scholarly journals Tolerant Larvae and Sensitive Juveniles: Integrating Metabolomics and Whole-Organism Responses to Define Life-Stage Specific Sensitivity to Ocean Acidification in the American Lobster

Metabolites ◽  
2021 ◽  
Vol 11 (9) ◽  
pp. 584
Author(s):  
Fanny Noisette ◽  
Piero Calosi ◽  
Diana Madeira ◽  
Mathilde Chemel ◽  
Kayla Menu-Courey ◽  
...  

Bentho-pelagic life cycles are the dominant reproductive strategy in marine invertebrates, providing great dispersal ability, access to different resources, and the opportunity to settle in suitable habitats upon the trigger of environmental cues at key developmental moments. However, free-dispersing larvae can be highly sensitive to environmental changes. Among these, the magnitude and the occurrence of elevated carbon dioxide (CO2) concentrations in oceanic habitats is predicted to exacerbate over the next decades, particularly in coastal areas, reaching levels beyond those historically experienced by most marine organisms. Here, we aimed to determine the sensitivity to elevated pCO2 of successive life stages of a marine invertebrate species with a bentho-pelagic life cycle, exposed continuously during its early ontogeny, whilst providing in-depth insights on their metabolic responses. We selected, as an ideal study species, the American lobster Homarus americanus, and investigated life history traits, whole-organism physiology, and metabolomic fingerprints from larval stage I to juvenile stage V exposed to different pCO2 levels. Current and future ocean acidification scenarios were tested, as well as extreme high pCO2/low pH conditions that are predicted to occur in coastal benthic habitats and with leakages from underwater carbon capture storage (CCS) sites. Larvae demonstrated greater tolerance to elevated pCO2, showing no significant changes in survival, developmental time, morphology, and mineralisation, although they underwent intense metabolomic reprogramming. Conversely, juveniles showed the inverse pattern, with a reduction in survival and an increase in development time at the highest pCO2 levels tested, with no indication of metabolomic reprogramming. Metabolomic sensitivity to elevated pCO2 increased until metamorphosis (between larval and juvenile stages) and decreased afterward, suggesting this transition as a metabolic keystone for marine invertebrates with complex life cycles.

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Travis C. Tai ◽  
Piero Calosi ◽  
Helen J. Gurney-Smith ◽  
William W. L. Cheung

AbstractOcean acidification (OA) affects marine organisms through various physiological and biological processes, yet our understanding of how these translate to large-scale population effects remains limited. Here, we integrated laboratory-based experimental results on the life history and physiological responses to OA of the American lobster, Homarus americanus, into a dynamic bioclimatic envelope model to project future climate change effects on species distribution, abundance, and fisheries catch potential. Ocean acidification effects on juvenile stages had the largest stage-specific impacts on the population, while cumulative effects across life stages significantly exerted the greatest impacts, albeit quite minimal. Reducing fishing pressure leads to overall increases in population abundance while setting minimum size limits also results in more higher-priced market-sized lobsters (> 1 lb), and could help mitigate the negative impacts of OA and concurrent stressors (warming, deoxygenation). However, the magnitude of increased effects of climate change overweighs any moderate population gains made by changes in fishing pressure and size limits, reinforcing that reducing greenhouse gas emissions is most pressing and that climate-adaptive fisheries management is necessary as a secondary role to ensure population resiliency. We suggest possible strategies to mitigate impacts by preserving important population demographics.


2019 ◽  
Vol 39 (4) ◽  
pp. 468-476 ◽  
Author(s):  
Amalia M Harrington ◽  
Heather J Hamlin

ABSTRACT Increased anthropogenic input of carbon dioxide into the atmosphere has caused widespread patterns of ocean acidification (OA) and increased the frequency of extreme warming events. We explored the sublethal effects of OA on the hemolymph chemistry and physiological response to acute thermal stress in the American lobster (Homarus americanus H. Milne Edwards, 1837). We exposed subadult lobsters to current or predicted end-century pH conditions (8.0 and 7.6, respectively) for 60 days. Following exposure, we assessed hemolymph L-lactate and calcium concentrations (as indicators of oxygen carrying capacity), ecdysterone concentrations, total protein content, and total hemocyte counts (THCs) as an indicator of immune response. We also assessed cardiac performance in the context of an acute warming event using impedance pneumography. Calcium, total protein, and ecdysterone concentrations were not significantly altered (P ≥ 0.10) by OA exposure. Control lobsters, however, had significantly higher levels of L-lactate concentrations compared to acidified lobsters, suggesting reduced oxygen carrying capacity under OA. THCs were also 61% higher in control versus acidified lobsters, suggesting immunosuppression under chronic OA. Lobsters exposed to acidified conditions exhibited reduced cardiac performance under acute warming as indicated by significantly lower (P = 0.040) Arrhenius Break Temperatures compared to control lobsters. These results suggest that although some physiological endpoints of American lobster are not impacted by OA, the stress of OA will likely be compounded by acute heat shock and may present additional physiological challenges for this species in the face of future change.


2017 ◽  
Vol 13 (2) ◽  
pp. 20160797 ◽  
Author(s):  
Sue-Ann Watson ◽  
Jennifer B. Fields ◽  
Philip L. Munday

Ocean acidification poses a range of threats to marine invertebrates; however, the emerging and likely widespread effects of rising carbon dioxide (CO 2 ) levels on marine invertebrate behaviour are still little understood. Here, we show that ocean acidification alters and impairs key ecological behaviours of the predatory cone snail Conus marmoreus . Projected near-future seawater CO 2 levels (975 µatm) increased activity in this coral reef molluscivore more than threefold (from less than 4 to more than 12 mm min −1 ) and decreased the time spent buried to less than one-third when compared with the present-day control conditions (390 µatm). Despite increasing activity, elevated CO 2 reduced predation rate during predator–prey interactions with control-treated humpbacked conch, Gibberulus gibberulus gibbosus ; 60% of control predators successfully captured and consumed their prey, compared with only 10% of elevated CO 2 predators. The alteration of key ecological behaviours of predatory invertebrates by near-future ocean acidification could have potentially far-reaching implications for predator–prey interactions and trophic dynamics in marine ecosystems. Combined evidence that the behaviours of both species in this predator–prey relationship are altered by elevated CO 2 suggests food web interactions and ecosystem structure will become increasingly difficult to predict as ocean acidification advances over coming decades.


2015 ◽  
Vol 73 (3) ◽  
pp. 970-980 ◽  
Author(s):  
Julia D. Sigwart ◽  
Gillian Lyons ◽  
Artur Fink ◽  
Magdalena A. Gutowska ◽  
Darren Murray ◽  
...  

Abstract Ocean acidification is an escalating environmental issue and associated changes in the ocean carbonate system have implications for many calcifying organisms. The present study followed the growth of Sepia officinalis from early-stage embryos, through hatching, to 7-week-old juveniles. Responses of cuttlefish to elevated pCO2 (hypercapnia) were investigated to test the impacts of near-future and extreme ocean acidification conditions on growth, developmental time, oxygen consumption, and yolk utilization as proxies for individual fitness. We further examined gross morphological characteristics of the internal calcareous cuttlebone to determine whether embryonically secreted shell lamellae are impacted by environmental hypercapnia. Embryonic growth was reduced and hatching delayed under elevated pCO2, both at environmentally relevant levels (0.14 kPa pCO2 similar to predicted ocean conditions in 2100) and extreme conditions (0.40 kPa pCO2). Comparing various metrics from control and intermediate treatments generally showed no significant difference in experimental measurements. Yet, results from the high pCO2 treatment showed significant changes compared with controls and revealed a consistent general trend across the three treatment levels. The proportion of animal mass contributed by the cuttlebone increased in both elevated pCO2 treatments. Gross cuttlebone morphology was affected under such conditions and cuttlebones of hypercapnic individuals were proportionally shorter. Embryonic shell morphology was maintained consistently in all treatments, despite compounding hypercapnia in the perivitelline fluid; however, post-hatching, hypercapnic animals developed denser cuttlebone laminae in shorter cuttlebones. Juvenile cuttlefish in acidified environments thus experience lower growth and yet increased calcification of their internal shell. The results of this study support recent findings that early cuttlefish life stages are more vulnerable towards hypercapnia than juveniles and adults, which may have negative repercussions on the biological fitness of cuttlefish hatchlings in future oceans.


2016 ◽  
Vol 74 (4) ◽  
pp. 1210-1219 ◽  
Author(s):  
Jesica D. Waller ◽  
Richard A. Wahle ◽  
Halley McVeigh ◽  
David M. Fields

Few studies have evaluated the joint effects of elevated temperature and pCO2 on marine organisms. In this study we investigated the interactive effects of Intergovernmental Panel on Climate Change predicted temperature and pCO2 for the end of the 21st century on key aspects of larval development of the American lobster, Homarus americanus, an otherwise well-studied, iconic, and commercially prominent species in the northeastern United States and Atlantic Canada. Our experiments showed that larvae (stages I–III) and postlarvae (stage IV) reared in the high temperature treatments (19 °C) experienced significantly lower survival, developed twice as fast, and had significantly higher oxygen consumption rates, than those in ambient treatments (16 °C). Larvae from the ambient temperature/high pCO2 (750 ppm) treatment had significantly longer carapace lengths, greater dry masses in stages I–III and higher C: N ratios in stage IV than larvae from all other treatments. Stage IVs raised in the high pCO2 treatment at 19 °C had significantly higher feeding rates and swimming speeds than stage IVs from the other three treatments. Together these results suggest that projected end-century warming will have greater adverse effects than increased pCO2 on larval survival, and changing pCO2 may have a complex effect on larval metabolism and behaviour. Understanding how the most vulnerable life stages of the lobster life cycle respond to climate change is essential in connecting the northward geographic shifts projected by habitat quality models, and the underlying physiological and genetic mechanisms that drive their ecology.


2015 ◽  
Vol 73 (3) ◽  
pp. 951-961 ◽  
Author(s):  
Kit Yu Karen Chan ◽  
Daniel Grünbaum ◽  
Maj Arnberg ◽  
Sam Dupont

Abstract Ocean acidification (OA) is widely recognized as an increasing threat to marine ecosystems. Many marine invertebrates have dual-phase life cycles in which planktonic larvae connect and sustain otherwise disconnected benthic adult populations. Many planktonic larvae are particularly sensitive to environmental stresses including OA. Here, we compared the developmental dynamics, survivorship, and swimming behaviours of plutei of two ecologically important echinoderm species that naturally experience variability in ambient pH: the purple urchin Strongylocentrotus purpuratus and the infaunal brittlestar Amphiura filiformis. Sensitivity to decreased pH differed between these two species and between maternal lineages. Larvae of both species experienced increased mortality and reduced growth rate under low pH conditions. However, larval brittlestars appeared more sensitive and experienced over 80% mortality after 7-d exposure to pH 7.7. Larval urchins from one maternal lineage underwent highly synchronized budding (release of blastula-like particles) at low pH. Observed budding temporarily increased numerical density and reduced individual size, leading to differences in growth and mortality rates between the two half-sibling groups and another population. Swimming speeds of larval brittlestars were reduced in decreased pH. In contrast, acidification had either no effect or positive effect on swimming speeds of larval urchins. The observed differences between species may be a reflection of pre-exposure in their natural habitats: larval brittlestars experience a relatively stable in situ pH environment, whereas larval urchins are occasionally exposed to low pH in upwelling regions. Urchins may therefore exhibit short-term compensatory responses such as budding and increased swimming speed. Natural selection could act upon the significant variations we observed between maternal lineages, resulting in more resilient populations confronting chronic exposure to OA.


2020 ◽  
Vol 77 (5) ◽  
pp. 1685-1697
Author(s):  
Marthe Larsen Haarr ◽  
Michel Comeau ◽  
Jöel Chassé ◽  
Rémy Rochette

Abstract Increasing ocean temperatures may affect life cycles of organisms whose biological processes are temperature-dependent. Our objective was to determine whether hatching time of American lobster (Homarus americanus), which has a 2-year reproductive cycle, has advanced in the southern Gulf of St Lawrence, Canada, in response to rising temperature. We investigated temporal trends in hatching time 1989–2014 using fisheries monitoring data. We considered two metrics: the first week of the year when ovigerous females with prehatch or hatching clutches were observed [onset-of-hatching (OH)] and the rate of change in the ratio of females with prehatch/hatching vs. developing clutches each spring fishing season [rate of clutch development (RCD)]. OH advanced by 5 weeks and RCD increased by 40% on average. Comparisons of OH and RCD to cumulative degree-days going back 2 years prior to hatching suggested an effect of higher fall temperatures during early ovarian and embryonic development. The advancement of hatching time in response to environmental conditions 6–18 months before hatching occurs could lead to a mismatch with larval prey species with shorter life cycles. These findings highlight the importance of monitoring phenology of fished species and the need for further research into potential impacts of phenological changes.


2015 ◽  
Vol 73 (3) ◽  
pp. 715-726 ◽  
Author(s):  
Sam H. C. Noonan ◽  
Katharina E. Fabricius

Abstract Increasing carbon dioxide (CO2) emissions are raising sea surface temperature (SST) and causing ocean acidification (OA). While higher SST increases the frequency of mass coral bleaching events, it is unclear how OA will interact to affect this process. In this study, we combine in situ bleaching surveys around three tropical CO2 seeps with a 2-month two-factor (CO2 and temperature) tank experiment to investigate how OA and SST in combination will affect the bleaching susceptibility of tropical reef corals. Surveys at CO2 seep and control sites during a minor regional bleaching event gave little indication that elevated pCO2 influenced the bleaching susceptibility of the wider coral community, the four most common coral families (Acroporidae, Faviidae, Pocilloporidae, or Poritidae), or the thermally sensitive coral species Seriatopora hystrix. In the tank experiment, sublethal bleaching was observed at 31°C after 5 d in S. hystrix and 12 d in Acropora millepora, whereas controls (28°C) did not bleach. None of the measured proxies for coral bleaching was negatively affected by elevated pCO2 at pHT 7.79 (vs. 7.95 pHT in controls), equivalent to ∼780 µatm pCO2 and an aragonite saturation state of 2.5. On the contrary, high pCO2 benefitted some photophysiological measures (although temperature effects were much stronger than CO2 effects): maximum photosystem II quantum yields and light-limited electron transport rates increased in both species at high pCO2, whereas gross photosynthesis and pigment concentrations increased in S. hystrix at high pCO2. The field and laboratory data in combination suggest that OA levels up to a pHT of 7.8 will have little effect on the sensitivity of tropical corals to thermal bleaching. Indeed, some species appear to be able to utilize the more abundant dissolved inorganic carbon to increase productivity; however, these gains offset only a small proportion of the massive bleaching-related energy losses during thermal stress.


Author(s):  
Samuel J. Gurr ◽  
Shelly A. Trigg ◽  
Brent Vadopalas ◽  
Steven B. Roberts ◽  
Hollie M. Putnam

Whereas low levels of thermal stress, irradiance, and dietary restriction can have beneficial effects for many taxa, stress acclimation remains understudied in marine invertebrates, despite being threatened by climate change stressors such as ocean acidification. To test for life-stage and stress-intensity dependence in eliciting enhanced tolerance under subsequent stress encounters, we initially conditioned pediveliger Pacific geoduck (Panopea generosa) larvae to (i) ambient and moderately elevated pCO2 (920 µatm and 2800 µatm, respectively) for 110 days, (ii) secondarily applied a 7-day exposure to ambient, moderate, and severely elevated pCO2 (750 µatm, 2800 µatm, and 4900 µatm, respectively), followed by 7 days in ambient conditions, and (iii) implemented a 7-day third exposure to ambient (970 µatm) and moderate pCO2 (3000 µatm). Initial conditioning to moderate pCO2 stress followed by second and third exposure to severe and moderate pCO2 stress increased respiration rate, organic biomass, and shell size suggesting a stress-intensity-dependent effect on energetics. Additionally, stress-acclimated clams had lower antioxidant capacity compared to clams under ambient conditions, supporting the hypothesis that stress over postlarval-to-juvenile development affects oxidative status later in life. Time series and stress intensity-specific approaches can reveal life-stages and magnitudes of exposure, respectively, that may elicit beneficial phenotypic variation.


2011 ◽  
Vol 8 (2) ◽  
pp. 2329-2356 ◽  
Author(s):  
P. L. Munday ◽  
V. Hernaman ◽  
D. L. Dixson ◽  
S. R. Thorrold

Abstract. Calcification in many invertebrate species is predicted to decline due to ocean acidification. The potential effects of elevated pCO2 and reduced carbonate saturation state on other species, such as fish, are less well understood. Fish otoliths (earbones) are composed of aragonite, and thus, might be susceptible to either the reduced availability of carbonate ions in seawater at low pH, or to changes in extracellular concentrations of bicarbonate and carbonate ions caused by acid-base regulation in fish exposed to high pCO2. We reared larvae of the clownfish Amphiprion percula from hatching to settlement at three pHNBS and pCO2 levels (control: pH 8.15 and 404 μatm CO2; intermediate: pH 7.8 and 1050 μatm CO2; extreme: pH 7.6 and 1721 μatm CO2) to test the possible effects of ocean acidification on otolith development. There was no effect of the intermediate treatment (pH 7.8 and 1050 μatm CO2) on otolith size, shape, symmetry between left and right otoliths, or otolith elemental chemistry, compared with controls. However, in the more extreme treatment (pH 7.6 and 1721 μatm CO2) otolith area and maximum length were larger than controls, although no other traits were affected. Our results support the hypothesis that pH regulation in the otolith endolymph of fish exposed to elevated pCO2 can lead to increased precipitation of CaCO3 in otoliths of larval fish, as proposed by an earlier study, however, our results also show that sensitivity varies considerably among species. Importantly, our results suggest that otolith development in clownfishes is robust to even the more pessimistic changes in ocean chemistry predicted to occur by 2100.


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