Take Me to Your Leader: Does Early Successional Nonhost Vegetation Spatially Inhibit Pissodes Strobi (Coleoptera: Curculionidae)?

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PLANTÐINSECT INTERACTIONS Take Me to Your Leader: Does Early Successional Nonhost Vegetation Spatially Inhibit Pissodes strobi (Coleoptera: Curculionidae)?

JORDAN M. KOOPMANS,1 HONEY-MARIE C. DE LA GIRODAY,1,2 B. STAFFAN LINDGREN,1 1,2,3 AND BRIAN H. AUKEMA

Environ. Entomol. 38(4): 1189Ð1196 (2009) ABSTRACT The spatial inßuences of host and nonhost trees and shrubs on the colonization patterns of white pine weevil Pissodes strobi (Peck) were studied within a stand of planted interior hybrid spruce [Picea glauca (Moench) Voss ϫ Picea engelmannii (Parry) ex Engelm.]. Planted spruce accounted for one third of all trees within the stand, whereas the remaining two thirds were comprised of early-successional nonhost vegetation, such as alder (Alnus spp.), paper birch (Betula papyrifera Marsh.), black cottonwood [Populus balsamifera ssp. trichocarpa (T. Ng.) Brayshaw], lodgepole pine [Pinus contorta (Dougl.) ex Loud.], trembling aspen (Populus tremuloides Michx), willow (Salix spp.), and Canadian buffaloberry [Shepherdia canadensis (L.) Nutt.]. Unlike the spruce trees, nonhost vegetation in the stand was not uniformly distributed. Spatial point process models showed that Canadian buffaloberry, paper birch, black cottonwoood, and trembling aspen had negative associations with damage caused by the weevil, even though the density of the insectsÕ hosts in these areas did not change. Moreover, knowing the locations of these nonhost trees provided as much, or more, inference about the locations of weevil-attacked trees as knowing the locations of suitable or preferred host trees (i.e., those larger in size). Nonhost volatiles, the alteration of soil composition, and overstory shade are discussed as potential explanatory factors for the patterns observed. New research avenues are suggested to determine whether nonhost vegetation in early successional stands might be an additional tool in the management of these insects in commercially important forests.

KEY WORDS nonhost volatiles, angiosperm volatiles, plantÐinsect interactions, Engelmann spruce weevil, spatial point processes

The white pine weevil Pissodes strobi (Peck) (Co- chemical responses and genetic variation therein leoptera: Curculionidae), native to North America, is (King et al. 1997, 2004; Alfaro et al. 2000, 2008; Tomlin a herbivorous insect that reproduces in the terminal et al. 2000). Physical characteristics, such as thickness leaders of young spruce and pine. In the spring, fe- of the primary cortex and the size of trees and their males oviposit in leaders of host trees generally Ͼ5yr leaders, also inßuence host selection (VanderSar and of age (He and Alfaro 2000). Developing larvae girdle Borden 1977, Kiss and Yanchuk 1991, Turnquist and the shoots, often leading to creases, crooks, and forks Alfaro 1996, King et al. 1997, van den Driessche 1997, in the tree (Silver 1968). Although mortality of trees Manville et al. 2002). Spatial factors that potentially is uncommon, stem defects and associated growth inßuence insect distribution have received less atten- reductions may reduce lumber yield by as much as tion, however (He and Alfaro 1997). Some of these 40% in commercially important forests (Alfaro et al. factors affect the vigor of young spruce, including 1997). After a brief pupation within the leader, adults overstory composition, sun exposure, soil drainage, emerge between July and September to overwinter in and edge vegetation (Lavallee et al. 1996, Taylor et al. the duff layer or on the tree itself in coastal areas 1996, Simard and Hannam 2000). Certain properties of (Silver 1968). White pine weevils complete their life these factors may be exploited in silvicultural recom- cycle in 1 yr (Silver 1968). Infestations may continue mendations to reduce impacts of white pine weevil. in stands of spruce for up to 50 yr (He and Alfaro Inßuences of spatial distribution and diversity of 2000). nonhost species, and their impacts on the host-selec- Past research on the distribution and impact of tion behavior, distribution, and abundance of white white pine weevils on host trees has focused primarily pine weevil, has not yet been studied to our knowl- on defensive mechanisms of the trees, including edge. New spruce forests are typically established as the result of natural or anthropogenic disturbances 1 University of Northern British Columbia, 3333 University Way, and therefore may contain diverse early successional Prince George, British Columbia V2N 429, Canada. species (Denslow 1980), such as alder (Alnus spp.), 2 Natural Resources Canada, Canadian Forest Service, 3333 Uni- versity Way, Prince George, British Columbia V2N 4Z9, Canada. trembling aspen (Populus tremuloides Michx), willow 3 Corresponding author, e-mail: [email protected]. (Salix spp.), and paper birch (Betula papyrifera 1190 ENVIRONMENTAL ENTOMOLOGY Vol. 38, no. 4

Marsh.), as well as various shrub species. Recent work Measurements for spruce and pine [lodgepole pine has suggested that the presence of nonhost vegetation Pinus contorta variety latifolia (Engelm.) ex S. Wats.] such as red alder (Alnus rubra Bong.) may affect the trees included age, root collar diameter, height, evi- levels of white pine weevil abundance (McLean 1989, dence of white pine weevil activity, and the presence Almond 2006). Increased plant diversity may decrease of other insects. The ages of spruce trees were esti- impacts by herbivores that exhibit narrow host mated by counting the number of whorls and con- breadths (Bianchi et al. 2006) but also may increase Þrmed by counting growth rings on a randomly se- impacts by more generalist herbivores (Koricheva et lected subset of trees destructively sampled poststudy. al. 2006). Root collar diameter was measured with a 150-mm In this study, we explore spatial factors that may caliper, and tree height was measured with a standard inßuence host selection and distribution of P. strobi. 8-m tape measure. Weevil activity was identiÞed by We Þt spatial point process models to a data set from the presence of oviposition punctures, fecal plugs, a population census of Ͼ1,000 trees in a stand con- emergence holes, larval cavities on broken leaders, taining moderate levels of white pine weevil. We seek and wilted (i.e., shepherdÕs crooks) or dead leaders to answer two questions regarding the pattern of wee- (Lavallee et al. 1996). In this paper, we refer only to vil distribution. First, does nonhost vegetation have those trees possessing dead or dying leaders as suc- either a positive or negative association with distribu- cessfully colonized. Four categories of weevil coloni- tion of white pine weevil attack? Second, if such an zation were identiÞed: 1, 2, and 3 yr of colonization or association exists, how does it compare with known never colonized. Spruce trees were judged to have predictors of weevil attack distribution, including multiple years of weevil colonization if they showed physical attributes of colonized spruce trees such as damage on the initial leader with subsequent attack of size? Expanding our understanding of insect interac- new shoots vying for apical dominance. An elevation tions with host and nonhost vegetation, in combina- grid was developed by recording elevation values at tion with existing knowledge of spruce defense mech- 10-m intervals along the transect and at two to four anisms, may yield new silvicultural tools for locations on the horizontal axis using a GPS (Meridian contending with this herbivore in commercially im- Gold Magellan; Thales Navigation, San Dima, CA). portant forests. Data were collected from 26 May to 17 June 2008. Data Analysis. Maps for the locations of all trees, including weevil-colonized trees, were created using the spatstat package v.1.13Ð3 in R v.2.6.2 (Ihaka and Materials and Methods “ ” Gentleman 1996, Baddeley and Turner 2005, R De- Site Selection and Data Collection. We censused a velopment Core Team 2008). Spatial trends in the x 0.154-ha stand of interior hybrid spruce with relatively and y directions of height and root collar diameter of even-aged trees displaying a moderate level of P. strobi colonized versus uncolonized spruce trees were stud- abundance near Prince George, British Columbia, ied using linear regression. Further effects of weevil Canada (53Њ52Ј N, 122Њ47Ј W). The spruce had been colonization status on height and diameter of spruce hand-planted and were 12 yr of age at the time of trees were studied by examining the signiÞcance of study. The stand also contained a variety of other such a term added to the prior regression models that nonhost vegetation from natural regeneration. With accounted for spatial trends. the exception of willow (Salix spp.), trees and shrubs Spatial point process models were used to examine were identiÞed to the species or subspecies level. For the effects of spatial trends (i.e., x and y, as well as the purposes of analysis, alder, which consisted of elevation), spatial attributes of host plants (i.e., height green alder [Alnus viridis ssp. crispa (Ait.) Turrill], and diameter at root collar), and locations of nonhost sitka alder [Alnus viridis ssp. sinuata (Regel) A. and D. plants on the prevalence of white pine weevil attack. Lo¨ve], and mountain alder [Alnus incana ssp. tenuifo- The response variable for each model, intensity (␭), a lia (Nutt.) Breit.] were grouped together at the genus spatially explicit estimated density of weevil attacks, level. Every live tree with Ͼ1-cm root collar diameter was measured as the number of trees with damaged was censused. (i.e., dead or dying) leaders per square meter. Co- Spatial location data for each tree was determined variates were converted to either density surfaces (for using a compass, vertex, and corresponding distance point processes such as locations of trees or shrubs) or transponder (Haglo¨f Sweden Vertex III v.1.4; Haglo¨f, a smoothed interpolation (for the marks of a point Madison, MS), with slope values and horizontal dis- process) before Þtting. Both types of surfaces incor- tance measurements corrected based on the internal porated a Gaussian kernel density smoother as a rep- clinometer. Tree species with multiple stems emerg- resentation of the point process deÞned within the ing from a single root collar, such as alder, were boundary (Cressie 1991, Baddely and Turner 2000). mapped at a single point location central to all of the Border corrections were tested, but not applied in the stems and were recorded as a single tree with the Þnal analyses, because the trees and boundary were corresponding number of stems as a stem density. well deÞned, and our results proved robust compared Stems without a well-deÞned root collar, yet that ap- with various edge corrections (results not shown). peared to be connected and were growing within a Parameters in these spatial point process regression 10-cm radius of each other, were also recorded as a models were estimated using maximum pseudolikeli- single tree. hood methods. SigniÞcance of individual variables was August 2009 KOOPMANS ET AL.: SPATIAL RELATIONSHIPS BETWEEN INSECTS AND NONHOSTS 1191

Table 1. Composition of a stand planted with interior hybrid Sx Al Be Pb 120 spruce near Prince George, British Columbia

Species Common name Code n Picea glauca ϫ engelmanni Spruce Sx 365 100 Alnus spp. Alder Al 361 Betula papyrifera Paper birch Be 210 Salix spp. Willow Sa 56 Populus tremuloides Trembling aspen Pt 36 80 Shepherdia canadensis Canadian buffaloberry Sc 25 Populus balsamifera ssp. Black cottonwood Pb 11 trichocarpa Pinus contorta Lodgepole pine Pl 5 60 ϭ A code for each species is provided for reference in Fig. 1 (ntotal 1,069). 40 judged by statistical comparison to a homogenous model (i.e., one estimating only an intercept or a constant intensity of weevil attack across the site), by 20 examining the change in deviance relative to a ␹2 reference distribution. Similarly, when we sought to examine additive effects of a second (or third) vari- 0 able while accounting for the effect of a previous Scale variable, a comparison of nested models was per- 20m formed by examining the change in deviance relative Pl Pt Sa Sc to a ␹2 reference distribution. Models were compared 120 using AkaikeÕs Information Criterion (AIC), and models with the lowest AIC values were judged to Þt the best (Akaike 1973). 100

Results 80 Distribution of Trees and Shrubs. A population census of the stand yielded 1,069 trees and shrubs from seven different genera (Table 1). Interior hybrid spruce comprised one third of the siteÕs population 60 (34%), whereas alder comprised another third (33.6%). The remaining third of the population consisted of six other species of trees and shrubs, pre- 40 dominantly young paper birch (19.6%). The location and identity of each tree species mapped within the stand is shown in Fig. 1. Spruce 20 were evenly distributed throughout the entire site without spatial trends in either the x or y direction (P Ͼ 0.05). The mean density of spruce was 0.24 2 0 stems/m , (i.e., ϳ2 by 2-m spacing). Alder was present Scale across the majority of the site with the exception of the 20m upper right section. Canadian buffaloberry, black cot- Fig. 1. Stem maps of all trees and woody shrubs found tonwood [Populus balsamifera ssp. trichocarpa (T. within stand. Each tree is represented by an open circle. Sx, Ng.) Brayshaw], willow, and trembling aspen were P. glauca ϫ engelmanni; Al, Alnus spp.; Be, B. papyrifera; Pb, found predominantly in the top half of the site (as P. balsamifera ssp. trichocarpa; Pl, P. contorta; Pt, P. tremu- depicted in Fig. 1), particularly in areas where alder loides; Sa, Salix spp.; Sc, S. canadensis. For ease of graphical was absent. There were also more paper birch in the representation, the top of the Þgure is oriented east (rather top half of the site, although a few small clusters of than due north). stems were noted in the central and lower regions. Only Þve lodgepole pine trees were present across the spruce trees that were not colonized by white pine site. weevil were distributed throughout the entire stand Distribution of Weevil Colonization. Figure 2 (Fig. 2A). Nineteen percent of trees had been colo- shows the distribution of all spruce trees according to nized once. These trees were distributed throughout their four categories of colonization by white pine the stand except for a small pocket within the upper- weevil, with a numerical summary in Table 2. Nearly most section (Fig. 2B). Fifteen of the 87 trees with one quarter of the 365 spruce trees, i.e., 87 trees, had weevils had been colonized twice (Table 2) and were been colonized by white pine weevil. The 76% of distributed in two clusters near 10 and 75 m on the 1192 ENVIRONMENTAL ENTOMOLOGY Vol. 38, no. 4

A. Never B. Colonized C. Colonized D. Colonized values were judged to have the best explanatory 120 Colonized 1x 2x 3x power. Despite the fact that spruce were spatially homogenous throughout the stand, Table 3A indicates that there was a signiÞcant spatial trend in weevil 100 attack in the vertical (y) direction, with more insect colonization present toward the lower portion of the plot (Fig. 2). Colonization of leaders by the white pine 80 weevil did not vary across the stand with respect to the moderate elevational differences or the horizontal (x) direction. Association of Weevils With Spruce Attributes. The 60 average diameter of all spruce trees was 32 mm at the root collar (Table 2), with larger trees being found toward the lower and left sides of the plot (diameter 40 in mm ϭ 44Ð0.470xÐ 0.125y, where the x and y axes are measured in meters and are the same as in Fig. 1; ϭ Ͻ F2,362 54.74; P 0.0001). After accounting for this 20 spatial trend, we found that, on average, spruce trees with signs of weevil colonization were almost 1 cm larger in root collar diameter than those that had not been colonized (F ϭ 25.81, P Ͻ 0.0001; Table 2). 0 1,361 Scale Increased densities of white pine weevil colonization 20m were associated with areas containing trees with larger Fig. 2. Map of all spruce trees within the stand according diameter at root collar, as indicated by the signiÞcant to level of white pine weevil colonization. Each tree is rep- positive slope for the diameter term in Table 3B. resented by an open circle. (A) Trees that have not been Spruce trees were 138 cm tall on average (Table 2). colonized. (B) Trees showing 1 yr of colonization, (C) 2 yr Similar to root collar diameter, there was a signiÞcant of colonization, and (D) 3 yr of colonization. For ease of spatial trend in height in the y direction, with taller graphical representation, the top of Þgure is oriented east trees predominantly located toward the lower por- (rather than due north). ϭ ϭ tions of the stand (height in cm 168Ð0.43y; F1,363 50.59; P Ͻ 0.0001). Greater evidence of weevil colo- vertical axis (Fig. 2C). Spruce trees with three leaders nization was noted in areas of the plot with taller trees colonized by P. strobi represented Ͻ1% of the total (Table 3B). Uncolonized trees were an average of 8 spruce population and were located exclusively in the cm shorter than spruce colonized by the weevil; how- lower portion of the stand between 0 and 20 m on the ever, this difference was not statistically signiÞcant vertical axis (Fig. 2D). When examined collectively, after accounting for the spatial trend in height ϭ ϭ Fig. 2BÐD, shows reduced activity by white pine wee- (F1,362 0.002, P 0.96; Table 2). Spruce within the vil in the upper third of our site from the 90- to 120-m stand had been hand-planted, and, aside from a few marks. One hundred eighteen spruce trees (i.e., nearly trees that had regenerated naturally, were 12 yr of age. one third of all spruce) existed between 90 and 120 m. As such, there were no spatial trends in age nor were Of these trees, only eight (6.8%) had been colonized. there any associations between weevil colonization Table 3 summarizes the association of individual and the age of the trees (P Ͼ 0.05). variables, such as spatial directions, spruce hosts, and Association of Weevils With Nonhost Vegetation. nonhost vegetation, with the prevalence of weevil Table 3C shows the effect of each nonhost species on colonization in the stand. Weevil abundance was mea- the intensity of white pine weevil activity (trees with sured as an estimated density, ␭, or trees with killed leaders killed/m2) across the stand, as well as the total leaders per square meter. Models with lower AIC stem density of all species including and excluding spruce. The stem density of vegetation did not explain Table 2. Mean (؎SE) root collar diameter and height of trees any variation in the distribution of white pine weevil categorized by colonization of white pine weevil in a 12-yr-old stand attack. Of the six nonhost species listed (i.e., excluding of planted interior hybrid spruce near Prince George, British lodgepole pine), Þve exhibited negative slope esti- Columbia mates, indicating that the presence of these trees Root collar among the spruce was correlated with lower weevil Colonization classiÞcation n Height (cm) diameter (mm) colonization densities. Four of these Þve nonhost species, Canadian buffaloberry, paper birch, black All spruce trees 365 31.9 (0.5) 138 (2) Never colonized 278 30.0 (0.6) 136 (2) cottonwood, and trembling aspen, were statistically All colonized 87 38.1a (1.0) 144 (3) signiÞcant (P Ͻ 0.05). The model for Canadian buf- Colonized one time 69 37.3 (1.3) 143 (4) faloberry exhibited the best explanatory power for the Colonized two times 15 41.5 (1.9) 153 (7) presence (or absence) of white pine weevil coloni- Colonized three times 3 39.4 (4.3) 142 (17) zation, because it had the lowest AIC value (653.3). a SigniÞcantly different from trees that had never been colonized Incorporating other variables in multiple regression (P Ͻ 0.0001, see text). equations containing a term for Canadian buffaloberry August 2009 KOOPMANS ET AL.: SPATIAL RELATIONSHIPS BETWEEN INSECTS AND NONHOSTS 1193

Table 3. Regression equations for single variables describing directional trends, host, and nonhost associations with distribution of white pine weevil colonization in a stand of interior hybrid spruce near Prince George, British Columbia

Intercept Slope a Term ␹2 P AICb Estimate SE Estimate SE Intercept onlyc (i.e., constant intestity) Ϫ2.87 0.11 676.2 A. Directional trendsd Elevational trend 19.29 21.36 Ϫ0.033 0.032 1.05 0.31 677.2 Trend in x direction Ϫ2.59 0.19 Ϫ0.044 0.025 3.19 0.07 675.1 Trend in y direction Ϫ2.03 0.21 Ϫ0.013 0.003 16.94 0.0021 661.3 B. Spruce characteristics Diameter (mm) Ϫ5.32 0.60 0.073 0.017 18.34 Ͻ0.0001 659.9 Height (cm) Ϫ5.48 0.75 0.018 0.005 12.44 Ͻ0.0001 665.8 C. Nonhost speciese Alder Ϫ3.05 0.17 0.73 0.48 2.17 0.14 676.1 Paper birch Ϫ2.68 0.14 Ϫ1.57 0.85 4.05 0.04 674.2 Black cottonwood Ϫ2.70 0.11 Ϫ41.42 14.83 14.00 0.0002 664.3 Lodgepole pine Ϫ2.82 0.12 Ϫ16.87 17.77 0.99 0.32 677.3 Trembling aspen Ϫ2.70 0.11 Ϫ12.78 4.78 12.92 0.0003 665.3 Willow Ϫ2.80 0.12 Ϫ2.20 2.05 1.30 0.25 677.0 Canadian buffaloberry Ϫ2.59 0.12 Ϫ40.89 12.09 24.99 Ͻ0.0001 653.3 Stem density (all trees) Ϫ3.36 0.50 0.22 0.22 0.98 0.32 677.3 Stem density (nonhosts) Ϫ3.26 0.38 0.11 0.12 1.14 0.29 677.1

The response variable for each equation is log(␭), where ␭ is the density estimate of female adult weevils measured by leaders killed per square meter. For example, the estimated density of weevils in locations with spruce 40 mm in diameter at root collar would (Ϫ5.32 ϩ 0.073 ϫ 40) be exp or 0.09 leaders killed/m2. a Change in deviance from a homogenous model tested against a ␹2 distribution with 1 degree of freedom (i.e., does the variable explain more spatial variation in weevil abundance than a surface with constant density?). b Akaike information criteria. Lowest numbers are judged to be best models. c Average density of insects is exp(Ϫ2.87) or 0.06 insects/m2, or approximately one in four spruce (density of spruce is 0.24 trees/m2; see text). d Mean elevation for the site was 670 m. Ranges for x and y are 0Ð18.9 and 0Ð120.1 m, respectively. e Terms for trees and shrubs are listed as a density in trees per square meter. did not signiÞcantly improve that modelÕs Þt. Knowing (Coleoptera: Curculionidae) (Dickens et al. 1992; the locations of trembling aspen or black cottonwood Schroeder 1992; Deglow and Borden 1998a, b; Huber provided as much inference on the locations of weevil- and Borden 2001; Deng et al. 2004; Dickens 2006; damaged trees through negative spatial associations as Broad et al. 2008). P. strobi shows attraction to host knowing the location of larger spruce trees positively volatiles such as monoterpenes and ethanol (Chenier associated with increased weevil colonization density and Philogene 1989), as well as a response to the (as judged by the similar AIC values of Ϸ665, among pheromone grandisol and its aldehyde grandisal these models). (Booth et al. 1983, Hibbard and Webster 1993). There- fore, the potential for disruption of host species recognition by nonhost volatiles is certainly plausible. For Discussion example, in laboratory bioassays, feeding of P. strobi is Our results showed that patterns of spatial inhibi- inhibited by the oil extract of western red cedar tion indicated by nonhost vegetation can provide as [Thuja plicata (Donn) ex D. Don] when present at much, or more, inference on the location of white pine levels similar to those found in nature (Alfaro et al. weevilÐdamaged trees as simply knowing the loca- 1979, 1981). The quantity of isoprenes and monoter- tions and attributes of their host trees such as height penes emitted by western red cedar are Ϸ0.02 Ϯ 0.01 and diameter, which along with leader size, are often and 0.07 Ϯ 0.05 ␮g/g leaf dry weight/h, respectively positively correlated with white pine weevil distribu- (Kesselmeier and Staudt 1999). Trembling aspen and tion (VanderSar and Borden 1977, Kiss and Yanchuk black cottonwood, both of which showed signiÞcant 1991, Turnquist and Alfaro 1996, King et al. 1997, van negative spatial associations with weevils in our study, den Driessche 1997, Manville et al. 2002). Although emit isoprenes at a rate of Ϸ50 ␮g/g leaf dry weight/h spatial correlations do not imply causation, and ma- (Benjamin et al. 1996, Kesselmeier and Staudt 1999). nipulative experiments are required to establish These emission rates are two orders of magnitude mechanistic links between pattern and process, sev- greater than the emission rates of western red cedar eral potential mechanisms between nonhosts and and also higher than the emission rates found in En- white pine weevil exist. gelmann or white spruce (16 and 7Ð15 ␮g/g leaf dry For example, nonhost volatiles may alter, enhance, weight/h, respectively; Kesselmeier and Staudt 1999). or reduce mate or host Þnding, as shown in numer- Paper birch also exhibited a signiÞcant negative spatial ous and diverse insect systems such as the diamond- association with weevils on our site. Emission rates of back moth (Plutella xylostella L.), cotton bollworm paper birch are unknown; however, silver birch (Bet- (Helicoverpa armigera Hubner), Colorado potato ula pendula Roth) may emit 5.4 ␮g/g leaf dry weight/h beetle (Leptinotarsa decemlineata Say), ambrosia bee- of monoterpenes (Hakola et al. 1998), again, far tles (Gnathotrichus retusus LeConte), and bark beetles greater than the amount found in western red cedar. 1194 ENVIRONMENTAL ENTOMOLOGY Vol. 38, no. 4

Although the chemical proÞle of Canadian buffa- volatiles or below-ground competitive interactions. loberry is unknown, isoprene emissions of redberry, Therefore, the signiÞcance of these nonhosts species on also within Rhamnaceae, may exceed the 50 ␮g/g leaf weevil colonization in early stages of stand development dry weight/h emitted by trembling aspen or black is likely from the presence of nonhost volatiles and pos- cottonwood (Kesselmeier and Staudt 1999). sibly the alteration of constitutive or induced defenses Aside from nonhost volatiles potentially acting on through nitrogen Þxation and macronutrient uptake in host Þnding or feeding behaviors above ground, al- below-ground processes. teration of nutrient regimens by nonhosts below It is possible that the area of decreased weevil abun- ground may affect the defensive chemistry of proxi- dance found within our stand was caused solely by a mate host plants (Stamp 2003, Cortini and Comeau lag in weevil dispersal, with avoidance of areas of 2008). For example, we know little of the mycorrhizal nonhosts strictly a statistical artifact. Weevil activity communities associated with nonhost species, which on our site seems to be increasing annually, as is typical may inßuence the defensive mechanisms of proximate in early stand development (King et al. 1997). How- trees by altering nutrient availability (Read 1991, ever, movements of P. strobi recorded during spring Gange and West 1994, Hartnett and Wilson 1999, Lan- ßight have shown that the insects are capable of ßying gley and Hungate 2003). The most statistically signif- 50 m or more (Godwin et al. 1957, Silver 1968, Harman icant nonhost species, Canadian buffaloberry, Þxes 1975). Hence, dispersal ability does not seem to be a nitrogen and may be a key source of this nutrient for limiting factor in the patterns observed. Likewise, it the development of maturing pine stands (Wei and seems unlikely that the current pattern of colonization Kimmins 1998). It is possible that Canadian buffa- across the stand reßects stand saturation, because both loberry inßuences the defensive mechanisms of young stand age (He and Alfaro 2000) and the directional spruce, leading to a differential distribution of white gradient observed (Table 3) instead of a regular pat- pine weevil colonization. We might expect, however, tern (He and Alfaro 1997) suggests that the level of that nitrogen enhancement would increase growth, white pine weevil colonization across the site has shifting resources away from plant defenses and in- likely not yet reached its peak (He and Alfaro 2000). creasing susceptibility to insect colonization (Herms Settlement patterns of white pine weevil in conifers and Mattson 1992). Indeed, the preference P. strobi are likely caused by multiple and interacting pro- exhibit for large, vigorously growing leaders suggests cesses. Our Þndings that some species of nonhost veg- that host trees allocating less resources toward growth etation in regenerating stands may be associated with and more toward defense may not be colonized. Like areas of reduced weevil activity provides new avenues Canadian buffaloberry, however, alder conditions soil for research. For example, it is unknown whether the by Þxing nitrogen (Cortini and Comeau 2008), and we present patterns of weevil colonization distribution in did not Þnd evidence of spatial inhibition between early stand development persist into later successional alder and white pine weevil attack in the stand. stages. Our work also highlights research avenues ex- Another potential mechanism of inhibition be- ploring potential mechanisms responsible for the pat- tween host and nonhost trees is direct competition for terns we observed. These opportunities include ex- water, nutrients, and sunlight among neighboring amining the alteration of host seeking behaviors by trees. Competition may, for example, reduce spruce insects through exposure to nonhost volatiles, and leader size and hence attractiveness to white pine examining how competition in plant communities af- weevil and lodgepole terminal weevil P. terminalis fects herbivore population dynamics by altering host Hopping (Alfaro and Omule 1990, Maclauchlan and plant defenses. Borden 1996). Although nonhost vegetation on the site was not distributed evenly, we found no association between stem density (either including or ex- Acknowledgments cluding nonhosts) and the presence or absence of weevil attack. Trees proximate to spruce may increase The authors thank T. Truant and F. McKee (UNBC) for overstory shade, which is also known to reduce the Þeld help and title suggestion, K. Menounos (city of Prince George) for permission to use the study site, and colleagues prevalence of weevil attack (Taylor and Cozens 1994, within the Forest Insect Research Group at UNBC for feed- Taylor et al. 1996). Alder may act as a shade source for back on data interpretation. Funding was provided by the spruce, potentially decreasing the likelihood of weevil Canadian Forest Service and NSERC (data collection and attack (McLean 1989, Almond 2006), although no spa- student training) and Genome British Columbia (implemen- tial correlations between alder and trees with white tation of statistical platform). pine weevil attack were evident in our stand. Trem- bling aspen, paper birch, and black cottonwood of- fered fractional overstory cover for spruce within the References Cited stand, because none of the host trees exceeded 3.5 m in height, and deciduous trees, excluding alder, did not Akaike, H. 1973. A new look at the statistical model iden- tiÞcation. IEEE Trans. Automat. Contr. 19: 716Ð723. exceed 3 m. Canadian buffaloberry is a low-growing Alfaro, R. I., and A. Y. Omule. 1990. The effect of spacing on shrub and did not provide any shade for spruce. sitka spruce weevil damage to sitka spruce. Can. J. For. Hence, any potential inhibition processes by the Res. 20: 179Ð184. deciduous vegetation and spruce selected by adult fe- Alfaro, R. I., H. D. Pierce Jr., J. H. Borden, and A. C. male weevils were likely limited to either above-ground Oehlschlager. 1979. A quantitative feeding bioassay for August 2009 KOOPMANS ET AL.: SPATIAL RELATIONSHIPS BETWEEN INSECTS AND NONHOSTS 1195

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