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The sensitivity of the early benthic juvenile stage of the European lobster Homarus gammarus (L.) to elevated pCO2 and temperature

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Daniel Peter Small at Fisheries and Oceans Canada
Daniel Peter Small
Piero Calosi at Université du Québec à Rimouski UQAR
Piero Calosi
Dominic Boothroyd
Dominic Boothroyd
Dominic Boothroyd
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Steve Widdicombe at Plymouth Marine Laboratory
Steve Widdicombe
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Abstract and Figures

The early benthic juvenile stage of many marine invertebrates is a key step in the transition from the planktonic larval stages to the benthic adult stage. It is characterised by high mortality, in part, due to sensitivities to abiotic factors. The impacts of elevated pCO2 and temperature on the physiology and life history of these sensitive life stages are, however, poorly understood. Consequently, the aim of the present study was to investigate the vulnerability of survival, growth, metabolic rate, feeding rate, organic content, and carapace mineralisation of the early benthic juvenile stage of the European lobster Homarus gammarus (L.) to predicted levels of elevated pCO2 [ocean acidification (OA) and carbon capture and storage (CCS) scenarios] and elevated temperature [ocean warming (OW)]. Early benthic juvenile H. gammarus exhibited increased mortality under both OA and CCS conditions at both experimental temperatures, and these mortalities were due to moult death syndrome. There were OA-related reductions in metabolism, food acquisition, and carapace mineral content, while CCS-exposed lobsters exhibited severe shell dissolution. We suggest that disruption of metabolic and calcium homoeostasis is associated with, and possible the cause of, the increased incidence of moult-related mortalities in juvenile lobsters. We conclude that early benthic juvenile lobsters are sensitive, in terms of physiology and life history traits, to both OA and CCS, with OW sometimes mitigating and at other times increasing sensitivities.
a Survival (%), b moult events, and c MDS occurrence (as % of moult events) of early benthic juvenile of the European lobster, Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2, thin striped bars indicate 9000 µatm pCO2. *Indicates significant effect of elevated pCO2 as determined by using the estimated marginal means test
a Survival (%), b moult events, and c MDS occurrence (as % of moult events) of early benthic juvenile of the European lobster, Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2, thin striped bars indicate 9000 µatm pCO2. *Indicates significant effect of elevated pCO2 as determined by using the estimated marginal means test
… 
Mean growth [% wet body mass (WMB) gain] of juvenile European lobster Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2, thin striped bars indicate 9000 µatm pCO2. *Indicates significant effect of elevated pCO2; #indicates significant effect of elevated temperature as determined by using the estimated marginal means test
Mean growth [% wet body mass (WMB) gain] of juvenile European lobster Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2, thin striped bars indicate 9000 µatm pCO2. *Indicates significant effect of elevated pCO2; #indicates significant effect of elevated temperature as determined by using the estimated marginal means test
… 
Mean rates of a oxygen consumption (µmol O2 min⁻¹ g⁻¹) and b food consumption rates (µg min⁻¹ mg⁻¹) of early benthic juvenile European lobster Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2, thin striped bars indicate 9000 µatm pCO2. *Indicates significant effect of elevated pCO2; #indicates significant effect of elevated temperature as determined by using the estimated marginal means test
Mean rates of a oxygen consumption (µmol O2 min⁻¹ g⁻¹) and b food consumption rates (µg min⁻¹ mg⁻¹) of early benthic juvenile European lobster Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2, thin striped bars indicate 9000 µatm pCO2. *Indicates significant effect of elevated pCO2; #indicates significant effect of elevated temperature as determined by using the estimated marginal means test
… 
Mean a total CHN, b N, c C, and d C:N of the abdomen (% DM⁻¹) of early benthic juvenile European lobster Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2. *Indicates significant effect of elevated pCO2; #indicates significant effect of elevated temperature as determined by using the estimated marginal means test
Mean a total CHN, b N, c C, and d C:N of the abdomen (% DM⁻¹) of early benthic juvenile European lobster Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2. *Indicates significant effect of elevated pCO2; #indicates significant effect of elevated temperature as determined by using the estimated marginal means test
… 
Mean a [Ca²⁺] and b [Mg²⁺] and c [Sr²⁺] in the carapace (µmol mg⁻¹) of early benthic juvenile European lobster Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2. *Indicates significant effect of elevated pCO2 as determined by using the estimated marginal means test
Mean a [Ca²⁺] and b [Mg²⁺] and c [Sr²⁺] in the carapace (µmol mg⁻¹) of early benthic juvenile European lobster Homarus gammarus after 5-week exposure to elevated temperature and pCO2 (mean ± SE): white bars indicate 10 °C. Grey bars indicate 13 °C. Clear bars indicate 450 µatm pCO2, thick striped bars indicate 1100 µatm pCO2. *Indicates significant effect of elevated pCO2 as determined by using the estimated marginal means test
… 
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1 3
Mar Biol (2016) 163:53
DOI 10.1007/s00227-016-2834-x
ORIGINAL PAPER
The sensitivity of the early benthic juvenile stage of the
European lobster Homarus gammarus (L.) to elevated pCO2
and temperature
Daniel P. Small1,2,3,4 · Piero Calosi2,5 · Dominic Boothroyd3 · Stephen Widdicombe4 ·
John I. Spicer2
Received: 15 June 2015 / Accepted: 2 February 2016 / Published online: 18 February 2016
© Springer-Verlag Berlin Heidelberg 2016
exhibited increased mortality under both OA and CCS
conditions at both experimental temperatures, and these
mortalities were due to moult death syndrome. There were
OA-related reductions in metabolism, food acquisition,
and carapace mineral content, while CCS-exposed lobsters
exhibited severe shell dissolution. We suggest that disrup-
tion of metabolic and calcium homoeostasis is associated
with, and possible the cause of, the increased incidence of
moult-related mortalities in juvenile lobsters. We conclude
that early benthic juvenile lobsters are sensitive, in terms
of physiology and life history traits, to both OA and CCS,
with OW sometimes mitigating and at other times increas-
ing sensitivities.
Abbreviations
OW Ocean warming
OA Ocean acidification
CCS Carbon capture and storage
pCO2 Partial pressure of carbon dioxide
HCO3− Bicarbonate
CO32− Carbonate
AT Total alkalinity
TCO2 Total carbon dioxide
Ωara Aragonite saturation
Ωcal Calcite saturation
WBM Wet body mass
DM Dry mass
MDS Moult death syndrome
C Carbon
H Hydrogen
N Nitrogen
Ca2+ Calcium ions
Mg2+ Magnesium ions
S2+ Strontium ions
Abstract The early benthic juvenile stage of many
marine invertebrates is a key step in the transition from
the planktonic larval stages to the benthic adult stage. It
is characterised by high mortality, in part, due to sensitivi-
ties to abiotic factors. The impacts of elevated pCO2 and
temperature on the physiology and life history of these
sensitive life stages are, however, poorly understood. Con-
sequently, the aim of the present study was to investigate
the vulnerability of survival, growth, metabolic rate, feed-
ing rate, organic content, and carapace mineralisation of
the early benthic juvenile stage of the European lobster
Homarus gammarus (L.) to predicted levels of elevated
pCO2 [ocean acidification (OA) and carbon capture and
storage (CCS) scenarios] and elevated temperature [ocean
warming (OW)]. Early benthic juvenile H. gammarus
Responsible Editor: H. O. Pörtner.
Reviewed by undisclosed experts.
* Daniel P. Small
dsmall@stfx.ca
1 Biology Department, St. Francis Xavier University, 2320
Notre Dame Avenue, Antigonish, NS B2G 2W5, Canada
2 Marine Biology and Ecology Research Centre, School
of Marine Science and Engineering, Plymouth University,
Drake Circus, Plymouth, Devon PL4 8AA, UK
3 National Lobster Hatchery, South Quay, Padstow, Cornwall
PL28 8BL, UK
4 Plymouth Marine Laboratory, Prospect Place, West Hoe,
Plymouth, Devon PL1 3DH, UK
5 Département de Biologie, Chimie et Géographie, Université
du Québec à Rimouski, 300 Allée des Ursulines, Rimouski,
QC G5L 3A1, Canada
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
... Similarly, laboratory studies are only indicative of what may occur in nature. Our results with respect to the impacts on mineralogy and, to some extent, growth, reflect those of other studies where more than one ovigerous female was used (Small et al., 2016;Menu-Courey et al., 2019). We chose to limit the confounding effects of inter-female variation and prior rearing history among treatments. ...
... Despite the capacity to preferentially incorporate more magnesium into the shell to maintain adequate mineral content, our results indicate juvenile lobsters may not capitalize on this strategy. Small et al. (2016) similarly found that acidified conditions only resulted in a decrease of mineral content (Ca 2+ , Mg 2+ , Sr 2+ ) in early benthic juvenile Homarus gammarus (Linnaeus, 1758) (Nephropidae) at elevated temperatures (Small et al., 2016). Elevated pCO 2 alone was shown to significantly increase [Mg 2+ ] in stage V post-larval juvenile H. americanus (Menu-Courey et al., 2019). ...
... Despite the capacity to preferentially incorporate more magnesium into the shell to maintain adequate mineral content, our results indicate juvenile lobsters may not capitalize on this strategy. Small et al. (2016) similarly found that acidified conditions only resulted in a decrease of mineral content (Ca 2+ , Mg 2+ , Sr 2+ ) in early benthic juvenile Homarus gammarus (Linnaeus, 1758) (Nephropidae) at elevated temperatures (Small et al., 2016). Elevated pCO 2 alone was shown to significantly increase [Mg 2+ ] in stage V post-larval juvenile H. americanus (Menu-Courey et al., 2019). ...
Physiological impacts of climate change on juvenile American lobster Homarus americanus H. Milne Edwards, 1837 (Decapoda: Astacidea: Nephropidae), a commercially important species
Article
  • Feb 2024
  • J CRUSTACEAN BIOL
The American lobster, Homarus americanus, H. Milne Edwards, 1837 is an ecologically, economically, and culturally valuable marine resource for the coastal communities in the Gulf of Maine. Lobsters in the Gulf of Maine are experiencing the effects of rapid warming and acidification due to climate change. Lobster shells are comprised of chitin with precisely precipitated minerals (calcite, amorphous calcium carbonate, and carbonate apatite) that provide structural integrity to the shell and protection against predators and microbial intrusion. We examined the combined effects of ocean warming and acidification on shell mineralogy, epibiont abundance, and growth in early benthic juveniles. Lobsters were grown under six different temperature/pCO2 treatment conditions over 52 days (three replicates per treatment) aligned with environmentally relevant as well as predicted future extremes. Elevated pCO2 and temperature led to a decrease in shell calcium and magnesium content, suggesting that these environmental stressors inhibit shell biomineralization. There was an interactive effect of the stressors on epibiont abundance with the probability of epibiont coverage increasing with increasing pCO2 and temperature. Elevated pCO2 alone was significantly correlated (P = 0.002) to decreased growth, but only for female lobsters. Ocean acidification and warming significantly affect shell integrity in juvenile lobster, increasing risk to injury and disease with potential downstream consequences for the lobster fishery.
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... Prior work has demonstrated complex singular and interactive effects of acidification and warming on Homarus species physiology at various life stages, including differential rates of calcification (Arnold et al., 2009;Ries et al., 2009;Small et al., 2015;Small et al., 2016;Menu-Courey et al., 2019;Small et al., 2020;San Antonio et al., 2024), diminished hemolymph and acid/base regulation Klymasz-Swartz et al., 2019), altered metabolic rates (Waller et al., 2016;Rato et al., 2017), differential vulnerability to disease partly based on life stage (Dove et al., 2004;Tlusty, 2012;McLean et al., 2018;Harrington et al., 2020b), as well as impairments in growth (Keppel et al., 2012;Agnalt et al., 2013;Waller et al., 2016;San Antonio et al., 2024) and survival (Small et al., 2015;Small et al., 2016). Very few studies have investigated the effects of these stressors on gene expression in lobsters. ...
... Prior work has demonstrated complex singular and interactive effects of acidification and warming on Homarus species physiology at various life stages, including differential rates of calcification (Arnold et al., 2009;Ries et al., 2009;Small et al., 2015;Small et al., 2016;Menu-Courey et al., 2019;Small et al., 2020;San Antonio et al., 2024), diminished hemolymph and acid/base regulation Klymasz-Swartz et al., 2019), altered metabolic rates (Waller et al., 2016;Rato et al., 2017), differential vulnerability to disease partly based on life stage (Dove et al., 2004;Tlusty, 2012;McLean et al., 2018;Harrington et al., 2020b), as well as impairments in growth (Keppel et al., 2012;Agnalt et al., 2013;Waller et al., 2016;San Antonio et al., 2024) and survival (Small et al., 2015;Small et al., 2016). Very few studies have investigated the effects of these stressors on gene expression in lobsters. ...
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... Decreased water pH causes acute acidosis of crustacean hemolymph which many are able to respond to by buffering their hemolymph via active ion transport (Pane and Barry, 2007;Small et al., 2010) or by reducing their metabolic rates and thus the metabolic production of CO 2 (Pane and Barry, 2007;Small et al., 2020). These responses can bring the hemolymph back into acid-base homeostasis (Meseck et al., 2016); however, the energetic costs of these processes can shift energy investment away from other processes such as growth and reproduction (Small et al., 2016;Swiney et al., 2016). Despite this, many species are well adapted to a broad range of pH conditions (Glandon and Miller, 2017;Glandon et al., 2018;Glandon et al., 2019;Gravinese et al., 2022;Algayer et al., 2023;Long et al., 2023). ...
... Larval European lobsters, Homarus gammarus, for example, show a slight increase in mortality during the first larval stage only with no effects on growth at any stage (Small et al., 2015). In contrast, juveniles suffered increased mortality, decreased growth, decreased metabolism, and carapace deformation under reduced pH conditions (Agnalt et al., 2013;Small et al., 2016) likely driven by the high cost of maintaining acid-base hemostasis and calcification rates (Small et al., 2020). Similarly, American lobster, Homarus americanus¸ larvae were unaffected even by extreme low pH conditions whereas juveniles suffered increased mortality and decreased growth (Noisette et al., 2021). ...
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... Direct, carryover, and maternal effects of ocean acidification on snow crab embryos and larvae respond very differently to OA; larval American lobsters (Homarus americanus) are highly resistant whereas juveniles are very sensitive [106] and European lobster (Homarus gammarus) have both sensitive and resistant larval stages and a very sensitive juvenile stage [107,108]. Thus, studies examining all larval stages as well the juvenile stage of snow crab should be performed before it can be concluded that the species as a whole will be resistant to OA. ...
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Full-text available
Ocean acidification, a decrease in ocean pH with increasing anthropogenic CO2 concentrations, is expected to affect many marine animals. To examine the effects of decreased pH on snow crab (Chionoecetes opilio), a commercial species in Alaska, we reared ovigerous females in one of three treatments: Ambient pH (~8.1), pH 7.8, and pH 7.5, through two annual reproductive cycles. Morphometric changes during development and hatching success were measured for embryos both years and calcification was measured for the adult females at the end of the 2-year experiment. Embryos and larvae analyzed in year one were from oocytes developed, fertilized, and extruded in situ, whereas embryos and larvae in year two were from oocytes developed, fertilized, and extruded under acidified conditions in the laboratory. In both years, larvae were exposed to the same pH treatments in a fully crossed experimental design. Starvation-survival, morphology, condition, and calcium/magnesium content were assessed for larvae. Embryo morphology during development, hatching success, and fecundity were unaffected by pH during both years. Percent calcium in adult females’ carapaces did not differ among treatments at the end of the experiment. In the first year, starvation-survival of larvae reared at Ambient pH but hatched from embryos reared at reduced pH was lowered; however, the negative effect was eliminated when the larvae were reared at reduced pH. In the second year, there was no direct effect of either embryo or larval pH treatment, but larvae reared as embryos at reduced pH survived longer if reared at reduced pH. Treatment either did not affect other measured larval parameters, or effect sizes were small. The results from this two-year study suggest that snow crabs are well adapted to projected ocean pH levels within the next two centuries, although other life-history stages still need to be examined for sensitivity and potential interactive effects with increasing temperatures should be investigated.
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... The juvenile phase is a crucial phase for the growth of spiny lobsters. The early juvenile stage is the key to the transition from the larval (planktonic) stage to the adult (benthic) stage, characterized by high mortality (Small et al., 2016). Searching for information related to natural food for juveniles in their natural habitat is urgently needed to develop aquaculture as a basis for managing feeding to increase the chances of success in raising lobster seeds. ...
FOOD PREFERENCES OF EARLY JUVENILE SCALLOPED SPINY LOBSTER IN EKAS BAY, LOMBOK, INDONESIA
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Ekas Bay is the largest bay on the island of Lombok which is the location for catching and cultivating spiny lobsters. This research was conducted from May to July 2021 on the Scalloped spiny lobster (Panulirus homarus). This study aims to identify the types of natural foods consumed and determine the preferred types of food, as well as the early juvenile feeding time of Scalloped spiny lobster located in Ekas Bay, East Lombok Regency, West Nusa Tenggara Province (NTB). Puerulus samples were collected in the last week of May 2021, enlarged puerulus was performed in submerged cages measuring 15 cm × 15 cm × 15 cm, mesh size <3 mm, with a density of 4 puerulus/m 2. The cages are placed at a location 70 m to the sea from the shoreline, at a depth of 0.5, 1.0, and 1.5 m. After reaching the juvenile phase, lobsters are collected during the new and full moon phases (06.00 am, 06.00 pm and 12.00 am, respectively) in June to July 2021. A total of 60 individual juvenile lobsters (algal phase) were analyzed for their stomach contents. The average percentage of the total Index of Relative Important (IRI) obtained for the identified taxa were bivalves (22.32%), copepods (23.64%), demosponges (24.98%), while digestibdle material was 29.06%. The electivity index data (Ei) shows that lobsters prefer bivalves over other taxa. Lobster samples taken in the morning had a stomach fullness rate of 50%, indicating active feeding at night. KEYWORDS: Spiny lobster; Ekas Bay; Food Preferences; Juvenile
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Article
  • Jul 1989
Submerged lobsters at 15°C were normoxaemic ( at a of 6·53 kPa) and normocapnie (; [HCO3-] = 9·3mequivl-1 and pHa = 7·78). After 3h in air the haemolymph was markedly hypoxic and hypercapnic (; ; and pHa = 7·64). Disturbance after 3h in air caused a greater increase in to 1·28 kPa and a fourfold increase in lactate levels to 3·6 mmol l-1. The combined respiratory and metabolic acidosis reduced pHa to 7·39. After 14 h in air, undisturbed lobsters remained hypoxic and hypercapnic (; ). Lactate levels had increased to 6·2mmoll-1. Despite this clear limit on respiratory gas exchange in air, oxygen transport by the haemolymph was restored. A rise in buffer base ([HCO3-] = 15·8mequivl-1) compensated for the potential respiratory and metabolic acidosis and pH was unchanged at 7·63. The combined effects of the increase in lactate (ΔlogP50/ Δlog[lactate] =–0·175) and calcium (ΔlogP50/Δlog[Ca2+] = — 0·20 at pH7·63) levels contributed to an increase in oxygen affinity of haemocyanin at constant pH. Consequently, mean increased from 0·2 to 0·38 mmol l-1 between 3h and 14 h in air. Resubmergence after 14 h in air resulted in a transient alkalosis due to retention of bicarbonate; oxygen and CO2 were rapidly restored to submerged levels. The lobster possesses the appropriate respiratory adaptations for survival during the relatively long periods of exposure in air encountered during commercial shipment.
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Metabolic Depression During Environmental Stress: The Role of Extracellular Versus Intracellular pH in Sipunculus Nudus
Article
  • Aug 1996
Environmental stresses such as hypoxia or hypercapnia are known to cause acid-base disturbances and in several organisms they lead to metabolic depression. The present study was undertaken to quantify the influence of these changes in acid-base parameters on metabolic rate. We determined the rate of oxygen consumption in a non-perfused preparation of the body wall musculature of the marine worm Sipunculus nudus at various levels of extra- and intracellular pH (pHe and pHi, respectively), P(CO2) and [HCO3-]. The acid-base status of the tissue was modified and clamped by long- term exposure to media set to specific values of extracellular pH, P(CO2) and [HCO3-]. At a pile of 7.90, which is equivalent to the normoxic normocapnic in vivo extracellular pH, and an ambient P(CO2) of 0.03 kPa (control conditions), pHi was 7.26±0.02 (mean ± S.D., N=5). A reduction of extracellular pH from 7.90 to 7.20 resulted in a significant decrease of phi to 7.17±0.05 at 0.03 kPa P(CO2) (normocapnia) and to 7.20±0.02 at 1.01 kPa P(CO2) (hypercapnia). At the same time, the rate of oxygen consumption of the tissue was significantly depressed by 18.7±4.7% and 17.7±3.0%, respectively. A significant depression of oxygen consumption by 13.7±4.7 % also occurred under hypercapnia at pHe 7.55 when pHi was elevated above control values (7.32±0.01). No significant changes in oxygen consumption were observed when pile was either drastically elevated to 8.70 under normocapnia (pHi 7.36±0.05) or maintained at 7.90 during hypercapnia (pHi 7.37±0.03). ATP and phospho-L-arginine concentrations, as well as the Gibbs free energy change of ATP hydrolysis (dG/dξ(ATP)), were maintained at high levels during all treatments, indicating an equilibrium between energy supply and demand. We conclude that the depression of aerobic energy turnover in isolated body wall musculature of S. nudus is induced by low extracellular pH. A model is proposed which could explain a reduced ATP cost of phi regulation during extracellular acidosis, thus contributing to metabolic depression.
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