Review Changes in Major Insect Pests of Pine Forests in Korea Over the Last 50 Years Won Il Choi 1, Youngwoo Nam 2, Cha Young Lee 2, Byoung Ki Choi 3, Yu Jin Shin 1, Jong-Hwan Lim 1, Sang-Hyun Koh 3 and Young-Seuk Park 4,5,* 1 Division of Forest Ecology and Climate Change Division, National Institute of Forest Science, Dongdaemun, Seoul 02445, Korea 2 Division of Forest Diseases and Insect Pests, National Institute of Forest Science, Dongdaemun, Seoul 02445, Korea 3 Warm Temperate and Subtropical Forest Research Center, National Institute of Forest Science, Seogwipo, Jeju 63582, Korea 4 Department of Biology, Kyung Hee University, Dongdaemun, Seoul 02447, Korea 5 Department of Life and Nanopharmaceutical Sciences, Kyung Hee University, Dongdaemun, Seoul 02447, Korea * Correspondence: [email protected]; Tel.: +82-2961-0946 Received: 29 June 2019; Accepted: 12 August 2019; Published: 15 August 2019 Abstract: Understanding the occurrence patterns of forest pests is fundamental for effective forest management from both economic and ecological perspectives. Here, we review the history of the occurrence patterns and causes of outbreaks and declines of pests in Korean pine forests over the last 50 years. During this period, the major pests of pine forests in Korea have shifted from pine caterpillar (Dendrolimus spectabilis Butler) to the pine needle gall midge (PNGM, Thecodiplosis japonensis (Uchida and Inouye)) and finally to pine wilt disease (PWD) caused by the pine wood nematode (Bursaphelenchus xylophilus (Steiner and Buhrer) Nickle). Outbreaks of pine caterpillar, a native species in Korea, have been recorded as far back as 900 years, and it was the most relevant forest pest in Korea until the 1970s. The decline of its importance has been attributed to reforestation and higher levels of subsequent natural enemy activity. The PNGM is an invasive species, first discovered in Korea in 1929, that became widely distributed by 1992 and the major forest pest in the 1980s and 1990s. A suite of parasitic wasps attacking the PNGM contributed at least partially to the decline of PNGM densities. Following the decline of the PNGM, damage from PWD has increased since 2003. These shifts in major forest pests might be related to changes in forest composition and interactions among forest pests. Therefore, a new management strategy for controlling forest pests is required to mitigate the decline of pine forests in Korea. Keywords: invasive species; natural enemies; pine caterpillar; pine needle gall midge; pine wilt disease 1. Introduction Understanding forest pest outbreaks is fundamental for the effective economic and ecological management of forest ecosystems. Outbreaks of forest pests are affected by both intrinsic and extrinsic factors. Intrinsic factors are related to the rate of population increase and cyclical population dynamics [1], while extrinsic factors include biological factors such as the interactions between species and the effects of abiotic factors such as temperature and precipitation [2]. Biological interactions include the bottom-up effects of forest composition and tree age and the top-down regulation exerted by natural enemies [2–4]. In addition, anthropogenic factors directly or indirectly influence forest pest dynamics [5]. Long-term monitoring data for pests and their analyses can allow us to understand Forests 2019, 10, 692; doi:10.3390/f10080692 www.mdpi.com/journal/forests Forests 2019, 10, 692 2 of 15 historical changes in natural forest ecosystems under the influence of both natural phenomenon and anthropogenic activities. Long-term monitoring programs on forest pests allow us to describe abundance patterns of pests [6,7]. Schwerdtfeger [8] described population changes of three species of pine-needle feeding Lepidoptera (Dendrolimus pini L., Hyloicus pinastri L. and Bupalus piniarius L.) in a pine plantation in Germany between 1880 and 1940. Using these data, Turchin and Taylor [9] showed the periodical occurrence of these species. Meanwhile, Tenow [10] studied the outbreaks of Oporina autumnata and Operophtera sp. in the Swedish Scandes Mountains on the basis of historical data from 1862 to 1968, and periodic outbreaks of Operophtera brumata L. continued until the 1990s [11]. In Korea, the monitoring of forest pests has been conducted for both major and occasional pests such as Thecodiplosis japonensis (Uchida and Inouye) (pine needle gall midge (PNGM)) and Hyphantria cunea (Drury) (fall webworm) populations since 1968 [12], including the measurement of annual changes of densities, dispersal, and distributions [13]. Choi and Park [12] reported the occurrence and dispersal patterns of these invasive species with their ecology and management histories. However, few studies have examined the long-term changes in forest pest populations in relation to the conditions of the forest ecosystem. Pine forests are one of the most important forests in Korea because of their dominance and cultural importance. Forests of Pinus densiflora Siebold and Zuccarini account for 26% of all Korean forests [14], and wood from P. densiflora has been intensively used in Korea since the Goryeo Dynasty (918–1392) [15]. The major forest pests in Korea have occurred in pine forests [12]. Here, we review the changes in the major pests of pine forests in Korea, in particular of stands of P. densiflora, over the last 50 years. We consider occurrence histories and ecologies of these pests as well as the environmental factors influencing the pests’ population dynamics. Management strategies based on natural enemies and chemical controls are discussed and new directions for forest pest management are proposed. 2. Forest Change and Monitoring Records in Korea Wood was the main building material in ancient Korea. Houses from different periods reflect the availability of wood for construction. Based on the materials used, Park and Lee [15] estimated that oak trees were the dominant material (57%) from 100 B.C. to 910 (Three Kingdoms Period of Korea), whereas pine trees were the dominant species from 910 to the 1910s (Goryeo and Joseon Dynasties) with increasing dominancy from 71% in the early period to 88% in the late period [15]. The change in forests from oak to pine likely influenced the distribution and occurrence of animals living in the forests [16]. As the pine trees became dominant in Korean forests, the pine caterpillar (PC) (Dendrolimus spectabilis Butler) outbreaks were recorded in the Goryeo and Joseon dynasties. After the first record of a PC outbreak in The History of Goryeo (Goryeosa) in 1101 (http://www.history.go.kr), more than 50 cases of PC outbreaks were subsequently recorded in the history books of the Goryeo (918–1392) and Joseon (1392–1897) dynasties, such as The History of Goryeo (Goryeosa), The Veritable Records of the Joseon Dynasty (Joseon Wangjo Sillok, also called as The Annals of the Chosun Dynasty) and Seungjeongwon Ilgi (http://www.history.go.kr). These historical records qualitatively describe both the occurrence and control of pests and the prevailing forest conditions, but they do so with little quantitative information. Modern Korean forests are considered a successful example of reforestation, and the annual growing stock and species composition of forests have changed dramatically as a result [17] (Figure1). After the Korean War in the early 1950s, deforestation was intensive, with the major causes of deforestation being utilization of wood as a fuel source and slash-and-burn agriculture [17]. In particular, Japanese red pines, P. densiflora, were intensively used for fuel from the 1950s to the early 1970s, with 10 million m3 of woods including pine woods consumed annually [18]. The area of slash-and-burn agriculture likewise increased until the early 1970s [19], when it was prohibited by the government new policy for reforestation, and the main domestic fuel sources were changed from wood to coal. Due to Forests 2019, 10, 692 3 of 15 Forests 2019, 10, x FOR PEER REVIEW 3 of 15 thiswood change to coal. in forestDue to management this change in policy, forest the manage growingment stock policy, in forests the growing increased stock from in 5.7 forests m3/ha increased in 1952 tofrom 146.0 5.7 m m3/3ha/ha in in 2015 1952 [14 to]. 146.0 Meanwhile, m3/ha in the 2015 dominance [14]. Meanwhile, of coniferous the dominance species decreased of coniferous from 57.3% species in 1970decreased to 41.8% from in 201057.3% (Figure in 19701a), to although 41.8% inP. 2010 densiflora (Figureremained 1a), although the most P. dominantdensiflora remained coniferous the species, most accountingdominant coniferous for 60% of species, conifers acco [14].unting for 60% of conifers [14]. FigureFigure 1.1. ((aa)) ChangesChanges ofof forestforest compositioncomposition inin KoreaKorea fromfrom 19601960 toto 20152015 andand ((bb)) annualannual changeschanges inin forestforest growinggrowing stockstock (m(m33//ha).ha). The graphsgraphs werewere redrawnredrawn basedbased onon datadata fromfrom StatisticalStatistical YearbookYearbook ofof ForestryForestry [14[14]]. 3. Monitoring of Korean Forest Pests 3. Monitoring of Korean Forest Pests The Korea Forest Research Institute (later renamed the National Institute of Forest Science The Korea Forest Research Institute (later renamed the National Institute of Forest Science in in 2015) initiated the Forest Insect Pests Monitoring Program in 1968. The occurrence of the PC, 2015) initiated the Forest Insect Pests Monitoring Program in 1968. The occurrence of the PC, the the major forest pests in 1960s, was checked annually at a series of national long term monitoring major forest pests in 1960s, was checked annually at a series of national long term monitoring sites. sites. The determination of the emergence period and leading edge of dispersal of the PNGM has The determination of the emergence period and leading edge of dispersal of the PNGM has been been done since the mid-1970s. Outbreaks of occasional forest pests and the annual density of fall done since the mid-1970s. Outbreaks of occasional forest pests and the annual density of fall webworm (H. cunea) have also been monitored from the 1970s, and the areas damaged by black webworm (H.