Role of Plant Enemies in the Forestry of Indigenous Vs

Ecological Applications, 18(5), 2008, pp. 1171–1181 Ó 2008 by the Ecological Society of America

ROLE OF PLANT ENEMIES IN THE FORESTRY OF INDIGENOUS VS. NONINDIGENOUS PINES

1,3 1 2 MARI´A J. LOMBARDERO, PATRICIA VA´ZQUEZ-MEJUTO, AND MATTHEW P. AYRES 1Departamento de Produccio´n Vegetal, Universidad de Santiago, 27002 Lugo, Spain 2Department of Biological Sciences, Dartmouth College, Hanover, New Hampshire 03755 USA

Abstract. Plantations of rapidly growing trees are becoming increasingly common because the high productivity can enhance local economies, support improvements in educational systems, and generally improve the quality of life in rural communities. Landowners frequently choose to plant nonindigenous species; one rationalization has been that silvicultural productivity is enhanced when trees are separated from their native herbivores and pathogens. The expectation of enemy reduction in nonindigenous species has theoretical and empirical support from studies of the enemy release hypothesis (ERH) in the context of invasion ecology, but its relevance to forestry has not been evaluated. We evaluated ERH in the productive forests of Galicia, Spain, where there has been a profusion of pine plantations, some with the indigenous Pinus pinaster, but increasingly with the nonindigenous P. radiata. Here, one of the most important pests of pines is the indigenous bark beetle, Tomicus piniperda. In support of ERH, attacks by T. piniperda were more than twice as great in stands of P. pinaster compared to P. radiata. This differential held across a range of tree ages and beetle abundance. However, this extension of ERH to forestry failed in the broader sense because beetle attacks, although fewer on P. radiata, reduced productivity of P. radiata more than that of P. pinaster (probably because more photosynthetic tissue is lost per beetle attack in P. radiata). Productivity of the nonindigenous pine was further reduced by the pathogen, Sphaeropsis sapinea, which infected up to 28% of P. radiata but was absent in P. pinaster. This was consistent with the forestry axiom (antithetical to ERH) that trees planted ‘‘off-site’’ are more susceptible to pathogens. Fungal infections were positively correlated with beetle attacks; apparently T. piniperda facilitates S. sapinea infections by creating wounds and by carrying fungal propagules. A globally important component in the diminution of indigenous ﬂora has been the deliberate large-scale propagation of nonnative trees for silviculture. At least for Pinus forestry in Spain, reduced losses to pests did not rationalize the planting of nonindigenous trees. There would be value in further exploration of relations between invasion ecology and the forestry of nonindigenous trees. Key words: enemy release hypothesis; exotic plants; forestry; herbivory; host choice; invasions; pathogen; Pinus pinaster; Pinus radiata; plantations; silviculture; Tomicus piniperda.

INTRODUCTION this principle applies, foresters would tend to benefit In recent history, foresters throughout the world have from working with indigenous tree species. On the other been introducing new tree species in efforts to increase hand, there might be advantages to nonindigenous trees forest productivity and meet the increasing demand for if they have been separated from their native herbivores wood in their countries (Zobel et al. 1987, Boyle et al. and pathogens (Sedjo 1983, Zobel et al. 1987, Gadgill 1999). The success or failure of silvicultural operations is and Bain 1999, Wingfield 2003). often determined by losses to herbivores and pathogens The idea that populations might suffer less damage (Graham 1939, Tainter and Baker 1996), which might be from biotic enemies when they occur outside their systematically different between indigenous and nonin- historical range has a long history (Darwin 1859, Elton digenous tree species (Gadgill and Bain 1999). For 1958), but has recently been formalized as the enemy example, it is axiomatic in forestry that trees can be release hypothesis (ERH; Williamson 1996, Crawley more susceptible to pests and pathogens when they are 1997) and has received considerable interest because of planted ‘‘off-site,’’ i.e., outside the soil and climate its relevance to invasion ecology (Keane and Crawley system to which they are adapted (Graham 1939, 2002, Stamp 2003, Colautti et al. 2004, Hierro et al. Kozlowski 1969, Speight and Wainhouse 1989). Where 2005). One prediction of ERH is that biotic enemies will have less impact on populations that have become established outside their indigenous range compared to Manuscript received 27 June 2007; revised 3 January 2008; accepted 8 January 2008. Corresponding Editor: B. A. populations of the same species occurring within their Hungate. historical distribution (e.g., DeWalt et al. 2004, Cripps et 3 E-mail: [email protected] al. 2006, Ishtiaq et al. 2006). This prediction is a 1171 1172 MARIÁ J. LOMBARDERO ET AL. Ecological Applications Vol. 18, No. 5 foundation for biological control programs (Vila et al. about 1950 in the Basque Country and about 1970 in 2005) and for the theory of evolution of increased Galicia (Alvarez 2004). Now the landscape of Galicia competitive ability (Blossey and No¨tzold 1995, Stastny contains a mosaic of pine stands that are P. radiata, P. et al. 2005, Blumenthal and Hufbauer 2007). Another pinaster, or (occasionally) a mixture of the two species. prediction, or perhaps extension, of ERH is that Tomicus spp. (Coleoptera: Scolytinae) are among the nonindigenous populations will experience less damage most ubiquitously important pests of pine in Eurasia from enemies than similar indigenous species with which (Bakke 1968, Browne 1968, La˚ngstro¨m 1983). T. they now co-occur (Agrawal et al. 2005, Cappuccino and piniperda (L.) and T. destruens (Woll.), both indigenous Carpenter 2005, Liu et al. 2007). This latter prediction is to Galicia (Gallego et al. 2004, Vasconcelos et al. 2006), of particular relevance to plant invasions because of the are indistinguishable from their feeding damage, and frequent importance of interspecific competition (Lau were considered synonymous until recently separated and Strauss 2005, Moorcroft et al. 2006, Epstein and using molecular techniques (Gallego and Galiań 2001, Molofsky 2007). It is also of importance to evaluating Kerdelhue et al. 2002, Kohlmayr et al. 2002); morpho- plants introduced for economic reasons, including forest logical separation remains uncertain (Pfeffer 1995, trees. To avoid confusion with the broader sense of Kohlmayr et al. 2002, Faccoli 2006). The biology of T. ERH, we refer to this specific theoretical prediction as piniperda, and its capacity for damaging forest produc- ‘‘enemy reduction in nonindigenous species’’ or ERNS. tivity, has been well documented, especially for northern One potential problem in extending ERNS to countries (e.g., Bakke 1968, Salonen 1973, La˚ngstro¨m silviculture is that previous studies have generally 1983), but there are also reports of damage to trees in focused on short-lived herbaceous plants (e.g., Agrawal nearly all European countries (e.g., Chararas 1968, et al. 2005, Liu and Stiling 2006, Parker and Gilbert Masutti 1969, Amezaga 1997) and in the United States 2007), which might be systematically different from trees (Czokajlo et al. 1997), where it recently has been because the relatively long lifespan of trees increases the accidentally introduced (Haack and Kucera 1993). Pinus probability of being colonized by indigenous enemies sylvestris L. tends to be the most common host of T. that are sufficiently polyphagous that they recognize and piniperda in central to northern Europe (La˚ngstro¨m attack nonindigenous trees. Presumably, the risks for 1984). In southern Europe, the beetle has traditionally nonindigenous trees from endemic herbivores and fed upon the indigenous pines, Pinus pinaster and P. pathogens depends upon whether the native forest nigra Arnold (Lieutier et al. 1997), but now also attacks community already contains tree species that are related P. radiata (Lombardero 1995, Amezaga 1996, 1997). T. to the introduced tree and therefore harbor enemies that destruens is poorly studied by comparison, but differs in can switch to the new tree (Roques et al. 2006). Another that it leaves shoots to attack stems in October to reason why ERNS might not extend to forestry is that January (Gallego and Galiań 2001) vs. early spring for the diversity and abundance of plant enemies is not T. piniperda (Kohlmayr et al. 2002). We assume that T. necessarily correlated with impacts on plant productiv- piniperda was the main species in our studies because ity. That is, plants may become adapted to their beetles were leaving the shoots in February to early historically important herbivores such that growth losses April. are minimized. In this case, introduced trees might suffer T. piniperda beetles cause three types of damage to greater losses of productivity than their indigenous trees: (1) they excavate galleries within the phloem of the counterparts even if the intensity of attacks by main stem, which interferes with vascular transport and herbivores and pathogens is comparable. Here we tested may kill the tree; (2) they feed on shoots in the canopy, whether ERNS explains patterns of herbivore attacks which involves excavating galleries in terminal branches, and tree growth within the silviculturally important thereby making branches more susceptible to wind region of Galicia, in northwestern Spain, where the breakage, reducing photosynthesis, destroying buds that nonindigenous pine, Pinus radiata D. Don., has recently would otherwise form shoots in the following year, and become a frequent choice of landowners over the leading to multiple-shoot malformations; and (3) they indigenous pine, Pinus pinaster Ait. facilitate the introduction of fungi that may be Pinus pinaster (maritime pine) occurs naturally pathogenic and/or produce staining in the xylem that throughout the Mediterranean region (including north- lowers the commercial value of wood (Seifert 1993). western Spain), and has good growth in our study area Sphaeropsis sapinea (Fr.) Dyko and Sutton (Diplodia of ;10 m3ha1yr1. However, Galician landowners tip blight, formerly Diplodia pinea (Desm.) Kickx) is a have begun to plant P. radiata instead of P. pinaster, fungal pathogen of pines. It is presumed to be mainly because P. radiata can attain even higher indigenous to western Europe because it was first productivity on the same sites (;15 m3ha1yr1; Xunta described from France (in 1842). Nowadays, S. sapinea de Galicia 1992). Radiata pine, indigenous to California, appears to be globally present wherever there is Pinus, is among the most widely planted tree species in the and it can be a consequential pathogen for numerous world, especially in the Southern Hemisphere (Lavery pines in ecosystems across the world (de Wet et al. 2000). and Mead 1998). It was introduced to Spain from Normally the fungus enters the plants through small France in about 1840, but was not widely planted until wounds (e.g., from insects or weather damage) and then July 2008 PESTILENCE AND PINE FORESTRY 1173 invades the tissue, causing dieback of the shoots and the In spring of 2004 we estimated the levels of crown death of the trees. Our studies included measurements of damage within each stand as the percentage of shoots S. sapinea damage because of its potential association that were attacked. Within all except eight stands, this with bark beetles. was done by complete measurement of five randomly We tested for ERNS with respect to feeding attacks by selected trees. For each tree, we calculated the percent- T. piniperda in crown shoots. This is the most age of shoots that had been attacked, which was widespread damage by T. piniperda.Reproductive apparent because of (1) drooping shoots, and/or (2) attacks in the stem are more catastrophic for the host the presence of a blob of resin at the entrance hole, tree (usually fatal), but are relatively rare in southern and/or (3) the presence of multiple shoots induced by Europe and restricted to occasional episodes of beetle previous shoot breakage. Thus, the measurements were outbreaks (La˚ngstro¨m and Hellqvist 1990, 1993). a composite of shoot damage over the previous two to Because the importance of enemy release for silviculture three years. In eight stands with the largest trees, we is mainly about the impacts on forest productivity, we randomly selected four main branches per tree, one in also tested the prediction that T. piniperda would reduce each cardinal direction, and calculated the average of growth of the indigenous P. pinaster more than it did the percentage of damage of the four branches. nonindigenous P. radiata. The main statistical analyses used stands as the sample unit. Each stand had an independent history METHODS (mostly different landowners), and ancillary analyses Study area confirmed that shoot damage was highly variable among Field studies were conducted near the small city of stands and quite homogenous within stands. We used Ra´bade, in Galicia, Spain. To address our research the following statistical model to compare attacks in questions, we needed a landscape with a mosaic of stands of the two species across the gradient of beetle alternative pine species and a gradient of T. piniperda abundance produced by the timber yard, while account- abundance. Galicia provided this in that the pine forests ing for effects of stand age: mainly consist of thousands of small private land A ¼ b þ b 3 lnðDÞþb 3 Age þ e ð1Þ holdings (usually ,1 ha) that have irregular boundaries 0 1 2 and are interspersed with scrub, cropland, grazing land, where A is the percentage of shoots attacked, trans- and small settlements. Occasional timber yards provide a formed to a normal distribution as ln(percentage þ 0.1), source of large numbers of T. piniperda that arrive with ln(D) is the natural log of distance in meters to the center the logs and emerge and disperse into the landscape of the timber yard, Age is the stand age in years, b’s are before the logs are sawed (La˚ngstro¨m and Hellqvist 1990, the coefficients fit to the data, and e is the residual for Borkowski 2001). This produces a gradient of T. each stand. The logarithmic transformation of distance piniperda abundance in the surrounding landscape. We provided a simple approximation of a diffusion model located such a timber yard that was centered in an area (Turchin and Thoeny 1993), assuming that the timber with numerous interspersed stands of Pinus pinaster and yard was the source of beetles. After fitting Eq. 1 to the P. radiata (Fig. 1). Pine plantations were 1–16 years old data, we visually evaluated the residuals for patterns and were established after construction of the sawmill; with respect to distance, stand age, and spatial location trees were planted 2.5 m apart in rows separated by 3.0– within the landscape. We then tested for differences in 3.5 m (usually 50–400 trees per stand). The study area shoot attacks between pine species by adding species as a was 390–450 m above sea level and was relatively categorical variable to the general linear model (equiv- homogenous with respect to soils (‘‘tierra parda de gley’’) alent to comparing the residuals of Eq. 1 between and climate (oceanic with a continental character). The species). annual mean temperature is 128–148C, with mean winter The fungus Sphaeropsis sapinea and summer temperatures of 58–68C and 208–228C, respectively. Under these conditions, T. piniperda over- In each of the 45 stands, we also recorded the number winter within the shoots of their host species. of trees infected by the fungus Sphaeropsis sapinea.In most cases, we did this by examining each tree within the Landscape pattern of attack preferences by T. piniperda stand, but in the three largest stands, we scored 100 trees We established a sampling design centered on the within a randomly located plot within the stand. Trees logging yard (4381270 N, 786410 W) that was presumed were classified as infected if there was clear evidence of to provide a source of colonizing bark beetles (Fig. 1, the distinctive shoot dieback and stem cankers from S. Appendix). Examination of the log yard verified the sapinea. presence of large numbers of T. piniperda; the study area contained no other comparable sources of T. piniperda. Comparison of attacks and growth in mixed-species stands We identified for study a total of 45 pine stands within We were also able to locate five even-aged stands that 1600 m of the logging yard (9:36 P. pinaster : P. radiata). contained a mix of P. pinaster and P. radiata, and Some other stands that had been fertilized or pruned encompassed a range of beetle attack densities. We used were excluded from the study. these stands to compare the effects of T. piniperda on 1174 MARIÁ J. LOMBARDERO ET AL. Ecological Applications Vol. 18, No. 5

FIG. 1. Location of the 45 study stands relative to the sawmill log yard (X at center), which provided a source of indigenous bark beetles, Tomicus piniperda. Solid circles represent Pinus pinaster (indigenous), and open circles represent Pinus radiata (introduced). Symbol sizes indicate the percentage of shoots attacked (standardized to that expected for stands of an average age of 6.2 years). growth of the two pine species. In each stand, we escaped beetle attacks, but were on the same soil and measured trunk diameter (at 1.30 m height), height, and experiencing the same climate (5–10 km from the percentage of crown damage of 15 randomly selected sawmill). Within each plantation, we measured the trees of each species. Crown damage was measured on diameter and height of a random sample of 10 trees, four randomly selected main branches per tree. We and determined the age of the plantation. tested for differences between species in all three variables with an ANOVA model that included stand, RESULTS species, and stand 3 species. Analyses of shoot damage Landscape pattern of attacks by Tomicus piniperda also included tree nested within stand 3 species as a random effect. Results supported the prediction of enemy reduction In the same stands, to compare the plant tissue lost in nonindigenous species (ERNS) in that Tomicus per attack by T. piniperda, we measured the diameter piniperda showed a preference for P. pinaster over P. and length of 106 P. pinaster shoots and 102 P. radiata radiata when attacking pine shoots within which to feed shoots that had broken off at the point of T. piniperda and overwinter (Fig. 2). Raw attack measurements attack and fallen to the ground (17–53 shoots per species (percentage of shoots attacked) were 18.5% 6 8.5% per stand). (mean 6 SE) vs. 5.9% 6 2.3% for P. pinaster vs. P. radiata (n ¼ 9, 36, respectively; Appendix). The study Comparison of tree growth in the absence of beetle attacks included a broad range of damage from T. piniperda due To verify that P. radiata can grow faster than P. to variation in proximity to the lumberyard and stand pinaster in the absence of beetle attacks, we located an age (Appendix, Fig. 1). Fitting Eq. 1 to the data showed additional three plantations of each species that had strong effects of both distance and stand age (P , July 2008 PESTILENCE AND PINE FORESTRY 1175

for Fisher exact test of difference between species). Among stands of P. radiata, the presence of the fungus was strongly related to crown damage from T. piniperda (Fig. 3).

Comparison of attacks in mixed-species stands Comparisons of attacks within mixed-species stands also supported the enemy release hypothesis by indicating higher attacks by the indigenous insect, T. piniperda, on the indigenous pine, P. pinaster, compared to the introduced pine, P. radiata. Across the ﬁve stands, the percentage of attacks ranged from 1.5% to 76%, and was always slightly higher in P. pinaster compared to P. radiata (Fig. 4a; for comparison of

species, F1, 140 ¼ 9.35, P ¼ 0.003; for comparison of stands, F4, 140 ¼ 407.20, P , 0.0001; for stand 3 species, F4, 140 ¼ 1.65, P ¼ 0.16). Variation among trees within stands and species was immeasurably low (F140, 450 ¼ 0.99, P ¼ 0.50). FIG. 2. Comparison of shoot attacks by T. piniperda in indigenous vs. introduced pines (P. pinaster vs. P. radiata)in There was a dramatic difference between P. pinaster Galicia, Spain. Each point represents one pine stand within a and P. radiata in the average length of a shoot that was landscape that included a range of low to high beetle abundance lost as the result of one T. piniperda attack: 10.6 6 0.4 (Fig. 1). Attack densities were standardized to that expected for cm vs. 17.1 6 0.6 cm, respectively (mean 6 SE; F ¼ stands of average age (6.2 years) and average northing (1317 1, 200 m). Note the log–log scale. 85.62, P , 0.0001). Variation among stands was modest by comparison (F6, 200 ¼ 4.14, P , 0.0006). In contrast,

2 beetles attacked shoots at about the same diameter in 0.0001 for both parameters, r ¼ 0.67). Examination of both species: 5.4 6 0.15 mm vs. 5.8 6 0.16 mm, the residuals indicated a pattern of decreasing attacks respectively (F ¼ 4.21, P ¼ 0.04). Again, there was from south to north, so we expanded Eq. 1 to include 1, 200 modest but significant variation among stands (F ¼ b 3 N, where N was northing in meters (Appendix), and 6, 200 3 3.88, P , 0.001). In P. radiata, the length (L, in cm) of b was a coefficient fit the data. This yielded the 3 killed shoots increased with diameter (D, in mm) at the following model: point of attack as L ¼ 5.9 þ D 3 2.07 (6 0.36 mm) (r2 ¼ A ¼ 17:38 2:68 3 lnðDÞþ0:39 3 Age 0:000552 3 N 0.24, P , 0.0001, N ¼ 102). In contrast, the length of ð2Þ killed shoots was barely related to diameter in P. pinaster: L ¼ 7.8 þ D 3 0.46 (60.23 mm) (r2 ¼ 0.03, P 2 where r ¼ 0.74, and ln(D), Age, and N were each ¼ 0.05, N ¼ 106). significant at P , 0.002 (t40 ¼ 8.27, 6.08, and 3.30, respectively). Average attack intensities in an average- aged stand (6.2 years) declined exponentially with distance from the timber yard, from ;15% at 450 m to ;2.2% at 900 m and ;0.3% at 1800 m (Fig. 2). At 600 m from the timber yard, the average percentage of shoots attacked increased from 3% to 6% to 14% to 30% as stand age increased from 4 to 6 to 8 to 10 years, respectively. After accounting for effects of spatial location and stand age, attacks on P. pinaster were still significantly greater than on P. radiata (t40 ¼ 8.60, P , 0.0001; Fig. 2). In back-transformed units, the expected attack intensities were 2.4-fold greater on P. pinaster than on P. radiata (e.g., 20% vs. 8% of shoots attacked in six-year-old stands of P. pinaster vs. P. radiata at 500 m from the source, 3.2% vs. 1.3% in six-year-old stands at 1000 m, and 14% vs. 6% in 10-year-old stands at 1000 m (Eq. 2, Fig. 2). FIG. 3. The percentage of P. radiata trees within a stand Fungus attacks that were infected with the fungal pathogen Sphaeropsis sapinea (log scale) was strongly related to crown damage by Tomicus Sphaeropsis sapinea infected 17 of 36 stands of P. piniperda (r2 ¼ 0.85, P , 0.0001, second-order polynomial, N ¼ radiata, but none of 9 stands with P. pinaster (P ¼ 0.009 39 stands). 1176 MARIÁ J. LOMBARDERO ET AL. Ecological Applications Vol. 18, No. 5

22.1 6 0.5 cm vs. 16.9 6 0.7 cm, and average heights were 11.45 6 0.22 m vs. 8.70 6 0.33 m (corresponding to stem volumes of 0.18 vs. 0.10 m3/tree for P. radiata vs. P. pinaster; Ministerio de Medio Ambiente 2002). Analysis of mixed-species stands situated near the sawmill showed that this growth differential disappeared or was even reversed in the presence of beetle attacks. Average tree diameter ranged from 5 cm to 22 cm across stands that were 6–16 years of age (Fig. 4b). Although beetle attacks were more frequent on P. pinaster, and P. radiata grew faster than P. pinaster in the absence of beetle attacks, tree diameter of the two species was nearly identical in four of ﬁve mixed-species stands near the sawmill. In the stand with highest beetle attacks, the diameter of P. pinaster was actually ;15% larger than surrounding P. radiata (Fig. 4b, 15-year-old stand). Similarly, the height growth of P. radiata pine was no more than that of P. pinaster in the two stands with .15% of shoots attacked (Fig. 4c, 15- and 16-year-old stands). P. radiata only exhibited its potential for greater height growth in two stands that experienced low beetle attacks (10- and 13-year-old stands).

DISCUSSION In support of ERNS and the enemy release hypothesis, attacks by the indigenous herbivore, Tomicus

FIG. 4. Comparison of P. pinaster and P. radiata within ﬁve mixed-species stands with respect to (a) the percentage of shoots in the crown attacked (log–log scale), (b) tree diameter (dbh, measured at 1.30 m), and (c) tree height. Each stand is represented by a point (mean 6 SE). Points above or below the diagonal line of equality indicate stands where the average for P. radiata was higher or lower, respectively, than the average for P. pinaster.

Comparison of tree growth As expected, P. radiata grew considerably faster than FIG. 5. Tree diameter (dbh) and height (means 6 SE) in P. pinaster in the absence of beetle attacks (Fig. 5). At three stands each of P. pinaster and P. radiata that escaped eight years old, for example, the average diameters were beetle attacks, in relation to stand age. July 2008 PESTILENCE AND PINE FORESTRY 1177 piniperda, were more than twice as great in stands of the that attack shoots of P. radiata vs. P. pinaster. If there is indigenous pine, P. pinaster, compared to stands of its no fitness cost for beetles that choose shoots of P. nonindigenous congener, P. radiata. This pattern held radiata, natural selection might favor behavioral chang- across a range of tree ages and proximity to beetle es in the beetles that erode the difference between pine source. P. pinaster also sustained more attacks than P. species in the intensity of shoot attacks by T. piniperda. radiata when the species were intermixed within stands, From a practical standpoint, reduced herbivory on although the difference was less (back-transformed introduced tree species only benefits forestry if it means ¼ 2.5% vs. 1.7% of shoots attacked; Fig. 4a). translates into increased productivity. The enemy release Thus, the silvicultural potential of P. radiata introduced hypothesis failed this test because, even though P. to Galicia might be enhanced by reduced attacks from radiata sustained fewer attacks than P. pinaster, the biotic enemies. This is analogous to the tendency for deleterious impacts on growth were actually greater for increased weediness in many introduced herbaceous P. radiata (eliminating or even reversing the tendency plants because of reduced herbivory (reviewed by for higher productivity of P. radiata in the absence of Colautti et al. 2004, Liu and Stiling 2006). It has been beetle attacks). We hypothesize that this is because a hypothesized that a secondary consequence of release larger fraction of photosynthetic tissue is lost per beetle from herbivore pressure would be reduced allocation to attack in P. radiata than in P. pinaster. The species are defenses by the introduced plants (because the defenses alike in that photosynthesis occurs within repeated have less value when herbivory is reduced), which could similarly sized modules of needle-bearing shoots that lead to the evolution of even faster growth (‘‘evolution extend from growing branches. Following an attack by of improved competitive ability’’ or EICA; Blossey and T. piniperda, the shoot distal to the point of attack dies No¨tzold 1995). If valid, EICA would have relevance for and falls to the ground, along with the needles that it forestry as well as weed ecology, although the most held. However, the average length of these lost shoots is obvious implications would be for tree breeding markedly longer in P. radiata compared to P. pinaster programs since natural selection is frequently con- (17.1 cm vs. 10.6 cm, respectively). This is because the strained in silviculture by long generation times, shoots of P. radiata are relatively slender compared to P. recurring plantings of ‘‘immigrant’’ genotypes, and pinaster, and T. piniperda attacks where the diameter limited natural regeneration (Mortenson and Mack was 5–6 mm, presumably because this matches the size 2006). of the internal feeding gallery required by the insect A simple explanation for higher attacks on P. pinaster (Haack et al. 2001). Since more of each shoot is lost per is that the indigenous herbivore has evolved host-finding beetle attack in P. radiata compared to P. pinaster,a behaviors that favor locating and accepting the indige- larger proportion of photosynthetic tissue is destroyed nous pine for feeding attacks. The appearance and with the same percentage of shoots attacked. Besides the secondary chemistry of P. pinaster and P. radiata are differences in shoot morphology, greater growth losses qualitatively similar. They share at least 24 different in P. radiata may also involve developmental responses terpenoid compounds, with a-pinene being a major to loss of apical meristems on branches (Honkanen et al. constituent in both species (Petrakis et al. 2001, 2005). 1994, Marquis 1996). Further study would be required However, these species are within different subsections to test if the high tolerance of P. pinaster to its native of the genus (Pinus vs. Anttenuatae; Price et al. 1998), herbivore is an adaptation or a coincidence, but it is and herbivores of pine are well attuned to subtle logical that plant populations will tend to suffer greater differences in host plant chemistry (Volz 1988, Almquist impacts from herbivores with which they lack an et al. 2006, Erbilgin et al. 2007). The terpene profiles of evolutionary history (Strauss and Agrawal 1999). these two species differ in numerous qualitative and The potential benefits to P. radiata of reduced attacks quantitative features that could influence host location by T. piniperda were further negated by its susceptibility and attack by Tomicus piniperda (Cool and Zavarin to the fungus S. sapinea. Although the logic of the 1992, Petrakis et al. 2005, Santos et al. 2006). enemy release hypothesis is easily extended from The fact that differences in attacks were less within herbivorous insects to plant pathogens, relatively few mixed-species stands than among single species stands studies have compared effects of pathogens on indige- suggests that discrimination between P. pinaster and P. nous vs. nonindigenous plants and the results have been radiata by T. piniperda involves more than contact variable (Blaney and Kotanen 2001, Georgen and chemoreception, and might include behavioral tenden- Daehler 2001, Mitchell and Power 2003, Parker and cies to forage within monospecific aggregations of P. Gilbert 2004, Agrawal et al 2005). The effects of S. pinaster. Host species preferences of the southern pine sapinea in Galicia ran counter to ERNS in that the beetle, Dendroctonus frontalis Zimm., the Bast scale, indigenous pine was completely uninfected or asymp- Matsucoccus feytaudi Duc., and perhaps many forest tomatic when growing interspersed with P. radiata that insects, also vary with the spatial scale at which their were highly infected. This could be explained by the host species are mixed (Jactel et al. 2005, 2006, Ylioja et hypothesis (antithetical to ERNS) that trees grown al. 2005, Martinson et al. 2007). It remains unknown outside their natural range (‘‘off-site’’) tend to be more whether there are fitness consequences for T. piniperda susceptible to pests and pathogens (Kozlowski 1969). In 1178 MARIÁ J. LOMBARDERO ET AL. Ecological Applications Vol. 18, No. 5 fact, S. sapinea, which is an opportunistic pathogen of recognized as a potential host by T. piniperda. In our conifers worldwide, is noted for causing little damage in study area (Galicia, Spain), silvicultural introductions natural settings even while having large impacts on pines have been dominated by two trees: Eucalyptus spp. and planted outside of their natural range (Eldridge 1961, Pinus radiata. Within two decades of widespread Swart et al. 1985, Harrington and Wingfield 1998). P. plantings, five of the pests traditionally associated with pinaster is not intrinsically immune to S. sapinea because P. pinaster in Galicia had become common pests of P. plantations in Hawaii have been seriously afflicted (Bega radiata (Halder 2002), and practically all conifer bark et al. 1978). Significant damage from S. sapinea has also beetles in the area are able to attack and reproduce in been reported for Pinus patula Schiede & Deppe and P. this tree species (Lombardero 1995). In contrast, not a radiata in South Africa (Harrington and Wingfield single indigenous insect has been recorded feeding on 1998), and for Pinus nigra in the United States (Peterson Eucalyptus. Presumably, this is because Eucalyptus is so 1981, Whitehill et al. 2007). Galicia is at an unusually far removed chemically from any indigenous plants that high latitude for plantings of P. radiata and winter no indigenous herbivores were preadapted to exploit it. climatic conditions there might predispose P. radiata for Nonetheless, the absence of herbivores on Eucalyptus infection by S. sapinea. Frost and minimum winter was short lived. Nearly as quickly as indigenous temperatures factors are recognized as factors that limit herbivores became pests of P. radiata, the Eucalyptus site suitability for P. radiata in Galicia (Lavery and snout beetle (Gonipterus scutellatus Gyllenhal, indige- Mead 1998) and have been implicated as facilitators of nous to Australia) became established in Galicia S. sapinea damage to pines in other regions (Bega et al. (Mansilla 1992) and became a severe pest (Cordero 1978, de Wet et al. 2000). and Satolamazza 2000). It can be said that this Probably the damage to P. radiata from S. sapinea introduction was a predictable consequence of interna- was also facilitated by Tomicus piniperda. There was a tional commerce (Brockerhoff et al. 2006). The resulting strong correlation between T. piniperda attacks and pestilence was also predictable because the snout beetles infections by S. sapinea (Fig. 3), and causation is likely themselves lack natural enemies in this region (an based on two mechanisms. First, S. sapinea generally application of the enemy release hypothesis at the next enters trees through existing wounds, such as those on higher trophic level; Mack et al. 2000). The recent shoots that break off after attacks by T. piniperda.InP. history of forestry includes numerous dramatic examples resinosa Ait., S. sapinea infections are facilitated by of herbivores that had only modest impacts in their wounding from bark beetles (Ips pini Say; Whitehill et native systems becoming major pests upon reaching al. 2007) and shoot and cone borers (especially regions where suitable host plants had been propagated Dioryctria spp.; Feci et al. 2002). Second, T. piniperda in large numbers: e.g., silviculture of P. radiata has been can function as a vector for fungal propogules. In plagued by Sirex noctilio F. in South America, New Ontario, where T. piniperda was recently introduced into Zealand, and Australia (Burgess and Wingfield 2001), by forests with a long history of S. sapinea infections, Rhyacionia buoliana (Denis & Schiffermu¨ller) in Chile culturable isolates of S. sapinea have already been found (Toro and Gessel 1999), and even by the normally on dispersing adults of T. piniperda and within T. benign Ips grandicollis (Eichhoff) in Australia (Abbott piniperda galleries in host trees (Hausner et al. 2005). 1993). The three-way association between P. radiata, T. The enemy release hypothesis suggests the attractive piniperda, and S. sapinea in Galicia adds to the examples prospect of high yield silviculture via escape from plant in which newly formed community interactions can pests (Gadgill and Bain 1999, Wingfield 2003). There is influence the establishment of nonindigenous plants, but ecological merit to the concept, as illustrated by our generalizations remain difficult because effects from results (Fig. 2), and the social and economic benefits can competitors, antagonists, and mutualists can benefit or be considerable (Sedjo 1983, Toro and Gessel 1999), at constrain populations of nonindigenous plants, depend- least in the short term. However, there are also reasons ing on the details (Nadel et al. 1992, Richardson et al. for questioning the widespread use of nonindigenous 2000, Mitchell et al. 2006). trees in forestry (Zobel et al. 1987). Reduced herbivory Nonetheless, there are some emerging principles does not necessarily translate into increased growth, regarding community interactions that are of clear which might be general if plants commonly become relevance to the use of nonindigenous trees in forestry. adapted to minimize growth losses from their native Herbivore damage to an introduced plant depends on herbivores (Leimu and Koricheva 2006, Parker et al. the availability of local herbivores that recognize the 2006). Furthermore, nonindigenous plants are not new plant as food and can cope with its defenses against necessarily released from pathogens; in fact, the attacks (Carpenter and Cappuccino 2005). The number susceptibility of trees to pathogens seems to often be of such potential colonizers will generally depend on the greater when they are planted outside of their natural phylogenetic relationship between the introduced plant distributions (Kozlowski 1969). Finally, the enemy and the indigenous flora (Mitchell et al. 2006, Roques et release hypothesis can also apply to the herbivores al. 2006). Although attacks by T. piniperda were less on themselves, which creates a risk of extreme pestilence if P. radiata than on the indigenous pine, it was still the nonindigenous trees are eventually colonized by July 2008 PESTILENCE AND PINE FORESTRY 1179 herbivores from the source of the introduction (Elton sustainable societies. Kluwer Academic Publishers, Boston, 1958), and the probability of this is enhanced by the Massachusetts, USA. increased commerce that naturally arises from silvicul- Brockerhoff, E. G., A. M. Liebhold, and H. Jactel. 2006. The ecology of forest insect invasions and advances in their tural success (Mack et al. 2000). There is a growing management. Canadian Journal of Forest Research 36:263– appreciation of losses to biodiversity and ecological 268. services that are associated with the replacement of Browne, F. G. 1968. Pest and diseases of forest plantation trees: indigenous flora by nonindigenous plants (Chapin et al. an annoted list of the principal species occurring in the 2000, Strauss 2001, Lodge et al. 2006). A globally British Commonwealth. Clarendon Press, Oxford, UK. Burgess, T. I., and M. J. Wingfield. 2001. Exotic pine forestry in important component of this trend has been the the Southern Hemisphere: a brief history of establishment deliberate large-scale propagation of nonindigenous trees and quarantine practices. South African Forestry Journal for silviculture (Zobel et al. 1987). At least for Pinus 192:79–83. forestry in Spain, reduced losses to pests do not provide a Cappuccino, N., and D. Carpenter. 2005. Invasive exotic plants strong rationale for planting nonindigenous trees. suffer less herbivory than non-invasive exotic plants. Biology Letters 1:435–438. ACKNOWLEDGMENTS Carpenter, D., and N. Cappuccino. 2005. Herbivory, time since introduction and the invasiveness of exotic plants. Journal of Research was supported by the Spanish Ministry of Ecology 93:315–321. Education, Grant: AGL2004-07507-C04-01/FOR and FEDER. Chapin, F. S., III, et al. 2000. Consequences of changing The manuscript benefited from comments from Paul Marino biodiversity. Nature 405:234–242. and Diego Gallego. Chararas, C. 1968. Adaptation faculty of Blastophagus piniperda L (Col., Scolytidae) on various Pinus and preference of LITERATURE CITED this insect with regard to these essences. Comptes Rendus Abbott, I. 1993. Review of the ecology and control of the Hebdomadaires des Seances de l’Academie des Sciences Serie introduced bark beetle Ips grandicollis (Eichhoff) (Coleop- D 266:238–241. tera: Scolytidae) in Western Australia, 1952–1990. CALM- Colautti, R. I., A. Ricciardi, I. A. Grigorovich, and H. J. Science 1:35–46. MacIsaac. 2004. Is invasion success explained by the enemy Agrawal, A. A., P. M. Kotanen, C. E. Mitchell, A. G. Power, W. release hypothesis? Ecology Letters 7:721–733. Godsoe, and J. Klironomos. 2005. Enemy release? An experi- Cool, L. G., and E. Zavarin. 1992. Terpene variability of ment with congeneric plant pairs and diverse above- and mainland Pinus radiata. Biochemical Systematics and Ecol- belowground enemies. Ecology 86:2979–2989. ogy 20:133–144. Almquist, A. C., J. Faldt, A. Yart, Y. Chevet, D. Sauvard, F. Cordero, A., and S. Satolamazza. 2000. The effect of three Lieutier, and A. K. Borg-Karlson. 2006. Selection in Tomicus species of Eucalyptus on growth and fecundity of the piniperda L.: composition of monoterpene hydrocarbons in Eucalyptus snout beetle (Gonipterus scutellatus). Forestry relation to attack frequency in the shoot feeding phase. 73:21–29. Zeitschrift fu¨r Naturforschung C 61:439–444. Crawley, M. J. 1997. Plant ecology. Blackwell Scientific, Alvarez, P. 2004. Viveros forestales y uso de planta en Oxford, UK. repoblacioń en Galicia. Universidad de Santiago, Santiago, Cripps, M. G., M. Schwarzlander, J. L. Mckenney, H. L. Hinz, Spain. and W. J. Price. 2006. Biogeographical comparison of the Amezaga, I. 1996. Monterrey pine (Pinus radiata D. Don) arthropod herbivore communities associated with Lepidium suitability for the pine shoot beetle (Tomicus piniperda L.) draba in its native, expanded and introduced ranges. Journal (Coleoptera: Scolytidae). Forest Ecology and Management of Biogeography 33:2107–2119. 86:73–79. Amezaga, I. 1997. Forest characteristics affecting the rate of Czokajlo, D., R. A. Wink, J. C. Warren, and S. A. Teale. 1997. shoot pruning by the pine shoot beetle (Tomicus piniperda L.) Growth reduction of Scots pine, Pinus sylvestris, caused by in Pinus radiata D. Don and P. sylvestris L. plantations. the larger pine shoot beetle, Tomicus piniperda (Coleoptera, Forestry 70:129–137. Scolytidae), in New York State. Canadian Journal of Forest Bakke, A. 1968. Ecological studies on bark beetles (Coleoptera: Research 27:1394–1397. Scolytidae) associated with Scots pine (Pinus sylvestris L.) in Darwin, C. 1859. On the origin of species by means of natural Norway with particular reference to influence of temperature. selection, on the preservation of favoured races in the Meddelelser fra det Norske Skogforsoksvesen 21:447–602. struggle for life. John Murray, London, UK. Bega, R. V., R. S. Smith, A. P. Martinez, and C. J. Davis. 1978. DeWalt, S. J., J. S. Denslow, and K. Ickes. 2004. Natural- Severe damage to Pinus radiata and P. pinaster by Diplodia enemy release facilitates habitat expansion of the invasive pinea and Lophodermium sp. on Malokai and Lanai in tropical shrub Clidemia hirta. Ecology 85:471–483. Hawaii. Plant Disease Repoter 62:329–331. De Wet, J., M. J. Wingfield, T. A. Coutinho, and B. D. Blaney, C. S., and P. M. Kotanen. 2001. Effects of fungal Wingfield. 2000. Characterization of Sphaeropsis sapinea pathogens on seeds of native and exotic plants: a test using isolates from South Africa, Mexico, and Indonesia. Plant congeneric pairs. Journal of Applied Ecology 38:1104–1113. Disease 84:151–156. Blossey, B., and R. No¨tzold. 1995. Evolution of increased Eldridge, K. G. 1961. Refreshing the genetic resource of Pinus competitive ability in invasive nonindigenous plants: a radiata. Appita 32:93–97. hypothesis. Journal of Ecology 83:887–889. Elton, C. S. 1958. The ecology of invasions by animals and Blumenthal, D. M., and R. A. Hufbauer. 2007. Increased plant plants. Methuen, London, UK. size in exotic populations: a common-garden test with 14 Epstein, M. J., and J. Molofsky. 2007. Invasiveness in plant invasive species. Ecology 88:2758–2765. communities with feedbacks. Ecology Letters 10:253–263. Borkowski, A. 2001. Threats to pine stands by the pine shoot Erbilgin, N., S. R. Mori, J. H. Sun, J. D. Stein, D. R. Owen, beetles Tomicus piniperda (L.) and T. minor (Hart.) around a L. D. Merrill, R. C. Bolanos, K. F. Raffa, T. M. Montiel, sawmill in southern Poland. Journal of Applied Entomology D. L. Wood, and N. E. Gillette. 2007. Response to host 125:489–492. volatiles by native and introduced populations of Dendrocto- Boyle, J. R., J. K. Winjum, K. Kavanagh, and E. C. Jensen, nus valens (Coleoptera: Curculionidae, Scolytinae) in North editors. 1999. Planted forests: contributions to the quest for America and China. Journal of Chemical Ecology 33:131–146. 1180 MARIÁ J. LOMBARDERO ET AL. Ecological Applications Vol. 18, No. 5

Faccoli, M. 2006. Morphological separation of Tomicus Keane, R. M., and M. J. Crawley. 2002. Exotic plant invasions piniperda and T. destruens (Coleoptera: Curculionidae: and the enemy release hypothesis. Trends in Ecology and Scolytinae): new and old characters. European Journal of Evolution 17:164–170. Entomology 103:433–442. Kerdelhue, C., G. Roux-Morabito, J. Forichon, J. M. Chambon, Feci, E., A. Battisti, P. Capretti, and S. Tegli. 2002. An E. Robert, and F. Lieutier. 2002. Population genetic structure association between the fungus Sphaeropsis sapinea and the of Tomicus piniperda L. (Curculionidae: Scolytinae) on cone bug Gastrodes grossipes in cones of Pinus nigra in Italy. different pine species and validation of T. destruens (Woll.). Forest Pathology 32:241–247. Molecular Ecology 11:483–494. Gadgill, P. D., and J. Bain. 1999. Vulnerability of planted forests Kohlmayr, B., M. Riegler, R. Wegensteiner, and C. Stauffer. to biotic and abiotic disturbances. New Forests 17:227–238. 2002. Morphological and genetic identification of the three Gallego, D., F. Cańovas, M. A. Esteve, and J. Galiań. 2004. pine pests of the genus Tomicus (Coleoptera, Scolytidae) in Descriptive biogeography of Tomicus (Coleoptera: Scolyti- Europe. Agricultural and Forest Entomology 4:151–157. dae) species in Spain. Journal of Biogeography 31:2011–2024. Kozlowski, T. T. 1969. Tree physiology and forest pests. Gallego, D., and J. Galiań. 2001. The internal transcribed Journal of Forestry 67:118–123. spacers (ITS1 and ITS2) of the rDNA differentiates the bark La˚ngstro¨m, B. 1983. Life cycles and shoot-feeding of the pine beetle forest pests Tomicus destruens and Tomicus piniperda. shoot beetles. Studia Forestalia Suecica 163:1–29. Insect Molecular Biology 10:415–420. La˚ngstro¨m, B. 1984. Windthrown Scots pines as brood material Georgen, E., and C. C. Daehler. 2001. Inflorescence damage by for Tomicus piniperda and T. minor. Silva Fennica 18:187– insects and fungi in native pili grass (Heteropogon contortus) 198. versus alien foundation grass (Pennisetum setaceum)in La˚ngstro¨m, B., and C. Hellqvist. 1990. Spatial distribution and Hawaii. Pacific Science 55:129–136. crown damage and growth losses caused by recurrent attacks Graham, R. A. 1939. Principles of forest entomology. of pine shoot beetles in pine stands surrounding a pulp mill in McGraw-Hill, New York, New York, USA. southern Sweden. Journal of Applied Entomology 110:261– Haack, R. A., and D. Kucera. 1993. New introduction: 269. common pine shoot beetle, Tomicus piniperda (L.). USDA La˚ngstro¨m, B., and C. Hellqvist. 1993. Scots pine susceptibility Forest Service, Northeastern Area, Pest Alert NA-TP-05-93. to attack by Tomicus piniperda (L.) as related to pruning date USDA Forest service, Washington, D.C., USA. and attack density. Annals of Forest Science 50:101–117. Haack, R. A., R. K. Lawrence, and G. C. Heaton. 2001. Tomicus Lau, J. A., and S. Y. Strauss. 2005. Insect herbivores drive piniperda (Coleoptera: Scolytidae) shoot-feeding characteris- important indirect effects of exotic plants on native tics and overwintering behavior in Scotch pine Christmas communities. Ecology 86:2990–2997. trees. Journal of Economic Entomology 94:422–429. Lavery, P. B., and D. J. Mead. 1998. Pinus radiata: a narrow Halder, I. C. 2002. Forest pests and diseases of southern endemic from North America takes the world. Pages 432–449 Europe. Institut Europeén de la Foreˆt Cultiveé (IEFC), in D. M. Richardson, editor. Ecology and biogeography of Cestas, France. Pinus. Cambridge University Press, Cambridge, UK. Harrington, T. C., and M. J. Wingfield. 1998. Diseases and Leimu, R., and J. Koricheva. 2006. A meta-analysis of tradeoffs ecology of indigenous and exotic pines. Pages 381–404 in between plant tolerance and resistance to herbivores: D. M. Richardson, editor. Ecology and biogeography of combining the evidence from ecological and agricultural Pinus. Cambridge University Press, Cambridge, UK. studies. Oikos 112:1–9. Hausner, G., M. Iranpour, J. J. Kim, C. Breuil, C. N. Davis, Lieutier, F., G. Vouland, and M. Pettinetti. 1997. Testing the E. A. Gibb, J. Reid, P. C. Loewen, and A. A. Hopkin. 2005. Fungi vectored by the introduced bark beetle Tomicus preferences of Scolytidae and other xylophagous insects. piniperda in Ontario, Canada, and comments on the Revue Forestie` re Française 49:215–224. taxonomy of Leptographium lundbergii, Leptographium tere- Liu, H., and P. Stiling. 2006. Testing the enemy release brantis, Leptographium truncatum, and Leptographium wing- hypothesis: a review and meta-analysis. Biological Invasions fieldii. Canadian Journal of Botany 83:1222–1237. 8:1535–1545. Hierro, J. L., J. L. Maron, and R. M. Callaway. 2005. A Liu, H., P. Stiling, and R. W. Pemberton. 2007. Does enemy biogeographical approach to plant invasions: the importance release matter for invasive plants? Evidence from a compar- of studying exotics in their introduced and native range. ison of insect herbivore damage among invasive, non- Journal of Ecology 93:5–15. invasive and native congeners. Biological Invasions 9:773– Honkanen, T., E. Haukioja, and J. Suomela. 1994. Effects of 781. simulated defoliation and debudding on needle and shoot Lodge, D. M., S. Williams, H. J. MacIsaac, K. R. Hayes, B. growth in Scots pine (Pinus sylvestris)—implications of plant Leung, S. Reichard, R. N. Mack, P. B. Moyle, M. Smith, source-sink relationships for plant-herbivore studies. Func- D. A. Andow, J. T. Carlton, and A. McMichael. 2006. tional Ecology 8:631–639. Biological invasions: recommendations for U.S. policy and Ishtiaq, F., J. S. Beadell, A. J. Baker, A. R. Rahmani, Y. V. management. Ecological Applications 16:2035–2054. Jhala, and R. C. Fleischer. 2006. Prevalence and evolutionary Lombardero, M. J. 1995. Planta hue´sped y escolı´tidos (Col.: relationships of haematozoan parasites in native versus Scolytidae) en Galicia (NO Peninsula Iberica). Boletıń introduced populations of common myna Acridotheres tristis. Sanidad Vegetal. Plagas 21:357–370. Proceedings of the Royal Society B 273:587–594. Mack, R. N., D. Simberloff, W. M. Lonsdale, H. Evans, M. Jactel, H., E. G. Brockerhoff, and P. Duelli. 2005. A test of the Clout, and F. A. Bazzaz. 2000. Biotic invasions: causes, biodiversity-stability theory: Meta-analysis of tree species epidemiology, global consequences and control. Ecological diversity effects on insect pest infestations, and re-examina- Applications 10:689–710. tion of responsible factors. Pages 235–256 in M. Scherer- Mansilla, J. P. 1992. Presencia sobre Eucalyptus globulus Labill Lorenzen, C. Ko¨rner, and E.-D. Schulze, editors. Forest de Gonipterus scutellatus Gyll. (Col. Curculionidae) en diversity and function: temperate and boreal systems. Galicia. Boletin de Sanidad Vegetal. Plagas 18:547–554. Ecological studies. Springer-Verlag, Berlin, Germany. Marquis, R. J. 1996. Plant architecture, sectoriality and plant Jactel, H., P. Menassieu, F. Vetillard, A. Gaulier, J. C. tolerance to herbivores. Vegetatio 127:85–97. Samalens, and E. G. Brockerhoff. 2006. Tree species diversity Martinson, S. J., R. W. Hofstetter, and M. P. Ayres. 2007. Why reduces the invasibility of Maritime pine stands by the bast does longleaf pine have low susceptibility to southern pine scale, Matsucoccus feytaudi (Homoptera: Margarodidae). beetle? Canadian Journal of Forest Research 37(10):1966– Canadian Journal of Forest Research 36:314–323. 1977. July 2008 PESTILENCE AND PINE FORESTRY 1181

Masutti, L. 1969. Pine stands of the Adratic coast and Sedjo, R. A. 1983. The comparative economics of plantation Blastophagus piniperda: a bad combination. Monti e Boschi forestry: a global assessment. Resources for the Future, 20:15–27. Washington, D.C., USA Ministerio de Medio Ambiente. 2002. III Inventario Forestal Seifert, K. A. 1993. Sapstain of commercial lumber by species Nacional, 1997–2006. Galicia Lugo. Direccioń General de of Ophiostoma and Ceratocystis. Pages 141–151 in M. J. Conservacioń de la Naturaleza, Madrid, Spain. Wingfield, K. A. Seifert, and J. F. Webber, editors. Mitchell, C. E., et al. 2006. Biotic interactions and plant Ophiostoma and Ceratocystis: taxonomy, ecology and path- invasions. Ecology Letters 9:726–740. ogenecity. APS Press, St. Paul, Minnesota, USA. Mitchell, C. E., and A. G. Power. 2003. Release of invasive Speight, M. R., and D. Wainhouse. 1989. Ecology and plants from fungal and viral pathogens. Nature 421:625–627. management of forest insects. Oxford Science Publications, Moorcroft, P. R., S. W. Pacala, and M. A. Lewis. 2006. Clarendon Press, Oxford, UK. Potential role of natural enemies during tree range expan- Stamp, N. 2003. Out of the quagmire of plant defense sions following climate change. Journal of Theoretical hypotheses. Quarterly Review of Biology 78:23–55. Biology 241:601–616. Stastny, M., U. Schaffner, and E. Elle. 2005. Do vigour of Mortenson, S. G., and R. N. Mack. 2006. The fate of alien introduced populations and escape from specialist herbivores conifers in long-term plantings in the USA. Diversity and contribute to invasiveness? Journal of Ecology 93:27–37. Distributions 12:456–466. Strauss, S. Y. 2001. Benefits and risks of biotic exchange Nadel, H., J. H. Frank, and R. J. Knight. 1992. Escapees and between Eucalyptus plantations and native Australian forests. accomplices: the naturalization of exotic Ficus and their Austral Ecology 26:447–457. associated faunas in Florida. Florida Entomologist 75:29–38. Strauss, S. Y., and A. A. Agrawal. 1999. The ecology and Parker, I. M., and G. S. Gilbert. 2004. The evolutionary evolution of plant tolerance to herbivory. Trends in Ecology ecology of novel plant–pathogen interactions. Annual and Evolution 14:179–185. Review of Ecology, Evolution and Systematics 35:675–700. Swart, W. J., P. S. Knox-Davies, and M. J. Wingfield. 1985. Parker, I. M., and G. S. Gilbert. 2007. When there is no escape: Spaheropsis sapinea, with special reference to its occurrence the effects of natural enemies on native, invasive, and in Pinus spp. in South Africa. Southern African Forestry noninvasive plants. Ecology 88:1210–1224. Journal 35:1–8. Parker, J. D., D. E. Burkepile, and M. E. Hay. 2006. Opposing Tainter, F. H., and F. A. Baker. 1996. Principles of forest effects of native and exotic herbivores on plant invasions. pathology. John Wiley and Sons, New York, New York, USA. Science 311:1459–1461. Toro, J., and S. Gessel. 1999. Radiata pine plantations in Chile. Peterson, G. W. 1981. Pine and juniper diseases in the Great New Forests 18:33–44. Plains. USDA Forest Service General Technical Report RM- Turchin, P., and W. T. Thoeny. 1993. Quantifying dispersal of 86. USDA Forest service, Washington, D.C., USA. southern pine beetles with mark recapture experiments and a Petrakis, P. V., V. Roussis, D. Papadimitriou, C. Vagias, and C. diffusion-model. Ecological Applications 3:187–198. Tsitsimpikou. 2005. The effect of terpenoid extracts from 15 Vasconcelos, T., A. Horn, F. Lieutier, M. Branco, and C. pine species on the feeding behavioural sequence of the late Kerdelhue. 2006. Distribution and population genetic struc- instars of the pine processionary caterpillar Thaumetopoea ture of the Mediterranean pine shoot beetle Tomicus pityocampa. Behavioural Processes 69:303–322. destruens in the Iberian Peninsula and Southern France. Petrakis, P. V., C. Tsitsimpikou, O. Tzakou, M. Couladis, C. Agricultural and Forest Entomology 8:103–111. Vagias, and V. Roussis. 2001. Needle volatiles from five Pinus Vila, M., J. L. Maron, and L. Marco. 2005. Evidence for the species growing in Greece. Flavour and Fragrance Journal enemy release hypothesis in Hypericum perforatum. Oecolo- 16:249–252. gia 142:474–479. Pfeffer, A. 1995. Zentral- und westpalaärktische Boeken- und Volz, H. A. 1988. Monoterpenes governing host selection in the kernka¨fer. Pro Entomologia. Museum of Natural History, bark beetle Hylurgops palliatus and Tomicus piniperda. Basel, Switzerland. Entomologia Experimentalis et Applicata 47:31–35. Price, R. A., A. Liston, and S. H. Strauss. 1998. Phylogeny and Whitehill, J. G. A., J. S. Lehman, and P. Bonello. 2007. Ips pini systematics of Pinus. Pages 49–69 in D. M. Richardson, (Curculionidae: Scolytinae) is a vector of the fungal editor. Ecology and biogeography of Pinus. Cambridge pathogen, Sphaeropsis sapinea (Coelomycetes), to Austrian University Press, Cambridge, UK. pines, Pinus nigra (Pinaceae). Environmental Entomology 36: Richardson, D. M., N. Allsopp, C. M. D’antonio, S. J. Milton, 114–120. and M. Rejmanek. 2000. Plant invasions: the role of Williamson, M. 1996. Biological invasions. Chapman and Hall, mutualisms. Biological Reviews 75:65–93. London, UK. Roques, A., M. A. Auger-Rozenberg, and S. Boivin. 2006. A Wingfield, M. J. 2003. Increasing threat of diseases to exotic lack of native congeners may limit colonization of introduced plantation forests in the Southern hemisphere: lessons from conifers by indigenous insects in Europe. Canadian Journal Cryphonectria canker. Australasian Plant Pathology 32:133– of Forest Research 36:299–313. 139. Salonen, K. 1973. On the life cycle, especially on the Xunta de Galicia. 1992. Plan forestal de Galicia. Consellerıáde reproduction biology of Blastophagus piniperda L. (Coleop- Agricultura Ganderıá e Montes, Santiago de Compostela, tera, Scolytidae). Acta Forestalia Fennica 127:1–72. Spain. Santos, A. M., T. Vasconcelos, E. Mateus, M. H. Farrall, Ylioja, T., D. H. Slone, and M. P. Ayres. 2005. Mismatch M. D. R. Gomes da Silva, M. R. Paiva, and M. Branco. between herbivore behavior and demographics contributes to 2006. Characterization of the volatile fraction emitted by scale-dependence of host susceptibility in two pine species. phloems of four Pinus species by solid-phase microextraction Forest Science 51:522–531. and gas chromatography-mass spectrometry. Journal of Zobel, B. J., G. van Wyk, and P. Stahl. 1987. Growing exotic Chromatography A 1105:191–198. forests. Wiley Press, New York, New York, USA.

APPENDIX Attribute summary for 45 stands of Pinus pinaster or Pinus radiata that were studied in Galicia, Spain (Ecological Archives A018- 042-A1).