SPECIAL TOPIC: SCALING-UP IN ECOLOGY

Oswald J. Schmitz

Scaling from plot experiments to landscapes: studying grasshoppersto inform forest ecosystem management

Received: 27 February 2004 / Accepted: 10 January 2005 / Published online: 11 May 2005� Springer-Verlag 2005

Abstract Ecologists studying food web interactionsroutinely conduct their experiments at scales of 1–10 m2

whereas real-world landscape-level management prob-lems exist on scales of 106 m2 or larger. It is oftenasserted that the experimental tradition in ecology haslittle to offer to environmental management becausesmall scale empirical insights are not easily, if at all,translatable to the large scale problems. Small scaleexperiments are very local in nature and they are con-ducted in ways that tend to homogenize backgroundenvironmental variation. Real world management isconducted across vast landscapes. Managers routinelymust wrestle with complexity that is introduced by theheterogeneous structure of those landscapes and theyoften have limited recourse to do careful experimenta-tion. How then is empirical ecological science ever toinform landscape-level management? The solution tothis dilemma lies in arriving at good working concep-tualizations of ecosystem structure and function thatembody principles that are relatively scale independent.In this paper, the evolutionary ecological principle offoraging versus predation risk avoidance trade-offs isproffered as one central organizing conceptualization forplant-herbivore interactions across all systems. Theutility of this conceptualization is first illustrated bypresenting results of detailed experiments involving spi-der predators, grasshopper herbivores, and two classesof plant resources that afford grasshoppers differentialprotection from predators: nutritionally superior butrisky grasses and less nutritious but safer herbs. Thepaper then shows how the foraging versus predation riskavoidance conceptualization in the context of a ‘‘land-scape of fear’’ can be applied to manage large herbivore

impacts of forest regeneration following forest harvest-ing. I present results of landscape-scale experiments thatmediate predation risk of the herbivores throughmanipulation of safe habitat in order to enlist herbivoresto facilitate boreal forest mixed species regenerationthrough preferential foraging of certain woody species.

Introduction

Ecologists have been perennially engaged in seekingways to illuminate and solve environmental problemsthat result from human impacts on ecosystems (Worster1994). Indeed, numerous success stories have been cele-brated (e.g. Likens and Bormann 1974; Schindler 1974;Carpenter et al. 1987). Yet, as the scale and magnitudeof human impacts continues to increase, ecologists arecontinually challenged to find tractable solutions atthese ever increasing scales of impact. For example,large scale landscape disturbance consequent to land useclearing, intensive forest management or climate changecan disrupt linkages among species in several trophiclevels propagating a host of direct and indirect effectsthat may require decades to fully manifest themselves(Fig. 1). It is often difficult and expensive to conductfully replicated factorial experiments with sufficient sta-tistical power to explore precisely alternative hypothesesabout the causal drivers of trophic dynamics at suchscales (e.g., Sinclair et al. 2000; Krebs et al. 2001). So,ecologists usually try to extrapolate insights about thenature and strength of trophic interactions from studysystems that can be made to conform more closely to thenorms of experimental research (i.e., studies havinggood control, replication, and high precision [Hairston1990]). By necessity, such research is conducted withinplots or enclosures on spatial scales of meters to hectaresover periods of weeks to months (Fig. 1). This mis-match of scale makes the transfer of scientific insightsto management somewhat challenging because the

Communicated by Craig Osenberg

O. J. SchmitzSchool of Forestry and Environmental Studies andDepartment of Ecology and Evolutionary Biology,Yale University, 370 Prospect Street,New Haven, CT, 06511 USAE-mail: oswald.schmitz@yale.edu

Oecologia (2005) 145: 225–234DOI 10.1007/s00442-005-0063-y

dynamics of small organisms, confined within smallplots, may be quite different from dynamics that involvelarge organisms that move freely over landscapes(Kareiva and Anderson 1988; Morales and Ellner 2002).The question that then emerges is this: How might weuse small-scale experimental research to inform man-agement that operates on large spatial scales?

I begin to answer this question using a case study ofmy own attempts to extrapolate research findings inNew England meadows to management of boreal for-ests. For both systems, the fundamental challenge is toknow whether or not trophic interactions among species(top-down control) or plant-soil interactions (bottom-upcontrol) is the dominant driver of species compositionand productivity of the ecosystems. It may seem to beinconceivable that insights about ecosystem functionderived from experiments involving spiders, grasshop-pers and herbaceous plants can be applied directly toguide the management of forest ecosystems comprised ofwoody plants and widely ranging mammalian predatorsand herbivores. I argue that this is merely a technicalityarising from a strict taxonomic view of the differentsystems. From a functional standpoint, both meadowand boreal systems can be viewed as systems of inter-acting carnivores, herbivores and plants (Fig. 2) makingthe exact spatial scale and taxonomic composition ofeach system only proximally relevant. The ability to scalefrom one system to another, in turn, rests on identifyingfundamental effects or mechanisms: effects that are evi-dent among systems regardless of spatial scale (Petersenet al. 2003).

In the following, I provide an overview of small-scaleexperimental research conducted within plots in a NewEngland meadow and show how I have arrived at aworking conceptualization of the mechanism drivingtrophic interactions in this system. I next detail the

reasoning used to claim that this should be considered afundamental mechanism. I then show how applicationof the mechanistic understanding can lead to productivechange in forest management.

Small scale research: mechanisms of trophicinteractions in a New England meadow system

Over the past 10 years, I have been conducting researchon trophic interactions among predators, herbivores andplants in a New England meadow ecosystem. Specificnatural history details of that system and an overview ofthe various experiments and protocols used are pre-sented in Schmitz (2003, 2004).

There is considerable plant, herbivore and carnivorespecies complexity in the ecosystem (Schmitz 2004).Nevertheless, the key observation is that there are twofairly distinct insect herbivore feeding guilds (sap-feeders

Fig. 2 Common conceptualization of interactions among domi-nant species in two ecosystems. On the left is an old-field ecosystemcomprised of the hunting spider predator (Pisaurina mira), thegeneralist grasshopper herbivore (Melanopuls femurrbrum), andtwo distinct classes of herbaceous plants: grasses and herbs. On theright is a boreal forest ecosystem comprised of wolves (Canis lupus),the generalist herbivores such as moose (Alces alces) and twodistinct classes of trees: deciduous aspen (Populus tremuloides) andconiferous white spruce (Picea glauca)

Fig. 1 Graphical representation of the temporal scale and spatialextent (depicted as area defined by two length dimensions) at whichbasic ecological research and management operate. The lower leftcorner depicts small plots within which small-scale, well replicatedfield experiments are conducted. It is possible to scale up resultsfrom plots to the field level, as depicted by the plot level grid nestedwithin the whole field level grid. Ecologists encounter a mismatchof scales when translating insights from plot experiments at thefield level to management at the landscape level because ofdifference in spatial and temporal extent of the respective systemsand differences in focal taxa. After Holling (1992)

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and leaf-chewers) present each year. These guilds mayhave widely different effects on plant species because oftheir feeding ecology and the degree to which predatorsinfluence their abundance. Top predator effects couldtransmit through the herbivore guilds to influence theabundance of plants and ecosystem function in severalcontingent ways. First, neither guild could have any neteffect on ecosystem structure and function, in the pres-ence or absence of predators, in which case oneconcludes that the field system is entirely bottom-upcontrolled. Second, strong top-down effects might betransmitted through only one feeding guild but not theother. In this case, one of the feeding guilds will play adominant role in shaping ecosystem structure andfunction. Finally, top-down effects could be transmittedthrough both feeding guilds. However, those effectscould be antagonistic, i.e., one guild could influence aparticular group of plant species and the other guildinfluences another group. If groups of plants competefor resources then the effects due to one feeding guildcould be reversed by the other feeding guild. In this case,there may be no net measurable effect of top-downmanipulations on the ecosystem in the aggregate.However, it would be incorrect to conclude that thesystem was bottom-up controlled in this case. Finally,top-down effects might be transmitted through bothfeeding guilds in the same way. Hence, the top-downeffects involving one feeding guild could synergisticallyenhance those of the other feeding guild.

Field research systematically addressing these con-tingencies (summarized in Schmitz 2004) revealed thatthe structure and short-term dynamics in this system is

largely determined by top-down interactions among fourspecies: the hunting spider Pisaurina mira, the grass-hopper herbivore Melanoplus femurrubrum, the grassPoa pratensis, and the competitive dominant herb Soli-dago rugosa. M. femurrubrum grasshoppers eat both P.pratensis and S. rugosa. But, they prefer P. pratensis inthe absence of predators and can inflict considerabledamage to it (Beckerman et al. 1997; Schmitz et al. 1997;Schmitz and Suttle 2001). Mortality risk caused bypredator presence forces grasshoppers largely to foregofeeding on grass and to seek refuge in and forage onleafy S. rugosa, thereby causing high damage levels tothis species (Beckerman et al. 1997; Schmitz 1998). Thus,P. mira spiders exert strong control by having a positiveindirect effect on P. pratensis abundance and a negativeindirect effect on S. rugosa abundance.

This insight leads to predictions about long-term top-predator effects on plant diversity and productivity inthis field system. In particular, the dominant interactionshaping the structure of the ecosystem is a behavior-mediated interaction involving P. mira spiders, M.femurrubrum grasshoppers, P. pratensis grass, and S.rugosa herb. The emerging hypothesis is that P. mirashould have a strong diversity-enhancing effect on herbspecies via a shift in plant species abundance (an even-ness effect) caused by M. femurrubrum grasshoppersswitching from feeding on P. pratensis to feeding heavilyon the competitively dominant herb S. rugosa. Over thelong term, such competitive release should cause manyof the 18 other less productive herb species to prolifer-ate. This amounts to a multi-trophic level variant of theclassic keystone predation hypothesis (Paine 1966;

Fig. 3 Consequences of 3-yearsof sustained meadow trophiclevel manipulations on the plotarea covered by Poa pratensisand Solidago rugosa. Positiveand negative indirect effects ofpredators on a P. pratensis andb S. rugosa mediated bygrasshopper antipredatorbehavior. Effect of shifts indominant plant speciesabundance on average yearly cplant productivity and d plantspecies evenness. Values shownare mean and 1 SE (n=10replicate plots). Bars withdifferent lower case lettersindicate significant differencesbased on a Tukey test atP<0.05 following aRandomized block ANOVA.Treatments: 1 level=plantsonly, 2 level=plants andherbivores, 3 level=plants,herbivores, and carnivores.After Schmitz (2003)

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Leibold 1996) in which P. mira acts as an indirectkeystone predator (Schmitz 2003).

This hypothesis was tested with a multiyear (1999–2001) field experiment that systematically manipulatedthe number of trophic levels in 2·2 m open field plotsand measured the response of each manipulation onplant diversity and productivity. The experiment con-sisted of two treatments (a predator exclusion and apredator and herbivore exclusion) and a control (naturalfield state) replicated ten times using a randomizedblocks design (Schmitz 2003). The experiment revealedsignificant, cumulative treatment effects on % P. prat-ensis cover and % S. rugosa cover (Fig. 3). Three yearsof predator exclusion resulted in significantly lower P.pratensis and S. rugosa cover relative to the one-trophiclevel, plant-only treatment (Schmitz 2003). Sustainedpredator presence (three trophic level treatment) resultedin increased P. pratensis cover and decreased S. rugosacover relative to the predator exclusion treatment (Sch-mitz 2003). Manipulation of trophic structure alsocaused significant shifts in plant species evenness (Sch-mitz 2003). Evenness was significantly higher in threetrophic level plots than in either the two-trophic level orone trophic level treatments (Fig. 3). In addition, therewas a significant decrease in estimated plant productivitywith increasing number of trophic levels in both sam-pling periods, owing largely to the suppression of thehighly productive, and competitive dominant plant S.rugosa (Fig. 3).

Fundamental mechanism

Despite the high species richness in all trophic levels inthis system, top-down effects appeared to transmit fairlylinearly down a chain comprised of a dominant predatorand herbivore species to the plant species. The emergingmechanistic insight from the highly replicated experi-ment was that the top predator controlled the structureand functioning of the natural ecosystem by causing thegeneralist grasshopper to trade-off foraging with hidingto avoid predation risk. This trade-off behavior alteredthe ability of a highly competitive plant species todominate the meadow ecosystem.

Evolutionarily, any species that is subject to preda-tion risk ought to respond flexibly to balance fitnessgains from foraging against fitness losses from predationrisk (Mangel and Clark 1988; Lima and Dill 1990; Lima1998). There is evidence that species do respond topredation risk (Lima 1998). This reasoning then leads tothe identification of a fundamental mechanism drivingtrophic interactions that can transcend spatial andtemporal scales, and taxa. In essence, one could viewecological systems as ‘‘landscapes of fear’’ (Brown et al.1999) in which species trade-off foraging against beingconsumed by their predators. Such a disarmingly simpleconception has far-reaching implications for predictingtrophic interactions among systems (Abrams 1984, 1992,1995; Werner and Peacor 2003; Schmitz et al. 2004). In

the present case, understanding the motivation for thetrade-off by the middle herbivore species in the food webis the core knowledge that should facilitate the appli-cation of scientific insights from the meadow system tothe boreal forest.

Scaling the insight: management of boreal forestecosystems for diversity and productivity

The dynamics of boreal forest ecosystems are driven bymany factors including fire, insects and mammalianherbivores (Shugart et al. 1992). A large body of evi-dence shows that among those factors, interactions be-tween large mammalian predators, herbivores andplants may play an important role in shaping ecosystemstructure and function (McLaren and Peterson 1994;Pastor and Naiman 1992; Krebs et al. 2001; Post et al.1999; Pastor and Cohen 1997; Niemela et al. 2001;Sinclair et al. 2000).

An important, large-scale (25 ha or larger) distur-bance in boreal systems is forest harvesting for timberand pulpwood. A limiting factor in long-term sustain-ability of boreal forests, and a central challenge to forestecosystem management, is a forest’s capacity to regen-erate following harvesting. My research has been part ofa collaborative effort (P.M.S. Ashton, B. Larson, R.Nesdoly, O.J. Schmitz, unpublished) aimed at identify-ing ecologically compatible ways of regeneratingsouthern boreal mixed-wood forests—forests dominatedby aspen (Populus tremuloides) and white spruce (Piceaglauca)—following harvesting in northwestern Sas-katchewan, Canada. Below, I provide a brief sketch ofthat research to demonstrate proof-of-scaling-concept.

Southern boreal mixed-wood is the most economi-cally important to the forest industry and its successfulregeneration is the most problematic management issuefor many companies.

Historically, attempts by the forest industry toregenerate boreal mix-woods after harvesting have lar-gely met with failure because aspen, a competitivedominant, suppresses regeneration of spruce (Yang1991) leading often to aspen monocultures with lowunderstorey plant species diversity.

One potential reason for the failure to regeneratemixed wood forests is that management has not devel-oped the appropriate conceptualization of the functionalecosystem. The traditional view, signified by the man-agement practice of large-scale harvesting, extensive sitepreparation after harvesting followed by intensivereplanting of spruce seedlings, is that forest ecosystemstructure and function is driven largely by bottom-uplocal soil-plant interactions. There is some recognitionthat top-down effects might also play a role, but it islargely viewed that they lead to undesirable outcomes.Specifically, ecosystems are viewed as having two func-tional trophic levels: herbivores and plants. In thisconception, herbivores damage regeneration so theirpopulation numbers should be reduced to prevent

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regeneration failure (Alverson et al. 1988; Tilghman1989; Sullivan et al. 1990; Anderson and Katz 1993;Andren and Angelstam 1993).

I argue that extending the conception of an ecosystemby considering three functional trophic levels in thecontext of landscapes of fear offers ways to utilize eco-logical interactions among species, rather than intensivemechanical site preparation or herbivore exclusion, tocreate environmental conditions that foster mixed woodregeneration.

In forest ecosystems, large herbivores such as white-tailed deer Odocoileus virginianus, and moose Alces al-ces, like grasshoppers, respond to predation risk byseeking refuge habitats or shifting the spatial location inwhich they forage (Edwards 1983; Andren and Angel-stam 1993; White et al. 2001; Lingle 2002). In the studysystem, both herbivore species prefer aspen (O.J. Sch-mitz, unpublished). So, each species conceivably couldreduce the abundance of the competitive dominant andthus release spruce to regenerate. However, forest har-vesting, especially clear-cutting, fragments the forestlandscape in ways that have a profound influence ofherbivore foraging. In particular, large openings in-crease the vulnerability of large herbivores such as deer,and moose to predation by both wolves Canis lupus andhumans. Consequently, these herbivore species selecthabitats to decrease risk, and accordingly have weak ormuch localized impacts on plant species (Andren andAngelstam 1993). If they do forage in the open riskyareas, they tend to be less selective owing to heightenedvigilance (Molvar and Bowyer 1994). Moreover, theytend to congregate in higher densities in riskier areasleading to increased frequency of antagonistic interac-tions, which in turn reduces foraging efficiency (Molvarand Bowyer 1994). Thus, management can create con-ditions that impact several aspects of large herbivorebehavior that accordingly enables aspen to proliferateon the landscape.

I now illustrate how managing forests in ways thatalter herbivore foraging preferences through predationrisk (landscapes of fear) can lead to management strat-egies that successfully regenerate boreal mixed woods.

We examined herbivore-mediated effects in twostages by enlisting management as a scientific experi-ment (sensu Walters and Holling 1990; Sinclair 1991).The first stage involved stand-level experiments aimed atunderstanding herbivore-mediated plant–plant interac-tions. The second stage involved experiments thatmanipulated landscape-scale ‘‘fear’’ to alter habitat useby herbivores.

Stand-level experiment: herbivore mediationof aspen-spruce competition

Herbivores may single-handedly shape communitystructure and function via direct interactions with theirplant resources. There are two ways of viewing that role.The traditional view holds that herbivores are damaging

to regeneration. An alternative view recognizes thatplant species compete for resources and that herbivoresshape the outcome of that interaction by preferentiallyfeeding on competitively dominant species (Louda et al.1990; Huntly 1991: see De Steven 1991 and Schmitz andSinclair 1997 for focus on tree species). Indeed, theorysuggests that in boreal forests, the successional pathwayduring stand development (and eventual composition ofspruce or aspen in the overstory) may be quite differentwhen herbivores are present than when they are absent(Pastor and Naiman 1992). Herbivores may have strongdirect effects by selectively feeding on plant species butthe trajectory taken during stand development is largelyan indirect consequence of herbivores mediating plant-plant interactions (Brandner et al. 1990). Theory (Pastorand Naiman 1992; Pastor and Cohen 1997) also suggeststhat in boreal systems, the effects of herbivores on thesuccessional trajectory taken by a stand may persist longafter herbivory has stopped (when trees have grownbeyond the herbivore’s reach).

In partnership with a local forest management com-pany, we established and monitored a large-scale fieldexperiment between 1997 and 2000. We studied standdevelopment in an aspen-spruce mixed wood forestwithin sites that had similar soil type, successional stageand fire disturbance origin. The experiment was initiatedby carefully harvesting all timber and vegetationexceeding 2.5 cm diameter-at-breast height (dbh) withinfour replicate 340·80 m strips (�2.7 ha) whose longaxes are oriented in an east-west direction. Harvestingwas done using a mechanical harvester that minimizedimpacts to the ground story vegetation.

The east-west orientation of the strips served twopurposes. First, the width of this gap resembles a largenatural canopy disturbance like that of several tree-falls(Ashton and Larson 1996). Second, boreal herbivoresmay differentially browse plant species at different dis-tances from the edge of a strip owing to predation risk(reviewed in Andren and Angelstam 1993). However,sun-exposed woody plants tend to have higher nutri-tional quality than do plants growing in shadier condi-tions (Robbins 1983). Thus there may be a predation-risk/food value trade-off that may cause variation in thestrengths of top-down control across an opening.

We crossed a silvicultural treatment, commonly em-ployed by management, with a herbivore exclusion in a2·2 design. Treatments were imposed on 5·20 m plots.Each treatment was randomly assigned to each transectin each of the four strips. The north-south orientedtransects run across the width of each strip. The treat-ments were imposed in three plot locations in eachtransect: north edge, center and south edge to controlfor confounding effects of plot location on plant pro-duction.

We compared with an unmanipulated control a sil-vicultural treatment that emulated a ground story dis-turbance used by the forest industry to prepare sites forplanting. The control preserved all vegetation below2.5 cm dbh thus releasing advanced regeneration (full

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plant competition, hereafter C+). The treatment was amechanical eradication of all aboveground vegetationbelow 2.5 cm dbh. This removed advanced regeneration(removal of above-ground competition, hereafter C�) butreleased root suckering of aspen. In each 5·20 m plot,we randomly selected one half-side (split plot design) inwhich we planted nine spruce seedling in each of six,2·2 m subplots. The other half-side was left as a naturalregeneration control.

The herbivore treatments were ultimately designed toseparate smaller mammal (snowshoe hare, Lepus amer-icanus) effects from large mammal (moose and deer)effects, but we did not detect differential effects of theselarge and small mammals during the course of theexperiment (O.J. Schmitz, unpublished). Thus, I describehere treatments that manipulated mammalian herbivorygenerally. The control (hereafter M+) allowed herbiv-orous mammals full access to the 5·20 m plots. Thetreatment excluded all mammals (hereafter M-) fromreplicate 5·20 m plots using 2.5 m high 5·5 cm gridpage wire fencing. We were concerned that the largeexclosure pens themselves might deter herbivores fromentering the experimental area. We therefore cut com-panion 80·340 m strips 80 m adjacent to each experi-mental strip and left them unmanipulated(umanipulated control strips). We used the same criteriafor site selection as those for the experimental strips. Wethen conducted browse surveys along 1.5 m-wide swaths

in eight transects running the full 340 m length of thestrips in the experimental and unmanipulated controlstrips (in experimental strips, exclosure pens did not fallalong a transect line). We did not find any significantdifferences in browsing (number of stems browsed perm2) between experimental and control strips at differentdistances along the sampling transects (All t-tests,P>0.65).

We measured two woody plant response variablesand one total (woody and herbaceous) plant response inthe experiment. We measured aspen stem density (ameasure of abundance: note, spruce density was fixed byplanting seedlings) and aspen and spruce height growth(an index of productivity) by subdividing each 5·20 mplot into twelve, 2·2 m subplots and then systematicallysampling every other plot. Height growth was measuredusing a meter stick. We measured the maximum heightof each clonal clump of aspen within each subplot(usually there were 2–3 clumps per subplot). To avoidpseudoreplication, we aggregated all subplot measuresto a plot average. We estimated stem density by count-ing all emergent stems in sampling subplots and thenscaling the subplot total to the entire plot to estimateplot density. In the same 2·2 m subplots, we counted allplant species to estimate plant species richness.

Aspen and spruce plants grew differently (All Ran-domized Block Anova’s, P<0.05, df=3,9) when ex-posed to natural conditions (herbivory and competition)

Fig. 4 Effect of stand-level manipulations on a aspen density, baspen height growth, c spruce height growth and d understoreyplant species richness. The experiment included the followingtreatments: C-, M-plant competition mediated mechanically andmammalian herbivores excluded; C+, M-plant competition notmanipulated and mammalian herbivores excluded; C-, M+ plantcompetition mediated mechanically and mammalian herbivores not

excluded; and C+, M+ plant competition not manipulated andmammalian herbivores not excluded (natural control state). Thedark bars represent plant responses along edges, lightly shaded barsrepresent plant responses in the center of the harvested strips. Barswith different lower case letters indicate significant differences basedon a Tukey test at P<0.05 following a Randomized blockANOVA. Values shown are mean and 1 SE (n=4 replicate plots)

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than under any of the other classical management-typetreatments, especially ones which excluded the herbi-vores (Fig. 4). The qualitative pattern of effect wassimilar in edge and in open plots. Tukey tests revealedthat aspen stem density and height growth was signifi-cantly lower in natural plots than in managed plots.Alternatively, spruce height growth was significantlyhigher in natural plots than in managed plots. Thiscombined evidence indicates that after 4 years, herbi-vores were capable of mediating the abundance of aspenand spruce in desired ways much better than the moretraditional management systems (i.e., mechanical sitemanipulation and herbivore exclusion). There was also aslight tendency for plots exposed to herbivory to havehigher understorey plant species richness than plots thatexcluded herbivores at both edge and center locations(Fig. 4, both Randomized Block Anova’s, P<0.09,df=3,9, followed by Tukey Tests).

The stand level experiment revealed that mammalianherbivores are capable of mediating plant speciesabundance, productivity, and richness in ways that arepredicted by a priori principles of trophic interactions.The limitation of this experiment, however, is that itremains uncertain if herbivore impacts uniformly scaleto the landscape level where clear-cut harvesting rou-tinely removes timber within 25–100 ha areas. Such ascale is at least an order of magnitude larger than thestrip cuts. Herbivores may not affect plants uniformlyacross such vast open spaces because of predation risk.Feeding in the middle of such large openings requiresthat herbivores move long distances away from escapecover afforded by the intact forest stands surroundingthe clear-cuts (Rothley 2002). Herbivores will insteadforage near the perimeter of the harvested area, despitethe high nutritional value of browse in the open,leading to exponential declines in browsing impactsfrom the edge to the center of the harvested area(Drolet 1978; Tomm et al. 1981; Andren and Angel-stam 1993). Such trade-off behavior will cause an un-even pattern of regeneration. Mix-wood regenerationwill proliferate around the perimeter of the harvestedarea; aspen monocultures will proliferate in the center.One potential solution then is to harvest the landscapein ways that alter the herbivores’ perceived risk ofpredation.

Landscape-level experiment: predation risk-mediatedherbivore use of harvested areas

Use of harvested areas by large mammalian herbivoresvaries with the size, shape and distribution of cut-overareas on the landscape (Tomm et al. 1981; Rothley2002) as well as with the spatial pattern of overstoreyremaining in residual patches (Forman and Godron1981; Hunter 1990; Rothley 2002). Changing land-scape-scale patch structure should thus cause deer tochange their use of the land matrix. Specifically,altering the degree of openness of harvested areas may

be one way to mitigate the risk of predation theyperceive.

Our goal during this stage of the research was to testwhether or not the herbivores could be drawn out to thecenter of the harvested areas and thus mediate aspen-spruce interactions more evenly across the harvestedareas. We therefore compared herbivore foraging im-pacts under two harvesting treatments relative to anunharvested control. The first harvesting treatment wasa classic overstorey removal (COR) or clear-cut. Thesecond treatment was a new harvesting strategy called apartial overstorey removal (POR) that retained habitatpatches within a harvested area. In a POR strategy,10–20 small patches (�1 ha) of uncut timber are leftthroughout the middle of a harvested area (�50–100 ha). The patches are arrayed to reduce the distancebetween open feeding areas and escape cover, therebyforeshortening the herbivore’s perception of predationrisk in the center of a harvested area.

We selected three harvesting areas and matched, ineach area, a COR, POR and control site that had similarsite conditions (as described in the Stand-level experi-ment section above). Harvested areas ranged in sizefrom 55 ha to 90 ha. We delineated a 250·250 m sam-pling grid that extended from the edge to the center ofeach treatment area or from the edge/forest margin tothe interior forest in the control. As an index of largeherbivore spatial use and impacts, we sampled thenumber of stems browsed along the entire length of five,1·250 m transects spaced at 50 m intervals within eachsampling grid.

This experiment revealed that browsing activity bylarge herbivores in the patch retention (POR) areas wassimilar to unharvested controls (Fig. 5). Browsingactivity was fairly uniform from the edge of the patchestoward the center. However, herbivore activity in tra-ditional clear cuts (COR) was quite different than ineither the POR or control. Browsing activity rapidlydeclined a short distance from the perimeter into theharvested area and remained low out to the center(Fig. 5), consistent with earlier findings (Drolet 1978;Tomm et al. 1981; Andren and Angelstam 1993). Itwould appear that harvesting the landscape in ways thatprotect values sought by herbivores (food and escapecover) will result in more even use of the harvestedlandscape. Thus, management can enlist the fear-factorassociated with herbivore habitat selection to regenerateforest stands in desired ways.

Discussion

The aim of this paper was to illustrate how one mightsuccessfully apply insights from field research that isnormally conducted at scales of 1–10 m2 to landscape-level management that occurs on scales of 106 m2 orlarger. The success of this application rests on derivingan appropriate conceptualization of species interactionswithin an ecosystem and then identifying a scaling

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principle (i.e., fundamental effect or mechanism [Peter-sen et al. 2003]) that transcend spatial scales. In thepresent case, that conceptualization was simply viewingan ecosystem as an interacting set of dominant carni-vore, herbivore and plant species (Fig. 2) whose inter-actions are mediated by herbivore trade-offs to balanceforaging against avoiding contact with predators. At thesame time, scaling from the meadow research to forestmanagement did not involve, and indeed could not in-volve, an explicit consideration of space.

For example, grasshoppers in the small scale researchavoided predators by switching from locations withhighly nutritious resources to locations containing safeplants. This resource switching mediated competitiveinteractions among plants in predictable ways. But, fromthe grasshoppers’ perspective, grasses and herbs aresimultaneously separate foods and habitats. Large her-bivores such as moose and deer, on the other hand,encounter both aspen and spruce plants fairly evenlywithin the same habitat. In this case, food resources arenested within a single habitat. But, they still mediatecompetitive interactions among the plants throughpreferential foraging. Escape cover is afforded to largeherbivores by an altogether different habitat structurewhich determines the degree to which the herbivoresmediate competitive interactions in large openings.Thus, it is the foraging-predation risk trade-off mecha-nism that is preserved across spatial scales and taxa. Thespecific way each herbivore species uses resources andhabitats to resolve the trade-off comes down to the oldidea of environmental grain (Hutchinson 1965; Pianka1978, see also Abrams and Schmitz 1999).

There is nothing novel about the individual elementsof the forest management research describe here. Theecology of aspen and spruce regeneration, aspen-spruceinteractions, and herbivore damage on forest plants iscertainly well known in the silviculture literature.Moreover habitat selection and foraging by largemammalian herbivores is well described in the wildlifemanagement literature. It is the way the elements arepackaged in a unifying conceptualization of ecosystemfunction that differs from that presented in previousmanagement literature. This is because forest manage-ment and wildlife management have often operated atcross-purposes.

The goal of forest management and harvesting typi-cally is to maximize the production of wood fiber. Thegoal of wildlife management is to manage habitat inways that maximize deer and moose species production.Accordingly, forest harvesting has been viewed as anti-thetical to wildlife management goals. Harvesting hasfragmented the forest landscape and it has introducedanthropogenic disturbances to the extent that habitatquality has become unsuitable for species to remainwithin the ecosystem. In contrast, successful wildlifemanagement creates conditions—high abundances ofherbivores—that are viewed by forest management asdetrimental to forest regeneration. The conceptualiza-tion presented here integrates those factors that have inthe past been investigated separately and often withoutproperly controlled experiments. Such integration showshow forest ecosystem management can enlist wildlifehabitat management that mediates predation risk andthe capacity of herbivore species to damage vegetationselectively as strategic management tools. The inspira-tion for applying this idea, however, comes from de-tailed, fully replicated mechanistic examination of small-scale systems comprised of arthropod predators andherbivores and plants.

Our ability to develop tools that facilitate reliableapplication of basic ecological insights to managementrequires that we develop conceptualizations that accountfor the important links and feedbacks among bioticcomponents of ecosystems as a whole. The ‘‘landscapeof fear’’ concept is one such candidate. Indeed, it is alsobeing applied to understand ecosystem dynamics atother spatial scales, involving other taxa including elk(Cervus canadensis) impacts on woody vegetation in theYellowstone Park ecosystems before and after wolfreintroduction (Laundre et al. 2001; Ripple et al. 2001,2003), and interactions among lynx (Lynx Canadensis),snowshoe hare, and woody vegetation in northern bor-eal ecosystem (Krebs et al. 2001). And so, creativesolutions to emerging environmental problems can bedeveloped by identifying fundamental mechanisms ofspecies interactions that transcend spatial scales of eco-logical organization and function.

Acknowledgments I wish to thank M. Ashton, B. Larson, R.Nesdoly, O. Ovadia, E. Post D. Skelly, and M.Urban for discussionand comments on various aspects of this work. The old-field eco-system research was supported by NSF grants DEB-9508604 and

Fig. 5 Effects of landscape-scale forest harvesting strategy on largeherbivore habitat use measured as browsing impacts along agradient from forest edge to the center of the cut-over area.Treatments are classic overstorey removal (COR), partial oversto-rey removal (POR) and unharvested control (CTRL). Values aremean and 95% CI

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DEB-0107780. The boreal ecosystem research was supported byMISTIK Management Ltd.

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