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The Widespread Distribution of the Venomous and Poisonous Blue-lined Octopus <italic>Hapalochlaena</italic> spp., in the East/Japan Sea: Possible Effects of Sea Warming
The Widespread Distribution of the Venomous and Poisonous Blue-lined Octopus Hapalochlaena spp., in the East/Japan Sea: Possible Effects of Sea Warming
Fisheries and aquatic sciences. 2012. Mar, 15(1): 1-8
Copyright ©2012, The Korean Society of Fisheries and Aquatic Science
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.
  • Received : September 09, 2011
  • Accepted : January 01, 2012
  • Published : March 30, 2012
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About the Authors
Ji Hoe Kim
Food Safety Research Division, National Fisheries Research and Development Institute, Busan 619-705, Korea
kimjihoe@korea.kr
Toshiyuki Suzuki
Biochemistry and Food Technology Division, National Research Institute of Fisheries Science, Fisheries Research Agency, 2-12-4, Fukuura, Kanazawa, Yokohama, Kanagawa 236-8648, Japan
Kil Bo Shim
Food Safety Research Division, National Fisheries Research and Development Institute, Busan 619-705, Korea
Eun Gyoung Oh
Food Safety Research Division, National Fisheries Research and Development Institute, Busan 619-705, Korea
Abstract
The geographical distribution of the toxic blue-lined octopus (commonly known as the blue-ringed octopus), Hapalochlaena spp., around the East/Japan Sea was investigated. Observation records of the octopus were gathered using commercial search engines on the Internet. A questionnaire to complement and enhance the base data was conducted that targeted fishermen from areas where the octopus was most likely to occur, i.e ., the southeast coast and islands of Korea in the East/Japan Sea. Overall, 32 observational records of the blue-lined octopus were found from Korea and Japan. In Korea, only one record, from 2003, was found on a website; none of the 240 fishermen who participated in the questionnaire reported seeing blue-lined octopus. However, a total of 31 observa-tions of the blue-lined octopus from 2004 to July 2010 were found from 17 different regions in the East/Japan Sea and neighboring waters in Japan. Twenty-two cases were from coastal Honshu Island, and nine were from the west coast of Kyushu Island, Japan. The northern distributional boundary of the blue-lined octopus on the Japanese coast was off Fukui Prefecture around latitude 36°10' N. Our results indicate that the blue-lined octopus is distributed extensively along the Japanese coast, at a low frequency, in the East/Japan Sea.
Keywords
Introduction
Members of the octopus genus Hapalochlaena are charac-terized by small body size and iridescent blue markings on their dorsal surfaces and arms. Hapalochlaena is composed of three octopus species, H. fasciata , H. lunulata , and H. macu-losa . All three are commonly called blue-ringed octopus be-cause of their distinctive patterns of iridescent blue rings or lines, but H. fasciata is the blue-lined octopus, H. lunulata the greater blue-ringed octopus, and H. maculosa the lesser blue-ringed octopus (Norman, 1998).
Hapalochlaena spp. are equipped with venom in their pos-terior salivary glands that aids in the capture of prey, and con-tain tetrodotoxin in their soft tissues (Sheumack et al., 1978; Williams and Caldwell, 2009). Envenomation by these species has been responsible for human fatalities and should be treated urgently (Williamson et al., 1996; Cavazzoni et al., 2008; Wil-liams, 2010). Two people died and 85 patients were hospital-ized due to the consumption of blue-ringed octopus in south-ern Vietnam in 2004 (Agence France-Presse, 2004).
Among the Hapalochlaena species, the blue-lined octopus, H. fasciata , is commonly found in the waters off the coast of Australia but its range extends through the Pacific Ocean north to Japan (Williamson et al., 1996). Hapalochlaena fasciata
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Geographical distribution of the blue-lined octopus observed in the East/Japan Sea and adjacent waters and the general pattern of surface currents in the sea and neighboring waters. Acute angled triangles indicate geographical distribution of the blue-lined octopus along the Pacific coast of Honshu Island, Japan (from Kubodera, 1994). The localities of circled numbers correspond to the place numbers in Table 1. TWC, Tsushima Warm Current; EKWC, East Korean Warm Current.
was distributed north to the southern islands of the Japanese coast until the 1970s (Hashimoto, 1977), but the distributional boundary of the species moved northward to the Boso Penin-sula (refer to Fig. 1 ) on the Pacific Coast of Honshu Island in the 1990s (Kubodera, 1994). Incidentally, a specimen of H. fasciata was found at the Oki Islands, Japan, in the East/Japan Sea in 2005 (Kohtsuka, 2006) and it was suggested that the octopus could have migrated into the East/Japan Sea.
Biotic and abiotic factors may influence the distribution of marine organisms (Kolar and Rahel, 1993; Bhattacharjee et al., 2009) and the distribution of cephalopods, including octo-puses, can be affected by environmental factors (Boyle, 1990; Semmens et al., 2004; Pierce et al., 2008; Leite et al., 2009). Water temperature has a fundamental effect on physiologi-cal processes and the maintenance of homeostasis in aquatic animals (Venables et al., 1978; Hoegh-Guldberg and Bruno, 2010), and it is probably one of the most important factors influencing the distribution of octopuses (Collins, 2002; Ché-dia et al., 2010). Recent sea warming could cause a shift in the distribution of marine organisms from low-latitude regions toward the poles (Walther et al., 2002; Parmesan and Yohe, 2003; Perry et al., 2005). The East/Japan Sea is one of the most rapidly warming large marine ecosystems in the world (Belkin, 2009), and its warming is expected to cause migration of marine organisms from subtropical waters. Spread of the blue-lined octopus from adjacent subtropical water into the East/Japan Sea could be a significant threat to Koreans and Japanese because the organism possesses a powerful toxin. Furthermore, coastal residents along the East/Japan Sea have no experience with the dangers of this species of octopus. Esti-mating the geographical distribution of the blue-lined octopus would be useful for public safety. However, there are very few published reports on the geographical distribution of the blue-lined octopus in the East/Japan Sea, except for one specimen that was found on Oki Island, Japan (Kohtsuka, 2006).
Although direct survey techniques, such as visual surveys and fishing data, are more effective for estimating the spatial distribution of octopuses (Pierce and Guerra, 1994; Hill and Wilkinson, 2004; Leite et al., 2009), these methods require extensive field research and funding. We hypothesized that, because Internet use is widespread and there is common ac-cess to the Internet in Korea and Japan (International Tele-communication Union, 2010), information on websites may be used as basic data for a large-scale distribution survey of an organism.
In this study, we conducted a survey to determine the geo-graphical distribution of the blue-lined octopus using Internet search engines and a questionnaire. Individual observation records of the blue-lined octopus were gathered from web-sites in Korea and Japan, and every datum was used to create a large-scale geographical distribution map in the East/Japan Sea.
Materials and Methods
- Study area
The East/Japan Sea is a semi-enclosed marginal sea sur-rounded by Korea, Japan, and Russia. It is connected to the ad-jacent ocean by shallow straits. Warm water originating from a branch of the Kuroshio Current, which is a strong warm cur-rent in the western North Pacific Ocean, flows into the East/Japan Sea through the Korea/Tsushima Strait and flows out through the other straits (Cho and Kim, 2000; Kim et al., 2001; Taegue et al., 2006; Na et al., 2009). The Northwest Pa-cific Ocean, especially the East/Japan Sea, the East China Sea, and the Kuroshio Current, are the most rapidly warming ma-rine environments in the world (Belkin, 2009). We designated the East/Japan Sea and adjacent waters as the survey area to determine changes in the distributional range of the blue-lined octopus in relation to climate change.
- Data collection
Four commercially available internet search engines were used to find records on the Internet. Daum ( http://www.daum.net/ ), Google Korea ( http://www.google.co.kr/ ), Naver (http://www.naver.com/), and Yahoo! Korea ( http://kr.yahoo.com/ ) were used for Korean information; goo (http://www.goo.ne.jp/), Google Japan ( http://www.google.co.jp/ ), MSN ( http://jp.msn.com/ ), and Yahoo! Japan ( http://www.yahoo.co.jp/ ) were used for Japanese information. The same search terms were entered in the search engines. Two words in the Korean language were entered at the same time in the Korean search engines because there is no common name for the blue-lined octopus (or the blue-ringed octopus) in Korea. One word ( Dok in Korean) meant toxin, poison or venom, and the other word ( Muneo , Jukkumi , or Nakji in Korean) meant octopus. We also searched for “ Hapalochlaena ,” “blue-ringed octopus,” and “blue-lined octopus” in English on the Korean web-sites. In contrast, the common Japanese name of the blue-lined octopus is Hyomondako (Kubodera, 1994) and this was en-tered in the Japanese search engines. Among the results from Japan, information found from the prefectures along the west coast of Kyushu Island and Honshu Island, Japan (such as Kumamoto, Nagasaki, Saga, Fukuoka, Yamaguchi, Shimane, Tottori, Hyogo, Kyoto, and Fukui) was included. Regardless of the source ( i.e ., the government, the press, and private re-cords, including scuba divers), all information was included. If the record was not complete, either lacking an observation date or place-name, the data were excluded. Overlapping in-formation was considered to be a single case. The individual observation data were collected discontinuously from July 2009 to August 2010.
- Questionnaire administered to fishermen
Korean fishermen living on the southeast coast of Korea, such as Tongyeong and Geoje, and Ulleung Island located in the East/Japan Sea, were surveyed during July and August 2010. The questionnaire participants were 145 fishermen from Tongyeong, 53 fishermen from Geoje, and 42 fishermen from Ulleung Island. Before starting the survey, we explained, with photographs, the general characteristics of the blue-lined octo-pus including body size, change in body color and the brilliant iridescent blue lines or blue rings.
Results
Internet reports of sightings of the blue-lined octopus around the East/Japan Sea are listed in Table 1 ; the locations were marked on a map and their geographical distribution is shown in Fig. 1 . The circled numbers in Fig. 1 correspond to the place numbers in Table 1 .
Overall, via the Internet, 32 sightings of the blue-lined octo-pus were found from 18 different regions in Korea and Japan. In Korea, there was some information on Hapalochlaena spp. on the Internet, but an actual record of the organism was found at only one website. The pictures taken at Jeju Island, Korea, in 2003 were from a solitary observation. The octopus in the picture taken at Jeju Island was recorded as H. fasciata on the website. Questionnaires to complement and enhance the base data targeted fishermen. However, none of the 240 fishermen questioned had observed a blue-lined octopus. Furthermore, none of the questionnaire participants knew that the blue-lined octopus existed or that an octopus can be dangerous.
In Japan, a total of 31 observation records of the blue-lined octopus were found on the Internet. Twenty-two cases were from the East/Japan Sea coast of Honshu Island, and nine cases were from the west coast of Kyushu Island ( Table 2 ). The blue-lined octopus was first recorded along the Japanese coast of the East/Japan Sea in Maizuru Bay in 2004 (number 16 in Table 1 and Fig. 1 ). After this observation, the octopus was found in various regions on the East/Japan Sea side of Japan. The northern distributional boundary of the blue-lined octopus in the East/Japan Sea was off Sakai, Fukui Prefecture, Japan (around latitude 36°10' N). Based on information from four websites, the blue-lined octopus was observed 14 times on Omi Island (numbers 11 to 24 in the Appendix 1), Yama-guchi Prefecture, located on the southwest coast of Honshu, Japan (number 10 in Fig. 1 ). Although observed depths and water temperatures were not recorded in every case, the blue-lined octopus was found to a maximum depth of 19 m and in a water temperature range of 12-18℃. Furthermore, a blue-lined octopus, while brooding her eggs, was photographed four times on Omi Island from February to April 2009. These observations provide evidence of reproduction of the octopus in the East/Japan Sea. The blue-lined octopus was observed in all months of the year except September and October, but was found most frequently in April around the East/Japan Sea
List of internet records of the blue-lined octopus: observed regions and dates around the East/Japan SeaThe place number is represented as a circled number inFig. 1.
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List of internet records of the blue-lined octopus: observed regions and dates around the East/Japan Sea The place number is represented as a circled number in Fig. 1.
Number of blue-lined octopus observed cases by month on the coast of the East/Japan Sea and adjacent waters
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Number of blue-lined octopus observed cases by month on the coast of the East/Japan Sea and adjacent waters
( Table 2 ). We found that the blue-lined octopus was distribut-ed extensively around the East/Japan Sea side of Japan. To the best of our knowledge, this is the first report on the large-scale geographical distribution of the blue-lined octopus around the East/Japan Sea.
Discussion
- Usefulness of the Internet for a large-scale distri-bution survey of the blue-lined octopus
The Internet is a widespread source of information and its use is prevalent in Korea and Japan. In 2008, the percentage of households with access to the Internet in Korea and Japan was 94.3% and 79.8%, respectively (International Telecom-munication Union, 2010). Many observation records of the blue-lined octopus around the East/Japan Sea were gathered via the Internet. The Internet search method used here is not comparable to common systematic fisheries survey methods, such as fishing data or visual survey techniques (Pierce and Guerra, 1994; Hill and Wilkinson, 2004; Leite et al., 2009). A systematic survey of the blue-lined octopus over wide geo-graphical regions is not easy because of its small size and be-cause its skin color makes it almost invisible. Moreover, col-lection of accurate fishing data is difficult because there is no commercial fishery for the blue-lined octopus (Norman, 1998) and very little is known about its population density in specific areas. The results of our survey may not be sufficient as part of a public safety program, although they can provide useful information to warn of possible food poisoning or bites.
Through this study, we proved the usefulness of the Internet for a large-scale survey of the blue-lined octopus. In many cases, the date and place of observation or photos taken in the field of the blue-lined octopus were gathered. Species-specific features of the blue-lined octopus, such as iridescent blue lines on the dorsal mantle, can be observed in most of the octopus photos posted on the Internet. Country-specific commercial search engines were used in Korea and Japan. Some records were found by all search engines, while others were found only by some search engines. Several search engines were needed because different search engines provided different re-sults. Similar results have been reported by other investigators who have compared the usefulness of Internet search engines for finding health information (Wu and Li, 1999; Merion et al., 2000).
- Geographical distribution of the blue-lined octo-pus around the East/Japan Sea and factors affect-ing its distribution
The blue-lined octopus is found along the Pacific Coast of Honshu Island and the southern islands of Japan (Kubodera, 1994), but very little is known about the geographical distribu-tion of the octopus on the East/Japan Sea coast of the country. Global warming is expected to cause migration of the blue-lined octopus from existing habitats, much the same as for fish (Walther et al., 2002; Parmesan and Yohe, 2003; Perry et al., 2005; Dulvy et al., 2008). Evidence of the spread of this octo-pus in the East/Japan Sea and adjacent waters was gathered in Korea and Japan. There was little evidence to suggest that this octopus occupies the Korean coast of the East/Japan Sea, con-trary to expectations. However, considerable evidence sup-porting the existence of blue-lined octopus in the East/Japan Sea was collected from Japan. In addition to the records listed in Table 1 , more data that lacked objective evidence, such as an observation date or location, were excluded from the Japan data. The excluded data did not affect the northern distribu-tional boundary of the species because most of the incomplete data were obtained from regions south of southwestern Hon-shu Island, Japan.
We found four photos of a blue-lined octopus brooding eggs taken at Yamaguchi, Japan, on a website. This is obvi-ous evidence that the blue-lined octopus is reproducing in the southern East/Ja-pan Sea. We suggest that the southern East/Japan Sea has become a favorable reproductive environment for the blue-lined octopus. Brooding blue-lined octopuses were found at water temperatures between 13℃ and 16℃ ( Table 1 ). Tranter and Augustine (1973) reported that the embryonic de-velopment time of the blue-lined octopus was about 2 months at seawater temperatures of 20.8-22.5℃. The embryonic de-velopmental period of Hapalochlaena spp. is temperature dependent: the higher the water temperature, the shorter the developmental period (Overath and von Boletzky, 1974). It is presumed that the embryonic development period of the blue-lined octopus at 13-16℃ will extend beyond 2 months.
Although biotic and abiotic factors affect the distribution of octopuses in the natural environment (Mather, 1982; Boyle, 1990; Collins, 2002; Semmens et al., 2004; Pierce et al., 2008; Leite et al., 2009; Chédia et al., 2010), the geographical distri-bution of the blue-lined octopus in the southern part of Japan is strongly influenced by the Kuroshio Current (Kubodera, 1994). The East/Japan Sea is also influenced by the Tsushima Warm Current, which is a branch of the Kuroshio Current. The distribution of the blue-lined octopus around the East/Japan Sea most likely corresponds to the flow of the Tsushima Warm Current along the Japanese coast ( Fig. 1 ). The Tsushima Warm Current flows into the East/Japan Sea through the Korea/Tsu-shima Strait and then separates into two or three branches. One branch, called the East Korean Warm Current, flows along the east coast of Korea and one branch flows along the Japanese coast, while the offshore branch is seasonally variable (Kaw-abe, 1982; Cho and Kim, 2000). Southeast regions, such as Tongyeong, Geoje, and Ulleung Island in Korea, are also in-fluenced by the Tsushima Warm Current, but no evidence of blue-lined octopus was collected from either Internet searches or questionnaires administered to local fishermen. Although the Tsushima Warm Current flows along the coasts of both Korea and Japan, there was a considerable difference in the distribution of the blue-lined octopus between the countries. We suggest that either the blue-lined octopus has received little attention in Korea or that there is another factor inter-rupting its settlement along the Korean coast.
The spread of the blue-lined octopus via water currents would be difficult because the octopus produces relative-ly large eggs and lacks a planktonic stage in its life history (Tranter and Augustine, 1973; Kubodera, 1994). Nevertheless, blue-lined octopus were found in large regions around the East/Japan Sea. This means that a part of the East/Japan Sea and adjacent waters may have changed to provide a suitable habitat for the blue-lined octopus, which originated in tropical and subtropical waters. The East/Japan Sea and the East China Sea around Korea and Japan are rapidly warming large marine ecosystems (Kim et al., 2001; Belkin, 2009). The net sea sur-face temperature increase in the East/Japan Sea and the East China Sea between 1982 and 2006 was 1.09℃ and 1.22℃, respectively (Belkin, 2009). The widespread distribution of the blue-lined octopus in the East/Japan Sea, originating from tropical or subtropical waters, is presumed to be caused by sea warming that occurred over a long period. Generally, pelagic species, especially fishes, are more sensitive to environmental change (including climate change) than benthos and demersal fish (Hiscock et al., 2004; Megrey et al., 2009; Rijnsdorp et al., 2009). Although the blue-lined octopus is a demersal spe-cies, the octopus was found at the relatively high northern lati-tude of 36°10' N. We suggest that sea warming has contributed to a slow northward shift in the distribution of the blue-lined octopus. Models predict that the surface water temperature in the East/Japan Sea will be 1-6℃ warmer in 2060 than at pres-ent (Murazaki et al., 2005). If the East/Japan Sea continues to warm, the blue-lined octopus will likely become more wide-spread, including along the Korean coast, especially along the southeast coast of the Korean Peninsula where it is signifi-cantly affected by the Tsushima Warm Current.
Recent sea warming is expected to cause migration of ma-rine organisms from adjacent subtropical waters to the East/Japan Sea. As we expected, the blue-lined octopus is widely distributed along the Japanese coast around the East/Japan Sea. Expansion of the range of the poisonous and venomous blue-lined octopus may increase human health risks. Invasion of the blue-lined octopus into the East/Japan Sea will increase concerns over health and food safety in Korea and Japan. Health and food safety authorities should educate the public on preventing food poisoning or envenomation by the blue-lined octopus.
- Appendix 1. Summary of records’ source of the blue-lined octopus observed around the East/Japan Sea
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Acknowledgements
The authors would like to thank Dr. Wol-Ae Lim, a re-searcher in NFRDI and Mr. Gwan-Gyu Kim, an officer on Ul-leung Island, Korea, for their assistance in the questionnaire survey. This work was funded by a grant from the National Fisheries Research and Development Institute, Korea (RP-2011-FS-020).
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