Biodiversity and Conservation 14: 1735–1760, 2005. Ó Springer 2005 DOI 10.1007/s10531-004-0697-9 The red turpentine beetle, Dendroctonus valens LeConte (Scolytidae): an exotic invasive pest of pine in China ZHENGLIANG YAN1, JIANGHUA SUN1, OWEN DON2 and ZHONGNING ZHANG1,* 1State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, 25 Beisihuanxilu, Haidian, Beijing 100080, China; 2California Department of Forestry and Fire Protection, 6105 Airport Rd, Redding, CA 96002, USA; *Author for correspondence (e-mail: [email protected]; fax: +86-10-62565689) Received 17 June 2003; accepted in revised form 9 February 2004 Key words: Bark beetle, Dendroctonus valens, Exotic pest, Outbreak, Pinus tabuliformis, Sclytidae Abstract. An exotic invasive pest of pines, the red turpentine beetle, Dendroctonus valens LeConte (Scolytidae) (RTB), was first detected in Shanxi Province, northern China, in 1998 and started causing widespread tree mortality there in 1999. This outbreak continues and has spread to three adjacent provinces, causing unprecedented tree mortality. Although it is considered a minor pest of pines in North America, RTB has proven to be an aggressive and destructive pest of Pinus tabuliformis, China’s most widely planted pine species. The bionomics and occurrence, distribution, response to host volatiles, and host preference of this pine beetle in China are compared with what is known of the beetle in its native range in North America. Factors likely contributing to D. valens success in China and control of the beetle outbreak are discussed. (À)-b-pinene was shown to be the most attractive host volatile for D. valens from the Sierra Nevada of California, whereas 3-(+)- carene is the most attractive host volatile for beetles in China. Monocultures of Pinus tabuliformis, several consecutive years of drought conditions and warm winters have apparently factored D. valens invasion and establishment in China. Introduction The red turpentine beetle, Dendroctonus valens LeConte (Coleoptera: Scolyti- dae), is a common pest of pines in its native range in North and Central America (Eaton and Lara 1967). It is considered to be a secondary pest and is often associated with more aggressive bark beetle species. Tree mortality and outbreaks attributed to D. valens alone are rare in its native range (Smith 1971; Cibrian et al. 1995). Recently, it has been reported as the cause of ponderosa pine (Pinus ponderosa Lawson) mortality in plantations in California and Mexico (Rappaport et al. 2001). Dendroctonus valens was introduced into China in the early 1980s when unprocessed logs were imported from the west coast of the United States (re- port on file at Chinese Academy of Sciences, Beijing). A report of plant diseases and insect pests in Shanxi province in the early 1980s provides no record of D. valens activity (Ying and Huang 1984). During those years, Shanxi province 1736 imported large quantities of unprocessed ponderosa pine logs for coal mine timber. D. valens was first discovered in Pinus tabuliformis forests in Qinshui and Yangcheng, Shanxi province, in 1998 and its first outbreak occurred in 1999 in many regions of Shanxi. DNA analysis indicates that western North America is the source of China’s D. valens (personal communication with Anthony Congeto, Texas A & M University). Since 1999, D. valens has spread rapidly from Shanxi province to the adjacent provinces of Hebei, Henan, and Shaanxi and infested over 500,000 ha of pine forest, causing extensive tree mortality. More than 10 million Pinus tabuliformis Carr. have been killed, as well as other pine species, including Pinus bungeana Zucc (Li et al. 2001; Miao et al. 2001; Zhang et al. 2002). Several consecutive years of drought conditions have stressed P. tabuliformis stands and contributed to the outbreak (Li et al. 2001). Because pines are a major reforestation species in China and P. tabuliformis widely planted across a large portion of the country, the po- tential range of D. valens is nationwide (Britton and Sun 2002). Herein is an evaluation of factors that likely have contributed to the current outbreak of D. valens in China and may influence its future course. Bionomics and occurrence The life circle and behavior of D. valens appear similar in North America and the People’s Republic of China (Table 1). However, some notable differences exist. Foremost among these is the beetle’s ability to colonize, kill, and reproduce in mature P. tabuliformis, resulting in an outbreak that has no parallel in the native range of D. valens. In North America, D. valens is re- ported to initiate attack on the tree near ground level and colonize a short distance both upward along the lower bole and downward along the upper roots (Smith 1971). In China, D. valens extensively colonizes and overwinters in roots (Britton and Sun 2002; Wu et al. 2002). It is speculated that extensive root colonization, in combination with the inoculation of fungal associates into roots, may help explain the beetle‘ tree-killing success in China (Owen 2001). In the United States, fungi isolated from D. valens include Leptographium terebrantis, L. procerum, Ophiostoma ips, and a Graphium spp. (Owen et al. 1987; Klepzig et al. 1991). Among the Ophiostoma fungi carried by Dend- roctonus bark beetles attacking ponderosa pine, L. terebrantis proved the most virulent (Owen et al. 1987 Parmeter et al. 1989). L. terebrantis has also been associated with the decline and mortality of a number of other Pinus spp. (Highley and Tattar 1985; Klepzig et al. 1991; Bannwart et al. 1998). It is yet unknown which, if any, of the know fungal associates of RTB are present in China or if RTB has formed new associations since its introduction. The flight distance of D. valens in the United States of America can exceed 16 km (Smith 1971). In China, flight distances up to 35 km have been docu- mented (Zhang et al. 2002). In China, no life stages of D. valens can overwinter in boles when the temperature is below À18 °C (Wu et al. 2002). Little 1737 Table 1. Comparison of bionomics and occurrence of D. valens in northern People’s Republic of China and western North America. Western North Americaa Chinab Longitude 60W to 97W and 103W to 125Wc 110E to 115E Latitude 15°Nto55°N (mainly 30°Nto50°N)c 35°12¢Nto39°16¢N Host All Pinus species including: Pinus species including: Pinus ponderosad Pinus lambertiana Pinus tabuliformise Pinus strobes Pinus resinosa Pinus bungeana Pinus rigida Pinus contorta Pinus aramandii Pinus echinata Pinus banksian Pinus radiate Occasional Hosts Picea, Pseudotsuga, Larix, Abries Picea meyeri Life stages Egg 2 week Egg 1–2 week Larvae 8 week Larvae 8–10 week Pupae 1 week Pupae 1–2 week Young adult 1 week Young adult 1 week Flight temperature 19–23 °C 14–28 °C Peak flight and attack activity usually Flight of overwintered adults occur in spring. In the warmer parts of begins in Mid April and peaks in its range (southern areas), RTB may mid May. Pupation of overwin- occur during intermittent warm peri- tered larva begins in early June, ods in the winter; In the colder parts, and eclosion begins in early July. the winter is passed in hibernation, D. valens adults can be detected chiefly in the adult stage and to a les- from May to October. ser extent in larval stage. Flight distance More than 16 km (more than 10 miles) Generally 20 km, Farthest flight distance is 35 km Attack pattern Bases of trees, concentrated in the Bases of the tree, roots exten- basal 1.8 meter of the tree, colonize a sively colonized and serve as short distance both up and down to overwintering sites the upper roots and lower bole Aggressive behavior Freshly cut stumps, the bases of trees Similar to those of the popula- that are dying, diseased or attacked by tion in the western North other insects; exposed roots and the America. When the population bases of trees that are weakened or density is high and the canopy injured. Fire-scorched trees and trees density of stands is low, the pest in campgrounds and around homes can quickly attack healthy trees also are frequently attacked with a breast-height diameter greater than 10 cm and over 20 years old aCited from Smith (1971), Gara and Vite´(1962), Vite´et al. (1964). bCited from Miao et al. (2001), Zhang et al. (2002), Wang et al. (2002), Wu et al. (2002). cNorth American distribution from Smith (1971). dPine species that is most frequently attacked (Smith 1971). ePine species most frequently killed in China. mortality occurs among larvae and adults that overwinter in the roots (Miao et al. 2001), however, indicating that roots are important for D. valens survival in China (Wu et al. 2002). D. valens primarily attacks Pinus tabuliformis Carr. and Pinus bungeana Zucc, especially the former, in China. It has been reported 1738 from Pinus armandi Franch, and Picea meyeri Redh. et Wils, but damage on these hosts is not confirmed (Zhang et al. 2002). As a major reforestation species in China, P. tabuliformis is widely planted across a large portion of the country, including degraded and marginal sites that contribute to tree stress and likely favor D. valens activity (Li et al. 2001). In general, mature and overmature P. tabuliformis forests are infested, while younger forests are sel- dom attacked (Miao et al. 2001). In D. valens-infested pine forests are also endangered by another beetle, Hylastes parallelus Chapuis (Wu et al. 2002). The interaction between these two beetles and the role of H. parallelus in D. valens infestation are unknown. Predators of D. valens in China are rare although Dendrocopos major Linnaeus (Piciformes: Picidae), Labidura riparia (Dermaptera: Labiduridae), Raphidia sinica Steinmann (Neuroptera: Raphidiidae), Tetramorium guineense Fabricius (Myrmicinae: Tetramoriini), two species of Paederus Fabricius (Coleoptera: Staphylinidae), one species of Thanasimus Latreille (Coleoptera: Cleridae), one species of Cryptolestes Ganglbauer (Coleoptera: Ostomatidae), one species of Hister L.