Int J Life Cycle Assess (2018) 23:1042–1048
DOI 10.1007/s11367-017-1394-8
CHALLENGES AND BEST PRACTICE IN LCAS OF SEAFOOD AND OTHER AQUATIC PRODUCTS
Consideration of carbon dioxide release during shell production
in LCA of bivalves
Nicholas E. Ray 1,2 & Teri O’Meara 3 & Timothy Wiliamson 2 & Jose-Luis Izursa 2 &
Patrick C. Kangas 2
Received: 10 March 2017 / Accepted: 5 September 2017 / Published online: 14 September 2017
# Springer-Verlag GmbH Germany 2017
Abstract
Purpose Life cycle assessment (LCA) can be used to under-
stand the environmental impacts of the shellfish aquaculture
and wild harvest industries. To date, LCA of shellfish exclude
carbon dioxide (CO2) release from bivalve shell production
when quantifying global warming potential per functional
unit. In this study, we explain the rationale for including
CO2 released during shell production in LCA of bivalves,
demonstrate a method for estimating this CO2 release, and
apply the method to previous studies to demonstrate the im-
portance of including CO2 from shell production in LCA.
Methods A simple approach for calculating CO2 from bivalve
shell production was developed utilizing the seacarb package
in R statistical software. The approach developed allows for
inclusion of site-specific environmental parameters such as
water temperature, salinity, pH, and pCO2 when calculating
CO2 release from shell production. We applied the method to
previously published LCA of bivalve production systems to
assess the impact of including this CO2 source in the LCA.
The past studies include aquaculture and wild harvest produc-
tion strategies and multiple bivalve species.
Results and discussion When we recalculated the total kg
CO2 released in past studies including CO2 release from shell
production, the additional CO2 release increased the total
Responsible editor: Ian Vázquez-Rowe
* Nicholas E. Ray
nray@bu.edu
1
Department of Biology, Boston University, Boston, MA 02215, USA
2
Department of Environmental Science and Technology, University of
Maryland, College Park, MD 20740, USA
3
Institute of Marine Science, University of Auckland, Auckland 1142,
New Zealand
global warming impact category (CO 2 equivalents) in
cradle-to-gate studies by approximately 250% of the original
reported value. Discussion of our results focuses on the im-
portance of different components of our calculations and site-
specific environmental parameters. We make predictions on
how the magnitude and importance of CO2 released during
shell production could change due to climate change and
ocean acidification, and provide suggestions on how CO2 re-
lease from shell production can be reduced through careful
selection of aquaculture facility location and aquaculture
practices.
Conclusions We provide a method for including CO2 from
shell release in LCA of bivalves and recommend that future
LCA of bivalves include this CO2 as part of the global
warming impact category.
Keywords Aquaculture . Bivalve . Calcium carbonate .
Fisheries . Shell
1 Introduction
Bivalves are an economically and ecologically valuable class
of organisms whose many benefits have been exploited by
humans for centuries. An important global food resource, bi-
valves made up 5.6% of the global seafood trade by quantity
in 2013, and production of bivalves grown in culture increased
by 34% between 2000 and 2014 (FAO 2002, 2016). Recently,
bivalve shells have been suggested as a possible method of
carbon (C) sequestration in addition to the value of the bivalve
meat as a food product. However, during the sequestration of
C in shell, carbon dioxide (CO2) is formed and released. This
CO2 release is quantifiable and significant. To date, no LCA
studies quantify or include the release of CO2 from bivalve
shell production. We hypothesize that inclusion of CO2
Int J Life Cycle Assess (2018) 23:1042–1048
released during bivalve shell production will significantly in-
crease the CO2-eq per functional unit in LCA of shellfish
production systems, and that inclusion of this CO2 is neces-
sary in future LCA.
Bivalve shells function as an exoskeleton, providing struc-
ture for the animal and protection from predators and unfavor-
able environmental conditions, such as low oxygen, high tem-
peratures, or desiccation. The shell grows along with the ani-
mal through the process of biogenic calcification, using dis-
solved bicarbonate (HCO3−) and calcium (Ca2+) to precipitate
calcium carbonate (CaCO3) as either calcite or aragonite (Eq.
(1)).
Ca2þ þ 2HCO−3 ⇌CaCO3 þ CO2 þ H 2 O ð1Þ
During biogenic precipitation of CaCO3, CO2 is released
(Frankignoulle et al. 1994, 1995; Ware et al. 1992). Some of
the CO2 produced during CaCO3 precipitation forms HCO3−,
while the rest remains as CO2 (the ratio of CO2 produced that
remains as CO2 and does not form HCO3− is abbreviated as
Ψ). Following Henry’s Law, this excess CO2 released during
shell production will be released to the atmosphere, or prevent
further uptake of atmospheric CO2 into the water body. Thus,
the production of CaCO3 shells by bivalves releases CO2.
In addition to CO2 release from shell production, bivalves
release CO2 during respiration. Due to these two sources of
CO2 release, a debate has developed as to whether the C se-
questered in shell during shell production should be included
in C trading systems. Munari et al. (2013) demonstrated that
sequestration of C in the shell (136.6 mol CO2 m−2 year−1) of
Mediterranean mussels (Mytilus galloprovinciallis) raised in
culture was less than the sum of CO2 released during respira-
tion (187.8 mol CO2 m−2 year−1) and shell production
(86.8 mol CO2 m−2 year−1). They argue that since CO2 pro-
duction is greater than CO2 sequestration, bivalve shell should
not be a part of C trading systems. Conversely, Filgueira et al.
(2015) argue for an ecosystem-based approach for determin-
ing the amount of CO2 released during bivalve shell produc-
tion. In LCA, CO2 released during respiration is not counted
in greenhouse gas (GHG) assessments, as consumers—such
as bivalves—are considered to be simply recycling CO2 se-
questered during photosynthesis of the consumed biomass.
However, the CO2 released during bivalve shell production
is not produced from the recycling of CO2 sequestered from
photosynthesis. Rather, it is produced during the precipitation
of CaCO3 from dissolved HCO3−, and thus must be included
in LCA.
In this paper, we demonstrate a simple method for calcu-
lating CO2 release from bivalve shell production, apply this
method to past LCA of bivalves, and discuss our results in
terms of the importance of including CO2 from shell produc-
tion in LCA.
1043
2 Materials and methods
2.1 Estimating CO2 release from bivalve shell production
To calculate CO2 release from shell production, three values
must be known: the shell mass at harvest, the percentage of
shell made up of CaCO3, and the ratio of CO2 released per
CaCO3 precipitated as a function of seawater buffering capac-
ity, expressed as Ψ (Frankignoulle et al. 1994). CO2 release
associated with shell production can be estimated using Eq.
(2):
CO2 ReleaseShellFormation ¼ Shell Mass at Harvest  Ψ
 Shell%CaCO3
g
44:01 CO2
 mol ð2Þ
g
100:0869
mol
CaCO3
Shell mass at harvest varies between site, species, and the
age at which the bivalve is harvested. Ψ can be calculated as a
function of pH, temperature, salinity, and pCO2. CaCO3 com-
poses slightly more than 95% of bivalve shell (Goulletquer
and Wolowicz 1989; Yoon et al. 2003). In order to convert
between kg CaCO3 and kg CO2, the ratio of molar masses
(100.0869 g mol−1 for CaCO3 and 44.01 g mol−1 for CO2) is
added to the calculation. To calculate Ψ for individual sites, we
used the seacarb package available in R statistical software
(Gattuso et al. 2016). The seacarb package offers multiple
calculations, from which we selected to use BFlag = 21^.
This option in the seacarb package calculates Ψ from user
input pCO2, pH, temperature, and salinity as variables, mak-
ing it the most useful option to calculate site-specific Ψ values.
2.2 Inclusion and estimation of shell CO2 release from past
LCA
Six previous studies encompassing LCA of seven bivalve cul-
ture and harvest systems were identified for assessing the
magnitude of including CO2 release from shell production in
the global warming impact category (Table 1). Two of these
studies investigated production of oysters raised in culture (de
Alvarenga et al. 2012; Fry 2012), three investigated produc-
tion of mussels raised in culture (Aubin and Fontaine 2014;
Fry 2012; Iribarren et al. 2010a), and two investigated the
energy required for wild harvest of mussels (Thrane 2004)
and unspecified bivalves (Schau et al. 2009). These studies
covered a range of scopes of the LCA. Results reported in past
studies used a variety of functional units, so we converted all
results and functional units to kg CO2-eq kg−1 ash-free dry
weight of tissue (AFDW). We selected AFDW as it allows for
direct comparison of the amount of edible product harvested,
1044 Int J Life Cycle Assess (2018) 23:1042–1048

Table 1 Summary of previous

bivalve aquaculture and fishery Study Location Species Scope Functional Reported kg CO2-eq
LCA studies considered in our unit used per functional unit
assessment of the importance of
including CO2 produced during de Alvarenga Brazil Oyster Cradle-to-grave 1 kg 11.31a
bivalve shell production et al. (2012) (Crassostrea
gigas)
Fry (2012)— Scotland Oyster Cradle-to-gate 1t 1281
oyster (Crassostrea
gigas)
Aubin and France Mussel (Mytilus Cradle-to-gate 1t 40.4a
Fontaine edulis)
(2014)
Fry (2012)— Scotland Mussel (Mytilus Cradle-to-gate 1t 252
mussel edulis)
Iribarren et al. Spain Mussel (Mytilus Cradle-to-gate 89.74 t/raft 38,415.88
(2010a) galloprovincial- year−1
is)
Thrane (2004) Denmark Mussel (Mytulis Cradle-to-dock L/kg 0.026a
edulis)
Schau et al. Norway Bivalve (no Cradle-to-dock kg/kg 0.29a
(2009) specific species)

a
Value reported here was converted using the methods described in the section BInclusion and estimation of shell
CO2 release from past LCA^

and can easily be converted to other functional units such as
kg CO2-eq kg−1 protein or kg CO2-eq calorie−1.
de Alvarenga et al. (2012) reported the climate change
impact of oysters in DALY. We converted their reported value
of 1.558 × 10−7 DALY kg−1 oysters in the climate change
impact category to kg CO2-eq kg−1 oysters by combining
the three components of BScenario A^ reported in the study
(oyster production and consumption, end-of-life, and transport
of shell to landfill), and then used the hierarchist perspective
normalization factor for Eco-indicator 99 of 9.08E5 to calcu-
late a global warming impact of 2.709-kg CO2-eq kg−1 oyster
produced (Goedkoop and Spriensma 2001).
Aubin and Fontaine (2014) reported a range of − 44.7–
125.5 kgCO2-eq t−1 mussels. We elected to use the mean value
(40.4-kgCO2-eq t−1 mussels) in our calculations and for com-
parison with other studies.
The two wild harvest studies only investigated gas use
during fishing operations and did not consider packaging,
the impact from boats used, or other infrastructure. Schau
et al. (2009) reported results as kg fuel kg−1 mollusk harvest-
ed, with a value of 0.09. Similarly, Thrane (2004) reported
results as 0.01-L fuel kg−1 mussels. We converted the L fuel
to kg fuel using the 0.832-kg-L1 value provided by the authors
for a value of 0.008-kg fuel kg−1 mussels. To convert the
values from Thrane (2004) and Schau et al. (2009) to kg
CO2-eq kg−1 harvest, we assumed the boats from those studies
had the same material and fuel use as auxiliary mussel rafts
(89.68 kg CO2 emitted and 28.29 kg diesel used t−1 harvest for
Thrane (2004)) and coastal trawlers (1662.12 kg CO2 emitted
and 524.33 kg diesel used t−1 harvest for Schau et al. (2009))
as those presented in Vázquez-Rowe et al. (2011). Using these
values, we estimated that both harvest vehicles produced
3.17 kg CO2-eq kg−1 diesel fuel used. We multiplied this value
by the previously estimated functional units in each study to
get estimates of kg CO2-eq kg−1 harvest. We calculated CO2
release to be 0.026 kg CO2-eq kg−1 harvest for Thrane (2004)
and 0.29 kg CO2-eq kg−1 harvest for Schau et al. (2009).
Multiple functional units were used in the previous studies, so
for consistency we converted all other functional units to 1-kg
AFDW tissue (Table 2). de Alvarenga et al. (2012) reported
550 g of shell and 450-g wet tissue per kg functional unit, while
Fry (2012) reported 160 kg of wet meat per every 840 kg of shell
for oysters and 609 kg of wet meat per 391-kg shell for mussels.
For the two wild harvest studies—Thrane (2004) and Schau et al.
(2009)—we assumed that wet meat made up 10% of the total
mass, as this is the same method Thrane (2004) used. In cases
where tissue and shell weight were not reported, they were
estimated using data from previous studies. Tissue and shell
weight for Mytilus edulis culture in Aubin and Fontaine (2014)
were estimated using the same values reported by Fry (2012),
and tissue and shell weight for Mytilus galloprovincialis in LCA
reported by Iribarren et al. (2010a) using values from Munari
et al. (2013) of 9.78 g per whole individual mussel, 45% of
which was wet tissue. Wet tissue weight was converted to
AFDW weight using Eq. (3), adapted from Hammen (1968):
WeightWetTissue þ 45:1
WeightDryTissue ¼ ð3Þ
84:29
The equation for conversion of wet to dry tissue does not
work for small units (i.e., < 10), so conversions were estimated
in gram, then converted back to kilogram. Reported kg CO2-
eq were modified to match the new functional unit of 1-kg
Int J Life Cycle Assess (2018) 23:1042–1048 1045

Table 2 Converted global warming impact data from past studies and estimated global warming impact associated with shell production. Functional
units from previous studies were converted to a standard functional unit of 1-kg ash-free dry tissue weight (AFDW)

Study Wet meat per Dry meat per Shell per Kg shell kg−1 Original kg CO2-eq Additional Percent
functional unit functional unit functional unit AFDW tissue kg−1 AFDW tissue kg CO2-eq release increase
(kg) (kg) (kg) from shell kg−1 in CO2-eq
AFDW (calculated) when shell
CO2 release
is included

de Alvarenga 0.45 0.06 0.55 9.2 188.5 2.4 1.3

et al. (2012)
Fry (2012)— 160 2.4 840 350 533.75 105.3 19.7
oyster
Aubin and 609 7.8 391 50.1 5.2 14.9 286.5
Fontaine
(2014)
Fry (2012)— 609 7.8 391 50.1 32.3 15.1 46.7
mussel
Iribarren et al. 40,380 479.6 49,357 103 80.1 29.3 36.6
(2010a)
Thrane (2004) 0.10 0.002 0.90 450 13 137.2 1055.4
Schau et al. 0.10 0.002 0.90 450 145 122.2 84.3
(2009)

AFDW tissue unit by dividing the reported global warming
impact value by the estimated quantity of AFDW tissue in the
original functional unit (Table 2). For the Iribarren et al.
(2010a) results, we did not use this conversion equation, in-
stead using the value of 0.69-g AFDW tissue per individual
mussel presented by Munari et al. (2013).
None of the studies investigated here reported site temper-
ature, salinity, or pH. To estimate Ψ for individual sites, these
values are needed. If the specific site location was identified,
we estimated the average annual water temperature using
www.seatemperature.org, then set pH equal to 8.1 and
salinity to 35 (Table 3). We selected these values as they rep-
resent the average pH and salinity of global oceans. We used
mean temperature as different temperatures provide different
temperatures yield different temperatures yield different
values for Ψ. If the site was not identified, we used a temper-
ature value of 20 °C. For all studies, we set the atmospheric
CO2 to 400 ppm. CO2 release from shell production was then
estimated using Eq. (1).
3 Results
reported CO2 release. Inclusion of shell CO2 release led to
much larger increases in the wild harvest studies than in the
cultured studies.
In the two oyster culture studies in Brazil and Scotland,
CO2 release from shell averaged 53.8 (± 72.8 SE) kg CO2
kg−1 AFDW, respectively. This large variation can mostly be
attributed to the large difference in tissue and shell per func-
tional unit reported in those two studies, as the other factor that
can yield differences in calculated CO2 release, Ψ, only dif-
fered by 0.09 between the study locations.
For the three mussel culture LCA, there was less variation
as shell was estimated to release an average of 19.8 (± 5.8 SE)
kg CO2 kg−1 AFDW. Comparatively, the mean CO2 release
from shell in the two LCA of wild harvest mussels was 129.7
(± 10.6 SE) kg CO2 kg−1 AFDW.
CO2-eq release in LCA of cultured oysters increased by an
average of 10.5% (± 13 SE), much less than the average in-
crease of 123.3% (± 100 SE) for cultured mussels. The only
cradle-to-grave LCA demonstrated the smallest increase at
1.3%. Cradle-to-gate studies of cultured bivalves demonstrat-
ed an average increase in the total kg CO2-eq kg−1 AFDW of
127% (± 73 SE).

When the shell CO2 release method was applied to the past
studies, CO2 release from shell production ranged from 2.4 to
137.2 kg CO2 kg−1 AFDW, and increased the total release of
CO2 reported in individual LCA from 1.3–1055% (Table 2).
There was large variability regarding the importance of in-
cluding CO2 release from shell production in wild harvest
LCA with a mean increase of 570% (± 687 standard error, or
SE), which can be attributed to the difference in the original
4 Discussion
Our results demonstrate that inclusion of CO2 released during
shell production yields large increases in the total kg CO2-eq
kg−1 AFDW in past LCA of bivalve production, indicating
that this source of CO2 release should be considered in future
LCA. The importance or magnitude to which inclusion of
1046
Table 3 Estimates of the ratio of
CO2 released per CaCO3 Study
precipitated (Ψ) for the LCA
considered in this study
de Alvarenga et al. (2012)
Fry (2012)
Aubin and Fontaine (2014)
Iribarren et al. (2010a)
Thrane (2004)
Schau et al. (2009)
a
Temperature values for two Scottish lochs in which mussels were raised from Karayücel and Karayücel (1999)
shell CO2 release increased the total CO2-eq per functional
unit varied widely. This variation can be attributed to the dif-
ference in harvest method, the ratio of shell to AFDW tissue,
and perhaps most importantly, the original reported kg CO2-eq
per functional unit in each study. Differences in site-specific Ψ
also contributed.
There was a marked difference in the meat to tissue ratio
between wild and cultured bivalves in the past studies we
investigated. While this may at first seem surprising, bivalves
raised in culture are able to put more energy toward growth
and less toward defense (shell), as farms are located in areas of
high food availability and farmers frequently clean the shells
of the bivalve to prevent damage from fouling organisms and
predators. These ideas are supported with data collected in
Chesapeake Bay, USA, where oysters raised in culture have
been shown to have five times less shell per gram of meat
compared to their wild counterparts (Higgins et al. 2011;
Newell et al. 2005). Species of bivalve with a low shell to
tissue ratio yield less CO2 from shell production than species
with high shell to tissue when kg AFDW tissue is used as the
functional unit. Farming bivalves with a lower shell to tissue
ratio could reduce the total CO2 release from the farming
operation if other factors such as equipment and gasoline
use remain the same. This suggests that bivalves raised in
culture could have lower total CO2 release associated with
their production than wild harvest, as the release of CO2 from
shell production in culture systems would be lower than in
wild harvest systems. To test this hypothesis, an LCA com-
paring wild harvest and aquaculture methods of bivalves is
needed.
Somewhat surprisingly, the inclusion of CO2 release from
shell production led to greater changes in the total kg CO2-eq
kg−1 AFDW in the LCA of cultured mussels (123.3%) than
cultured oysters (10.5%). As oysters generally have a higher
shell to AFDW ratio than mussels, we expected large in-
creases in CO2 release when including that produced during
shell production. We attribute this result to the higher initial
CO2 emissions per functional unit in the oyster studies. The
variation in shell to AFDW is also likely why the release of
CO2 from shell production was so small for the de Alvarenga
Int J Life Cycle Assess (2018) 23:1042–1048
Location Mean annual Calculated
temperature Ψ
(°C)
Florianopolis, Brazil 22.3 0.63
Scotland 11a 0.72
Mont-St.-Michel Bay, France 12.3 0.71
Galicia, Spain 16.0 0.68
Denmark 10.3 0.73
Not defined (Boutside of Norwegian waters^) 20 0.65
et al. (2012) cradle-to-gate study of cultured oysters. In that
study, the shell to AFDW ratio of was 9.2. However, if we
substitute the shell to AFDW from the other oyster culture
study of 350, the inclusion of CO2 from shell production leads
to a 56% increase in total kg CO2-eq kg−1 AFDW unit com-
pared to the 1.3% increase calculated.
In order to negate the CO2 release associated with shell pro-
duction, shell should be used as an alternative to other products
with a greater CO2 footprint. One such alternative is the use of
shell as an alternative to mined and milled limestone. de
Alvarenga et al. (2012) investigated the potential benefits of pro-
cessing waste oyster shell as an alternative to limestone. The
study demonstrated that while there was a slightly greater release
of CO2-eq by doing this (1885 kg CO2-eq kg−1 AFDW for
landfill compared to 1888 kg CO2-eq kg−1 AFDW for processing
to limestone), considering other impact categories and using
weighting factors designated by Eco-indicator 99, utilizing shell
as a resource was beneficial. The authors estimated that shell
could be transported up to 323 km for processing while main-
taining a lower overall environmental impact than extracting and
processing limestone. If CO2 release from shell production was
included in the Alvarenga et al. study (1862 CO2-eq kg−1 AFDW
if shell was returned to the water compared to 1911 CO2-eq kg−1
AFDW if shell is processed), the maximum transportation dis-
tance that could maintain an environmental benefit would de-
crease, but there would still be a benefit to replacing limestone
with discarded oyster shell. Iribarren et al. (2010b) also investi-
gated the use of mussel shell in industrial CaCO3 production in
Galicia, Spain. The results of that study suggest that the process-
ing of shell is more environmentally damaging than simply send-
ing the shell to a landfill, but creates a valuable commodity from
a waste product. Yoon et al. (2004) incorporated oyster shell into
cement at different ratios, and indicated shell could be a replace-
ment for quarried sand. Additionally, shells can be recycled to
restore lost estuarine habitats. In the Chesapeake Bay, USA, the
Oyster Recovery Partnership has collected over 100,000 bushels
of shell since 2010, and used that shell to create restored reefs
throughout the Chesapeake Bay in an attempt to restore valuable
ecosystem services (Oyster Recovery Partnership 2016). This
shell is used in place of poured concrete, which is frequently used
Int J Life Cycle Assess (2018) 23:1042–1048 1047

to create structure for reefs. Using crushed shell instead of poured

concrete to restore habitats likely has a lower overall release of
CO2 to the atmosphere.
While not as important as shell to AFDW ratio in total CO2
release from shell production, Ψ can be highly variable be-
tween sites, and will change with a changing climate and
ocean acidification. Temperature, salinity, pH, and pCO2 all
impact the amount of CO2 released during the production of
bivalve shells (Fig. 1) by altering Ψ. By using these variables,
we can optimize locations for restoration or aquaculture that
would maximize sequestration by reducing production of
CO2. As Ψ values decrease, CO2 released during shell produc-
tion also decreases. The lowest values of Ψ are associated with
higher salinity, temperature, and pH (Fig. 1). Climate change
predictions estimate a 3 °C rise in temperature (IPCC 2007),
salinity increases in highly saline areas and salinity decreases
for fresher areas (Durack et al. 2012), and a decrease in pH
from 8.1 to 7.8 by the end of the century (IPCC 2007).
Although increased temperatures would decrease Ψ values,
changes in salinity and pH would far outweigh temperature
effects, resulting in an overall increase in Ψ by at least 17%,
followed by increased release of CO2 during shell production.
Human-driven climate change has resulted in a global in-
crease in surface temperature of approximately + 0.2 °C per
decade since 1980 (Hansen et al. 2006). In coastal areas where Fig. 1 Changes in the ratio of CO2 released to CaCO3 precipitated (Ψ)
under changing temperature and salinity conditions associated with
bivalve culture is practiced, water temperatures have also in- global warming and salt water intrusion (a) when pCO2 is 400 ppm
creased rapidly. As an example, in Narragansett Bay, USA, and pH is 8.1, and b increased atmospheric CO2 concentrations and
water temperature increased 1.26 °C between 1959 and 2008 ocean acidification when temperature is 20 °C and salinity is 35. Values
(Melrose et al. 2009). If salinity (35), pH (8.1), and pCO2 over the lines in (a) indicate salinity, and values over the lines in (b)
indicate pH
(400 ppm) remained the same for this time period, with only
temperature changing, a bivalve shell would release 1% less
CO2:CaCO3 over its lifetime in 2008 than in 1959, with Ψ these approaches have a lower CO2 emission than the differ-
equal to 0.72 in 1958 (mean temperature 11.27 °C) and 0.71 ence in shell CO2 release between the salinities.
in 2008 (mean temperature 12.55 °C). While seeming small, While we used a pH value of 8.1 in this study, estuarine
this 1% change would yield large changes in shell production systems experience highly variable changes in pH on both
CO2 release at an ecosystem scale, or the scale of a bivalve daily and seasonal scales (Wallace et al. 2014), in addition to
aquaculture facility. the changes predicted by ocean acidification. These fluctua-
Aquaculture facilities could also be located in areas of tions can be driven by the decomposition of organic matter
higher salinity to target reducing CO2 emissions from shell due to loading of excess nutrients, or simple diel patterns of
production. If temperature (20 °C), pCO2 (400 ppm), and plankton photosynthesis and respiration. In Narragansett Bay,
pH (8.1) remain constant, Ψ is 0.65 when salinity is 35 and daily pH values have been demonstrated to vary between 8.5
0.74 when salinity is 20, a 14% increase at the lower salinity. and 7.9 (Nixon et al. 1976) and between 8.6 and 7.6 on an
While some bivalve species require specific salinities to grow, annual basis (Hinga 1992). The average pH value over the
others do not. Farm owners may also point to different taste of course of the bivalve’s life cycle is needed to calculate the
product based on the salinity that shellfish was raised in. We CO2 release from shell production. Thus, in a year of lower
suggest that species that are able to be survive in higher salin- pH, Ψ would be higher, and vice versa.
ity waters should be grown there to minimize shell CO2 re-
lease. If the farmers believe their product tastes best when
raised in a lower salinity, the shellfish could instead be grown 5 Conclusions
in saline water, then moved to a recirculating system managed
for the targeted salinity, or to a different site with lower salinity We developed and demonstrated a simple method for calcu-
for a few days before harvest to improve product taste while lating the CO2 released during bivalve shell production for use
maintaining a lower rate CO2 emission from shell, assuming in LCA. When we applied this approach to previous studies,
1048
we found that the amount of CO2 released during shell pro-
duction is significant and can lead to dramatic increases in
calculated kg CO2-eq per functional unit in bivalve LCA We
encourage that future LCA of bivalves include the CO2 re-
leased during shell production.
Acknowledgements We would like to thank Dr. Robinson BWally^
Fulweiler, who provided constructive and helpful suggestions that im-
proved the quality of this manuscript, as did feedback from several anon-
ymous reviewers. Kevin McLaren, Johnny Shockley, and Tal Petty pro-
vided tours of their oyster farms and provided guidance on the daily
operation and needs of shellfish culture operations. N. Ray was supported
on a Teaching Fellowship from Boston University and a Warren-McLeod
Graduate Fellowship from the Boston University Marine Program during
preparation of this manuscript.
References
Aubin J, Fontaine C (2014) Environmental impacts of producing bouchot
mussels in Mont-Saint-Michel Bay (France) using LCA with em-
phasis on potential climate change and eutrophication. In: Schenck
R, Huizenga D (eds) Proceedings of the 9th international conference
on life cycle assessment in the agri-food sector (LCA food 2014), 8–
10 October 2014, San Francisco, USA. ACLCA, Vashon
de Alvarenga RAF, Galindro BM, de Fátima HC, Soares SR (2012) The
recycling of oyster shells: an environmental analysis using life cycle
assessment. J Environ Manag 106:102–109
Durack PJ, Wijffels SE, Matear RJ (2012) Ocean salinities reveal strong
global water cycle intensification during 1950 to 2000. Sci 336:455–458
FAO (2002) The state of world fisheries and aquaculture 2002. Rome
FAO (2016) The state of world fisheries and aquaculture 2016. Rome
Filgueira R, Byron CJ, Comeau LA, Costa-Pierce B, Cranford PJ,
Ferreira JG, Grant J, Guyondet T, Jansen HM, Landry T,
McKindsey CW, Petersen JK, Reid GK, Robinson SMC, Smaal
A, Sonier R, Strand O, Strohmeier T (2015) An integrated ecosys-
tem approach for assessing the potential role of cultivated bivalve
shells as part of the carbon trading system. Mar Ecol Prog Ser 518:
281–287
Frankignoulle M, Canon C, Gattuso JP (1994) Marine calcification as a
source of carbon dioxide: positive feedback of increasing atmo-
spheric CO2. Limnol Oceanogr 39:458–462
Frankignoulle M, Pichon M, Gattuso JP (1995) Aquatic calcification as a
source of carbon dioxide. In: Beran MA (ed) Carbon sequestration
in the biosphere, NATO ASI series, vol 133. Springer-Verlag, New
York, pp 265–272
Fry JM (2012) Carbon footprint of Scottish suspended mussels and inter-
tidal oysters. Scottish Aquaculture Research Forum. http://www.
sarf.org.uk/cms-assets/documents/84294-350790.sarf078-final-
report—revised-oct2012. Accessed 5 Feb 2017.
Gattuso JP, Epitalon JM, Lavigne H, Orr J (2016) Seacarb: seawater
carbonate chemistry. R package version 3.1.1. http://CRAN.R-
project.org/package=seacarb
Goedkoop M, Spriensma R (2001) The Eco-indicator 99: a damage ori-
ented method for life cycle impact assessment: methodology annex.
Accessed online: http://www.pre-sustainability.com/download/
EI99_annexe_v3.pdf
Goulletquer P, Wolowicz M (1989) The shell of Cardium edule, Cardium
glaucum, and Ruditapes philippinarum: organic content,
Int J Life Cycle Assess (2018) 23:1042–1048
composition, and energy value, as determined by different methods.
J Mar Biol Assoc UK 69:563–572
Hammen CS (1968) Aminotransferase activities and amino acid excre-
tion of bivalve mollusks and brachiopods. Comp Biochem Physiol
26:697–705
Hansen J, Sato M, Ruedy R, Lo K, Lea DW, Medina-Elizade M (2006)
Global temperature change. Proc Natl Acad Sci 103:14288–14293
Higgins CB, Stephenson K, Brown BL (2011) Nutrient bioassimilation
capacity of aquacultured oysters: quantification of an ecosystem
service. J Environ Qual 40:271–277
Hinga KR (1992) Co-occurrence of dinoflagellate blooms and high pH in
marine enclosures. Mar Ecol Prog Ser 86:181–181
IPCC (2007) Climate change 2007: the physical science basis.
Contribution of working group I to the fourth assessment report of
the intergovernmental panel on climate change: Solomon S, Qin D,
Manning M, Chen Z, Marquis M, Averyt KB, Tignor M and Miller
HL (eds) Cambridge University Press, Cambridge, United Kingdom
and New York, NY, USA
Iribarren D, Moreira MT, Feijoo G (2010a) Life cycle assessment of fresh
and canned mussel processing and consumption in Galicia (NW
Spain). Resour Conserv Recycl 55:106–117
Iribarren D, Moreira MT, Feijoo G (2010b) Implementing by-product
management into the life cycle assessment of the mussel sector.
Resour Conserv Recycl 54:1219–1230
Karayücel S, Karayücel İ (1999) Growth and mortality of mussels
(Mytilus edulis) reared in lantern nets in Loch Kishorn, Scotland.
Turk J Vet Anim Sci 23:397–402
Melrose DC, Berman MS, Smith LM, Oviatt CA (2009) The ecological
effects of climate change on the Narragansett Bay estuary. ICES
Conference Manuscript, 2009
Munari C, Rossetti E, Mistri M (2013) Shell formation in cultivated
bivalves cannot be part of carbon trading systems: a study case with
Mytilus galloprovincialis. Mar Environ Res 92:264–267
Newell RIE, Fisher TR, Holyoke RR, Cornwell JC (2005) Influence of
eastern oysters on nitrogen and phosphorus regeneration in
Chesapeake Bay, USA. In: Dame R, Olenin S (ed) The comparative
roles of suspension feeders in ecosystems. Vol. 47, NATO Science
Series IV: Earth and Environmental Sciences. Springer,
The Netherlands
Nixon SW, Oviatt CA, Garber J, Lee V (1976) Diel metabolism and
nutrient dynamics in a salt marsh embayment. Ecol 57:740–750
Oyster Recovery Partnership (2016) 2016 Impact Report. Accessed on-
line: https://oysterrecovery.org/wp-content/uploads/2017/02/ORP_
2016_ImpactReport.pdf
Schau EM, Ellingsen H, Endal A, Aanondsen SA (2009) Energy con-
sumption in the Norwegian fisheries. J Clean Prod 17:325–334
Thrane M (2004) Energy consumption in the Danish fishery: identifica-
tion of key factors. J Ind Ecol 8:223–239
Vázquez-Rowe I, Iribarren D, Hospido A, Moreira MT, Feijoo G (2011)
Computation of operational and environmental benchmarks within
selected Galician fishing fleets. J Ind Ecol 15:776–795
Wallace RB, Baumann H, Grear JS, Aller RC, Gobler CJ (2014) Coastal
ocean acidification: the other eutrophication problem. Estuar Coast
Shelf Sci 148:1–13
Ware JR, Smith SV, Reaka-Kudla ML (1992) Coral reefs: sources or sinks
of atmospheric CO2? Coral Reefs 11:127–130
Yoon GL, Kim BT, Kim BO, Han SH (2003) Chemical-mechanical char-
acteristics of crushed oyster-shell. Waste Manag 23:825–834
Yoon H, Park S, Lee K, Park J (2004) Oyster shell as substitute for
aggregate in mortar. Waste Manag Res 22:158–170