1. Introduction
Pests and diseases are the main cause of forest damage [
1], and the economic losses caused mainly include the loss of forest assets [
2], the discounted expenditure of the disposal, removal and replacement of damaged trees [
3,
4], the loss of forest recreational and landscape value [
5] and the loss of carbon sinks [
6]. Infected by diseases and insect pests, 85 million hectares of forests worldwide were destroyed between 2003 and 2012, and the most of the disease occurred in temperate North America [
7]. China’s average annual economic losses caused by forest pests and diseases in 1996–2010 exceeded CNY 100 billion, including direct economic losses and loss of ecological service value [
8,
9,
10].
Pine wood nematode disease is native to North America, and is mainly distributed in Portugal and Spain in North America, East Asia and Europe [
11,
12,
13]. In China, Japan, South Korea, Portugal and Spain, pine wood nematode disease has caused massive deaths of pine trees, leading to severe economic losses [
14,
15]. China first discovered pine wood nematodes in the Sun Yat-sen Mausoleum in Nanjing in 1982. After nearly 40 years of spreading, the area infected by pine wood nematode disease in 2019 expanded to 588 counties of 18 provinces (autonomous regions, municipalities) in the country [
16]. What is more serious is that pine wood nematodes have a tendency to break through the previous suitable geo-environment range and spread northward and toward high altitudes. The middle temperate zone has become the front line for pine wood nematode disease prevention and control [
17].
The rapid spread of pine wood nematode disease has caused huge economic losses to the infected countries. These losses come from direct wood loss on the one hand [
18,
19,
20], and expenditure incurred to reduce the spread or impact of pine nematode disease [
21,
22], including spraying pesticides, felling, fumigation or burning infected trees [
23,
24], as well as economic losses due to the loss of export markets and import restrictions due to pine wood nematodes [
25]. According to evaluations, the average annual economic loss of pine wood nematode disease in China is CNY 7.8 billion [
26], and the economic loss in Zhejiang province, where the pine wood nematode disease is the most severe, was CNY 621 million in 2004 [
27].
The research on the economic loss evaluation of forestry biological disease is mainly focused on the construction of evaluation theory and index system [
28,
29,
30,
31]. There are very limited studies on the economic loss evaluation covering macro-geographic scales and long-term sequences. In view of this, using the provincial-level incidence data of pine wood nematode disease in China from 1998 to 2017, this study constructs a pine wood nematode disease economic loss evaluation index and quantifies the economic loss in China.
3. Results
3.1. Trends in Areas Infected by Pine Wood Nematode Disease in Mainland China from 1998 to 2017
According to the fluctuation trend of the disease occurrence area, the pine wood nematode disease situation is divided into three stages in China. The first stage was from 1998 to 2001, when the pine wood nematode disease area showed a slowly rising trend. The second stage was from 2001 to 2013, during which the area of pine wood nematode disease showed a downward trend. The third stage was from 2013 to 2017, when the area of pine wood nematode disease increased rapidly (
Figure 1).
The area of pine wood nematode disease showed two extremes in 2001 and 2013. During the period from 1998 to 2001, the incidence area of pine wood nematode disease increased significantly, with an average annual increase of 5%, and reached to a maximum value of 84,688 hectares in 2001. During the period from 2001 to 2013, the incidence area of pine wood nematode disease showed a downward trend, and reached a minimum of 38,356 hectares in 2013. However, since then, the epidemic has expanded again, showing a more rapid growth trend than before, with an average annual increase of 22%, and the diseased area in 2017 reached 85,024 hectares (
Table A1).
At the provincial level, in the past two decades, pine wood nematode disease has broken out in a total of 18 provinces in China, and the severity of pine wood nematode disease has varied among regions (
Figure 2).
Jiangsu, Zhejiang, Anhui, Shandong and Guangdong Province have experienced pine wood nematode disease for 20 consecutive years. Henan, Guangxi, Sichuan, and Yunnan provinces got infected again after the epidemic area was successfully removed. Among them, the cumulative disease in Henan and Yunnan Provinces occurred for less than 10 years, and in Guangxi and Sichuan Provinces it occurred for more than 10 years. The pine wood nematode disease was discovered between 2000 and 2002 in Shanghai, and the epidemic area was successfully removed afterwards; Liaoning Province was the new epidemic area in 2016.
From the spatial perspective, the scale infected declined from the east to the west in general. The province with the most severe pine wood nematode disease is Zhejiang Province, with an average annual diseased area of 22,667 hectares, followed by Guangdong Province, with an average annual diseased area of 15,333 hectares, and Jiangsu Province, with average annual diseased area of 12,667 hectares. The other provinces all had diseased areas of less than 6667 hectares. The average annual area infected in Guangxi, Guizhou and Yunnan Province was less than 667 hectares, and the average annual area infected in Shanghai was only 16 hectares.
Overall, Zhejiang, Guangdong, Jiangsu, and Anhui provinces were the provinces most severely infected by pine wood nematode disease for 20 consecutive years, and the cumulative diseased area was greater than 66,667 hectares. Liaoning Province had an average annual area of 1594 hectares, and the disease spread rapidly. At the same time, due to the northeast forest farm and the high geographical latitude, Liaoning Province is the front line for the northward spread of pine wood nematode disease. Pine wood nematode disease has occurred in the southern region for 20 consecutive years, and the disease area has been increasing, and spreading rapidly to the north (
Table A2).
3.2. The Economic Losses of Pine Wood Nematode Disease in Mainland China from 1998 to 2017
The economic losses caused by the pine wood nematode disease during the 20 years from 1998 to 2017 showed a rising trend. Here, 2008 can be seen as the watershed for the disease losses. The loss before 2008 was relatively small, except for 2001 and 2004. After 2008, the disease loss growth rate was higher than 10%, especially in 2016 and 2017, the disease loss growth rate reached 44.5% and 36.2%, respectively. The downward trend only occurred in 1999–2000, 2008, and 2011 during the 20 years (
Figure 3).
From 1998 to 2017, the total economic loss of pine wood nematode disease was CNY 7.17 billion /year. The direct economic loss accounted for 21.4% of the total economic loss, and indirect economic loss accounted for 78.6% (
Table A3). The direct economic losses were mainly the loss of forest material resources and ineffective expenditure for forestry management expenditure, with an average annual economic losses of more than CNY 800 and 600 million, accounting for 53% and 42% of the total direct economic loss, respectively. The average annual economic expenditure of prevention expenditure was less than CNY 100 million, accounting for 5% of direct economic losses (
Table A4). Among the tertiary indicators, the main loss was the loss of forest by-products, with the average annual economic loss being more than CNY 770 million, accounting for 50% of direct economic loss. The loss of ineffective forestation was mainly the loss of afforestation expenditure, with the average annual economic loss of around CNY 540 million, accounting for 35% of direct economic loss (
Table A5).
The indirect economic loss is mainly the loss of adjustment service value and the support service value, with the average annual economic losses being about CNY 4 and 1.4 billion, accounting for 70% and 25% of the total indirect economic loss (
Table A6). Among the tertiary indicators, the losses of climate regulation services and hydrological regulation services were CNY 940 and 760 million, accounting for 30% and 21% of indirect economic losses, respectively. The average annual economic losses of gas regulation and purification environment were around CNY 320 and 280 million. The loss of support service value was mainly from soil conservation services, with the average annual economic loss of CNY 470 million, accounting for 13% of the indirect economic loss. The average annual economic loss of the biodiversity service value was CNY 350 million, accounting for less than 1% of indirect economic losses; the annual loss of aesthetic landscape service value was CNY 150 million, accounting for 5% of indirect economic losses (
Table A7).
3.3. Economic Loss of Pine Wood Nematode Disease at Provincial Scale in Mainland China from 1998 to 2017
According to the evaluation, the economic losses of pine wood nematode disease in various provinces of China from 1998 to 2017 showed an upward trend. Zhejiang, Guangdong and Jiangsu provinces were the areas with the most severe economic losses in disease (
Figure 4.). Zhejiang’s average annual economic loss was CNY 2.14 billion, accounting for 28% of the national economic loss, of which direct economic loss was CNY 480 million and indirect economic loss was CNY 1.66 billion. The average annual economic loss in Guangdong Province was CNY 1.81 billion, accounting for 23% of the national economic loss. The average annual economic loss in Jiangsu Province was CNY 1.22 billion, accounting for 15% of the national economic loss, of which the direct economic losses accounted for 3%, and indirect economic losses accounted for 12% (
Table A8).
The economic loss of the pine wood nematode disease also showed a decreasing trend from the east to the west. The average annual economic loss in Fujian Province was CNY 550 million, followed by Jiangsu Province. In addition, Anhui Province, Liaoning Province, Shandong Province, Jiangxi Province, and Chongqing Municipality also suffered huge losses, and the average annual economic loss was more than CNY 200 million. Among them, except for Chongqing and Liaoning Provinces, the other provinces are located in the southeast of China. Regarding Liaoning Province, although it was a new epidemic area in 2016, its annual economic loss was CNY 320 million, accounting for 4% of the national average annual economic loss of pine wood nematode disease.
Zhejiang, Guangdong, Jiangsu, Anhui, and Fujian suffered the most in terms of direct economic loss. Among them, Zhejiang Province lost CNY 480 million, Guangdong Province lost CNY 340 million and Jiangsu Province lost CNY 280 million, accounting for 29.8%, 25.3%, and 17.0% of the national economic loss. Yunnan Province lost CNY 3.25 million in economic loss, Shanghai lost CNY 250,000, and the losses of others were greater than CNY 10 million and less than CNY 100 million (
Table A9). Zhejiang, Guangdong, Jiangsu, Fujian and Anhui suffered the most in terms of indirect loss (
Table A10).
In general, the indirect economic losses were greater than the direct economic losses. Fujian, Guangxi, and Guangdong Province were the regions with the largest ratios of indirect economic losses against direct economic losses, which were 4.9, 4.5, and 4.4, respectively. The regions with the smallest ratios of indirect economic losses to direct economic losses were Shanghai, Henan and Anhui province, the values for which were 1.2, 2.6, and 2.9.
4. Discussion
The pine wood nematode disease in China has continuously expanded since 1998. Due to global warming, the suitable range of pine wood nematodes has continued to expand, and new vector insects and susceptible tree species have been developed in the process. In 2012, pine wood nematode disease was found in Tianzhushan Forest Park, with an annual average temperature of only 7.9 °C, in Shanyang County, Shaanxi Province, at an altitude of 1700–1800 m. For the first time,
Pinus armandii Franch was identified as a natural susceptible tree species for pine wood nematodes [
54]; for the first time in 2016, the
Monochamussaltuarius Gebler was confirmed to be a transmission vector of pine wood nematodes, and Korean pine is another new host of Chinese pine wood nematodes [
55].
The number pine wood nematode outbreaks in China is soaring, and human activity is an important factor affecting the spread rate and scale of pine wood nematode disease [
56]. Coastal cities such as Shantou City in Guangdong Province and Dalian City in Liaoning Province became the first portals in the province infected and spread inward, indicating that the long-term expansion of pine wood nematodes is due to the transportation of pine wood nematode logs [
25], as sea transportation played a huge role in transportation. In addition, Henan and Guangxi Zhuang Autonomous Regions have relapsed after the epidemic area was successfully eliminated, which may be due to the fact that the two provinces have planted horsetail pines and black pines with different degrees of latent infection [
57]. Pine wood nematode disease has an incubation period, which cannot be detected and treated in time, leading to re-spread. The original technology of Yunnan Province to use
Poria cocos for the harmless treatment of pine wood nematode disease has made outstanding contributions to the effective control of pine wood nematode disease. In 2004, after the first discovery of pine wood nematode disease in Ruili City, the area of the disease continued decreasing, and the affected area was finally removed within 5 years. After that, the disease was discovered again in 2013. However, due to the small area of the disease, the treatment was quickly successful.
From 1998 to 2017, the economic losses of the pine wood nematode disease in China showed regional disparities, and the southeast region was the worst-hit area for disease economic losses. On the one hand, due to the long outbreak and large disease area in the southeast region, the pine wood nematode disease occurred in Jiangsu, Anhui, Shandong, Zhejiang and Guangdong provinces for 20 consecutive years, and the scale of the disease is expanding. On the other hand, the quality of forest resources in southern China is high, and pine forests are widely distributed. Especially in Guangdong, where there is sufficient rainfall and suitable climate conditions, the forest ecosystem per unit area has high value, so the losses are huge. In addition, Liaoning Province is located in the northeast forest farm, and pine wood nematodes have developed new hosts and new vector insects here, so they spread very quickly. The area of disease increased 10 times within a year, and economic losses increased rapidly.
In this study, a long-term series of dynamic evaluation was achieved using the forestry output value index and dynamic equivalent factor method. The forestry output value index is a continuity index that reflects the inter-annual changes in forestry production. Using this index, the calculation parameters and evaluation results can be converted and discounted to the currency level of the current year to achieve a dynamic evaluation of direct economic losses. The dynamic equivalence factor uses different inter-annual food prices to construct standard equivalents, uses development stage coefficients to reflect inter-annual changes in people’s willingness to pay, and finally uses rainfall and GPP data to reflect the value of services of forest ecosystem. It not only can achieve dynamic evaluation at temporal resolution, but dynamic evaluation at spatial resolution can also be achieved.
In order to achieve quantitative evaluation, the evaluation index system constructed in this study is relatively simple and practical. We choose turpentine as the main forest by-product to assess the value of its loss due to the data accessibility, though there are a variety of forest by-products of pine trees, considering the practical difficulties in data collection. To some extent, this will lead to a lower assessment result.
Although the content of the evaluation of indirect economic losses is basically the same as the value of ecosystem services, evaluation scopes [
50] and the choice of methods [
58] are different. Forest types [
59] and site conditions [
60], are also adapted to local conditions. In addition, the evaluation results obtained in this study are based on the currency level in the year of the disease. Due to inflation and other reasons, compared with the results released by the China National Forestry Administration [
26], our evaluation results are relatively smaller, and the overall gap is not large.
This study builds a highly practical pine wood nematode disease economic loss evaluation system, and quantitatively calculates the economic losses of China’s pine wood nematode disease from 1998 to 2017, which fills the gap in the quantitative assessment of economic losses caused by pine wood nematode diseases in long-term series. Economic loss evaluation is not only an important part of natural resource and environmental value accounting, but also an essential basis for formulating disease prevention and control programs and an important basis for evaluating the effectiveness of disease control. With the continuous expansion of pine wood nematode disease, evaluation of the loss of value of pine wood nematode forest ecosystem services has practical significance for people to strengthen environmental protection awareness, improve forest management, and scientifically invest in forestry production.
This study also has the following limitations: (1) default individual parameters. Although the quantitative evaluation index system constructed in this study is based on practicability, due to the difficulty of data collection, there are still problems with the default parameters of individual revisions in practical applications. Our solution is to use the trend function for prediction, so it is possible to have some impact on the results. (2) Underestimate cultural value. Although this study included the cultural service value of forest ecosystems in the evaluation index system, more and more studies have proved that the cultural value of ecosystems has been largely ignored in the past [
61], and many of the cultural services of ecosystems are important aspects that have not yet achieved satisfactory research progress [
62]. (3) Substitute faces with points. Most of the parameters used in the quantitative calculation process are collected from different literatures, and these data are mostly sample survey data, which is not representative to a certain extent.