MEPS

Marine Ecology Progress Series

MEPS is a leading hybrid research journal on all aspects of marine, coastal and estuarine ecology. Priority is given to outstanding research that advances our ecological understanding.

Online: ISSN 1616-1599

Print: ISSN 0171-8630

DOI: https://doi.org/10.3354/meps

Impact Factor2.1 (JCR 2025 release)

Article Acceptance Rate52.2% (2024)

Average Time in Review216 days (2024)

Total Annual Downloads2.961.862 (2025)

Volume contents
Mar Ecol Prog Ser 770:45-61 (2025)

Effects of multiple stressors on embryos and emerging larvae of the American lobster

ABSTRACT:

Environmental changes in the ocean can impose significant physiological costs and morphological changes to many marine organisms, and early life stages such as eggs and larvae are predicted to be particularly vulnerable to climate change drivers including warming and acidification. Although sensitivity to ocean change stressors during development has the potential to influence the performance, and ultimately the recruitment, of postlarvae and juveniles, the nature and strength of physiological modifications during embryo development is understudied in the ecologically and economically important American lobster Homarus americanus. We investigated the long-term, interactive impacts of ocean acidification and ocean warming on the development and physiology of brooded lobster embryos. We exposed ovigerous females to a combination of 2 temperatures and 2 pH levels for 5 mo, throughout which we measured development, metabolic rate, biochemical composition, and enzyme activity in their brooded embryos. The physiology of American lobster embryos appears to be robust to ocean acidification conditions but sensitive to warming, particularly for metabolic traits. We also found that warming induced a reduction in the size of freshly hatched larvae. Understanding how environmental change influences these early life stages of lobsters can improve predictions for how this species will fare in a changing ocean environment.

KEYWORDS

Aiken DE, Waddy SL (1986) Environmental influence on recruitment of the American lobster Homarus americanus: a perspective. Can J Fish Aquat Sci 43:2258-2270 Crossref

Alter K, Jacquemont J, Claudet J, Lattuca ME and others (2024) Hidden impacts of ocean warming and acidification on biological responses of marine animals revealed through meta-analysis. Nat Commun 15:2885 PubMedCrossref

Anger K, Storch V, Anger V, Capuzzo JM (1985) Effects of starvation on moult cycle and hepatopancreas of Stage I lobster (Homarus americanus) larvae. Helgol Meeresunters 39:107-116 Crossref

Atkinson D (1994) Temperature and organism size—a biological law for ectotherms? Adv Ecol Res 25:1-58 Crossref

Baeza J, Fernández M (2002) Active brood care in Cancer setosus (Crustacea: Decapoda): the relationship between female behaviour, embryo oxygen consumption and the cost of brooding. Funct Ecol 16:241-251 Crossref

Baeza JA, Simpson L, Ambrosio LJ, Mora N, Guéron R, Childress MJ (2016) Active parental care, reproductive performance, and a novel egg predator affecting reproductive investment in the Caribbean spiny lobster Panulirus argus. BMC Zool 1:6 Crossref

Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. JStat Software 67(1):1-48

Brickman D, Alexander MA, Pershing A, Scott JD, Wang Z (2021) Projections of physical conditions in the Gulf of Maine in 2050. Elementa Sci Anthropocene 9:00055 Crossref

Campbell A (1990) Aggregations of berried lobsters (Homatus [sic] americanus) in shallow waters off Grand Manan, Eastern Canada. Can J Fish Aquat Sci 47:520-523 Crossref

Campbell A, Pezzack DS (1986) Relative egg production and abundance of berried lobsters, Homarus americanus, in the Bay of Fundy and off Southwestern Nova Scotia. Can J Fish Aquat Sci 43:2190-2196 Crossref

Carloni JT, Wahle R, Geoghegan P, Bjorkstedt E (2018) Bridging the spawner-recruit disconnect: trends in American lobster recruitment linked to the pelagic food web. Bull Mar Sci 94:719-735 Crossref

Carloni JT, Goldstein JS, Watson WH III (2021) Movements of egg-bearing American lobsters Homarus americanus during late stage brooding and hatching. Mar Ecol Prog Ser 661:163-173 Crossref

Carter HA, Ceballos-Osuna L, Miller NA, Stillman JH (2013) Impact of ocean acidification on metabolism and energetics during early life stages of the intertidal porcelain crab Petrolisthes cinctipes. J Exp Biol 216:1412-1422 PubMedCrossref

Castro KM, Cobb JS, Gomez-Chiarri M, Tlusty M (2012) Epizootic shell disease in American lobsters Homarus americanus in southern New England: past, present and future. Dis Aquat Org 100:149-158 PubMedCrossref

Ceballos-Osuna L, Carter HA, Miller NA, Stillman JH (2013) Effects of ocean acidification on early life-history stages of the intertidal porcelain crab Petrolisthes cinctipes. J Exp Biol 216:1405-1411 PubMedCrossref

Chassé J, Miller RJ (2010) Lobster larval transport in the southern Gulf of St. Lawrence. Fish Oceanogr 19:319-338 Crossref

Ciais P, Gasser T, Paris JD, Caldeira K and others (2013) Attributing the increase in atmospheric CO2 to emitters and absorbers. Nat Clim Change 3:926-930 Crossref

Cowan DF, Watson WH III, Solow AR, Mountcastle AM (2007) Thermal histories of brooding lobsters, Homarus americanus, in the Gulf of Maine. Mar Biol 150:463-470 Crossref

Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 measurements. PICES Special Publication 3

Doney SC, Balch WM, Fabry VJ, Feely RA (2009) Ocean acidification: a critical emerging problem. Oceanography 22:16-25 Crossref

Eriksson SP, Nabbing M, Sjöman E (2006) Is brood care in Nephrops norvegicus during hypoxia adaptive or a waste of energy? Funct Ecol 20:1097-1104 Crossref

Esmann M (1988) ATPase and phosphatase activity of Na+,K+-ATPase: molar and specific activity, protein determination. Methods Enzymol 156:105-115 Crossref

Estrella BT, Cadrin SX (1995) Fecundity of the American lobster (Homarus americanus) in Massachusetts coastal waters. ICES Mar Sci Symp 199:61-72

Fernández M, Pardo LM, Baeza JA (2002) Patterns of oxygen supply in embryo masses of brachyuran crabs throughout development: the effect of oxygen availability and chemical cues in determining female brooding behavior. Mar Ecol Prog Ser 245:181-190 Crossref

Förster C, Baeza JA (2001) Active brood care in the anomuran crab Petrolisthes violaceus (Decapoda: Anomura: Procellanidae): grooming of brooded embryos by the fifth pereiopods. J Crustac Biol 21:606-615 Crossref

Forster J, Hirst AG (2012) The temperature-size rule emerges from ontogenetic differences between growth and development rates. Funct Ecol 26:483-492 Crossref

Forster J, Hirst AG, Atkinson D (2012) Warming-induced reductions in body size are greater in aquatic than terrestrial species. Proc Natl Acad Sci USA 109:19310-19314 PubMedCrossref

Friends of Casco Bay (2024) Continuous monitoring stations. Link

Gattuso JP, Epitalon JM, Lavigne H, Orr J (2022) seacarb: seawater carbonate chemistry. R package version 3.3.2. CRAN.R-project.org/package=seacarb

Glas PS, Courtney LA, Rayburn JR, Fisher WS (1997) Embryonic coat of the grass shrimp Palaemonetes pugio. Biol Bull 192:231-242 PubMedCrossref

Gledhill DK, White MM, Salisbury J, Thomas H and others (2015) Ocean and coastal acidification off New England and Nova Scotia. Oceanography 28:182-197 Crossref

Goldstein JS, Watson WH III (2015) Seasonal movements of American lobsters in southern Gulf of Maine coastal waters: patterns, environmental triggers, and implications for larval release. Mar Ecol Prog Ser 524:197-211 Crossref

Goldstein JS, Watson WH III (2015) Influence of natural inshore and offshore thermal regimes on egg development and time of hatch in American lobsters, Homarus americanus. Biol Bull 228:1-12 PubMedCrossref

Goldstein JS, Watson WH III (2019) Biochemical changes throughout early- and middle-stages of embryogenesis in lobsters (Homarus americanus) under different thermal regimes. PeerJ 7:e6952 PubMedCrossref

Goldstein JS, Zarrella-Smith KA, Pugh TL (2022) Recent declines in American lobster fecundity in southern New England: drivers and implications. ICES J Mar Sci 79:1662-1674 Crossref

Goldstein JS, Grizzle RE, Watson WH III (2025) Habitat composition influences residency and seasonal lobster movements in the Great Bay Estuary, New Hampshire. Estuaries Coasts 48:2 Crossref

Gravinese PM (2018) Ocean acidification impacts the embryonic development and hatching success of the Florida stone crab, Menippe mercenaria. J Exp Mar Biol Ecol 500:140-146 Crossref

Hamdoun A, Epel D (2007) Embryo stability and vulnerability in an always changing world. Proc Natl Acad Sci USA 104:1745-1750 PubMedCrossref

Helluy SM, Beltz BS (1991) Embryonic development of the American lobster (Homarus americanus): quantitative staging and characterization of an embryonic molt cycle. Biol Bull 180:355-371 PubMedCrossref

Henry RP, Wheatly MG (1992) Interaction of respiration, ion regulation, and acid-base balance in the everyday life of aquatic crustaceans. Am Zool 32:407-416 Crossref

Hodgdon CT, Khalsa NS, Mazur MD, Chen Y (2022) Climate-driven changes in growth and size at maturity of Gulf of Maine lobster stocks: implications for stock assessment models. Fish Bull 120:240-251 Crossref

Hunt CW, Salisbury JE, Vandemark D (2022) Controls on buffering and coastal acidification in a temperate estuary. Limnol Oceanogr 67:1328-1342 Crossref

Jury SH, Watson WH III (2000) Thermosensitivity of the lobster, Homarus americanus, as determined by cardiac assay. Biol Bull 199:257-264 PubMedCrossref

Jury SH, Gutzler BC, Goldstein JS, Carloni JT, Watson WH (2024) Behavioral thermoregulation of ovigerous American lobsters (Homarus americanus). Fish Res 278:107068 Crossref

Keppel EA, Scrosati RA, Courtenay SC (2012) Ocean acidification decreases growth and development in American lobster (Homarus americanus) larvae. J Northwest Atl Fish Sci 44:61-66 Crossref

Khodabandeh S, Charmantier G, Charmantier-Daures M (2006) Immunolocalization of Na+,K+-ATPase in osmoregulatory organs during the embryonic and post-embryonic development of the lobster Homarus gammarus. J Crustac Biol 26:515-523 Crossref

Le Bris A, Mills KE, Wahle RA, Chen Y and others (2018) Climate vulnerability and resilience in the most valuable North American fishery. Proc Natl Acad Sci USA 115:1831-1836 PubMedCrossref

Lemoine NP, Burkepile DE (2012) Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 93:2483-2489 PubMedCrossref

Leong PKK, Manahan DT (1997) Metabolic importance of Na+/K+-ATPase activity during sea urchin development. J Exp Biol 200:2881-2892 PubMedCrossref

Long WC, Swiney KM, Foy RJ (2013) Effects of ocean acidification on the embryos and larvae of red king crab, Paralithodes camtschaticus. Mar Pollut Bull 69:38-47 PubMedCrossref

Long WC, Swiney KM, Foy RJ (2016) Effects of high pCO2 on Tanner crab reproduction and early life history, Part II: carryover effects on larvae from oogenesis and embryogenesis are stronger than direct effects. ICES J Mar Sci 73:836-848 Crossref

Lucu C, Towle DW (2003) Na(+)+K(+)-ATPase in gills of aquatic crustacea. Comp Biochem Physiol A Mol Integr Physiol 135:195-214 PubMedCrossref

Lueker TJ, Dickson AG, Keeling CD (2000) Ocean pCO2 calculated from dissolved inorganic carbon, alkalinity, and equations for K1 and K2: validation based on laboratory measurements of CO2 in gas and seawater at equilibrium. Mar Chem 70:105-119

Lyons GN, Halsey LG, Pope EC, Eddington JD, Houghton JDR (2013) Energy expenditure during activity in the American lobster Homarus americanus: correlations with body acceleration. Comp Biochem Physiol A Mol Integr Physiol 166:278-284 PubMedCrossref

Maas AE, Lawson GL, Bergan AJ, Wang ZA, Tarrant AM (2020) Seasonal variation in physiology and shell condition of the pteropod Limacina retroversa in the Gulf of Maine relative to life cycle and carbonate chemistry. Prog Oceanogr 186:102371 Crossref

Marsh A, Manahan D (1999) A method for accurate measurements of the respiration rates of marine invertebrate embryos and larvae. Mar Ecol Prog Ser 184:1-10

McMahan MD, Cowan DF, Chen Y, Sherwood GD, Grabowski JH (2016) Growth of juvenile American lobster Homarus americanus in a changing environment. Mar Ecol Prog Ser 557:177-187 Crossref

Mills KE, Pershing AJ, Brown CJ, Chen Y and others (2013) Fisheries management in a changing climate: lessons from the 2012 ocean heat wave in the Northwest Atlantic. Oceanography 26:191-195 Crossref

Monteiro JN, Bueno-Pardo J, Pinto M, Pardal MA, Martinho F, Leitão F (2023) Implications of warming on the morphometric and reproductive traits of the green crab, Carcinus maenas. Fishes 8:485 Crossref

Moore EM, Langley TG, Goldstein JS, Watson WH (2020) American lobster, Homarus americanus, reproduction and recruitment in a New England estuary. Estuaries Coasts 43:2141-2151 Crossref

Morse BL, Comeau M, Rochette R (2018) Ontogenetic changes in movement patterns and activity levels of American lobsters (Homarus americanus) in Anse-Bleue, southern Gulf of St. Lawrence. J Exp Mar Biol Ecol 505:12-23 Crossref

Niemisto M, Fields DM, Clark KF, Waller JD, Greenwood SJ, Wahle RA (2021) American lobster postlarvae alter gene regulation in response to ocean warming and acidification. Ecol Evol 11:806-819 PubMedCrossref

Noisette F, Calosi P, Madeira D, Chemel M and others (2021) 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 11:584 PubMedCrossref

Pardo JCF, Costa TM (2021) Multiple-stressor effects of warming and acidification on the embryonic development of an estuarine fiddler crab. Estuar Coast Shelf Sci 254:107296 Crossref

Perez FF, Fraga F (1987) Association constant of fluoride and hydrogen ions in seawater. Mar Chem 21:161-168

Perkins HC (1972) Developmental rates at various temperatures of embryos of the northern lobster (Homarus americanus Milne-Edwards). Fish Bull 70(1)

Pershing AJ, Alexander MA, Hernandez CM, Kerr LA and others (2015) Slow adaptation in the face of rapid warming leads to collapse of the Gulf of Maine cod fishery. Science 350:809-812 PubMedCrossref

Pershing AJ, Mills KE, Dayton AM, Franklin BS, Kennedy BT (2018) Evidence for adaptation from the 2016 marine heatwave in the Northwest Atlantic Ocean. Oceanography 31:152-161 Crossref

Pershing AJ, Alexander MA, Brady DC, Brickman D and others (2021) Climate impacts on the Gulf of Maine ecosystem. Elementa Sci Anthropocene 9:00076 Crossref

Pinsky ML, Worm B, Fogarty MJ, Sarmiento JL, Levin SA (2013) Marine taxa track local climate velocities. Science 341:1239-1242 PubMedCrossref

Qadri SA, Camacho J, Wang H, Taylor JR, Grosell M, Worden MK (2007) Temperature and acid-base balance in the American lobster Homarus americanus. J Exp Biol 210:1245-1254 PubMedCrossref

Quinn BK (2017) Threshold temperatures for performance and survival of American lobster larvae: a review of current knowledge and implications to modeling impacts of climate change. Fish Res 186:383-396

R Core Team (2024) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

Romero MC, Tapella F, Stevens B, Buck CL (2010) Effects of reproductive stage and temperature on rates of oxygen consumption in Paralithodes platypus (Decapoda: Anomura). J Crustac Biol 30:393-400 Crossref

Sal Moyano MP, Ceraulo M, Luppi T, Gavio MA, Buscaino G (2023) Anthropogenic and biological sound effects on the maternal care behavior of a key crab species. Front Mar Sci 10:1050148 Crossref

Salisbury JE, Jönsson BF (2018) Rapid warming and salinity changes in the Gulf of Maine alter surface ocean carbonate parameters and hide ocean acidification. Biogeochemistry 141:401-418 PubMedCrossref

Salisbury J, Green M, Hunt C, Campbell J (2008) Coastal acidification by rivers: a threat to shellfish? EOS Trans Am Geophys Union 89:513 Crossref

Sasaki GC, Capuzzo JM, Biesiot P (1986) Nutritional and bioenergetic considerations in the development of the American lobster Homarus americanus. Can J Fish Aquat Sci 43:2311-2319 Crossref

Schiffer M, Harms L, Pörtner HO, Mark FC, Storch D (2014) Pre-hatching seawater pCO2 affects development and survival of zoea stages of Arctic spider crab Hyas araneus. Mar Ecol Prog Ser 501:127-139 Crossref

Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675

Sibert V, Ouellet P, Brêthes JC (2004) Changes in yolk total proteins and lipid components and embryonic growth rates during lobster (Homarus americanus) egg development under a simulated seasonal temperature cycle. Mar Biol 144:1075-1086 Crossref

Siedlecki SA, Salisbury J, Gledhill DK, Bastidas C and others (2021) Projecting ocean acidification impacts for the Gulf of Maine to 2050: new tools and expectations. Elementa Sci Anthropocene 9:00062 Crossref

Sisti AR, Jellison B, Shields JD, Rivest EB (2024) Brood-grooming behavior of American lobsters Homarus americanus in conditions of ocean warming and acidification. Mar Ecol Prog Ser 744:83-99 Crossref

Sisti AR, Jellison BM, Shields JD, Rivest EB (2025) Physiological effects of acute exposure to acidification conditions in embryos of the American lobster (Homarus americanus). J Exp Mar Biol Ecol 585:152095 Crossref

Smith PK, Krohn RI, Hermanson GT, Mallia A and others (1985) Measurement of protein using bicinchoninic acid. Anal Biochem 150:76-85

Styf HK, Nilsson Sköld H, Eriksson SP (2013) Embryonic response to long-term exposure of the marine crustacean Nephrops norvegicus to ocean acidification and elevated temperature. Ecol Evol 3:5055-5065 PubMedCrossref

Thatje S, Lovrich GA, Anger K (2004) Egg production, hatching rates, and abbreviated larval development of Campylonotus vagans Bate, 1888 (Crustacea: Decapoda: Caridea), in subantarctic waters. J Exp Mar Biol Ecol 301:15-27 Crossref

Truchot JP (1978) Mechanisms of extracellular acid-base regulation as temperature changes in decapod crustaceans. Respir Physiol 33:161-176 PubMedCrossref

Waddy SL, Aiken DE (1995) Temperature regulation of reproduction in female American lobsters (Homarus americanus). ICES J Mar Sci 199:54-60

Waldbusser GG, Salisbury JE (2014) Ocean acidification in the coastal zone from an organism’s perspective: multiple system parameters, frequency domains, and habitats. Annu Rev Mar Sci 6:221-247 PubMedCrossref

Waller JD, Wahle RA, McVeigh H, Fields DM (2017) Linking rising pCO2 and temperature to the larval development and physiology of the American lobster (Homarus americanus). ICES J Mar Sci 74:1210-1219 Crossref

Waller JD, Reardon KM, Caron SE, Masters HM, Summers EL, Wilson CJ (2019) Decrease in size at maturity of female American lobsters Homarus americanus (H. Milne Edwards, 1837) (Decapoda: Astacidea: Nephropidae) over a 50-year period in Maine, USA. J Crustac Biol 39:509-515 Crossref

Wear RG (1974) Incubation in British decapod Crustacea, and the effects of temperature on the rate and success of embryonic development. J Mar Biol Assoc UK 54:745-762 Crossref

Wheatly MG, Henry RP (1987) Branchial and antennal gland Na+/K+-dependent ATPase and carbonic anhydrase activity during salinity acclimation of the euryhaline crayfish Pacifastacus leniusculus. J Exp Biol 133:73-86 Crossref

Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257-272 Crossref

Whiteley NM, Suckling CC, Ciotti BJ, Brown J, McCarthy ID, Gimenez L, Hauton C (2018) Sensitivity to near-future CO2 conditions in marine crabs depends on their compensatory capacities for salinity change. Sci Rep 8:15639 PubMedCrossref

B. Jellison (Corresponding Author)

  • Department of Biological Sciences, University of New Hampshire, Durham, NH 03824, USA
  • Virginia Institute of Marine Science, William & Mary, Gloucester Point, VA 23062, USA
brittany.jellison@unh.edu

A. Sisti (Co-author)

  • Virginia Institute of Marine Science, William & Mary, Gloucester Point, VA 23062, USA

J. Shields (Co-author)

  • Virginia Institute of Marine Science, William & Mary, Gloucester Point, VA 23062, USA

B. Thomas (Co-author)

  • Virginia Institute of Marine Science, William & Mary, Gloucester Point, VA 23062, USA

B. Sweezey (Co-author)

  • Texas A&M University, Galveston, TX 77554, USA

E. Rivest (Co-author)

  • Virginia Institute of Marine Science, William & Mary, Gloucester Point, VA 23062, USA

Handling Editor:
James McClintock, Birmingham, Alabama, USA

Reviewers:
L. Leiva and 2 anonymous referees

Acknowledgements:

This research was funded by an award from NOAA National Sea Grant’s American Lobster Initiative to E.B.R. and J.D.S. (NA19OAR4170393). A.R.S. was supported by a National Science Foundation Graduate Research Fellowship and the Virginia Institute of Marine Science Graduate Student Association Spring 2022 Research Grant. We thank Kathleen Reardon with the Maine Department of Marine Resources and Dr. Tracy Pugh, Massachusetts Division of Marine Fisheries, for assistance in obtaining lobsters for this study. Arien Widrick, Amelia Slater, and Gabe Thompson helped with optimization and running of assays, system maintenance, and lobster care over the course of the experiment.

© The authors 2025. Open Access under Creative Commons by Attribution Licence. Use, distribution and reproduction are un­restricted. Authors and original publication must be credited.