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1.Northeast Forestry University,Harbin 150000,China; 2.Heilongjiang Provincial Water Resources Department,Harbin 150000,China

Abstract The pond smelt (Hypomesus olidus),originally transplanted from North Korea,was introduced to China in 1938 and gradually distributed to various areas of China.The pond smelt was the first fish species introduced to the water of China.It not only has the function of protecting water quality,and also has high economic and nutritional values which are helpful for diversifying the fishery productive activities of China.The present review analyzed the transplantation and production status of pond smelt in China,described the key situations and factors influencing the establishment and current level of aquaculture development.Since its introduction,the pond smelt transplantation in China was distributed in Northeast of China.From the 1980s,reservoirs and lakes all over China began to transplant pond smelt,and the transplantation of pond smelt went into the outbreak period.In order to improve the efficiency of transplantation,scientific and technical personnel studied the simple and practical technology of artificial breeding and transplantation,the medicine for preventing and controlling saprolegniasis which often leads to death of fertilized eggs.To meet the demand of market,more and more pond smelt processing products have been studied and developed,such as grilled,milk flavor,fish sauce,ham-sausage,and brew vinegar of pond smelt.The pond smelt farming in China has broad prospects development,yet there are also challenges to overcome.It is recommended to take proper policies for pond smelt development,strengthen pond smelt scientific research,transplantation technology training,establish pond smelt fisheries association,support dominant enterprises,and implement brand strategy.

Key words China,Fish farming,Fish industry,Pond smelt,Transplantation

1 Introduction

The pond smelt (Hypomesusolidus) is distributed in the northern hemisphere roughly north latitude 33 degrees to the north Pacific on both sides and the Eastern Arctic Ocean coastal waters.In Asia,it was found in China’s northeast part of water,North Korea,Japan and the Far East of Russia.In North America,it is found in the north of California,Canada and Alaska[1-2].The pond smelt was the first fish species introduced to the water of China,and the general perspective is that the entrance of this species was to protect the water quality.In 1938,Chinese began to transplant pond smelt from Hamgyongbuk-do (North Hamgyong Province) of North Korea[3],but they began to introduce other fishes in the 1950s[4].The earliest transplantation of pond smelt in China was in the reservoir waters in Dalian and Changchun[3].The pond smelt not only has the function of protecting water quality,but also has high economic and nutritional values which are helpful for diversifying the fishery productive activities of China.In the 1980s,it was mainly for export earnings.After the 1990s,due to the decline of international market prices,it gradually turned to the domestic market.In this study,we mainly described the key situations and factors of pond smelt farming influencing the establishment and current level of lake and reservoir aquaculture development in China,as well as the challenges facing the consolidation of the pond smelt industry.

2 Pond smelt transplantation in China

At present,two speciesHypomesusolidusandHypomesusjaponicusbelonging to genusHypomesusare known as the pond smelt in China.TheH.oliduspasses into a land-locked form without difficulty,so it was transplanted artificially to lakes and reservoirs in almost all regions.The pond smelt was introduced to the Northeast China through the importation of embryonated eggs from North Korea in 1938 to 1942.Fish eggs were transplanted to the Xishan Reservoir and Longwangtang Reservoir of Dalian in Liaoning Province,South Lake and Jingyuetan Lake of Changchun in Jilin Province,Jingpo Lake,Xunke County and Hailin County in Heilongjiang Province (Fig.1).In 1942,more than 20 million fertilized eggs from Gaoyuan County in North Korea were put into the Aquaculture Farm of Fengcheng County in Liaoning Province by Wang Lequan and others[3].However,The pond melt transplantation had not formed the fish production in the 1940s.

There are more than 90 000 km2of lake and reservoir water areas in China[5],and most of these areas are suitable for fish farming.Administration departments have been studying how to use the idle water resources to provide more protein and promote economic development.Highly adaptive species that are widely adapted to the diversity of the ecological environment around China were given a priority consideration.From 1984 to 1985,the Fresh Water Fisheries Research Institute of Liaoning province began to transplant 25 million fertilized eggs from Shuifeng Reservoir to Tumenzi Reservoir.Unexpectedly,the fisheries production in Tumenzi Reservoir reached 2 250 kg in 1986.The Ministry of Water Resources of the People’s Republic of China held a meeting to arrange the start of the whole country to transplant the pond smelt[6].From then,reservoirs and lakes all over China began to transplant the pond smelt,and the transplantation of pond smelt went into the outbreak period.By the spring of 1989,there were 95 lakes and reservoirs (a total water surface area of 110 000 ha) transplanting and releasing about 49 billion grains of fertilized eggs in 17 provinces,where people caught fish in 68 transplantation waters,and 22 waters initially or officially formed production capacity.As of 1994,nearly 20 provinces (a total of 110 reservoirs and lakes) transplanted the pond melt (Fig 2).The national pond smelt fish production hit 200 t in 1988,soared to 6 000 t in 1994,the highest since transplantation began in 1938[7-8].

Note: five-pointed stars indicate the transplantation sites.

Fig.1Mapforthelocationofpondmelttransplantationin1938-1942

Note: five-pointed stars indicate the transplantation provinces.

Fig.2Mapfortransplantationprovincesofpondsmeltin1984-1994

2.1BostenLakeAquacultureFarmLocated in Xinjiang Uygur Autonomous Region,with the water area of 1 228 km2,this aquaculture farm began to transplant the pond smelt in 1991.The fishery production was 42 t in 1993[9],now it has already reached 2 000 t annually (Fig.3).

Data source:FishingStatisticofBostenLakeAquacultureFarm

Fig.3ProductionofthepondsmeltinBostenLakein1993-2016

The Aquaculture Farm transferred 500 million fertilized eggs from Chaiwopu Lake to Bosten Lake in 1991.Official experimental fishing data indicated that the pond smelt formed populations in 1993 and the farm began large-scale fishing in 1995 (Fig.4).In order to improve the value of pond smelt products,they founded Lanxiang Aquatic Food Limited Company to produce grilled,fried,boiled and frozen pond smelt (Fig.5 and Fig.6).

With the characteristics of delicious taste,and free of pollution,the Japanese merchants preferred the pond smelt.The products are mainly exported to Japan and accounted for 70% of Japanese market.Pond smelt production occupies the first production volume for fish cultivation and the first economic income for Bosten Lake.

2.2XiquanyanReservoirAquacultureFarmBuilt in 1995,Xiquanyan Reservoir Aquaculture Farm is located in Heilongjiang Province.The average area of water body for cultivation is 3 000 ha.This Aquaculture Farm has the potential to produce 4 000 t of fish derived from silver carps and bighead carps[10-11].Nevertheless,the Aquaculture Farm faces continued difficulties in obtaining a constant and sufficient water supply because of large amount of irrigation water.Following the first pond smelt eggs imported from North Korea in 2008,other transplantations between 2009 and 2010 produced fries used to populate the water body[12].According to statistics of Xiquanyan Reservoir Aquaculture Farm,The fish production of pond smelt in Xiquanyan Reservoir Aquaculture Farm was 150,220,250,310,320,400,and 450 t in 2010,2011,2012,2013,2014,2015,and 2016,respectively.

The fishermen usually catch pond smelt in spring and autumn.At a reasonable price,they process the grilled or frozen pond smelt and sell it to the domestic market (Fig.7,Fig.8,and Fig.9).In Xiquanyan Reservoir Aquaculture Farm,the total yield of the pond smelt ranked second,but the economic income ranked first of all the fish.

3 Transplantation technology of pond smelt

In China,the spawning grounds of pond smelt are located on the shore of lakes,reservoirs or rivers.With the water temperature reaching 3-16℃,pond smelts begin to lay eggs[7].The eggs are sticky,attached to sand,roots and plants.Temperature has a major effect on the development of pond smelt eggs which have the normal development at the temperature of 6-16℃ in China[13].Pond smelt grows,matures,spawns and dies in a year.About 5%-15% of them escape death and spawn again in the next year[14].

The adult pond smelts are caught from rivers,reservoirs or lakes all over China in every spring,or specifically March to May.The eggs,squeezed into plastic bowl or box from the fish abdomen,will be mixed with pond smelt semen and stirred with fishtail for about one minute.The fertilized eggs are attached to the collectors of palm bark which will sink to the bottom of large basins filled with water[15-17].The moist collectors covered with fertilized eggs are transported to reservoirs and lakes all over the country.The collectors are placed in the shallow waters of lakes or reservoirs hatching eggs.Within the appropriate temperature range,the higher the temperature,the faster the eggs development.The hatching days and the water temperature show an exponential relationship.The equation isD=100.89e-0.142T[13].

Photo source: taken by Lei Nian

Fig.4FishermencatchingthepondsmeltinBostenLake

Photo source: taken by Simayi Aihemaiti

Fig.5Technicianresearchingpondsmeltproducts

Photo source: provided by Altai Glacier Fish Limited Company

Fig.6FreshpondsmeltsofBostenLakewaitingforfreezing

Photo source: taken by Yu Hongxian

Fig.7WorkersofAquacultureFarmsortingthepondsmelt

Photo source: taken by Yu Hongxian

Fig.8Pondsmeltdryingunderthesun

Photo source: taken by Yu Hongxian

Fig.9Productsofgrilledpondsmelt

4 Feeding habits of pond smelt

Cladocerans and copepods are two important components in feeding of pond smelt.Go Ueshima and Hideshige Tahara[18]examined the feeding habits of pond smelt and the impact on the zooplankton community in Lake Suwa,Japan,from May to December 2001.Results showed that herbivorous zooplankters the cladoceranBosmifatalisand the calanoid copepodEodiaptornusjaonicuswere the most important prey items,accounting for about 80% of the total prey biomass in the diet of the pond smelt.The research results of Xie Yuhao and Pu Xiaoping[19]showed that the pond smelt is an omnivorous fish which are mainly fed by zooplankton (Cladocerans and Copepods,etc.),the components of its food vary with habitats.Lai Ying[9]analyzed the relationship between the disappearance of Calanoida population and the introduction ofH.olidusin Bosten Lake from 1984 to 2006.The result showed that the occurrence rate of Calanoida in the diets ofH.oliduswas high when there was abundant variety of food item.Rapid increase ofH.oliduspopulation resulted in the intensification of predation stress on Calanoida,caused the reduction of Calanoida both in species number and population size,and finally,the disappearance of Calanoida in Bosten Lake.Du Zhaohongetal.[20]studied the feeding habits ofH.olidusin Daihai Lake.The major food is Cladocera,copepods,followed by a very small amount of algae and rotifers.Lu Ziyin and Hu Qingjie[21]analyzed the feeding habits of pond smelt in Miyun Reservoir from 1996 to 1998.The main food of pond smelt is cladocerans and copepods,followed by rotifers.The average biomass of zooplankton in the Miyun Reservoir was 1.97 mg/L,peak appeared in from March to April (Rotifera) and June to October (Cladocera and Copepods 2 to 3.22 mg/L) and the biological changes are very suitable for pond smelt breeding and growth.After putting pond smelt fertilized eggs in April 2009,zooplankton species and density of Baishan reservoir decreased sharply from 3 395 ind./L in 1981 to 129 ind./L in 2009[22].

5 Diseases of pond smelt in China

A total of 111 fish species were internationally introduced into China for aquaculture which may spread widely,become invasive and could include the spread of infectious diseases in new areas[13].At present,parasitic diseases of fish is one of the highest occurrences of fish diseases in aquaculture[24].It is already known that various species of freshwater fish are an important intermediate host for a variety of human and animal infecting trematodes[25-29].Without confirmation,people simply thought that the pond smelts would be free from parasitic infestation,particularly they having a clean and translucent body,living in clear and uncontaminated lake or reservoir water.Consequently,people enjoy catching pond smelt and eat them crude in China.Nevertheless,extensive papers in Japan and Korea have reported the role of pond smelt as a second intermediate host for Clonorchis sinensis and they could be the sources of human infections[30-31].Even so,reports regarding the situation of diseases in pond smelt in China are limited.According to the publications of journals and books in China by the end of December 31,2015,pond smelt farming had not reported any parasite,viral or bacterial diseases with the exception of the saprolegnia which attacks the fertilized eggs when the water temperature reaches 18℃[1,32-35].The water mold can cause death of embryonic eggs,directly affecting the hatching rate of pond smelt fry.In the early days,aquaculture farms used the malachite green to control mildew.In order to prevent water pollution,the medicine for preventing and controlling water mildew is methyl blue and bleaching powder at present.

6 Processing technology of pond smelt

6.1GrilledpondsmeltThe fresh pond smelts are prepared by low temperature drying,then dipped and seasoned,and baked.The water content,rehydration rate,salt absorption rate and sensory evaluation were taken as evaluation index.The process criterion of grilled pond smelt is that drying temperature is 60℃,drying time is 40 h,baking temperature is 170℃ and baking time is 18 min[36].

6.2MilkflavorpondsmeltThaw: thaw time for summer and autumn: single fish 25-30 min,piece of frozen fish 2.0-2.5 h; thaw time for winter and spring: single fish 1.0-1.5 h,piece of frozen fish 3-4 h.Grading: excluding broken abdomen,no head or no tail fish,fish body length of 6-8 cm.Salt: immersion 30 min in 8% of the salt water,off odor,to make the fish tissue solid.Water rinse: wash the fish body surface with flowing water.Drying: fish dehydration in far infrared oven at the temperature of 140℃ for 25 min.Frying: fried 1-2 min in a frying pan at 180-200℃ until fish float.Seasoning: the fried fish dipped in seasoning liquid,soak for 1 min; seasoning recipe: sugar 68.5 g,salt 35.6 g,fresh ginger 30.2 g,MSG 18.5 g,butter 38 g,cook wine 5.5 mL,soy sauce 25 mL.Packing: each bag 75 g,neatly,hot filling.Vacuum seal: vacuum level 0.09 MPa.Sterilization: sterilization formula 15-40-15 min/121.1℃.Cooling: anti pressure cooling to 38℃.Wipe the bag: wipe the water vapor of the bag surface[37-38].

6.3FishSauceofpondsmeltLei Wangetal.[39]studied the processing of fish sauce of pond smelt.Taking pond smelt as key raw,under the fermentation of surimi liquid koji and soybean koji,Saccharomyces rouxii (As2.180) and Torulopsis globose (As2.202) are added in the post-mature stage to enhance the quality and flavor of fish sauce.The additive amount of yeast is 10% (As2.202:As2.180 of 1:1),the re-fermentation temperature is 30℃,the concentration of salt is 15% and re-ferment for another 6 days.The flavor of fish sauce is improved.

6.4Ham-sausageofpondsmeltZheng Shouwei and Ma Chunyan[40]studied the productive technology of pond smelt ham-sausage.Ham-sausage of pond smelt is produced by using pork and pond smelt as the raw material.Taking the fish surimi 15%,minced pork 77.4%,gravy salt 3.5%,compound fragrant-pungent power 1.5%,cooking wine 1.6%,and white sugar 1%,combining with the productive technology of high temperature sterilizing,it is able to make a kind of fish-pork combination ham-intestines.

6.5BrewvinegarpondsmeltRaw material classification,selection,processing: not allowing the acquisition of water pollution,electrical catch,dynamite catch raw fish.Shipping raw materials should not be too much,to prevent extrusion,and prevent the sunlight and rain.To be ice preservation when the temperature is too high.Not allowed to use watertight container transport,preventing blisters fish.Gently rinse the fish body in the sink filled with ice water after the selection of raw fish.Salt,acid,water soaking: rinsing clean raw fish immediately in 7 to 9 degrees Baume of saline (containing 0.3% polyphosphate) and 0.1% hydrochloric acid mixture soaking for 30 min,fish with salt water ratio of 1∶(1-2),rinsing with water to neutral,to maintain the temperature of the liquid mixture 10℃ below,so as to improve the processing quality of the fish.Pickled: raw fish in marinated liquid of 20℃ for about one hour,stirring every half an hour,remove and drain.Frying: put about 10% raw fish of oil weight into the oil heated to 170℃,fry fish to yellow brown to the surface of a solid sense.Vinegar brewing: fried fish dipped in vinegar juice (containing vinegar 100 kg,soy sauce 10 kg,sugar 10 kg,onion 10 kg,ginger 10 kg,and mix well for use),soak 2 min,remove and drain the juice.Vacuum packing: fish into the three-layer composite bag (PET/Al/CPP),immediately vacuum sealed,vacuum control at 0.093 MPa.Sterilization and cooling: fish packaged in a high pressure sterilization pot,sterilization conditions for 15-40-15/121℃,negative pressure 0.088 MPa,cooling to room temperature.Quality Inspection: after the high pressure sterilization,immediately wipe the surface of the bag of water storage,(37±2)℃ stored for 7 d,rejecting bulging bags,quality inspection,sleeve outer bag,seal and label the finished product.

6.6OtherprocessingmethodsThere are many kinds of methods of eating the pond smelt,such as braised fish,braised fish in soy sauce,dry fish,steamed fish,fried fish slices,fish balls and so on[41-42].

7 Market development prospects of pond smelt

Due to the small size of fish body,Chinese people do not like to eat pond smelt.From the 1930s to the 1970s,this kind of fish was mainly used for the purification and protection of drinking water source,such as reservoirs or lakes.Living in clean water and having no any pollution,pond smelt is very popular in Japanese market.In the 1980s,it was introduced only to Kuandian County,Liaoning Province,the annual export of pond smelt reached more than 400 t,foreign exchange earnings of 400 000 USD.Pond smelt has been the biggest export earnings in Kuandian County[43].Since the 1990s,with the rapid economic development,environmental pollution problems are becoming more and more prominent in China.The aquaculture pollution has become the serious problem on sustainable health of people.The use of chemicals in aquaculture farms has raised environmental problems owing to their potential impacts on food safety and downstream aquatic ecosystems[44].People are beginning to enjoy pond smelt which lives in clean water without any pollution and is more popular in domestic market.More and more pond smelt processing products have been studied and developed to meet the market demand and add the market value,such as grilled,milk flavor,fish sauce,ham-sausage,and brew vinegar of pond smelt.

8 General prospects of pond smelt industry in China

From the perspective of industrial and environmental value,the pond smelt farming in China has broad prospects development considering that actual production levels barely satisfy the needs of the domestic market,and even for more exportation.To this end,efforts will be made to consolidate and develop the pond smelt industry.In this situation,it is required to overcome the challenges and come up with pertinent recommendations.

8.1PoliciesforpondsmeltdevelopmentChina has a long history of aquaculture,and has made great achievements in ensuring the supply of protein.However,lessons have been learnt that the development of China’s aquaculture has been at the cost of environment.Government should release forethoughtful policies to extend science and technology,apply ecological healthful innovations,enhance green growth and make sure that aquaculture development does not sacrifice the environment.Pond smelt aquaculture is a green growth industry which will be the key to a more responsible and prosperous aquaculture in China.Government must foster a scientific pond smelt resource-based industry clusters,to play its due role.Besides,the relevant government departments should give policy support in increasing support standard transformation,new fishing nets,and technical training to make the fisheries enterprises become stronger and bigger.

8.2StrengtheningscientificresearchofpondsmeltThere are many aspects to be further studied about the pond smelt.Pond smelt is sub cold water fish species.The highest and lowest critical temperatures for its embryo development are respectively reported as 21℃ and 4℃ respectively,and favorable temperature at 10-15℃,and the larvae can grow and develop normally when the water temperature is lower than 20℃[13,45].The water temperature at the middle and lower water levels of tropical and subtropical reservoirs and lakes is not higher than 20℃ in summer,accordingly there are possibilities for expanding the pond smelt in more other regions.The behaviors of pond smelt and the changes in its population structure are different in different water bodies.It is recommended to study the competitive relationships between pond smelt and other species,species optimization and selection of pond smelt,and increase the pond smelt processing post-culturing,so as to provide added market value.

8.3TransplantationtechnologytrainingWith low educational level,fishermen are weak in the awareness of about the safety operation on water,the protection of fishery resources.Professional and technical personnel should organize fishermen and provide technical training for them every year,to carry out technical training and functional identification of fishermen,improve the overall quality and skills of fishing practitioners,and standardize the management of the reservoir or lake area,in order to strengthen pond smelt artificial breeding work,stabilize and increase the population of pond smelt.

8.4PondsmeltfisheriesassociationFishermen in the reservoir or lake areas are eager to establish pond smelt professional association.Fishermen’s Association will play a very important role for fishermen to spread risk and provide risk protection,in the financial support,reasonable fishing,safe production,standardized and orderly management,extension of wide product sales channels,protection of fisheries practitioners legal rights and interests and other aspects.

8.5SupportingleadingenterprisesIn order to accelerate the development and growth of leading enterprises of the pond smelt fisheries industry,promote the process pond smelt industry,and improve the level of fishery industrialization,financial sector should strengthen credit efforts,and government should give discount loan,financing,taxation and other preferential policies,and fishery administrative departments and fisheries technology extension unit should provide information and technology support.

8.6ImplementingbrandstrategyTo develop the deeply processed products and take famous brand products as the breakthrough point,pond smelt industry should make transformations in three aspects,namely from primary products to final products,to further improve the processing quality,and finally realize the multiple added value; from the low content of science and technology to high-tech transformation; from no brand to famous brand.In addition,it is recommended to establish a full range of brand image of public fish products,increase the added value of products and market share,to bring into play the brand effect.According to market demand,pond smelt industry should do a good job in the certification of organic foods,build and cultivate green brand of pond smelt,and greatly promote the development of green food and organic food of pond smelt.

Acknowledgements

We are very grateful to Wang Baoquan,Shi Weiliang,Xie Yuhao and other predecessors who held the research about pond smelt in China.Also,we thank the governmental departments,producer associations,and the owners of the fish farms for providing the data to this study.