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Consequences of oyster mortality episodes on benthic-pelagic coupling in Thau lagoon (France)
UMR MARBEC, Sète : Richard, Le Gall, Mortreux, Ouisse, Lagarde, Fiandrino, Fortune, Munaron,
Messiaen, Oheix, Derolez, Belamy, Foucault, Devique, Roque d’Orbcastel
Montpellier: Bec, Mostajir, Hatey, McKenzie
Palavas: Callier
UMR IHPE: Montagnani, Rolland
UMS MEDIMEER: Mas, Parin
LDV34: Keck, Dedet, Singevin
Students: Bourreau, Vanhuysse, Chantalat, Degut, Neveu, Bourguoin
ShellFish farmers: Fournier, Navarro, Zecchinon, Tarbouriech, Galavielle, Avila, Chastel, Anthony
Mortaflux WP5: FATE
1
The Thau lagoon is exploited by shellfish
cultures
Oyster Crassostrea gigas
Pre-growing of oyster juveniles
into suspended lanterns
Context
Growing of oysters on ropes
2
Bio
de
po
siti
on
Bivalve
BacteriaDetritus
biodepositsPhyto Zoo
Nutrients
Se
dim
en
tW
ate
r co
lum
n
O2
PIM
POM
Protist
SPM
excretionrespiration
filt
rati
on
resp
ira
tio
n
sed
ime
nta
tio
n
min
era
lisa
tio
n
Influence on ecosystem functionInfluence on ecosystem functionInfluence on ecosystem functionInfluence on ecosystem function
Context
For sustainable development of shellfish culture:
� Necessity to study Aquaculture/Environment interactions
3
2008 : Mortality of oyster juveniles (40-100%)Period: April-May
Pathogen: Virus Herpes Os-HV1 µ var
→ Impact on produc5on
Thau : 2001 : 10 -15 000 T → 2017: 7 000
4
Context
2014-2015: Mortality of commercial-sized oysters
(40-50%)Period: June-July
Pathogen: Vibrio aestuarianus
→ Impact on summer sales
Context and General objectives
- sick organisms are not
separated from conspecifics
- Dead organisms are kept in
the environment until the total
disappearance of their flesh.
5
What are the consequences of this practice on (ii) dissolved and
particulate fluxes, (ii) planktonic components, (iii) pathogen transfers into
the benthic-pelagic coupling of the Thau Lagoon?
6
- sick organisms are not
separated from conspecifics
- Dead organisms are kept in
the environment until the total
disappearance of their flesh.
Oyster juveniles Commercial-sized oysters
MORTAFLUX
(2015-2016, Ifremer DS, EC2CO)
VIVALDI WP5 Fate, juvenile (2017, H2020)
VIVALDI WP5 FATE, adult
(2016-2018, H2020)
Context and General objectives
Individual Lantern Table
ex situMetabolic Pelagic Benthic chambers
Conception & Realisation
(UMR MARBEC + UMS MEDIMEER)
in situ
Approaches
scalesRope Bag
Rearing unit
7
Individual Lantern Table
ex situMetabolic Pelagic Benthic chambers
Conception & Realisation
(UMR MARBEC + UMS MEDIMEER)
in situ
Approaches
scalesRope Bag
Rearing unit
8
First ResultsO
2C
onsu
mpt
ion
(µm
ol.h
-1.c
ham
ber-1
)
C L DW
A)
C)
NH
4F
lux
(µm
ol.h
-1.c
ham
ber-1
)
PO
4F
lux
(µm
ol.h
-1.c
ham
ber-1
)
D)
NH
4/P
O4
Rat
io T
f
B)
C L DW C L DW
C L DW0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
-0.005
0
0.005
0.01
0.015
0.02
0.025
0.03
0.035
0
5
10
15
20
25
30
35
40
45
-0.05
0
0.05
0.1
0.15
0.2
0.25
0.3
0.35
0.4
a b
c
b
a
b
c
b
ab
d
c
a
b
d
c
- OsHV-1 infection (L):
decrease oxygen consumption and
ammonium excretion of oyster juveniles.
- Mineralisation of the flesh of dead
oysters (D) :
Induce an increase of ammonium and
phosphate fluxes and a decrease in the
N/P ratio
with potential incidence on planktonic
communities…
Richard et al. 2017 Aquaculture 475 40-51.9
40
Inst
anta
neou
sra
te (
%) 30
20
10
0
Moribund
Mortality
DE
CD
A
B
CD C
a
b
c c bccc
OsH
V
Pos
t-pe
ak 3
Bef
ore
Pos
t-pe
ak 1
Mor
ibun
d
Mor
talit
y pe
ak
Pos
t-pe
ak 2
Sta
rtin
g
W16 W17 W18 W19 W20 W21 W22
1 SP
M > 0.2 µm
Moribund and mortality rate dynamics
Higher moribund rate was observed one week
before the mortality peak
First Results
10
40
Pos
t-pe
ak 3
Bef
ore
Pos
t-pe
ak 1
Mor
ibun
d
Mor
talit
y pe
ak
Pos
t-pe
ak 2
Sta
rtin
g
Inst
anta
neou
sra
te (
%)
W16 W17 W18 W19 W20 W21 W22
30
20
10
0
Moribund
Mortality
DE
CD
A
B
CD C
a
b
c c bccc
0
50
100
150
0
2
4
6
8 Fleshwater
OsH
V-1
fles
h(lo
g10
(C9C
10 +
1.g
-1)
OsH
V-1 S
PM
> 0.2 µm
(C9C
10.mL
-1)
-Quantification of OsHV-1 in flesh one week
(W17) before moribund period (W18)
-No quantification of OsHV-1 as free form, ie.
in < 0.2µm-filtered-water
-Presence of OsHV1 in water column as
associated form to suspended matter >
0.2µm
Highest OsHV-1 concentration in water
column during moribund period (W18)
DNA OsHV-1 dynamics in oyster flesh and water column
First Results
11
First ResultsC
iliat
es(I
nd.L
-1)
40
30
20
10
0
Moribund
Mortality
DE
CD
A
B
CD C
a
b
c c bccc
OsH
V
Pos
t-pe
ak 3
Bef
ore
Pos
t-pe
ak 1
Mor
ibun
d
Mor
talit
y pe
ak
Pos
t-pe
ak 2
Sta
rtin
g
W16 W17 W18 W19 W20 W21 W22
1 SP
M > 0.2 µm
Pos
t-pe
ak 3
Bef
ore
Pos
t-pe
ak 1
Mor
ibun
d
Mor
talit
y pe
ak
Pos
t-pe
ak 2
Sta
rtin
g
0
0.1
0.2
0.3
W16 W17 W18 W19 W20 W21 W22
AA,B
B,CC,D C,DE
aa
b ccc
Pos
t-pe
ak 3
Bef
ore
Pos
t-pe
ak 1
Mor
ibun
d
Mor
talit
y pe
ak
Pos
t-pe
ak 2
Sta
rtin
g
0500
10001500200025003000
W16 W17 W18 W19 W20 W21 W22
Other
Lohmaniella sp
Strobilidium sp.
Balanion sp
Uronema sp
Strombidium sp.
Phy
topl
ankt
on(C
hlbµ
g.L-1
)In
stan
tane
ous
rate
(%
)
During moribund and mortality periods:
Increase of picophytoplankton and ciliate
abundances
Uronema sp. & Balanion sp.
Planktonic microbial component dynamics
12
nd
Pos
t-pe
ak 3
Bef
ore
Pos
t-pe
ak 1
Mor
ibun
d
Mor
talit
y pe
ak
Pos
t-pe
ak 2
Sta
rtin
g
W16 W17 W18 W19 W20 W21 W22
Cili
ate
Flu
x(µ
gC.g
DW
.h-1
)C)
-6
-4
-2
0
A
B B
nd
nd
W16 W17 W18 W19 W20 W21 W22
0
0
50
100
150
0
2
4
6
8 Fleshwater
OsH
V-1
fles
h(lo
g10
(C9C
10 +
1.g
-1)
OsH
V-1 S
PM
> 0.2 µm
(C9C
10.mL
-1)
-100-80-60-40-20
0
Chl
a <
3 µm
F
lux
(µgC
.gD
W.h
-1)A)
AA
B BC
nd
Depletion of small (< 3 µm) phytoplankton at starting
and moribond periods
High depletion of ciliates within moribund period
Depletion of Planktonic microbial components
First Results
13
Pos
t-pe
ak 3
Bef
ore
Pos
t-pe
ak 1
Mor
ibun
d
Mor
talit
y pe
ak
Pos
t-pe
ak 2
Sta
rtin
g
W16 W17 W18 W19 W20 W21 W220.E+00
5.E+05
1.E+06
2.E+06
2.E+06
3.E+06
3.E+06Absencepresence
40
Inst
anta
neou
sra
te (
%) 30
20
10
0
Moribund
Mortality
DE
CD
A
B
CD C
a
b
c c bccc
nd ndOsH
V-1
tran
sfer
(C9C
10.la
nter
n-1 .
h-1 ) Significant DNA OsHV-1 releases in water
column in presence of oyster juveniles
Highest releases were observed in
moribund period (W18) and begun one
week before (W17)
14
+09
+09
+09
+09
+09
+07
+00
Releases of DNA OsHV-1 in water column
First Results
y = 0.7541xR² = 0.4568
0
1
2
3
4
5
6
7
0 1 2 3 4 5 6 7 8
OS
HV
1 T
rans
fer
(Log
10 (
copi
esC
9C10
+1.
lant
ern-1
.h-1
) )
OSHV1 Flesh(Log10 (copiesC9C10 + 1.g-1 ))
Significant correlation between
OsHV-1 releases in water column
and OsHV1 concentration in oyster
flesh
→OsHV-1 releases may be
associated to decaying flesh
Relation between OsHV-1 releases and flesh concentrations
First Results
15
NanoBacteria
Micro
OsHV-1 FleshPico
StrombidiumStrobilidium
OsHV-1 waterBalanion
Uronema
45.6%
26.5
%
Significant correlation between :
[OsHV-1] flesh and picoplankton (0-3 µm)
[OsHV-1] in water column and biomass of
the ciliate Balanion sp.
Ciliates are known to be saprophyte and to grow on bacteria and picoplankton.
Depletion of picoplankton and ciliate have been observed in presence of oysters before and within
moribund period.
→ Flesh in decomposition, Picoplankton and ciliates may be implicated in OsHV-1 transmission via
filtration activity
Relation between OsHV-1 & microbial components
First Results
16
0
50
100
150
200
250
300
350[0.2-3] µm
[3-20] µm
>20 µm
OsHV-1 was NOT observed
outside farms
Inside farm, OsHV-1 was mainly
associated to 0-3 µm fraction but
also with 3-20 µm fraction with
different temporal dynamics
Relation between OsHV-1 & suspended matter
according to fraction size
First Results
17
Conclusions
1) Mortality episode of oyster juveniles in the Thau lagoon induced:
- Increase of NH4 and PO4 concentrations, decrease of N/P
- Bloom of picophytoplankton and ciliates (Uronema, Balanion)
during moribund period in relation to leaching and decomposition of decaying oyster
flesh.
- OsHV-1 releases, two weeks before mortality peak with highest mean observed
during moribund period
(2.5 x 109 OsHV-1.lantern-1.h-1 or 3000 x 109 OsHV-1.h-1 at table scale)
2) OsHV-1 was associated to suspended matter, mainly with (0.2-3 µm) and (3-20
µm) fractions. [OsHV-1] was correlated to flesh [OsHV-1], picoplankton and ciliates.
18
.
→ releases of OsHV-1, depletion of decaying flesh, picoplankton and ciliates may be
involved in spread of the disease.
Perspectives
Adult > Juvenile
(100g, 15 Kg.m-2) (1g, 2.4 Kg.m-2)
FurtherFurtherFurtherFurther analysisanalysisanalysisanalysis::::
3) Effect of commercial-sized oyster mortality?
OsHV-1 sedimentation via biodeposition?
?1) Ecological niche of pathogens?
2) Consequences of mortality on benthic system?
19
Recommendations
- Do pathogen analysis and/or temperature challenge before to introduce
oysters into environment.
- Do not introduce oyster juveniles during the risk period (17°C-24°C)
- Do not introduce infectious and moribund organisms.
- If mortality phenomena occurs, exclude moribunds as much as possible.
Nevertheless, exclusion would not be a sufficient solution to limit the spread of
the disease.
20
OsHV-1 being mainly associated to 0.2-3µm fraction, solution could be to develop polyculture
systems integrating oysters and other suspension-feeders which efficiently retain 0-3 µm
particles, which will act as biofilters.
To open the debate: Since OsHV-1 induces mortality of other species at larval stage (clam,
pecten…), what are the consequences of oyster mortality episodes on marine biodiversity
and specially on other key species?
