In: Oysters ISBN 978-1-62100-518-6

Editor: Jian G. Qin, pp. 181-202 © 2012 Nova Science Publishers, Inc.

Chapter 7

EXPLORING CORRELATIONS BETWEEN

SPAWNING MEDIATED RESPONSE

AND SUMMER MORTALITY IN PACIFIC

OYSTER CRASSOSTREA GIGAS

Yan Li1, Kirsten Benkendorff

2, Jian G. Qin3,

and Xiaoxu Li4

1School of Agriculture and Food Sciences, The University of Queensland,

Brisbane, Queensland 4072, Australia 2School of Environmental Sciences and Management, Southern Cross

University, Lismore, NSW 2480 Australia 3School of Biological Sciences, Flinders University,

Adelaide, SA, Australia 4South Australian Research and Development Institute (SARDI),

Henley Beach, SA, Australia

ABSTRACT

Pacific oyster, Crassostrea gigas, is one of the most important

species for aquaculture and ecological indicators for environmental

changes. However, mass summer mortality has become a widespread

challenge to Pacific oyster aquaculture industry in recent decades. Due to

Corresponding author Email: kirsten.benkendorff@scu.edu.au.

Yan Li, Kirsten Benkendorff, Jian G. Qin et al. 182

the energy cost for gametogenesis, the reproductive season is considered

a period of high risk for mortality events. This chapter reviews both

immunity and energy metabolism in Pacific oysters, providing an

appropriate approach to evaluate the integrative health condition in

oysters, with a focus on the spawning-dependent stress response via

comparison between pre- and post-spawning oysters under environmental

stress. This review endeavor reflects the likely consequences of oyster

spawning under food deprivation, heat shock and bacterial challenge and

contributes to our understanding of the underlying mechanisms for oyster

summer mortality. As oysters have already been used as important

bioindicators in the environment and are representatives for intertidal

populations, the implications of spawning impacts on resilience to

environmental stress may be applicable to other compatible species in

similar geographic distributions. By drawing on the broader literature

from other commercial species, particularly clams, mussels, cockles and

abalone, we synthesized the current evidence for spawning related

immuosuppression contributing to epidemic disease and mortality in

molluscs. This review provides insights into the understanding of global

warming effects on ocean productivity in a world-wide aquaculture

species whose reproduction is triggered by temperature increases.

Keywords: oyster spawning, immunosuppression, energy depletion, summer

mortality, global warming

INTRODUCTION

Pacific oyster Crassostrea gigas has a competitive advantage and

dominates other molluscan species in global distribution and aquaculture

production (Food and Agriculture Organisation [FAO] of the United Nations,

2002). At present, Pacific oyster has become one of the most important edible

oysters in many parts of the world as a worldwide aquaculture species. In

recent decades, however, mass summer mortality in cultured Pacific oysters

has become a widespread phenomenon in the world [1-4]. It has been

estimated that up to 50% of the harvestable crop can be lost in a given year,

and these losses can be even higher in some areas [2, 5]. Therefore, the

motivation behind this review is a desire to provide insights into the

underlying cause of summer mortality, based on a synthesis of the current

literature.

As a sessile bivalve living in the intertidal zone, oysters are frequently

subject to various environmental stresses. As proposed in fish [6], Le Roux et

Exploring Correlations… 183

al. [7] suggested that oyster mortality could occur as a result of complex

interactions between the host, environmental factors and disease agents (e.g.

Figure 1). Oysters are permanently exposed to various stressful situations and

required physiological adaptations to survive [8]. Under such stressful

conditions immunosuppression can be induced, which in turn will severely

compromise the capacity of defense against parasites and pathogens [9]. This

may result in high bacterial loads, disease outbreaks or subsequent mortalities

[10, 11]. In such a situation, the interaction between environmental conditions

and disease agents can play an important role to induce oyster mortality.

Figure 1. Interactions between the host, pathogen and the environment provide an

explanation for summer mortality in oyster populations.

The abilities of oysters to cope with pathogens, stress, and their interactive

effects change over seasons [12, 13]. It has been reported that summer

mortality is generally associated with water temperature elevation and

coincides with the period of sexual ripeness in oysters (i.e., pre-spawning and

post-spawning) [1, 14-16]. Despite discrepancies among different oyster

farms, oyster spawning usually occurs simultaneously with increasing water

temperature. Both high temperature and spawning impact molluscan

physiology, resulting in high energetic demands. Therefore, Cheney et al. [2]

and Goulletquer et al. [16] conclude that summer mortality in Pacific oysters

results from the synergy of biotic and abiotic processes that are related to

critical developmental stages in the life history of the species.

This review covers (1) oyster reproductive biology and energy

requirements; (2) the response of oysters to nutritional stress under different

spawning conditions [17]; (3) impacts of heat shock and spawning on oyster

physiology and health [19]; and (4) spawning-dependent immune response to

Yan Li, Kirsten Benkendorff, Jian G. Qin et al. 184

bacterial challenge [21]. Through a systematic review of the impact of

spawning on the physiology and immunology of Pacific oysters Crassostrea

gigas, we demonstrate that the energy expended for spawning compromises

the immune response and physiology of oysters, leaving post-spawning oysters

more susceptible to mortality under environmental stress. These findings have

potential implications for the development of preventive measures to reduce

mortality of post-spawning oysters during the physiologically vulnerable

period.

1. OYSTER REPRODUCTIVE PROCESS

AND ENERGY REQUIREMENTS

Oyster reproductive activities are cyclic and follow distinct seasonal or

annual patterns. In temperate regions, oysters typically follow a seasonal

reproduction cycle with periods of gonad maturation in late spring and

spawning in summer [22]. Spawning typically results in reduction in the

condition index and body weight (Fig 2A) [13]. For this reason, there has been

significant research towards the development of non-spawning triploid oysters

to maximize productivity in oyster aquaculture [23].

The gametogenic stage is classically categorised according to the

reproductive scale reported by Lubet [24]: Stage 0 is the undifferentiated

gonads, characterised by empty gonads (sexual repose). There is no presence

of follicles peripherally to the digestive gland, making sex determination

difficult. Stage I is the gonad in the early-developmental stage, known by the

decrease of the interfollicular connective tissue after gonia multiplication and

expansion of the follicles, and contains oogonia or spermatogonia and primary

oocytes or spermatocytes. Stage II is the gonad at a late-developmental stage

when the oocyte and spermatozoa are observed and secondary oocytes and

spermatocytes predominate in the follicles. Stage III A shows intense

gametogenic activity, characterized by the absence of the interfollicular

connective tissue. Stage III B is advanced with further gonad maturation,

during which the male oyster gonads are present, the homogenous stage after

the disappearance of spermatids running toward the centre of the follicle.

Stage III C is shown in spent gonads, characterised by the presence of ruptured

follicles and residual gametes in the oyster gonads. Then a reproductively

quiescent or subsequent “rest” period is followed, i.e., the post-spawning

period [25]. In this review, we have simplified the stages of gametogenesis

Exploring Correlations… 185

into “pre-spawning”, encompassing stage II and stage III A; spawning for

stage III B and III C; and “post-spawning”.

Figure 2. The difference in physiological and immune parameters in pre-spawning, and

post-spawning oysters Crassostrea gigas: A) Condition index and tissue dry weight;

B) Tissue glycogen content; C) Antimicrobial activity [Adapted from 13].

Yan Li, Kirsten Benkendorff, Jian G. Qin et al. 186

As gonad development is a high energy-demanding process, it not only

requires mobilization of exogenous energy from ingested food, but also

requires endogenous energy reserves from body tissues [26-28], especially

glycogen from mantle tissues (Figure 2). In oysters, the reproductive effort and

costs are similar in the male and female, with 27% of oxygen consumption for

reproductive processes [29]. Being the basic bio-energy fuel, carbohydrates

are stored mainly as glycogen in bivalves [19, 30]. It has been demonstrated

that glycogen plays a central role in energetic and metabolic supply during

gametogenesis [1, 22, 27, 30]. However, the capacity of glycogen storage

reduces sharply and reaches its lowest after spawning [1, 13, 31]. Meanwhile,

glycogen phosphorylase and synthase in oysters are also suppressed by

spawning [32]. As glycogen reserves supply additional energy to mobilise

other energetic reserves [33, 34], low glycogen is often correlated with oyster

mortality events [1, 31, 35, 36].

The low energy reserves available after spawning could result in indirect

effects on oyster immunity. Energy is required for routine immune function

but under stress, all available energy will be diverted away from the immune

system to the maintenance of metabolic activities. This relationship between

the physiological status and immune activity can be observed in spawning

oysters. Concomitant with the drop in the condition index (Fig 2A) and

glycogen content (Fig 2B), there is also a drop in the antibacterial activity (Fig

2C). This combined impact on the metabolic reserves and immune activity

leads oysters to a vulnerable condition, subject to potential infection after

spawning. In a laboratory study on the recovery of oyster physiology and

immunity, we have demonstrated that the first 8 days after spawning is a

critically vulnerable period for oysters [37].

2. SPAWNING-DEPENDENT RESPONSE

TO NUTRITIONAL STRESS

Oysters are likely to encounter low food availability in the ocean due to

heterogeneous distribution of seston particles at both spatial and temporal

scales. Berg and Newell [38] reported that chlorophyll a fluctuated eight fold

from summer to autumn in the same location within a year. Even within a tidal

cycle, both quantity and quality of seston can vary as much as across seasons

[39]. Particularly in nutrient poor areas (i.e., with low terrestrial nutrient input

or upwelling), oysters are frequently subjected to low food supply [40]. Most

Exploring Correlations… 187

nutrition studies on oysters have been focused on the effects of dietary

deficiency on growth [eg., 41, 42, 43], but there has been little consideration of

summer morality as a consequence of starvation concomitant with

reproduction. However, starved spawning oysters provide an ideal model to

study spawning-dependent response to metabolic stress.

Figure 3. The condition index (A), mantle glycogen (B) and phagocytic activity (C) of

oysters: “pre S” and “post S” represent the starved pre- and post-spawning oysters;

“pre C” and “post C” represent the fed pre- and post-spawning oysters as controls.

Feeding recommenced on day 80 in the starved groups [Adapted from 17].

Yan Li, Kirsten Benkendorff, Jian G. Qin et al. 188

We designed a manipulative experiment where pre- and post-spawning

oysters were deprived of food for 80 days and then refed for 52 days [17]. The

results demonstrated that starvation and spawning had a rapid and dramatic

effect on oyster condition (Figure 3A). During 80-days of food deprivation,

the mantle tissue thinned out and the body became slightly translucent in post-

spawning oysters. Due to a lack of available gonad mass for absorption and the

thinned mantle tissue, post-spawning oysters need to catabolise energy stored

in other tissues different from pre-spawning oysters (Fig 3B shows these

effects on energy storage). Despite reaching a similar low level of condition

index and glycogen after 80-day food deprivation, the recovery process in pre-

spawning oysters was much quicker than that of post-spawning oyster upon

refeeding (Figure 3), suggesting that pre-spawning oysters are more resilient to

food deprivation than post-spawning individuals.

Under food deprivation, the mantle glycogen of post-spawning oysters is

lower than pre-spawning oysters and is further depleted with reduction of

adductor glycogen during food deprivation [17]. This implies that post-

spawning oysters have developed adaptations to use adductor glycogen as a

source of spare energy to maintain their metabolism and to cope with food

deprivation. Mantle and gill proteins in pre- and post-spawning oysters are

also reduced and maintained at a low level upon food deprivation [43]. Pre-

spawning oysters exhibited strong metabolic resilience to food deprivation as

indicated by faster glycogen (Figure 3B) and protein recovery in starved pre-

spawning oysters than in post-spawning oysters upon refeeding. After 80-day

food deprivation, the slower energy restoration in post-spawning oysters

shows that spawning can suppress the metabolic response to feeding after

starvation in oysters. Spawning activity retards energy recovery after having

experienced a period of food shortage.

Although the synergetic effect of food deprivation and spawning does not

directly cause mortality, concurrent energetic and immunological dysfunctions

may possibly lead to mass mortality in post-spawning oysters [17]. Results on

haemocyte phagocytosis and hemolymph antimicrobial activity demonstrate

that post-spawning oysters have low immune resilience under food deprivation

[17]. As reported by Delaporte et al. [44], there would be less energetic supply

for haemocyte phagocytosis due to the cost of spawning. Similarly, the low

energy intake during food deprivation can decrease haemocyte phagocytosis,

as found in our study and others [45, 46]. When feeding was resumed,

phagocytosis in pre-spawning oysters increased much quicker than that in

post-spawning oysters (Figure 3C). Similarly, food resumption enhanced the

antimicrobial activity, but pre-spawning oysters showed a faster recovery than

Exploring Correlations… 189

post-spawning oysters. In the natural environment, therefore, starved post-

spawning oysters are likely to be more sensitive to potentially lethal stressors,

e.g., bacterial challenge and heat shock. In a worst case scenario, the

synergistic effect of spawning and poor nutritional condition could lead to

mass mortality, especially in summer under high temperature stress when

pathogens prevail.

3. IMPACTS OF HEAT SHOCK AND SPAWNING ON OYSTER

PHYSIOLOGICAL AND IMMUNE RESPONSES

Among various environmental conditions, temperature has long been

recognised as a key factor that influences all physiological processes in oysters

[47]. With elevated temperatures, animals need to increase metabolism to

acquire an adequate energetic supply for survival [48]. Pacific oysters can

adapt to a wide range of temperatures from 3 to 35ºC [49]. Furthermore,

oysters can exhibit adaptive plasticity to heat shock, known as "induced

thermotolerance" [8]. Indeed, thermotolerance has been demonstrated in the

laboratory, with exposure to a single sublethal heat shock (e.g., 37ºC) enabling

oysters to transiently tolerate extreme, otherwise lethal temperatures (43ºC) for

an hour [19]. This phenotypic plasticity of the heat-shock response is

associated with the expression of heat-shock proteins in oysters [50, 51].

In Pacific oysters, Hsp70 is the primary family of Hsp that is responsive to

thermal stress [50]. The thermal limits of oysters are correlated with changes

in isoform expression in the Hsp70 family, which can be detected by western

blotting techniques. Thermal adaptation in oysters is known to be dependent

on hydrographic and biological factors, including ambient temperature and

reproductive stress [19, 50]. As the cost of protein synthesis is estimated to be

18~26% of the energy budget of ectothermal organisms [52], the metabolic

adaptation in spawning oysters is also subject to a deficiency in energy supply

[19]. In order to examine the underlying causes leading to this phenomenon,

thermotolerance of the Pacific oyster was assessed using pre- and post-

spawning oysters that were sequentially treated with sublethal (37ºC) and

lethal heat shocks (44ºC) [19].

In comparison, although both pre and post-spawning oysters were

recorded to have some adaptability of induced thermotolerance via the

expression of Hsp69, the ability to resist sublethal and lethal temperature

shock was reduced in post-spawning oysters. A preventative 37ºC exposure

Yan Li, Kirsten Benkendorff, Jian G. Qin et al. 190

significantly reduced oyster mortality after exposure to a second heat shock of

44ºC, but in post-spawning oysters, mortality remained at 80%, compared to

less than 10% in pre-spawning oysters [19]. As suggested by Kregel [53]

morbidity and mortality from thermal shock is due to the dysfunction of some

critical target tissues that are heat sensitive and vital to the animal. We found

that both Hsp72 and Hsp69 had heat shock-dependent stimulation in the gills

of pre-spawning oysters, but not in post-spawning oysters indicating that

spawning can reduce heat shock protein synthesis [19]. Impairment of heat

shock protein synthesis in the gill and the consequent protein denaturation is

likely to lead to hyperthermic killing. Ultimately, dysfunction in the gill, the

most important respiratory organ of marine animals, will cause a mismatch

between oxygen delivery and the ability to respond to heat shock, which

finally leads to the collapse of physiological function [54, 55].

Besides depletion of glycogen in post-spawning oysters, spawning and

heat shock were concomitant with decreasing adenylate energy charge (AEC),

indicative of lower cellular energy for metabolic activity. After heat shock, the

AEC value in pre-spawning oysters was maintained within the range of 0.5 -

0.7 (Table 1), which is the sub-optimal stress range according to Cattani et al.

[57]. This indicates that pre-spawning oysters can maintain normal energy

metabolism at a cellular level irrespective of induced thermotolerance.

Table 1. Effects of heat shock and spawning on adenylate energy

charge in oyster mantle tissue (Mean ± SE). “Pre HS” and “Post HS”

represent the heat shocked pre- and post-spawning oysters; “

Pre Con” and “Post Con” represent non-heat treated

pre- and post-spawning oysters [Source from 19]

Day Pre HS Post HS Pre Con Post Con

0 Oysters were heated at 37ºC for 1 hour (sublethal heat shock)

0.64 ± 0.01 0.55 ± 0.01 0.71 ± 0.04 0.61 ± 0.01

1 0.69 ± 0.02 0.54 ± 0.01 0.76 ± 0.07 0.63 ± 0.03

2 0.64 ± 0.03 0.58 ± 0.01 0.70 ± 0.04 0.63 ± 0.01

3 0.65 ± 0.02 0.54 ± 0.03 0.70 ± 0.02 0.63 ± 0.01

5 Oysters were reheated at 44ºC for 1 hour(lethal heat shock)

6 0.59 ± 0.01 0.39 ± 0.02 0.76 ± 0.06 0.66 ± 0.02

10 0.63 ± 0.04 0.32 ± 0.02 0.71 ± 0.01 0.67 ± 0.02

* The bold italic numbers are less than 0.5 which is the critical threshold for oyster

AEC values based on Shofer and Tjeerdema [56].

Exploring Correlations… 191

However, post-spawning oysters had much lower AEC levels, especially

after lethal heat shock (Table 1). The low AEC values and high mortality

recorded in post-spawning oysters subjected to lethal heat shock are consistent

with a study by Shofer and Tjeerdema [56], where AEC values between 0.3 -

0.5 were suggested to be within a critical range from which the capacity to

recover from stress is impossible. This critical limit may be attributed to a

transition to anaerobic metabolism when temperature is beyond

thermotolerance, which leads to insufficient cellular energy supply [54]. In this

stressful situation, the physiological trade-offs will divert energy reserves

towards essential maintenance [47], although the residual energy reserves

(glycogen) seem not to be adequate for energy modulation in post-spawning

oysters.

A cumulative effect of spawning and heat shock was observed on the

immunocompetence of oysters, demonstrated by reduced haemocyte

phagocytosis and hemolymph antimicrobial activity [19]. These results

support the hypothesis that the energy expended during reproduction

compromises the thermotolerance and immune status of oysters, leaving them

easily subject to mortality if heat stress occurs in the post-spawning stage. This

reflects the likely consequences of spawning under thermal stress, thus

contributing our understanding of oyster summer mortality. Consequently,

these results have implications for the long-term persistence of molluscs under

the influence of global warming [19].

4. SPAWNING-DEPENDENT IMMUNE RESPONSE

TO BACTERIAL CHALLENGE

Although oysters have developed physiological adaptation for survival

[8], stress can suppress their immunocompetence and substantially

compromise the ability to defend against parasites and pathogens [9, 19].

There is some evidence that reduction of defense efficiency can lead to high

bacterial loads, disease outbreaks and mass mortality in oysters [10, 11]. We

have already demonstrated that oyster immunity is impacted by the

physiological stress of spawning, as well as environmental stressors such as

low nutrient availability and high temperature. However, infection by

pathogens can be regarded as another stressor. Typically an animal will

respond to infection by mounting an immune response. Therefore, the question

remains as to whether spawned oysters can respond effectively to bacterial

Yan Li, Kirsten Benkendorff, Jian G. Qin et al. 192

challenge or if their immune systems are too compromised from the low

energy reserves.

To investigate this issue further, we developed two models to simulate a

bacterial challenge [47]. The first model involved the injection of extracellular

products from Vibrio harveyi into the oysters to establish whether they were

more susceptible to virulence factors after spawning. The second model

involved the injection of heat killed Vibrio harveyi into the oysters to examine

the sublethal immune responses to a challenge. The injection of heat-killed

bacteria caused less than 6% mortality in both pre- and post- spawning oysters.

However, the injection of bacterial extracellular products resulted in ~ 30%

mortality in pre-spawned oysters. Mortality was significantly high at ~50% in

post-spawning oysters, indicating that they are less able to resist the toxic

factors secreted by bacterial pathogens.

In the sublethal bacterial challenge model, no significant differences were

observed between pre- and post-spawning oysters in the total haemocyte

abundance and the phagocytic rate, suggesting that spawning does not have a

direct effect on cell-mediated immunity [21]. Nevertheless, we did observe

lower phagocytosis in post-spawning oysters than pre-spawning oysters in the

control groups throughout the study period (Figure 4A). Despite seasonal

variation, a reduction of phagocytosis has also been observed during spawning

in field populations [58]. However, the effect of spawning might be over-

ridden by the impact of simulated bacterial challenge, as all challenged oysters

had double the phagocytic rate of the controls, irrespective of spawning status.

Consequently, post-spawning oysters appear to be capable of eliciting a

similar cellular immune response as pre-spawning oysters, to cope with

invasion by foreign particles. This finding is coincident with previous

observations that haemocyte phagocytosis is similar between summer

mortality-susceptible oysters and summer mortality-resistant oysters [59].

Therefore, Lambert et al. [60] concluded that relevant indicators other than

haemocyte profiles are required to help explain oyster survival during summer

mortality events.

Unlike the cellular immune response, the humoral immune function was

not only influenced by simulated bacterial challenge, but was also suppressed

by spawning (Figure 4B). Antimicrobial agents are synthesized by the

haemocytes [61] and stored in the cells as reserves, then released only after

stimulation by microbial infection or other similar challenges [10, 62].

Consequently, the nonviable bacterial injection was expected to increase the

antimicrobial activity in comparison to seawater injection, by stimulating the

release of active factors. However, the opposite effect was observed, whereby

Exploring Correlations… 193

the antimicrobial activity was reduced upon simulated bacterial challenge,

despite an increase in haemocyte numbers and phagocytosis. Therefore, the

changes in antimicrobial activity are not directly synchronised with the shifts

in cellular immune functions. This could be related to the use of nonviable

bacteria, which may not have the right cues to stimulate release and upregulate

the synthesis of new antimicrobial factors. Therefore the patterns observed in

this study may simply result from changes in the basal levels of constitutively

expressed antimicrobial resources in the hemolymph. These constitutive

factors appear to be utilised within 2 – 4 days after the injection of nonviable

bacteria and are not replenished to the level of the controls by 7 days after

simulated bacterial challenge. The basal levels of antimicrobial activity were

also generally lower in post-spawning oysters, suggesting trade-offs in the

humoral immune system under physiological stress [21].

Figure 4. Immune responses in Crassostrea gigas with respect to a simulated bacterial

challenge and spawning status: A) phagocytic activity and B) antimicrobial activity.

‘NBC’ represents nonviable bacterial suspension injection challenge; ‘FSW’ represents

seawater injection; ‘Con’ represents oysters without injection [Adapted from 21].

Yan Li, Kirsten Benkendorff, Jian G. Qin et al. 194

Concomitant with the decrease in antimicrobial activity, an initial

reduction in hemolymph protein was found upon simulated bacterial challenge

[21], suggesting the participation of hemolymph protein in antimicrobial

activity. In post-spawning oysters, the hemolymph protein declined over time

in controls and although it increased slightly after injection, this occurred at a

much slower rate than observed in pre-spawning oysters. As a range of plasma

antibacterial peptides and bacteriolytic enzymes are involved in bivalve

immune defense [62-64], it is likely that these proteinaceous substances were

rapidly mobilized in response to simulated wounding by injection in both of

pre- and post-spawning oysters. However, the ability to recover humoral

immune function after simulated bacterial challenge is clearly impacted by

spawning (Figure 4B). This implies that after exhausting the basal levels of

humoral antimicrobial proteins, post-spawning oysters have insufficient

metabolic resources to initiate the expression of new proteins and peptides to

continue fighting infection. Therefore, the humoral immune function may not

be maintained effectively in post-spawning oysters exposed to prolonged or

repeated infections. Coupled with the degradation of host proteins by bacterial

extracellular products, this may weaken the oysters to a point of no recovery.

Therefore, despite the apparently normal cellular immune function in post-

spawning oysters, the spawning-suppressed humoral immune function could

be fatal to oysters when facing opportunistic pathogens in the environment,

particularly in warm environments where the growth rate of Vibrio spp. is high

[65].

5. POTENTIAL IMPLICATIONS

The published literature and anecdotal reports suggest that many of the

mortalities in Pacific oysters are the result of multiple factors or stressors [2, 3,

66]. Although there was no massive mortality in summer during our field

study, the coupled relationship of low antibacterial activity and energy

reserves is a strong indication of the fragile condition of spawned oysters [13].

In the present study, the synergistic impacts of environmental stress and

spawning on physiology and immunocompetence provide one plausible

explanation for the phenomenon of summer mortality in the Pacific oyster.

This research review reflects the likely consequences for post-spawning

oysters under food deprivation [17], thermal stress [19] and bacterial challenge

[21], thus contributing to our understanding of the underlying biological

reasons for mass oyster mortality in the post-spawning period. Meanwhile, this

Exploring Correlations… 195

review greatly improves our knowledge of the sublethal changes that occur in

the immunological and physiological responses of oysters under stress, as well

as the natural temporal variation. Results from the references cited provide

good baseline information for future monitoring of oyster health.

Since the mid-1970s, large-scale episodic events, such as disease

epidemics, mass mortalities and biological population explosions have been

occurring in marine environments with increasing frequency, intensity and

range [67]. Notable examples are the polar-ward expansion of oyster diseases

and concerns of escalating summer mortality in European and Australian

bivalve aquaculture. Oscillations in the earth’s climate also lead to associated

fluctuations in the temperature regimes of many marine and terrestrial

ecosystems. Consequences in marine ecosystems include changes in the timing

of reproduction, as well as changes in reproductive success, recruitment,

growth performance and mortality of species and finally, changes in their

geographical distribution [54]. These factors will be the major threat to

aquaculture and the economic and ecological sustainability of marine fisheries

in the near future.

The Pacific oyster offers a good opportunity to assess the impacts of

climate change on ocean productivity, as an important world-wide aquaculture

species whose reproduction is triggered by temperature increases. Meanwhile,

it is possible that the incidents of mass mortality in marine organisms,

including species such as abalone, mussels and clams that also have great

economic value, will increase globally, coincident with unpredictable

environmental patterns [68]. For Pacific oyster aquaculture, although the post-

spawning period falls into the out-of-season seafood marketing, husbandry

management during this period is critical to reduce mortality. To prevent

mortality at this vulnerable period, it is recommended that farmers try to

reduce or avoid any anthropogenic disturbance to spawned animals. In

intertidal farming areas, submerging spawned oysters into deeper seawater

could reduce stress from exposure to high air temperature during low tide.

Removing any seen morbid and moribund individuals will help reduce fouling

of the water and stop the spread of infection. The impact of physio-chemical

aspects of seawater in culture areas, as well as culture practices should also be

taken into account. Food supplementation for spawned populations should be

considered if natural food availability is low during the recovery period (eg.,

cultivation area shift), particularly in lean farming areas.

As oysters are already used as important bioindicators in the environment

and can be representative for intertidal populations [69], the implications of

spawning impact on resilience to environmental stress should be compatible to

Yan Li, Kirsten Benkendorff, Jian G. Qin et al. 196

other species in similar geographic distributions with a similar reproduction

pattern. This review highlights the sensitivity of spawned molluscs to

environmental stressors and therefore provides vital information for the

development of future adaptation strategies in a changing global environment.

An improved understanding of the interactions between the host, pathogen and

environment will facilitate long-term economic and environmental

sustainability in marine biological resources.

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