in soils betweenislands of sprouting trees and shrubs than in soilsbeneath the islands.

Some of the more interesting research questionsrelating to successional dynamics relate to the roleof the belowground community. What triggers thebuildup of inhibitory microbes in some disturbedareas and how widespread is that phenomenon?How long can mycorrhizal fungi or beneficial rhi-zosphere bacteria persist in the absence of hostplants? How does the composition of the early suc-cessional community influence the composition ofthe soil microbial community and how does thatin turn influence the successional trajectory?

E. Threads of Continuity: Legaciesand Guilds

Scientists studying the recovery of plants and ani-mals following the eruption of Mt. St. Helens inMay 1980, found some surprises. Quoting fromJ. F. Franklin et al:

"Successional theory traditionally empha-sizes invading organisms or immigrants . . .but this script for ecosystem recovery couldbe played out at only a few sites (at Mt. St.Helens), as surviving organisms over most ofthe landscape provided a strong and wide-spread biological legacy from the preeruptionecosystem. In fact, essentially no posteruptionenvironment outside the crater was com-pletely free of preeruption biological influ-ences, although there were substantial differ-ences in the amounts of living and deadorganic material that persisted."

Within 3 years after the eruption, 230 plant spe-cies-90% of those in preeruption communi-

ties—had been found within the area affected bythe blast deposit and mudflows.

"Plant and animal species that live be-lowground or that have reproductive struc-tures belowground were the most likely sur-vivors . . . Fossorial mammals, such as thepocket gopher (Thomomys talpoides), and sub-terranean and log-dwelling invertebrates,such as ants, survived in the areas of deepestdeposits. The most obvious of survivingplants were 'weedy' species such as commonfirewood (Epilobium angustifilium), thistle(Cirsium sp.), pearly everlasting (Anaphalismargaritacea), various species of blackberry(Rubus sp.), and bracken fern (Pteridium aquili-num). These plants typically have perennatingstructures belowground and display vigorousshoot growth which can penetrate overlyingdeposits." (Franklin et al., 1985)

Webster defines legacy as "anything handeddown from . . . an ancestor." In an ecologicalcontext, legacies are anything handed down froma predisturbance ecosystem, including:

surviving propagules and organisms, such asburied seeds, seeds stored in serotinous cones,surviving roots and basal buds, mycorrhizalfungi and other soil microbes, invertebrates,and mammals;dead wood; andcertain aspects of soil chemistry and structure,such as soil organic matter, large soilaggregates, pH, and nutrient balances.

Most, if not all, legacies probably influence thesuccessional trajectory of the recovering system toone degree or another. That is clearly the case withsurviving plant propagules, which directly affectcomposition of the early successional community.Other legacies may shape successional patterns inmore subtle ways or perhaps not at all—this is arelatively new area of ecology that needs muchmore research. Despite the uncertainties, however,a variety of plausible mechanisms exist throughwhich legacies might influence succession.

1 50

FORESTS, COMPETITION AND SUCCESSION

Soil Biology

As already discussed, the composition of the soilbiological community following disturbance is alegacy that potentially influences the relative suc-cess of different plant species during succession.

Dead Wood

Dead wood has the potential to influence systemrecovery in several ways. Standing dead snags miti-gate environmental extremes within disturbedareas by shading and preventing excessive heat lossat night. Down logs within forests are centers ofbiological activity, including not only organ-isms of decay, but also roots, mycorrhizal hyphae,nitrogen-fixing bacteria, amphibians, and smallmammals. As Franklin et al. noted at Mt. St. Hel-ens, logs provide protective cover for their inhabit-ants during catastrophic disturbances. After distur-bance, down logs reduce erosion by acting asphysical barriers to soil movement and providecover for small mammals that disseminate mycor-rhizal spores from intact forest into the disturbedarea. The sponge-like water-holding capacity ofold decaying logs helps seedlings that are rootedin them survive drought.

Soil Aggregates and SoilOrganic Matter

Plants and associated microbes literally glue miner-als together to form soil aggregates, which are inti-mate mixtures of minerals, organisms, and nutri-ents. These aggregates are essentially little packagesof mycorrhizal propagules, other microbes, andnutrients that are passed from the old forest tothe new. Soil organic matter in general, whethercontained in aggregates or not (most is), providesa legacy of nutrients for the new stand. Dependingon its origin and stage of decay, soil organic mattercan either stimulate or inhibit plant pathogens.

Soil Chemistry

Different plant species may affect soil chemistryquite differently: by the particular array of nutrientsthey accumulate, their effect on soil acidity, or allel-ochemicals they release. To the degree these chemi-cal imprints persist after the plant is gone constitute

legacies which, in theory at least, could influencethe composition of the early successional com-munity.

Legacies interact with one another, creatingchains of direct and indirect influence. At Mt. St.Helens, for example, pocket gophers, which sur-vived below ground, facilitated the establishmentof some plant species by digging up soil buriedbeneath the ash. The exposed soil provided estab-lishing plants with nutrients and mycorrhizalspores, and its organic matter retained water duringdrought. As discussed previously, sproutingplants, and those growing from buried seeds, oftenbecome foci for the recovery of other plants. What-ever the reason, whether providing shelter, perchsfor birds that disseminate seeds, or food for mycor-rhizal fungi, pioneers that sprout from roots orburied seed constitute legacies that influence therecovery of other species within the system. Thelegacies provided by pioneers do not necessarilyaffect other species uniformly, hence can shape suc-cessional trajectories by favoring the establishmentof some species over others.

One hypothesis holds that species within a givencommunity form into guilds based on commoninterests in mycorrhizal fungi and perhaps otherbeneficial soil organisms. According to this view,early colonizers during secondary succession facili-tate subsequent colonization by members of thesame guild by providing a legacy of mycorrhizalfungi (and perhaps other beneficial soil organisms)and inhibit colonization by members of otherguilds because they provide no such legacy. Theguild concept may be extended to include animalsthat are tied into a relational network with plantsand their mycorrhizal fungi. For example, truffles,the belowground fruiting bodies of some speciesof mycorrhizal fungi, are the primary food sourcefor some small mammals, and the small mammalsspread spores of the fungi. In forests of the PacificNorthwest, the primary diet of the endangerednorthern spotted owl is the northern flying squirrel,whose primary diet is truffles. Hence the long-termwelfare of both flying squirrels and spotted owlsdepends on successional trajectories that lead backto trees that support truffle-producing mycorrhizalfungi.


G. Summary ofSuccessional Mechanisms

To summarize this section, patterns of species es-tablishment and changing dominance during suc-cession are likely to result from a mixture of ran-dom factors and complex interactions amongplants, animals, and microbes. To a certain degree,composition of a pioneer community is determinedby which species arrive first, which is, in turn, afunction of interactions between the nature andtiming of disturbance on the one hand and the earlysuccessional environment, which filters colonizersaccording to their adaptations, on the other. Bio-logical legacies facilitate recovery of the system andact to shape the new community in the image ofthe old. Dominance changes over time in part be-cause developmental patterns differ among spe-cies—some are fast growing and short-lived, othersare slow growing and long lived, and yet othersare somewhere in between—and in part because,for various reasons, some species establish moresuccessfully in a preexisting community than ina newly disturbed site. Interactions among plantspecies during succession often include elements ofboth facilitation and inhibition, and are influencedby complex interactions among climate, resourceavailability, and many nonplant species such as ani-mals, pathogens, mycorrhizal fungi, and other soilmicrobes. Moreover, the nature of interaction maychange with time: inhibition becoming facilitationor facilitation becoming inhibition. As a result, onemust proceed cautiously when judging interactionsamong plants during succession.

Glossary

Competition Interaction between individuals of the samespecies (intraspecific competition) or between differentspecies (interspecific competition) at the same trophiclevel, in which the growth and survival of one or allspecies or individuals are affected adversely. The compet-itive mechanism may be direct (active), as in allelopathyand mutual inhibition, or indirect, as when a commonresource is scarce. Competition leads either to the replace-ment of one species by another that has a competitiveadvantage or to the modification of the interacting speciesby selective adaptation (whereby competition is mini-

mized by small behavioral differences, e.g., in feedingpatterns). Competition thus favors the separation ofclosely related or otherwise similar species. Separationmay be achieved spatially, temporally, or ecologically(i.e., by adaptations in behavior, morphology, etc.). Thetendency of species to separate in this way is known asthe competitive exclusion or Gause principle.

Niche (ecological) Functional position of an organism inits environment, comprising the habitat in which theorganism lives, the periods of time during which it occursand is active there, and the resources it obtains there.

Sera! stage A phase in the sequential development of aclimax community.

Sere Characteristic sequence of developmental stages oc-curring in plant succession.

Succession Sequential change in vegetation and the animalsassociated with it, either in response to an environmentalchange or induced by the intrinsic properties of the organ-isms themselves. Classically, the term refers to the colo-nization of a new physical environment by a series ofvegetation communities until a final equilibrium state,the climax, is achieved. The presence of the colonizers,the pioneer plant species, modifies the environment sothat new species can join or replace the initial colonizers.Changes are rapid at first but slow to a more or lessimperceptible rate at the climax stage, composed of cli-max plant species. The term applies to animals (especiallyto sessile animals in aquatic ecosystems) as well as toplants. The characteristic sequence of developmentalstages (i.e., nudation, migration, ecesis, competition, re-action, and stabilization) is termed a sere.

Trophic level A step in the transfer of food or energywithin a chain. There may be several trophic levels withina system, for example, producers (autotrophs), primaryconsumers (herbivores), and secondary consumers (car-nivores); further carnivores may form fourth and fifthlevels. There are rarely more than five levels since usuallyby this stage the amount of food or energy is greatlyreduced.

Bibliography

Allaby, M., ed. (1994). "The Concise Oxford Dictionaryof Ecology." Oxford: Oxford Univ. Press.

Amaranthus, M. P., and Perry, D. A. (1989). Interactioneffects of vegetation type and Pacific madrone soil inoculaon survival, growth, and mycorrhiza formation ofDouglas-fir. Can. J. For. Res. 19, 550-556.

Amaranthus, M. P., Li, C.-Y., and Perry, D. A. (1990).Influence of vegetation type and madrone soil inoculumon associative nitrogen fixation in Douglas-fir rhizo-spheres. Can. J. For. Res. 20, 368-371.

Amaranthus, M. P., Trappe, J. M., and Perry, D. A. (1993).Soil moisture, native revegetation, and Pinus lambertiana


seedling growth, and mycorrhiza formation follow-ing wildfire and grass seeding. Restor. Ecol. Sept. 188-195.

Atsatt, P. R., and O'Dowd, D. J. (1976). Plant defenseguilds. Science 193, 24-29.

Borchers, J. G., and Perry, D. A. (1992). The influenceof soil texture and aggregation on carbon and nitrogendynamics in southwest Oregon forests and clearcuts.Can. J. For. Res. 22, 298-305.

Borchers, S. L., and Perry, D. A. (1990). Growth andectomycorrhiza formation of Douglas-fir seedlingsgrown in soils collected at different distances frompioneering hardwoods in southwest Oregon. Can. J. For.Res. 20, 712-721.

Bossema, I. (1979). Jays and oaks: An eco-ethological studyof a symbiosis. Behaviour 70, 1-117.

Bourliere, F. (1983). Animal specie diveristy in tropicalforests. In "Tropical Rain Forest Ecosystems" (F. B.Golley, ed.), pp. 77-91. New York: Elsevier.

Chanway, C. P., Turkington, R., and Holl, F. B. (1991).Ecological implications of specificity between plantsand rhizosphere micro-organisms. Adv. Ecol. Res. 21,121-169.

Clements, F. E. (1916). "Plant Succession, an Analysis ofthe Development of Vegetation," Pub. 242, pp. 1-512.Washington: Carnegie Institute.

Connell, J. H., and Slatyer, R. 0. (1977). Mechanismsof succession in natural communities and their role incommunity stability and organization. Am. Nat. 111,1119-1144.

Denslow, J. S., and Gomez Diaz, A. E. (1990). Seed rainto tree-fall gaps in a Neotropical rain forest. Can. J. For.Res. 20, 642-648.

Ehrenfeld, J. G. (1990). Dynamics and processes of barrierisland vegetation. Rev. Aquat. Sci. 2(3,4), 437-480.

Finegan, B. (1984). Forest succession. Nature 312, 109-114.Fleming, T. H., Breitwisch, R., and Whitesides, G. H.

(1987). Patterns of tropical vertebrate frugivore diversity.Annu. Rev. Ecol. Syst. 18, 111-136.

Franklin, J. F., MacMahon, J. A., Swanson, F. J., andSedell, J. R. (1985). Ecosystem responses to the eruptionof Mount St. Helens. Nat. Geogr. Res. Spring, 198-216.

Gleason, H. A. (1926). The individualistic concept of theplant association. Bull. Torrey Bot. Club 53, 7-26.

Gomez-Pompa, A., and Vazquez-Yanes, C. (1981). Succes-sional studies of a rain forest in Mexico. In "Forest Suc-cession, Concepts and Applications." (D. C. West,H. H. Shugart, and D. B. Botkin, eds.), pp. 246-266.New York: Springer-Verlag.

Hairston, N. G., Smith, F. E., and Slobodkin, L. B. (1960).Community structure, population control, and competi-tion. Am. Nat. 94, 421-425.

Hall, F. G., Botkin, D. B., and Strebel, D. E. (1991).Large-scale patterns of forest succession as determinedby remote sensing. Ecology 72, 628-640.

Harvey, A. E., Jurgensen, M. F., Larsen, M. J., and Gra-ham, R. T. (1987). Relationships among soil microsite,ectomycorrhizae, and natural conifer regeneration of oldgrowth forests of western Montana. Can. J. For. Res.17, 58-62.

Hibbs, D. E. (1983). Forty years of forest succession incentral New England. Ecology 64, 1394-1401.

Howe, H. F., and Smallwood, J. (1982). Ecology of seeddispersal. Annu. Rev. Ecol. Syst. 13, 201-228.

Hunter, A. F., and Aarssen, L. W. (1988). Plants helpingplants. BioScience 38(1), 34-40.

Janos, D. P. (1980). Vesicular-arbuscular mycorrhizae affectlowland tropical rain forest plant growth. Ecology 61,151-162.

Kauffman, J. B. (1991). Survival by sprouting followingfire in tropical forests of the eastern Amazon. Biotropica22, 219-224.

Lanner, R. M. (1985). Some attributes of nut-bearing treesof temperate forest origin. In "Attributes of Trees asCrop Plants" (M. G. R. Cannell and J. E. Jackson, eds.),pp. 426-437. England: Institute of Terrestrial Ecology.

Lawton, J. H., and Strong, D. R., Jr. (1981). Communitypatterns and competition in folivorous insects. Am. Nat.118, 317-338.

Lawton, J. H., and Brown, V. K. (1992). Redundancy inecosystems. In "Biodiversity and Ecosystem Function"(E.-D. Shulze and H. A. Mooney, eds.), Springer-Verlag.

MacArthur, R. H. (1964). Environmental Factors AffectingBird Species Diversity. American Naturalist 98, 387-397.1972. Geographical Ecology. Harper & Rowe, NewYork. 269 pp.

Marx, D. H. (1975). Mycorrhiza and establishment of treeson strip-mined land. Ohio J. Sci. 75, 288-297.

Maser, C., Trappe, J. M., and Nussbaum, R. A. (1978).Fungal-small mammal interrelationships with emphasison Oregon coniferous forests. Ecology 59, 799-809.

Nepstad, D., Uhl, C., and Serrao, E. A. (1990). Sur-mounting barriers to forest regeneration in abandoned,highly degraded pastures: A case study from Paragorni-nas, Para, Brazil. In "Alternatives to Deforestation"(A. B. Anderson, ed.), pp. 215-229. New York: Colum-bia Univ. Press.

Peet, R. K., and Christensen, N. L. (1980). A populationprocess. Vegetatio 43, 131-140.

Perry, D. A., Margolis, H., Choquette, C., Molina, R.,and Trappe, J. M. (1989b). Ectomycorrhizal mediation ofcompetition between coniferous tree species. New Phytol.112, 501-511.

Pickett, S. T. A., Collins, S. L., and Armesto, J. J. A.(1987a). A hierarchical consideration of causes and mech-anisms of succession. Vegetatio 69, 109-114.

Pickett, S. T. A., Collins, S. L., and Armesto, J. J. (1987b).Models, mechanisms and pathways of succession. Bot.Rev. 53(3), 335-371.

153FORESTS. COMPETITION AND SUCCESSION

Pickett, S. T. A., and Mconnell, M. J. (1989). Changingperspectives in community dynamics: A theory of succes-sional forces. TREE 4(8), 241-245.

Schisler, D. A., and Linderman, R. G. (1989). Influence ofhumic-rich organic amendments to coniferous nurserysoils on Douglas-fir growth, damping-off and associatedsoil microorganisms. Soil Biol. Biochem. 21(3), 403-408.

Schoener, T. W. (1989). Food webs from the small to thelarge. Ecology 70(6), 1559-1589.

Stenstrom, E., Ek, M., and Unestam, T. (1990). Variationin field response of Pinus sylvestris to nursery inoculationwith four different ectomycorrhizal fungi. Can. J. For.Res. 20, 1796-1803.

Stone, L., and Roberts, A. (1991). Conditions for a speciesto gain advantage from the presence of competitors. Ecol-ogy 72(6), 1964-1972.

Strong, D. R., Simberloff, D., Abele, L. G., and Thistle,A. B., eds. (1984). "Ecological Communities: Concep-tual Issues and the Evidence." Princeton: Princeton Univ.Press.

Tilman, D. (1985). The resource-ratio hypothesis of plantsuccession. Am. Nat. 125(6), 827-852.

Tilman, D., and Downing, J. A. (1994). Biodiversity andstability in grasslands. Nature 367, 363-365.

Valdes, M. (1986). Survival and growth of pines with spe-cific ectomycorrhizae after 3 years on a highly erodedsite. Can. J. Bot. 64, 885-888.

Forests, Competition and Succession' - Oregon State University

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