EARLY PRIMARY SUCCESSION ON MOUNT ST. HELENS: IMPACT … · Stem-boring, leaf-mining, and...

191

Ecology, 83(1), 2002, pp. 191–202q 2002 by the Ecological Society of America

EARLY PRIMARY SUCCESSION ON MOUNT ST. HELENS:IMPACT OF INSECT HERBIVORES ON COLONIZING LUPINES

JOHN G. BISHOP1

Department of Botany, University of Washington, Seattle, Washington 98195-5325 USA

Abstract. Lupinus lepidus var. lobbii, the earliest plant colonist of primary successionalhabitats at Mount St. Helens, can dramatically influence successional rates and ecosystemdevelopment through N fixation and other facilitative effects. However, 15 yr after theeruption, lupine effects remained localized because high rates of population growth in newlyfounded patches (l 5 11.2, 1981–1985) were short lived (l 5 1.51, 1991–1995), despitewidespread habitat availability. To investigate this paradox, I examined 60 colonizing lupinepatches, ranging from low-density patches at the edge of the expanding lupine population,to high-density patches in the population core, including 41 patches created in 1992. Sur-vival, reproduction, and herbivory (for a subset of plants and years) were measured on;12 000 plants for up to 5 yr (1991–1995).

Stem-boring, leaf-mining, and seed-eating lepidopterans and anthomyiid flies, feedingin edge patches and in low-density margins of core patches, strongly affected edge patchdemography, but not that of central core areas. For example, in 1994–1995, 77% of edgeplants were afflicted by tortricid stem borers vs. 24% in the core, and from 1993–1995gelechiid leafminers infested 68% of plants in the youngest edge patches, vs. only 8% atthe core. Associated adult mortality was 88%, compared to ;30% when absent. Seedpredators consumed 36% (range 4–92%, 1991–1995) of seeds in both core and edge patches,with seed loss negatively correlated with seedling number the following year. In contrastto edge patches, resource-dependent seedling mortality appears to govern short-term dy-namics in high-density core areas. In conclusion, edge region herbivore effects can accountfor the observed 7.5-fold difference in l between patches founded 10 yr apart. Locally,increased lupine mortality creates access to high-quality sites, facilitating succession, butat larger spatial scales diminished population growth is likely to retard facilitation andsuccession.

Key words: colonization; demography; facilitation; herbivory; invasion; legume; Lepidoptera;Lupinus; Mount St. Helens (Washington, USA); primary succession; seed predation.

INTRODUCTION

For many colonizing plants, establishment in pri-mary successional habitats depends upon ameliorationof physical conditions, either abiotically or through thefacilitative effect of other species. For example, studiesof soil development conclude that nitrogen is in shortsupply early in primary succession, a deficiency thatappears especially striking on soils deriving from vol-canic ash and lava flows, where N may be undetectableinitially (Vitousek et al. 1987, del Moral and Bliss1993). In such systems, the presence of nitrogen-fixingspecies is capable of radically altering the pace andpattern of ecosystem and community development(Clements 1916, Connell and Slatyer 1977, Marrs etal. 1983, Vitousek et al. 1987, Vitousek and Walker1989). Under the facilitative model of succession, therates of population increase and spatial spread of ni-trogen-fixing species critically affect the rate of suc-

Manuscript received 1 November 1999; revised 27 May 2000;accepted 30 June 2000; final version received 15 January 2001.

1 Present address: School of Biological Sciences, Wash-ington State University, 14204 NE Salmon Creek Avenue,Vancouver, Washington 98686 USA.E-mail: [email protected]

cession, and it is therefore of interest to understand thefactors that control the population dynamics of thesespecies.

Consumers of nitrogen-fixing species, e.g., herbi-vores, may positively impact rates of succession byliberating resources, or they may decrease rates by de-mographically preventing facilitation. Most studies ex-amining consumer effects on primary succession in-volve marine systems, where inhibition and tolerancemodels of succession may be more important than fa-cilitative models (Lubchenco and Gaines 1981, Farrell1991, Sousa and Connell 1992, Hixon and Brostoff1996). These studies provide examples of consumer-mediated deceleration, acceleration, and deflection ofsuccessional rates and trajectories (Hixon and Brostoff1996). The only study demonstrating herbivore effectson terrestrial primary succession is that of Bach (1994),showing that on lake shore sand dunes, chrysomelidbeetles specializing on willow decreased host abun-dance, thereby changing community trajectories. Cur-rently, herbivores are not considered an influential fac-tor in terrestrial primary succession (e.g., Walker andChapin 1987, del Moral and Wood 1988, Wood andAnderson 1990, Miles and Walton 1993). This is par-

192 JOHN G. BISHOP Ecology, Vol. 83, No. 1

PLATE 1. Lupinus lepidus in low-density edge regions attacked by (a) stem-boring Hysticophora spp. (foreground) and(b, c) leaf-mining Chionodes spp., visible as light-colored webbing and woven gravel retreats.

ticularly true for invertebrate herbivores, whose abilityto more generally influence plant population and com-munity dynamics is a topic of debate (Brown et al.1987, 1988, Crawley 1989, Gange et al. 1989, Ehrlen1995, Louda and Potvin 1995, Strong et al. 1995, Loudaand Rodman 1996, Root 1996, Maron 1997).

In this paper, I describe patterns of herbivory andthe demographic consequences of that herbivory in apopulation of the legume Lupinus lepidus var. lobbiithat is colonizing the primary successional landscapecreated by Mount St. Helens’ 1980 eruption. In 1981,several individual lupines colonized the otherwise bar-ren north slope of Mount St. Helens from remnant pop-ulations elsewhere on the volcano. For the next severalyears the lupine population spread rapidly outwardfrom this initial invasion focus and lupines were themost successful colonist of upland primary succes-sional habitats (del Moral et al. 1995). By 1990, thelupine population comprised a central core region ofextremely high lupine density surrounded by numer-ous, low-density edge patches up to 2 km from the core(Fig. 1; del Moral et al. 1995, Fagan and Bishop 2000).Intervening areas between the edge and core patches,as well as the expanding margins of core patches, con-tain low-density, patchily distributed lupine. By 1992,population growth rates (l) in recently founded, low-density edge region patches had dropped to an average

of l 5 1.51 (mean of 13 edge patches studied from1991 to 1995), far below those observed during theearly stages of colonization (l 5 11.2, for the originalcolonizing patch, 1981–1985; Fagan and Bishop 2000).

L. lepidus on Mount St. Helens has been the focusof numerous studies demonstrating its ability to ame-liorate physical conditions. For example, L. lepidus canfix more than 7 kg·ha21·yr21 of N, compared to back-ground rates of only 2 kg·ha21·yr21 of N, and dramat-ically increases organic matter accumulation (Kerle1985, Halvorson et al. 1991, Halvorson et al. 1992).Live lupines competitively suppress other ruderal spe-cies, whereas dead lupines facilitate these same species(Morris and Wood 1989, del Moral and Bliss 1993,Titus and del Moral 1998a). However, L. lepidus’s po-tential impact on community development has beentempered by its surprisingly slow rate of spread in re-cent years, associated with decreased l (Halvorson etal. 1992, del Moral and Bliss 1993).

A number of hypotheses could explain recent de-creases in rates of lupine population increase and spa-tial expansion. For example, dispersal limitation,caused by lupines’ relatively large seeds (4–8 mg),could curtail spatial spread (Wood and del Moral 1987).However, long-distance dispersal does occur. Founderindividuals were .4 km from the nearest survivingpatches, in 1991 edge patches existed .1 km from the

January 2002 193HERBIVORY, DEMOGRAPHY, AND COLONIZATION

FIG. 1. Map of study patches on the Pumice Plains and debris avalanche. Locations were obtained by standard surveymethods using a TopCon Total Station. Patches with dates denote location and founding dates of core patches. Contourintervals are 14.7 m. Elevations are in feet (3600–4400 feet 5 1100–1340 m). The crater is 1.5 km southeast. Large solidcircles 5 core patches; small solid circles 5 young edge, experimentally established; solid squares 5 young edge, natural;solid triangle 5 old edge; diamonds 5 source of transplants. Southern 1984 core patch is drawn to scale. The fourth corepatch is ;700 m north-northeast of the 1981 patch. Inset shows location of Mount St. Helens National Volcanic Monument,denoted by open rectangle. Tick marks in inset represent 468159 N latitude and 1228109 W longitude.

nearest seed source (personal observation), and seedsare occasionally deposited in traps many meters fromlupine populations (del Moral and Wood 1988, Woodand del Moral 1988, Wood and del Moral 2000). Thus,while dispersal limitation may play a role, it is not anadequate explanation for changes in spread rates. An-other plausible explanation is that lupines colonizedmost suitable habitat shortly after the eruption, and farepoorly in currently available habitats. This explanationis also inadequate. L. lepidus is characteristic of high-altitude pumice communities, and resource-poor gla-

cial moraines (Franklin and Dyrness 1973, Kruckeberg1987). Following the eruption, L. lepidus colonizedsubstrates 200–600 m below pre-eruption elevations,.1000 m below its elevation elsewhere in the region.At these lower elevations, decreased drought stress andlonger growing seasons are known to increase lupinegrowth rates, size, and fecundity relative to plants atpre-eruption elevations (Braatne and Bliss 1999).

Another plausible hypothesis is that decreased l isthe demographic consequence of insect herbivory.High levels of seed predation and other insect herbivore


damage have been documented in L. lepidus at MountSt. Helens (Halvorson et al. 1992, Bishop and Schem-ske 1998, Fagan and Bishop 2000; see Plate 1). Inaddition, short-term removal experiments demonstratethat these herbivores can reduce population growth andrates of spread (Fagan and Bishop 2000). Here I presentthe results of a large-scale (60 patches), long-term (5yr) demographic survey of core and edge patches thatallows extrapolation from the experimental results ofFagan and Bishop. Specifically, I describe patterns ofherbivory that differ between core and edge patchesand that are closely related to host density. I also useextensive demographic data to ask whether the damageby different herbivore guilds likely affects lupine de-mography (survivorship, fecundity, and populationgrowth), and whether these effects vary among coreand edge portions of the population.

METHODS

Species and study site

The study site was formed on 18 May 1980 by amassive debris avalanche, followed by pyroclasticflows (incandescent gas and pumice), lahars, and tephradeposition. The lupine patches in this study lie in a 60-km2 primary successional landscape, atop 4–80 m ofnewly emplaced rock, and 300–1500 m from the near-est secondary successional habitats. Thus, there wasno pre-eruption seed bank, herbivores, or other bioticlegacy surviving in these sites. The study patches arescattered across 6 km2, with an elevation range of1150–1350 m (3700 ft–4400 ft in Fig. 1). Environ-mental conditions on the Pumice Plains are stressful;the pumice and rock substrates initially had little water-holding capacity, few nutrients, and nitrogen was un-detectable (Nuhn 1987, Halvorson et al. 1991, 1992,del Moral and Bliss 1993). Although yearly precipi-tation is high (2.4 m), there is pronounced summerdrought (rainfall in July and August is frequently ,10mm/mo), and surface temperatures reach 508C (Reyn-olds and Bliss 1986). Lupinus lepidus possesses severalfeatures, e.g., the ability of seedling roots to quicklyreach moister subsurface soil, that allow it to avoiddrought stress (Braatne and Bliss 1999).

Mature plants of L. lepidus var. lobbii are ,15 cmhigh, with prostrate herbaceous stems spreading up toa 45-cm radius from a fibrous caudex. L. lepidus isself-compatible, and pollen addition experiments inlarge patches show that fruit set is not pollinator limited(J. G. Bishop, unpublished data). Seeds are explosivelydehisced, but have no obvious adaptations for second-ary dispersal, moving primarily by wind and duringsnowmelt. The flowers, flower stalks, and fruits arefrequently attacked by lupine aphids (Macrosiphum al-bifrons), pentatomid bugs (Chlorochroa ligata), larvaeof an anthomyiid fly (Crinurina sp.), and by two lep-idopteran species specializing on lupines, the micro-lepidopteran Schinea sueta and the lycaenid Plebejus

icarioides montis (Bishop and Schemske 1998). Larvaeof several lepidopteran species also mine the leaves(Gelechiidae: Chionodes spp.) and bore into the caudex(Tortricidae: Hystricophora sp.); these are also lupinespecialists and rarely attack adjacent L. latifolius. Dam-age by leafminers is easily recognized as a woven massof whitened or yellowed leaves, and damage by caudexborers as a gray pallor accompanied by wilting (seePlate 1); both types of damage are readily quantified.Damage to fruits and seeds by chewing insects is moresubtle and must be assessed through dissection.

Field methods

Twelve patches (3 core, 9 edge) were selected fordemographic study in 1991, and 7 additional patches(1 core, 6 edge) were selected in 1992. Core patches,founded 1981–1984, include the original colonizingpatch and several high-density satellites. Edge patchesare widely spaced secondary or tertiary foci, generallylocated uphill of the core, and can be divided into twoage groups: those founded 1987–1988 (‘‘old edge’’)and those founded 1990–1991 (‘‘young edge’’). These19 patches represent a substantial proportion of the coreand older edge patches that existed by 1991. Extensivesurveys in 1994 identified only three additional largepatches in the region illustrated in Fig. 1, and about40 additional patches among edge patches, mostly com-parable to young edge patches.

To increase the sample size of newly-founded patch-es and to examine the probability of patch establish-ment, I established 41 additional edge patches prior tothe start of the 1992 growing season. Each experimentalpatch consisted of eight 1-yr-old individuals arrangedin a circle 1 m in diameter. Founders were from oneor two nearby patches (Fig. 1), representing likelysources of natural colonists. Sites were chosen withoutregard to microsite characteristics, except that theywere not placed within gullies and were located .30m from existing patches so as to avoid external de-mographic influence. These patches are similar in den-sity, percent cover, and size distribution to natural edgepatches, so they are grouped with ‘‘young edge’’ patch-es.

To provide an indication of successional status, per-cent cover of lupines and percent cover of all otherplants were estimated in 1993 for each patch by esti-mating the number of 10 3 10 cm squares occupiedby each species. Differences among patch types (core,old edge, young edge) were examined using Tukey testsfor multiple comparisons (Zar 1984).

All edge patches were censused by establishing apermanent grid around the patch. In core patches, be-cause of their much higher density, five or nine 25 325 cm quadrats were placed randomly along transectsrunning from the periphery to the center of the patch.An additional four or seven 1 3 1 m quadrats werelocated at patch margins in order to sample the low-density periphery of the core. The number of quadrats


varied because additional quadrats were placed in larg-er patches. When increased patch size made samplingentire patches and quadrats infeasible, sections of gridsor quadrats were subsampled and some patches weredropped from the study (2 in 1994, and 13 in 1995).All patches were censused in late August (15–28 Au-gust), but plants were usually located and tagged inJune and July. All plants were marked, and their lo-cation determined to the nearest centimeter, to allowrelocation. Plant diameter, which correlates stronglywith biomass (Pearson’s r 5 0.95, df 5 49, P ,0.0001), and herbivore damage were measured at eachcensus.

Herbivory.—Foliage damage by leaf-miningChionodes caterpillars, which is conspicuous, wasrare until 1993. It was quantified first as present orabsent (1993), then, in 1994–1995, on a 0–5 scaleof leaf destruction: 0 5 0–5%, 1 5 6–25%, 2 5 26–50%, 3 5 51–75%, 4 5 76–95%, 5 5 95–100% de-struction). Caudex-boring Hystricophora sp. was notapparent from 1990 to 1992, but in 1993–1994 itcaused nearly 100% mortality in several patches notunder study. Mortality caused by Hystricophora be-tween August 1994 and July 1995 was quantified bysurveying live plants and plants that had died sinceAugust 1994 for Hystricophora presence. Becausedead lupines take .1 yr to decay, and because Hys-tricophora forms extensive galleries in the root andcaudex, stem borer presence was easily identified insummer, 1995. Its presence in live plants is detectedby wilting, gray pallor, and the accumulation of frasssurrounding holes in the caudex.

Reproduction.—I censused each plant’s infructesc-ences and the number of fruits on a sample of seveninfructescences per plant, if available, at roughly 2-wkintervals. In addition, a sample of infructescences wascollected to estimate seeds per fruit and damage byseed predators. Sample sizes fluctuated because (a) insome years (i.e., 1993) weather conditions resulted inlittle or no reproduction, and (b) to minimize demo-graphic effects, fruits were not collected from patcheswith low fruit set. Overall for the years 1991–1996,seed production and damage was measured for 2957fruits from 347 plants from core patches, and 2594fruits from 369 plants from edge patches.

Fruits were checked for (a) the presence of damage,indicated by an entry or exit hole produced by a seedpredator; (b) the total number of mature or nearly ma-ture seeds, not counting aborted seeds; and (c) the num-ber of these seeds damaged by chewing. Not countingaborted seed results in underestimation of insect dam-age, because many are caused by inflorescence-attack-ing hemipterans and homopterans. Seed production be-fore predation was estimated for each plant by multi-plying total fruits (known for every plant) by averageseeds per fruit (from that patch or a nearby one of thesame patch type). Using average seeds per fruit to cal-culate seeds per plant is reasonable, as most of the

interplant variation within patches in seed productionis due to fruit number rather than seeds per fruit (Bishopand Schemske 1998). The number of seeds matured(i.e., after predispersal predation) was estimated by dis-counting each plant’s seed production by estimates ofproportion of seeds damaged by chewing insects.

Analyses.—For each of the three types of herbivoredamage, leaf mining, caudex boring, and seed preda-tion, there are two classes of analyses. I first askedwhether each type of herbivory differs between patchtype (core and edge), and whether there is an additionaleffect of plant density. Second, I analyzed the effectsof patch type, herbivory, and density, on mortality, seedand seedling production, and population growth. Re-gression analyses included year as a covariate, whenappropriate. In edge patches, density was calculated bydefining area as the rectangle bounding the outermostplants. Variables were transformed to improve modelfit, but not to de-correlate residuals. Instead, signifi-cance levels for multiple and stepwise regressions weredetermined by randomization tests performed as fol-lows. For each regression analysis, dependent variabledata were randomly permuted among cases 4999 times,while holding the independent variable data constant,to create 4999 new data sets. The regressions wererepeated for each permuted data set, and the P valuewas calculated as [rank of the actual regression coef-ficients among 4999 random ones 4 5000] (Manly1991). Table 3 lists dependent and independent vari-ables. Proportion of seeds damaged in each patch wasanalyzed with ANOVA using sequential sums ofsquares, with year and patch type as factors. Signifi-cance levels were determined using randomization testsas for the regression analysis, with P values calculatedas the [rank of the actual F statistic 4 5000] (Manly1991). All analyses were done using S-Plus 3.3 (Statsci1994).

Logistic regressions were used to determine (1) theeffect of patch type (core vs. edge), density, and plantdiameter on Hystricophora infestion (1994–1995 only,for four edge and four core patches) and (2) whetherleaf damage or Hystricophora infestation affected theprobability of surviving until the next census, withpatch type, year, and plant diameter as covariates. Foryears in which degree of leaf damage was measured,logistic regression was used to determine whetherplants with the most damage (.74%) had an increasedprobability of death. Survivorship distributions (prob-ability of surviving until a given age) were estimatedfor 1991–1995 for all patch type and cohort combi-nations using Kaplan-Meier estimates for 5246 plants(Kalbfleisch and Prentice 1980). Effects of patch typeand cohort on survivorship distributions were analyzedwith an accelerated life model, assuming a Weibulldistribution. Details of this analysis are available inAppendix A. Appendix B contains photographs show-ing the impact of insect herbivores.


TABLE 1. Site and sample characteristics by patch type. Statistics are reported as median (range).

SitePatches

surveyedYear

foundedArea sampled

(m2)

Initialpopulation

sizeDensity

(plants/m2)

Edge, youngEdge, oldCore

5064

1990–19911987–19881981–1985

90 (48–600)225 (144–300)

4 (1–10)

3 (1–24)131 (35–160)

.40,000

0.13 (0.001–1.70)a

1.01 (0.03–5.06)b

73 (0.25–1622)c

Notes: Number of plants sampled does not include dead plants. Values of density and percent cover with different superscriptletters are significantly different, P , 0.01.

TABLE 2. Mean of population and quadrat means (6 1 SD).

Measure Years

Edge

Younger Older Core

Proportion plants damaged

Average area damage

Seed number

l (5er)

1993–1995

1994–1995

1991–19921993–1995

1981–19851991–1995

0.68 6 0.4a

1.85 6 1.1a

231 6 425a

51 6 120a

NA1.51 6 0.75

0.48 6 0.3b

1.43 6 1.5a

174 6 358b

7 6 33b

NA1.46 6 0.93

0.08 6 0.1c

0.18 6 0.3b

161 6 394b

35 6 60ab

11.3 6 2.70.91 6 0.19

Notes: Plant damage refers to leaf mining by Chionodes spp. Average area damaged is the mean leafminer damage classon a scale of 0 (0–5%) to 5 (95–100%). Values in the same row with different superscript letters are significantly different(P , 0.05) after applying variable-wide sequential Bonferroni correction. Population growth rate (l) is the median of thegeometric mean Nt11/Nt for each patch taken across years. Core data from 1981–1985 are courtesy of C. M. Crisafulli. NA5 not applicable.

RESULTS

Percent cover of lupines was .11003 higher in thecore than at the edge; percent cover of other specieswas 2653 higher at the core than at the edge, andmedian patch densities were 5613 greater in the corethan in young edge patches (Table 1). These resultsprovide independent support for lumping patches intoclasses representing different stages of colonization.Note that the densities in edge patches appear too lowto invoke either intraspecific or interspecific resourcecompetition as an explanation for the 7.5-fold decreasein population growth in these regions (Table 2). All 41transplant patches survived the first growing season,with a median of 3 survivors per patch, and 38 of 41survived for 6 yr. Natural and transplant young edgepatches were similar in percent cover (both 0.4%) andlupine density (mean 6 SD; 0.03 6 0.1 plants/m2 vs.0.08 6 0.05 plants/m2 in 1992).

Foliage and caudex damage.—Foliage damage byleaf-mining Chionodes caterpillars increased dramati-cally through the study period. While leaf damage wasnot apparent in 1991–1992, by 1995 a median of 68%of plants were damaged in young edge patches, and themedian damage score averaged across patches was 1.85(2 5 26–50%, Table 2). Edge patches suffered muchgreater damage than core patches (Table 2, Fig. 2), andincreasing density of L. lepidus resulted in decreaseddamage at both the core and the edge, even with yearand patch type entered first as covariates (Table 3, lines1 and 2). At the core, this negative relationship between

density and herbivory results from herbivory concen-trated at the margins of the patch.

Similarly, though quantified only in 1994–1995,damage by caudex-boring Hystricophora increasedthrough the study period, and was much higher in edgepatches (Table 4), and Hystricophora presence was pos-itively density dependent in edge patches but nega-tively density dependent in core patches. Logistic re-gression indicated that core plants at 1.16-m spacingwere 153 more likely to be infested by Hystricophorathan plants at 0.16 m, whereas the odds of infestationfor widely spaced plants at the edge is 0 relative toplants at 0.16-m spacing (odds 5 probability of infes-tation 4 probability of no infestation; Table 4).

Seed production and predation.—Seed productionper plant (post predation) decreased dramaticallythrough the study period (compare 1991–1992 with1993–1995 in Table 2). The presence of Chionodesleafminers, which increased over time, was associatedwith 32 fewer seeds per plant (Table 3, line 4), a 97%decrease compared to 33 6 71 seeds per plant (mean6 1 SD of all populations, after seed predation). Seedloss to predispersal seed predators, primarily lycaenidcaterpillars (Plebejus icarioides) and anthomyiid flylarvae (Crinurina spp.), averaged 36% across all pop-ulations and years. ANOVA and post hoc comparisonsindicated that mean seed loss was greater in core patch-es and decreased over time (effect of patch type: F 549, df 5 1, P , 0.0001; effect of year: F 5 11, df 54, P 5 0.001; patch type 3 year interaction: F 5 6, df


TABLE 1. Extended.

Percentcover lupine

Percentcover other

plants

Number of live plants sampled

1991 1992 1993 1994 1995

0.03 (0.01–0.1)a

0.06 (0.02–0.15)a

66.3 (4–92)b

0.12 (0.00–1.9)a

0.12 (0.06–0.5)a

31.8 (0.00–108.8)c

41399291

213603757

130017151894

143318281496

114898

298

FIG. 2. Magnitude of leaf damage caused by Chionodesspp. (patch averages), vs. density. The change of damage-class scale on the bottom graph reflects a difference in scoringmethod between 1993 (present/absent) and later years [scaleof 0 (no damage) to 5 (100% damage)]. Note logarithmicplant density scale. Lines are local regression (LOESS) es-timates.

5 4, P 5 0.018; P-values estimated by randomizationtest; total df 5 215). The strong patch type 3 yearinteraction corresponds to the observation that over 7yr of observations, percent fruit damage in core patchesundergoes a damped oscillation between 4% and 82%,whereas damage in edge patches declines after 1991(Fig. 3). Regression analysis reveals that the effect ofseed predation carries over into the next year’s seedlingabundance. Seedlings per square centimeter of leaf areawere significantly negatively affected by the proportionof fruits damaged, but not affected by the total numberof seeds (before predation) in the previous year (Table3, line 5).

Survivorship and annual mortality.—The odds of dy-ing increased through the study period and were twiceas great in core patches as in edge patches, correspond-ing to a decrease in survivorship from 0.65 to 0.32(logistic regression: effect of each additional year onodds 5 4.413, P , 0.0001; effect of edge vs. core 51.933, P , 0.0001; N 5 8867; effect indicates increasein odds of death). Logistic regression did not detectsignificant effects of Chionodes presence on mortalityfrom 1993 to 1995, an effect that may have beenmasked by Hystricophora, but did indicate that a leafdamage score .4 (.75% leaf loss, N 5 109) raised

the overall probability of death in 1994–1995 from 0.80to 0.90 (P 5 0.03, df 5 2261).

Graphical inspection of age-specific survivorshipcurves suggests that patch type, cohort, and year havestrong effects on survivorship (Fig. 4). These conclu-sions are supported by the accelerated life model anal-ysis for patch type and cohort, which shows decreasingsurvivorship in younger patches and later cohorts (P, 0.0001 for each level of each factor, df 5 5239, r2

5 0.41; see Appendix A for details). Of particular noteis that seedling mortality (as indicated by the transitionfrom the first to the second growing season) was 40%higher in core patches than in edge patches (excludingcore 1991 and edge 1994). In contrast, postseedlingmortality was comparable between patch types. Thepattern at the core is attributable to high lupine estab-lishment and rapid growth of other species in 1991,followed by low establishment thereafter. In 1994 sur-vivorship was low in all patch types for all cohorts(Fig. 4) demonstrating that high mortality late in thestudy is not attributable to a deterministic 4 or 5 yrlifespan. In edge patches this appears to be due to Hys-tricophora-caused mortality, whereas in core patchesHystricophora was less common (Table 4), and sur-vivorship is comparable to previous years.

Population growth (l 5 Nt11/Nt) was higher on av-erage in edge patches than in core patches, and highestin the young edge patches (Table 2), but even in edgepatches l averaged seven times less than in the originalpatch 10 yr earlier. l fluctuated greatly between patchesand years, with r (5 loge l) ranging between 21.2 and.5 in edge patches in 1992–1993 alone (data notshown, see Fig. 5 for range over all years). In addition,population growth appears to be strongly affected bydensity (Fig. 5), even when patch type and year areentered first as covariates (Table 3, line 3). In otherwords, negative density dependence is as strong acrossthe range of densities found in young edge patches(median density 5 0.13 plants/m2) as it is in core patch-es (median density 5 73 plants/m2).

DISCUSSION

Stem-boring, leaf-mining, and seed-eating lepidop-terans and anthomyiid flies, feeding in edge patchesand in the low-density margins of core patches, mark-edly increased mortality and decreased propagule pro-duction. This conclusion, in combination with the ex-perimental results of Fagan and Bishop (2000), con-


TABLE 3. Results of regression analyses of leafminer damage and demographic rates.

Dependent variable

Independent variables†

Year

Coeff. P

Patch type

Coeff. P

Density (Nt /m2)‡

Coeff. P

Patch type3 Density

Coeff. P r2 N

A) Leafminer damagePlants damaged by Chion-

odes, 1993–1995 (%)Average Chionodes dam-

age, 1994–1995r in patch or quadrat

[5loge(l)]

20.03

0.08

20.33

0.16

0.61

,0.0001

0.34

0.93

1.97

0.0002

0.0001

,0.0001

20.09

20.33

20.21

,0.0001

,0.0001

,0.0001

20.06

20.30

20.22

0.008

0.004

0.008

0.56

0.51

0.33

236

143

249

B) Lupine seed productionSeed production per repro-

ductive plant§\1.4 0.0006 224.6

214.50.00020.005

232.2 0.0002 3.2 0.0002 0.27 2023

C) Seedling densitySeedlingst11/cm2 of lupine\ 0.01 0.64 20.08 0.006 20.12 0.02 20.001 0.87 0.16 109

Notes: Results are from stepwise regression with variables entered in order from left to right; patch type is a dichotomousvariable with core 5 0, edge 5 1, except as noted. Listed under each independent variable are regression coefficients (Coeff.)and P values.

† All significance levels determined by randomization tests are based on regressions of 4999 permuted data sets.‡ Variable was loge-transformed to improve model fit.§ Top coefficient is for old edge relative to young edge, bottom values are for core relative to young edge.\ Multiple regression.

TABLE 4. (A) Hystricophora infestation and associated per-centage mortality in edge vs. core patches; (B) results oflogistic regression analysis for the effect of patch type andnearest-neighbor distance (NN) on Hystricophora presence.

A) Hystricophora infestation

Category

Edge (N 5 703)

Plants(%)

Mortality(%)

Core (N 5 345)

Plants(%)

Mortality(%)

InfestedUninfested

7723

9759

2476

9593

B) Regression analysis (R2 5 0.78, N 5 1048)

Variable Coefficient Odds P

InterceptEdge relative to coreNN at core (m2)NN at edge (m2)

0.290.472.71

210.04

1.6015.030.00

0.220.0000.0000.000

Notes: (A) The ‘‘Plants’’ columns report the percentagesof infested and uninfested plants. (B) Coefficients indicatethe increment in log odds. ‘‘Odds’’ refers to the odds ofinfestation relative to core or edge plants with 0.16-m spacing.For example, edge plants are 1.63 more likely to be infestedthan are core plants.

FIG. 3. Time series of percentage fruit damaged withpointwise 95% binomial confidence intervals. Estimates aremeans of plant means. Values for 1990 are anecdotal, butbased on a large number of fruit dissections (Bishop andSchemske 1998); values for 1996 are from Fagan and Bishop(2000).

tradicts the view that insect herbivores do not influencecolonization by native species or of primary succes-sional habitats, suggesting instead that specialist insectherbivores restrict population growth and spatial spreadof lupines colonizing Mount St. Helens. For example,in 1994, 77% of edge plants were infested with theHystricophora stem borer, and infested plants had 97%mortality, compared to 59% for uninfested plants and25–40% for edge plants in the previous 3 yr (Fig. 4).

Mortality in 1995 not caused by Hystricophora waspartly attributed to the Chionodes leafminer, which in-fests the majority of edge plants and removes .25%of leaf area on average (Fig. 2, Table 2). Herbivoresalso curtailed edge plant seed production. In 4 of 6 yr,pre-dispersal seed predators removed 37–69% of ma-turing seeds (Fig. 3) and directly affected seedlingnumbers the next season. Moreover, leaf damage byChionodes prevented many plants from producing anyseeds. Because established seedlings often have highsurvivorship in edge patches (Fig. 4), and L. lepidus


FIG. 4. Survivorship curves: comparison of patch typeand cohort (year of germination); N 5 8867 plants. Age 1 isthe end of the first growing season for each cohort. A smallfraction of plants survive past 5 yr.

FIG. 5. Annual population growth (r 5 loge l) for patchesand quadrats as a function of density, by patch type, for 1991–1995. Line slopes are from multiple regression; horizontallines denote r 5 0. For the abscissa label, the original unitsof density were Nt /m2.

has a short-lived seed bank (Bishop 1996), the loss ofseeds may directly decrease recruitment to adult stages.

Removal of the Chionodes leafminer and several lessabundant herbivores from two edge patches in 1995produced a temporary fivefold increase in populationgrowth rate (l), mediated primarily by increased plantgrowth and seed production (Fagan and Bishop 2000).Our combined studies show that such leafminer effectsoccur throughout edge region patches and have per-sisted from 1993 to 1999. Fagan and Bishop did notfind any significant effect of herbivore removal on mor-tality, nor of predispersal seed predators in edge patch-es. The current study suggests that the fivefold effectof removal actually underestimates the impact of insectherbivores because both pre-dispersal seed predationand Hystricophora-caused mortality are frequentlygreater than they were in 1995–1996. Thus, herbivoreimpacts likely account for the observed 7.5-fold de-crease in l compared to initial rates of l 5 11.3 (Table2). Models of spatial spread predict that diminished lat the edge of an expanding population will greatlyaffect spread rates, suggesting that herbivory in edgeregions may explain L. lepidus’ failure to rapidly ex-ploit available habitat (Skellam 1951, Moody and Mack1988, Andow et al. 1990, Fagan and Bishop 2000).

Edge vs. core

Herbivory in core patches was lower compared toedge patches and had relatively little demographic im-pact. Hystricophora and Chionodes caterpillars werescarce in core patches. When present, they were con-centrated in the lower density margins of the corepatches, where their presence might easily be over-looked, yet where models predict the greatest effectsof decreased propagule production on spatial spread.Fagan and Bishop (2000) found no effect of herbivoreremoval on l in core patches, but their experiment wasnot designed to distinguish between central and mar-ginal zones of the core.

Greater herbivory in edge patches and core margins,compared to the denser center of the core, runs counterto expectations based on resource concentration,wherein the densest host populations sustain the highestherbivore density. While negative relationships be-tween host density and herbivory are not uncommon,the underlying mechanisms remain obscure (Kunin1999). It seems unlikely here that greater herbivoreload at low-density is attributable to the larger basinof attraction of each plant, because the herbivores are


nearly absent from the central core areas, and becausethis pattern has persisted for 7 yr. Alternatively, highloads on edge and margin plants may reflect resourcequality for herbivores, which may in turn be a functionof plant stress, plant vigor, or nutrient stoichiometry(Price 1991, Elser and Urabe 1999). Margin and edgeplants do appear more vigorous than their central coun-terparts.

A third hypothesis for core–edge differences is thatfaunal buildup is more advanced in core areas, andsupports higher trophic levels that suppress herbivores.In fact, spatial variation in tritrophic interactions islikely at Mount St. Helens. The abundance of generalistpredators and parasitoids of lepidopteran larvae ismuch higher in the core than at the edge, as are ver-tebrate predators, especially birds (Fagan and Bishop2000; J. Edwards, unpublished data). Subtle differ-ences in faunal succession might also explain thedamped oscillation in fruit damage on core plants overa 7-yr period (1990–1996), and the contrasting mono-tonic decrease at the edge (Fig. 3).

Density-dependent mortality and population growth

Several observations imply that high mortality incore patches (Fig. 4, 1992–1994 cohorts) is attributableto resource competition. Intraspecific density reaches1600 plants/m2 in some quadrats, median intraspecificneighbor distance was .7 cm only in 1991, and coverof all species averages 54% (Table 1). Seedling mor-tality was much higher than that for established plants,except in 1991 (Fig. 4), a hallmark of competition (Sil-vertown and Lovett Doust 1993). Finally, populationgrowth in core patches appears negatively density de-pendent (Fig. 5), even when year is entered as a cov-ariate (Table 3), and despite the fact that herbivory isconcentrated in low-density margins. This suggests thatinsect-caused mortality and propagule loss may be un-important to core population dynamics. This suggestionis confirmed by the effect of insect removal, whichincreased seed production in core patches without af-fecting r (Fagan and Bishop 2000).

Whether plant populations are often limited by prop-agule loss to herbivores is a continuing controversy(Crawley 1989, 1990, 1992, Louda 1989). In lupinesat Mount St. Helens, the demographic significance ofpropagule loss varies spatially. High levels of seed pre-dation in core patches may have little effect on l be-cause competition predominates, but propagule pro-duction in edge patches is closely linked to l and rateof spread. However, core patches may depend on seedproduction, since recruitment following disturbancescaused by erosion, lahars, and large mammals dependson the newly formed, but short-lived, seed bank (Bish-op 1996). Long-lived seed banks are thought to dampenpopulation-level effects of seed predation in other lu-pine species, but these systems too are frequently dis-turbed and seed banks could become depleted by seedpredation (Breedlove and Ehrlich 1972, Dollinger et

al. 1973, Harrison and Maron 1995, Maron and Simms1997). In lupines at Mount St. Helens, competition andherbivory govern dynamics in different portions of thepopulation and their relative importance changes overtime. Negative density-dependent population growthalso occurred in edge patches, where the median den-sity is only 0.13 plants/m2 and total cover averagedonly 0.4%, even when year is included first as a cov-ariate (Table 3). Resource competition is an unlikelyexplanation for negative density dependence at theedge, but positive density-dependent herbivory in edgeareas by Hystricophora may be partially responsible.

Community and ecosystem implications

Farrell (1991) presents a model of consumer-drivensuccession, wherein the effect of consumers dependson the model of succession (e.g., tolerance, inhibition,or facilitation). According to this view, consumers ofpioneer species will increase rates of succession whenpioneers inhibit later successional species, but consum-ers will decrease rates or alter trajectories of successionwhen early species facilitate later ones. Vertebrate her-bivores, for example, can severely delay succession inN-limited grasslands by feeding on a legume that con-rols the size of N pools (Ritchie et al. 1998). In contrast,effects of herbivory on dune primary succession (Bach1994) and marine primary succession (e.g., Hixon andBrostoff 1996) are mediated by interactions that fallunder tolerance or inhibition models of succession. AtMount St. Helens, episodic lupine mortality may in-crease local rates of succession, because invading ru-derals are inhibited by live lupines but facilitated bydead lupines (Morris and Wood 1989). This effect issimilar to that of L. arboreus in coastal grasslands,where mortality caused by hepialid moth larvae me-diates access by exotic plants to lupine-enriched Npools (Maron and Jefferies 1999). However, at the land-scape scale, delay in L. lepidus arrival caused by her-bivores is likely to slow primary succession throughdecreased rates of N mineralization, accumulation oforganic matter, and other facilitative effects (Halvorsonet al. 1991, Halvorson et al. 1992, del Moral 1993,Titus and del Moral 1998b). Thus, at Mount St. Helensinsect herbivores may simultaneously prevent buildupof N pools at large spatial scales and mediate accessto those pools at smaller scales.

ACKNOWLEDGMENTS

I thank D. Schemske and members of his lab for guidance,discussion, and comments at all stages of this study, and D.McCrumb, D. Kline, M. Jackson for extensive field assis-tance. L. Anderson, E. Anderson, P. Chilsen, B. Cook, I.Dews, B. Fagan, A. Holzapfl, K. Koerner, B. Nakamura, I.Parker, D. Parks, J. Ramsey, D. Schemske, J. Titus, K. Warner,and R. Williamson, also provided invaluable field assistance.C. Crisafulli kindly provided unpublished data. Commentsby K. Clay, B. Fagan, J. Kingsolver, J. Maron, J. Titus, andthree anonymous reviewers improved the manuscript. Thiswork was supported by the UW Plant Molecular Integrationand Function Committee, NSF dissertation improvementgrant DEB-9213143 and NSF training grant BIR-9256532.


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APPENDIX A

Failure time analysis of lupine survival is available in ESA’s Electronic Data Archive: Ecological Archives E083-004-A1.

APPENDIX B

Photographs showing the impact of insect herbivores are available in ESA’s Electronic Data Archive: Ecological ArchivesE083-004-A2.

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