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Molluscan aquaculture in general and bivalve farming in particular have brought significant social and economic benefits to coastal communities. Bivalve aquaculture accounts for 14%-16% of the average per capita animal protein of 1.5 billion people, supporting more than 200,000 livelihoods, mainly in developing countries (FAO 2018). Most bivalves produced in the world (89%) are from aquaculture (FAO 2016). To date, molluscan aquaculture has accounted for 21.42% (17.14 million tonnes) of total aquaculture production, with Asia being the largest contributor (92.27%) (FAO 2018).

One of the main challenges in bivalve aquaculture is the recurrence of mass mortalities, which reduce the production and cause high economic losses. Massive mortality of various cultured bivalves such as mussels (McFarland et al. 2016, Tan et al. 2016), clams (Ortega et al. 2016), cockles (Defeo et al. 2013), oysters (Vohmann et al. 2009), and scallops (Leverone et al. 2007) have been reported worldwide. Mortality may affect all life stages from larvae and spat in the hatchery, as well as juveniles and adults in grow-out farms (Tomaru et al. 2001, Nakamura 2005, Malham et al. 2012, Yurimoto et al. 2014). In fact, all natural bivalve populations have also suffered mass mortalities (Wootton et al. 2003), and although there is a large amount of anecdotal evidence supporting this, such events are not always published in the scientific literature.

In general, bivalve mass mortalities can be the result of extrinsic factors, including both physicochemical and biotic factors, such as big waves (Thorarindsottir et al. 2009), high silt load (Mouthon 2001), high fluctuation of water salinity (Levinton et al. 2011, Pollack et al. 2011, Munroe et al. 2013, Yurimoto et al. 2014), high fluctuation of water temperature (Brown et al. 2008, Rodrigues et al. 2015, Ortega et al. 2016), dissolved oxygen depletion (Ilarri et al. 2011, Harri et al. 2011), low food availability (Tan et al. 2016), predation (McKindsey et al. 2007), and toxic compounds (Ramli et al. 2013, Simoes et al. 2015). Intrinsic physiological factors may also play a role, including the effects of infectious pathogens and poor body condition (Marie-Agnes et al. 2015, Zannella et al. 2017). The intrinsic physiological factors on bivalve mass mortalities have been reviewed intensively by Paillard et al. (2004), Carballal et al. (2015), Marie-Agnes et al. (2015), Robledo et al. (2014), and Zannella et al. (2017). To date, no review has been published on the extrinsic factors on bivalve mass mortality.

It is clear from the literature that bivalve mortality is difficult to assign a cause to the deaths unequivocally (Callaway et al. 2013, Malham et al. 2012). Therefore, there is a need for scientific rigorous reviews on the possible factors that could lead to mass mortality of bivalve species. Such information will aid in establishing a good aquaculture development plan and fishery management plan to be implemented in both commercial fisheries and conservation. This review summarizes the potential extrinsic factors that contribute to episodic mass mortalities of marine bivalves. The currently available data on bivalve mass mortality cases associated with extrinsic factors were summarized in Table 1. For the sake of clarity, the term "mass mortalities" as used in this article refers to a sudden loss of more than 30% of the bivalve stock (Soletchnik et al. 2007).


Bivalve mass mortality episodes have been documented to be associated with environmental factors such as big waves (Thorarindsottir et al. 2009), high silt load (Mouthon 2001), low water salinity (Levinton et al. 2011, Pollack et al. 2011, Munroe et al. 2013, Yurimoto et al. 2014), high fluctuation of water temperature (Ford et al. 2006, Brown et al. 2008), and depletion of dissolved oxygen (Ilarri et al. 2011, Harriet al. 2011). Big waves generated by heavy storms have indirectly caused mass mortality of bivalves by dislodging and washing the bivalves to harsh environments. In Lonafjordur, northeastern Iceland, the mass mortality of the ocean quahog Arctica islandica in 2007 was associated with big waves during a heavy storm, by dislodging and washing the A. islandica to relatively shallow waters with hard bottoms unsuitable for the burrower. Under these circumstances, A. islandica eventually dies because of predation as it is exposed (Thorarindsottir et al. 2009). A similar mass mortality episode was reported in Caraguatatuba Bay, Southeast Brazil, where a high number of stranded trigonal clams Tivela mactroides (27-150 ind/[m.sup.2]) were recorded from September 2007 to December 2008 along the 4-km stretch of the bay by Turra et al. (2016).

High levels of inorganic suspended solids are one of the major stressors to bivalves that cause abrasion of the gills, physiological stress, and increase their susceptibility to diseases (Ellis et al. 2002, Zheng et al. 2009). In 1978, the mass mortality of the Pacific littleneck clam Protothaca staminea and the frilled venus clam Chione undatella in Mugu Lagoon, CA, was documented because of heavy sedimentation during an intense rainstorm (Peterson 1985). Moreover, the Asian clam Corbicula fluminea population also experienced rapid die-offs triggered by high silt loads during spring floods and low dissolved oxygen levels associated with decreased water flow in France (Strayer 1999, Mouthon 2001). The mass mortality episodes of bivalves associated with high levels of suspended particles is believed to be due to physical difficulties affecting respiration and filtration rates, ultimately leading to a series of negative physiological effects (Armstrong & Seddon 2008). Laboratory experimental studies have shown that long-term (24 days) exposure of high levels of inorganic suspended solids (>1,000 mg/L) resulting in clogged feeding structures of Sinonovacula constricta, reducing feeding efficiency, increasing suspended solid stress, and ultimately leading to death (Szostek et al. 2013, Yang et al. 2017). Bivalve juveniles are more susceptible to high levels of inorganic suspended particles. A moderate concentration of 270 mg/L of inorganic suspended particles resulted in a mortality rate of 30% for juvenile Crassostrea rivularis (2.33 [+ or -] 0.78 cm), whereas higher levels (810 mg/L) of suspended particles resulted in a mortality rate of 60% (Ye et al. 2010).

Salinity has major effects on the osmotic physiology of bivalves. Prolonged exposure to low salinity often leads to mass mortality in marine bivalves. In south Texas and Louisiana, because of freshets (Levinton et al. 2011, Pollack et al. 2011) and opening of flood control spillways (LDWF 2011), prolonged exposure to low salinity was reported to induce Crassostrea virginica mass mortality. Moreover, it was reported that during a flooding incident, the salinity of Saint Lucia fell from 45 to less than 10, resulting in a mass mortality of Solen cylindraceus (Cyrus et al. 2010). A similar mass mortality episode occurred in Selangor, Malaysia. The decline in water salinity caused by heavy precipitation led to more than 30% mortality of the blood cockles Anadara granosa population in early 2012 (Yurimoto et al. 2014). Furthermore, Hurricane Irene and Tropical Storm Lee generated extreme flooding in the Delaware River watershed, resulting in prolonged bay-wide low salinity and consequent historically high mortalities for the oyster C. virginica stock in upper reaches of Delaware Bay in 2011 (Munroe et al. 2013).

Harsh winters can lead to extinction or almost total mortality in a bivalve population. In the winter of 1954, the sediments of the Wadden Sea were frozen to a depth of 10-15 cm, resulting in almost total mortality of the common cockle Cerastoderma edule (Kristensen 1958). In the harsh winter of 1962/63, total mortality of the common cockle Cardium edule was documented in Llanrhidian Sands (Burry Inlet, South Wales), as well as mass mortalities in other parts of the United Kingdom, including Morecambe Bay, Shoeburyness, and Whitstable (Hancock & Urquhart 1964). During the same harsh winter period, Crisp (1964) reported a mass mortality of the native oyster Ostrea edulis in southern England, whereas Perkins and Williams (1964) observed a mass mortality of C. edule populations in the Solway Firth, caused directly by ice formation on the upper shore. In the subtropical region, since 1998, the noble scallop Chlamys nobilis cultured in the southern coast of China often suffered from mass mortality in winter (Huang 2000, Zhou et al. 2006, Lan et al. 2018).

Warm temperatures can also cause mass mortality of bivalve species in synergy with low dissolved oxygen (Mohamed 2003, Ilarri et al. 2011). The presence of high organic matter and warm water led to a mass mortality of juvenile Cerastoderma edule in Arcachon Bay and Galicia (Gonzalez & Perez Camacho 1984). Similar mass mortality episodes have been observed on thousands of kilometers of sandy beaches in Uruguay and Argentina since the early 1990s, when the mass mortality of the yellow clam Mesodesma mactroides populations was associated with the warm seasons (Fiori & Cazzaniga 1999, Defeo et al. 2013). Moreover, a long-term study (22 y; from 1985 to 2007) showed that the warming of the sea surface water due to climate change resulted in decreasing abundance and individual size, and caused shell abnormalities in the yellow clam M. mactroides along the sandy beaches in Uruguay (Ortega et al. 2016). At high stocking densities, warm water has a greater impact on bivalve mortality. The mortality rate of the Zhikong scallop Chlamys farreri has been reported to reach 85%-90% in the high stocking density culture areas in northern China when the temperature reached 23-26[degrees]C in the year 2000 (Xiao et al. 2005). In fact, some bivalve species are highly sensitive to temperature rise, and experimental studies have shown that an increase in water temperature of 3[degrees]C in summer resulted in 100% mortality of adult mussels Mytilus galloprovincialis (Gazeau et al. 2014).

Most bivalves are relatively intolerant of low dissolved oxygen. The mass mortalities of Crassostrea gigas in Puget Sound, WA, and Tornalas Bay, CA, in the late 1990s were associated with low dissolved oxygen in summer (Cheney et al. 2000). Moreover, the unusually low river flow to the Minho Estuary, Spain, caused oxygen depletion and high temperatures, resulting in massive mortality of Corbicula fluminea in 2009 (Ilarri et al. 2011). This species is relatively sensitive to hypoxia (Matthews & McMahon 1999); therefore, low dissolved oxygen levels often associated with massive die-offs (Mouthon & Daufesne 2006, Werner & Rothhauot 2008, Vohmann et al. 2009). In addition, mass mortalities of pearl oysters occurred in most parts of Indonesia from 1992 to 1994, ranging from 30% to 85% (depending on the farm and its location). It was due to erratic weather patterns that influenced the flow of air and water currents and caused relatively high temperature and low dissolved oxygen (Anonymous 1994). Furthermore, the low dissolved oxygen levels created by eutrophication are also an important factor in triggering bivalve mass mortality (Tan & Ransangan 2015a). Collapse of the Cerastoderma edule population in the Bay of Somme (north France) during the period 1982 to 1985 was attributed to eutrophication and the induction of anoxia (Desprez et al. 1992, Rybarczyk et al. 1996). A similar mass mortality episode was reported in Kozhikode coast, India, where the low dissolved oxygen level of 0.96-1.67 ml/L created by a bloom of the phytoplankton Noctiluca sp. in 2002 was associated with a mass mortality of the green mussel Perna viridis (Mohamed 2003).


Food availability is considered to be the prime limiting factor for bivalve recruitment in shallow well-mixed estuarine systems (Herman et al. 1999, Beukema et al. 2002). The newly hatched planktotrophic bivalve larvae have very few nutrient reserves; therefore, the availability of food in the first few days after hatching is critical for their survival (Pawlik 1992). Experimental efforts showed extremely low survival rates (<20%) of Patinopecten yessoensis larvae with the prolonged starvation period of 72 h (Cai et al. 2014). The prolonged starvation caused permanent damage to larval feeding ability, such as the ability of larval cilia to collect and ingest food particles, and further inhibited the energy generation for continuing development, which was likely responsible for the mortality (Zheng et al. 2005, Cai et al. 2014. In addition, the food availability also determines the time and size of larval metamorphoses. For instance, excess food usually leads to early metamorphosis and larger size being attained, whereas metamorphosis is usually delayed when food is scare (Morey & Reznick 2000). The delay of metamorphosis is another challenge that will further reduce the survival of bivalves (Tan & Ransangan 2014). Even very short delays (few hours) can sometimes lead to a serious decline in fitness of juveniles and adults, in particular decreased survival and reduced postmetamorphic growth rates or development (Pechenik 2006).

For juvenile and adult bivalves, early studies have shown that low phytoplankton abundance only has a negative impact on growth and is unlikely to cause mortality (Kamermans 1993, Tomaru et al. 2001). For example, low phytoplankton concentrations with low current velocities in the Wadden Sea only resulted in a negative effect on the growth of Cerastoderma edule, but with no link to mass mortality (Kamermans 1993). Some other studies have shown that food depletion indirectly leads to massive die-off of bivalves by weakening the bivalve and increases the susceptibility of bivalves to diseases. For instance, mass mortality of the pearl oyster Pinctada martensii in western Japan in 1998 was thought to be due to food depletion followed by disease infection (Tomaru et al. 2001). Recent studies have highlighted a clear relationship between food depletion and mass mortality of bivalves (Watermann et al. 2008, Vohmann et al. 2009). For instance, the mass mortality of Corbiculafluminea in the River Rhine in 2003 was mainly due to the low food abundance (Vohmann et al. 2009). Given the high metabolic rates and food demands of C. fluminea, this species does not compensate for the increased metabolic costs in nutrient poor habitats, thus leading to mass mortality (McMahon 2002, Weitere et al. 2009). Similar events have been documented on the east Frisian coast of Germany, where the mass mortalities of Crassostrea gigas in 2005 were associated with limited water exchange and low food availability (Watermann et al. 2008). In addition, the mass mortality (>50%) of juvenile quahogs (hard clams) Mercenaria occurred frequently (2001, 2002, and 2004) in the Mid-Atlantic region when phytoplankton abundance was low (Chl-a less than 3 [micro]g/L) (Zarnoch & Schreibman 2008).

Other than food abundance, several studies have shown that the survival and growth performance of bivalves are also influenced by food composition (Ren et al. 2000, Rouillon & Navarro 2003, Tan & Ransangan 2016a). Different bivalve species have different phytoplankton group preferences. For example, Ensis directus, Placopecten magellanicus, Arctica islandica (Shumway et al. 1985), Crassostrea gigas, and Mytilus galloprovincialis (Sidari et al. 1998) have shown preferential intake of dinoflagellates rather than diatoms. Oysters Crassostrea virginica have been shown to have difficulty digesting diatoms, particularly Platymonas suecica, because the rigid cell walls of the diatoms are resistant to enzymatic digestion and physical breakdown (Romberger & Epifanio 1981, Tan & Ransangan 2014). By contrast, other studies have shown that Chlamys farreri (Xu & Yang 2007), Mytilus edulis (Rouillon & Navarro 2003), and Perna viridis (Sivalingam 1977) prefer diatoms, mainly excluding dinoflagellates from their diet. A mass mortality episode of P. viridis was reported in Marudu Bay, Malaysia, in 2010 (Tan & Ransangan 2015b, 2016a, 2016b). Feeding preferences and plankton ecology studies have revealed that the high composition of less favorable foods (>90% Chaetoceros and Bacteriastrum) suggests that although the total phytoplankton abundance was not depleted, the lack of a suitable food source could be the causative factor of mortality (Tan & Ransangan 2016a).


Predation has been associated with some mass mortality episodes of bivalves (Moller & Rosenberg 1983, Beukema et al. 1998, Masski & Guillou 1999). Juvenile bivalves, particularly newly recruited bivalves, are often subjected to predation by crustaceans (Masski & Guillou 1999, Hiddink et al. 2002). Moller and Rosenberg (1983) reported that predation by the brown shrimp Crangon crangon on juvenile cockles in Sweden reduced the annual production of Cerastoderma edule by 68%. The effect of predation is greater when the recruitment of new C. edule is low, or the growth rate is relatively low, and it takes longer to reach the critical size for being captured. In the Wadden Sea, the main predator of newly recruited Macoma balthica is the O-group shrimp C. crangon (Beukema et al. 1998). These shrimp selectively prey on small (<3 mm) bivalve spat (Hiddink et al. 2002).

Other crustaceans, particularly the green crab Carcinus maenas, are also considered to be the major predators of small bivalves. In the Bay of Morlaix, France, juvenile cockles Cerastoderma edule with a shell length of less than 11 mm have been shown to be the target of juvenile green crabs, accounting for 85% of their total mortality (Masski & Guillou 1999). The green crab is a voracious predator and has a preference for bivalves, particularly the soft-shell clam Mya arenaria (<17 mm) (Miron et al. 2005) and the eastern oyster Crassostrea virginica, where it alone can remove up to 80% of small clams in unprotected areas (Floyd & Williams 2004).

For adult bivalves, seabirds are the main predator, of which no less than 70% of food consumption (by weight) in the Wadden Sea carnivorous seabirds (Somateria mollissima, Haematopus ostralegus, and Calidris canutus) is bivalves (Scheiffarth & Nehls 1997). Predation by birds, particularly oyster catchers, is one of the factors resulting in the mass mortalities of the cockle Cerastoderma edule in northwestern Europe (Ducrotoy et al. 1991) and Wadden Sea (Jensen 1992, Beukema 1993). Moreover, mass mortality episodes of Corbicula fluminea due to predation by oyster catchers were observed during low water levels in the summer of 2003 and at the end of March 2004 along the Nederrijn near Wageningen (Cadee & Soes 2004). In addition, bivalve species introduced in an environment can act as invading prey, enhancing mortality on native bivalves by increasing predator abundance. The introduction of Arcuatula in San Diego Bay, CA, led to an indirect increase in the predation of native species (Chione undatella and Laevicardium substriatum), especially for poorly defended species (Castorani & Hovel 2015).

In addition, it has been reported that bivalves grazing on their own larvae have significantly reduced the settlement of Cerastoderma edule larvae up to 33%-40% (Andre et al. 1993, Malham et al. 2012). Bivalves grazing on their own planktonic larvae at different stages have been reported in Crassostrea gigas, C. edule (Troost et al. 2009), and Mytilus edulis (Lehane & Devenport 2006), in which larviphagy activity reduced the settled larvae by not less than 33% (Andre et al. 1993). Larviphagy behavior was also reported in the green mussel Perna viridis (Tan & Ransangan 2016a), M. edulis (Lehane & Devenport 2004), the Pacific oyster C. gigas, and C. edule (Troost et al. 2009). The bivalve veliger is known to drift around the potential settling grounds to increase the chances of encountering suitable substrata (Andre et al. 1993). This could also result in a high susceptibility for larvae to predation by adult suspension feeders (Andre et al. 1993). Different stages of veligers (100-300 [micro]m) have been observed in the stomach contents of adult P. viridis (Tan & Ransangan 2016a) and M. edulis (Lehane & Devenport 2004), revealing the possibility of bivalve grazing on bivalve larvae of different developmental stages.



Harmful algal blooms (HAB) that produce biotoxins are a global phenomenon and a threat to bivalves (Shumway 1990, Hallegraeff 2003, Basti et al. 2018). This has led to a growing concern on the effects of HAB on shellfish resources, both in terms of seafood safety and production efficiency. HAB caused by Prorocentrum minimum (Sellner et al. 1995), Heterocapsa circularisquama (Matsuyama et al. 1996), Aureococcus anophagefferens (Bricelj & MacQuarrie 2007), Karenia brevis (McFarland et al. 2016), and Dinophysis sp. (Simoes et al. 2015) have been associated with mass mortality of bivalves. Leibovitz et al. (1984) recorded a preliminary report in the scientific literature on bivalve mass mortality episodes associated with the bloom of P. minimum. A massive die-off of the scallop Argopecten irradians during P. minimum blooms was hypothesized to be due to physical damage from the apical tooth, a sharp anterior spine on some Prorocentrum taxa (Leibovitz et al. 1984). This hypothesis has not been confirmed, and no follow-up studies were carried out on scallops during a natural bloom of P. minimum until the P. minimum blooms in Chesapeake Bay resulted in mass mortality of wild eastern oyster Crassostrea virginica populations (Sellner et al. 1995). Laboratory observations have confirmed that P. minimum caused poor larval development and can kill juvenile oysters by altering the immune system competence; hence, disease resistance is compromised (Hegaret & Wikfors 2005).

The first record of bivalve mass mortality associated with the dinoflagellate Heterocapsa circularisquama was recorded in Uranouchi Bay in 1988, which caused mass mortality of the pearl oyster Pinctada fucata martensii, Pacific oyster Crassostrea gigas, Manila clam Ruditapes philippinarum, and blue mussel Mytilus galloprovincialis around the western part of Japan (Yamamoto & Tanaka 1990, Matsuyama 1999). Since then, H. circularisquama has frequently caused mass mortalities of more than 12 natural and cultured bivalve species in embayments of western Japan (Yamamoto & Tanaka 1990, Matsuyama et al. 1996). The toxin produced by the dinoflagellate H. circularisquama is very specific and only harmful to bivalves, but harmless to other animals (Basti et al. 2009). It has been shown to induce several deleterious effects in juvenile and adult bivalves, ranging from behavioral alteration (Basti & Segawa 2010) to impairments of the basic physiological functions of feeding and respiration (Matsuyama 1999). Before death, clams exhibit an extreme retraction of their mantle edge and siphon, as well as recurrent "vomiting" behavior before initiating a closure reaction, followed by paralysis and death (Basti & Segawa 2010). The Manila clam R. philippinarum exposed to H. circularisquama exhibited morphological changes, accompanied by accumulation of mucus-like substances in the gills, a profound reduction in filtration activity, and lysosomal destabilization in hemocytes (Kim et al. 2011).

The first occurrence of bivalve mass mortality episode associated with Aureococcus anophagefferens was in 1985. The brown tide (0.9-1.5 x [10.sup.6] cells/mL) incident caused reproductive failure and mass mortalities (30%-100%) to natural and transplanted Mytilus edulis mussels in Narragansett Bay (Tracey 1988). At the same time, the bay scallop Argopecten irradians fishery in New York state collapsed because of two blooms of A. anophagefferens in the summers of 1985 and 1986 (Bricelj & Kuenstner 1989). The peak concentration of the brown tide ([10.sup.9] cells/L) coincided with the A. irradians spawning season, resulting in recruitment failure (Bricelj et al. 1987). Laboratory studies have shown that the brown tide of A. anophagefferens consistently inhibits the growth of veligers in a dose-dependent manner, leading to arrested development in the early veliger D-stage. Growth rates of -7 mm juveniles were completely suppressed at 400 cells/[micro]L or less of this isolate in both unialgal and mixed assemblages (Bricelj et al. 2004). Feeding reduction was noted in adult bivalves via inhibition of gill lateral cilia responsible for the generation of feeding currents (Gainey & Shumway 1991). Moreover, 80% of the juvenile Mercenaria (1 mm), which survived 2 wk of exposure to a severe A. anophagefferens bloom (800 cells/[micro]L) were completely unable to resume normal growth rates (Bricelj & MacQuarrie 2007). In addition, exposure of greater than 200 cells/[micro]L of A. anophagefferens was sufficient to cause permanent metamorphic failure of hard clam larvae. These lead to vulnerability to secondary fatality factors, particularly predation and environmental stress factors (bivalve larvae have low toleration range of environmental parameters) (Bricelj & MacQuarrie 2007).

Information on the effects of the brevetoxin producer Karenia brevis on bivalves is very limited, although it is wellknown for causing mass fish kills. In 1987, K. brevis bloomed on one of the most productive beds of the bay scallop Argopecten irradians in North Carolina, resulting in a 21% mortality rate and almost total recruitment failure (98%) of the scallop population (Summerson & Peterson 1990). Laboratory observations showed that K. brevis had a cell density higher than 500 cells/mL to inhibit the metamorphosis and caused mortality to bay scallop A. irradians larvae (Leverone & Blake 2002). Moreover, nearly total mortality (>90%) of cage-cultivated Perna viridis mussels was observed in the southeastern United States in early 2012 following the K. brevis blooms (>[10.sup.5] cells/L) (McFarland et al. 2016). Laboratory observations also showed that A. irradians and Crassostrea virginica exhibit a 79% and 38% reduction in clearance rate at 1,000 cells/mL of K. brevis culture compared with the control (Leverone et al. 2007).

Chemical Toxic Compounds

Toxic chemical compounds, including pulverized fuel ash (PFA), ammonia, and oil spills, are also associated with mass mortality of bivalves. PFA, more commonly known as fly-ash, is a by-product of burning of pulverized coal in the coal-fired electricity power stations. Pulverized fuel ash contains significant quantities of various heavy metals, the concentration of which can vary considerably depending on the origin of the coal and the type of combustion process (Bowmer et al. 1994). Intermittent exposure to PFA resulted in mass mortalities of Cerastoderma edule (Jenner & Bowmer 1990). Moreover, the results of an experimental study showed a 43% mortality rate of the cockle C. edule when exposed to 100% PFA sediment for 3 mo (Bowmer et al. 1994).

Total ammonia in the aquatic environment comprises two principal forms: the ionized ammonium ion ([N[H.sub.4].sup.+]) and unionized ammonia (N[H.sub.3]). The unionized form of ammonia is much more toxic than the ionized ammonium ion. Laboratory studies have shown that the 96-h lethal concentration to Perna viridis, which caused 50% mortality, is much lower for ammonia (7.6 mg/L) than ammonium (13 mg/L) (Reddy & Menon 1979). In fact, some bivalve species are more sensitive to ammonia, with 0.11 and 0.8 mg/L of ammonia sufficient to cause 50% mortality of the unionid mussel Villosa iris and the Asian clam Corbicula fluminea, respectively, in 96 h (Cherry et al. 2005). For ammonium, exposure of the adult cockle Anadara antiquata to 64.3 mg/L ammonium for 96 h resulted in a 33% mortality rate. Stress manifestations include excessive shell gaping, foot protrusion, mucus secretion coupled with necrosis, hyperplasia, cilial shortening, lamellar shrinkage, abscess formation and eventual epithelial ruptures, and proliferations in the gills and gut. These postexposure injuries promoted mortality of A. antiquata to 61.6% within 14 days (Matojo & Pratap 2009). A massive Anadara granosa die-off in the Sungai Buloh River, Malaysia, in the year 2011 was associated with a high ammonia concentration of 4 mg/L (Ramli et al. 2013).

Oil spills can have long-term effects on ecosystems. The greatest impact of spilled oil is likely to be found near-shore, where animals and plants can be physically coated and smothered by oil or exposed to toxic components over extended periods of time. For this reason, sedentary species, particularly bivalves, are sensitive to oil toxicity. On 24th March 1989, the oil tanker Exxon Valdez grounded on Blight Reef in northern Prince William Sound in Alaska and caused one of the largest marine oil spills ever recorded. More than 42 million liters of crude oil was released into the Blight Reef in northern Prince William Sound (Galt & Payton 1990). The immediate toxicity effect of oil spill resulted in 40% mortality of the blue mussel Mytilus trossulus (Andres et al. 1993). It has been estimated that 40%-60% of bivalves would either be killed or would be sublethally affected by the residual oil (Peterson et al. 2003). In addition, mass mortalities of Cerastoderma edule and Ensis siliqua (razor-shell) were observed after a major oil spill, following the grounding of the Sea Empress in 1996 off the southwest coast of Wales (SEEEC 1998). Interestingly, Mytilus edulis underwent significant immunosuppression but did not show oil-induced mortality. In April 2010, the explosion of the Deepwater Horizon offshore oil platform exploited by British Petroleum in the Gulf of Mexico spilled about 779,000 tonnes of crude oil. The oil spill from the Deepwater Horizon reached the Louisiana coastline and entered Barataria Bay, a productive oyster-growing estuary, and caused 77% mortality (La Peyre et al. 2014).

In the bivalve aquaculture industry, bivalve mass mortalities have increased worldwide since the 1960s. This increase can be explained as a result of research progress on identification of mass mortalities and the intensification of bivalve aquaculture, or may reflect changes in environmental conditions in production areas caused by water pollution. Moreover, most of the mass mortality reports reviewed herein is from monitored and commercially exploited shellfishery beds, whereas the mortality rate of noncommercial stocks is often under-reported. Based on published literatures, several general groups of factors have been identified as the causative factors of bivalve mass mortality, but most bivalve mass mortality episodes are triggered by the synergistic effects of two or more factors (Malham et al. 2012, Callaway et al. 2013, Tan & Zheng 2019). Repeated episodes of bivalve mass mortality are typically induced by increasing the water temperature with low dissolved oxygen in the presence of high organic matter. Warmer water temperature promotes excessive microbial growth in the presence of high organic matter (Joint & Smale 2017). Low dissolved oxygen is primarily due to the decomposition of organic matter that consumes dissolved oxygen (Degerman et al. 2013). It has been reported that the synergistic effect of high water temperature and low dissolved oxygen can trigger mass mortality of Cerastoderma edule, Mesodesma mactroides, Crassostrea gigas, and Corbicula fluminea in Arcachon Bay and Galicia (Gonzalez & PerezCamacho 1984), Argentina (Defeo et al. 2013), California (Cheney et al. 2000), and Spain (Ilarri et al. 2011), respectively. The effects of elevated temperature on survival and energy metabolism are species specific, with some bivalve species such as Crassostrea virginica (Ivanina et al. 2013) and Mytilus galloprovincialis (Gazeau et al. 2014) being highly sensitive to temperature increases. Experimental studies showed 65% mortality in C. virginica after a 15-wk exposure at 27[degrees]C (Ivanina et al. 2013). Another experimental study showed that the mortality rate of the adult mussel M. galloprovincialis was 100% when water temperature increased by 3[degrees]C in summer (Gazeau et al. 2014). Elevated temperature can have a negative impact on the bioenergetics of bivalves, leading to energy deficiency that can have an impact on their growth, reproduction, and immune systems, which could lead to mortality (Ivanina et al. 2013). Moreover, predation of bivalves by crustaceans has been reported to be influenced by environmental factors. Predation of the oyster C. virginica by the blue crab Callinectes sapidus, stone crab Menippe adina, and black drum Pogonias cromis was observed during periods of higher salinity (less than 10) in Breton Sound, LA (La Peyre et al. 2013). In addition, physical disturbance such as heavy storms (wind greater than 20 m/s) in Lonafjordur resulted in large quantities of Arctica islandica being swept from their natural sandy habitat to shallower water, which exposed them to predators (Thorarindsottir et al. 2009).


In conclusion, clear identification of the main causative factors of mass mortality events in bivalves is extremely difficult because it involves complex interactions between bivalve physiological condition and environmental factors; thus, the cause of death can rarely be explained by a single factor. Most extrinsic factors indirectly contribute to mass mortalities by weakening individual bivalves, making them more susceptible to predation and disease infection. It is anticipated that the physical and chemical properties of the marine environment will continue to change and there may be more extrinsic factors impacting mortality in bivalves. Hence, more studies are needed to understand the relative influence of each factor and the synergistic effects of the integrated factors on the overall physiological state, health, and resilience of bivalves.


This work was financially supported by the Fundamental Research Grant Scheme (FRGS0467-2017) from the Ministry of Education, Malaysia, and the Postdoctoral Grant Scheme (PRF0007-2017) from the Universiti Malaysia Sabah.


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(1) Key Laboratory of Marine Biotechnology of Guangdong Province, Shantou University, 243 Daxue Road, Shantou 515063, Guangdong, China; (2) Borneo Marine Research Institute, Universiti Malaysia Sabah, Jalan UMS, 88400 Kota Kinabalu, Malaysia

(*) Corresponding author. E-mail:

DOI: 10.2983/035.038.0202
Extrinsic factors associated with bivalve mass mortalities.

Environmental variable  Affected species         Outbreak location

Big waves               Arctica islandica      Lonafjordur northeastern
                        Tivela mactroides      Caraguatatuba Bay,
                                                 southeast Brazil
High silt load          Protothaca staminea    Mugu Lagoon, CA
                        Chione undatella       Mugu Lagoon, CA
                        Corbicula fluminea     France
Low water salinity      Crassostrea rivularis  South Texas and
                        Solen cylindraceus     Saint Lucia
                        Anadara granosa        Selangor, Malaysia
                        Crassostrea virginica  Delaware Bay
Low water temperature   Cerastoderma edule     Wadden Sea
                        Cardium edule          Llanrhidian Sands
                        Ostrea edulis          Southern England
                        C. edule               Solway Firth
                        Chlamys nobilis        Southern coast of China
Warm water temperature  C. edule               Arcachon Bay and Galicia
                        Mesodesma mactroides   Uruguay and Argentina
Depletion of dissolved  Crassostrea gigas      Puget Sound, WA, and
  oxygen                                         Tornalas Bay, CA
                        C. fluminea            Minho estuary, Spain
                        Pinctada maxima        Indonesia
                        C. edule               Bay of Somme
                                                 (north France)
                        Perna viridis          Kozhikode coast, India

Environmental variable      Year                References

Big waves               2007          Thorarindsottir et al. (2009)
                        2007 to 2008  Turra et al. (2016)
High silt load          1978          Peterson (1985)
                        1978          Peterson (1985)
                        1996 to 1999  Strayer (1999) and Mouthon (2001)
Low water salinity      2008 and 2010 Levinton et al. (2011) and
                                        Pollack et al. (2011)
                        2002 to 2008  Cyrus et al. (2010)
                        2012          Yurimoto et al. (2014)
                        2011          Munroe et al. (2013)
Low water temperature   1954          Kristensen (1958)
                        1962/63       Hancock and Urquhart (1964)
                        1962/63       Waugh (1964)
                        1962/63       Perkins and Williams (1964)
                        1998          Huang (2000)
Warm water temperature  Early 1980s   Gonzalez and Perez Camacho (1984)
                        1990s         Fiori and Cazzaniga (1999) and
                                        Defeo et al. (2013)
Depletion of dissolved  Late 1990s    Cheney et al. (2000)
                        2009          Ilarri et al. (2011)
                        1992 to 1994  Anonymous (1994)
                        1982 to 1985  Desprez et al. (1992) and
                                        Rybarczyk et al. (1996)
                        2002          Mohamed (2003)
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Author:Soon, Tan Kar; Ransangan, Julian
Publication:Journal of Shellfish Research
Geographic Code:90ASI
Date:Aug 1, 2019

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