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Attachment capacity of the sea urchin Paracentrotus lividus in a range of seawater velocities in relation to test morphology and tube foot mechanical properties

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Abstract

Intertidal rocky shores are stressful environments where benthic invertebrates experience large wave-induced hydrodynamic forces that can detach them from the substratum. The tube feet of echinoids counteract these forces and help them remain securely affixed. Sea urchins display a high degree of phenotypic plasticity which may help them cope with hydrodynamic stress. We evaluated whether habitats presenting different seawater velocities induce plastic responses in the attachment capacity of the sea urchin Paracentrotus lividus by quantifying their morphology and the adhesive and mechanical properties of their tube feet. Intertidal adult sea urchins from three subpopulations were collected around the Crozon peninsula (France). Localities differed according to measured water velocities. Size was significantly lower in the two most exposed sites where sea urchins also presented a higher density of tube feet. Tube foot adhesive properties were not significantly different between sites, but their extensibility and toughness were significantly higher in individuals from the most exposed site. Using this information, we calculated a safety factor to predict the flow velocity that would cause detachment from the substratum. It showed individuals from the most exposed habitat would resist higher flow velocities (up to 7.59 ± 0.90 m s−1). Both morphometry and tube foot mechanical properties vary among subpopulations and show an intraspecific plasticity in P. lividus. Although, differences in sea water velocity may be one cause of this intraspecific variation, it likely results from a combination of biotic and abiotic factors.

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Abbreviations

σ :

Stress

Δl :

Extension

ε :

Strain

µ :

Dynamic viscosity

ρ :

Density

ADV:

Acoustic Doppler velocimeter

ANOVA:

Analysis of variance

CC:

Cap de la Chèvre

C d :

Drag coefficient

C l :

Lift coefficient

F d :

Disk detachment force

F g :

Global detachment force

F hydro :

Hydrodynamic force

F max :

Maximal attachment force

F t :

Traction force

FWL:

Fractional weight loss

IL:

Illien

I :

Length

l o :

Initial length

L :

Sea urchin length (test diameter with spines)

MO:

Morgat

PS:

Polystyrene

PVC:

Polyvinyl chloride

Re :

Reynolds number

SCT:

Cross-sectional surface area of the stem connective tissue layer

S d :

Disk adhesive surface

SF:

Safety factor

S g :

Global adhesive surface area

S pl :

Planform projected surface area

S pr :

Profile projected surface area

SHOM:

French National Hydrographic Service

t :

Temperature

T :

Tenacity

TF:

Number of adoral tube feet

T d :

Disk tenacity

T g :

Global tenacity

u :

Water velocity

UV:

Ultraviolet

References

  • Boudouresque CF, Verlaque M (2007) Ecology of Paracentrotus lividus. In: Laurence JM (ed) Edible sea urchins: biology and ecology, 2nd edn. Elsevier, Tampa, pp 243–285. doi:10.1016/S0167-9309(07)80077-9

    Google Scholar 

  • Denny MW (1985) Wave forces on intertidal organisms: a case study. Limnol Oceanogr 30:1171–1187. doi:10.4319/lo.1985.30.6.1171

    Article  Google Scholar 

  • Denny MW (1988) Biology and the mechanics of the wave swept-environment. Princeton University Press, Princeton

    Book  Google Scholar 

  • Denny MW (1991) Biology, natural selection and the prediction of maximal wave-induced forces. S Afr J Mar Sci 10:353–363. doi:10.2989/02577619109504644

    Article  Google Scholar 

  • Denny MW, Gaylord B (1996) Why the urchin lost its spines: hydrodynamic forces and survivorship in three echinoids. J Exp Biol 199:717–729

    CAS  Google Scholar 

  • DeWitt TJ, Schneider SM (2004) Phenotypic plasticity: functional and conceptual approaches. Oxford University Press, Oxford

    Google Scholar 

  • Ebert TA (1980) Relative growth of sea urchin jaws: an example of plastic resource allocation. Bull Mar Sci 30(2):467–474

    Google Scholar 

  • Ebert TA (1996) Adaptative aspects of phenotypic plasticity in echinoderms. Oceanol Acta 19(3–4):347–355

    Google Scholar 

  • Ebert TA, Hernández JC, Clemente S (2014) Annual reversible plasticity of feeding structures: cyclical changes of jaw allometry in a sea urchin. Proc R Soc B 281:20132284. doi:10.1098/rspb.2013.2284

    Article  Google Scholar 

  • Edwards PB, Ebert TA (1991) Plastic responses to limited food availability and spine damage in the sea urchin Strongylocentrotus purpuratus (Stimpson). J Exp Mar Biol Ecol 145:205–220. doi:10.1016/0022-0981(91)90176-W

    Article  Google Scholar 

  • Fernández C (1996) Croissance et nutrition de Paracentrotus lividus dans le cadre d’un projet aquacole avec alimentation artificielle. Dissertation, Université de Corse, Corsica

  • Fernández C, Boudouresque C (1997) Phenotypic plasticity of Paracentrotus lividus (Echinodermata: Echinoidea) in a lagoonal environment. Mar Biol Prog Ser 152(1–3):145–154

    Article  Google Scholar 

  • Flammang P (1996) Adhesion in echinoderms. In: Jangoux M, Lawrence JM (eds) Echinoderm studies, vol 5. Balkema, Rotterdam, pp 1–60

    Google Scholar 

  • Flammang P, Jangoux M (1993) Functional morphology of coronal and peristomial podia in Sphaerechinus granularis (Echinodermata Echinoidea). Zoomorphol 113:47–60. doi:10.1007/BF00430976

    Article  Google Scholar 

  • Frank PW (1981) A condition for a sessile strategy. Am Nat 118:288–290

    Article  Google Scholar 

  • Gallien WB (1986) A comparison of hydrodynamic forces on two sympatric sea urchins: implications of morphology and habitat. Master thesis, University of Hawaii, Hawaii

  • Gaylord B (2000) Biological implications of surf-zone flow complexity. Limnol Oceanogr 45(1):174–188. doi:10.4319/lo.2000.45.1.0174

    Article  Google Scholar 

  • Gaylord B, Blanchette CA, Denny MW (1994) Mechanical consequences of size in wave-swept algae. Ecol Monogr 64:287–313. doi:10.2307/2937164

    Article  Google Scholar 

  • Grosjean P, Spirilet C, Gosselin P, Vaitilingon D, Jangoux M (1998) Land-based, closed-cycle echiniculture of Paracentrotus lividus (Lamarck) (Echinoidea Echinodermata): a long-term experiment at a pilot scale. J Shellfish Res 17(5):1523–1531

    Google Scholar 

  • Guidetti P, Mori P (2005) Morpho-functional defences of Mediterranean sea urchins, Paracentrotus lividus and Arbacia lixula, against fish predators. Mar Biol 147(3):797–802. doi:10.1007/s00227-005-1611-z

    Article  Google Scholar 

  • Haag N, Russell M, Hernández JC (2016) Effects of spine damage and microhabitat on resource allocation of the purple sea urchin Strongylocentrotus purpuratus (Stimpson 1857). J Exp Biol Ecol 482:106–117. doi:10.1016/j.jembe.2016.05.005

    Article  Google Scholar 

  • Hart AM, Lasi FE, Glenn EP (2002) SLODS: slow dissolving standards for water flow measurements. Aquat Eng 25:239–252. doi:10.1016/S0144-8609(01)00085-1

    Article  Google Scholar 

  • Helmuth B, Denny M (2003) Predicting wave exposure in the rocky intertidal zone: Do bigger waves always lead to larger forces? Limnol Oceangr 48(3):1338–1345. doi:10.4319/lo.2003.48.3.1338

    Article  Google Scholar 

  • Hennebert E, Haesaerts D, Dubois Ph, Flammang P (2010) Evaluation of the different forces brought into play during tube foot activities in sea stars. J Exp Biol 213:1162–1174. doi:10.1242/jeb.037903

    Article  Google Scholar 

  • Hernández JC, Russell MP (2010) Substratum cavities affect growth-plasticity, allometry, movement and feeding rates in the sea urchin Strongylocentrotus purpuratus. J Exp Biol 213:520–525. doi:10.1242/jeb.029959

    Article  Google Scholar 

  • Jacinto D, Cruz T (2012) Parcentrotus lividus (Echinodermata: Echinoidea) attachment force and burrowing behavior in rocky shores of SW Portugal. Zoosymposia 7:231–240.

    Google Scholar 

  • Kawamata S (1998) Effect of waves-induced oscillatory flow on grazing by a subtidal sea urchin Strongylocentrotus nudus (A Agassiz). J Exp Mar Biol Ecol 224:31–48. doi:10.1016/S0022-0981(97)00165-2

    Article  Google Scholar 

  • Kawamata S (2010) Inhibitory effects of wave action on destructive grazing by sea urchins: a review. Bull Fish Res Agen 32:95–102

    Google Scholar 

  • Kiliç A, Teymen A (2008) Determination of mechanical properties of rocks using simple methods. Bull Eng Geol Environ 67:237. doi:10.1007/s10064-008-0128-3

    Article  Google Scholar 

  • Lauzon-Guay JS, Scheibling RE (2007) Seasonal variation in movement, aggregation and destructive grazing of the green sea urchin (Strongylocentrotus droebachiensis) in relation to wave action and sea temperature. Mar Biol 151:2109–2118. doi:10.1007/s00227-007-0668-2

    Article  Google Scholar 

  • Lawrence JM (1987) A functional biology of echinoderms. Croom Helm Ltd. Publishers, London

    Google Scholar 

  • Levitan DR (1991) Skeletal changes in the test and jaws of the sea urchin Diadema antillarum in response to food limitation. Mar Biol 111:431–435. doi:10.1007/BF01319415

    Article  Google Scholar 

  • Lewis JB, Storey GS (1984) Differences in morphology and life history traits of the echinoid Echinometra lucunter from different habitats. Mar Ecol Prog Ser 15:207–211

    Article  Google Scholar 

  • Märkel K, Titschack H (1965) Das Festhaltevermögen von Seeigeln und die Reißfestigkeit ihrer Ambulacralfüßchen. Sond Zeit Naturw 10:268

    Article  Google Scholar 

  • Minor MA, Scheibling RE (1997) Effects of food ration and feeding regime on growth and reproduction of the sea urchin Strongylocentrotus droebachiensis. Mar Biol 129:159–167. doi:10.1007/s002270050156

    Article  Google Scholar 

  • Moran AL (1999) Size and performance of juvenile marine invertebrates: potential contrasts between intertidal and subtidal benthic habitats. Am Zool 39:304–312. doi:10.1093/icb/39.2.304

    Article  Google Scholar 

  • Moureaux C (2011) Plasticité phénotypique du squelette des piquants d’échinides propriétés et fonctions d’un matériau biologique. Dissertation. Université Libre de Bruxelles, Brussels

  • Puijalon S, Bornette G, Sagnes P (2005) Adaptations to increasing hydraulic stress: morphology, hydrodynamics and fitness of two higher aquatic plant species. J Exp Bot 56:777–786. doi:10.1093/jxb/eri063

    Article  CAS  Google Scholar 

  • Russell MP (1987) Life history traits and resource allocation in the purple sea urchin, Strongylocentrotus purpuratus. J Exp Mar Bio Ecol 108:199–216. doi:10.1016/0022-0981(87)90085-2

    Article  Google Scholar 

  • Russell MP (1998) Resource allocation plasticity in sea urchins: rapid, diet induced, phenotypic changes in the green sea urchin, Strongylocentrotus purpuratus (Müller). J Exp Mar Bio Ecol 220:1–14. doi:10.1016/S0022-0981(97)00079-8

    Article  Google Scholar 

  • Russell MP (2001) Spatial and temporal variation in growth of the green sea urchin, Strongylocentrotus droebachiensis, in the Gulf of Maine, USA. In: Barker M, Balkema (eds) Proc 10th Int Echinoderm Conf. Balkema, Rotterdam, pp 533–538

    Google Scholar 

  • Russell MP, Ebert TA, Garcia V, Bodnar A (2013) Field and laboratory growth estimates of the sea urchin Lytechinus variegatus in Bermuda. In: Johnson C (ed) Proc 13th Int Echinoderm Conf. CRC Press, Boca Raton, pp 133–139. doi:10.1201/b13769-19

    Google Scholar 

  • Santos R, Flammang P (2005) Morphometry and mechanical design of tube feet stems in sea urchins: a comparative study. J Exp Mar Biol Ecol 315:211–223. doi:10.1016/j.jembe.2004.09.016

    Article  Google Scholar 

  • Santos R, Flammang P (2006) Morphology and tenacity of the tube foot disc of three common European sea urchins species: a comparative study. Biofouling 22(3):187–200. doi:10.1080/08927010600743449

    Article  Google Scholar 

  • Santos R, Flammang P (2007) Intra- and interspecific variation of attachment strength in sea urchins. Mar Ecol Prog Ser 332:129–142. doi:10.3354/meps332129

    Article  Google Scholar 

  • Santos R, Flammang P (2008) Estimation of the attachment strength of the shingle sea urchin, Colobocentrotus atratus, and comparison with three sympatric echinoids. Mar Biol 154(1):37–49. doi:10.1007/s00227-007-0895-6

    Article  Google Scholar 

  • Santos R, Gorb S, Jamar V, Flammang P (2005a) Adhesion of echinoderm tube feet to rough surfaces. J Exp Biol 208:2555–2567. doi:10.1242/jeb.01683

    Article  Google Scholar 

  • Santos R, Haesaerts D, Jangoux M, Flammang P (2005b) The tube feet of sea urchins and sea stars contain functionally different mutable collagenous tissue. J Exp Biol 208:2277–2288. doi:10.1242/jeb.01641

    Article  Google Scholar 

  • Santos R, Hennebert E, Varela Coelho A, Flammang P (2009). The echinoderm tube foot and its role in temporary underwater adhesion. In: Gorb S (ed) Functional surfaces in biology, vol. 2. Springer, Dordrecht, pp 9–41. doi:10.1007/978-1-4020-6695-5_2

    Google Scholar 

  • Sharp DT, Gray LE (1962) Studies on factors affecting the local distribution of two sea urchins, Arbacia punctulata and Lytechinus variegatus. Ecol 43(2):309–313. doi:10.2307/1931986

    Article  Google Scholar 

  • Siddon E, Witman JD (2003) Influence on chronic, low-level hydrodynamic forces on subtidal community structure. Mar Ecol Prog Ser 261:99–110. doi:10.3354/meps261099

    Article  Google Scholar 

  • Sloan NA (1984) Echinoderm fisheries of the world: a review. In: Keegan B, O’Connor B (eds) Proc 5th Int Echinoderm Conf. Balkema, Rotterdam, pp 24–29

    Google Scholar 

  • Smith AB (1978) A functional classification of the coronal pores of echinoids. Palaeontol 21(4):759–789

    Google Scholar 

  • Statzner B, Holm T (1982) Morphological adaptations of benthic invertebrates to stream flow—an old question studied by means of a new technique (Laser Doppler Anemometry). Oecol 53(3):290–292. doi:10.1007/BF00389001

    Article  Google Scholar 

  • Stearns SC (1989) The evolutionary significance of phenotypic plasticity: phenotypic sources of variation among organisms can be described by developmental switches and reaction norms. Biosci 39:436–446. doi:10.2307/1311135

    Article  Google Scholar 

  • Stewart HL, Britton-Simmons KH (2011) Streamlining behaviour of the red sea urchin Strongylocentrotus franciscanus in response to flow. J Exp Biol 214:2665–2659. doi:10.1242/jeb.056580

    Google Scholar 

  • Thomanek L, Helmuth B (2002) Physiological ecology of intertidal organisms: a synergy of concepts. Integr Comp Biol 42:771–775. Doi:10.1093/icb/42.4.771

    Article  Google Scholar 

  • Toubarro D, Gouveia A, Ribeiro RM, Simões N, da Costa G, Cordeiro C, Santos R (2016) Cloning, characterization and expression levels of the Nectin gene from the tube feet of the sea urchin Paracentrotus lividus. Mar Biotechnol 18(3):372–383. Doi:10.1007/s10126-016-9698-4

    Article  CAS  Google Scholar 

  • Troadec P, Le Goff R et al (1997) Etat des lieux et des milieux de la rade de Brest et de son bassin versant. http://etudes.bretagne-environnement.org/index.php?lvl = notice_display&id = 14288. Accessed 14 July 2013

  • Tuya F, Cisneros-Aguirre J, Ortega L, Haroun RJ (2007) Bathymetric segregation of sea urchins on reefs of the Canarian Archipelago: Role of flow-induced forces. Estuar Coast Shelf Sci 73:481–488. doi:10.1016/j.ecss.2007.02.007

    Article  Google Scholar 

  • Underwood AJ (1999) Physical disturbances and their direct effect on an indirect effect: responses of an intertidal assemblages to as severe storm. J Exp Mar Biol Ecol 232:125–140. doi:10.1016/S0022-0981(98)00105-1

    Article  Google Scholar 

  • Vogel S (1994) Life in moving fluids. 2nd edn. Princeton University Press, Princeton

    Google Scholar 

  • Vogel S (2003) Comparative biomechanics: life’s physical world. Princeton University Press, Princeton

    Google Scholar 

  • Whitman DW, Agrawal AA (2009) What is phenotypic plasticity and why is it important. In: Withman DW, Ananthakrishnan TN (eds) Phenotypic plasticity of insects: mechanism and consequences. Science Publishers, Enfield, pp 1–63. doi:10.1201/b10201-2

    Chapter  Google Scholar 

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Acknowledgements

M. Cohen and C. Moureaux are holders of Belgian FRIA - Fund for Research in Industry and Agriculture PhD fellowships. Ph. Dubois and P. Flammang are Research Directors of the National Fund for Scientific Research (FRS-FNRS, Belgium). The study was supported by an ARES—Research and Higher Education Academy doctoral grant. We thank M. Bauwens and Ph. Pernet for their contributions in conducting the field work, M. Collard for her advices and unconditional assistance, S. MZoudi, M. Bauwens and Th. Dupont and for their valuable technical support in the laboratory. We thank the editor and two reviewers for their useful and constructive feedback on the manuscript.

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Correspondence to Mishal Cohen-Rengifo.

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Animals used in our experiments were maintained and treated in compliance with the guidelines specified by the Belgian Ministry of Trade and Agriculture for the care and use of animals.

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Cohen-Rengifo, M., Moureaux, C., Dubois, P. et al. Attachment capacity of the sea urchin Paracentrotus lividus in a range of seawater velocities in relation to test morphology and tube foot mechanical properties. Mar Biol 164, 79 (2017). https://doi.org/10.1007/s00227-017-3114-0

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