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Western North American Naturalist 63(4), ©2003, pp. 440-451

ATTRIBUTES ASSOCIATED WItH PROBABILITY OF INFESTATION BY THE PINON , IPS CONFuSus (COLEOPTERA: SCOLYTIDAE), IN PINON PINE, PINUS EDULIS

Jose E Negronl and Jill L. Wilson2

ABSTRACT.-We examined attributes of pinon pine (Pinus edulis) associated with the probability of infestation by pinon ips (Ips con}usus) in an outbreak in the Coconino National Forest, Arizona. We used data collected from 87 plots, 59 infested and 28 uninfested, and a logistic regression approach to estimate the probability ofinfestation based on plot­ and tree-level attributes. Pinon pine stand density index was a good predictor ofthe likelihood ofinfestation by pinon ips at the plot level, and a cross-validation analysis confirmed that the model correctly classified 82% ofthe cases. Diam­ eter at root collar and pifion dwarf mistletoe infestation level were good predictors ofindividual tree infestation, and a cross-validation analysis indicated that the model correctly classified 72% of the cases. Results suggest that the occur­ rence of pinon ips infestations may be related to stress factors associated with increased stocking and pinon dwarf mistletoe infestations.

Key words: Ips confusus, pinon ips, bark , Pinus edulis, pinon pine.

Piiion-juniper woodlands are the most widely winter from about November to March in distributed forest type in the western United colonies in the basal portion of standing trees States. Covering about 19 million ha in the West (Chansler 1964). In the spring new host trees (Evans 1988), these woodlands are the most are initially attacked by male beetles, which common vegetation types in Arizona and New excavate a nuptial chamber and are then joined Mexico. Piiion-juniper woodlands provide habi­ by females attracted by a male-produced phero­ tat for many wildlife species, serve as water~ mone. After mating, each female constructs an sheds, offer numerous wood products and egg gallery where oviposition takes place. After recreational opportunities, and have ritual and hatching, the larvae feed on the inner bark, ceremonial importance for Native Americans. and pupation occurs in a pupal chamber under The pinon ips, Ips confusus (LeConte), is the bark (Furniss and Carolin 1977, Wood 1982, an important disturbance agent in these wood­ Eager 1999). lands. Primary hosts are pinon (Pinus edulis Endemic populations of this invade Englem) and single-leaf pinon (Pinus mono­ and kill scattered, stressed pifions. Substantial phylla Torrey & Fremont), but other pines are tree mortality is often observed with increased also recorded as hosts. The pinon ips is a insect population levels. Population increases small, cylindrical, brown bark , 4---6 mriJ. can result from the availability of recently in length, 1.5-2.0 mm wide, and is character­ downed or uprooted trees, which provide suit­ ized by the specific arrangement of5 spines in able habitat for insect popuiation growth. Pre­ the declivity of each elytron. In pinon ips and disposing agents such as drought or infesta­ 4 other closely related species, the 3rd spine, tions of pinon mistletoe (Arceuthobium divari­ which is the largest, has a notch on the ventral catum Engelmann) are also believed to increase side. In the western United States the insect. the likelihood of piiion ips attack (Wilson and occurs in southern California, Arizona, New Tkacz 1992). Mexico, west Texas, Nevada, Utah, Colorado, Wilson and Tkacz (1992) observed increased and Wyoming. It also occurs in Baja California piiion ips=caused mortality of pinon in stands Norte and Chihuahua in Mexico (Wood and with many trees between 17.8 and 27.9 cm in Bright 1992). In the Southwest the insect has diameter at root collar and total basal areas be­ at least 3-4 generations a year. Adults over- tween 22.9 and 45.9 m2 . ha-1 in an outbreak

lCorresponding author. USDA Forest Service, Rock")' Mountain Research Station, 240 W. Prospec~ Ft. Collins, CO 80526. 2USDA Forest Service, Forest Health Protection, 2500 South Pine Knoll, Flagstaff, A:l86001. Present address: USDA Forest Service, Forest Health Protec­ tion, 3815 Schreiber Way, Coeur d' Alene, ID 83815.

440 2003] SUSCEPTIBILITY TO PINON Ips INFESTATION 441 in the Apache-Sitgreaves National Forest, Ari­ zona. They also noted that many trees killed had heavy infestations ofpifion dwarfmistletoe. Aside from this study, no data are available on stand and tree conditions that increase the susceptibility to pinon ips attack and mortality. In this study we examine stand and tree characteristics associated with the occlirrence ofpifion ips infestations in an outbreak area in the Coconino National Forest, Arizona, and develop simple models to estimate the proba­ Coconino bility ofinfestation by pifion ips. National Forest

METHODS

In the spring of 1991, an outbreak ofpifion Arizona ips was detected south of the Twin Arrows area ofthe Coconino National Forest, ca. 32 km southeast of Flagstaff, Arizona (Fig. 1). Numer­ ous pifions began to fade as a result of pifion ips attacks. Pinon ips populations appearec;l to have increased in uprooted trees left in place after land-clearing operations in combination .Fig. 1. Study site in the eastern part of the Coconino Nationai Forest, about 32 Ian (20 miles) southeast of Flag­ with an area-wide drought. An aerial survey staff, AZ, 1997. estimated the affected area at 5260 ha (USDA Forest Service unpublished data). This survey was used to delineate out study area. We con­ ducted our sampling July-August 1991. All area per hectare for pifion, for juniper, and for plots were resurveyed in October 1998, where~ both species combined. We calcll1ated a met­ upon we recorded any mortality that may have ric stand density index for pifion, jumper, and occurred since initial plot installation. both species combined by adding the stana density contribution of each individual tree Plot Establishment following Long and Daniel (1990). We modified The study area is centered at III°18'45/W thyir formula by substituting diameter at root longitude, 35°03'45/N latitude in the Elliott collar for diameter at breast height as follows: Canyon 7.5-minute quadrangle. We established fixed~radius plots on line transects across the Stand density index = sum ((DRCk) / 25)1.6 affected area. Ten transects, spaced ca. 0.8 km apart, were placed perpendicular to both sides where k is the di~eter at root collar (cm) of of Forest Service Road 126 that bisects the the kth tree in the stand. study area. Nine transects comprised 9 plots For pifion trees an ocular estimate ofcrown spaced 60.4 m apart, with the lOth transect ratio was obtained. For this estimate 2 observers composed of 6 plots, for a total of 87 plots. inspected the tree from different directions Plots had a radius of 8.01 m, an area of 0.02 and agreed in their estimates to within 10%. ha, and at least 1 live or ips-killed pinon. At Average crown width was also obtained for all each plot we recorded the following informa~ pifions by averaging the length of the longest tion for all trees: species, diameter at root col­ axis and its perpendicular axis. lar, and status (live, ips~killed, or other dead). A pifion dwarf mistletoe infection level index Only trees ~2.54-cm diameter at root collar was obtained for all live and recently dead were sampled. The only other tree species pifions, which still had visible infections. Trees present in the study area was Utah juniper, were evaluated on a scale of0-3, with 1 point Juniperus osteosperma (Torrey) Little. With scored for every one-third of the crOwn in this information we calculated average diame­ which mistletoe infections were viSible. We ter at root collar, number of trees and basal then added the score for every one-third to 442 WESTERN NORTH AMERICAN NATURALIST [Volume 63 obtain the mistletoe infection level for the faded in coloration completely but were clearly tree. The mistletoe infection level index was a dying. Some barkbeetles can successfully attack modification ofthe 6-class dwarfmistletoe rat~ a portion of a tree without killing it, which is ing technique developed by Hawksworth (1917). referred to as a strip attack. However, We did The 6-class system has been the standard not observe this in our study site. Therefore, dwarf mistletoe rating system for many years we modeled the probability of infestation at and is widely accepted because it works well both the plot and the individual tree level, and is easy to use. We modified the system for using logistic regression with .2 possible out­ 2 reasons. First, the 6"class system was devel~ comes. To develop plot-level infestation prob­ oped for ponderosa pine, which most com­ ability models, we used average plot data. To monly has a sparse crown that is relatively develop tree-level infestation probability mod­ easy to examine for dwarfmistletoe. Piiion pines els, we used the individual tree data for the have a full, denser crown that poses increased infested plots since these plots included both difficulty in adequately examining for dwarf infested and uninfested trees. mistletoe infections. Second, in our plots we Using the logistic approach, we obtain rated live trees and recently killed trees. Since models in the follOwing form: infections are more difficult to detect in piiion pines and in recently dead trees, by modifYing P (infestation) = 1 / 1 + e b'X , the system we could obtain more conservative ratings while still retaining the strengths of where b'x represents a linear combination of the 6-class system. explanatory variables X with their estimated For each plot we recorded the distance from parameters b, and e is the base ofnaturalloga­ the center of the plot to the nearest most re~ rithms. cently killed piiion outside the plot. For each For the plot~level probability of infestation ips-killed piiion in every plot, we recorded the model, we used logistic regression procedures distance to the most recently killed pinon in SPSS, which estimate the parameters using whether it was outside or inside the plot. Ips­ maximum likelihood ratios (NOTUS-sis 1999). killed piiion pines fade from green to light yel­ For the tree"level model we used PROC low to bright orange within a few days. Shortly NLMIXED in SAS because it allows fitting thereafter the needles begin to fall. The most the logistic regression model assuming the recently killed tree can be determined by presence of correlation effects of trees within observing the rate of foliage discoloration and plots (SAS Institute 1999). needle loss. After the logistic models were formulated, Established plots were termed infested if We divided the plot-level data sets into 6 groups they included at least a single tree killed by with equal numbers ofinfested and uninfested piiion ips and uninfested ifno ips-killed trees plots in each group. We also divided the tree­ were present in the plot. From the 87 plots, 59 level data set into 6 groups composed of equal were infested and 28 uninfested. numbers ofinfested plots. We sequentially ex­ cluded each group from analysis and generated DataAnalysis logistic models using the same independent We conducted Mann-Whitney tests to exam­ variables. Observed values from the excluded ine differences in the variables measured be­ groups were then used to obtain estimates of tween infested and uninfested plots; we used probability of infestation for those groups by analysis ofvariance to compare characteristics substituting these values into the models gen" of live and ips-killed trees within infested erated. This process allowed us to examine plots because it provides a framework for using model performance using a cross"validation the plot and tree status interaction as the error framework. We then used boxplots to examine term to account for correlation effects of trees the distribution 'of estimated probabilities within plots. obtained from the cross validation for the At the plot level there are 2 possibilities: uninfested and infested plots for the plot~level the plot is either infested or not, At the indi­ data and for the killed and live trees for the vidual tree level there are again 2 possibilities: tree-level data. the tree is either killed or alive. At the time of For plot-level data and tree-level data, we measurement some ips-attacked trees had not used the estimated probabilities of infestation 2003] SUSCEPTIBILIlY TO PINON Ips INFESTATION 443

TABLE 1. Means (± standard error ofthe mean) ofvariables measured for plots infested with Ips confusus, uninfested, and all plots combined, Coconino National Forest, AZ, 1997". Variable Infested Uninfested All Number ofplots 59 28 87 Trees per hectare-all species 592.2 (41.5) a 333.6 (36.5) b 509.0 (33.1) Trees perhectare-piiion 370.2 (32.6) a 155.3 (23.4) b 301.1 (25.7) Trees per hectare-juniper 224.5 (19.7) a 178.3 (26.1) a 209.6 (15.9) Basal area-all species (m2 . ha-1) 27.8 (1.9) a 18.4 (2.4) b 24.8 (1.6) Basal area-piiion (m2 . ha-1) 7.0 (0.7) a 2.5 (0.7) b 5.6(0.5) Basal area-juniper (m2 . ha-1) 20.8 (1.8) a 15.9 (2.3) a 19.2 (1.4) Percent basal area in piiion 30.7 (2.9) a 26.6 (6.5) b 29.4 (2.9) Stand density index-all species 496.7 (31.6) a 325.3 (39.1) b 441.5 (26.2) Stand density index~piiion 155.5 (14.0) a 58.8 (14.3) b 124.4 (11.6) Stand density index-juniper 341.2 (27.9) a 266.5 (37.2) a 317.1 (22.6) Diameter at root collar (cm)-all species 20.5 (0.7) a 21.3 (1.5) a 20.7 (0.7) Diameter at root collar (cm~piiion 14.0 (0.5) a 11.9 (1.1) a 13.3 (0.5) Diameter at root collar (cm)-juniper 32.9 (1.9) a 31.2 (2.6) a 32.4 (1.5) Piiion crown ratio (%) 69.5 (In) a 79.7(2.9)b 72.8 (1.8) Piiion crown width (m) 2.5 (0.1) a 2.4 (0.2) a 2.4 (0.1) Piiion mistletoe infection level 0.9 (0.1) a 0.3 (O.l)b 0.7(0.1) Distance to nearest attacked tree (m) 15.5 (0.8) a 17.6 (1.5) a 16.2 (0.7) Residual basal area- all species (m2 . ha-1) 22.9 (1.9) a 18.4 (2.4) a 21.4 (1.5) Residual basal area-piiion (m2 • ha-1) 2.1 (0.4) a 2.5 (0.7) a 2.2 (0.4) Percent residual basal area in piiion 10.3 (2.1) a 26.6 (6.5) b 15.6 (2.6) aFo~ each variable, means followed by different letters are significantly different according to a--Mann-Whitney test (P > 0.(5). Typej error was not maintained acrOSS all variables.

from the cross-validation analysis @d assigned and higher mistletoe infection level. After the them to an uninfested or live category if the outbreak had subsided, there were no differ­ probability was <0.5 and to an infested or killed ences in total residual basal area or pinon category ifthe probability was 0.51 to 1. We then residual basal area, but the percent basal area conducted a cross-tabulation analysis using in pifion was much lower in infested plots the observed and the predicted categories to (Table 1). Within infested plots, ips=killed trees estimate percentage ofcorrect classification. were signifiCantly larger in diameter at root To examine model behavior, we substituted collar, had higher mistletoe infection level, a range of potential values into the final plot~ smaller crown ratios, and longer crown widths and tree-level models. With model behavior (Table 2). The mistletoe infection level was a information for the plot~level data, we deter­ conservative measurement because we were mined the pinon stand density index level at not able to record it for dead trees with no which the probability of infestation approaches foliage. 0.5 and then examined differences in stand The largest numbers of pinons observed conditions for plots with pifionstand density across all plots including live and dead trees index above and below that level using Mann~ were in the 10.2-cm size class, with decreas= Whitney tests. ing numbers observed with increasing diame­ ter classes (Fig. 2). The distributiOn oflive and RESULTS killed trees by diameter classes within infested plots indicates that few trees were killed by Plohlevel and Tree-level Differences pinon ips in the 5.1-cm=diameter class, one­ On infested plots (Table 1) we found signifh third of the trees were .killed in the 10.2-cm­ cantly more trees per hectare (including all diameter class, close to one-half ofthe trees species), more pifion trees per hectare, greater were killed in the 15.2~cm-diameterclass, and basal area per hectare (all species), greater for all other diameter classes more trees were pinon basal area per hectare, higher percent killed than live with the exception ofthe largest basal area represented by pifion, higher stand class where only 2 trees were observed (Fig. 3). density index (all species), higher pifion stand In SUfi, the proportion ofkilled trees increased density index, lower average pifion crown ratio, with increasing size classes. No plot=level or 444 WESTERN NORTH AMERICAN NATURALIST [Volume 63

TABLE 2. Means (:t standard error of the mean) for live TABLE 3. Logistic regression coefficients, standard error, ,and Ips confUSus"kiIIed trees in infested plots, Coconino and significance for constants and explanatory variables National Forest, AZ, 1997a• for predicting the probability of infestation by Ips con- fusus at the plot and individual tree level. Variable Live Ips conjUsus_kiIIed Model B Standard Significance Number oftrees 215 209 Variable error Diameter at root collar (cm) 9.5 (0.5) a 17.0 (0.6) b PLOT LEVEL Mistletoe infection Constant -0.910 0.445 0.041 level 0.6 (0.1) a 1.4 (0.1) b Pinon pine Nearest attacked tree 6.7(0.2) a 6.3 (0.3) a metric stand CroWn ratio (%) 66.9 (1.5) a 63.7 (1.6) b density index 0.Ql8 0.005 0.001 Crown width (m) 1.9 (0.1) a 3.0 (0.1) b TREE LEVEL "For each variable, means followed by different letters are significantly differ- Constant -2.461 0.402 0.001 entaccording to analysis ofvariance (P > 0.05). Diameter at root collar 0.378 0.059 0.001 Mistletoe infec- tion level 0.556 0.152 0.001 tree·level differences were observed in rela­ tion to the proximity ofthe plot or tree to pre­ viously infested trees (Tables 1, 2). sity index was 124.4 (11.6). The interquartile Probability ofPlot-level range was 116.8 with 50% of the observations Infestation between the values of 46.9 and 163.7. In our We tested average crown ratio of pinon, data there were 25 plots with pinon stand den­ average crown width ofpifion, average mistle­ sity index <50 and 62 plots with pifion stand toe infection level, average diameter at root density index >50. Plots with pifion stand den­ collar for all species, average diameter at root sity index > 50 exhibited increased stocking, collar for pinon, total basal area, pinon basal larger average diameter at root collar, higher area, percent basal area in pinon, trees per percentage of pinon, reduced average pinon hectare, pifions per hectare, staIid density index crown ratio, increased average pinon crown (all species), and pifion stand density index as width, and increased mistietoe infection level explanatory variables ofthe probability ofinfes­ (Table 4). tation. Ofthese, pmon stand density index was Probability ofTree-level the single best explanatory variable, with in· Infestation creasing stand density index associated with iricreas!=ld probability ofi.rlfestation as indicated The folloWing variables were tested as ex­ by the positive logistic regression coefficient planatory variables for the probability ofinfes­ (Table 3). Based on the probabilities of infesta~ tation at the individual tree levet diameter at tion for the infested and uninfested plots ob­ root collar, mistletoe infection level, average tained from the cross-validation analysis, pifion crown width of tree, and crown ratio. Of the stand density index exhibited good discrimina­ variables examined, the combination ofdiame­ toiy power; as there is no overlap in the obser~ ter at root collar and mistletoe infection level vations between the 25th and the 75th per­ was the best explanatory variable; both vari­ centiles (Fig. 4). The median probability ofinfes· ables had positive logistic regression coeffi­ tation was 0.83 for infested plots and 0.44 for cients, indicating that increased diameter at uninfested plots. The cross-tabulation analysis root collar and mistletoe infection level are indicated that the model correctly classified associated with increased probabilities ofinfes­ 82% of the plots. Substituting values of stand tation (Table 3). The probabilities of infesta­ density index from 25 to 600 (with intervals of tion obtained for individual tree mortality from 10) into the model demonstrates that the prob­ the cross-validation analysis revealed that ability ofinfestation approaches 0.5 with pifion although the median between the 2 groups is stand density index of 50, surpasses 0.8 with quite different, 0.69 for the killed trees and pifion stand density index of150, and is asymp­ 0.26 for the live trees, there is overlap in the totic to 1 with pinon stand density index of observations between the 25th and 75th per­ 350 (Fig. 5). The mean ± (standard error ofthe centiles between the 2 groups (Fig. 6). The mean) for observed values ofpifion stand den- cross-tabulation analysis indicated that the 2003] SUSCEPTIBILITY TO PINON Ips INFESTATION 445

160 ~ 140 -5 Q) 120 ::sCi) t:: 100 i:t..... 80 0 ~ Q) 60 ..c E 40 ::l ~ 20 0 5.1 10.2 15.2 20.3 25.4 30.5 35.6 40.6-- 45.7 Diameter at root collar (crn) si~e class

Fig. 2. Total number Give and Ips confusus-killed) ofPinus edulis in each diameter at root collar size class (cm) across all plots. Diameter at root collar of each size class indicates the upper limit ofthe class, Coconino National Forest, AZ, 1997.

120-,r-~~-~~---~~----~---'---J 13 C 1OO..l+-'----l If'-~----l tJ iive !9 killed II percent Q)d) 8:.::: 80J.l------l II-~-~---~-~-~---­ Q)::S . 0.."0 "C Q) 60 CCI) (\J::S

Fig. 3. Number oflive and Ips confusus-killed Pinus edulis in infested plots in each diameter at root collar (cm) size class and percent oftrees killed by Ips confusus in each size class; Diameter at root collar ofeach size class indica,tes the upper limit ofthe class, Coconino National Forest, AZ, 1997.

model correctly classified 72% of the cases. lodgepole pine (Pinus contorta Douglas), those Model behavior obtained by using a range of with a metric stand density index between 313 diameters at root collar of 3~25 em and mistle­ and 625 exhibited increased mortality levels toe infection levels of 0-3 demonstrates how caused by mountain pine beetle (Dendrocto­ the probability ofinfestation increases as both nus ponderosae Boplqns). Anhold et al. (1996) variables increase (Table 5). proposed manag~m~nt guidelines based on stand d~nsity index to reduce lodgepole pine DISCUSSION stand susceptibility to mountain pine beetle. Other studies with mountain pine beetle have Results indicate that high stand density lev­ recognized that high stocking levels in pon­ els of pinon make stands more susceptible to derosa pine (Pin1lS ponderosa Lawson) are often pinon ips infestations. Anhold and Jenkins associated with -caused mortality (1987) showed that in stands composed of>80% (Schmid and Mata 1992, Schmid et al. 1994, 446 WESTERN NORTH AMERICAN NATURALIST [Volume 63

1.0 0.9 <:: <:: o o '§ 0.8 '-~Q) en 0.7 .S1 .!: .!: '0 '0 ~ 0.6 ~ 0.5 :0 :0 ..0 ..0 '" e'" & 0.4 c.. 0.3

o 100 200 300 400 500 600 infested uninfested Pinus edulis metric stand density index Plot Status

Fig. 5. Probability ofplot-level infestation as a function Fig. 4. Distribution ofthe probability of plot~levelinfes" ofPinus edulis stand density index as modeled with logis­ tation by Ips confusus for infested and uninfested plots tic regression. obtained from cross-validation analysis. Lower and upper ends of the box represent the 25th and 75th percentiles, respectively, the line inside the box represents the median, whiskers ofthe box represent the largest and smallest val­ ues not considered outliers, and lines outside the whiskers juniper. Still, results for this study indicate represent outliers. that pifion ips infestation is likely to be more prevalent in stands with pinon stand density index >50. Basal area, stand density index, Olsen et al. 1996). Furthermore, bark beetle and percent basal area levels obtained in this mortality has been associated with reduced study are consistent with others reported in growth rates caused by increased stocking; lev­ the literature. Smith and Schuler (1988) exam­ els in ponderosa pine (Sartwell 1971, Sartwell ined pifion-juniper woodlands in north central and Stevens 1975, Negron 1997, Negron et al. New Mexico, southeastern and southwestern 2000), lodgepole pine (Shrimpton and Thomp~ Colorado, and Arizona (north of the Mogollon son 1983), and Picea glauca (Moech) Voss (white !lim) and reported mean total basal area of spruce; Hard et al. 1983, Hard 1985). Reduced 25.0 m2 . ha-1; mean stand density index for growth rates may result in weakened trees. all species combined, for pinon only, and Such trees may be unable to mobilize carbo­ juniper only of 540, 248, and 276, respective­ hydrates and other resources needed for de~ ly; and mean percent basal area in pifion of43. fensive mechanisms, thereby increasing their Our data are also consistent with those of susceptibility to (Waring and Pitman Barger and Ffolliott (1972), who reported a 1980, Christiansen et al. 1987). Alternatively, density of 333.1 trees per hectare and a total Amman et al. (1988a, 1988b) and Amman and basal area of14.6 m2 • ha-1 for a stand south of Logan (1998) have suggested that reductions Flagstaff, which was dominated by Utah in stand densities by partial cutting result in juniper. reduced mountain pine beetle attacks to lodge~ Although Utah juniper constituted the major~ pole pine because they alter the microclimate ity of the basal area in the study site, pinon by increasing insolation, light intensity, and stand density index was a good predictor of . wind movement, and by reducing humidity. the likelihood ofinfestation. Other studies have However, considering the intense heat, solar related host availability to the likelihood ofbark radiation, and xeric environment that charac­ beetle infestation or the amount of potential terize pinon-juniper woodlands, it is unlikely mortality caused by bark beetles (Sartwell 1971, that these microclimate changes affect pinon Safranyik et al. 1974, Sartwell and Stevens 1915, ips significantly. Schmid and Frye 1916, Furniss et al. 1979, 1981, Total basal areas, pifion basal areas, and per­ McCambridge et al. 1982, Reynolds and Hol­ cent basal areas represented by piiion were all sten 1994, 1996, Negron 1997, 1998, Negron Significantly higher in infested plots. Pinon et al. 1999, 2000). However, in these studies basal area represented only 29% of the basal the host species was the dominant species on area across all plots, the remainder being the sites. 2003] SUSCEPTIBILITY TO PINON Ips INFESTATION 447

TABLE 4. Means (± standard error ofthe mean) for selected variables characterizihg plots with Pinus edulis metric stand density index <50 and >50, Coconino National Forest, AZ, 1997a. Variable sm < 50 sm> 50 Number ofplots 25 62 Trees per hectare-all species 292.6 (31.2) a 596.2 (39.7) b Trees per hectare-pinon 104.8 (10:8) a 380.2 (30.4) b Basal area-all species (m2 • ha-1) 19.4 (2.6) a 27.0 (1.9) b Basal area-pinon (m2 . ha-1) 1.0 (0.1) a 1.4 (0.6) b Percentbasal area in pinon 13.9 (5.3) a 35.6 (3.1) b Stand density index-all species 321.6 (40.7) a 487.5 (31.2) b Stand density index-piiion 25.3 (3.1) a 164.4 (13.1) b Diameter at root collar (cm)-all species 22.1 (1.6) a 19.9 (0.7) a Diameter at root collar (cm)_pinon 9.9 (0.9) a 14.6 (0.5)b Pinon crown ratio (%) 81.1 (3.8) a 69.4 (1.8) b Piiion crown width (m) 1.9 (0.2) a 2.6 (0.1) b Piiion mistletoe infection level 0.2 (0.1) a 0.9 (0.1) b Distance to nearest attacked tree (m) 11.1 (1.5) a 15.8 (0.8) a Residual basal area-all species (m2 . ha-1) 19.2 (2.6) a 22.3 (1.8) a Residual basal area-pinon (m2 . ha-1) 0.7 (0.1) a 2.8 (0.5)b Percent residual basal area in pinon 12.3 (5.4) a 16.9 (3.0) b aFar each variable, meaoS followed by different letters are significantly different according to a Maon-Whitney test (P > 0.05). Type I error was not maintained across all variables.

Foxx and Tierney (1987) suggested that piiion that the nature of the relationship between roots might reach 6 m below the ground but primary bark beetles and dwarf mistletoes was that juniper roots can attain even greater depths. at the time poorly understood. The statement Schuler and Smith (1988) proposed that these remains true, as the laIowledge base of this differences in rooting habits between juniper relationship is still limited. The bulk of the and pinon might cause intraspecific competi­ evidence suggests that there may be a positive tion for moisture that may be greater than relationship in ponderosa pine between mistle­ interspecific competition between pinons and toe infestations by the southwestern mistletoe, junipers. This may explain why pinon stand Arceuthobium vaginatum (Willdenow) Presl density index is a good predictor of infesta­ subsp. cryptopodium (Engelmann) Hawksworth tion, even when pinon represents a minor por­ & Wiens, and mountain pine beetle and round~ tion ofsite occupancy. headed pine beetle, Dendroctonus adjunctus At the individual tree level, the probability Blandford. McCambridge et al. (1982) reported ofinfestation increased with increasing diame­ increased mortality of ponderosa pine caused ter at root collar and mistletoe infection level. by mountain pine beetle in trees infected with In our study site the smallest tree attacked the southwestern dwarf inistletoe in northern was 4.3 cm, the largest 41.7 cm. The largest Colorado. Stevens and Flake (1974) indicated piiion observed was 45.2 cm. We also observed that trees infected with this mistletoe were increased proportions ofpinon ips-killed trees commOn in an area affected by an outbreak of with increasing diameter at root collar size the rotindheaded pine beetle in the Sacramento classes. Wilson and Tkacz (1992) confirmed Mountains, New Mexico. In another study that >50% of the trees with diameter at root from the same area, Negron (1997) reported collar between 11.8 and 21.9 cm were attacked average dwarf mistletoe ratings (Hawksworth by pinon ips, whereas <50% of trees smaller 1917) that were twice as high in plots infested than 17.8 were attacked. Tree size influences by roundheaded pine beetle compared to un­ the susceptibility to attack by pifion ips, and infested plots. However, in lodgepole pine, our data suggest that preference is exhibited studies seem to show no relationship between for larger-diameter classes in the stand. infections by the lodgepole pine dwarf mistle­ Dwarfmistletoe infection level was another toe (Arceuthobium americanum Nuttall ex important factor in determining the likelihood Engelmann) and mountain pine beetle attacks. of attack by pinon ips, as mistletoe infection Hawksworth and Johnson (1989) maintain that level increases, so also does the likelihood of this may be the case because mistletoe~ attack. Stevens and Hawksworth (1984) stated infected trees tend to have thinner phloem 448 WESTERN NORTH AMERICAN NATURALIST [Volume 63

TABLE 5. Probability oftree-level infestation as a function 1.0 of Pinus edulis diameter at root collar (DRC), and mistle~ toe infection level as modeled with logistic regression. c 0 0.8 Mistletoe infection level' ~ DRC ~ (cm) 0 1 2 3 .0; 0.6 '0 g 3 0.12 0.19 0.~9 0.41 4 0.13 0.21 0.32 0.45 :0 0.4 ..c'" 5 0.15 0.24 0.35 0.49 (Le 6 0.17 0.27 0.39 0.53 0.2 7 0.19 0.30 0.42 0.56 8 0.22 0.33 0.46 0.60

O.O-'=------j-~--~---,-----~ 9 0.25 0.36 0.50 0.63 killed live 10 0.27 0.40 0.54 0.67 Pinus edulis status. 11 0.31 0.43 0.57 0.70 12 0.34 0.47 0.61 0.73 13 0.37 0.51 0.64 0.76 Fig. 6. Distribution ofthe probability of tre~-levelinfes­ 14 0.41 0.54 0.68 0.78 tation by Ips confusus for killed and live trees obtained 15 0.44 0.58 0.71 0.81 from cross-validation analysis. Lower and upper ends of 16 0.48 0.6~ 0.74 0.83 the box represent the 25th and 75th percentiles, respec­ 17 0.52 0.69 0.77 0.85 tively, the line inside the box represents the median, 18 0.55 0.68 0.79 0.87 whiskers ofthe box represent the largest and smallest val­ 19 0.59 Q.7.~ 0.81 0.88 ues not considered outliers, and lines outside the whiskers 20 0.63 0.75 0.84 0.90 represent outliers. 21 0.66 0.77 0.86 0.91 22 0.69 0.80 0.87 0.92 23 0.72 0.82 0.89 0.93 according to Roe and Amman (1970). Amman 24 0.75 0.84 0.90 0.94 25 0.78 0.86 0.91 0.95 (1972) indicated that thicker phloem in lodge­ pole pine contributes to increase'd survival of aSee te.xt for e.,..planation ofmistletoe infection index. the mountain pine beetle. As a consequence, mistletoe~infested lodgepole pines may not serve as adequate hosts for mountain pine 30% to 10%. This resulted in a reduction of beetle because they may lack the necessary pinon in basal area in affected areas to the phloem. Furthermore, Hawksworth et al. (1983) same levels found in unaffected stands. Piiion found little relationship between dwarf mistle­ mortality associated with piiion-ips outbreaks toe intensity and phloem thickness in lodge­ mayor may not be compatible with manage­ pole pine in Colorado. ment objectives. Widespread mortality can Infections ofdwarf mistletoe have a variety result in an accumulation of fuels that may of effects on the host, including reductions in considerably increase fire hazard. Piiion trees tree height and diameter growth rates, increased are highly valued as wildlife habitat and as a mortality, and decreased seed production source ofnuts for human consumption. On the (Hawksworth and Shaw 1984). Hawksworth other hand, tree mortality can also result in (1961) showed reductions in mean radial growth openings where herbaceous production is for the last 5 years in severely infected pon­ increased, which is a benefit to livestock, deer, derosa pines. This suggests that as infections and elk. intensify within the tree and vigor declines, its Although pinons are shade intolerant, estab­ susceptibility to barkbeetle attack may increase. lishment of pinon regeneration is most com­ At the plot level we observed increased mistle­ mon under the shade of older trees that mod~ toe infection levels in the piiion ipS-infested erate the environment for seedlings. Premature plots. Higher mistletoe infection levels in in~ exposure to extreme sun and heat can scald fested plots may be a function of increased and kill seedlings (Gottfried 1987). Therefore, stocking densities, which may facilitate tree~ piiion regeneration may be negatively affected to~tree movement ofdwarfmistletoe. when overstory piiions are killed by ips infes~ The piiion~ips outbreak reduced total and tations. pinon basal area. All observed mortality Results of this study suggest that piiion occurred in piiion, and the percent basal area stand density index is a good predictor of of pinon in infested stands decreased from stand susceptibility to pinon ips in our study 2003] SUSCEPTIBILITY TO PINON Ips INFESTATION 449

area. This increased susceptibility may be due AMMAN, G.D., G.D. LESSARD, L.A. RASMUSSEN, AND C.G. to reduced vigor of trees in dense stands. At O'NEIL. 1988a. Lodgepole pine vigor, regeneration, the individual tree level, piiion ips appears to and infestation by mountain pine beetle following partial cutting in the Shoshone National Forest, prefer larger-diameter trees and those with Wyoming. Research Paper INT-396, USDA Forest intensifYing dwarf mistletoe infection. Dwarf Service, Intermountain Research Station, Ogden, mistletoe infection may increase susceptibility UT. to pinon ips by causing additional stress on AMMAN, G.D., M.D. MCGREGOR, RE SCHMITZ, AND RD. OAKES. 1988b. Susceptibility of lodgepole pine to the tree. The simple models presented in this infestation by mountain pine beetles follOwing par­ study can help identifY areas and trees that tial cutting of stands. Canadian Journal of Forest may be susceptible to pinon ips mortality Research 18:688-695. when populations ofthis insect increase. Where ANHOLD, J.A., AND MJ. JENKINS. 1987. Potential mountain ips-caused mortality may be of concern, man­ pine beetle (Coleoptera: Scolytidae) attack on lodge­ pole pine as described by stand density index. Envi­ agement techniques that include thinning to ronmental Entomology 16:'738-742. reduce pinon stand density index below 50 ANHOLD, J,A., M.J. JENKINS, AND J,N. LONG. 1996. Manage­ will' reduce the likelihood of tree mortality. ment oflodgepole pine stand density to reduce sus­ Since trees with severe mistletoe infections in ceptibility to mountain pine beetle attack. Western the larger-diameter classes are more likely to Journal ofApplied Forestry 11(2):50-53. BARGE'R, RL., AND P.E FFOLLIOTT. 19'/2. Physical charac­ be attacked, they may be good candidates for teristics and utilization ofmajor woodland treespecies removal if the overall management objectives 'in Arizona. Research Paper RM-83, USDA Forest can be achieved. Service, Rocky Mountain Forest and Range Experi­ Because our models were developed using ment Station, Fort Collins, CO. CHANSLER, J,E 1964. Overwintering habits of Ips lecontei data from a small area, extrapolation to other Sw. and Ips confusus (Lee.) in Arizona and New localities areas must be done with discretion. Mexico. Research Note RM-27, USDA Forest Ser­ The important variables observed in our study vice, Rocky Mountain Forest and Range Experiment will likely be of equal importance in other Station, Fort Collins, CO. sites, but values may vary with changing forest CHRISTIANSEN, E., R.H. WARING, AND A.A. BERRYMAN. 1987. Resistance of conifers to bark beetle attack: conditions. Nevertheless, our models may be searching for general relationships. Forest Ecology useful stepping-stones for the development of and Management 22:89-106. biological models that may be applicable to EAGER, T.J, 1999. Factors affecting the health of pinyon larger geographical areas (Hedden 1981). pine trees (Pinus edulis) in the pinyon-juniper wood­ lands of western Colorado. Pages 39'7-399 in Pro­ ceedings: Ecology and management of pinyon­ ACKNOWLEDGEMENTS juniper communities within the Interior West. Pro­ ceedings RMRS-P-9, Rocky Mountain Research Sta­ We thank the follOwing individuals: Yvonne tion, USDA Forest Service, Fort Collins, CO. Bonser, Brian Madland, Kristen Miller, Justin EVANS, RA. 1988. Management of pinyon-juniper wood­ Selvik, and Erika Wiltenmuth for field assis­ lands. General Technical Report INT-249, USDA Forest Service, Intermountain Research Station, tance and data collection; Frederick W Smith Ogden, UT. and Linda A. Joyce for reviews of earlier ver­ Foxx, S.T., AND G.D. TIERNEY. 1987. Successional changes sions ofthe manuscript; Rudy King for statisti­ in community structure of pinyon_juniper wood­ cal support; and the anonymous reviewers lands of north-central Arizona. Pages 69-79 in R whose comments greatly improved the manu­ Everett, compiler, Proceedings: Pinyon-Juniper Conference, 13-16 January 1986, Reno, NY. USDA script. This study was a cooperative effort be­ Forest Service, Intermountain Research Station, tween the USDA Forest Service, Rocky Moun­ Ogden, UT. tain Research Station, Fort Collins, Colorado, FURNISS M.M., RL. LMNGSTON, AND M.D. MCGREGOR. and the USDA Forest Service, Forest Health 1981. Development ofa stand susceptibility classifi­ cation for Douglas-fir beetle. Pages 115-128 in RL. Protection, Region 3, Flagstaff, Arizona. Hedden, S.J, Barras, and J.E. Coster, technical coor­ dinators, Hazard-rating systems in forest insect pest LITERATURE CITED management: symposium proceedings. General Technical Report WO-27, USDA Forest Service, AMMAN, G.D. 1972. Mountain pine beetle brood produc­ Washington, DC. tion in relation to thickness of lodgepole pine FURNISS, M.M., M.D. MCGREGOR, M.W FOILES, AND A.D. phloem. Journal ofEconomic Entomology 65:138--140. PARTRIDGE. 1979. Chronology and characteristics of A\1MAN, G.D., AND J.A. LOGAN. 1998. Silvicultural control a Douglas-fir beetle outbreak in northern Idaho. ofmountain pine beetle: prescriptions and the influ­ General Technical Report INT-59, USDA Forest ence of microclimate. American Entomologist 44: Service, Intermountain Forest and Range Experi­ 166--177. ment Station, Ogden UT.

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FURNISS, RL., AND V.M. CAROLIN. 1977. Western forest mating extent of mortality associated with the Dou­ insects. Miscellaneous Publication 1339, USDA For~ glas-fir beetle in the Central and Northern Rockies. est Service, Washington, DC. Western Journal ofApplied Forestry 14(3):1-7. GOTIFRIED, GJ 1987. Regeneration ofpinyon. Pages 249­ NEGRON, lE, lL. WILSON, AND lA. ANHOLD. 2000. Stand 254 in RL. Everett, compiler, Proceedings: Pinyon­ conditions associated with roundheaded pine beetle Juniper Conference, 13-16 January 1986, Reno, NY. (Coleoptera: Scolytidae) infestations in Arizona and General Technical Report INT~215, Intermountain Utah. Environmental Entomology 29:20-27. Research Station, USDA Forest Service, Fort Collins, N ORU~SIS, M.J. 1999. SPSS regression models~. SPSS Inc., CO. Chicago, IL. HARD, lS. 1985. Spruce beetles attack slowly growing OLSEN, WK, J.M. SCHMID, AND S.A. MATA. 1996. Stand spruce. Forest Science 31:839-850. characteristics associated with mountain pine beetle HARD, lS., RA. WERNER, AND E.H. HOLSTEN. 1983. Sus­ infestations in ponderosa pine. Forest Science ceptibility of white spruce to attack by spruce bee­ 42:310-3;1.7. tles during the early years of an outbreak in Alaska. REYNOLDS, KM., AND E.H. HOLSTEN. 1994. Classification Canadian Journal ofForest Research 13:678-684. of spruce beetle hazard in Lutz spruce (Picea X HAWKSWORTH, EG. 1961. Dwarf mistletoe of ponderosa lutzii) stands on the Kenai Peninsula, Alaska. Cana­ pine in the Southwest. USDA Technical Bulletin dian Journal ofForest Research 24:1015-10;1.1. 1246, USDA, Washington, DC. ~. 1996. Classification ofspruce beetle hazard in Lutz _~__. 1977. The 6-class dwarf mistletoe rating system. and Sitka spruce stands on the Kenai Peninsula, General Technical Report RM-48, USDA Forest Ser­ Alaska. Forest Ecology and Management 84:251-262. vice, Rocky Mountain Forest and Range Experiment ROE, A.L., AND G.D. AMMAN. 1970. The mountain pine Station, Fort Collins, CO. beetle in lodgepole pine forests. Research Paper HAwKswORTH, EG., AND D.W JOHNSON. 1989. Biology and INT-71, USDA Forest Service, Intermountain Forest management of dwarfmistletoe in lodgepole pine in and Range Experiment Station, Ogden, UT. the Rocky Mountains. General Technical Report SAFRANYIK, L., D.M. SHRIMPTON, AND H.S. WHITNEY. 1974. RM-169, USDA Forest Service, Rocky Mountain Management of lodgepole pine to reduce losses Forest and Range Experiment Station, Fort Collins, from the mountain pine beetle. Forestry Technical CO. Report 1, Forestry Service, Environment Canada. HAWKSWORTH, EG., KC. LISTER, AND D.B. CAHILL. 1983. SAR1WELL, C. 1971. Thinning ponderosa pine to prevent Phloem thickness in lodgepole pine: its relationship outbreaks of mountain pine beetle. Pages 41--52 in to dwarf mistletoe and mountain pine beetle (Cole­ D.M. Baumgartner, editor, Proceedings: Precommer­ optera: Scolytidae). Environmental Entomology 12: cial Thinning of Coastal and Intermountain Forests 1447-1448. in the Pacific Northwest, 3-4 February 1971, Pull~ HAWKSWORTH, EG., AND C.G. SHAW III. 1984. Damage man, WA. Cooperative Extension Service and Depart­ and loss caused by dwarf mistletoes in coniferous ment ofForest and Range Management, Washington forests ofwestern North America. Pages 285-297 in State University, Pullman. RKS. Wood and G.J. JeIlis, Plant diseases: infection, SARTWELL, C., AND RE. STEVENS. 1975. Mountain pine damage, and loss. Blackwell Scientific Publications, beetle in ponderosa pine, prospects for silvicultural Oxford. control in second~growthstands. Journal of Forestry HEDDEN, RL. 1981. Hazard~rating system development 73:136---140. and validation: an overview. Pages 9-12 in Hazard­ SAS INSTITUTE. 1999. SAS/STAT@ user's guide, version 8. rating systems in forest insect pest management: SAS Institute Inc., Cary, NC. 3884 pp. symposium proceedings. General Technical Report SCHMID, J.M., AND RH. FRYE. 1976. Stand ratings for WO-27, USDA Forest Service, Washington, DC. spruce beetles. Research Note RM-309, USDA For­ HOPPING, G.R 1965. North American species in group IX est Service, Rocky Mountain Forest and Range Ex­ of Ips De Geer (Coleoptera: Scolytidae). Canadian periment Station, Fort Collins, CO. Entomologist 97:422-434. SCHMID, J.M., AND S.A. MATA. 1992. Stand density and LONG, J.N., AND T.W DANIEL. 1990. Assessment of grow­ mountain pine beetle-caused tree mortality in pon­ ing stock in uneven-aged stands. Western Journal of derosa pine stands. Research Note RM-515, USDA Applied Forestry 5:93-96. Forest Service, Rocky Mountain Forest and Range MCCAMBRIDGE, EE, EG. HAWKSWORTH, C.B. EDMINSTER, Experiment Station, Fort Collins, CO. AND lG. LAUT. 1982. Ponderosa pine mortality result­ SCHMID, J.M., S.A. MATA, AND RA. OBEDZINSKI. 1994. ing from a mountain pine beetle outbreak. Research Hazard rating ponderosa pine stands for mountain Paper RM-235, USDA Forest Service, Rocky Moun~ pine beetles in the Black Hills. Research Note RM­ tain Forest and Range Experiment Station, Fort 529, USDA Forest Service, Rocky Mountain Forest CoIlins, CO. and Range Experiment Station, Fort CoIlins, CO. NEGRON, lE 1991. Estimating probabilities of infestation SCHULER, T.M., AND EW SMITH. 1988. Effect of species and extent ofdamage by the roundheaded pine bee­ mix on size/density and leaf-area relations in south­ tle in ponderosa pine in the Sacramento Mountains, west pinyon/juniper woodlands. Forest Ecology and New Mexico. Canadian Journal of Forest Research Management 25:211-220. 27:1936---1945. SHRIMPTON, D.M., AND A.J. THOMPSON. 1983. Growth _--_-__. 1998. Probability ofinfestation and extent of mor~ characteristics oflodgepole pine associated with the tality associated with the Douglas-fir beetle in the start of mountain pine beetle outbreaks. Canadian Colorado Front Range. Forest Ecology and Manage­ Journal ofForest Research 13:137-144. ment 107:71-85. SMITH, EW, AND T. SCHULER. 1988. Yields of southwest­ NEGRON, J.E, WC. SCHAUPp, JR., KE. GIBSON, J. ANHOLD, ern pinyon-juniper woodlands. Western Journal of D. HANSEN, R THIER, AND P. MOCETIINI. 1999. Esti- Applied Forestry 3:70-74. 2003] SUSCEPTIBILITY TO PINON Ips INFESTATION 451

STEVENS, RE., AND H.W FLAKE, JR. 1974. A roundheaded case study. Pages 187-190 in Ecology and manage­ pine beetle outbreak in New Mexico. Research Note ment of oak and associated woodlands: perspectives RM-259, USDA Forest Service, Rocky Mountain in the southwestern United States and northern Forest and Range Experiment Station, Fort Collins, Mexico. General Technical Report RM-218, USDA CO. Forest Service, Rocky Mountain Forest and Range STEVENS, RE., AND EG. HAWKswORTH. 1984. Insect-dwarf Experiment Station, Fort Collins, CO. mistletoe associations: an update. Pages 9~101 in WOOD, D.L. 1982. The role of pheromones, kairomones, EG. Hawksworth and R.E Scharpf, technical coordi­ and allomones in the host selection and colonization nators, Biology of dwarf mistletoes: proceedings of behavior of bark beetles. Annual Review of Ento­ the symposium. General Technical Report RM-111, mology 27:411-446. USDA Forest Service, Rocky Mountain Forest and WOOD, S.L., AND D.E. BRIGHT, JR. 1992. A catalog of Range Experiment Station, Fort Collins, CO. Scolytidae and Platypodidae (Coleoptera), part 2: WARING, RH., AND G.B. PITMAN. 1980. A simple model taxonomic index, volume A. Great Basin Naturalist for host resistance to bark beetles. Research Note Memoirs 13, Brigham Young University, Provo, UT. 65, Forest Research Laboratory, School of Forestry, Oregon State University, Corvallis. Received 28 January 2002 WILSON, J.L., AND B.M. TKAcz. 1992. Pinyon ips outbreak Accepted 26August;l002 in pinyon juniper woodlands in northern Arizona: a