A Review on the Biology and Physiology of Loach Misgurnus Anguillicaudatus in China

Indian Journal of Geo Marine Sciences Vol. 47 (04), April 2018, pp.759-765

Review Article

A review on the biology and physiology of loach Misgurnus anguillicaudatus in China

James Milton 1， Bilal Ahmad Paray 2 & Irfan A. Rather 3*

1College of Fishery, Key Lab of Agricultural Animal Genetics, Breeding and Reproduction of Ministry of Education, Huazhong Agricultural University, Wuhan, Hubei, 430070, PR China 2Department of Zoology, College of Science, King Saud University, Riyadh, 11451, Saudi Arabia 3Department of Applied Microbiology and Microbiology, Yeungnam University, Gyeongsan, Gyeongbuk 38541, Korea

*[E-mail: [email protected]/[email protected]]

Received 30 August 2016 ; revised 10 October 2016

Misgurnus anguillicaudatus (Cantor 1842) is the most common loach in the world, habitually, available in Asian regions like China, Korea, India, and Japan. It lives in streams and rice paddy fields, preferably with a soft muddy bottom. The body of a typical loach is elongated with five pairs of barbs surrounding the mouth, and a single short-based dorsal fin. This species is omnivorous and source of diet usually varies from fish and insects, to plant detritus. The fish spawn multiple times per year during a spawning season that lasts from mid-April until mid-October. M. anguillicaudatus diploid individuals (2n=50) are common in wild populations. Different polyploidy populations have been reported in various locations in China. It has a delicious taste with high nutritional value, used as a traditional Chinese medicine. The most serious problem in both loach hatcheries and farms is bleeding in head, opercula, and lower jaw, swollen muscles, anus, liver, and spleen, and empty intestines. Characterization and expression profiles of tissue-specific immune genes are highly useful in understanding gene functions, tissue physiology, and transcriptomics of M. anguillicaudatus.

[Keywords: Misgurnus anguillicaudatus; Loach; Teleost, Diploid]

Introduction anguillicaudatus tend to mature very rapidly, China has a long history of reservoir fishery possessing an omnivorous digestive system, can live activities. Many reservoirs have been constructed in closely packed together, one of the most sought after China since 1950 for various purposes and are also fish with high market value. So, only a few decades used as important resources for fishery development. ago, loach fish have been farmed down in Japan 10 . The earliest stocking activity of fish seed collected Loach farms have been transformed from earth from rivers took place in Dong Qian Hu reservoir, ditches to concrete ditches 11 , migration is made which was impounded some 1000 years ago in the impossible due to such confinements 12,13 , and many Zhejiang province 1. At present, reservoir fisheries different chemicals used in the farming process has have become an important component of the fishery caused a short life span and reproduction abilities industry in China, making a substantial contribution within the fish themselves 14 . Many of the habitats and to people’s fish supplies and rural livelihoods. environments were loach fish thrive have been Environmental conservation and wise use of resources cultivated into farms for distribution to other are of major concern in developmental activities 2. countries, such as Korea, and Japan. This species are Misgurnus anguillicaudatus (M. anguillicaudatus ) now one of the most commercially viable options for is an autochthonous freshwater fish from eastern farmers and fisheries 15 . Circa 1990s, a process and Asia 3,4 . The production of M. anguillicaudatus is of system were implemented in order to allow a full life great demand, since they are used both for traditional for loach fish raised in fisheries and as of 2010, more Chinese medicine and food, especially in China, than 204 552 tons were measured and recorded 15 . Japan, and Korea. It is commonly called a Pond loach 5, Oriental weather fish 6, Oriental weather Distribution loach 7, loach (Chinese Academy Fishery Science Loach fish (in their native habitats) can be found in 2003) dojo, dojo loach 8, Japanese Loach 9. M. a number of locations around the world; but, 760 INDIAN J . MAR. SCI., VOL. 47, NO. 04, APRIL 2018

predominantly appear in, Korea, China, India, in their invaded range in Washington, their diets Thailand, Vietnam, Laos, Siberia, Japan, Cambodia, primarily consisted of crustaceans, such as amphipods and Taiwan 10,16,17,18 . Loach fish have been introduced and cladocerans, as well as chrionomids with minimal and recorded in countries such as Australia 19 , detritus and plant matter 16 . However, in another study, Hawaii 20 , mainland USA 21 , Mexico and Palau 22 , the non-native fish i n Australia were found with higher Philippines 23 , Turkmenistan 24 , Germany 25 , Italy 26 and levels of algae and detritus in their stomachs 33 . It was Spain 27 , and the Netherlands 28 . reported that loach can successfully wean to The Loach M. anguillicaudatus (Cypriniformes; formulated feeds that is feeding larval loach with Cobitidae), is a teleost, found in a number of enriched cladocerans supplemented with formulated freshwater areas; but, most predominantly in ditches, feed after 30 days 34 . rice paddy fields, streams, and places with mud and soft earth 29,10,11,13 . Due to its highly tolerable Reproduction environmental nature, fisheries and cultivation of the This species is primarily nocturnal, spending species has tremendously increased. It can live at most of the day burrowed into mud from where it temperatures anywhere from 2 to 30 oC and breathes emerges at night to feed and mate. These fish, like atmospheric oxygen through a gut located in their hind many other cypriniform fish, are generally quarter. The loach is able to survive outside water for considered selected organisms in that they matur e short time, and during drought situations, it hides into quickly, reproduce multiple times, and produce a the mud until water avaiblity 30 . great number of offspring. Members of this species The loach fish is an instantly recognizable creature, are sexually distinct and reproduce sexually. Males due to the 5 barbs found around its mouth, a short, of the species mature rapidly within a year and dorsal fin, and a long body (Figure 1). Males who females mature within one or two years 35 . In their have matured also possess a long, thick pectoral ray 31 . nat ive range, these fish spawn multiple times per M. anguillicaudatus , though similar in appearance, year during a spawning season lasting from mid - can be told apart from different forms and species of April until mid-October. Reproduction occurs at Misgurnus, due to three distinct characteristics, night in which the male locates a female based on morphological in nature 17 . scent and wraps his body around the female 1. Missing a thin stripe from the pelvis to the stimulating her to re lease a cloud of eggs that he abdomen. rapidly fertilizes 36 . The loach usually lives in 2. Odd spots located on the body, dark in color. ditches and streams around paddy fields, 3. Large spot, dark in color, located on the immigrating into water-laden paddies in order to caudal base (upper section) and a caudal lay its eggs in the summer 10,11,12 . The female peduncle featuring some crests (low adipose). produces 1800-15500 eggs per batch with an Oriental weather fish are benthic omnivores that average survival of 2000 eggs per batch 31,37 . The generally feed on insect larvae, snails, worms, eggs are small with a diameter of 800 -850mm and ostracods, cladocerans, fish eggs, algae and detritus 4. are reddish in color with adhesive properties, Kim et al . demonstrated that M. anguillicaudatus however they are broadcast into the water column readily and efficiently consume mosquito larvae and upon conception 37 . Eggs hatch within 30 hours and have successfully used them to control mosquito larvae re main in water columns for a short period populations in South Korea 32 . Tabor et al . found that before settling at the bottom 38 .

Fig. 1 — Lateral view of Misgurnus anguillicaudatus (Cantor, 1842). MILTON et al .: BIOLOGY AND PHYSIOLOGY OF LOACH 761

Table 1 — Karyological data on diploid, triploid and tetraploid samples of the loach Misgurnus anguillicaudatus Chromosome No Karyotype NF Locality 2n = 50 14 M, SM +36T 64 Sapporo, Hokkaido, Japan 2n = 50 10 M+4SM+36T, ST 64 Chinai River, Shiga + fish market, Japan 4n = 100c 16 M +12SM+72T 128 Wuhan; Shashi, China 2n = 50 8 M+ 6SM +36T 64 Chongqing, Luzhou, China 2n = 50 10 M +4SM +36T, ST 64 Fish market, Matsuzaka, Mie, Japan 2n = 50 6 M + 8SM +36T 64 Hebeiyixian, Baoding, China 2n = 50 10 M+4SM +36A 64 Fish Farm, Tottori, Japan 2n = 50 8 M+6SM +36T 64 Guiling, Yashan, China 2n = 50 8 M +6SM + 36T 64 Progeny of bloodstock from fish market 4n = 100 16 M + 12SM+ 72T 128 Wuhan; Shashi, Hubei, China 2n = 50 8 M+6SM + 36T 64 Shengnongjia, Yichang, China 2n = 50 10 M+4SM+36ST 64 Hokkaido, Japan 2n = 50 10 M +4SM+36T 64 Honghu, Hubei, China 6n=150 24M+18sm+108T 150 Wuhan, China 2n = 50 10 M+ 4SM+36T 64 Honghu, Hubei, China

Ploidy Table 2 — Biochemical analysis of serum parameters of cultured As to the loach, diploid individuals (2n=50) are and wild Misgurnus anguillicaudatus 39 common in wild populations of Japan and a small Parameter Range number of tetraploids (4n=100) have been found 40 Minimum Maximum among specimens obtained from fish dealers . In Glucose (mmol /l) 3.54 5.37 China, populations of both diploid (2n=50) and Cholesterol (mmol /l) 3.39 5.14 tetraploid (4n=100) loaches have been recorded 15,41 . Triglyceride (mmol /l) 0.88 1.81 Different polyploidy population was reported in Total protein (gm/l) 27.13 44.52 various locations in China, diploid population in Urea nitrogen (mmol /l) 1.97 3.70 Sichuan, Guangxi, Heilongjiang, Hebei and Total bilirubin (µmol /l) 5.08 8.38 Alanine aminotransferase (IU/l) 42.00 79.00 Shenglongjia, Zhijiang, Wuhan city, Chibi and Direct bilirubin (µmol /l) 1.36 3.36 Honghu and Chang Jiang River (Hubei Creatinine (µmol /l) 8.00 16.00 province) 15,42,43,44,45,46,47 triplod population in Hohhot, Uric acid (µmol /l) 0.02 0.03 Neimenggu, Tianjin, Hangzhou, Zhejiang, Chibi, Hubei, Honghu, Hubei and Shashi, Hubei 46 tetraploid where certain disasters (of an environmental nature) population in Wuhan, Shashi, Zhijiang, Wuhan city, can decrease specific anemic systems. This could be a Chibi and Honghu and Chang Jiang river (Hubei great indicator to reticulocyte count and its Province) 15,41,46,48,49 pentaploidy population in Liangzi regenerative reaction. Lake area, Yangtze River Basin 50 hexaploid population in Hubei 51 and also triploid population in Medicinal Value Japan 52 . Higher polyploid loaches, such as pentaploids Since 1950s, mud loach are consumed as a and hexaploids, have been produced by fertilization delicious fish food with high nutritional value and as a and manipulation strategies using diploid gametes traditional Chinese medicine. M. anguillicaudatus from the natural tetraploid loach 53,54,55,56,49,57,58,59 . The was widely cultured in the Jiangsu province of China, bringing great profit to their economy in recent previous and present cytogenetic results are 60 summarized in Table 1. years . The loach, for a long time, had been employed as traditional Chinese medicine in folk Haematology remedies for treatment of hepatitis, osteomyelitis, In fishery management, a high importance can be carbuncles, inflammations, and cancers, as well as for placed on cross examining both the status and health restoration of health in debilities caused by various of loach fish and some noteworthy conditions have pathogens and aging 61 . Some active substances been found in their blood as shown in Table 2. They obtained from loach were found to be of high medical have been observed to retain high amounts of mature value 62,63,64,65,66 . Studies on the medicinal values of erythrocytes over immature ones. This could also lead loach showed at various compounds by several to the fact that dissolved oxygen becoming a problem authors (Table 3). 762 INDIAN J. MAR. SCI., VOL. 47, NO. 04, APRIL 2018

Table 3 — Medicinal Properties of Misgurnus anguillicaudatus Organs Compound Use Skin Mucus Glycoprotein Skin mucus Lecitins Lyse tumor cells Muscle Antimicrobial peptides Potent antimicrobial activities against bacteria and fungi without haemolytic activity Mucus Novel polysaccharide (MAP) Potential biomedical drugs against Bacterial and viral infections and exhibit antitumour activity Muscle MAPP (Polypeptides) Antimicrobial polypeptide

Table 4 — Bacterial diseases reported in Misgurnus anguillicaudatus Agent Symptoms Treatment Vibrio Vulnificus ulcer showed that muscle Ciprofloxacin, gentamycin, norfloxacin, cefuroxime, cefoperazone, ceftazidime and ceftriaxone treatment. Aeromonas sobria redness of body, bleeding spots on the body surface Nil and ulcer foci Aeromonas veronii Skin ulcers, yellow liver and hyperaemia of the Not reported intestine wall Vibrio cholorae bleeding in head, opercula, lower jaw, fins, and fin Antimicrobial agents bases, swollen muscle, Aeromonas sobria Ulcer disease Antimicrobial drugs; Norfloxacin arafloxacin hydrochloride , thiamphnicol and sulfamethoxazole Aeromonas sobria Ulcer disease Antimicrobial drugs Aeromonas hydrophila abnormal swimming behavior, diffuse bleeding on Antibiotics the skin around the anal orifice M. anguillicaudatus and makes them unsuitable for Diseases 71 Bacterial infection is a common and serious human consumption . Mass mortalities have been reported in M. anguillicaudatus due to infection by economic problem in the cultivation of M. 72 anguillicaudatus . Mud loach are susceptible to a wide Centrocestus Formosanus, a trematode parasite . range of bacterial infections. Mortality has been reported Lernaea cyprinacea (anchor worm), an ectoparasitic on M. anguillicaudatus living in different habitats for crustacean, causes infections in skin and the buccal cavity wall of M. anguillicaudatus, which makes the many decades. A serious mortality of cultured loach M. 73 anguillicaudatus occurred in farms of Donghai County, fish susceptible to secondary infections of bacteria . Jiangsu Province in October 2008 67 and 2010 60 . Subclinical covert infectious pancreatic necrosis Currently, the most serious problem in both loach (IPN), a highly contagious viral disease caused by hatcheries and farms are bleeding in the head, opercula, IPNV and a bi-segmented double-stranded RNA virus belonging to the family Birnaviridae, have been and lower jaw, swollen muscles, anus, liver, and spleen, 74 and empty intestines 67 . There are reports of hemorrhages detected in M. anguillicaudatus . at the body surface (including base of fin, head, mouth, and abdomen), ulceration of muscles, and high-level Conclusions mortalities of loach M. anguillicaudatus cultured in M. anguillicaudatus is one of the most important China. Another important bacterial infection is the aquaculture species in China. The frequent outbreaks epizootic ulcerative syndrome. Owing to the intensive of disease have caused decreased production and culture, bacterial infections often occurred which economic losses. Studies on molecular mechanisms of resulted in serious losses 68,69,70 . Recently, it was reported this fish may be conducive to the development of that Vibrio sp. infected M. anguillicaudatus in some better aquaculture management strategies in loach farms of China 60 . Table 4 gives a summary of the Misgurnus farming. However, the gene sequence bacteria affecting freshwater loach. information of M. anguillicaudatus available in the A pathogenic Asian nematode species of public database is not extensive. DNA library Camallanus , C. Cotti Fujita, 1927, were collected construction and analysis of Expressed Sequence from aquarium-kept M. anguillicaudatus and Tags (ESTs) are efficient approaches for collecting deposited by Dr. N. P. Boyce in 1979. Clinostomum genomic information and identifying immune genes. Complanatum (Rudulphi, 1819) is a digenetic The characterization of all tissue-specific immune trematode which causes yellow grubs in the muscle of genes and their expression profiles are highly useful MILTON et al .: BIOLOGY AND PHYSIOLOGY OF LOACH 763

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