Abstract
The Dungeness crab, Cancer magister, is an important resource species, and in Puget Sound, USA, where the adults occur in inshore waters that have summer pH as low as 7.6, future levels are predicted as low as 7.1. Using eggs and larvae from females captured in Puget Sound in late 2012, this laboratory study examined hatching success, larval survival, and larval development rate at target pH of 8.0, 7.5, and 7.1, which represent present open ocean, present coastal upwelling, and projected upwelling conditions. Toward the end of their development, the eggs of one C. magister were exposed to the three treatments and they began to hatch after 22 days. Hatching probability was unaffected by lower pH, but hatching was delayed at pH 7.1. In a second experiment, significantly more C. magister larvae survived after 45 days at pH 8.0 than at the two lower pH: 58, 14, and 21 %. The sizes of the zoeae were unaffected by treatment, but larvae in the low-pH treatments progressed through larval stages more slowly. This study shows that low-pH seawater slows embryonic and early larval development and causes appreciable larval mortality. It suggests that ocean acidification could have a measurable impact on the population dynamics of C. magister.
Similar content being viewed by others
Notes
Schweitzer and Feldmann (2010) proposed elevating the Cancer subgenus, metacarcinus, outlined by Nations (1975) to the generic level re-classifying the Dungeness crab as Metacarcinus magister based solely on the shape of carapace teeth. Due to a lack of molecular evidence (Harrison and Crespi 1999) to support Nations’ subdivisions, the lead author elected to maintain the use of Cancer magister.
References
Arnberg M, Calosi P, Spicer JI, Tandberg AHS, Nilsen M, Westerlund S, Bechmann RK (2013) Elevated temperature elicits greater effects than decreased pH on the development, feeding and metabolism of northern shrimp (Pandalus borealis) larvae. Mar Biol 160:2037–2048
Bates D, Maechler M, Bolker B (2013) lme4: linear-mixed effects models using S4 classes. http://CRAN.R-project.org/package=lme4
Bollens SM, van den Hoof R, Cordell JR, Frost BW (2010) Feeding ecology of juvenile Pacific salmon (Oncorhynchus spp.) in a northeast Pacific fjord: diet, availability of zooplankton, selectivity for prey, and potential competition for prey resources. Fish Bull 108:393–407
Busch DS, Maher M, Thibodeau P, McElhany P (2014) Shell condition and survival of Puget Sound pteropods are impaired by ocean acidification conditions. PLoS ONE 9:e105884
Byrne M (2011) Impact of ocean warming and ocean acidification on marine invertebrate life history: vulnerabilities and potential for persistence in a changing ocean. Oceanogr Mar Biol 49:1–42
Carter HA, Ceballos-Osuna L, Miller NA, Stillman JH (2013) Impact of ocean acidification on the metabolism and energetics of early life stages in the intertidal porcelain crab Petrolisthes cinctipes. J Exp Biol 216:1412–1422
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
Crawley M (2007) The R book, 2nd edn. Wiley, West Sussex
Dickson AG, Sabine CL, Christian JR (2007) Guide to best practices for ocean CO2 552 measurements: PICES special publication 3
Dupont S, Thorndyke MC (2009) Impact of CO2-driven ocean acidification on invertebrates early life-history—What we know, what we need to know and what we can do. Biogeosci Discuss 6:3109–3131
Dupont S, Ortega-Martinez O, Thorndyke M (2010) Impact of near-future ocean acidification on echinoderms. Ecotoxicology 19:449–462
Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884
Fabry VJ, Seibel BA, Feely RA, Orr JC (2008) Impacts of ocean acidification on marine fauna and ecosystem processes. ICES J Mar Sci 65:414–432
FAO (2016) Species fact sheet Cancer magister. http://www.fao.org/fishery/species/3461/en. Accessed 8 Feb 2016
Feely RA, Alin SR, Newton J, Sabine CL, Warner M, Devol A, Krembs C, Maloy C (2010) The combined effects of ocean acidification, mixing, and respiration on pH and carbonate saturation in an urbanized estuary. Estuar Coast Shelf Sci 88:442–449
Gaumer TF (1973) Controlled rearing of Dungeness crab larvae and the influence of environmental conditions to their survival. Oreg Fish Comm, Portland, NOAA 73082801, NMFS 1 5 R
Gruber N, Hauri C, Lachkar Z, Loher D, Frölicher TL, Plattner G-K (2012) Rapid progression of ocean acidification in the California Current System. Science 337:220–223
Harrison MK, Crespi BJ (1999) Phylogenetics of Cancer crabs (Crustacea: Decapoda: Brachyura). Mol Phylogenet Evol 12:186–199
Hays GC, Richardson AJ, Robinson C (2005) Climate change and marine plankton. Trends Ecol Evol 20:337–344
Henry RP, Wheatly MG (1992) Interaction of respiration, ion regulation, and acid-base balance in everyday life of aquatic crustaceans. Am Zool 32:407–416
Hirota R, Fukuda Y (1985) Dry weight and chemical composition of the larval forms of crabs (Decapoda: Brachyura). Bull Plankton Soc Jpn 32:149–153
Hobbs RC, Botsford LW (1992) Diel vertical migration and timing of metamorphosis of larvae of the Dungeness crab Cancer magister. Mar Biol 112:417–428
Hobbs RC, Botsford LW, Thomas A (1992) Influence of hydrographic conditions and wind forcing on the distribution and abundance of Dungeness crab, Cancer magister, larvae. Can J Fish Aquat Sci 49:1379–1388
Hoffman GE, Smith J, Johnson KS, Send U, Levin LA, Micheli F, Paytan A, Price NN, Petersen B, Takeshita Y, Matson PG, Crook ED, Kroeker KJ, Gambi MC, Rivest EB, Frieder CA, Yu PC, Martz TR (2011) High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6:1–11
Jamieson GS, Phillips A (1993) Megalopal spatial distribution and stock separation in Dungeness crab (Cancer magister). Can J Fish Aquat Sci 50:416–429
Jensen, GC (2014) Crabs and shrimps of the Pacific Coast: a guide to shallow-water decapods from Southeastern Alaska to the Mexican border. ISBN 978-0-9898391-0-5 MolaMarine, Bremerton
Jensen CJ, Bentzen P (2012) A molecular dissection of the mating system of the Dungeness crab Metacarcinus magister (Brachyura: Cancridae). J Crustac Biol 32:443–456
Kemp IM, Beauchamp DA, Sweeting R, Cooper C (2013) Potential for competition among herring and juvenile salmon species in Puget Sound, Washington. North Pacific Anadromous Fish Commission technical report no. 9, pp 139–143
Kleinbaum DG, Klein M (2005) Survival analysis. A self-learning text, 2nd edn. Springer, New York
Kroeker KJ, Kordas RL, Crim RN, Hendricks IE, Ramajo L, Singh GG, Duartes CM, Gattuso J (2013) Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob Change Biol 19:1884–1896
Kurihara H, Matsui M, Furukawa H, Hayashi M, Ishimatsu A (2008) Long-term effects of predicted future seawater CO2 conditions on the survival and growth of the marine shrimp Palemon pacificus. J Exp Mar Biol Ecol 367:41–46
Lavigne H, Gattuso J (2013) Seacarb: seawater carbonate chemistry with R. R package version 2.4.8
Lee K, Kim T-W, Byrne RH, Millero FJ, Feely RA, Liu Y-M (2010) The universal ratio of boron to chlorinity for the North Pacific and North Atlantic oceans. Geochim Cosmochim Acta 74:1801–1811
Long WC, Swiney KM, Foy RJ (2013a) Effects of ocean acidification on the embryos and larvae of red king crab, Paralithodes camtschaticus. Mar Pollut Bull 69:38–47
Long WC, Swiney KM, Harris C, Page HN, Foy RJ (2013b) Effects of ocean acidification on juvenile Red King crab (Paralithodes camtschaticus) and Tanner crab (Chionecetes bairdi) growth, condition, calcification and survival. PLoS ONE 8:1–10
Lough RG (1974) Dynamics of crab larvae (Anomura, Brachyura) off the central Oregon coast, 1969–1971. Dissertation, Oregon State University
Lueker TJ, Dickson AG, Keeling CD (2000) Ocean pCO2 calculated from dissolved 557 inorganic carbon, alkalinity, and equations for K1 and K2: validation based on laboratory 558 measurements of CO2 in gas and seawater at equilibrium. Mar Chem 70:105–119
McElhany P, Busch D (2013) Appropriate pCO2 treatments in ocean acidification experiments. Mar Biol 160:1807–1812
Miller JJ (2015) The effect of low pH on early life stages of the decapod crustacean, Dungeness crab (Cancer magister). Master thesis, University of Washington, Seattle
Miller GM, Watson S-A, McCormick MI, Munday PL (2013) Increased CO2 stimulates reproduction. Glob Change Biol 19:3037–3045
Moloney CL, Botsford LW, Largier JL (1994) Development, survival and timing of metamorphosis of planktonic larvae in a variable environment, the Dungeness crab as an example. Mar Ecol Prog Ser 113:61–79
Murray JW, Gill G (1978) The geochemistry of iron in Puget Sound. Geochim Cosmochim Acta 42:9–19
Nations JD (1975) The genus Cancer (Crustacea: Brachyura): systematics, biogeography, and fossil record. Nat Hist Mus Los Angel Cty Sci Bull 23:1–104
Pane EF, Barry JP (2007) Extracellular acid-base regulation during short-term hypercapnia is effective in a shallow-water crab, but ineffective in a deep-sea crab. Mar Ecol Prog Ser 334:1–9
Park W, Shirley TC (2005) Diel vertical migration and seasonal timing of the larvae of three sympatric Cancrid crabs, Cancer spp., in southeastern Alaska. Estuaries 28:266–273
Pauley GB, Armstrong DA, Heun TW (1986) Species profiles: life histories and environmental requirements of coastal fishes and invertebrates (Pacific Northwest)–Dungeness crab. US Fish Wildl Serv Biol Rep 82(11.63). US Army Corps of Engineers, TREL-82-4
Poole RL (1966) A description of laboratory-reared zoeae of Cancer magister Dana, and megalopae taken under natural conditions (Decapoda Brachyura). Crustaceana 11:83–97
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0. http://www.R-project.org/
Rasmuson LK (2013) The biology, ecology and fishery of the Dungeness crab, Cancer magister in Lesser M ed. Adv Mar Biol 65:95–148
Reilly PN (1983) Predation on Dungeness crabs, Cancer magister, in central California. In: Wild PW, Tasto RN (eds) Life history, environment, and mariculture studies of the Dungeness crab, Cancer magister, with emphasis on the central California fishery resource. Calif Fish and Game Fish Bul, vol 172, pp 155–164
Reum JCP, Alin SR, Feely RA, Newton J, Warner M, McElhany P (2014) Seasonal carbonate chemistry covariation with temperature, oxygen, and salinity in a fjord estuary: implications for the design of ocean acidification experiments. PLoS ONE 9:e89619
Schindler DE, Rogers DE, Scheuerell MD, Abrey CA (2005) Effects of changing climate on zooplankton and juvenile Sockeye salmon growth in southwestern Alaska. Ecology 86:198–209
Schweitzer CF, Feldmann RM (2010) Re-evaluation of the Cancridae Latreille, 1802 (Decapoda: Brachyura) including three new genera and three new species. Contrib Zool 69:223–250
Shanks AL (2013) Atmospheric forcing drives recruitment variation in the Dungeness crab (Cancer magister), revisited. Fisheries Oceanography, pp 1–10
Shirley S, Shirley T, Rice S (1987) Latitudinal variation in the Dungeness crab, Cancer magister, zoeal morphology explained by incubation temperature. Mar Biol 95:371–376
Stone RP, O’Clair CE (2001) Seasonal movements and distribution of Dungeness crabs Cancer magister in a glacial southeastern Alaska estuary. Mar Ecol Prog Ser 214:167–176
Stumpp M, Wren J, Melzner F, Thorndyke MC, Dupont ST (2011) CO2 induced seawater acidification impacts sea urchin larval development I: elevated metabolic rates decrease scope for growth and induce developmental delay. Comp Biochem Phys A 160:331–340
Sulkin SD, McKeen GI (1989) Laboratory study of survival and duration of individual zoeal stages as a function of temperature in the brachyuran crab Cancer magister. Mar Biol 103:31–37
Therneau T (2013) Survival: survival analysis. R package version 2.37-4. http://CRAN.R-project.org/package=survival
Walther K, Anger K, Pörtner HO (2010) Effects of ocean acidification and warming on the larval development of the spider crab Hyas araneus from different latitudes (54° vs. 79°). Mar Ecol Prog Ser 417:159–170
Whiteley NM (2011) Physiological and ecological responses of crustaceans to ocean acidification. Mar Ecol Prog Ser 430:257–271
Wittmann AC, Pörtner HO (2013) Sensitivities of extant animal taxa to ocean acidification. Nat Clim Change 3:995–1001
Yamazaki H, Sperline RP, Freiser H (1992) Spectrophotometric determination of pH and its application to determination of thermodynamic equilibrium constants. Anal Chem 64:2720–2725
Acknowledgments
We would like to thank Casimir Rice, Kathleen Neely, Mark Tagal, Dan Bascom, Jerry Leonard, Shallin Busch, Paul Williams, Nick Tolimieri, and Phil Levin for their help on this project.
Funding
Research was funded by NOAA Ocean Acidification program, the Suquamish Tribe, NOAA Northwest Fisheries Science Center, Washington Sea Grant, and the United States Environmental Protection Agency. All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Responsible Editor: J. Grassle.
Reviewed by Undisclosed experts.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Miller, J.J., Maher, M., Bohaboy, E. et al. Exposure to low pH reduces survival and delays development in early life stages of Dungeness crab (Cancer magister). Mar Biol 163, 118 (2016). https://doi.org/10.1007/s00227-016-2883-1
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00227-016-2883-1