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Can the timing and duration of planktonic larval development contribute to invasion success? A case study comparing range expansion in the European green crab, Carcinus maenas, and the native lined shore crab, Pachygrapsus crassipes, in the northeast Pacific

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Abstract

Major El Niño events and oceanic heat waves are linked to the range expansion of many marine species. For the shores of the northeast Pacific, we compared range expansion in the European green crab, Carcinus maenas, which was introduced to San Francisco Bay prior to 1990, to that of the native lined-shore crab, Pachygrapsus crassipes. The initial northern range limit of these species was central California and southern Oregon, respectively. Both species increased their northern range along the open coast to northern Oregon, Washington and Vancouver Island after strong El Niño events. C. maenas, however, in just a matter of decades, successfully established populations in estuaries from Oregon to inlets on the west coast of Vancouver Island, and possibly also in the Salish Sea, while P. crassipes, never has in recorded history. We hypothesize that this difference in invasion success is due to the shorter larval duration of C. maenas, < 2 months, compared to that of P. crassipes, 3–4 months and timing of larval release, winter for both species. Because the residency times of water in the inlets of the west coast of Vancouver Island are typically 1–2 months, they can act as incubators for the larvae of C. maenas, while those of P. crassipes are likely flushed out to the open sea before they can complete their development. We propose that the life history of a species coupled with the hydrodynamic setting in which its pelagic larvae develop contribute to the success of range expansion.

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References

  • Austin JA, Barth JA (2002) Drifter behavior on the Oregon-Washington shelf during downwelling-favorable winds. J Phys Oceanogr 32:3132–3144. https://doi.org/10.1175/1520-0485(2002)032%3c3132:DBOTOW%3e2.0.CO;2

    Article  Google Scholar 

  • Behrens Yamada S, Gillespie GE (2008) Will the European green crab (Carcinus maenas) persist in the Pacific Northwest? ICES. J Mar Sci 65:725–729. https://doi.org/10.1093/icesjms/fsm191

    Article  Google Scholar 

  • Behrens Yamada S, Kosro PM (2010) Linking ocean conditions to year class strength of the invasive European green crab Carcinus Maenas. Biol Invasions 12:1791–1804

    Article  Google Scholar 

  • Behrens Yamada S, Dumbauld BR, Kalin A, Hunt CE, Figlar Barnes R, Randall A (2005) Growth and persistence of a recent invader in estuaries of the Northeastern Pacific. Biol Invasions 7:309–321

    Article  Google Scholar 

  • Behrens Yamada S, Peterson WT, Kosro PM (2015) Biological and physical ocean indicators predict the success of an invasive crab, Carcinus maenas, in the northern California Current. Mar Ecol Prog Ser 537:175–189

    Article  Google Scholar 

  • Behrens Yamada S, Thomson RE, Gillespie GE, Norgard TC (2017) Lifting barriers to range expansion: the European green crab Carcinus maenas (Linneaus, 1758) enters the Salish Sea. J Shellfish Res 36(1):1–8

    Article  Google Scholar 

  • Behrens Yamada S, Gillespie GE, Thomson RE, Norgard TC (2021a) Ocean indicators predict the range expansions of the European green crab Carcinus maeans on the North American Pacific coast. J Shellfish Res 40(2):399–413. https://doi.org/10.2983/035.040.0212

    Article  Google Scholar 

  • Behrens Yamada S, Fisher JL, Kosro PM (2021b) Relationship between ocean ecosystem indicators and year class strength of the invasive European green crab (Carcinus maenas). Prog Oceanogr 196:102618. https://doi.org/10.1016/j.pocean.2021.102618

    Article  Google Scholar 

  • Boulding EG, Behrens Yamada S, Schooler SS, Shanks AL (2020) Periodic invasions during El Niño events by the predatory lined shore crab (Pachygrapsus crassipes): forecasted effects of its establishment on direct-developing indigenous prey species (Littorina spp.). Can J Zool 98:787–797. https://doi.org/10.1139/cjz-2019-0250

    Article  CAS  Google Scholar 

  • Brasseale E, Grason EW, McDonald PS, Adams J, MacCready P (2019) Larval transport modeling support for identifying population sources of the European Green Crab in the Salish Sea. Estuaries Coasts 42:1586–1599. https://doi.org/10.1007/s12237-019-00586-2

    Article  CAS  Google Scholar 

  • Buffington C (2019) European green crab, Carcinus maenas (2019) Washington Department of Fish and Wildlife European Green crab monitoring program for inland waters of the Salish Sea: Puget Sound, San Juan Island, and the Strait of Juan de Fuca. A report prepared for the Pacific States Marine Fisheries Commission. 19 pages

  • Canepa JA, Terhorst CP (2019) Phenotypic variation across the range of the lined shore crab Pachygrapsus crassipes Randall 1840 (Decapoda Grapsidae). Crustaceana 92(4):385–396. https://doi.org/10.1163/15685403-00003879

    Article  Google Scholar 

  • Cassone BJ, Boulding EG (2006) Genetic structure and phylogeography of the lined shore crab, Pachygrapsus crassipes, along the northeastern and western Pacific coasts. Mar Biol 149:213–226

    Article  Google Scholar 

  • Cohen A, Carlton JT, Fountain MC (1995) Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San Francisco Bay. California Mar Biol 122(2):125–237

    Google Scholar 

  • Cohen AN Carlton JT (1995) Nonindigenous aquatic species in a U.S. estuary: a case study of the biological invasions of the San Francisco Bay and delta. A Report for the US fish and wildlife service, Washington D.C.

  • Cohen AN, Weinstein A., Emmett MA, Lau W, Carlton JT (2001) Investigations into the Introduction of Non-indigenous Marine Organisms via the Cross-Continental Trade in Marine Baitworms. A report for the U.S. Fish and Wildlife Service, San Francisco Bay Program, Sacramento CA. San Francisco Estuary Institute, Oakland CA. https://www.sfei.org/sites/default/files/biblio_files/2001-Baitworms357.pdf

  • Cronin TW (1982) Estuarine retention of larvae of the crab Rhithorpanopeus harrisii. retention. Estuar Coast Shelf Sci 15:207–220

    Article  Google Scholar 

  • Curtis LJF, Curtis DL, Matkin H, Thompson M, Choi F, Callow P, Gillespie GE, Therriault T., Pearce CM (2015) Evaluating transfers of harvested shellfish products, from the west to the east coast of Vancouver Island, as a potential vector for European Green Crab (Carcinus maenas) and other non-indigenous invertebrate species. DFO Can Sci Advis Secretar Res Doc (2015/014). vi + 74 pp. https://waves-vagues.dfo-mpo.gc.ca/Library/359729.pdf

  • Dawirs R (1985) Temperature and larval development of Carcinus maenas (Decapoda) in the laboratory, predictions of larval dynamics in the sea. Mar Ecol Prog Ser 24:297–302

    Article  Google Scholar 

  • deRivera CE, Hitchcock N, Teck SJ, Steves BP, Hines AH, Rui GM (2007) Larval development rate predicts range expansion of an introduced crab. Mar Biol 150:1275–1288. https://doi.org/10.1007/s00227-006-0451-9

    Article  Google Scholar 

  • DiBacco C, Therriault TW (2015) Reproductive periodicity and larval vertical migration behavior of European green crab Carcinus maenas in a non-native habitat. Mar Ecol Prog Ser 536:123–134

    Article  Google Scholar 

  • DiBacco C, Sutton D, McConnico L (2001) Vertical migration behavior and horizontal distribution of brachyuran larvae in a low-inflow estuary: implication for bay-ocean exchange. Mar Ecol Prog Ser 217:191–206

    Article  Google Scholar 

  • DiBacco C (2001) The influence of bay versus coastal habitats on development and survival of striped shore crab larvae (Pachygrapsus crassipes Randall 1840). Bull S Calif Acad Sci 99: 161–170 https://www.thefreelibrary.com/The+Influence+of+Bay+versus+Coastal+Habitats+on+Development+and...-a068646748

  • Foreman MGG, Thomson RE, Smith CI (2000) Seasonal current simulations for the western continental margin of Vancouver Island. J Geophys Res 105(C8):19665–19698. https://doi.org/10.1029/2000JC900070

    Article  Google Scholar 

  • Fulton SW, Grant FE (1900) Note on the occurrence of the European green crab, Carcinus maenas, Leach, in Port Phillip. Victorian Naturalist 17:147–148

    Google Scholar 

  • Gillespie G, Rusch B, Gormican SJ, Marshall R, Munro, D (2001) Further investigations of the fishery potential of the exotic varnish clam (Nuttallia obscurata) in British Columbia. DFO Canadian Science Advisory Secretariat Research Document 2001/143

  • Gillespie GE, Phillips AC, Paltzat DL, Therriault TW (2007) Status of the European green crab, Carcinus maenas, in British Columbia—2006. Can Tech Rep Fish Aquat Sci 2700: vii + 39 p

  • Gillespie GE, Norgard TC, Anderson ED, Haggarty DR, Phillips AC. (2015) Distribution and biological characteristics of European green crab, Carcinus maenas, in British Columbia, 2006–2013. Can Tech Rep Fish Aquat Sci 3120. viii + 88 pp. https://www.researchgate.net/publication/321627506_Distribution_and_biological_characteristics_of_European_green_crab_Carcinus_maenas_in_British_Columbia_2006-2013

  • Gonçalves F, Ribeiro R, Soares AMVM (1995) Laboratory study of effects of temperature and salinity on survival and larval development of a population of Rhithropanopeus harrisii from the Mondego River Estuary. Portugal Marine Biol 121(4):639–645

    Article  Google Scholar 

  • Grason EW, McDonald PS, Adams J, Litle K, Apple JK, Pleus A (2018) Citizen science program detects range expansion of the globally invasive European green crab in Washington State (USA). Manage Biol Invasions 9(1):39–47

    Article  Google Scholar 

  • Grosholz ED, Ruiz GM (1995) Spread and potential impact of the recently introduced European green crab, Carinus maeans, in in central California. Mar Biol 122:239–247

    Article  Google Scholar 

  • Grosholz E, Lovell S, Besedin E, Katz M (2011) Modeling the impact of the European green crab on commercial shellfisheries. Ecol Appl 2(3):915–924

    Article  Google Scholar 

  • Hart JFL (1982) Crabs and their relatives of British Columbia. B.C. Prov. Mus.Handb. 40, 267 pp. Victoria, B.C., Ministry of Provinvial Secretary and Government Services

  • Hiatt RW (1948) The biology of the lined shore crab Pachygrapsus Crassipes Randall. Pacific Sci 2:135–213

    Google Scholar 

  • Hickey BM (1979) The California current system—hypothesis and facts. Prog Oceanogr 8(4):191–279. https://doi.org/10.1016/0079-6611(79)90002-8

    Article  Google Scholar 

  • Hickey BM (1989) Poleward flow near the northern and southern boundaries of the U.S. west coast. In: Neshyba SJ, Mooers CMK, Smith RL, Barber RT (eds) Poleward flows along eastern ocean boundaries. Springer-Verlag, New York, pp 160–175

    Google Scholar 

  • Hickey BM, Thomson RE, Yih H, LeBlond PH (1991) Velocity and temperature fluctuations in a buoyancy-driven current off Vancouver Island. J Geophys Res 96:10507–10538

    Article  Google Scholar 

  • Hidalgo FJ, Barón PJ, Orensanz JM (2005) A prediction come true: the green crab invades the Patagonia coast. Biol Invasions 7:547–555

    Article  Google Scholar 

  • Hill AE, Hickey BM, Shillington FA, Strub PT, Brink K., Barton E., Thomas AC (1998) Eastern ocean boundaries coastal segment. In: Robinson AR, Brink KH (eds) The Sea, vol. 11, The Global Coastal Ocean-Regional Studies and Syntheses. Wiley. pp 29–67

  • Holbrook J, Cannon GA, Kachel D (1983) Two-year observations of coastal-estuarine interaction in the Strait of Juan de Fuca. In: Gade H et al (eds) Coastal Oceanography. Plenum Press, New York, pp 411–426

    Chapter  Google Scholar 

  • Huyer A, Barth JA, Fleischbein J, Kosro PM, Smith RL (1998) The Coastal Ocean off Oregon and Northern California during the 1997/1998 El Niño, Part 1: Temperature, Salinity and Geostropic Velocity Fields. Trans Am Geophys Union 79(45):F485

    Google Scholar 

  • Jensen GC (1995) Pacific Coast crabs and shrimps. Sea Challengers, Monterey, California

  • Jensen G. (2014) Crabs and shrimps of the Pacific coast. MolaMarine, Bremerton WA

  • Kelley AL, de Rivera CE, Grosholz ED, Ruiz GM, Behrens Yamada S, Gillespie G (2015) Thermogeographic variation in body size of Carcinus maenas, the European green crab. Mar Biol 162:1625–1635. https://doi.org/10.1007/s00227-015-2698-5

    Article  Google Scholar 

  • Khangaonkar T, Yang Z, Kim T, Roberts M (2011) Tidally averaged circulation in Puget Sound sub-basins: Comparison of historical data, analytical model, and numerical model. Estuar Coast Shelf Sci 93(4):305–319. https://doi.org/10.1016/j.ecss.2011.04.016

    Article  Google Scholar 

  • Khangaonkar T, Long W, Xu W (2017) Assessment of circulation and inter-basin transport in the Salish Sea including Johnstone Strait and Discovery Islands pathways. Ocean Model 109:11–32

    Article  Google Scholar 

  • Le Roux PJ, Branch BM, Joska PAP (1990) On the distribution, diet and possible impact of the invasive European shore crab Carcinus maenas (L.) along the South African coast. S Afr J Mar Sci 9:85–93

    Article  Google Scholar 

  • Lough R (1975) Dynamics of crab larvae (Anomura, Brachyura) off the Central Oregon Coast, 1969–1971. PhD thesis, Oceanography, Oregon State University https://ir.library.oregonstate.edu/collections/j3860c90v?locale=en

  • MacCready P, Geyer WR, Burchard H (2018) Estuarine exchange flow is related to mixing through the salinity variance budget. J Phys Oceanogr 48:1375–1384. https://doi.org/10.1175/JPO-D-17-0266.1

    Article  Google Scholar 

  • Miller TW (1996) First record of the green crab, Carcinus maenas in Humboldt Bay. California Calif Fish Game 82(2):93–96

    Google Scholar 

  • Morris RH, Abbott D, Haderlie EC (1980) Intertidal invertebrates of California. Stanford University Press, Stanford

    Google Scholar 

  • Mueller KW, Jefferson NT (2019) First detection of the invasive European green crab Carcinus maenas (Linnaeus, 1758) on Lummi Nation reservation tidelands. Harvest Management Division Technical Report, December 2019, Lummi Natural Resources Department, Bellingham, Washington, pp 74 + iv, including appendices.

  • Pawlowicz R (2017) Seasonal cycles, hypoxia, and renewal in a coastal fjord (Barkley Sound, British Columbia). Atmos Ocean 55(4–5):264–283. https://doi.org/10.1080/07055900.2017.137424

    Article  CAS  Google Scholar 

  • Pearcy WG, Schoener A (1987) Changes in the marine biota coincident with the 1982–1983 el Niño in the northeastern Subarctic Pacific Ocean. J. Geophys. Res. Oceans 92(C13):41417–14428. https://doi.org/10.1029/JC092iC13p14417

    Article  Google Scholar 

  • Petersen C (2006) Range expansion in the northeast Pacific by an estuary mud crab – a molecular study. Biol Invasions 8:565–576

    Article  Google Scholar 

  • Quayle DB (1988) Pacific oyster culture in British Columbia. Can Bull Fish Aquat Sci 218. Department of Fisheries and Oceans, Ottawa, Canada. https://waves-vagues.dfo-mpo.gc.ca/Library/109165.pdf

  • Queen JC (1930) Marine decapod Crustacea of the Coos Bay, Oregon district. Master of Arts thesis, Biology, University of Oregon

  • Queiroga H, Costlow JD, Moreira MA (1997) Vertical migration of the crab Carcinus maenas first zoea in an estuary: implication for tidal steam transport. Mar Ecol Prog Ser 149:121–132

    Article  Google Scholar 

  • Ricketts EF, Calvin J, Hedgpeth JW (1968) Between Pacific tides, 4th edn. Stanford University Press, Stanford

    Google Scholar 

  • Roche DG, Torchin ME (2007) Established populations of the North American Harris mud crab, Rhithropanopeus harrisii (Gould 1841) (Crustacea: Brachyura: Xanthidae) in the Panama Canal. Aquat Invasions 2(3):155–161

    Article  Google Scholar 

  • Sanford E, Sones JL, García-Reyes M, Goddard JHR (2019) Largier JL (2019) Widespread shifts in the coastal biota of northern California during the 2014–2016 marine heatwaves. Sci Rep 9(4216):1–14. https://doi.org/10.1038/s41598-019-40784-3

    Article  CAS  Google Scholar 

  • Say T (1817) An account of the crustacea of the United States. J Acad Natur Sci Philadelphia 1:57–63

    Google Scholar 

  • Schlotterbeck REE (1976) The larval development of the lined shore crab, Pachygrapsus crassipes Randall, 1840 (Decapoda Brachyura, Grapsidae) reared in the labratory. Crustaceana 30(2):184–200. https://doi.org/10.1163/156854076x00567

    Article  Google Scholar 

  • Shanks AL (2006) Mechanisms of cross-shelf transport of crab megalopae inferred from a time series of daily abundance. Mar Biol 148:1383–1398

    Article  Google Scholar 

  • Shanks AL, Eckert GL (2005) Population persistence of California Current fishes and benthic crustaceans: a marine drift paradox. Ecol Monogr 75(4):505–524

    Article  Google Scholar 

  • Shanks A, Schroeder SL, Dlouhy B (2011) Report of the zooplankton sampling adjacent to the proposed Jordan Cove LNG Terminal. Oregon Institute of Marine Biology. Charleston, Oregon

  • Shanks A (1985) The effects of larval behavior and distribution on the cross shelf dispersal of coastal crabs. Ph.D. Thesis, Scripps Institution of Oceanography, Biology Department, University of California, San Diego.

  • Sutherland DA, McCready P, Banas NS, Smedstad LF (2011) A model study of the Salish Sea estuarine circulation. J Phys, Oceanogr 41:1125–1143

    Article  Google Scholar 

  • Therriault TW, Herborg L-M, Locke A, McKindsey CW (2008) Risk assessment for European green crab (Carcinus maenas) in Canadian waters. DFO Can. Sci. Advis. Secretar. Res. Doc. 2008/042. iv + 40 pp. Available at: http:// www.dfo-mpo.gc.ca/csas-sccs/publications/resdocs-docrech/2008/2008_042-eng.htm.

  • Thomson RE, Mihaly SF, Kulikov EA (2007) Estuarine versus transient flow regimes in Juan de Fuca Strait. J Geophys Res Oceans 112:C09022. https://doi.org/10.1029/2006JC003925

    Article  Google Scholar 

  • Thomson RE, Heesemann M, Davis EE, Hourston RAS (2014) Continental microseismic intensity delineates oceanic upwelling timing along the west coast of North America. Geophys Res Lett. https://doi.org/10.1002/2014GL061241

    Article  Google Scholar 

  • Thomson RE, Spear DJ, Krassovski MV, Hourston RAS, Juhasz TA, Mihaly SF (2017) Buoyancy-driven coastal current blocks ventilation of an anoxic fjord on the Pacific coast of Canada. J Geophys Res Oceans. https://doi.org/10.1002/2016JC012512

    Article  Google Scholar 

  • Thomson RE, Kulikov EA, Spear DJ, Johannessen SC, Wills WP (2020) A role for gravity currents in cross-sill estuarine exchange and subsurface inflow to the southern Strait of Georgia. J Geophys Res Oceans. https://doi.org/10.1029/2019JC015374

    Article  Google Scholar 

  • Thomson, RE, Hickey BM, LeBlond PH (1989) The Vancouver Island Coastal Current: Fisheries barrier and conduit. In: Beamish, R., McFarlane, G. (eds.) Effects of ocean variability on recruitment and an evaluation of parameters used in stock assessment models. Spec Publ Fish Aquat Sci 108. Ottawa. Available https://waves-vagues.dfo-mpo.gc.ca/Library/114022.pdf

  • Thomson RE (1981) Oceanography of the British Columbia coast. Can. Spec. Pub. Fish. Aquat. Sci. Department of Fisheries and Oceans, Ottawa, Ont.

  • Wonham MJ, Hart MW (2018) El Niño Range Extensions of Pacific Sand Crab (Emerita analoga) in the Northeastern Pacific. Northwest Sci 92(1): 53–60. http://www.bamfieldmsc.com/wp-content/uploads/2018/06/WonhamHart.2018.emerita.range_.extension.pdf

  • Zeng C, Naylor E (1996) Occurrence in coastal water and endogenous tidal swimming rhythms of late megalopae of the shore crab Carcinus maenas: implication for onshore recruitment. Mar Ecol Prog Ser 136:69–79

    Article  Google Scholar 

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Acknowledgements

We thank everyone who contributed to creating this manuscript. Emily Grason of Washington Sea Grant, Chelsea Buffington of Washington Department of Fish Wildlife, Lorenz Sollmann of the United States Fish and Wildlife Service, Neil Harrington of the Jamestown S’Kallam Tribe, Karl Mueller and Nick Jefferson of the Lummi Nation, Graham Gillespie, Tammy Norgard, Elizabeth Boulding, Armand Kuris, Ladd Johnson, Greg Jensen, Brett Dumbauld, Connor McCracken, James Carlton, Rick Harbo, Andy Lamb, Bernard Handby, Andrew McCurdy and many others provided data on the most recent range expansion of the two crab species. Olga Yakovenko and Tammy Norgard diligently created Figs. 1 and 2 respectively. Thoughtful comments by Elizabeth Boulding, James Carlton, Claudio Di Bacco, Graham Gillespie, Greg Jensen and two anonymous reviewers greatly improved a previous version of this manuscript. The data on range expansion for the two species were compiled from various sources and listed in Supplemental Tables 1 and 2.

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  1. Sylvia Behrens Yamada

    Present address: , 3062 NW Snowberry Place, Corvallis, OR, 97330, USA

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  1. Department of Integrative Biology, Oregon State University, Corvallis, OR, 97331, USA

    Sylvia Behrens Yamada

  2. Oregon Institute of Marine Biology, P.O. Box 5389, Charleston, OR, 97420, USA

    Alan L. Shanks

  3. Institute of Ocean Sciences, Fisheries and Oceans Canada, Sidney, BC, V8L 4B2, Canada

    Richard E. Thomson

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Behrens Yamada, S., Shanks, A.L. & Thomson, R.E. Can the timing and duration of planktonic larval development contribute to invasion success? A case study comparing range expansion in the European green crab, Carcinus maenas, and the native lined shore crab, Pachygrapsus crassipes, in the northeast Pacific. Biol Invasions 24, 2917–2932 (2022). https://doi.org/10.1007/s10530-022-02820-8

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