Abstract
The non-indigenous European green crab (Carcinus maenas) has well-documented impacts on many native species. In the Atlantic Canada region, the green crab distribution is increasingly overlapping with the distribution of mud crabs (primarily Dyspanopeus sayi), a prominent native species. Despite the potential for antagonistic interactions, the relationship between the two species has not been examined, particularly in the context of the diversity of habitats available in the region. This study used observational beach seine data collected between 2009 and 2013 from the southern Gulf of St. Lawrence to explore the temporal and spatial relationships between mud crabs and green crabs, and detected a negative relationship between these species. Twenty-four-hour laboratory experiments examined their predator–prey interactions and assessed the influence of habitat complexity on the outcomes of these interactions. Mud crabs and similar-sized green crabs collected during July and August of 2010 and 2011 were used as prey for large green crab. These predators consumed almost twice as many mud crab compared with juvenile green crab in the two less structured habitats (no substrate or sandy substrate), but predation rates were statistically similar in oyster bed habitat. In that particular habitat, mud crab mortality dropped by ~65 %, whereas the generally lower mortality affecting juvenile green crabs was unaffected by habitat. These results suggest that complex habitats mediate predator–prey interactions and dampen the effect of green crab prey preference. As green crab continues to invade areas dominated by mud crabs, they may threaten the sustainability of this native species.
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References
Almeida JA, González-Gordillo JI, Flores AAV, Queiroga H (2011) Cannibalism, post-settlement growth rate and size refuge in a recruitment-limited population of the shore crab Carcinus maenas. J Exp Mar Biol Ecol 410:72–79. doi:10.1016/j.jembe.2011.10.011
Anderson MJ, Gorley RN, Clarke KR (2008) Permanova + for PRIMER: Guide to software and statistical methods. PRIMER-E. Plymouth Marine Laboratory, Plymouth
Audet D, Davis D, Miron G, Moriyasu M (2003) Geographical expansion of a nonindigenous crab, Carcinus maenas (L.), along the Nova Scotian shore into the southeastern Gulf of St. Lawrence, Canada. J Shellfish Res 22:255–262
Baeta A, Cabral HN, Marques JC, Pardal MA (2006) Feeding ecology of the green crab, Carcinus maenas (L., 1758) in a temperature estuary, Portugal. Crustaceana 79:1181–1193. doi:10.1163/156854006778859506
Bélair M, Miron G (2009) Predation behaviour of Cancer irroratus and Carcinus maenas during conspecific and heterospecific challenges. Aquat Biol 6:41–49. doi:10.3354/ab00166
Blakeslee AMH, McKenzie CH, Darling JA, Byers JE, Pringle JM, Roman J (2010) A hitchhiker’s guide to the Maritimes: anthropogenic transport facilitates long-distance dispersal of an invasive marine crab to Newfoundland. Divers Distrib 16:879–891. doi:10.1111/j.1472-4642.2010.00703.x
Botto F, Iribarne O (1999) Effects of the SW Atlantic burrowing crab Chasmagnathus granulata on a Spartina salt marsh. Mar Ecol Prog Ser 178:79–88. doi:10.3354/meps178079
Breen E, Metaxas A (2009) Overlap in the distributions between indigenous and non-indigenous decapods in a brackish micro-tidal system. Aquat Biol 8:1–13. doi:10.3354/ab00195
Carlton JT, Cohen AN (2003) Episodic global dispersal in shallow water marine organisms: the case history of the European shore crabs Carcinus maenas and C. aestuarii. J Biogeogr 30:1809–1820. doi:10.1111/j.1365-2699.2003.00962.x
Clarke KR, Gorley RN (2006) PRIMER v6: user manual/tutorial, PRIMER-E. Plymouth Marine Laboratory, Plymouth UK 192 pp
Cohen AN, Carlton JT, Fountain MC (1995) Introduction, dispersal and potential impacts of the green crab Carcinus maenas in San Fransciso Bay, California. Mar Biol 122:225–237. doi:10.1007/BF00348935
Connell J (1961) Effects of competition, predation by Thais lapillus, and other factors on natural populations of the barnacle Balanus balanoides. Ecol Monogr 31:61–104. doi:10.2307/1950746
Crowder LB, Cooper WE (1982) Habitat structural complexity and the interactions between bluegills and their prey. Ecology 63:1802–1813. doi:10.2307/1940122
Cunningham PN, Hughes RN (1984) Learning of predatory skills by shorecrabs Carcinus maenas feeding on mussels and dogwhelks. Mar Ecol 16:21–26. doi:10.3354/meps016021
Cushing JM (1991) A simple model of cannibalism. Math Biosci 107:47–71. doi:10.1016/0025-5564(91)90071-P
Day E, Lawton P (1988) Mud crab (Crustacea: Brachyura: Xanthidae) substrate preference and activity. J Shellfish Res 9:257–312. doi:10.2983/035.029.0302
Diehl S (1992) Fish predation and benthic community structure: the role of omnivory and habitat complexity. Ecology 73:1646–1661. doi:10.2307/1940017
Dittel A, Epifanio CE, Natunewicz C (1996) Predation on mud crab megalopae, Panopeus herbstii H. Milne Edwards: effect of habitat complexity, predator species and postlarval densities. J Exp Mar Bio Ecol 198:191–202. doi:10.1016/0022-0981(96)00003-2
Dumas JV (1993) Predation by Herring Gulls (Larus argentatus Coues) on two rocky intertidal crab species [Carcinus maenas (L.) & Cancer irroratus Say]. J Exp Mar Bio Ecol 169:89–101. doi:10.1016/0022-0981(93)90045-P
Ebersole EL, Kennedy VS (1995) Prey preferences of blue crabs Callinectes sapidus feeding on three bivalve species. Mar Ecol Prog Ser 118:167–178. doi:10.3354/meps118167
Ellis JC, Allen KE, Rome MS, Shulman MJ (2012) Choosing among mobile prey species: Why do gulls prefer a rare subtidal crab over a highly abundant intertidal one? J Exp Mar Bio Ecol 416–417:84–91. doi:10.1016/j.jembe.2012.02.014
Fernández M (1999) Cannibalism in Dungeness crab Cancer magister: effects of predator–prey size ratio, density, and habitat type. Mar Ecol Prog Ser 182:221–230. doi:10.3354/meps182221
Fernández M, Iribarne O, Armstrong D (1993) Habitat selection by young-of-the-year Dungeness Crab Cancer magister and predation risk in intertidal habitats. Mar Ecol Prog Ser 92:171–177
Finke DL, Denno RF (2002) Intraguild predation diminished in complex-structured vegetation: implications for prey suppression. Ecology 83:643–652. doi:10.1890/0012-9658%282002%29083%5B0643:IPDICS%5D2.0.CO;2
Grabowski JH (2004) Habitat complexity disrupts predator–prey interactions but not the trophic cascade on oyster reefs. Ecology 85:995–1004. doi:10.1890/03-0067
Gregory GJ, Quijón PA (2011) The impact of a coastal invasive predator on infaunal communities: assessing the roles of density and a native counterpart. J Sea Res 66:181–186. doi:10.1016/j.seares.2011.05.009
Grosholz ED, Ruiz GM (1996) Predicting the impact of introduced marine species: lessons from the multiple invasions of the European Green Crab Carcinus maenas. Biol Conserv 3207:59–66. doi:10.1016/0006-3207(94)00018-2
Heck KL, Hays G, Orth RJ (2003) Critical evaluation of the nursery role hypothesis for seagrass meadows. Mar Ecol Prog Ser 253:123–136. doi:10.3354/meps253123
Hedvall O, Moksnes PO, Pihl L (1998) Active habitat selection by megalopae and juvenile shore crabs Carcinus maenas: a laboratory study in an annular flume. Hydrobiologia 376:89–100. doi:10.1023/A:1017081611077
Hernández Cordero AL, Seitz RD (2014) Structured habitat provides a refuge from blue crab, Callinectes sapidus, predation for the bay scallop, Argopecten irradians concentricus (Say 1822). J Exp Mar Bio Ecol 460:100–108. doi:10.1016/j.jembe.2014.06.012
Hill JM, Weissburg MJ (2013) Habitat complexity and predator size mediate interactions between intraguild blue crab predators and mud crab prey in oyster reefs. Mar Ecol Prog Ser 488:209–219. doi:10.3354/meps10386
Hunt CE, Behrens Yamada S (2003) Biotic resistance experienced by an invasive crustacean in a temperate estuary. Biol Invasions 5:33–43. doi:10.1023/A:1024011226799
Jensen G, McDonald P, Armstrong D (2002) East meets west: competitive interactions between green crab Carcinus maenas, and native and introduced shore crab Hemigrapsus spp. Mar Ecol Prog Ser 225:251–262. doi:10.3354/meps225251
Johnson EG, Hines AH, Kramer MA, Young AC (2008) Importance of season and size of release to stocking success for the blue crab in Chesapeake Bay. Rev Fish Sci 16:243–253. doi:10.1080/10641260701696837
Kneib RT, Lee SY, Kneib JP (1999) Adult–juvenile interactions in the crabs Sesarma (Perisesarma) bidens and S. (Holometopus) dehaani (Decapoda:Grapsidae) from intertidal mangrove habitats in Hong Kong. J Exp Mar Bio Ecol 234:255–273. doi:10.1016/S0022-0981(98)00149-X
Kuroda M, Wada K, Kamada M (2005) Factors influencing coexistence of two brachyuran crabs, Helice tridens and Parasesarma plicatum, in an estuarine salt marsh, Japan. J Crustacean Biol 25:146–153. doi:10.2307/1549938
Langellotto GA, Denno RF (2006) Refuge from cannibalism in complex-structured habitats: implications for the accumulation of invertebrate predators. Ecol Entomol 31:575–581. doi:10.1111/j.1365-2311.2006.00816.x
Lloyd M (1968) Self regulation of adult numbers by cannibalism in two laboratory strains of flour beetles (Tribolium castaneum). Ecology 49:245–259. doi:10.2307/1934453
Long WC, Van Sant SB, Haaga JA (2015) Habitat, predation, growth, and coexistence: Could interactions between juvenile red and blue king crabs limit blue king crab productivity? J Exp Mar Bio Ecol 464:58–67. doi:10.1016/j.jembe.2014.12.011
Luppi TA, Spivak ED, Anger K (2001) Experimental studies on predation and cannibalism of the settlers of Chasmagnathus granulata and Cyrtograpsus angulatus (Brachyura: Grapsidae). J Exp Mar Bio Ecol 265:29–48. doi:10.1016/S0022-0981(01)00322-7
Malyshev A, Quijón PA (2011) Disruption of essential habitat by a coastal invader: new evidence of the effects of green crabs on eelgrass beds. ICES J Mar Sci 68:1852–1856. doi:10.1093/icesjms/fsr126
Mascaró M, Seed R (2001) Choice of prey size and species in Carcinus maenas (L.) feeding on four bivalves of contrasting shell morphology. Hydrobiologia 449:159–170. doi:10.1023/A:1017569809818
Matheson K, Gagnon P (2012) Effects of temperature, body size, and chela loss on competition for a limited food resource between indigenous rock crab (Cancer irroratus Say) and recently introduced green crab (Carcinus maenas L.). J Exp Mar Bio Ecol 428:49–56. doi:10.1016/j.jembe.2012.06.003
McDonald PS, Jensen GC, Armstrong DA (2001) The competitive and predatory impacts of the nonindigenous crab Carcinus maenas (L.) on early benthic phase Dungeness crab Cancer magister Dana. J Exp Mar Bio Ecol 258:39–54. doi:10.1016/S0022-0981(00)00344-0
Mills EL, Leach JH, Carlton JT, Secor CL (1993) Exotic species in the Great Lakes: a history of biotic crises and anthropogenic introductions. J Great Lakes Res 19:1–54. doi:10.1016/S0380-1330(93)71197-1
Miron G, Audet D, Landry T, Moriyasu M (2005) Predation potential of the invasive green crab (Carcinus maenas) and other common predators on commercial bivalve species found on Prince Edward Island. J Shellfish Res 24:579–586. doi:10.2983/0730-8000(2005)24
Moksnes PO (2004) Self-regulating mechanisms in cannibalistic populations of juvenile shore crabs Carcinus maenas. Ecology 85:1343–1354. doi:10.1890/02-0750
Norberg RA (1977) An ecological theory on foraging time and energetics and choice of optimal food-searching method. J Anim Ecol 46:511–529. doi:10.2307/3827
Palacios K, Ferraro SP (2003) Green crab (Carcinus maenas Linnaeus) consumption rates on and prey preference among four bivalve prey species. J Shellfish Res 22:865–871. doi:10.2983/035.029.0302
Paolucci E, MacIsaac H, Ricciardi A (2013) Origin matters: alien consumers inflect greater damage on prey populations than do native consumers. Divers Distrib 19:988–995. doi:10.1111/ddi.12073
Peterson CH (1982) The importance of predation and intra- and interspecific competition in the population biology of two infaunal suspension-feeding bivalves, Protothaca staminea and Chione undatella. Ecol Monogr 52:437–475. doi:10.2307/2937354
Pickering T (2011) Predator–prey interactions between the European green crab (Carcinus maenas) and bivalves native to Prince Edward Island. MSc thesis dissertation, University of Prince Edward Island, Charlottetown, 169 pp
Pickering T, Quijón PA (2011) Potential effects of a non-indigenous predator in its expanded range: assessing green crab, Carcinus maenas, prey preference in a productive coastal area of Atlantic Canada. Mar Biol 158:2065–2078. doi:10.1007/s00227-011-1713-8
Pirtle J, Eckert G, Stoner A (2012) Habitat structure influences the survival and predator–prey interactions of early juvenile red king crab Paralithodes camtschaticus. Mar Ecol Prog Ser 465:169–184. doi:10.3354/meps09883
Pyke G, Pulliam H, Charnov E (1977) Optimal foraging: a selective review of theory and tests. Q Rev Biol 52:137–154. doi:10.2307/2824020
Ricciardi A, Atkinson SK (2004) Distinctiveness magnifies the impact of biological invaders in aquatic ecosystems. Ecol Lett 7:781–784
Ropes JW (1968) The feeding habits of the green crab, Carcinus maenas (L.). Fish B-NOAA 67:183–203
Rossong MA, Williams PJ, Comeau M, Mitchell SC, Apaloo J (2006) Agonistic interactions between the invasive green crab, Carcinus maenas (Linnaeus) and juvenile American lobster, Homarus americanus (Milne Edwards). J Exp Mar Bio Ecol 329:281–288. doi:10.1016/j.jembe.2005.09.007
Rossong MA, Quijón PA, Snelgrove PVR, Barrett TJ, McKenzie CH, Locke A (2012) Regional differences in foraging behaviour of invasive green crab (Carcinus maenas) populations in Atlantic Canada. Biol Invasions 14:659–669. doi:10.1007/s10530-011-0107-7
Schausberger P (2003) Cannibalism among phytoseiid mites: a review. Exo Appl Acarol 29:173–191. doi:10.1023/A:1025839206394
Sih A, Bolnick DI, Luttbeg B, Orrock JL, Peacor SD, Pintor LM, Preisser E, Rehage JS, Vonesh JR (2010) Predator–prey naïveté, antipredator behavior, and the ecology of predator invasions. Oikos 119:610–621. doi:10.1111/j.1600-0706.2009.18039.x
Stoner AW, Ottmar ML, Haines SA (2010) Temperature and habitat complexity mediate cannibalism in red king crab: observations on activity, feeding, and prey defense mechanisms. J Shellfish Res 29:1005–1012. doi:10.2983/035.029.0401
Thiel M, Dernedde T (1994) Recruitment of shore crabs Carcinus maenas on tidal flats: mussel clumps as an important refuge for juveniles. Helgol Meeresunters 48:321–332
Weldon J, Garbary D, Courtenay S, Ritchie W, Godin C, Thériault M-H, Boudreau M, Lapenna A (2005) The Community Aquatic Monitoring Project (CAMP) for measuring marine environmental health in coastal waters of the southern Gulf of St. Lawrence: 2004 overview. Can Tech Rep Fish Aquat Sci 2624:viii-53
Williams PJ, MacSween C, Rossong M (2009) Competition between invasive green crab (Carcinus maenas) and American lobster (Homarus americanus). N Z J Mar Freshw Res 43:29–33. doi:10.1080/00288330909509979
Acknowledgments
Dr E. Paolucci and an anonymous reviewer provided valuable comments on a preliminary version of this manuscript. This study was funded by a NSERC Discovery grant to PAQ and a NSERC CGSM to HG. RC was funded by the Canada Excellence Research Chairs Program. The Community Aquatic Monitoring Program (CAMP) is jointly coordinated by Fisheries and Oceans Canada–Gulf Region and the Southern Gulf of St. Lawrence Coalition on Sustainability.
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Gehrels, H., Knysh, K.M., Boudreau, M. et al. Hide and seek: habitat-mediated interactions between European green crabs and native mud crabs in Atlantic Canada. Mar Biol 163, 152 (2016). https://doi.org/10.1007/s00227-016-2927-6
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DOI: https://doi.org/10.1007/s00227-016-2927-6