Indian Journal of Geo Marine Sciences Vol. 49 (06), June 2020, pp. 933-939

Review Article

A brief perspective on Japanese (Anguilla japonica Temminck & Schlegel, 1846) an indispensable part of Japanese culture

V K Yadava, S Pandeyb & P Kaushik*,c aDepartmemnt of Botany, Banaras Hindu University, Varanasi – 221 005, India bDepartment of Zoology, Dr Bhim Rao Ambedkar University Agra, UP – 282 004, India cNagano University, 1088 Komaki, Ueda, Nagano – 386 0031, Japan *[E-mail: [email protected]]

Received 15 November 2019; revised 02 January 2020

Anguilla japonica, also known as , is an integral part of Japanese culture from centuries. This fish spawns in the Mariana islands, and subsequently the larval stages migrate towards east Asia. Whereas, the sexually maturing return back to the spawning grounds in the ocean. Being commercially vital, the glass eels are intensively captured to be used in aquaculture systems along east Asia. This practice along with the climate change contributes to a significant decline in the Japanese eel population. Further, to counteract the increasing demand of Japanese eel in domestic market, their mass production through aquaculture systems require a higher amount of innovation in terms of their feeding and rearing technology. Here we have summed up all the important information about the Japanese eel based on the thorough survey of already published literature. Overall, this review will be useful for a better understanding of the currently available information pertaining to the species.

[Keywords: Eel, Habitat, Life cycle, Ocean, ]

Introduction freshwater8. , i.e. egg and larvae are the Japanese eel (Anguilla japonica) also known as saline environment life stages of Japanese eel9. At this Unagi in Japan is a member of genus Anguilla and stage, Japanese eel possess a transparent body, with a this genus has 16 species of freshwater eel including size of around 60 mm10. Later, glass eels migrate to the Japanese eel1. In Japan, A. japonica is an the freshwaters during the early wintertime or late important part of Japanese culture, and it is consumed spring. In freshwater, glass eels undergo physical as Kabayaki, that is the method in which the eel is cut, transformations from elvers to the more advanced seasoned with a sweet sauce and grilled for some yellow eel stage11. With maturity, elvers switch into minutes before serving2. It is also consumed as ―silver‖ eelsphase. Thereafter, silver eels migrate to ―‖ in which Kabayaki is enjoyed with rice. several kilometers downstream towards the oceans for Japanese eel is well dispersed in freshwaters of spawning12. The northwestern Pacific ocean region Taiwan, China, Korea, and Japan3. Moreover, the has been reported as the spawning grounds for the sequencing results of A. japonica individuals didn't Japanese eel, and by following the retrogressive show any genetic differences among the individuals geomagnetic direction from that of their glass eel found in these nations. At the moment, the wild stage, Japanese eel reaches the waters near the population of this Japanese eel is lower than it used to western division of the Mariana islands13,14. be in the past, and therefore, it is outlined as an During this process of migration, the endocrine endangered species by the International Union for the signals accompanied by the changes in the behavior Conservation of Nature (IUCN)4. But due to the with the catadromous migration are essential for raising demands for Japanese eel it is also raised in Japanese eel. Recently it has been established that aquaculture ponds in the east Asian countries5,6. estradiol-17β operates critically in physiological Eels are also widely used in Chinese traditional alterations of the peripheral tissues of Japanese eel medicine system for strength and as an aprotectant to during the spawning migration15. In the past decades, chronic diseases7. During its life cycle, Japanese the use of next-generation sequencing (NGS) eel undergoes two metamorphoses both under technology, and data analysis pipelines have changed different environmental conditions, saline waters and our perspective regarding the understanding of fish 934 INDIAN J GEO-MAR SCI, VOL 49, NO 06, JUNE 2020

genomics, and gene regulation16,17. NGS methods operculum (gill cover) is pretty modest even so the used for the genotyping via single-nucleotide branchiostegal rays, found underneath the polymorphisms (SNPs) are helpful in the operculum27. This is helpful in force induction during development of genetic maps, and in identification of feed ingestion and even to engulf food/prey28. the quantitative traits locus (QTLs) affecting the At the earlier life stages, Japanese eel bears a critical traits18,19. laterally compressed body containing lipids and In the recent past significant decline in the glycosaminoglycan, which are useful later during Japanese eel populations were observed in the wild. metamorphosis29. The Japanese eel spends most of its The potential causes of this decline are: climate life in freshwater for several years where they develop change, alterations inside the ocean-atmosphere, into a mature yellow eels. Later on, at full maturity habitat degradation, or overfishing20,21. However, the they change colour to silver and hence known silver precise reasons for this decline are uncertain, but the eels30. The silver eels then migrate towards the ocean eel aquaculture that sustains on the wild-caught glass to their spawning site in the ocean (Fig. 2). eel appears to be drastically influencing the abundance of Japanese eel population in the wild. To overcome this problem, development of artificial breeding technologies for the Japanese eel are in progress but, there is still a lot to be done before an artificial breeding technology become popular for achieving the commercial production targets22,23. Further, Japanese eel being one among the most important fish species in east Asia; only few studies have assessed the stock of this species. Recently, it has been pointed out that Japanese fishery estimates for glass eel are usually not correct as unlawful and unreported glass eel catches are manifest in Japan24. Following the importance and population status of

Japanese eel, the review is focused on reporting some useful information on Japanese eel concerning its role Fig. 1 — Life stages of Japanese eel in Japanese culture from a historical perspective. Further, the review also focuses on its distribution, life cycle, and spawning activity along with the genomics application in Japanese eel research. Lastly, some of the leading causes responsible for its population decline are also discussed in this review.

Distribution and life cycle The Japanese eel is distributed across east Asia, inhabiting rivers and streams of China, Japan, Taiwan, Korea, and northern Philippines during juvenile stages (Fig. 1) and subsequently upon maturity migrates to some 3000 km to their spawning grounds west of the Mariana Islands in the mid- Pacific25. Anguilla japonica is found in all types of benthic environments including rivers, streams, estuaries and lakes that are connected to the sea. The existence of glass eels is also reported in the northern Luzon Island of the Philippines. Japanese eel, as compared to other eel species, possess an elongated

body, along with a dorsal fin. The vertebrae in Fig. 2 — The distribution map of the Japanese eel (Source: 26 Japanese eel usually range between 114-118 . The Shinoda et al.31) YADAV et al.: A BRIEF PERSPECTIVE ON JAPANESE EEL (ANGUILLA JAPONICA) 935

Artificial induction of life cycle and it depends on pH and several enzymes. Later, Japanese eel matures by the activity of after six days of hatching the pancreas start to gonadotropic hormones emitted from their pituitary develop, and hence proper digestion of ingested food gland. Artificially induced maturity is critical in the via several types of pancreatic enzymes, viz. Japanese eel as they do not spawn naturally under trypsinogen, amylase, and lipase41. During the captivity32. The use of artificial hormone treatment for leptocephali stage the larvae acquire several kinds of the completion of maturity has been tried since 1960s, bacteria as a part of gut microbiota because of its therefore several attempts have been made to ability to choose from several food sources that end standardize the artificial maturity treatment for the up in increasing its gut microbiota42. Japanese eels. The exogenous supply of gonadotropic On the basis of feeding habits, it can be concluded hormones to the inseminated eggs at the earlier that the larvae of Japanese eel feed upon marine snow developmental stages, results in the difficulties in the (organic matter)40; whereas, the glass eels are time of ovulation33–35. The collection of a large omnivorous and feeds mainly on amphipods, number of downstream-migrating eels from the wild copepods, and insect larvae as they process a well especially the female eels for the egg production were developed stomach and mid-gut. At yellow eel phase, challenging; therefore, the use of reared or framed they behave as a nocturnal predator; using olfactory eels was thus considered by orally supplying the system to locate their prey. This behaviour of estrogen (estradiol-17β) at the glass eel stage for the Japanese eel continues till the silver eel stage and induction of feminization. Thereafter, the maturity thereafter the silver eel stop feeding and prepare for was provoked during the later stages15. Whereas, for their journey to the spawning grounds. Under usual the induction of maturation and for attaining the circumstances, eel usually feeds upon small fishes, complete life cycle hormonal treatments were invertebrates, and on crustaceans26. suggested regularly36. Okamura et al.37 produced the second-generation larvae using the management Spawning practices and hormonal treatments, that were Japanese eel utilizes the ocean environment for metamorphosed to the glass eels. This was a huge their spawning activity around the deep tropical breakthrough that a ―full-lifecycle culture‖, was waters. Japanese eel is a panmictic population and developed in the case of Japanese eel for the first time migrate to extensive distances offshore to spawn in a in the history of this species37. Although, the common spawning area43. The spawning zones of leptocephali growth under artificial condition is Japanese eel were found in North Pacific as slower than that of natural environment and confirmed by several surveys that gathered freshly metamorphosis could not start even after the total hatched larvae and eggs from the region. Precisely, length of 60 mm (common size for metamorphosis in the spawning-zone of Japanese eel is positioned the wild). To overcome this issue, starvation latitudinally between 12-15° N44,45. The otolith treatment was contemplated to speed up the analyses along with the observations on larvae metamorphosis at an appropriate size38. Based on the gathered during the surveys confirmed that spawning research in this direction, indeed there are firm hopes of Japanese eel manifests all through new moon for early technology development for the stable mass durations. Therefore, it is being hypothesized that production of glass eels. Japanese eel spawn just right before the new moon in the vicinity of shallow saline waters. Pop-up tag Food habits experiments with the Japanese eel and as well as with During the early growth stages, the larvae feed on anguillid eels confirmed that they migrate concerning marine snow, right before their glass eel phase. Later depths of about 100-400 m46,47. Moreover, Japanese these glass eels travel to the estuaries and headwaters eel possess a geomagnetic perception which might be of rivers and sustain their life by feeding upon small useful in their assistance to spawning grounds48. insects, shrimp, and sometimes by feeding upon small Apart from these, there are speculations that the fishes39,40. Eels are said to be temperature-dependent species uses different types of odors and pheromones, on their feeding habits as no feeding activity is to identify their mates for spawning activity. The observed at temperature below 10 ºC. During the newly hatched preleptocephali were collected in the larval stages, nutrition is critical for the Japanese eel, vicinity of Mariana Islands, west to Suruga Seamount 936 INDIAN J GEO-MAR SCI, VOL 49, NO 06, JUNE 2020

(14–17° N, 142–143° E)49. Pop-up satellite related traits in the juvenile stages (leptocephali and transmitting tags are frequently utilized to know the glass eel) of Japanese eel63. Other flavours of NGS detailed migratory behavior of eels in the northern that are exceptionally valuable for non-model and southern hemisphere. These experiments outlined organisms include restriction site-associated DNA that silver eels are remarkable swimmers, and their sequencing (RAD-seq) and double digest restriction- directions are guided partially by a geomagnetic site associated DNA (ddRADseq) which provided perception50. Accurately, how they arrive at their useful information with respect to the panmictic spawning grounds has not been investigated in detail nature of Japanese eel64. Using these approaches, so far51. Recently, Aoyama et al.52 concluded that, eel researchers have provided useful information on the eggs were found disseminated between 150-180 m genome duplication. In a study by Igarashi et al.60, deep confronting the shallow spawning depths for from Kuma river, Japan pointed out that panmixia Japanese eel52. Other ocean-atmosphere or climatic does not occur in Japanese eels but exhibit the conditions are also responsible for larvae production sympatric speciation. Recently, Higuchi et al.65. and survival53. studied ovulation of the Japanese eel applying comparative trans-omics analyses (transcriptome and Population genetics and genomics of Japanese eel metabolome) along with feeding behavior of Japanese Further, to determine the genetic variation at the eel in which they concluded that the prolonged intake nucleotide level, the advancement in genomics has of a high-carbohydrate diet along with a deficient opened new horizons. Same is valid with the DHA/EPA/ARA ratio in the feed is the primary cause development of the latest proteomic tools for the of the ovulation problems in Japanese eel. The estimation of the amino acid level changes54,55. Since genotyping performed with SNPs could provide 1970s, a sharp decline in the population of Japanese useful information about the population structure of eel was noticed and this has ignited the studies related Japanese eel, as shown in the previous studies66,67. to the genetic structure in the Japanese eel via Moreover, SNPs discovery using RAD-seq is cost- molecular approaches employing the use of molecular effective, and recently, a study concluded a little markers for the management of Japanese eel. But the degree of population differentiation between cohorts studies have resulted in contrasting results regarding Japanese eel collected from eight different locations the population structure of Japanese eel, for example, of China68. using allozyme and mitochondrial DNA markers the concept of panmixia in Japanese eel was established Causes of population decline and this viewpoint was challenged by employing The decline in the fish population is not uncommon microsatellites (SSRs) and very recently with single and Japanese eel is not an exception to this trend. The nucleotide polymorphism (SNPs)56–60. Japanese eel populations everywhere in its natural The use of genomics in fisheries is proved very environment, have declined due to the blend of useful and also widely accepted in fisheries science in overfishing and habitat degradation. Tsukamoto et al.69 recent decade. Similarly, in the case of Japanese eel described the causes of population decline as the studies involving the genomic approaches has short/annual variations (El Niño), the mid-term increased many-fold in the recent past. Several draft changes (global warming) and long-term changes like genome sequences of Japanese and European eel are glacial cycles and continental drift. However, the available for comparative genomics which opens decline in Japanese eel population is partly held many possibilities for the eels61. While, the responsible for the fact that their reproductive ecology transcriptomic studies were also performed for the is hidden under the vast ocean and therefore the actual Japanese eel, and a lot of new information is added cause of their population decline is hard to point out70. related to gene expression at different environmental Global warming also interferes with spawning activity conditions like stress and maturity62. Moreover, there and further also in the transportation of resultant is still a lot of work needs to be done in the direction leptocephali. Lots of such unfavorable larval transit are of proteomics and metabolomics. assumed to lower the recruitment achievements at river Using these genomic tools, fine mapping of the mouths as glass eels71,72. Indeed, the most important QTLs for some of the important polygenic traits was causes of population decline are pollution, loss of performed such as body size and metamorphosis habitat, changing climate, predation and overfishing73,74. YADAV et al.: A BRIEF PERSPECTIVE ON JAPANESE EEL (ANGUILLA JAPONICA) 937

Based on the recruitment trends of glass eels, it was survival rate and optimizing the advancement of estimated that the population of Japanese eel has Japanese eel larvae is usually maximized with suitable declined by almost 40 %(ref. 71). The overfishing is also food supply and by adopting sustainable practices. responsible for the severe decline in Japanese eel Herewith, it is suggested to focus on the substitution population as close to 80 % of the Japanese eels at the of fishmeal with sustainable protein resources. glass stage is caught by human beings before, they Moreover, application and developments in the field could reach the yellow phase. Similar trends for other of genomics will help in overcoming the population eel species have been recorded by the many workers, decline noticed by Japanese eel stock. Further, e.g. around 20 % of decline was noticed for the application of NGS approaches and tools can shed freshwater eels in a decade75,76. more light on the essential mysteries of Japanese eel Moreover, climate change by changing species behavior and research. interactions is considered as one among the significant causes of population declines and Conflict of Interest extinctions. Therefore, identifying these proximate The authors declare no conflict of interest. causes of population declines may be critical for Author Contributions pointing out the root causes for decline of Japanese PK conceived of and designed the project; eel population. This climate change driven effect in supervised the study and corrected the final draft. the Pacific ocean is known as El Niño. The resultant VKY, SP and PK wrote the manuscript. All authors ocean currents resulted in the exceptionally 77,78 read and approved the final manuscript. depreciated eel catches in East Asia . 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