Marine Biology

, Volume 148, Issue 6, pp 1357–1367 | Cite as

Phenotype-environment matching in the shore crab (Carcinus maenas)

  • P. A. ToddEmail author
  • R. A. Briers
  • R. J. Ladle
  • F. Middleton
Research Article


The shore crab (Carcinus maenas) exhibits a range of carapace pattern polymorphisms, but little is known regarding their function or maintenance. If patterns represent some form of crypsis, then associations between carapace colouration and substrate are expected; to determine whether such relationships exist, frequency of crab morphs and quantity of substrate type were measured from fifteen 10×40 m2 quadrats at each of three sites along the southern shore of the Firth of Forth, Scotland. Five thousand one hundred and thirty-seven crabs and 3.6 km of line intercept transect data were collected during a 9-week period. Crab abundance, relative frequency of morphs and substrate type varied significantly among the three sites. Plain crabs were strongly associated with macro-algal substrates whereas patterned crabs were associated with mussel beds. This pronounced phenotype-environment matching, as well as various characteristics of the carapace patterns themselves, suggests that patterned crabs are cryptic on polychromatic backgrounds. The frequency of patterned crabs and the percentage of white pigment on the carapace both declined significantly with carapace width. The loss of pattern coincides with an ontogenetic shift in habitat use and we present evidence to suggest that individual crabs lose their pigment, rather than larger patterned crabs being preferentially removed from the population by predators. Throughout their life history, shore crabs encounter high variation in predation, food supply, and physical habitat; to survive they have evolved a strategy that includes elements of pattern polymorphism, crypsis, ontogenetic shifts, and plastic responses.


Plastic Response Carapace Width White Pigment Rock Pool Green Crab 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



This study was funded and supported by the School of Life Sciences, Napier University. East Lothian Council, Scotland, kindly gave their permission to conduct this research on land under their jurisdiction. Many thanks to A. Brunton, A. Tan and P. Ward for their field assistance, discussion, and editing. We would also like to thank the two anonymous reviewers for their comments and constructive criticism.


  1. Abello P, Aagaard A, Warman CG, Depledge MH (1997) Spatial variability in the population structure of the shore crab Carcinus maenas (Crustacea: Brachyura) in shallow-water, weakly tidal fjord. Mar Ecol Prog Ser 147:97–103CrossRefGoogle Scholar
  2. Abramsky Z, Rosenzweig ML, Subach A (2002) Measuring the benefit of habitat selection. Behav Ecol 13:497–502CrossRefGoogle Scholar
  3. Bedini R (2002) Colour change and mimicry from juvenile to adult: Xantho poressa (Olivi, 1792) (Brachyura, Xanthidae) and Carcinus maenas (Linnaeus, 1758) (Brachyura, Portunidae). Crustaceana 75:703–710CrossRefGoogle Scholar
  4. Bostrom C, Mattila J (1999) The relative importance of food and shelter for seagrass-associated invertebrates: a latitudinal comparison of habitat choice by isopod grazers. Oecologia 120:162–170CrossRefGoogle Scholar
  5. Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13:115–155Google Scholar
  6. Brian MV (1965) Caste differentiation in social insects. Symp Zool Soc Lon 14:13–38Google Scholar
  7. Brian JV (2002) Inter-population variability in the shore crab (Carcinus maenas) and its potential use as a bio-marker of anthropogenic effects. PhD Dissertation. Napier University, EdinburghGoogle Scholar
  8. Brian JV, Fernandes T, Ladle RJ, Todd PA (2005) Patterns of morphological and genetic variability in UK populations of the shore crab (Carcinus maenas). J Exp Mar Biol Ecol (in press)Google Scholar
  9. Bull JJ (1983) Evolution of sex determining mechanisms. Benjamin-Cummings, Melano ParkGoogle Scholar
  10. Crothers JH (1966) The biology of the shore crab Carcinus maenas (L.) 1. The background—anatomy, growth and life history. Field Stud 2:407–434Google Scholar
  11. Crothers JH (1968) The biology of the shore crab Carcinus maenas (L.) 2. The life of the adult crab. Field Stud 2:579–614Google Scholar
  12. Crowe TP, Underwood AJ (1998) Testing behavioural “preferences” for suitable microhabitat. J Exp Mar Biol Ecol 225:1–11CrossRefGoogle Scholar
  13. DeWitt TJ, Sih A, Wilson DS (1998) Costs and limits of phenotypic plasticity. Trends Ecol Evol 13:77–81CrossRefGoogle Scholar
  14. Eggleston DB, Armstrong DA (1995) Pre- and post-settlement determinants of estuarine dungeness crab recruitment. Ecol Monogr 65:193–216CrossRefGoogle Scholar
  15. Ekendahl A (1998) Colour polymorphic prey (Littorina saxatilis Olivi) and predatory effects of a crab population (Carcinus maenas L.). J Exp Mar Biol Ecol 222:239–246CrossRefGoogle Scholar
  16. Ekendahl A, Johannesson K (1997) Shell colour variation in Littorina saxatilis Olivi ( Prosobranchia: Littorinidae): a multifactor approach. Biol J Linn Soc 62:401–419CrossRefGoogle Scholar
  17. Endler JA (1978) A predators view of animal color patterns. Evol Biol 11:319–364Google Scholar
  18. Endler JA (1984) Progressive background in moths, and a quantitative measure of crypsis. Biol J Linn Soc 22:187–231CrossRefGoogle Scholar
  19. Endler JA (1988) Frequency-dependent predation, crypsis and aposematic coloration. Proc R Soc Lond B 319:505–523Google Scholar
  20. English S, Wilkinson C, Baker V (1997) Survey manual for tropical marine resources. Australian Institute of Marine Science, TownsvilleGoogle Scholar
  21. Etter RJ (1988) Physiological stress and color polymorphism in the intertidal snail Nucella lapillus. Evolution 42:660–680CrossRefGoogle Scholar
  22. Forsman A, Appelqvist S (1999) Experimental manipulation reveals differential effects of colour pattern on survival in male and female pygmy grasshopper. J Evol Biol 12:391–401CrossRefGoogle Scholar
  23. Glanville PW, Allen JA (1997) Protective polymorphism in populations of computer-simulated moth-like prey. Oikos 80:565–571CrossRefGoogle Scholar
  24. Goodhart CB (1987) Why are some snails visibly polymorphic, and others not? Biol J Linn Soc 31:35–58CrossRefGoogle Scholar
  25. Gosselin LA, Chia FS (1995) Distribution and dispersal of early juvenile snails: effectiveness of intertidal microhabitats as refuges and food sources. Mar Ecol Prog Ser 128:213–223CrossRefGoogle Scholar
  26. Greenwood MDF, Hill AS (2003) Temporal, spatial and tidal influences on benthic and demersal fish abundance in the Forth estuary. Estuar Coast Shelf Sci 58:211–225CrossRefGoogle Scholar
  27. Grimm GG, Yarnold PR (1995) Reading and understanding multivariate statistics. American Psychological Association, WashingtonGoogle Scholar
  28. Guarino SM, Gambardella C, Ianniruberto M, de Nicola M (1993) Colour polymorphism in Idotea baltica from the bay of Naples and its ecological significance. J Mar Biol Assoc UK 73:785–794Google Scholar
  29. Hacker SD, Madin LP (1991) Why habitat architecture and color and important to shrimps living in pelagic Sargassum: use of camouflage and plant-part mimicry. Mar Ecol Prog Ser 70:143–155CrossRefGoogle Scholar
  30. Hannaford Ellis CJ (1984) Ontogenetic change of shell colour patterns in Littorina neglecta Bean (1844). J Conchol 31:343–347Google Scholar
  31. Harris DJ, Jones JS (1995) Genotype-specific habitat selection and thermal ecology in Nucella lapillus (L.) (the dogwhelk). Heredity 74:311–314Google Scholar
  32. Hayward PJ, Ryland JS (1998) Handbook of the marine fauna of north-west Europe. Oxford University Press, OxfordGoogle Scholar
  33. Hedvall O, Moksnes P, Pihl L (1998) Active habitat selection by megalopae and juvenile shore crabs Carcinus maenas: a laboratory study in an annular flume. Hydrobiologia 375/376:89–100CrossRefGoogle Scholar
  34. Hogarth PJ (1975) Pattern polymorphism and predation in the shore crab, Carcinus maenas (L.). Crustaceana 28:316–319Google Scholar
  35. Hogarth PJ (1978) Variation in the carapace pattern of juvenile Carcinus maenas. Mar Biol 44:337–343CrossRefGoogle Scholar
  36. Hogarth PJ (1983) Crabs in labs: the shore crab (Carcinus maenas) as teaching material. J Biol Educ 17:105–111Google Scholar
  37. Hovel KA, Lipcius RN (2002) Effects of seagrass habitat fragmentation on juvenile blue crab survival and abundance. J Exp Mar Biol Ecol 271:75–98CrossRefGoogle Scholar
  38. Hull SL, Rollinson D (2000) Sex-biased colour polymorphism in the marine ostracod Paradoxostoma variabile (Crustacea). J Mar Biol Assoc UK 80:69–73CrossRefGoogle Scholar
  39. Johannesson K, Ekendahl A (2002) Selective predation favouring cryptic individuals of marine snails (Littorina ). Biol J Linn Soc 76:137–144CrossRefGoogle Scholar
  40. Johnson CR, Field CA (1993) Using fixed-effects model multivariate analysis of variance in marine biology and ecology. Oceanogr Mar Biol Annu Rev 31:177–221Google Scholar
  41. Jones JS, Leith BH, Rawlings P (1977) Polymorphism in Cepaea: a problem with too many solutions? Annu Rev Ecol Syst 8:109–143CrossRefGoogle Scholar
  42. Kamenos NA, Moore PG, Hall-Spencer JM (2004) Attachment of the juvenile queen scallop (Aequipecten opercularis (L.)) to maerl in mesocosm conditions; juvenile habitat selection. J Exp Mar Biol Ecol 306:139–155CrossRefGoogle Scholar
  43. Kono H, Reid PJ, Kamil AC (1998) The effect of background cuing on prey detection. Anim Behav 56:963–972CrossRefPubMedGoogle Scholar
  44. Lively CM (1986) Predator-induced shell dimorphism in the acorn barnacle Chthmalus anisopoma. Evolution 40:232–242CrossRefGoogle Scholar
  45. McGraw IJ, Kaiser MJ, Naylor E, Hughes RN (1992) Intraspecific morphological variation related to the moult-cycle in colour forms of the shore crab Carcinus maenas. J Zool Lond 228:351–359Google Scholar
  46. McKnight A, Mathews LM, Avery R, Lee KT (2000) Distribution is correlated with color phase in green crabs, Carcinus maenas (Linnaeus, 1758) in southern New England. Crustaceana 73:763–768CrossRefGoogle Scholar
  47. Merilaita S (1998) Crypsis through disruptive coloration in an isopod. Proc R Soc Lond B 265:1059–1064CrossRefGoogle Scholar
  48. Merilaita S (2003) Visual background complexity facilitates the evolution of camouflage. Evolution 57:1248–1254PubMedGoogle Scholar
  49. Merilaita S, Lyytinen A, Mappes J (2001) Selection for cryptic coloration in a visually heterogeneous habitat. Proc R Soc Lond B 268:1925–1929CrossRefGoogle Scholar
  50. Miner BG, Morgan SG, Hoffman JR (2000) Postlarval chromatophores as an adaptation to ultraviolet radiation. J Exp Mar Biol Ecol 249:235–248CrossRefPubMedGoogle Scholar
  51. Moczek AP (1998) Horn polyphenism in the beetle Onthophagus taurus: larval diet quality and plasticity in parental investment determine adult body size and male horn morphology. Behav Ecol 9:636–641CrossRefGoogle Scholar
  52. Moksnes P (2002) The relative importance of habitat-specific settlement, predation and juvenile dispersal for distribution and abundance of young juvenile shore crabs Carcinus maenas L. J Exp Mar Biol Ecol 271:41–73CrossRefGoogle Scholar
  53. Moksnes P, Pihl L, van Montifrans J (1998) Predation of postlarvae and juveniles of the shore crab Carcinus maenas: importance of shelter, size and cannibalism. Mar Ecol Prog Ser 166:211–225CrossRefGoogle Scholar
  54. Moran N (1992) The evolutionary maintenance of alternative phenotypes. Am Nat 139:971–989CrossRefGoogle Scholar
  55. Nijhout HF (1999) Control mechanisms of polyphenic development in insects—in polyphenic development, environmental factors alter some aspects of development in an orderly and predictable way. Bioscience 49:181–192CrossRefGoogle Scholar
  56. Orth RJ, Montfrans J (2002) Habitat quality and prey size as determinants of survival in post-larval and early juvenile instars of the blue crab Callinectes sapidus. Mar Ecol Prog Ser 231:205–213CrossRefGoogle Scholar
  57. Palma A, Steneck RS (2001) Does variable coloration in juvenile marine crabs reduce risk of visual predation? Ecology 82:2961–2967CrossRefGoogle Scholar
  58. Palma A, Orrego C, Arriagada M (2003) Crypsis in early benthic phases of Brachyura decapod crustaceans in central Chile. Rev Chil Hist Nat 76:149–156Google Scholar
  59. Parsonage S, Hughes J (2002) Natural selection and the distribution of shell colour morphs in three species of Littoraria (Gastropoda: Littorinidae) in Moreton Bay, Queensland. Biol J Linn Soc 75:219–232CrossRefGoogle Scholar
  60. Pietrewicz A, Kamil AC (1979) Search image formation in the blue jay (Cyanocitta critata). Science 204:1332–1333PubMedCrossRefGoogle Scholar
  61. Pittman SJ, McAlpine CA (2001) Movements of marine fish and decapod crustaceans: process, theory and application. Adv Mar Biol 44:294Google Scholar
  62. Powell BL (1962) Types, distribution and rhythmical behaviour of the chromtophores of juvenile Carcinus maenas (L.). J Anim Ecol 31:251–261CrossRefGoogle Scholar
  63. Reid DG, Abello P, Warman CG, Naylor E (1994) Size-related mating success in the shore crab Carcinus maenas (Crustacea: Brachyura). J Zool Lond 232:397–407CrossRefGoogle Scholar
  64. Reid DG, Abello P, Kaiser MJ, Warman CG (1997) Carapace colour, inter-moult duration and the behavioural and physiological ecology of the shore crab Carcinus maenas. Estuar Coast Shelf Sci 44:203–211CrossRefGoogle Scholar
  65. Richards RA (1992) Habitat selection and predator avoidance: ontogenetic shifts in habitat use by the Jonah crab Cancer borealis (Stimpson). J Exp Mar Biol Ecol 156:187–197CrossRefGoogle Scholar
  66. Roman J, Palumbi SR (2004) A global invader at home:population structure of the green crab, Carcinus maenas, in Europe. Mol Ecol 13:2891–2898PubMedCrossRefGoogle Scholar
  67. Schlichting CD (1986) The evolution of phenotypic plasticity in plants. Annu Rev Ecol Syst 17:667–693CrossRefGoogle Scholar
  68. Shapiro AM (1976) Seasonal polyphenism. Evol Biol 9:259–333Google Scholar
  69. Shen CJ (1935) An investigation of the post-larval development of the shore-crab Carcinus maenas, with special reference to the external secondary sexual characters. Proc Zool Soc1–33Google Scholar
  70. Sprung M (2001) Larval abundance and recruitment of Carcinus maenas L. close to its southern geographic limit: a case of match and mismatch. Hydrobiologia 449:153–158CrossRefGoogle Scholar
  71. Smith DAS (1975) Polymorphism and selective predation in Donax faba Gmelin (Bivalvia: Tellinacea). J Exp Mar Biol Ecol 17:205–219CrossRefGoogle Scholar
  72. Symonds FL, Langslow DR, Pienkowski MW (1984) Movements of wintering shorebirds within the Firth of Forth: species differences in usage of an intertidal complex. Biol Conserv 28:187–215CrossRefGoogle Scholar
  73. Ter Braak CJF, Smailauer P (1998) CANOCO reference manual and user’s guide to Canonco for windows: software for community ordination (version 4). Microcomputer Power, IthacaGoogle Scholar
  74. Thiel M, Dernedde T (1994) Recruitment of shore crabs Carcinus maenas on tidal flats: mussel clumps ad an important refuge for juveniles. Helgolander Meeresun 48:321–332CrossRefGoogle Scholar
  75. Todd PA, Sidle RC, Chou LM (2002a) Plastic corals from Singapore 1. Coral Reefs 21:391–392Google Scholar
  76. Todd PA, Sidle RC, Chou LM (2002b) Plastic corals from Singapore 2. Coral Reefs 21:407–408Google Scholar
  77. Todd PA, Ladle RJ, Lewin-Koh NJI, Chou LM (2004a) Genotype x environmental interactions in transplanted clones of the massive corals Favia speciosa and Diploastrea heliopora. Mar Ecol Prog Ser 271:167–182CrossRefGoogle Scholar
  78. Todd PA, Sidle RC, Lewin-Koh NJI (2004b) An aquarium experiment for identifying the physical factors inducing morphological change in two massive scleractinian corals. J Exp Mar Biol Ecol 299:97–113CrossRefGoogle Scholar
  79. Uvarov R (1966) Grasshoppers and locusts. A handbook of general acridology. Cambridge University Press, CambridgeGoogle Scholar
  80. Wahle RA (1992) Body-size dependent anti-predator mechanisms of the American lobster. Oikos 65:52–60CrossRefGoogle Scholar
  81. Wente WH, Phillips JB (2003) Fixed green and brown color morphs and a novel color-changing morph of the Pacific tree frog Hyla regilla. Am Nat 162:461–473CrossRefPubMedGoogle Scholar
  82. Whiteley DAA, Owen DF, Smith DAS (1997) Massive polymorphism and natural selection in Donacilla cornea (Poli, 1791) (Bilvalvia: Mesodesmatidae). Biol J Linn Soc 62:475–494CrossRefGoogle Scholar
  83. Yoshimura T, Yamakawa H (1988) Microhabitat and behavior of settled pueruli and juveniles of the Japanese spiny lobster Panulirus japonicus at Kominato, Japan. J Crust Biol 8:524–531CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2005

Authors and Affiliations

  • P. A. Todd
    • 1
    Email author
  • R. A. Briers
    • 2
  • R. J. Ladle
    • 3
  • F. Middleton
    • 2
  1. 1.Marine Biology Laboratory, Department of Biological SciencesNational University of SingaporeSingaporeSingapore
  2. 2.School of Life SciencesNapier UniversityEdinburghUK
  3. 3.School of Geography and EnvironmentUniversity of OxfordOxfordUK

Personalised recommendations