On lin e F irs t A rtic le Biodiversity and Conservation of Fish in the Beibu Gulf

1Key Laboratory of South China Sea Fishery Resources Exploitation and Utilization, Ministry of Agriculture and Rural Affairs, South China Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Guangzhou 510300, China 2Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou 510300, China 3Scientific Observation and Research Field Station of Pearl River Estuary Ecosystem, Guangdong Province, Guangzhou 510300, China 4Guangdong Provincial Key Laboratory of Fishery Ecology and Environment, Guangzhou 510300, China 5Laboratory of Biological Invasion and Adaptive Evolution, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, China Article Information Received 01 March 2022 Revised 25 March 2022 Accepted 17 April 2022 Available online 08 November 2022 (early access)


INTRODUCTION
F ishes are the most important members of vertebrates which contribute more than 50% of the total number of living vertebrate animals (Nelson, 2006). Fishes are also one of the seriously threatened animal groups (Bruton, 1995). Fishes are very important food and biological resources to humans. The production of fisheries and aquaculture reached 1.79 × 10 8 tons in 2018 (FAO, 2020). Biodiversity conservation of fishes has very high ecological and economic value and is the important cornerstone for human sustainable development (Worm and Branch, 2012). Compiling an inventory of fishes in a region is the preliminary step toward biodiversity conservation and sustainable development (Mora et al., 2008;Stephenson and Stengel, 2020). In the past thirty years, many researchers have paid attention to fish biodiversity in the freshwater ecosystems of continent (e.g. South America), large rivers (e.g. Yangtze River and Mekong River), and biodiversity hotspots such as Hainan Island and Leizhou Peninsula (Reis et al., 2016;Fu et al., 2003;Kang, 2013;Xiong et al., 2018aXiong et al., , 2019. However, some regions of marine biodiversity hotspots were overlooked or greatly underestimated, such as the Beibu Gulf.

O n l i n e F i r s t A r t i c l e
The Beibu Gulf is a shared sea waters between China and Vietnam, located in the northern continental shelf of the South China Sea. Due to its geographic and climatic conditions, the Beibu Gulf has highly productive and abundant fisheries resources and is an important fishery and aquaculture sea region . For betterprotected fish biodiversity and fisheries resources, China government announced a fishing ban in Beibu Gulf in 1999. Although all types of fishing were forbidden by the Chinese government during the fishing moratorium periods, there were still fishing activities by the Vietnamese fishermen in the Beibu Gulf during that periods (Vu, 2013). Some researchers had surveyed fish biodiversity in the South China Sea . However, information of fish biodiversity is very disrupted due to lack of unified management and research between China and Vietnam government, which limited the conservation of fish biodiversity and fishery sustainability in the Beibu Gulf.
The objective of this paper was to review the status of the fish community composition and diversity in the Beibu Gulf. We also examined major cause of the decline of fishes and provide the management recommendation. This study provides information about the protection and conservation of fishes in the Beibu Gulf and gives fundamental suggestions for sustainabl use of fish and fishery resources of the Beibu Gulf in the future.

STUDY AREA
The Beibu Gulf is a semi-enclosed sea area in the north of the South China Sea. The Beibu Gulf is surrounded by the China and Vietnam and located in 17°00′-21°45′N, 105°40′-110°10′E (Fig. 1). It is an area of about 1.28×10 5 km 2 . The average water depth is about 40 m, with a maximum depth being about 100 m. The climate of Beibu Gulf is subtropical maritime and is dominated by monsoons, with an average temperature of 37.1℃. The average rainfall is about 1670 mm. Some rivers such as Red River, Fangcheng River, Nanliujiang River flow into the Beibu Gulf, and result in an extensive estuarine and mangrove ecosystem .

DIVERSITY OF FISH SPECIES
A total of 1519 fish species belonging to 42 orders, 198 families were recorded in the Beibu Gulf (Table I). The Perciformes was the order with the highest number of fish species (907 species, accounting for 59.67%) in Beibu Gulf, followed by Scorpaeniformes with 81 species, Pleuronectiformes with 71 species, Tetraodontiforme with 70 species, Anguilliformes with 66 species, Clupeiformes with 59 species. Each of the other orders possesses less than 40 fish species (Fig. 2, Table I). It is noted that 107 fish species were listed as endangered species by IUCN (Table I).
It was noted that 928 species belonging to 28 orders, 124 families and 409 genera of reef associated fishes were recorded in the Beibu Gulf (Table I). The eight most highest number of families, each with more than 20 species, and which accounted for approximately 43.71% of the total number of fish species were Gobiidae (83)

THREATS TO FISHES
Overfishing Overfishing was one of the most important threats to ichthyological biodiversity and fishery resources in the Beibu Gulf (Dulvy et al., 2003;Yu and Mu, 2006). With the engine boats introduced in the 1960s and promoted popular in the 1980s, the fishing efforts and catches had increased sharply in the past forty years (Wang et al., 2019). Lack of precise data of fishing catches in the Beibu Gulf, some researchers estimated that fishing catch had reached 8.57 × 10 5 tons each year (Zou et al., 2013). Recently, some studies have shown that the fish community compositions have changed drastically in the Beibu Gulf due to overexploitation of fishing resources (Wang et al., 2019). Now, the average stock density of many important fishes have decreased less than 10% of that in the 1960s (Wang et al., 2021). Many traditionally commercial fish species (large size and high value), such as Epinephelus spp., Lutjanus spp. and Larimichthys crocea, have been replaced by short-lived, low trophic level and small fishes (Chen et al., 2011). For example, the biomass of piscivorous fish species has decreased to only 6% of that in the 1960s . Furthermore, the population of many fishes, namely Evynnis cardinalis, Saurida tumbil, S. undosquamis, Argyrosomus macrocephalus, and Nemipterus virgatus have shown miniaturization and early sexual maturity due to overexploitation (Wang et al., 2019;. Aquarium trade has increased quickly and formed a multi-billion-dollar industry in the past forty years, and over 1000 marine fishes are involved in the global aquarium fish industry (Dey, 2016). However, it was totally different with freshwater ornamental fishes, over 90% them of which are farmed (Evers et al., 2019), the vast majority of marine fishes were caught from wild (King, 2019). It is known that Beibu Gulf supported the high biodiversity of coral reef fishes (Arai, 2015). The most important export region was Asia, which accounts for over half of the global market for aquarium fish. Both China and Vietnam were important exports of aquarium trade in Asia. Many coral fishes were captured for the aquarium trade (Arai, 2015). A great number of coral reef fish species, such as Chaetodon octofasciatus, C. auripes, C. lunulatus, C. melannotus, C. speculum, C. wiebeli, C. modestus, C. baronessa, C. triangulum, C. trifascialis, C. auriga, C. lineolatus, C. adiergastos, and C. lunula, were captured for aquarium purposes in Beibu Gulf.
Many fish species were traded as traditional Chinese medicines. There were over 60 fish species in the Beibu Gulf (Rhincodon typus, Halaelurus buergeri, Hippocampus histrix, Mustelus griseus, etc., Table I) are listed in the Chinese traditional medicines (SCSO, 1978). For example, seahorses (Syngnathidae) were rare traditional medicines in China, although some small-scale culture of seahorses occurred in Southern China. The farmers did not have enough knowledge of biology and breeding technology of seahorse, hence these small seahorse farms eventually were closed. The seahorse medicine now came from field capture. Now, all seahorse have been listed on the CITES (IUCN website, 2021).

Habitat destruction
The mangroves, coral reef, and seagrass habitats located in the Beibu Gulf (Wang et al., 2021), provided a wide range of habitat to support high diversity of fishes (Table I). However, some important habitats of fishes were destroyed for aquaculture, because of the port and other human utilizations. The mangrove areas have decreased leading to the loss of over one third of shrimp ponds in Leizhou Peninsula (Lei et al., 2022). In the past thirty years, the Beibu Gulf has become one of the busiest shipping O n l i n e

F i r s t A r t i c l e
regions of the world, and over half of the oil tankers and commercial ships sail through this sea region (Wang et al., 2021). Fangcheng port, which was the largest port in west China, planned to establish over 50.3 km shoreline and over 200 deep water berths. These large-scale human constructions had destroyed many important habitats of fish (Lei et al., 2022). Finally, the stocks of many important commercial fishes, including L. sanguineus, Therapon theraps, Gerres filamentosus, Carcharhinus menisorrah and Gymnocranius griseus have decreased quickly (Yu and Mu, 2006).

Pollution and eutrophication
Pollution had caused significant changes in the structure and function of bioresources (phytoplankton, zooplankton) and fish communities in marine and coastal ecosystems (Islam and Tanaka, 2004). Recently, some studies have focused on different forms of pollution (e.g. heavy metal, organic pollutant, microplastics) in the Beibu Gulf (Kaiser et al., 2016;Koongolla et al., 2020;Wang et al., 2020). Meanwhile, large number of nutrient imports in Beibu Gulf due to urban extension have resulted in aquaculture pollution and other human disturbances (Xiong et al., 2018a;. These overloaded nutrients caused eutrophication and harmful algal blooms and eventually fish mortality as hypoxia and toxic compounds (Xiong et al., 2018a(Xiong et al., , 2019.

Non-native species
China waters have recently been found to be threatened with non-native aquatic species (Xiong et al., 2015(Xiong et al., , 2017Wang et al., 2016). For developing aquaculture, a great number of non-native species have been introduced into China (Lin et al., 2015). The Beibu Gulf is an important aquaculture and fishery catch region of China (Kang et al., 2018) which provided large-scale aquaculture of some non-native species (Xiong et al., 2018a(Xiong et al., , 2019Wang et al., 2021). For example, the red drum (Sciaenops ocellatus), introduced for aquaculture in the surrounding regions of Beibu Gulf got widely distributed and caused great threat to native biodiversity (Xiong et al., 2018b, c;Lin et al., 2020). In order to improve the production and quality of aquaculture, more and more non-native species will have to be introduced into the Beibu Gulf in the future (Wang et al., 2021).
The Beibu Gulf is the station of origin of the maritime silk road. Now, Guangxi Beibu Gulf Port has built a total of 256 productive berths, which could berth ships of up to 2.00×10 5 tons, and its routes are been able to reach more than 100 countries in the world, with direct access to more than 200 ports in the world (Qin, 2017). Now, the Beibu Gulf has become the busiest waterway in the world.
Over half of the oil tankers and commercial ships pass through the Beibu Gulf every year (Wang et al., 2014). Inevitably, some non-native species were introduced in the Beibu Gulf by the ballast water of the ship (Wang et al., 2021), and some non-native species, such as algae (Alexandrum catenclla, and Scrippsiella trochoidea) had been distributed large scale and formed red tide, which caused a great number fish to die because of lack of oxygen (Wang et al., 2021).
Recently, aquarium became the most important introduction pathway of non-native aquatic species in China (Xiong et al., 2015(Xiong et al., , 2017Wang et al., 2016). We could buy non-native species for aquarium in some cities around the Beibu Gulf, such as Beihai, Fangchenggang (Wang et al., 2021). Many non-native fishes such as Xenostrobus securis, Glossogobius giuris, Hemichromis bimaculatus, Hippichthys spicifer, and Poecilia velifera were very popular aquarium species in the world. Thus, countries around the Beibu Gulf (China, Vietnam) cultivated a great number of non-native species, including fishes, crayfish, shellfish (Wang et al., 2021). Inevitably, some non-native fishes had escaped and found suitable habitats in the Beibu Gulf. For example, jewelfish (H. bimaculatus) had became one of the most widely distributed non-native species in the wetlands around the Beibu Gulf (Xiong et al., 2018a(Xiong et al., , 2019.

CONSERVATION
Fish biodiversity and fisheries resource is of high economic and ecological conservation significance in the Beibu Gulf. Firstly, fish was the most important protein source for about 2.7 hundred million people (92.7 million in Vietnam and 174 million in China) living in the coastal of Beibu Gulf. Secondly, Beibu Gulf provide diverse habitats (mangroves, seagrass, Coral reef, shelf, estuaries), with high biodiversity and endemism (Liu, 2013).
The establishment of protected areas was an effective measurement for fish biodiversity conservation (Xiong et al., 2018a(Xiong et al., , 2019. However, there were only a few marine protected areas that covered quite small area of the Beibu Gulf (Trung et al., 2014). In addition, the different lifehistory stages of many fishes inhabited different habitats, such as mangroves-seagrass-coral reef (Kimirei et al., 2011). Thus, the establishment of marine protected areas should cover not only important fish habitats (such as mangroves, seagrass, Coral reef) but also the connecting galleries among these habitats (Sambrook et al., 2019). Therefore, more and larger protected areas should be been stablished in the Beibu Gulf covering important fish habitats and connecting galleries in the future.

O n l i n e F i r s t A r t i c l e
Biodiversity and Conservation of Fish

O n l i n e F i r s t A r t i c l e
In order to better protect fish biodiversity and fisheries resource, China government had announced fishing ban in Beibu Gulf since 1999 (June 1-August 1 from 1999-2003, June 1-August 1 from 2004-2016; May 1-August 16 from 2017). In the fishing ban period, all forms of fishing were not allowed in the Beibu Gulf. However, some Vietnamese fishermen still continued their fishing activities during the period of fishing ban in the Beibu Gulf (Vu, 2013). The effects of fishing ban caused tensions between China and Vietnam (Vu, 2013). Therefore, we hope the government of China and Vietnam to take more co-operations to consolidated time quantum and scope in the Beibu Gulf.
The biological information (biology, ecology, distribution, and life-history) of many fish was lack, which was limited to the scientific management of bioresources and fisheries sustainability. Especially some migratory fish species (including anadromous, catadromous, and mangroves seagrass Coral reef fishes) spend partial life history in different habitats. These migratory fishes should have been paid more attention. A great number of studies have been funded by China's Belt and Road initiative. However, few studies focused on conservation of fish biodiversity and fishery sustainability in the Beibu Gulf. We call on more international cooperation of fishery scholars among China, Vietnam and other ASEAN countries.

CONCLUSIONS
A rich diversity of fish species has been observed in the Beibu Gulf, with about 107 fish species are endangered species (Table 1). However, overfishing, pollution, habitat destruction, and non-native species are main threat to fish biodiversity and sustainable utilization of fish resources in the Beibu Gulf. Therefore, more international cooperation about protected areas, fishing bans, and scientific researches should be implemented for effective protecting fish biodiversity and fisheries resource sustainability.