Published online December 15, 2022
Journal of Ecology and Environment (2022) 46:30
Sookyung Shin1 , Jung-Hyun Kim2 , Duhee Kang1 , Jin-Seok Kim2 , Hong Gu Kang3 , Hyun-Do Jang1 , Jongsung Lee1 , Jeong Eun Han1 and Hyun Kyung Oh1*
1Department of Biological Resources Research, National Institute of Biological Resources, Incheon 22689, Republic of Korea
2Korean Plant Diversity Institute, Gimpo 10111, Republic of Korea
3NATURING, Seoul 04797, Republic of Korea
Correspondence to:Hyun Kyung Oh
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
Background: Climate change significantly influences the geographical distribution of plant species worldwide. Selecting indicator species allows for better-informed and more effective ecosystem management in response to climate change. The Korean Peninsula is the northernmost distribution zone of warm temperate evergreen broad-leaved (WTEB) species in Northeast Asia. Considering the ecological value of these species, we evaluated the current distribution range and future suitable habitat for 13 WTEB tree species designated as climate-sensitive biological indicator species.
Results: Up-to-date and accurate WTEB species distribution maps were constructed using herbarium specimens and citizen science data from the Korea Biodiversity Observation Network. Current northern limits for several species have shifted to higher latitudes compared to previous records. For example, the northern latitude limit for Stauntonia hexaphylla is higher (37° 02’ N, Deokjeokdo archipelago) than that reported previously (36° 13’ N). The minimum temperature of the coldest month (Bio6) is the major factor influencing species distribution. Under future climate change scenarios, suitable habitats are predicted to expand toward higher latitudes inland and along the western coastal areas.
Conclusions: Our results support the suitability of WTEB trees as significant biological indicators of species’ responses to warming. The findings also suggest the need for consistent monitoring of species distribution shifts. This study provides an important baseline dataset for future monitoring and management of indicator species’ responses to changing climate conditions in South Korea.
Keywords: climate change, habitat suitability, Korean Biodiversity Observation Network, northward shift, species distribution model
Over the past 40 years (1980–2019), the annual temperature in South Korea has increased by 1.4°C, exceeding the global average (Moon et al. 2020), and is projected to increase by 0.63°C per decade throughout the 21st century (National Institute of Meteorological Sciences 2019). Climate change has already impacted the species distribution and community structure in forest ecosystems of South Korea, as shown by poleward shifts in the geographic distribution of evergreen broad-leaved trees and reductions in the area of subalpine coniferous forest (Kim et al. 2019; Yun et al. 2011a). If the average temperature rises by 1°C over the next 100 years in South Korea, the climate zone will move approximately 150 km northward and 150 m upward (Kong 2007). Thus, assessments of the impact of climate change on species distribution are necessary to reveal the extent of potential ecological risks.
Large-scale and long-term data are required to identify ecological changes in response to warming and enable better-informed and more effective ecosystem management for climate change mitigation and adaptation (Ims and Yoccoz 2017; Shin et al. 2021a; Urban et al. 2016). In particular, indicator species are important for monitoring environmental changes, providing warnings of impending ecological shifts, and assessing the efficacy of ecosystem management decisions (Lee et al. 2010; Siddig et al. 2016). The National Institute of Biological Resources of South Korea has designated 130 climate-sensitive biological indicator species (CBIS), including vertebrate, invertebrate, and flora species, in order to monitor the influence of climate change on the distribution of biological species on the Korean Peninsula (National Institute of Biological Resources 2017). These CBIS are continuously monitored and managed to determine all changes in life cycle, distribution, or population size owing to climate change. Notably, the CBIS are intensively monitored through the Korean Biodiversity Observation Network (K-BON), which is a citizen science project in which citizens observe and record the surrounding biodiversity.
The climate of the Korean Peninsula includes both warm temperate and cold climate zones (Yun et al. 2020) and affects the geographical distribution limits of evergreen broad-leaved tree species in warm-temperature zones (Choi 2013; Eom and Kim 2020). South Korea is the northernmost distribution zone of warm temperate evergreen broad-leaved (WTEB) forests in Northeast Asia; thus, the distribution limits of WTEB trees in this region have important ecological value (Choi 2013; Eom and Kim 2020; Yun et al. 2011a). For example, the following northernmost distributions of evergreen broad-leaved tree species and their typical communities have been designated as natural monuments for conservation and research purposes (Cultural Heritage Administration 2003): the
Quantifying the current distributional ranges of species is crucial for identifying shifts in response to future climate warming (Shin et al. 2021b). The impact of climate change on species can also be predicted using species distribution models, which are based on the statistical relationship between species occurrences and environmental characteristics (Franklin 2013; Pearson and Dawson 2003). Thirteen species of WTEB trees have been designated as CBIS and are being intensively monitored nationwide (National Institute of Biological Resources 2019). Today, the increasing spatial and temporal extents of monitoring data for CBIS (National Institute of Biological Resources 2020) are expected to enhance our understanding of the distribution range of these 13 WTEB tree species. Therefore, the aim of this study was to determine the current distribution range and predict the future suitable habitat of 13 WTEB tree species designated as CBIS in South Korea. The specific objectives of this study were as follows: 1) to construct a dataset of species distribution based on accurate data; 2) to identify northern distribution limits based on the current distribution map; 3) to identify the major climatic variables affecting species distribution; 4) to predict the suitable habitat ranges under current and future climate conditions. Our results provide useful baseline data for future monitoring and management of CBIS responses to changing climate conditions.
South Korea (33°–38° N, 124°–131° E) is located within the middle latitudes of the Northern Hemisphere, on the east coast of the Eurasian Continent and adjacent to the Western Pacific (National Geographic Information Institute 2020). It has a temperate climate with four seasons and substantial precipitation in comparison with that of the Eurasian continental features. Subalpine coniferous, deciduous broad-leaved, and warm temperate evergreen forests are common in the northern, central, and southern and island regions, respectively.
We selected the following 13 WTEB tree species designated as CBIS in South Korea:
We collected distribution records for the 13 WTEB tree species from specimens deposited at the herbarium of the National Institute of Biological Resources in South Korea (KB) (https://species.nibr.go.kr/) and the K-BON citizen science dataset. Civic organizations and citizen scientists in the K-BON observe the surrounding biodiversity and record their information (i.e., date, species name, geological location, and photos) using the citizen science platform NATURING (http://www.naturing.net/).
To determine the accuracy of the collected distribution data, we performed a validation process for all records. In the case of herbarium specimens, we included only records with the collection ID ‘NIBRVP-’, indicating that they had been confirmed by internal experts. We discarded records with obvious geocoding errors such as mismatches between administrative districts and coordinates, as well as those located in the ocean. For the citizen science data in K-BON, we selected only records with geotagged photographs in the NATURING platform. We then followed the validation procedure of species identification by experts to ensure the accuracy of the citizen science data. Finally, planted records located in villages, botanical gardens, and parks were deleted from the dataset.
We then constructed a database of valid species distributions for 13 WTEB tree species consisting of administrative districts, coordinates, date, and references (Tables S1–S13). All records were mapped according to the WGS84 coordinate system using the ArcMAP 10.0 geographical information software package (ESRI, Redlands, CA, USA). We also established the northern distribution limit by connecting the northernmost latitude points for the West Sea–Inland–East Sea on the species distribution map.
We downloaded 19 bioclimatic factors related to temperature and precipitation changes with a resolution of 30 arc-seconds from the WorldClim database v. 2.1 (http://www.worldclim.org/), which provides average data for 1970–2000. These variables represent annual trends (e.g., mean annual temperature and precipitation), seasonality (annual range of temperature and precipitation), and extreme or limiting environmental factors (temperature of the coldest and warmest month; precipitation in wet and dry quarters) (Fick and Hijmans 2017). Many of the bioclimatic variables were spatially correlated, which can result in model over-fitting when simulating the potential species distribution (Cook and Ranstam 2016). To reduce multi-collinearity among these variables, highly correlated variables (Pearson’s correlation coefficients |
Species distribution models were created using Maximum Entrophy software v. 3.4.1 (http://biodiversityinformatics.amnh.org/open_source/maxent/). This is one of the most popular tools based on presence-only occurrence records for modeling that has high predictive power across all sample sizes; thus, it is widely used to predict the distribution of many taxa (Elith et al. 2011; Kaky et al. 2020). To minimize the sampling bias effect in the datasets, we randomly selected only one record per grid cell (30 arc-seconds, consistent with the resolution of bioclimatic data) using ArcToolBox in Arc GIS 10.4.1 (ESRI). We mostly used the default settings in MaxEnt (i.e., linear, quadratic, and hinge features) (Phillips et al. 2006), except for the following settings: 30% random test percentage, 10-fold cross-validation, logistic output format and threshold rules with the maximum training sensitivity plus specificity. Model performance was evaluated using the area under the curve (AUC) values of the receiver operating characteristics curves. AUC values below 0.7 were considered poor, values between 0.7 and 0.8 were considered fair, values between 0.8 and 0.9 were considered good, and those above 0.9 were considered excellent (Phillips et al. 2006). For a better interpretation of species distribution changes under current and future climate conditions, we converted the potential distribution projections into binary maps (suitable and unsuitable habitats) according to the threshold value.
In this study, we constructed a distribution dataset for 13 WTEB tree species designated as CBIS using specimens and K-BON data (Tables S1–S13). More than 100 distribution records were collected for all species except
The distribution models for 13 WTBE tree species had AUC values > 0.90, indicating excellent model fit to the data (Table 3). The major bioclimatic variables affecting the spatial distribution differed among species. The distribution of
The response curves of the major bioclimatic variables showed the most likely ranges of occurrence for the 13 WTEB tree species (Fig. 2). According to the response curves for the two largest contributing climatic variables, the occurrence probability of
Current suitable habitats for 13 WTEB tree species were predicted in coastal areas of western and southern provinces in South Korea, where these species currently exist (Fig. 3). We also predicted potential suitable habitats in the Yeongdong coastal region of Gangwon-do, where these species are currently absent. Future projections to the 2070s showed that the distribution of WTEB tree species may extend to inland areas, which are at a higher latitude than that of current habitats (Fig. 3). Under the future climate scenario of SSP2-4.5, a suitable habitat was predicted along the western coastal areas of the metropolitan region and Chungcheongnam-do. Expansion toward higher latitudes was more marked under SSP5-8.5 than under SSP2-4.5.
Climate change significantly influences the geographical distributions of plant species worldwide (Kelly and Goulden 2008; Liang et al. 2018). Previous studies have reported the distribution and northern limits of WTEB tree species in relation to increased temperatures in South Korea. For example, Uyeki (1941) described the northern limit of 64 WTEB tree species on Daecheongdo Island–Byeonsan–Yeongam–Jukdo Island–Ulleungdo Island. Since then, Yun et al. (2011a) reported a northward shift of WTEB tree species from their previous limit to Baengnyeongdo Island–Cheongyang–Jeongeup–Pohang–Ulleungdo Island. Here, we constructed current distribution ranges to identify up-to-date northern limits for 13 WTEB tree species designated as CBIS from a total of 3,451 herbarium specimen and K-BON data.
In our study, the northern limits for several species were identified at higher latitudes than previous records (Table 2). The distribution of
The West Sea Islands lie at the northernmost line in the west of the southern coast floristic subregion of South Korea and are a very important region in terms of plant geography as they define the northern limits of many warm temperate broad-leaved species (Lee and Choi 2008; Kim et al. 2011). The West Sea Islands also allow the northward distribution of many southern plants under the influence of the West Sea Warm Current; however, accurate species distributions are unknown because of a lack of sufficient research on this island area. More recently, a new distribution of plant species has been reported on the islands through floristic studies of uninhabited islands and a detailed survey of specific islands; this was prompted by the need to understand the flora of the island region and the ease of survey access (Lee and Choi 2008, 2010; Kim et al. 2011; Son et al. 2016; Song et al. 2021). In our study, the northern limits for several species were identified at higher latitudes than previously recorded (Yun et al. 2011a). However, it is unclear if this northward species distribution shift is due to climate change, as we do not know whether they were distributed this way in the past but were just now discovered, or whether this is a novel distribution resulting from climate change. Nevertheless, establishing the current northern limits in our study provide key baseline data for detecting future shifts in species distribution. In particular, subsequent continuous monitoring data can reveal the geographical responses of species to climate changes.
The latitudes of the northern distribution limits for
Climate is a key factor impacting species distribution. In particular, identifying the climatic conditions of the northernmost regions of warm temperate forests is an important research topic for classifying vegetation zones and monitoring vegetation community structure. Many studies have reported the climatic conditions that characterize the distribution of warm temperate trees (Koo et al. 2001; Yun et al. 2011b; Eum and Kim 2020). Eum and Kim (2020) reported that the annual mean temperature of the northern limits of the warm temperate forest zone was 13–14°C (Eum and Kim 2020). Koo et al. (2001) highlighted the winter temperature as an important climate element contributing to the distribution limits of WTEB plants, with a mean temperature of –4°C and a mean minimum temperature of –9°C in January. Yun et al. (2011b) also revealed that the minimum temperature of the coldest month, which determines the distribution of WTEB trees, was –5.95°C. In this study, we found that the minimum temperature of the coldest month (Bio6) was a major factor contributing to the distribution of 10 WTEB tree species (Table 3) and was positively correlated with the habitat suitability of these species (Fig. 2). Although there was a slight difference in the temperature range that correlated with an increased occurrence probability for each species, most species preferred the minimum temperature of the coldest month to be at least –4.0°C.
In this study, the major factors affecting the distribution and preferred climate range of each species were identified by extracting the current climatic variables based on actual species locations. Our results were consistent with those of previous studies revealing the impact of winter temperature as a major factor on species distribution. Precipitation-related variables were also significant factors affecting several species’ spatial distribution. These results provide an important basis for understanding changes in the distribution of indicator species under future climate conditions.
According to the future projection of climate zones for the Korean Peninsula, the temperate climate zone in the southern region is predicted to gradually expand and occupy most of the Korean Peninsula by 2100 (Yun et al. 2020). Future climatic conditions may lead to expansion of the distribution range of warm temperate tree species that prefer warm environments, with the suitable habitats of southern species already predicted to increase under future climate change (Yun et al. 2011b; Koo et al. 2018). Our study also revealed a potential expansion in the distribution range of 13 WTEB tree species during 2061–2080 under two climate change scenarios (Fig. 3). These expanded trends toward higher latitudes coincide with previous studies on
Although increasing temperature and precipitation are projected to expand the distribution of warm temperate tree species, the actual distribution is affected by more complex factors, including biotic and terrain factors (Leach et al. 2016). For example, the warming-induced invasion of exotic species and habitat destruction from human activities can limit such distribution shifts. In particular, distributional shifts and/or migration of plant species were limited by the dispersal process (Koo et al. 2018). In our study, the potential habitats of WTEB species included the Yeongdong coastal region of Gangwon-do, which is far from their actual distribution. Because we only considered climatic factors when constructing the species distribution models, our results show the climatic habitat suitability of 13 WTEB species. Furthermore, considering the ecological characteristics of the target species when predicting their potential distribution will improve the accuracy of predictions related to the responses of the species to future environmental changes. Nevertheless, our species distribution model exhibited excellent performance, revealing the key role of temperature-related variables and predicting the expansion of suitable habitat areas under future global climate change.
This study reveals the current distribution range and future suitable habitats of 13 WTEB tree species designated as CBIS in South Korea. The major contribution of this study was the construction of up-to-date and accurate distribution maps based on herbarium specimens collected from multiple flora surveys as well as real-time K-BON citizen science data collected nationwide. Our findings confirmed the important role of citizen science data in understanding the distribution ranges of CBIS. This study also revealed an upward shift in the northern limits of several species when compared to their previous distributional ranges, as well as the expansion of suitable habitats under future climate change scenarios. Our results support the suitability of these 13 WTEB tree species as significant biological indicators of species responses to warming, highlighting the need for the continuous monitoring of their population demographics and distribution shifts. The database developed in this study also provides useful baseline data for identifying future shifts in species responses to climate change in South Korea.
Supplementary information accompanies this paper at https://doi.org/10.5141/jee.22.053.
Table S1. Distribution records of
We are grateful to the many citizen scientists that participated in the K-BON project, whose monitoring and records allowed us to construct an up-to-date and accurate species distribution dataset. We also thank the anonymous reviewers for their helpful comments on drafts of this article.
AUC: Area under the curve
CBIS: Climate-sensitive biological indicator species
HadGEM3-GC3.1: Hadley Centre Global Environmental Model in the Global Coupled configuration 3.1
K-BON: Korea Biodiversity Observation Network
SSP: Shared Socioeconomic Pathway
WTEB: Warm temperature evergreen broad-leaved
SS conceived the ideas, conducted the data collection and analysis, and wrote the manuscript. JHK conceived the ideas, checked the database, and reviewed the manuscript. DK conducted the data collection and analysis. JSK and HDJ checked the database and reviewed the manuscript. HGK conceived the ideas and reviewed the manuscript. JL and JEH reviewed the manuscript. HKO examined the manuscript. All authors read and approved the final manuscript.
This work was supported by a grant from the National Institute of Biological Resources (NIBR), funded by the Ministry of Environment (MOE) of the Republic of Korea (NIBR202225101).
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
The authors declare that they have no competing interests.
|View Full Text||Article as PDF|
|Print this Page||Export to Citation|
Research 2023-05-10 46:04High ranavirus infection rates at low and extreme temperatures in the tadpoles of Japanese treefrogs (Dryophytes japonicus) that breed in rice paddies in the summer
Nam-Ho Roh1#, Jongsun Kim2#, Jaejin Park2 and Daesik Park2*
Research 2022-09-29 46:25Distribution characteristics of Manchurian and China–Japan–Korea flora in Korean Peninsula
Nam Shin Kim1, Chi Hong Lim1*, Jin Yeol Cha1, Yong Chan Cho2, Song Hie Jung2, Shi Zhu Jin3 and Ying Nan3
Research 2022-08-19 46:22Tissue-cultured regeneration and ecological values in major bamboo species
Avinash Sharma1*, Chowlani Manpoong1, Anwesha Gohain2, Himanshu Pandey3, Gompi Padu1 and Hage Aku1