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Stage-Specific Changes in Physiological and Life-History Responses to Elevated Temperature and PCO2 during the Larval Development of the European Lobster Homarus gammarus (L.)

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An organism’s physiological processes form the link between its life-history traits and the prevailing environmental conditions, especially in species with complex life cycles. Understanding how these processes respond to changing environmental conditions, thereby affecting organismal development, is critical if we are to predict the biological implications of current and future global climate change. However, much of our knowledge is derived from adults or single developmental stages. Consequently, we inves- tigated the metabolic rate, organic content, carapace minerali- zation, growth, and survival across each larval stage of the Eu- ropean lobster Homarus gammarus, reared under current and predicted future ocean warming and acidification scenarios. Lar- vae exhibited stage-specific changes in the temperature sensitivity of their metabolic rate. Elevated PCO2 increased C∶N ratios and interacted with elevated temperature to affect carapace mineral- ization. These changes were linked to concomitant changes in sur- vivorship and growth, from which it was concluded that bottle- necks were evident during H. gammarus larval development in stages I and IV, the transition phases between the embryonic and pelagic larval stages and between the larval and megalopa stages, respectively. We therefore suggest that natural changes in optimum temperature during ontogeny will be key to larvae sur- vival in a future warmer ocean. The interactions of these natu- ral changes with elevated temperature and PCO2 significantly alter physiological condition and body size of the last larval stage be- fore the transition from a planktonic to a benthic life style. Thus, living and growing in warm, hypercapnic waters could com- promise larval lobster growth, development, and recruitment.
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Division of Comparative Physiology and Biochemistry, Society for Integrative and
Comparative Biology
Stage-Specific Changes in Physiological and Life-History Responses to Elevated Temperature
and Pco2 during the Larval Development of the European Lobster Homarus gammarus (L.)
Author(s): Daniel P. Small, Piero Calosi, Dominic Boothroyd, Steve Widdicombe and John I.
Spicer
Source:
Physiological and Biochemical Zoology,
(-Not available-), p. 000
Published by: The University of Chicago Press. Sponsored by the Division of Comparative
Physiology and Biochemistry, Society for Integrative and Comparative Biology
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Stage-Specic Changes in Physiological and Life-History Responses
to Elevated Temperature and PCO
2
during the Larval Development
of the European Lobster Homarus gammarus (L.)
Daniel P. Small
1,2,3,4,
*
Piero Calosi
2,5
Dominic Boothroyd
3
Steve Widdicombe
4
John I. Spicer
2
1
Biology Department, St. Francis Xavier University, 2320
Notre Dame Avenue, Antigonish, Nova Scotia B2G 2W5,
Canada;
2
Marine Biology and Ecology Research Centre,
School of Marine Science and Engineering, Davy Building,
Plymouth University, Drake Circus, Plymouth, Devon, PL4
8AA, United Kingdom;
3
National Lobster Hatchery, South
Quay, Padstow, Cornwall, PL28 8BL, United Kingdom;
4
Plymouth Marine Laboratory, Prospect Place, West Hoe,
Plymouth, PL1 3DH, United Kingdom;
5
Département de
Biologie, Chimie et Géographie, Université du Québec à
Rimouski, 300 Allée des Ursulines, Rimouski, Quebec G5L
3A1, Canada
Accepted 5/8/2015; Electronically Published 6/11/2015
ABSTRACT
An organisms physiological processes form the link between its
life-history traits and the prevailing environmental conditions,
especially in species with complex life cycles. Understanding how
these processes respond to changing environmental conditions,
thereby affecting organismal development, is critical if we are to
predict the biological implications of current and future global
climate change. However, much of our knowledge is derived from
adults or single developmental stages. Consequently, we inves-
tigated the metabolic rate, organic content, carapace minerali-
zation, growth, and survival across each larval stage of the Eu-
ropean lobster Homarus gammarus, reared under current and
predicted future ocean warming and acidication scenarios. Lar-
vae exhibited stage-specic changes in the temperature sensitivity
of their metabolic rate. Elevated PCO
2
increased CN ratios and
interacted with elevated temperature to affect carapace mineral-
ization. These changes were linked to concomitant changes in sur-
vivorship and growth, from which it was concluded that bottle-
necks were evident during H. gammarus larval development in
stages I and IV, the transition phases between the embryonic
and pelagic larval stages and between the larval and megalopa
stages, respectively. We therefore suggest that natural changes in
optimum temperature during ontogeny will be key to larvae sur-
vival in a future warmer ocean. The interactions of these natu-
ral changes with elevated temperature and PCO
2
signicantly alter
physiological condition and body size of the last larval stage be-
fore the transition from a planktonic to a benthic life style. Thus,
living and growing in warm, hypercapnic waters could com-
promise larval lobster growth, development, and recruitment.
Keywords: Homarus gammarus, ocean warming, ocean acid-
ication, life history, larval development, seafood.
Introduction
The persistence of marine species with complex life histories
requires the successful completion of all ontogenetic stages at
local and global scales (Byrne 2012). Changes in life-history traits
and subsequent population dynamics of such species can be
linked to the environment via physiological processes (Calow
and Forbes 1998; Ricklefs and Wikelski 2002; Young et al. 2006).
Two major climate-related issues are the rapid increase in global
mean values for sea surface temperature and rising levels of oce-
anic PCO
2
. By 2100, ocean surface temperatures are predicted to
have increased by between 37and 57C (Sokolov et al. 2009; IPCC
2013), while atmospheric PCO
2
levels are predicted to increase
to 1,000 matm from their preindustrial levels of 280 matm,
driving a reduction in oceanic pH of approximately 0.4 units
(Caldeira and Wickett 2003, 2005; IPCC 2013). Coupled with
decreasing pH are changes to other ocean carbonate-chemistry
parameters, such as dissolved inorganic carbon and carbonate
saturation states (Feely et al. 2004). Understanding the phys-
iological responses underpinning changes to life-history traits
due to complex climate change is critical if we are to link or-
ganismal and population responses to such change (Pörtner
2010). This is also important if we are to subsequently provide
guidelines for stakeholders and policymakers to successfully
deliver sound stock management and species conservation
strategies (Wikelski and Cooke 2006; Young et al. 2006). De-
spite the urgent need for a good understanding of the physi-
ological processes underlying and mediating responses of ma-
rine larvae to climate-change drivers, physiological traits are
understudied compared with more conventional life-history
*Corresponding author; e-mail: dsmall@stfx.ca.
Physiological and Biochemical Zoology 88(5):000000. 2015. q2015 by The
University of Chicago. All rights reserved. 1522-2152/2015/8805-5009$15.00.
DOI: 10.1086/682238
000
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traits (such as growth and survivorship), particularly in marine
crustaceans (Whiteley 2011).
Temperature is a major driver of crustacean larval devel-
opment (e.g., Lindley 1998; Hartnoll 2001; Daoud et al. 2010)
and is largely responsible for determining development time,
survival, and size at maturity (Atkinson 1995; Weiss et al. 2010).
Maximum larval growth and survival occur at optimum tem-
peratures (Sastry and McCarthy 1973), which in the American
lobster Homarus americanus was estimated to be around 187C,
as growth and survival decreased above or below 187C (Mac-
Kenzie 1988). The underlying physiological responses to elevated
temperature in crustacean larvae are, comparatively speaking,
poorly studied. Larval respiration rates increase with increasing
temperature up to a maximum value, beyond which respiratory
gas exchange is compromised (Schatzlein and Costlow 1978;
Vernberg et al. 1981; Anger 1987). At this point larvae exhibit
oxygen- and capacity-limited thermal tolerance similar to that of
adults (Storch et al. 2009a, 2009b). However, both the ontogeny
of aerobic scope and metabolic rates during larval development
are still largely unknown. Given that the development of optimal
thermal windows denes, in part, a speciesbiogeographic ranges
(Pörtner 2001), this understanding is critical if we are to predict
the effects of ocean warming on species distributions and pop-
ulation dynamics (e.g., Storch et al. 2009a, 2009b, 2011; Bartolini
et al. 2013).
In addition to changes in temperature, elevated PCO
2
elicits a
range of life-history responses in larval crustaceans, including
increased mortality (e.g., Kurihara et al. 2004; Walther et al.
2010; Long et al. 2013), reduced survival or growth (e.g., Kuri-
hara et al. 2008; Walther et al. 2010), and little or no effect
(Arnold et al. 2009; Arnberg et al. 2013; Carter et al. 2013;
Ceballos-Osuna et al. 2013). Some studies have revealed subtle,
but important, effects of PCO
2
on larval organic content and
mineralization, metabolism, and energetic trade-offs between
physiological processes (e.g., Arnold et al. 2009; Carter et al.
2013; Ceballos-Osuna et al. 2013; Schiffer et al. 2013). However,
with the exception of Arnold et al. (2009) and Arnberg et al.
(2013), these studies mainly focus on specic larval stages and
may therefore miss changes in sensitivity to elevated PCO
2
due
to ontogenetic shifts in physiological functions between stages,
which may ultimately drive the responses of later larval stages
to climate change (Byrne 2012; Dupont et al. 2013).
While our understanding of the independent effects of
warming and ocean acidication on the physiology of marine in-
vertebrateslarvae is rapidly growing, their co-occurrence in the
future ocean makes it imperative to study their potential impact
when coupled (Pörtner and Farrell 2008; Widdicombe and Spicer
2008). This is particularly relevant because elevated PCO
2
has
been shown to increase an organisms sensitivity to elevated
temperatures via narrowing of its aerobic thermal windows
(Metzger et al. 2007; Pörtner and Farrell 2008). More specically,
Walther et al. (2010, 2011) explicitly related larval sensitivities
to elevated temperature and PCO
2
to their physiological devel-
opment, showing that changes in aerobic thermal windows dur-
ing larval development may cause stage-specic bottlenecks. The
potential for further stage-specic bottlenecks and potential car-
ryover effects between larval stages is still largely undetermined
(cf. Dupont et al. 2013), despite the importance of such bottle-
necks in determining population viability (Byrne 2012).
The aim of this study was to investigate individual-larval-
stage responses, in terms of both physiological and life-history
traits, to both elevated temperature and elevated PCO
2
through-
out larval development of the European lobster Homarus gam-
marus. This species was chosen because of its complex life cycle,
which includes dispersive larval stages and dramatic behavioral,
anatomical, physiological, and environmental transitions be-
tween pelagic larvae and benthic juveniles (Gruffydd et al. 1975;
Cobb and Wahle 1994; Cobb and Castro 2006). After hatching,
H. gammarus undergo four larval molts, with the rst three larval
stages, SISIII, being fully pelagic. SI is an important transitional
stage between benthic embryos and pelagic larvae. The onset of
the fourth stage, SIV, marks the transition from pelagic larvae to
semipelagic, benthic-seeking megalopa.Upon settlement, the SIV
megalopa metamorphoses into the rst true benthic postlarval
stage, SV (Charmantier et al. 1991; Cobb and Wahle 1994). In
addition to the complexity of its life cycle, H. gammarus is of
great economic importance for many shing communities in
Europe, with an estimated 4,625 t landed during 2012 (FAO
2014). Its geographic range extends from north of the Arctic
Circle and along the European and Mediterranean coasts as
far south as Morocco (Cobb and Wahle 1994; Cobb and Castro
2006). Owing to its economic importance, any potential changes
in local population distribution or condition due to the pre-
dicted elevated temperature and PCO
2
levels associated with
climate change would have serious socioeconomic effects on
local inshore sheries.
In order to assess the potential effect of combined global drivers
on the physiological development and survival of H. gammarus,
larvae were reared under predicted future scenarios of both
ocean warming (Sokolov et al. 2009; IPCC 2013) and acidica-
tion (Caldeira and Wickett 2003, 2005; IPCC 2013). Rates of ox-
ygen consumption were measured as an indicator of energy de-
mand, while organic content and carapace mineralization were
measured as indices of larval condition. Growth, in terms of wet
body mass, selected morphometrics, and survival were measured
as indices of key life-history traits. Measurement of all of these
key aspects of lobster biology at each developmental stage will
enable us to see how physiological changes occurring between
larval stages help dene the way in which life-history traits at
the subsequent stage of development will respond to environ-
mental drivers.
Material and Methods
Animal Husbandry
Ovigerous females were caught off the coast of south Cornwall
in July 2011 and kept in an aquarium (1,200 L) at the National
Lobster Hatchery (Padstow, UK), with seawater sourced from
the nearby Camel Estuary (Padstow; 5073219.67N, 4756
5.85W). Stock seawater was mechanically and biologically l-
tered and subjected to weekly water changes (salinity p35, Tp
197C, dissolved oxygen p8mgL
21
). Females were fed twice
000 D.P.Small,P.Calosi,D.Boothroyd,S.Widdicombe,andJ.I.Spicer
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a week on whole mussels ad lib. Newly hatched larvae (SI,
Np4,160) were removed within 6 h of hatching with a sieve
(0.5 #0.5-mm square mesh). They were transferred to a large
rearing cone (75 L) lled with constantly aerated seawater con-
taining N-chloro tosylamide (2 mg L
21
) to prevent bacterial in-
fection. Larvae were treated in this water for 60 min before being
transferred, again with a sieve, to the experimental system de-
scribed below.
Experimental Setup
The experimental system (g. A1) consisted of six aquaria (20 L),
each containing six rearing cones (2 L). Each cone was supplied
with recirculating seawater (ow rate p10 mL min
21
), the water
having been subjected to mechanical and biological ltering. Of
the six aquaria, three were designated haphazardly to the control-
temperature condition and three to the elevated-temperature
condition.
Control temperature was chosen as nominal 177C to represent
the seasonal average for southwest Cornwall, and elevated tem-
perature was designated as a nominal 217C to represent the 47C
increase associated with ocean warming predicted for the end of
this century (Sokolov et al.2009; IPCC 2013). The temperature of
the water owing to the cones was controlled by a water chiller
with heating elements (SeaChill TR10, TECO, Ravenna, Italy),
and water outow into the aquaria acted as a water bath to pro-
vide stable experimental temperatures. Each cone had a mesh
(0.5 mm
2
square) on the outow, which allowed the removal of
small, broken-down food waste but the retention of larger food
particles and the larvae themselves. To ensure good water quality,
the system was ushed with fresh seawater (ow rate p10 mL
min
21
) for 8 h each day.
Within each aquarium, three of the six cones were desig-
nated control PCO
2
(420 matm) and the other three designated
elevated PCO
2
(1,100 matm). Each cone was constantly aerated,
and equilibration of sea water with the desired level of PCO
2
was achieved by bubbling an appropriate gas mixture into the
water contained in each cone. Control PCO
2
was produced by
bubbling untreated air into the seawater contained in three of
the six cones in each aquarium. Elevated PCO
2
was achieved by
following the method of Findlay et al. (2008), in which CO
2
-
enriched air was injected into the seawater in the remaining
six cones in each aquarium. Levels of PCO
2
in the air supplied
to acidied cones were measured continuously throughout the
exposure period with a CO
2
gas analyzer (Li-820, Li-Cor Bio-
sciences, Lincoln, NE).
Water chemistry was monitored daily. Measurements of pH
(National Bureau of Standards scale) were obtained with a pH
electrode (HI-1210B/5, Hanna Instruments, Leighton Buzzard,
UK) connected to a handheld pH meter (HI-98160, Hanna In-
struments) that was calibrated daily with pH buffer standards
(Mettler-Toledo, Leicester, UK). Temperature was measured
with a thermocouple (HH802U, Omega Engineering, Stamford,
CT), and salinity was measured with a refractometer (S/Mill
hand refractometer, Atago, Tokyo). Seawater samples (250 mL)
were taken every 5 d, xed with HgCl
2
(0.02%) to eliminate
microbial activity (Riebesell et al. 2010), stored in borosilicate
asks (250 mL), and maintained in dark and dry conditions
until total alkalinity (A
T
) was determined with an alkalinity ti-
trator (As-Alk2, Apollo SciTech, Bogart, GA). Carbonate-system
parameters of PCO
2
(matm), total carbon dioxide (TCO
2
,mmol
kg
21
), bicarbonate concentration (HCO
3
2
,mmol kg
21
), carbon-
ate concentration (CO
3
22
,mmol kg
21
), calcite saturation (Ω
ca
), and
aragonite saturation (Ω
ara
) were calculated from A
T
,pH,tempera-
ture, and salinity with the CO
2
SYS program (Lewis and Wallace
1998), with constants provided by Mehrbach et al. (1973) and
retted by Dickson and Millero (1987) and KSO
4
constants from
Dickson (1990). Water-chemistry parameters for all treatments
during the exposure period are presented in table 1.
Table 1: Water-chemistry parameters recorded in control and experimental seawaters over the experimental period
177C217C
420 matm 1,100 matm 420 matm 1,100 matm
Temperature (7C) 17.2 5.03
A
17.2 5.03
A
21.3 5.03
B
21.3 5.03
B
Salinity 33.0 5.01
A
33.0 5.01
A
33.1 5.02
B
33.1 5.02
B
pH 8.08 5.01
A
7.73 5.01
B
8.11 5.01
A
7.76 5.01
B
A
T
(mEq kg
21
)
a
2.17 5.04 2.18 5.04 2.22 5.03 2.23 5.03
PCO
2
(matm)
a
454 511
A
1,154 517
B
426 511
A
1,181 536
B
TCO
2
(mmol kg
21
)
a
1,981 542
A
2,121 534
B
1,987 520
A
2,154 527
B
HCO
3
2
(mmol kg
21
)
a
1,829 540
A
2,015 532
B
1,806 517
A
2,039 526
B
CO
3
22
(mmol kg
21
)
a
135 51.6
A
65 51.5
B
167 54.9
C
76 51.3
B
Ω
cala
3.26 5.04
A
1.57 5.04
B
4.06 5.12
C
1.87 5.03
B
Ω
araa
2.10 5.03
A
1.01 5.02
B
2.60 5.08
C
1.25 5.02
D
Note. Data are means 5SE for all environmental parameters measured throughout the exposure period. For pH, the National Bureau of Standards
scale was used. A
T
ptotal alkalinity. PCO
2
pcarbon dioxide partial pressure. TCO
2
ptotal carbon dioxide. HCO
3
2
pbicarbonate concentration. CO
3
22
p
carbonate concentration. Ω
cal
pcalcite saturation. Ω
ara
paragonite saturation. Superscript capital letters indicate signicant differences between treatments.
a
Parameters calculated with the CO
2
SYS program (Lewis and Wallace 1998), with constants provided by Mehrbach et al. (1973) and retted by
Dickson and Millero (1987) and KSO
4
constants from Dickson (1990).
Lobster Larvae Vulnerability to Ocean Change 000
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Determination of Survivorship
The number of live individuals in each cone at each intermolt
period was counted, and cumulative survival was expressed as
the percentage of the number of individuals introduced into
the cone at day 0. This also took into account individuals re-
moved (and not replaced) for measurements. Survival was also
expressed as the percentage of individuals present in each cone
during the previous stage, to capture stage-specic changes in
survivorship.
Estimation of Metabolic Rate
Therateofoxygenconsumption(asaproxyformetabolic
rate) for one individual from each cone (Np9 per treatment)
at each intermolt period was measured, following closely the
semiclosed-respirometry method of Spicer and Eriksson (2003).
Individuals were placed in blacked-out respiration chambers
(40 mL) containing ltered seawater at the same temperature
and PCO
2
as the individual had been exposed to during the
experiment. Individuals were left in open chambers to adjust
and recover from handling for 30 min before oxygen mea-
surements were made. Determination of rates of oxygen con-
sumption was carried out over a 120-min period for SISIII and
over a 90-min period for SIV. Preliminary trials indicated that
the time individuals were left recovering in open chambers be-
fore the rst measurement did not signicantly affect rates of
oxygen consumption, and random blanks showed negligible
background changes in PO
2
and therefore negligible background
microbial respiration. Oxygen concentration (percent) was mea-
sured at the beginning and end of the incubation period with
an oxygen electrode (1302, Strathkelvin Instruments, Glasgow,
UK) housed in a temperature-controlled chamber (TC50, Strath-
kelvin Instruments) coupled to an oxygen meter (781, Strath-
kelvin Instruments). Rates of oxygen consumption were calcu-
lated from the decline in oxygen concentration per unit time
per body mass unit in the respirometer with oxygen solubility
coefcients obtained from Green and Carritt (1967) and are ex-
pressed as mmol O
2
min
21
g wet mass
21
at STP.
Determination of Growth and Morphometrics
Two individuals at each intermolt period were removed from
each cone (Np18 per treatment). Excess water was removed
by gently blotting individuals with ne tissue paper before wet
body mass (WBM, mg) was measured with a precision balance
(3719MP, Sartorius, Göttingen, Germany; dp0.1 mg). After
weighing, all individuals were laid straight and at on their right-
hand side to be photographed with a macro-enabled digital cam-
era (Powershot A710 IS, Canon, Reigate, UK). Photographs were
analyzed with ImageJ software (Rasband WS, US National In-
stitutes of Health, Bethesda, MD) to obtain measurements of total
body length (tip of rostrum to end of uropods), carapace length
(CL: rear of eye socket to rear of carapace), abdomen length (AL:
front of rst abdominal segment to rear of fth abdominal seg-
ment), rostrum length (tip of rostrum to rear of eye socket), and
chelae length (tip to base of cheliped propodus). Individuals were
then rinsed with ultrapure water, carefully blotted dry with tissue
paper, and frozen at Tp2207C for subsequent determination
of organic content and carapace mineralization.
Determination of Organic Content
The organic content (carbon, hydrogen, and nitrogen, i.e.,
CHN levels) of larval Homarus gammarus at each intermolt
stage was analyzed in one individual from each cone (Np9
per treatment). Individuals were freeze-dried and weighed with
a high-precision balance (AT201, Mettler-Toledo; dp0.01 mg).
If dry mass was !2.5 mg, the complete individual was placed in
a tin cup (diameter p2 mm, height p5 mm) and crushed. If
dry mass was 12.5 mg, the individual was ground into a uniform
powder with a mortar and pestle, and a 2-mg subsample was
removed and placed in a tin cup. Dried and powdered samples
were analyzed with an elemental microanalyzer (EA1110 CHNS,
Carlo Erba, Italy, modied by Elemental Analysis, Okehampton,
UK).
Determination of Carapace Mineral Content
Carapace mineral content was determined in larvae at each in-
termolt stage in one individual per cone (Np9 per treatment).
Each carapace was carefully removed with ne forceps and me-
ticulously cleaned of all tissue under low-power magnication
(#1050, SZXI6 binocular microscope, Olympus, Tokyo). Each
individual carapace was then weighed with a high-precision bal-
ance (AT201, Mettler-Toledo; dp0.01 mg) before being freeze-
dried for 24 h (Modulyo freeze drier, Thermo Electron, Wal-
tham, MA) at 2507C. The dry mass of each freeze-dried carapace
was determined with a high-precision balance (AT201, Mettler-
Toledo; dp0.01 mg) before being digested in 2 mL nitric acid
(79% concentration, trace analysis grade) in a microwave di-
gestion unit (MarsXpress, CEM, Matthews, NC). Digests were
thendilutedto10mLwithultrapurewaterandanalyzedfor
[Ca
21
], [Mg
21
], and [Sr
21
] with an ICP-Optical Emission Spec-
trometer (Varian 725-ES, Agilent Technologies, Santa Clara,
CA). Carapace mineral content is expressed as mmol mg
21
(cara-
pace dry mass).
Statistical Analysis
Data were rst tested for the assumption of normal distribu-
tions with a Kolmogorov-Smirnov test and then tested for
homogeneity of the variances with Levenes test. When assump-
tions were not met, residuals were analyzed against treatment
to determine how much residual variation was not due to
the assigned treatment. In all cases, no signicant relationship
between the factors investigated and residuals was found (P
0.05). A two-way ANCOVA with WBM as a covariant was per-
formed to analyze the effects of temperature, PCO
2
, and their
interactions on all measurements made at each intermolt stage.
Differences between treatments were determined by estimated
marginal means. WBM had no signicant effect on any param-
000 D.P.Small,P.Calosi,D.Boothroyd,S.Widdicombe,andJ.I.Spicer
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eters measured throughout larval development (P0.05) and
was therefore removed from subsequent analysis. The variable
tankwas included in all analyses as a random factor. There
was a signicant effect of tank at SI. Removing tank 1 from the
analysis resulted in the effect of tank no longer being statistically
signicant, yet all other results remained the same. It was con-
cluded that, while signicant, tank 1 had no effect on the overall
analysis. In all other cases, the variable tank was found not to be
signicant, and it was thus removed from analysis.
Results
Survivorship
Cumulative survival to SIV of Homarus gammarus larvae
reared under control PCO
2
was 2.18% at Tp217C, compared
to 0.56% at Tp177C, this difference in survival being signif-
icant (F1, 35 p36.029, P<0.001; table 2). No signicant effect
of elevated PCO
2
on cumulative survival was detected (P0.05).
When survival was considered as relative percent change from
the previous developmental stage (g. 1), survival of larvae from
SI to SII signicantly decreased at the higher temperature at
both PCO
2
levels (F1, 35 p25.911, P<0.001; g. 1) and higher
PCO
2
, but only at Tp177C(F1, 35 p4.960, Pp0.033; g. 1).
There were no further signicant effects of elevated PCO
2
on
survival from the previous developmental larval stage of H.
gammarus (P0.05; g. 1). Survival from SII to SIII and from
SIII to SIV was signicantly greater at the elevated temperature
(Tp217C; Fmin 1, 35 p6.107, Pp0.026; g. 1). There were no
signicant effects of the interactions between elevated tem-
perature and PCO
2
on survival throughout larval development
(P0.05; g. 1).
Growth and Morphometrics
Under control conditions, WBM between SI and SIV increased
from 12.6 50.4 to 51.3 51.5 mg, while CL and AL increased
Table 2: Selected life-history traits, survival, and growth of Homarus gammarus throughout larval development
under elevated temperature and PCO
2
177C217C
420 matm 1,100 matm 420 matm 1,100 matm
Cumulative survival (%):
Stage II 72.9
A
64.2
B
57.5
C
55.8
C
Stage III 11.0 9.1 12.9 12.4
Stage IV .6
A
.6
A
2.1
B
2.2
B
Duration (d):
Stage I 4.0 5.0 4.0 5.0 3.0 5.0 3.0 5.0
Stage II 6.7 5.1 6.6 5.2 5.0 5.0 5.0 5.0
Stage III 13.8 51.7
A
14.2 51.7
A
8.2 5.3
B
7.4 5.2
B
Total 24.6 24.9 16.2 15.4
Wet body mass (mg):
Stage I 12.6 5.4 12.6 5.3 12.8 5.3 12.7 5.3
Stage II 21.4 5.4 21.9 5.4 22.3 5.4 22.7 5.5
Stage III 31.6 51.0 31.8 51.0 31.9 51.0 32.2 51.2
Stage IV 51.3 51.5
A
50.4 51.6
A
44.5 51.4
B
45.6 51.6
B
Total length (mm):
Stage I 8.05 5.10 7.99 5.11 7.95 5.14 8.25 5.15
Stage II 9.84 5.12 9.97 5.14 10.18 5.10 10.43 5.09
Stage III 11.36 5.16 11.61 5.20 11.30 5.13 11.60 5.18
Stage IV 13.31 5.36
A
13.20 5.39
A
12.15 5.16
B
12.42 5.16
B
Carapace length (mm):
Stage I 2.86 5.05 2.83 5.05 2.82 5.06 2.88 5.06
Stage II 3.73 5.45 3.82 5.07 3.82 5.03 4.04 5.08
Stage III 4.62 5.07 4.68 5.09 4.73 5.08 4.83 5.08
Stage IV 5.41 5.11
A
5.23 5.11
A
4.80 5.08
B
4.90 5.07
B
Abdomen length (mm):
Stage I 5.19 5.08 5.16 5.08 5.13 5.09 5.37 5.10
Stage II 6.11 5.11 6.15 5.10 6.37 5.09 6.38 5.08
Stage III 6.73 5.11 6.92 5.14 6.57 5.07 6.77 5.11
Stage IV 7.90 5.26
A
7.97 5.28
A
7.34 5.10
B
7.52 5.11
B
Note. Data are presented as means 5SE. Superscript letters represent signicant differences between treatments.
Lobster Larvae Vulnerability to Ocean Change 000
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from 2.86 50.05 to 5.41 50.11 mm and from 5.19 50.08 to
7.90 50.26 mm, respectively (table 2). There were no signif-
icant effects of elevated temperature or PCO
2
, in isolation or
in consort, on WBM, CL, or AL of SI, SII, or SIII individuals
(P0.05). At SIV, WBM, CL, and AL were all signicantly
higher at Tp177C than at Tp217C(Fmin 1,57 p2.391, Pmax p
0.014; g. 2). There was no signicant effect of elevated PCO
2
,
in isolation or in consort with elevated temperature, on SIV
WBM, CL, or AL (P0.05). Finally, there were no visible signs
of abnormal development due to elevated temperature or PCO
2
noted during the exposure period.
Rates of Oxygen Consumption
Rates of oxygen consumption under control conditions de-
creased from 0.42 50.03 to 0.28 50.02 mmol min
21
g
21
(STP) between SI and SIV. There were no signicant effects
of interactions between elevated temperature and PCO
2
on the
rates of oxygen consumption at any stage of larval develop-
ment (P0.05). There were signicant effects of elevated tem-
perature and PCO
2
in isolation, which we discuss stage by stage.
At SI, rates of oxygen consumption were signicantly lower at
Tp217C than at Tp177C(F1, 31 p9.930, P<0.0001; g. 3),
with no signicant effect of elevated PCO
2
(P0.05). At SII
and SIII, rates of oxygen consumption were signicantly higher
at Tp217C than at Tp177C(Fmin 1, 31 p25.793, P<0.0001;
g. 3). There were, again, no signicant effects of elevated PCO
2
on the rates of oxygen consumption at SII or SIII (P0.05).
At SIV, the rates of oxygen consumption were signicantly
higher at 1,100 matm PCO
2
than at 420 matm PCO
2
(F1, 30 p4.550,
Pp0.042; g. 4d), with no signicant effect of elevated tem-
perature (P0.05; g. 3).
Organic Content
Dry mass (DM, percent of WBM) of larval H. gammarus reared
under control conditions ranged from 17.25% 50.33% at SI
Figure 1. Survival of larval Homarus gammarus of each developmental stage under elevated temperature and PCO
2
(means 5SE); survival
is expressed as percentage of live individuals from the previous developmental stage. a, Stage II; b, stage III; c, stage IV. White bars represent
177C, and gray bars represent 217C. Open bars represent 420 matm PCO
2
, and hatched bars represent 1,100 matm PCO
2
. Different numbers above
bars highlight signicant differences between treatments within stages.
Figure 2. Effect of elevated temperature on the growth of stage IV
Homarus gammarus larvae (means 5SE): a, wet body mass (mg);
b, carapace length (mm). White bars indicate 177C and gray bars 217C.
Control and elevated-PCO
2
treatments were pooled at each temper-
ature. Different numbers above bars represent signicant differences
between treatments.
000 D.P.Small,P.Calosi,D.Boothroyd,S.Widdicombe,andJ.I.Spicer
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to 12.40% 53.23% at SIV, and ash content (percent of DM)
ranged from 49.59% 50.47% to 59.58% 51.20%. Between SI
and SIV,nitrogen content (percent of DM) ranged from 8.61% 5
0.11% to 6.65% 50.28%, while carbon and hydrogen content
(percent of DM) ranged from 36.14% 50.30% to 29.38% 5
0.87% and from 5.66% 50.07% to 4.39% 50.12%, respec-
tively.There was a signicant increase in DM and a signicant
decrease in N, resulting in a subsequent decrease in CN of SIV
individuals due to elevated PCO
2
(Fmin 1, 24 p4.958, P<0.030;
g. 4). There were no further signicant effects of elevated tem-
perature or PCO
2
, in isolation or in consort, on any other aspect
of organic content of SI, SII, or SIII individuals (P0.05).
Carapace Mineral Content
Carapace [Ca
21
]and[Mg
21
]increasedfrom60.4953.10 and
6.21 50.19 mmol mg
21
in SI individuals to 152.69 512.46
and 9.56 50.27 mmol mg
21
, respectively, in SIV individuals
reared under control conditions. Carapace [Mg
21
]increased
signicantly between Tp177C and Tp217C under 420 matm
PCO
2
but not under 1,100 matm PCO
2
, as indicated by the pres-
ence of a signicant interaction (F1, 19 p9.906, Pp.006; g. 5).
There were no further effects of elevated temperature and PCO
2
,
in isolation or in consort, on any other aspect of the carapace
mineral content of SI, SII, SIII, or SIV larvae (P0.05).
Figure 3. Effect of elevated temperatureontheratesofoxygenconsumption(mmol O
2
min
21
g
21
,STP)oflarvalHomarus gammarus (means 5
SE) at stage I (a), stage II (b), stage III (c), and stage IV (d). White bars indicate 177Candgraybars217C. Control and elevated-PCO
2
treatments
were pooled at each temperature. Different numbers above bars represent signicant differences between treatments; NS pnot signicant.
Figure 4. Effect of elevated PCO
2
on organic content and rates of oxygen consumption of stage IV larval Homarus gammarus (means 5SE):
a, dry body mass (expressed as percent wet body mass [WBM]); b, nitrogen levels (expressed as percent dry mass [DM]); c, carbon-to-nitrogen
ratio (CN); d, oxygen consumption (mmol O
2
min
21
g
21
, STP). White bars indicate 420 matm PCO
2
and gray bars 1,100 matm PCO
2
. Control and
elevated-temperature treatments were pooled at each PCO
2
treatment. Different numbers above bars represent signicant differences between
treatments.
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Discussion
Elevated temperature resulted in stage-specic differences in
the metabolic rates of larval lobsters. SI and SIV larvae ex-
hibited a reduction in metabolic rate at elevated temperature,
perhaps suggesting energetic limitations, and lower survival,
reduced growth, and greater sensitivity to elevated PCO
2
,com-
pared to SII and SIII larvae. Changes in temperature sensitivity
of metabolic rate between individual larval stages can inform
our understanding of their life-history responses, in terms of
survival and growth; our ndings support the idea that life-
history dynamics can ultimately be linked to the environment
via physiological processes (Calow and Forbes 1998; Ricklefs
and Wikelski 2002; Young et al. 2006).
Thermal Sensitivity of Lobster Larvae
Throughout the larval development of Homarus gammarus,
elevated temperature elicited greater physiological and/or life-
history responses than elevated PCO
2
. This was also the case for
the northern shrimp Pandalus borealis (Arnberg et al. 2013).
In H. gammarus, elevated temperature resulted in an increase
in survival and a decrease in development time but also a
decrease in body size at SIV. The overall growth and survival
patterns in H. gammarus observed here are consistent with
those reported for the larvae of other decapod crustaceans
(e.g., Sastry and McCarthy 1973; Johns 1981a,1981b;Mac-
Kenzie 1988; Anger 2001; Weiss et al. 2009a,2009b). Survival
under control conditions between SII and SIII was low, but
not exceptionally so (Addison and Bannister 1994; Ennis 1995).
When the underlying metabolic rates of H. gammarus larvae
are considered, it is possible to show complex, stage-dependent
responses to elevated temperature that must be carefully con-
sidered if the effects of elevated temperature on larval devel-
opment are to be adequately described. Specically, the met-
abolic rate of SI individuals was lower at 217Cthanat177C,
this being coupled to a subsequent decrease in survival to SII.
In contrast, SII and SIII exhibited increased metabolic rates
at 217C, compared to 177C, with higher survival to SIII and
SIV. These temperature-induced changes in metabolic rate and
survival between stages may represent ontogenetic shifts in
optimum temperature, as reported for survival in a number of
other marine crustaceanslarvae (e.g., Costlow et al. 1960, 1962,
1966). In our study, increases in survival were positively cor-
related with increases in metabolic rate reaction norms of
the previous stage (g. 6), indicating that in H. gammarus
these shifts in survival may be attributed to temperature-
induced changes in larvae metabolic rate. Crustaceans living
above their optimal temperature range often experience a lev-
eling off or decrease in their metabolic rates (Dehnel 1960;
Sastry and McCarthy 1973; Vernberg et al. 1981; Anger 1987;
Magozzi and Calosi 2015). In our study, this may indicate a
decrease in SI aerobic capacity (Sastry and McCarthy 1973;
Storch et al. 2009a, 2009b). Measurements of larval respira-
tion rates integrate both active and maintenance metabolisms
(Storch et al. 2009a,2009b), and so in our study the decrease in
metabolic rates suggests that at 217C, SI larvae had reached or
already passed their pejus temperatures (sensu Pörtner 2001).
Subsequently, the increase in metabolic rates due to elevated
temperature in SII and SIII may indicate an increased aerobic
scope, compared to that of SI, and an ontogenetic shift in ther-
mal optimum and aerobic scope during H. gammarus larval
development, as reported in some brachyuran crabs (Sastry and
McCarthy 1973).
Figure 5. Effect of elevated temperature and PCO
2
on carapace mineralization of stage IV larval Homarus gammarus (means 5SE): a, carapace
[Ca
21
](mmol mg
21
); b, carapace [Mg
21
](mmol mg
21
).Whitebarsindicate177Candgraybars217C. Open bars indicate 420 matm PCO
2
,
and hatched bars indicate 1,100 matm PCO
2
. Different numbers above bars represent signicant differences between treatments; NS pnot
signicant.
000 D.P.Small,P.Calosi,D.Boothroyd,S.Widdicombe,andJ.I.Spicer
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In contrast to those at other stages, SIV larvae did not
exhibit a signicant thermal metabolic response. This could
be interpreted as a further decrease in aerobic scope (Storch
et al. 2009a,2009b)orasadevelopmentalshiftinoptimal
temperature conditions. This shift was accompanied by a 20%
reduction in total growth between the control and elevated-
temperature treatments. Temperature-related reductions in
size have been attributed to decreases in development rates
and increases in molt frequencies (Templeman 1936). How-
ever, in H. gammarus there was no signicant effect of tem-
perature on the body size of SI, SII, or SIII larvae. The decrease
in body mass due to elevated temperature was conned to
SIV larvae and may indicate the metabolic vulnerability of
this stage to elevated temperature. This said, cumulative ef-
fects across different larval stages could not be ruled out (e.g.,
Dupont et al. 2013). For crustaceans, changes in WBM and
body size are limited to, and dened by, the postmolt hard-
ening phase (Anger 2001). Stage-specic temperature-related
changes in growth could be attributed to energetic demands
of that specic developmental stage, such as the reallocation
of energy away from growth and into the development of cer-
tain physiological milestones(Agard 1999). Such milestones
include the development of osmoregulation and respiratory
regulation capabilities and structures at the transition between
SIII and SIV larvae in both the Norway lobster Nephrops nor-
vegicus and the American lobster Homarus americanus (Char-
mantier et al. 1988, 2001; Spicer and Eriksson 2003). It has
been suggested that energy reallocation during transitional
stages results in the production of smaller megalopa as a result
of a mismatch between energetic demands and supply in ecto-
therms exposed to high temperature (Atkinson 1995).
In situ, hatching of H. gammarus larvae occurs in spring
and early summer as seawater temperatures exceed 87C(Rich-
ards and Wickins 1979; Charmantier and Mounet-Guillaume
1992; Cobb and Wahle 1994). Stage I larvae then rapidly con-
centrate at the surface (Cobb and Wahle 1994), experienc-
ing temperatures ranging from 87Cuponhatchingto177C
in surface waters during the summer (Western Channel Ob-
servatory temperature data; D. P. Small, personal observations).
Such environmental temperature shifts during larval export may
be indicative of the shifting optimum temperatures between stages
described in our study. Stages with narrower aerobic scopes and
lower optimal temperatures (e.g., SI and SIV) are transitory stages
between colder and warmer environments (SI) and vice versa
(SIV). Thermal stress during these stages, therefore, will likely
produce potential bottlenecks in larval development and recruit-
ment (e.g., Bartolini et al. 2013).
Effect of Elevated PCO
2
on Larval Growth
While temperature appears to be the dominant driver inu-
encing H. gammarus larval development, larval stages exhib-
iting temperature-dependent decreases in metabolic rates (SI
and SIV) were also those sensitive to elevated PCO
2
, possibly
because these stages were close to or beyond their pejus tem-
perature thresholds (sensu Pörtner and Farrell 2008; Storch
Figure 6. Relationship between the rates of oxygen consumption and
subsequent survival of larval Homarus gammarus reared under ele-
vated temperature and PCO
2
:a, stage I rates of oxygen consumption
and subsequent survival to stage II (yp60.77x143.03); b, stage II
rates of oxygen consumption and subsequent survival to stage III
(yp69.05x28.94); c, stage III rates of oxygen consumption and sub-
sequent survival to stage IV (yp102.71x221.36). Circles indicate 177C
at 420 matm PCO
2
, diamonds indicate 177C at 1,100 matm PCO
2
, squares
indicate 217C at 420 matm PCO
2
, and triangles indicate 217C at 1,100 matm
PCO
2
. Rates of oxygen consumption are expressed as mmol g
21
min
21
,
STP, and survival is expressed as percent survival from previous de-
velopmental stage.
Lobster Larvae Vulnerability to Ocean Change 000
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et al. 2009a,2009b). Early larvae and spawning adults are
proposed to be the life-history stages least tolerant to elevated
temperature and PCO
2
, as a result of ontogenetic changes in
physiological tolerance during development (Pörtner and Far-
rell 2008; Walther et al. 2011). Expanding on this, our nd-
ings show how H. gammarus SI and SIV larvae have the nar-
rowest tolerance range of the four larval stages in relation to
temperature. Under elevated PCO
2
at the control temperature
(177C),survivalfromSItoSIIwas10%lowerthanthatat
control PCO
2
, which can be explained by an increase in ener-
getic demands associated with molting in SI larvae due to el-
evated PCO
2
(Schiffer et al. 2013). Survival effects of PCO
2
were
not detectable at high temperature, possibly because of the
high mortality in relation to elevated temperature at this stage.
SIV individuals also exhibited sensitivity to elevated PCO
2
in
terms of organic content and carapace mineralization. Me-
tabolism and DM increased in SIV individuals because of ele-
vated PCO
2
at 177and 217C, along with a signicant decrease
in N content and a consequent increase in the CNratio.The
increase in metabolism indicates increased energy demands
and, coupled with the changes in CN ratios, suggests that
increased energetic demands were accompanied by increased
protein turnover, a response observed in most organisms ex-
posed to stressful environments (Anger 2001; Weiss et al.
2009a,2009b). Walther et al. (2010) also observed signicant
changes in organic content due to temperature and elevated
PCO
2
; however, changes in CNratiosatthemegalopastage
of the spider crab Hyas araneus were accompanied by de-
creasing DM.
In terms of carapace mineralization, there was a signicant
effect of the interaction between elevated temperature and
PCO
2
on SIV carapace [Mg
21
]. This resulted in carapace [Mg
21
]
signicantly increasing with elevated temperature but de-
creasing because of elevated PCO
2
at elevated temperatures.
SIV carapace [Ca
21
] was not affected by elevated temperature
or PCO
2
. Decreases in carapace mineralization have previously
been demonstrated for SIV H. gammarus (Arnold et al. 2009)
and larval H. araneus (Walther et al. 2011), although, inter-
estingly, adult H. americanus exposedtoelevatedP
CO
2
in-
creased mineralization levels (Ries et al. 2009). The decrease
in carapace [Mg
21
] due to elevated PCO
2
at 217C, compared to
an increase due to elevated PCO
2
and temperature at 177C,
supports the idea of an elevated temperature-related increase
in sensitivity to elevated PCO
2
. The responses in terms of or-
ganic content and mineralization in this study, as well as those
observed by Arnold et al. (2009) and Walther et al. (2011), in-
dicate changes in resource allocation, possibly because of the
development of physiological structures and functions at mega-
lopa stages (Agard 1999) and possibly because of the energetic de-
mands generally during larval development (Arnold et al. 2009;
Walther et al. 2010, 2011). Altogether, the current observations
provide a mechanistic basis for the effect of elevated PCO
2
on
developmental stages and corroborate the idea that particular life
stages will represent critical bottlenecks for population growth
and stock sustainability during times of ocean change (e.g., Wal-
ther et al. 2010; Byrne 2012).
Conclusions
Understanding the physiological ontogeny of marine larvae
in the light of ocean change is crucial if we are to understand
populationspotential responses to ocean change. Alterations
to larval body size, organic content, and carapace minerali-
zation at the pelagic-benthic transition phase (i.e., megalopa
stage) due to elevated temperature and PCO
2
may have pro-
found ecological consequences affecting the survival, growth,
and performance of subsequent juvenile stages (Jarrett and
Pechenik 1997; Pechenik et al. 2002; Jarrett 2003; Giménez
et al. 2004; Nasrolahi et al. 2012; Pansch et al. 2012). Equally,
the transition between embryonic and SI larvae, the benthic-
pelagic transition phase, may also be of great importance for
modulating population dynamic processes, because physio-
logical sensitivity in early developmental stages has been
linked to the occurrence of extreme climatic events and the
reduction in the number of adults (Bartolini et al. 2013). While
H. gammarus recruitment in terms of overall survival may
appear to increase with elevated temperature, the associated
temperature-related decrease in megalopa body size could also
have important negative consequences, as demographic pro-
cesses of lobster stocks are body size dependent (Wahle 1992;
Wahle and Steneck 1992; Cobb and Wahle 1994; Wahle and
Fogarty 2006), with larger size at settlement leading to greater
survival (Wilbur 1980). If we consider that, under elevated-PCO
2
conditions, SIV individuals appear to undergo energetic trade-
offs between growth and condition, further negative effects of
climate change on lobster recruitment and population dynam-
ics may be expected. The current ndings highlight that stage-
specic sensitivity to elevated temperature and PCO
2
in species
with complex life cycles, such as H. gammarus, may inuence
future recruitment patterns, in ways more complex than pre-
viously concluded from studies based on temperature and PCO
2
alone.
Acknowledgments
We thank the technicians of the National Lobster Hatchery,
Dr.C.Daniels,C.Ellis,andDr.J.Scolding,alongwithvol-
unteers, for their help with technical support and knowl-
edge on lobster larval rearing. This work was carried out while
D.P.S. was in receipt of a Plymouth Universityfunded PhD
studentship, with additional funding awarded to the National
Lobster Hatchery from the National Marine Aquarium (Plym-
outh, UK). P.C. was in receipt of a Research Council of the
United Kingdom (RCUK) Research Fellowship to investigate
ocean acidication at Plymouth University, and J.I.S. was in
receipt of RCUK funding. This project is a contribution to the
Task 1.4, Identify the potential for organism resistance and
adaptation to prolonged CO
2
exposure,of the Natural Envi-
ronment Research Council (NERC) Consortium Grant Im-
pacts of ocean acidication on key benthic ecosystems, com-
munities, habitats, species, and life cycles(NERC grant NE/
H017127/1) to J.I.S. and P.C.
000 D.P.Small,P.Calosi,D.Boothroyd,S.Widdicombe,andJ.I.Spicer
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APPENDIX
Figure A1. Diagram of the experimental setup. a, Temperature control; dark gray lines and arrows indicate the ow of control (177C)
treatment water; light gray lines and arrows indicate the ow of elevated-temperature (217C) treatment water. A pheader tanks with ltration.
Bpchiller units with heating elements to control water temperature. C pwater inow into individual rearing cones; note that there is a
swappingof treatment water to aid temperature control within tanks. D psump tanks with ltration. E pwaste water overow. F pdaily
8-h ow of new, clean seawater to ensure water quality. b,Individuallarvalrearingcone.Apwater inow (set at designated temperature
level). B pair inow (set at designated PCO
2
level). C pwater height in cone. D pwater overow through mesh to allow broken food removal
but retain larvae and larger food particles. E pcone lid to prevent excess evaporation and spray. F pwater level in surrounding tank. A color
version of this gure is available online.
Lobster Larvae Vulnerability to Ocean Change 000
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... The combined effects of ocean acidification (OA) and warming on marine life have been studied for at least two decades, but they are still challenging to interpret and predict. A growing number of experiments using ecologically and economically important species, such as Pacific herring (Villalobos et al., 2020), Pacific oysters (Lemasson et al., 2018), gilthead seabream, meagre (Pimentel et al., 2016), American and European lobster (Small et al., 2015;Waller et al., 2017) have shown an exacerbated impact of OA on survival, physiology, and growth when it was combined with elevated temperatures. Synergistic impacts (the result of stressors interacting and producing a greater effect than the cumulative or individual effects) of climate change vary across life stages with the tendency that early life stages are more sensitive and less tolerant to environmental stressors than adults (Kikkawa et al., 2003;Ishimatsu et al., 2004;Kurihara, 2008). ...
... Only two studies have assessed the joint effects of OA and ocean warming on lobster larvae of the genus Homarus. They provide the first insight on how lobsters may respond to the synergistic effects of environmental changes predicted for the end of the 21st century (Small et al., 2015;Waller et al., 2017). These studies have in common an experimental design based on only two temperatures and two pCO 2 regimes, comparing (in a factorial design) ambient temperature and pCO 2 conditions with increased temperature and pCO 2 . ...
... There was no evidence of an effect of elevated pCO 2 on development time from hatching to stage III. Our results are consistent with studies focusing on temperature only (Schmalenbach and Franke, 2010) as well as pCO 2 and temperature (Arnold et al., 2009;Small et al., 2015;Waller et al., 2017) where pCO 2 had no effect on lobster larval development rate. This led us to further enquire if there was possibly a trade-off between slower development rate under pCO 2 . ...
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Climate change combined with anthropogenic stressors (e.g. overfishing, habitat destruction) may have particularly strong effects on threatened populations of coastal invertebrates. The collapse of the population of European lobster (Homarus gammarus) around Helgoland constitutes a good example and prompted a large-scale restocking program. The question arises if recruitment of remaining natural individuals and program-released specimens could be stunted by ongoing climate change. We examined the joint effect of ocean warming and acidification on survival, development, morphology, energy metabolism and enzymatic antioxidant activity of the larval stages of the European lobster. Larvae from four independent hatches were reared from stage I to III under a gradient of 10 seawater temperatures (13–24°C) combined with moderate (∼470 µatm) and elevated (∼1160 µatm) seawater pCO2 treatments. Those treatments correspond to the shared socio-economic pathways (SSP), SSP1-2.6 and SSP5-8.5 (i.e. the low and the very high greenhouse gas emissions respectively) projected for 2100 by the Intergovernmental Panel on Climate Change. Larvae under the elevated pCO2 treatment had not only lower survival rates, but also significantly smaller rostrum length. However, temperature was the main driver of energy demands with increased oxygen consumption rates and elemental C:N ratio towards warmer temperatures, with a reducing effect on development time. Using this large temperature gradient, we provide a more precise insight on the aerobic thermal window trade-offs of lobster larvae and whether exposure to the worst hypercapnia scenario may narrow it. This may have repercussions on the recruitment of the remaining natural and program-released specimens and thus, in the enhancement success of future lobster stocks.
... Decapods are considered less sensitive to decreasing levels of carbonate saturation than are other calcifiers, because of their tightly regulated physiology and calcification process in adults, which is not directly dependent on environmental carbonate chemistry (Boßelmann et al., 2007;Taylor et al., 2015). However, the early life-history stages are particularly vulnerable to OA (Walther et al., 2010;Carter et al., 2013;Ceballos-Osuna et al., 2013;Long et al., 2013a;Small et al., 2015;Gravinese, 2018), either through maternal carryover effects Swiney et al., 2016) or direct effects including reduced growth rate (Allan and Maguire, 1992;Coffey et al., 2017;Ragagnin et al., 2018), increased oxidative stress and energy metabolism Hu et al., 2016), exoskeleton dissolution (Bednaršek et al., 2020); reduced egg production (Kurihara et al., 2008;Meseck et al., 2016), and increased mortality (Kurihara et al., 2008;Long et al., 2013a,b;Coffey et al., 2017;Swiney et al., 2017;Tomasetti et al., 2018). Maintaining biomineralization under OA may come with high energetic costs, causing organisms to divert energy from vital physiological processes, such as reproduction (Long et al., 2013a;Meseck et al., 2016), and growth (Wood et al., 2008). ...
... Thresholds were identified across different life stages, indicating sensitivity through the duration of the entire life history cycle, rather than being related to one life stage-specific bottleneck. Recent studies suggest that juveniles may be particularly sensitive to OA and other global change drivers (e.g., Walther et al., 2010;Small et al., 2015;Menu-Courey et al., 2019). We note that duration of exposure required to impact decapod physiology was highly variable among endpoints and life stages, ranging from 9 days to 1 year for sublethal responses, and 7-180 d for lethal responses, in comparison to 2-14 days for pteropods (Bednaršek et al., 2019(Bednaršek et al., , 2021, making decapod habitats characterized by prolonged low pH exposure and thus higher risks. ...
... Other multiple stressor related studies report opposing effects that are most likely species, life-stage and treatment specific; temperature combined with OA did not affect European lobster juveniles (Small et al., 2016), but on juvenile red king crab, temperature and OA had an antagonist effect with a small increase in temperature and a synergistic negative effect with a larger increase . The effect of warming in combination with OA may be more severe for larval and megalopae stages; four out of five studies reported significant negative effects of increased temperatures on survival (Walther et al., 2010;Small et al., 2015;Waller et al., 2017;Gravinese et al., 2018), while three of the five studies noted that temperature had a more substantial impact on larval mortality than pH (Small et al., 2015;Waller et al., 2017;Gravinese et al., 2018). ...
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Assessing decapod sensitivity to regional-scale ocean acidification (OA) conditions is limited because of a fragmented understanding of the thresholds at which they exhibit biological response. To address this need, we undertook a three-step data synthesis: first, we compiled a dataset composed of 27,000 datapoints from 55 studies of decapod responses to OA. Second, we used statistical threshold analyses to identify OA thresholds using pH as a proxy for 13 response pathways from physiology to behavior, growth, development and survival. Third, we worked with the panel of experts to review these thresholds, considering the contributing datasets based on quality of the study, and assign a final thresholds and associated confidence scores based on quality and consistency of findings among studies. The duration-dependent thresholds were within a pH range from 7.40 to 7.80, ranging from behavioral and physiological responses to mortality, with many of the thresholds being assigned medium-to-high confidence. Organism sensitivity increased with the duration of exposure but was not linked to a specific life-stage. The thresholds that emerge from our analyses provide the foundation for consistent interpretation of OA monitoring data or numerical ocean model simulations to support climate change marine vulnerability assessments and evaluation of ocean management strategies.
... By incorporating physiological knowledge, conservation strategies can be better developed and tested by generating models that predict how organisms may respond to environmental change (Cooke et al. 2012). In terms of invertebrate larvae, understanding their physiological responses to acute temperature changes can inform on their vulnerability at an individual, population, and community level and can provide valuable insight into what influences larval community assembly under various environmental conditions (Small et al. 2015;Vorsatz et al. 2021d). Indeed, the metabolic responses to variable salinity have been widely addressed for embryos and larvae of mangrove and mangrove-associated crabs (Anger and Charmantier 2000;Charmantier et al. 2002;Diele and Simith 2006;Simoni et al. 2013;Simith et al. 2014). ...
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Macroinvertebrates that rely on a supply of planktonic larvae for recruitment play a significant role in maintaining productivity in mangrove ecosystems. Thus, identifying the spatial distribution and physiological limitations of invertebrate larval communities within mangroves is important for targeted conservation efforts to maintain population persistence amid the threat of climate change. Here, the role of spatial, lunar, and environmental factors in structuring invertebrate larval communities in Ting Kok, the second largest mangrove forest in Hong Kong, was examined. Results indicate that, spatially, invertebrate larval communities were influenced by environmental filtering, habitat type, and the lunar tidal cycle. This indicates the fundamental role of habitat heterogeneity and connectivity for the transport, distribution, and development of crustacean larvae. Larvae of key sesarmids exhibited metabolic depression at water temperatures forecasted to be regularly experienced by the year 2050, according to current climate projections. The impacts of climate change, coupled with habitat destruction and degradation of hydrological connectivity, make larval communities increasingly vulnerable to mass-mortality and displacement. This places ecosystem productivity and functionality at risk through cascading negative effects of recruitment limitation. Further focus on this subject will help disentangle the effects of process rates and scales of transport that underlie community assemblages in mangrove systems. Furthermore, identifying physiological bottlenecks of key taxa and habitat provisioning that enhance larval survival will be helpful to prioritize strategies for conservation management in dynamic intertidal settings.
... are marked with an asterisk heterogeneity was noted for all pCO 2 bins, with a Q range from 46.2 to 91.5 across bins(Table A3). While the 1500-1999 µatm bin displayed a clear decrease in exoskeleton ion content under high CO 2 conditions, the variance in individual effect sizes, and the variance for all responses in the dataset, were not explained by CO 2 level alone.As mineralization responses of crustaceans to environmental stress, particularly ocean acidification, are not uniform and can vary between species and elements quantified (for differing responses, seeLong, Swiney, Harris, et al., 2013;Page et al., 2017;Small et al., 2015, as examples), we also analyzed the changes in Ca 2+ and Mg 2+ levels separately under high pCO 2 conditions. Effect sizes for Ca 2+ ...
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Crustaceans comprise an ecologically and morphologically diverse taxonomic group. They are typically considered resilient to many environmental perturbations found in marine and coastal environments, due to effective physiological regulation of ions and hemolymph pH, and a robust exoskeleton. Ocean acidification can affect the ability of marine calcifying organisms to build and maintain mineralized tissue and poses a threat for all marine calcifying taxa. Currently, there is no consensus on how ocean acidification will alter the ecologically relevant exoskeletal properties of crustaceans. Here, we present a systematic review and meta-analysis on the effects of ocean acidi-fication on the crustacean exoskeleton, assessing both exoskeletal ion content (cal-cium and magnesium) and functional properties (biomechanical resistance and cuticle thickness). Our results suggest that the effect of ocean acidification on crustacean exoskeletal properties varies based upon seawater pCO 2 and species identity, with significant levels of heterogeneity for all analyses. Calcium and magnesium content was significantly lower in animals held at pCO 2 levels of 1500-1999 µatm as compared with those under ambient pCO 2. At lower pCO 2 levels, however, statistically significant relationships between changes in calcium and magnesium content within the same experiment were observed as follows: a negative relationship between calcium and magnesium content at pCO 2 of 500-999 µatm and a positive relationship at 1000-1499 µatm. Exoskeleton biomechanics, such as resistance to deformation (microhardness) and shell strength, also significantly decreased under pCO 2 regimes of 500-999 µatm and 1500-1999 µatm, indicating functional exoskeletal change co-incident with decreases in calcification. Overall, these results suggest that the crustacean exoskeleton can be susceptible to ocean acidification at the biomechanical level, potentially predicated by changes in ion content, when exposed to high influxes of CO 2. Future studies need to accommodate the high variability of crustacean responses to ocean acidification, and ecologically relevant ranges of pCO 2 conditions, when designing experiments with conservation-level endpoints.
... Increasing temperatures are also reported to have adverse effects on survival rates of crustacean larvae, including American lobster larvae [28], Florida stone crab larvae [29] and barnacle Amphibalanus improvisus larvae [30]. However, we still know relatively little about how climate change parameters, especially warming and freshening, affect the physiology of the juvenile stage of many crustacean species, while several studies have focused on the effects of ocean acidification (pCO 2 ) [31,32]. Juveniles are considered as potential life-history bottlenecks determining the future success of the species [33][34][35]. ...
... Increasing temperatures are also reported to have adverse effects on survival rates of crustacean larvae, including American lobster larvae [28], Florida stone crab larvae [29] and barnacle Amphibalanus improvisus larvae [30]. However, we still know relatively little about how climate change parameters, especially warming and freshening, affect the physiology of the juvenile stage of many crustacean species, while several studies have focused on the effects of ocean acidification (pCO 2 ) [31,32]. Juveniles are considered as potential life-history bottlenecks determining the future success of the species [33][34][35]. ...
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