Strandings, bycatches and injuries of aquatic mammals in China, 2000–2006, as reviewed from official documents: A compelling argument for a nationwide strandings programme

Marine Policy 51 (2015) 242–250

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Strandings, bycatches and injuries of aquatic mammals in China, 2000–2006, as reviewed from official documents: A compelling argument for a nationwide strandings programme Yamin Wang a,n, Wei Li a,b, Koen Van Waerebeek c a

College of Ocean, Shandong University at Weihai, Weihai, Shandong, China Simon F. S. Li Marine Science Laboratory, School of Life Science, Chinese University of Hong Kong, Shantin, Hong Kong SAR, China c Peruvian Centre for Cetacean Research (CEPEC), Centro Peruano de Estudios Cetológicos, Lima 20, Peru b

art ic l e i nf o

a b s t r a c t

Article history: Received 27 March 2014 Received in revised form 15 July 2014 Accepted 16 July 2014

In the present study, the species composition, geographical and seasonal patterns of strandings, bycatches and injuries of aquatic mammals reported in Chinese mainland waters, from 2000 to 2006, were analyzed based on national official documents. A total of 97 strandings, 66 bycatches and 30 injuries, involving at least 18 species (possibly 20) in eight families of Cetacea and two families of Carnivora, were recorded. Finless porpoises (Neophocaena spp.), spotted seal (Phoca largha) and bottlenose dolphins (Tursiops spp.) were the most common species in all three categories, in total comprising 59.8% of strandings, 97.0% of bycatches and 86.7% of injuries. Strandings occurred throughout the year, but records of both bycatches and injuries peaked in spring (March to May), corresponding to the major fishing season and may reflect the negative impacts of fishing activities. The highest species diversity found in Fujian Province may be linked to upwelling and high production in the Strait of Taiwan. Serious difficulties were encountered in overall data interpretation and between-provinces comparability, mainly due to a lack of quantified observer effort and variable expertise levels. Hence the establishment of a coordinated nationwide network is recommended, providing a mechanism for the instant reporting of aquatic mammal events, as well as the adoption of a standardised data recording system including necropsy protocols. Better-quality data should allow quantitative analyses leading to an improved understanding of anthropogenic threats in China's aquatic mammal populations. The need to upgrade reserve management, such as the Dalian protected area in Liaoning, is also stressed. & 2014 Elsevier Ltd. All rights reserved.

Keywords: China Aquatic mammals Strandings Bycatches Fisheries Marine protected areas

1. Introduction Most cetaceans and some other marine mammals are distributed over large areas and spend the majority of their lives underwater, which makes observations difficult and studies expensive to conduct [63,9]. Many species either migrate great distances between feeding and breeding grounds or are characterized by other large-scale movements, adding to the difficulties of conducting research or monitoring programmes. As a consequence, examination of stranded cetaceans and other aquatic mammals found ashore has long been an invaluable source of information on the morphology, diet, life history, and population structure of these animals, and has helped to identify threats [19,37,5]. Longterm systematically recorded information on the time and location

n

Corresponding author. E-mail address: [email protected] (Y. Wang).

http://dx.doi.org/10.1016/j.marpol.2014.07.016 0308-597X/& 2014 Elsevier Ltd. All rights reserved.

of stranding events can provide clues regarding spatial distribution and seasonal movements, although caution is needed in the interpretation of such information. The stranding location is highly influenced by physical oceanographic features such as wind and tides [28,19,60,5]. The species composition in the records may be reflective of both distribution and disproportionate fishing efforts. There are many possible causes for strandings. Injuries (both natural and anthropogenic) and diseases may incapacitate individuals and lead them being carried passively by currents [61,39]. The injury and mortality of many populations of small cetaceans worldwide is primarily due to bycatch [41]. In some species, bycatch has caused or contributed to population-threatening levels of mortality. For example, studies found evidence of bycatch in stranded specimen samples for 63% of harbor porpoises Phocoena phocoena (Linnaeus, 1758) on the US East Coast [6] and for 79% of short-beaked common dolphins Delphinus delphis Linnaeus, 1758 examined in SW England [30]. Bycatch led even to the functional extinction of the vaquita Phocoena sinus Norris

Y. Wang et al. / Marine Policy 51 (2015) 242–250

and McFarland, 1958 [22,44,68] and the baiji Lipotes vexillifer Miller, 1918, respectively. Effective mitigation measures require the identification of high-risk areas, the magnitude of threats and the most vulnerable species. Some populations of aquatic mammals in Chinese waters are expected to decline rapidly, and a few, such as the Yangtze finless porpoise [49,67], could even emulate the extreme example of the baiji, an obligate freshwater odontocete known only from the middle-lower Yangtze River, which became functionally extinct before any effective intervention was carried out [44]. Unsustainable bycatch in fisheries of the Yangtze River is considered the primary cause of the demise of the species [44]. According to a FAO [14] report on the State of World Fisheries and Aquaculture, China remains the leader of global fisheries landings, with production at approximately 15 million tonnes in 2010. In 2007, there was a total of 288,779 marine fishing vessels with a combined power of 14.7 million kW, equipped with mainly drift and set gill nets and trawl nets, gears well-documented to cause high marine mammal bycatch rates worldwide (e.g. [46,65,40]). Studies conducted in the USA showed that, in 1994, 2500 fishing vessels operating gill nets captured approximately 6491 marine mammals and 8030 vessels operating with trawl nets captured 228 marine mammals [40]. In view of the intensive fishing activity in Chinese waters and absence of any bycatch reduction efforts, it is important to determine the level of interactions between fisheries and aquatic mammals. The highest quality of bycatch data is attained through ship-board observer programmes, but these tend to be expensive and require well-trained technicians [32]. In addition, the wide spatial distribution of aquatic mammals and the large number of fishing vessels present serious obstacles to the implementation of effective observer programmes. These factors are especially relevant in China. Consequently, data gleaned from post-mortem and clinical examinations of, respectively, stranded and injured animals are an important supplement to information obtained from ship-board observer programmes. In addition, direct reports from fishermen and information from fishery enforcement personnel in China provide relevant insights. Many countries have established reporting schemes, stranding collection networks or national databases run by various organizations (e.g. [2,70,24,25,45]) and make information available through periodic publications or in other formats. However, recording efforts are dismal in Chinese waters, which support approximately 50 aquatic mammal species along 18,400 km of coastline and in the Yangtze River. Reports of strandings in historical literature are scarce. There are published records of 1 female rough-toothed dolphin Steno bredanensis (G. Cuvier in Lesson, 1828) in 1973 [21]; 1 female ginkgo-toothed beaked whale Mesoplodon ginkgodens Nishiwaki & Kamiya, 1958, in 1980 [43,56]; 1 short-finned pilot whale Globicephala macrorhynchus Gray, 1846, in 1991 [54]; 1 Blainville's beaked whale Mesoplodon densirostris (de Blainville, 1817) in 1994 [69], and 4 gray whales Eschrichtius robustus (Lilljeborg, 1861) strandings between 1949 and 1996 [70]. The government has made little attempt to establish a standard reporting scheme or network and the status of most populations of aquatic mammals is poorly known. This lack of information hampers a proper understanding of threats and conservation needs and obstructs attempts to determine whether existing conservation measures are being effective. The authors organized the collection of official documents related to strandings, bycatches and injuries of aquatic mammals in the waters of mainland China from provincial fishery administrations for the years 2000 to 2006. The objectives of this paper are: (i) to provide an initial analysis of the species composition and the spatial and monthly patterns of aquatic mammals that were stranded, captured or injured in China based on existing official records; (ii) to encourage the standardized reporting of such

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events and to promote the establishment of a national reporting network for aquatic mammal strandings, bycatches and injuries; and (iii) to provide suggestions for improved future conservation and management policies of aquatic mammals in China.

2. Material and methods In response to an official letter from the Aquatic Fauna and Flora Conservation Office, Fishery Administration Center, Ministry of Agriculture, China, provincial and municipal fishery administrations in mainland China analyzed historical records of strandings, bycatches and injuries of aquatic mammals. Because there was no specific recording scheme targeting aquatic mammals, all the relevant data were retrieved from records within the overall category of wildlife protection. Strandings in the present paper refer to the beaching or washing ashore of live or dead aquatic mammals, as well as dead animals found floating in the water. A mass stranding was treated in this article as a single event [4]. Injuries refer to injured but live animals found floating in the water. Bycatches are animals that were reported directly by fishermen and those found entangled by fishery enforcement officers during patrols. Using reports by fishermen inevitably results in a serious underestimation of the real magnitude of bycatch because they are not obliged to report bycatch, and certainly avoid such reporting in the event of illegal fishing. However, fishermen often report to other institutions rather than fishery enforcement, which was how most bycatch information was obtained. For example, some fishermen in Weihai, Shandong, sent finless porpoise carcasses to a local university for research each time there was a bycatch. Reporting to fishery enforcement usually occurs when the fishermen are unfamiliar with an animal or for opportunistic reasons. Although they may overlap, strandings, bycatches and cases of injury were separated into distinct categories for the discussion of spatial and temporal distribution. The reports were from 8 coastal provinces (minus Jiangsu), 2 coastal municipalities and 4 provinces across which the Yangtze River flows. The period covered from 2000 to 2006, before which time there were few official records. The information supplied in each of the cases varied, but included a description of the numbers, species, reporting dates and locations, handling organizations and any treatments. Some provinces provided more detailed information, such as sex, body length, weight and body condition (alive, dead, state of injury or decomposed). However, most records included no information on the types of injuries or causes of death, nor explanations for each stranding event. Due to non-quantified and unstandardized observer effort, apparently highly variable between provinces, as well as low sample sizes per province, any comparative statistical analysis would be meaningless. Observers did not distinguish between common bottlenose dolphin Tursiops truncatus (Montagu, 1821) and Indo-Pacific bottlenose dolphin Tursiops aduncus (Ehrenberg, 1833) while both species are distributed in Chinese waters [50]. Therefore this paper refers to generic bottlenose dolphins (Tursiops spp.). Similarly, the two main morphotypes of finless porpoise [16] were not specified. The taxonomy of finless porpoises has recently been revised [23,49,51,57] with two species recognized in Chinese waters. In cooler waters predominates the narrow-ridged form Neophocaena asiaeorientalis (Pilleri and Gihr, 1972), with one subspecies Yangtze finless porpoise N. asiaeorientalis asiaeorientalis occupying the middle and lower reaches of the Yangtze River, and another subspecies, the East Asian finless porpoise N. asiaeorientalis sunameri distributed in coastal waters from the Taiwan Strait, including the western coast of Taiwan, through the East China Sea

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north to the Bohai and Yellow Seas. A second species, the IndoPacific finless porpoise Neophocaena phocaenoides (G. Cuvier, 1829), with a characteristically wide dorsal ridge, occurs in China's warmer waters from the Taiwan Strait south and east towards the Persian Gulf [23,49,57]. This study refers to generic finless porpoises Neophocaena spp. considering that records almost certainly cover both species. Common minke whales in the North Pacific, including the study area, are considered to be the subspecies Balaenoptera acutorostrata scammoni Deméré, 1986. However, no dedicated taxonomic work has been published on this taxon in Chinese waters.

3. Results

Table 1 Species composition in stranding, bycatch and injury records of aquatic mammals in the waters of mainland China for the period 2000–2006. Species are as reported by government personnel; identifications could not be authenticated by the authors. The only pantropical spotted dolphin case involved a mass stranding of 26 individuals. Species

Total

Stranding

Bycatch

Injury

Cetacea Balaenidae North Pacific right whale

1

1

0

0

Balaenopteridae Blue whale Common minke whale Fin whale Sei whale

2 6 4 1

2 6 4 1

0 0 0 0

0 0 0 0

Delphinidae Bottlenose dolphins (Tursiops spp.) False killer whale Indo-Pacific humpback dolphin Long-beaked common dolphin Pantropical spotted dolphin Pygmy killer whale Risso's dolphin Rough-toothed dolphin

18 2 10 2 1(26) 1 4 4

10 1 10 2 1 0 3 2

7 0 0 0 0 0 1 1

1 1 0 0 0 1 0 1

Lipotidae Baiji

1

1

0

0

Kogiidae Pygmy sperm whale

2

2

0

0

Phocoenidae Finless porpoises

88

39

33

16

Physeteridae Sperm whale

2

2

0

0

Ziphiidae Blainville's beaked whale

1

1

0

0

Carnivora Mustelidae Common otter

1

0

0

1

Phocidae Spotted seal Total

42 203

9 97

24 66

9 30

3.1. Species composition There were 97 stranding events (122 stranded animals), 66 bycatch animals and 30 injuries recorded between 2000 and 2006, affecting a total of 18 species1 in 8 families of cetaceans (8 species of the family Delphinidae, 4 species of Balaenopteridae, 1 species each in family of Phocoenidae, Kogiidae, Balaenidae, Physeteridae, Lipotidae and Ziphiidae), 1 species of Mustelidae and 1 in Phocidae (Table 1). The majority of stranding events were of a single animal. Only the pantropical spotted dolphin Stenella attenuata (Gray, 1846) was represented by a mass stranding of 26 individuals in July 2002, in Guangxi. The finless porpoises, spotted seal Phoca largha (Pallas, 1811) and bottlenose dolphins (Tursiops spp.) made up the large majority of all records, in total comprising 59.8% of strandings, 97.0% of bycatches and 86.7% of injury records. Among stranding records for 18 species the highest number of strandings was of finless porpoises (n ¼39), followed by bottlenose dolphins (n¼ 10), IndoPacific humpback dolphins Sousa chinensis (Osbeck, 1765) (n ¼10), spotted seals (n ¼ 8) and common minke whales Balaenoptera acutorostrata (Lacépède, 1804) (n ¼ 6). The 66 records of reported bycatch included 5 species, primarily finless porpoises (n ¼33) and spotted seals (n ¼24), but also bottlenose dolphins (n ¼7), a rough-toothed dolphin (n ¼ 1) and a Risso's dolphin Grampus griseus (G. Cuvier, 1812) (n ¼ 1). The category of injured animals included 7 species with 16 finless porpoises and 9 spotted seals predominant in this category, and 1 individual of each of the following species: roughtoothed dolphin, bottlenose dolphin, pygmy killer whale Feresa attenuata Gray, 1874 and false killer whale Pseudorca crassidens (Owen, 1846). 3.2. Spatial distribution With the exception of Jiangsu where no records were kept, the other 8 coastal and 4 riverine provinces and 2 coastal municipalities had stranding records (Fig. 1); with the highest number of reported strandings in Fujian (n ¼24), followed by Zhejiang (n ¼20), Shandong (n ¼13) and Guangxi (n ¼10). The diversity of stranded animals was highest in Fujian, with 10 species involved. Fujian was also the only province where strandings of the pygmy sperm whale Kogia breviceps (de Blainville, 1838), the Blainville's beaked whale, the false killer whale and the rough-toothed dolphin were recorded. Zhejiang had records of 3 species, but finless porpoises accounted for 75% of individuals, were finless porpoises. That species also made up 9 of 13 stranded individuals in Shandong, while there was only a single stranding record of the 1 Possibly 20 species, in case both bottlenose dolphin species and both finless porpoise species were included in the sample.

Indo-Pacific humpback dolphin. The first and only North Pacific right whale Eubalaena japonica (Lacépède, 1818) stranded on the coast of China, was also recorded in Shandong Province. Only 6 provinces had bycatch records. Fujian had the fourth highest number (n¼ 11) but the largest diversity, with 4 species out of a total of 5 reported as bycatch in China. However, approximately 70% of the individuals caught in Fujian were bottlenose dolphins. The bycatch records for other provinces were confined to finless porpoises or spotted seals. The highest number was reported for Shandong (n¼ 19; 95% of which finless porpoises), followed by Hebei (n ¼14; 71% of which spotted seals) and Liaoning (n ¼14, 93% finless porpoises). In terms of the records of injured aquatic mammals found floating alive in the water, Shandong had the greatest number (n ¼14), of which 71.4% were finless porpoises, 21.4% spotted seals, and 1 was a sea otter Enhydra lutris (Linnaeus, 1758).

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Fig. 1. Spatial distribution of stranding, bycatch and injury records of aquatic mammals in the waters of mainland China (2000–2006). Records set within boxes are in provinces for which specific location information is lacking.

For spotted seals, nearly all stranding, bycatch and injury records came from coastal areas of the Bohai Sea. For the (marine) East Asian finless porpoise, Shandong, Zhejiang and Fujian together included 93.1% of the strandings, 80% of the bycatches and 100% of the injuries. Yangtze finless porpoises were found along the Yangtze River in Hubei, Hunan, Jiangxi and Anhui, but the locations of highest concentration were areas around Yuanjiang in Hunan and Honghu in Hubei (Fig. 1). For bottlenose dolphins, 100% of the bycatch and 70% of the strandings were recorded in Fujian; most were in the Taiwan Strait and the coastal area of Quanzhou. Other records of bottlenose dolphins came from Hainan and Guangxi, but the numbers were relatively low. The Indo-Pacific humpback dolphin had 10 stranding records, all distributed in areas in which it was well-known, particularly the coastal waters of Xiamen (Liu & Huang 2000), which recorded 7 cases. The baiji had only 1 stranding record in Shanghai, at the mouth of the Yangtze River, in 1999.

3.3. Seasonality The exact sighting dates were recorded for only 68 of 97 strandings, 58 of 66 bycatches and 25 of 30 injuries. Strandings, bycatches and injuries occurred in all months, but strandings were most frequently recorded in spring and summer months, between March and August. Bycatches and injuries were most frequently reported in spring (Fig. 2A). This general trend may be not applicable to all species, but it was reflective of the seasonal patterns of finless porpoises, spotted seals and bottlenose dolphins, those species with the highest proportions of records in all 3 categories. For finless porpoises, strandings in spring made up more than 50% of all records (Fig. 2B). The large majority of bycatches (93.3%) were recorded in spring, concentrated in May. For bottlenose dolphins, strandings were recorded more evenly throughout the year, but bycatch was also most frequently reported in spring (71.4%). Spotted seals were recorded only in

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Y. Wang et al. / Marine Policy 51 (2015) 242–250

higher during spring and summer, a common phenomenon in many field observer programmes, it could partially or fully explain the observed peaks in those seasons. 3.4. Causes of stranding and injury and treatments There was almost no information documenting the cause of strandings. Of all 97 stranding records, only 6 provided possible causes: 1 sei whale Balaenoptera borealis Lesson, 1828 stranded in Hainan was suspected to have contracted a bacterial infection (however no pathology report was available); 1 finless porpoise ‘stranded when chasing prey’; 1 old baiji stranded with a severe head injury and 3 stranded Indo-Pacific humpback dolphins were presumably killed by an underwater explosion used to remove rocks for construction purposes. Only 1 stranded animal was recorded as highly decomposed and difficult to examine postmortem and at least 34 stranding events were live strandings (others had no description). The descriptions of injuries were also extremely limited: 1 finless porpoise was recorded injured in a water gate and another was hurt in a fishing net. The records included a minimal description of how different agencies dealt with the stranded, bycaught and injured animals. Live animals were brought to rehabilitation facilities, after which 66.7% were released, 22.6% were kept in aquaria for educational display and 10.7% were kept in wildlife rescue centers. There were four ways of handling the carcasses: 70 were processed into skeletal specimens for display in universities, aquaria, museums and research institutes; 66 were buried in situ; 42 were used for research; and 10 were kept frozen. Very limited documentation or literature could be found on the types of injuries or causes of death.

4. Discussion 4.1. Spatial and temporal distribution patterns

Fig. 2. Seasonal distribution of strandings, bycatches and injuries of: A: all species; B: finless porpoises; and C: spotted seals, in the waters of mainland China (2000– 2006). Monthly samples for B and C were pooled into seasons due to small sample sizes.

winter and spring; more than 50% of bycatch records were in May (Fig. 2C), but the sample was small. Importantly, despite these observed patterns, without data on seasonal variation in survey effort no quantitative analysis and no firm conclusions can be made regarding the apparent seasonality of strandings, bycatches and injuries. For instance, in case observer effort may have been

Analyses of stranding data provide an overview of the species diversity and occurrence in a particular region. For example, species rarely occurring in the north-western region (NWR) of the USA are seldom found in records of the NWR Marine Mammal Stranding Network [39]. Comparing live survey data with stranding data in a region of northeastern Scotland indicated matching species composition [3]. In the present study, species diversity in the records of Fujian was notable: 10 out of the total 17 species that were found stranded nationally, 4 of 5 bycatch species and 5 of 11 injured species occurred in this province. This diversity probably reflects the species diversity in coastal waters of Fujian. Li [33] reports a total of 18 species of marine mammals sighted in Fujian water, which is approximately half of all species in Chinese waters. This high diversity might be related to the highly productive marine environment of the Taiwan Strait (1171100 –1251000 E, 221000 –271100 N). There are several areas of nutrient-rich upwelling in the Taiwan Strait, which help create five major fishing grounds for a total area of 213,237 km2 [7]. Our records from 2004 to 2006 included 5 species that have rarely or not before been recorded in China: the blue whale Balaenoptera musculus (Linnaeus, 1758), the pygmy sperm whale, the rough-toothed dolphin, the Blainville's beaked whale and the pygmy killer whale. Blue whales have not been seen in Chinese waters since 1938, and they rarely visited mainland Chinese coastal waters, even when they were flourishing [53]. Wang [56] reported earlier only four other records of pygmy sperm whale from the Hong Kong area, and two records of rough-toothed dolphin (1, Hong Kong; 1 Shanghai area). Till date, pygmy killer whale was only known from Taiwan [56]. The stranded Blainville's

Y. Wang et al. / Marine Policy 51 (2015) 242–250

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Fig. 3. A: Location of the main habitats for adult spotted seals in China: (1) Shuangtaizi Estuary; (2) Huping Island, Liaoning; (3) Miaodao Archipelago, Shandong Province, B: The layout of the national protected area in Dalian with combined distribution of strandings, bycatches and injuries of spotted seals in Hebei and Liaoning (2000–2006).

beaked whale was the first male of this species found in mainland China [58]. Thus, stranding data is valuable to supplement existing knowledge on large-scale distribution of marine mammals, especially for cryptic or rare species. The spatial and temporal distribution of stranded species is likely correlated with their parent population in the region [62], and thus provides information on population movement patterns [39]. The finless porpoise is one of the few permanent residents in Chinese waters and has a wide distribution [69]. Most cases of

bycatch and injuries were reported in Shandong, particularly in Yantai and Weihai, and were concentrated in April and May. This is the time when finless porpoises in the Yellow Sea perform seasonal migrations and aggregate in shallow coastal waters (Yantai to Weihai and Qingdao to Shidao) to obtain access to the spawning ground of their prey, mainly the fishes Sillago sihama (Forsskål, 1775), Lateolabrax japonicas (Cuvier, 1828), Pseudosciaena polyactis Bleeker, 1877 and Trichiurus haumela (Forsskål, 1775), in preparation for the reproductive season after May [8]. The fishing

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season in May also attracts a great number of fishing vessels, which increases the risk of small cetaceans being caught incidentally or injured. Predictable peaks revealed in bycatch and injury records, whether caused by increased species abundance or intensified fishing activities (or both), could help in the design of specific conservation measures (e.g. limiting the number of fishing vessels at times when vulnerable marine mammal species aggregate in the region). Spatial and temporal distribution of spotted seals as revealed in our records was also generally consistent with field survey data. The Bohai and Yellow Seas are the most southern habitats for spotted seals [55]. Stranding, bycatch and injury records of seals were recorded from January to June, while spotted seals appear in Bohai Bay from November to May [36]. There are three important resting and molting sites known for the adult seals: the Shuangtaizi Estuary, Huping Island in Liaoning and Miaodao Archipelago in Shandong (Fig. 3A), along with the surrounding sea area as their foraging habitat [35,36,57]. Our data not only emphasize the importance of Huping Island and Miaodao Archipelago, but also suggest a new important habitat, in Hebei (47.6% of all spotted seals recorded). However, the coastal waters of Hebei might be used intensively only by juveniles, because 11 out of 15 spotted seals recorded in Hebei (excluding Tianjin) were very young. Our study may suggest that young spotted seals, unlike adults, are dispersed in the entire Bohai Bay, searching for food. Evaluation of spatial and temporal patterns of stranding, bycatch and injury events in spotted seals also revealed problems in current marine protected areas. Huping Island is protected under the Dalian National Spotted Seal Nature Reserve. However, all 10 records of stranding and injury of seals occurred here, either in the core protected area (n¼8) or the buffer zone (n¼ 2) (Fig. 3B), suggest the need for better monitoring. Furthermore, potential habitats that are not currently protected (e.g. the coastal area of Hebei) might require more attention. In fact, at national and county levels, the effectiveness of protecting marine areas should be continually evaluated and modifications should be made when necessary. Stranding data could benefit conservation management in many ways, but it is used primarily for monitoring purposes, such as tracking long-term trends of living animals [4] or identifying unusual mortality events [39]. Systems that collect stranding data generally consider these inadequate to assess population health or accurately reflect the status of the entire population [1]. Although the proportions of species in stranding records may reflect the relative abundance of each species in the respective region [42,62], there are various factors affecting the stranding patterns: for example, currents that influence the location of landing, low buoyancy that makes the body sink before reaching the land [39] or high anthropogenic mortality [38]. For instance, 14 of 18 bottlenose dolphins were recorded in Fujian; however, this does not mean that they were primarily living in this region. Bottlenose dolphins have a wide distribution from Bohai Sea to the South China Sea and no study has indicated an especially large population in Fujian [64]. These figures are more likely to reflect the overlapping dolphin habitat and fishing ground, which is crowded with numerous fishing vessels from Fujian, Guangdong and Taiwan provinces [64]. Therefore, although stranding data provide some insights, surveys are needed to estimate abundances, detailed necropsies of fresh carcasses to gather natural history data, cranial and molecular evidence for population identification and, generally, improved field observer programmes before a realistic perspective on the status of aquatic mammals in Chinese waters can be obtained. 4.2. Setting up a reporting network with standardized recording The stranding, bycatch and injury cases of aquatic mammals provided in this review should be considered minimal and not

representative of true total numbers. This is especially true for bycatch, as fishermen rarely report bycatch events, even if mandatory. Take the Yangtze finless porpoise as an example. In 1991, the estimated population size in Yangtze River was 2700 individuals [66]. In 2001, the Symposium on Cetacean Conservation in China suggested that the population included fewer than 2000 individuals, based on surveys carried out in 1997, 1998 and 1999. Surveys in 2006 revealed a further decrease in population size, with an estimation of 1200–1400 individuals [52,68]. Comparing this steep decline with only 24 official records in this study clearly indicates additional mortality is occurring. The official records before 2000 are almost nonexistent, with only a few cases mentioned in publications. In recent years, media reporting of cetacean stranding events in China has increased, which might stimulate public interest and may then increase reporting efforts. Rescue networks for aquatic mammals are also emerging (e.g. the Guangdong Provincial Aquatic Wild Animal Rescue Network, which involves various government managed organizations, private companies and aquaria that provide rescue and rehabilitation for injured animals). However, an effective nationwide reporting system that would facilitate timely rescue and ensure collection of adequate information is still lacking. Such a network, crucial for population management, should be an accessible channel for people who witness stranding, bycatch and injury events. Previously, the main channel was the local fishery authority. Fisheries enforcement authorities in China have numerous duties, mostly concerning the inspection of fishing boats without licenses and illegal fishing methods, such as rolling hooks, electro-fishing and explosions [10,34,67]. Little effort can be spared for aquatic mammal conservation. On the other hand, the channel of reporting to fishery enforcement is likely to deter fishermen and impedes timely rescue. Our records show that many fishermen are willing to contact only academic institutions after stranding, bycatch and injury events. A nationwide reporting system would best be composed of trained volunteers based at academic institutions, fishery authorities and aquaria, supported by individuals who could provide professional advice, along all coastal areas of China and shores of the Yangtze River. Educational activities could also be organized to enhance public response capability and awareness to report events involving aquatic mammals. The second aim of setting up a nationwide reporting system is to maximize and improve data collection. Today, the majority of carcasses are buried on the spot or immediately turned into skeletal specimens; therefore, little chance for examination, necropsy or molecular genetic studies is available and the opportunities to identify threats and acquire biological data of affected species are missed. Stranding information recorded by provincial governments differed to a large degree. Some provinces (e.g. Fujian and Hebei) had relatively systematic recording year by year and provided information on type of event, species, date, location, body length and weight. The records of Yantai in Shandong even included information on who made the report and the cost of retrieval. Some provinces had only a very rough description or simply the total number of cases over several years (e.g. Zhejiang and Tianjin). One reason for the discrepancy in the quantity and quality of information collected is the wide variety of agencies that handle the cases. Different agencies hold different views about the importance of particular data. Fishery authorities usually have limited capability to record details, and often lack marine mammal expertise more likely available at universities. For instance, 18 bycaught finless porpoises from the coastal area of Weihai were sent to Shandong University at Weihai in May 2006, allowing biological observations of reproductive status, eye morphology, injuries and pathologies, in particular skin conditions. To achieve the aim of obtaining maximal information, the nationwide reporting system should pay attention to this kind of detailed anatomical information and also standardize methods for measuring and

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recording data, creating a rigorous dataset. A well-managed cooperative reporting system can collect all of the needed information from every event. Detailed biological examination is important in various respects. For example, descriptions and measurements of external and skeletal features are necessary for species identification and taxonomic considerations [39]. A Peruvian beaked whale Mesoplodon peruvianus Reyes, Mead & Van Waerebeek 1991, was reported stranded in Fujian [59], however a critical analysis of this paper by one of the authors (KVW) concluded that the skull did not belong to M. peruvianus and that its cranial morphologic affinity was close to M. ginkgodens Nishiwaki and Kamiya 1958. Analysis of stomach contents and teeth supplement knowledge of food habits and age; sampling of tissues for histopathology and the isolation of pathogens allow the correct diagnosis of infectious and other diseases [15]; while tissues can be used to carry out DNA and contamination analysis [48,29]. Body condition status (degree of decomposition) should be recorded, e.g. coded as live, fresh or edible carcass, early decomposition, advanced decomposition and mummified or skeletal remains [18]. The greater the decomposition, the less information can be obtained. Our current biggest concern is to evaluate the threats of fisheries on aquatic mammals, and careful written and photographic documentation of wounds, with diagnosis or post-mortem examination of the cause of death could provide useful insights [27]. Such information can help to determine whether stranding or death has resulted from entanglement, vessel collision, gunshots or other causes [20,18] Interactions between marine mammals and fisheries involved almost all existing fishing gears [17], and they are relatively simple to identify in freshly dead cetaceans because of their sensitive hairless skin [13]. Net marks or remains of netting still attached indicate an encounter with a gill or trawl net, or a discarded “ghost” net; a hook in the mouth or a caught flipper are likely attributable to long-line fishery; dorsal fins, flukes or flippers cut off and belly slits may be caused by fishermen attempting to facilitate the disentanglement process or sink the cetacean, less commonly propeller damage. Ship strikes may lead to multiple bone fractures, massive internal hemorrhaging, severed appendages or multiple incisive injuries from propellers [20,27,11,18,47]. However, although fishery encounters might cause injury and stranding, they are not always lethal. A nationwide monitoring and reporting system should use standardized methodologies and observer effort must be quantified as to allow comparative statistical analysis. More work should be done to identify the cause of death through the application of standard necropsy protocols [12]. Long-term accumulated data can reveal what type of gears pose the greatest entanglement risk [26], what species or populations are most susceptible to entanglement, which could provide a basis for mitigation measures such as gear modification or vessel control [31,26]. Effort-adjusted, standardized data would make comparisons possible between geographical locations and over time. Finally, information gathered should be published or otherwise made available to scientists for further investigations.

5. Conclusion The data obtained from national official documents clearly do not provide a comprehensive list of strandings, bycatches and injuries of aquatic mammals that occurred in the waters of mainland China from 2000 to 2006. It is suspected that they comprise only a minor fraction of true levels of mortality and other negative anthopogenic interactions, thus are inadequate to determine the status of marine mammal populations in Chinese waters. However, the data do provide some welcome preliminary insights, and

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indicate areas for future action and improvements. First, the efficiency of the existing recording and monitoring systems is problematic, resulting in a lack of useful information. The cause of strandings (live or dead) and injuries is rarely examined or recorded, limiting a proper understanding of the threats to aquatic mammal species in China and hampering good intentions to take appropriate management actions. A mechanism for reporting following a national standard recording protocol is desirable as to create a coordinated network for obtaining the maximum amount and quality of data. Second, bycatch and injuries most frequently occurred during peak fishing seasons and around highintensity fishing areas, which are thought to reflect the negative impact of anthropogenic activities, especially fisheries, on aquatic mammal populations in mainland Chinese waters. Third, the need to make improvements in protected marine areas is highlighted. The spatial planning of reserves should consider the changing patterns of habitat usage by the target species. In addition, better monitoring and the proactive prohibition of illegal fishing and direct takes of protected species, and within protected areas, are strongly recommended.

Acknowledgments The authors thank Phillip Hammond for his critical reading of an early version of the manuscript. Constructive comments by William McLellan and two other anonymous reviewers are also acknowledged.

References [1] Aguilar A, Borrell A, Pastor T. Biological factors affecting variability of persistent pollutant levels in cetaceans. J Cetacean Res Manag 1999;1:83–116 (Special issue). [2] Baird RW, Langelier KM, Stacey PJ. Stranded whale and dolphin program of B. C.(British Columbia)-1987 report. Wildlife Vet Rep 1988;1:9–12. [3] Baumgartner N, Goold JC, Reid RJ, Robinson KP. Patterns of cetacean strandings in NE Scotland (1992–2005): How do strandings data compare to live animal surveys? European Research on Cetaceans, 20 (2006) (on CD-ROM). [4] Berrow SD, Rogan E. Review of cetaceans stranded on the Irish coast, 1901– 2005. Mam Rev 1997;27:51–76. [5] Borsa P. Marine mammal strandings in the New Caledonia region, Southwest Pacific. Comp Rendus Biol 2006;329:277–88. [6] Cox TM, Read AJ, Barco S, et al. Documenting the bycatch of harbor porpoises, Phocoena phocoena, in coastal gillnet fisheries from stranded carcasses. Fish Bull 1998;96:727–34. [7] Dai T. Sustainable yield of fishery resources in the Taiwan Straits and its adjacent waters. Mar Fish Res 2005;26:1–8 ([in Chinese]). [8] Dong J, Wang G, Xiao Z. Migration and population difference of the finless porpoise in China. Mar Sci 1993;5:42–5 ([in Chinese]). [9] Drouot V, Gannier A, Goold JC. Diving and feeding behavior of sperm whales (Physeter macrocephalus) in the Northwestern Mediterranean Sea. Aq Mamm 2004;30:419–26. [10] Du B, Li H, Zhang X. Progress in the conservation research of Baiji. Zool Res 2003;24:395–400. [11] Du Fresne SP, Grant AR, Norden WS, Pierre JP. Factors affecting cetacean bycatch in a New Zealand trawl fishery. DOC Res Development Ser, 282, Wellington, New Zealand; 2007. [12] Duignan PJ. Diseases in New Zealand sea mammals. Surveillance 2000;27:9–15. [13] Duignan PJ. Disease investigations in stranded marine mammals, 1999–2002. . Wellington, New Zealand: Dept Conserv Sci Ser; 2003. [14] FAO. The state of world fisheries and aquaculture 2010. Rome, Italy: Food and Agricultural Organisation; 2010. [15] Foster G, Jahans K, Reid RJ, Ross HM. Isolation of Brucella species from cetaceans, seals and an otter. Vet Rec 1996;138:583–6. [16] Gao A, Zhou K. Geographical variation of external measurements and three subspecies of Neophocaena phocaenoides in Chinese waters. Acta Theriol Sin 1995;15:81–92. [17] Gilman E, Brothers N, McPherson G, Dalzell P. A review of cetacean interactions with longline gear. J Cet Res Manag 2006;8:215–23. [18] Geraci JR, Lounsbury Marine VJ. Mammals Ashore. A field guide for strandings. 1st edition. Galveston, TX: Texas A&M University Sea Grant College Program; 1993 (Publication TAMU-SG-93-601).

250

Y. Wang et al. / Marine Policy 51 (2015) 242–250

[19] Guenther TJ, Baird RW, Langelier KM et al. Cetacean strandings and entanglement in fishing gear on the Canadian West Coast during 1991. International Whaling Commission, Document SC/44/015; 1992. [20] Hare MP, Mead JG. Handbook for determination of adverse human–marine mammal interactions from necropsies. NWAFC Process Report 87–06. Washington, DC: Marine Mammal Program, National Museum of Natural History, Smithsonian Institution; 1987; 1–35. [21] Huang W. A rough-toothed dolphin, Steno bredanensis, from the East China Sea. Acta Zool Sin 1980;26:280–5 (in Chinese). [22] Jaramillo-Legoretta A, Rojas-Bracho L, Brownell Jr. RL, Read AJ, Reeves RR, Ralls K, Taylor BL. Saving the vaquita: immediate action, not more data. Cons Biol 2007;21:1653–5. [23] Jefferson TA, Wang JW. Revision of the taxonomy of finless porpoises (genus Neophocaena): the existence of two species. J Mar Animals Ecol 2011;4 (1):3–16. [24] Jepson PD, Bennett PM, Deaville R, Allchin CR, Baker JR, Law RJ. Relationships between polychlorinated biphenyls and health status in harbor porpoises (Phocoena phocoena) stranded in the United Kingdom. Environ Toxicol Chem 2005;24:238–48. [25] Jepson PD, Deaville R, Patterson IAP, Pocknell AM, Ross HM, Baker JR, Howie FE, Reid RJ, Colloff A, Cunningham AA. Acute and chronic gas bubble lesions in cetaceans stranded in the United Kingdom. Vet Path 2005;42:291–305. [26] Johnson A, Salvador G, Kenney J, Robbins J, Landry S, Clapham P. Fishing gear involved in entanglements of right and humpback whales. Mar Mamm Sci 2005;21:635–45. [27] Kemper CM, Flaherty A, Gibbs SE, Hill M, Long M, Byard RW. Cetacean captures, strandings and mortalities in South Australia 1881–2000, with special reference to human interactions. Austral Mamm 2005;27:37–47. [28] Klinowska M. Interpretation of the UK cetacean strandings records. Rep Int Whal Comm 1985;35:459–67. [29] Krahn MM, Ylitalo GM, Burrows DG, et al. Organochlorine contaminant concentrations and lipid profiles in eastern North Pacific gray whales (Eschrichtius robustus). J Cet Res Manag 2001;3:19–29. [30] Kuiken T, Simpson VR, Allchin CR, et al. Mass mortality of common dolphins (Delphinus delphis) in South West England due to incidental capture in fishing gear. Vet Record 1994;22:81–9. [31] Laist DW, Knowlton AR, Mead JG, Collet AS, Podesta M. Collisions between ships and whales. Mar Mamm Sci 2001;17:35–75. [32] Lewison RL, Crowder LB, Freeman SA. Understanding impacts of fisheries bycatch on marine megafauna. Trends Ecol Evol 2004;19:594–604. [33] Li S. Studies on sea mammals and its distribution from Fujian waters. J Oceanog Taiwan Strait 1997;16:479–85 ([in Chinese]). [34] Liu Y. The problem and strategies of existing marine fishery administration of China. Hebei Fish 2003;1:44–6 ([in Chinese]). [35] Lu S, Liu Z, Zhong X. Survey of spotted seal's population off the coast of Yantai city. Chin Fish Econ 2002;4:34–5 ([in Chinese]). [36] Ma Z, Han J, Jiang D, Zhang W. Population dynamics of spotted seals in the waters around Huping Island in Bohai Sea. Fish Sci 2007;26:455–8 ([in Chinese]). [37] Macleod CD, Pierce GJ, Santos MB. Geographic and temporal variations in the strandings of beaked whales (Ziphiidae) on the coasts of the UK and the Republic of Ireland from 1800 to 2002. J Cet Manag Res 2004;6:79–86. [38] Mead JG. An analysis of cetacean strandings along the eastern coast of the United States. In: Geraci Jr. St, Aubin SD, editors. Biology of Marine Mammals: Insights Through Strandings. Washington: The Marine Mammal Commission; 1979. p. 54–68. [39] Norman SA, Bowlby CE, Brancato MS, et al. Cetacean strandings in Oregon and Washington between 1930 and 2002. J Cet Res Manag 2004;6:87–99. [40] Read AJ, Drinker P, Northridge S. Bycatch of marine mammals in U.S. fisheries. Conserv Biol 2006;20:163–9. [41] Reeves RR, Smith BD, Crespo EA, Notarbartalo di Sciara G, editors. Dolphins, whales and porpoises: 2002–2010 conservation action plan for the world's cetaceans. Gland, Switzerland; Cambridge, UK: IUCN/SSC Cetacean Specialist Group; 2003. [42] Sergeant D. Ecological aspects of cetacean strandings. In: Geraci R, St. Aubin DJ, editors, Biology of marine mammals: insights through strandings. Report No. MMC- 77/13. Bethesda, MD: Marine Mammal Commision; 1979. p. 94–113.

[43] Shi Y, Wang X. The toothed whales in the offshore of Liaoning Province. Transact Liaoning Zool Soc 1983;4:83–7 ([in Chinese]). [44] Turvey ST, Pitman RL, Taylor BL, et al. First human-caused extinction of a cetacean species? Biol Lett 2007;3:537–40. [45] Van Bressem MF, Raga JA, Di Guardo G, et al. Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Dis Aquat Organ 2009;86:143–57. [46] Van Waerebeek K, Reyes JC. Post-ban small cetacean takes off Peru: a review. Rep Int Whal Comm 1994;15:503–20 ([Special Issue]). [47] Van Waerebeek K, Baker AN, Félix F, Gedamke J, et al. Vessel collisions with small cetaceans worldwide and with large whales in the Southern Hemisphere, an initial assessment. Lat Am J Aq Mamm 2007;6(1):43–69. [48] Varanasi U, Stein JE, Tilbury KL, et al. Chemical contaminants in gray whales (Eschrichtius robustus) stranded in Alaska. NOAA Technical Memorandum NMFS-NWF-SC-11. Washington and California, USA; 1993. [49] Wang D, Turvey ST, Zhao X, Mei Z. Neophocaena asiaeorientalis ssp. asiaeorientalis. IUCN Red List of Threatened Species. Version 2013.2. 〈www.iucnred list.org〉; 2013, [Downloaded 13.01.14]. [50] Wang JY, Chou LS, White BN. Osteological differences between two sympatric forms of bottlenose dolphins (genus Tursiops) in Chinese waters. J Zool 2000;252(2):147–62. [51] Wang JY, Frasier TR, Yang SC, White BN. Detecting recent speciation events: the case of the finless porpoise (genus Neophocaena). Heredity 2008;101:145–55. [52] Wang K. Poyang Lake- the last refuge of Yangtze River finless porpoise? China Nat 2007;3:21–3. [53] Wang P. Distribution of cetaceans off the coast of China. Chin J Zool 1984;6:52–6 ([in Chinese]). [54] Wang P. Fauna of marine mammals in China. Acta Oceanol Sin 1993;12:273–8. [55] Wang P. Status and conservation of spotted seals in Bohai Sea. Fish Sci 1993;12:4–7. [56] Wang P. Chinese cetaceans. Ocean Enterprises Ltd; 1999; 1–325 ([in Chinese]). [57] Wang P, Han J, Ma Z. Status survey of spotted seal (Phoca largha) in Bohai and Yellow Sea. J Wildlife 2008;29:29–31 ([in Chinese]). [58] Wang P, Tong S, Yuan H. Stranding of Blainville's beaked whale (Mesoplodon densirostris) along the coast of Huian. Fujian province, China. Fish Sci 2006;25 (10):524–7 (in Chinese). [59] Wang P, Yao CJ, Han J, Ma Z, Wang Z. Investigations of stranded and by-caught beaked whales around the coastal waters of Chinese mainland. Acta Theriol Sinica 2011;31(1):37–45. [60] Wiley DN, Asmutis RA, Pitchford TD, Gannon DP. Stranding and mortality of humpback whales, Megaptera novaeangliae, in the mid-Atlantic and southeast United States, 1985-1992. Fish Bull 1995;93:196–205. [61] Wood FG. The cetacean stranding phenomena: a hypothesis. In: Geraci JB, Aubin St DJ, editors. Biology of marine mammals: Insights through strandings. Marine Mammal Commission report no: MMC-77/13; 1979. p. 129–88. [62] Woodhouse CD. Marine mammal beachings as indicators of population events. Marine Mammal Strandings in the United States: Proceedings of the Second Marine Mammal Stranding Workshop 3–5 Dec 1987, Miami, FL. US Department of Commerce, NOAA Technical Report NMFS, 98; 1991, p. 111–15. [63] Würsig B. Cetaceans. Science 1989;244:1550–7. [64] Yang G, Zhou K, Xu X. Population density, distribution, and incidental catches of bottlenose dolphins in Xiamen-Dongshan waters of the Taiwan strait. Acta Ecolog Sin 2000;20:1002–7 ([in Chinese]). [65] Zerbini AN, Kotas JE. A note on cetacean bycatch in pelagic driftnetting off southern Brazil. Rep Int Whal Comm 1998;48:519–24. [66] Zhang X, Liu R, Zhao Q, et al. The population of finless porpoise in the middle and lower reaches of Yangtze River. Acta Theriol Sinica 1993;13:260–70. [67] Zhang X, Wang D, Liu R, et al. The Yangtze River dolphin or Baiji (Lipotes vexillifer): population status and conservation issues in the Yangtze River, China. Aq Conser: Mar Freshw Ecosyst 2003;13:51–64. [68] Zhao X, Barlow J, Taylor BL, et al. Abundance and conservation status of the Yangtze finless porpoise in the Yangtze River. China Biol Conser 2008;141:3006–18. [69] Zhou K, Leatherwood S, Jefferson TA. Records of small cetaceans in Chinese waters: a review. Asian Mar Biol 1995;12:119–39. [70] Zhu Q, Jiang B, Tang T. Strandings and its reasons in cetacea. Mar Sci 2000;24:7–9 ([in Chinese]).