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Recruitment of the limpet Patella ulyssiponensis and its relationship with crustose coralline algae: patterns of juvenile distribution and larval settlement

Published online by Cambridge University Press:  04 November 2019

M. I. Seabra Open the ORCID record for M. I. Seabra [Opens in a new window] ,
T. Cruz ,
J. N. Fernandes ,
T. Silva  and
S. J. Hawkins
M. I. Seabra*
Affiliation:
MARE, Marine and Environmental Sciences Centre, Laboratório de Ciências do Mar, Universidade de Évora, Apartado 190, 7521-903 Sines, Portugal
T. Cruz
Affiliation:
MARE, Marine and Environmental Sciences Centre, Laboratório de Ciências do Mar, Universidade de Évora, Apartado 190, 7521-903 Sines, Portugal Departamento de Biologia, Escola de Ciências e Tecnologia, Universidade de Évora, Évora, Portugal
J. N. Fernandes
Affiliation:
MARE, Marine and Environmental Sciences Centre, Laboratório de Ciências do Mar, Universidade de Évora, Apartado 190, 7521-903 Sines, Portugal
T. Silva
Affiliation:
MARE, Marine and Environmental Sciences Centre, Laboratório de Ciências do Mar, Universidade de Évora, Apartado 190, 7521-903 Sines, Portugal
S. J. Hawkins
Affiliation:
Marine Biological Association of the UK, Citadel Hill, Plymouth PL1 2PB, UK Ocean and Earth Science, University of Southampton, Waterfront Campus, European Way, Southampton SO14 3ZH, UK
*
Author for correspondence: M. I. Seabra, E-mail: [email protected]
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Abstract

Recruitment of the limpet Patella ulyssiponensis was investigated in relation to the presence of living crustose coralline algae (CCA) in rocky-shore habitats. Juvenile limpets (≤10 mm maximum shell length) were counted in CCA-present and CCA-absent habitats, on three shores in SW Portugal during summer 2007 and winter 2009. Furthermore, the settling response of laboratory-reared larvae of P. ulyssiponensis to CCA-covered substratum, and bare-rock, was examined. Across the intertidal zone, we found a clear association between the distribution and abundance of juveniles and the presence of CCA. Although the presence of CCA was not an absolute requisite for juvenile occurrence, null juvenile densities were mostly recorded in CCA-absent areas. The highest juvenile densities (maximum of 64 individuals in 15 × 15 cm) were consistently found in CCA-dominated habitats, namely steep wave-exposed areas at low-shore and rock-pools. The hypothesis of CCA-enhanced settlement was not supported, as settlement intensities of laboratory-reared larvae were similar between chips of rock encrusted by CCA and chips of bare-rock. From the overall number of settlers onto CCA-encrusted rock chips, 51% were found in tiny pits lacking CCA. This was the first study of the settlement patterns of larvae of the genus Patella using naturally occurring rocky substrata. These results are preliminary and should be confirmed with choice-experiments and improved monitoring of the position of settlers. We suggest that CCA plays a role in the recruitment of P. ulyssiponensis, potentially promoting survivorship of early benthic stages, but possibly not enhancing settlement.

Keywords

Coralline crustslimpet recruitmentpatellid larvaePatellogastropodarocky-shore habitatssettlement cuesSW Portugal
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 99 , Issue 8 , December 2019 , pp. 1787 - 1796
Copyright
Copyright © Marine Biological Association of the United Kingdom 2019 

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Footnotes

The online version of this article has been updated since original publication. A notice detailing the changes has also been published.

References

Aquino de Souza, R, Tyler, P and Hawkins, SJ (2009) Artificial oocyte maturation in Patella depressa and Patella vulgata using NaOH-alkalinized seawater. Marine Biology Research 5, 37–41.Google Scholar
Barker, MF (1977) Observations on the settlement of the brachiolaria larvae of Stichaster australis (Verrill) and Coscinasterias calamaria (Gray) (Echinodermata: Asteroidea) in the laboratory and on the shore. Journal of Experimental Marine Biology and Ecology 30, 95–108.Google Scholar
Barnes, JR and Gonor, JJ (1973) The larval settling response of the lined chiton Tonicella lineata. Marine Biology 20, 259–264.Google Scholar
Bowman, RS (1981) The morphology of Patella spp. juveniles in Britain, and some phylogenetic inferences. Journal of the Marine Biological Association of the United Kingdom 61, 647–666.Google Scholar
Bowman, RS (1985) The biology of the limpet Patella vulgata L. in the British Isles: spawning time as a factor determining recruitment success. In Moore, PG and Seed, R (eds), The Ecology of Rocky Coasts. New York, NY: Columbia University Press, pp. 178–193.Google Scholar
Bowman, RS and Lewis, JR (1986) Geographical variation in the breeding cycles and recruitment of Patella spp. Hydrobiologia 56, 41–56.Google Scholar
Branch, GM (1975 a) Intraspecific competition in Patella cochlear Born. Journal of Animal Ecology 44, 263–281.Google Scholar
Branch, GM (1975 b) Mechanisms reducing intraspecific competition in Patella spp.: migration, differentiation and territorial behaviour. Journal of Animal Ecology 44, 575–600.Google Scholar
Branch, GM (1976) Interspecific competition experienced by South African Patella species. Journal of Animal Ecology 45, 507–529.Google Scholar
Branch, GM (1981) The biology of limpets: physical factors, energy flow and ecological interactions. Oceanography and Marine Biology: An Annual Review 19, 235–280.Google Scholar
Castro, JJ (2004) Predação humana no litoral rochoso alentejano: caracterização, impacte ecológico e conservação (PhD thesis). University of Évora, Évora, Portugal.Google Scholar
CIEMAR (2018) Substrato duro intertidal. Monitorização de Ambientes Marinhos do Porto de Sines - MAPSi 2015/2017. Relatório final. Laboratório de Ciências do Mar da Universidade de Évora, 74 pp.Google Scholar
Coleman, RA, Underwood, AJ, Benedetti-Cecchi, L, Aberg, P, Arenas, F, Arrontes, J, Castro, J, Hartnoll, RG, Jenkins, SR, Santina, PD, Hawkins, SJ, Coleman, RA, Underwood, AJ and Jenkins, SR (2006) A continental scale evaluation of the role of limpet grazing on rocky shores. Oecologia 147, 556–564.Google Scholar
Davies, PS (1967) Physiological ecology of Patella. II. Effect of environmental acclimation on the metabolic rate. Journal of the Marine Biological Association of the United Kingdom 47, 61–74.Google Scholar
Davies, PS (1969) Physiological ecology of Patella. III. Desiccation effects. Journal of the Marine Biological Association of the United Kingdom 49, 291–304.Google Scholar
de Figueiredo, MAO, Kain, JM and Norton, TA (1996) Biotic interactions in the colonization of crustose coralline algae by epiphytes. Journal of Experimental Marine Biology and Ecology 199, 303–318.Google Scholar
Delany, J, Myers, AA and McGrath, D (1998) Recruitment, immigration and population structure of two coexisting limpet species in mid-shore tidepools, on the west coast of Ireland. Journal of Experimental Marine Biology and Ecology 221, 221–230.Google Scholar
Delany, J, Myers, AA and McGrath, D (2002) A comparison of the interactions of the limpets Patella vulgata and Patella ulyssiponensis with crustose coralline algae. In Myers, A (ed.), New Survey of Clare Island: Marine Intertidal Ecology. Dublin: Royal Irish Academy, pp. 79–90.Google Scholar
Dodd, JM (1957) Artificial fertilization, larval development and metamorphosis in Patella vulgata L. and Patella coerulea L. Pubblicazione della Stazione Zoologica di Napoli 29, 172–186.Google Scholar
Espinosa, F, Rivera-Ingraham, G and Garcia-Gomez, JC (2010) Early stages of development in the endangered limpet Patella ferruginea Gmelin, 1791 (Gastropoda: Patellidae). The Nautilus 124, 51–53.Google Scholar
Ferranti, MP, Monteggia, D, Asnaghi, V and Chiantore, M. (2018) Artificial reproduction protocol, from spawning to metamorphosis, through noninvasive methods in Patella caerulea Linnaeus, 1758. Aquaculture Research 49, 3386–3391.Google Scholar
Firth, LB and Crowe, TP (2008) Large-scale coexistence and small-scale segregation of key species on rocky shores. Hydrobiologia 614, 233–241.Google Scholar
Gardner, J (1986) A method for the investigation of the shell structure of newly settled limpets. Journal of Molluscan Studies 52, 35–37.Google Scholar
Gee, JM (1965) Chemical stimulation of settlement in larvae of Spirorbis rupestris (Serpulidae). Animal Behaviour 13, 181–186.Google Scholar
Guallart, J, Peña, JB, Luque, Á and Templado, J. (2017) Where have all the youngest gone? The postlarval and young stages of the Mediterranean endangered limpet Patella ferruginea Gmelin, 1791. Mediterranean Marine Science 18, 385–392.Google Scholar
Guerra, MT and Gaudêncio, MJ (1986) Aspects of the ecology of Patella spp. on the Portuguese coast. Hydrobiologia 142, 57–69.Google Scholar
Hawkins, SJ and Hartnoll, RG (1983) Grazing of intertidal algae by marine invertebrates. Oceanography and Marine Biology: An Annual Review 21, 195–282.Google Scholar
Hawkins, SJ and Jones, HD (1992) Marine Field Course Guide 1. Rocky Shores. London: Marine Conservation Society.Google Scholar
Hawkins, SJ, Watson, D, Hill, AS, Harding, P, Kyriakides, MA, Hutchinson, S and Norton, TA (1989) A comparison of feeding mechanisms in microphagous, herbivorous, intertidal, prosobranchs in relation to resource partitioning. Journal of Molluscan Studies 55, 151–165.Google Scholar
Hawkins, SJ, Hartnoll, RG, Kain, JM and Norton, TA (1992) Plant–animal interactions on hard substrata in the northeast Atlantic. In John, DM, Hawkins, SJ and Price, JH (eds), Plant–Animal Interactions in the Marine Benthos. Oxford: Clarendon Press, Systematics Association Special Volume, pp. 1–32.Google Scholar
Hodgson, AN, Le Quesne, WJF, Hawkins, SJ and Bishop, JDD (2007) Factors affecting fertilisation success in two species of patellid limpet (Mollusca: Gastropoda) and development of fertilisation kinetics models. Marine Biology 150, 415–426.Google Scholar
Johnson, CR, Sutton, DC, Olson, RR and Giddins, R (1991) Settlement of crown-of-thorns starfish: role of bacteria on surfaces of coralline algae and a hypothesis for deepwater recruitment. Marine Ecology Progress Series 71, 143–162.Google Scholar
Keough, MJ and Downes, BJ (1982) Recruitment of marine invertebrates: the role of active larval choices and early mortality. Oecologia 54, 348–352.Google Scholar
Kooistra, WHCF, Joosten, AMT and van den Hoek, C (1989) Zonation patterns in intertidal pools and their possible causes: a multivariate approach. Botanica Marina 32, 9–26.Google Scholar
Lebour, BMV (1931) The eggs and larvae of the British prosobranchs with special reference to those living in the plankton. Journal of Marine Biology 22, 105–166.Google Scholar
Lewis, JR and Bowman, RS (1975) Local habitat-induced variations in the population dynamics of Patella vulgata. Journal of Experimental Marine Biology and Ecology 17, 165–203.Google Scholar
Maneveldt, GW, Wilby, D, Potgieter, M and Hendricks, MGJ (2006) The role of encrusting coralline algae in the diets of selected intertidal herbivores. Journal of Applied Phycology 18, 619–627.Google Scholar
McGrath, D (1992) Recruitment and growth of the blue-rayed limpet, Helcion pellucidum (L.), in south east Ireland. Journal of Molluscan Studies 58, 425–431.Google Scholar
McGrath, D and Foley, H (2005) Settlement and recruitment of the blue-rayed limpet, Patella pellucida L. in Galway Bay, west coast of Ireland. In Wilson, JG (ed.), The Intertidal Ecosystem: The Value of Ireland's Shores. Dublin: Royal Irish Academy, pp. 100–114.Google Scholar
McQuaid, CD and Froneman, PW (1993) Mutualism between the territorial intertidal limpet Patella longicosta and the crustose alga Ralfsia verrucosa. Oecologia 96, 128–133.Google Scholar
Morse, ANC (1991) How do planktonic larvae know where to settle? American Scientist 79, 154–167.Google Scholar
Morse, AN and Morse, DE (1984) Recruitment and metamorphosis of Haliotis larvae induced by molecules uniquely available at the surfaces of crustose red algae. Journal of Experimental Marine Biology and Ecology 75, 191–215.Google Scholar
Morse, DE, Hooker, N, Duncan, H and Jensen, L (1979) γ-aminobutyric acid, a neurotransmitter, induces planktonic abalone larvae to settle and begin metamorphosis. Science 204, 407–410.Google Scholar
Morse, DE, Hooker, N, Morse, ANC and Jensen, RA (1988) Control of larval metamorphosis and recruitment in sympatric agariciid corals. Journal of Experimental Marine Biology and Ecology 116, 193–217.Google Scholar
Nelson, WA (2009) Calcified macroalgae – critical to coastal ecosystems and vulnerable to change: a review. Marine and Freshwater Research 60, 787–801.Google Scholar
Orton, JH, Southward, AJ and Dodd, JM (1956) Studies on the biology of limpets: II. The breeding of Patella vulgata L. in Britain. Journal of the Marine Biological Association of the United Kingdom 35, 149–176.Google Scholar
Pearce, CM and Scheibling, RE (1990) Induction of metamorphosis of larvae of the green sea urchin, Strongylocentrotus droebachiensis, by coralline red algae. Biological Bulletin 179, 304–311.Google Scholar
Pérez, S, Fernández, N and Ribeiro, PA (2016) Standardization of a Patella spp. (Mollusca, Gastropoda) embryo–larval bioassay and advantages of its use in marine ecotoxicology. Ecotoxicology and Environmental Safety 127, 175–186.Google Scholar
Pérez, S, Sánchez-Marín, P, Bellas, J, Viñas, L, Besad, V and Fernández, N (2019) Limpets (Patella spp. Mollusca, Gastropoda) as model organisms for biomonitoring environmental quality. Ecological Indicators 101, 150–162.Google Scholar
Plaganyi, EE and Branch, GM (2000) Does the limpet Patella cochlear fertilize its own algal garden? Marine Ecology Progress Series 194, 113–122.Google Scholar
Quinn, GP (1988) Effects of conspecific adults, macroalgae and height on the shore on recruitment of an intertidal limpet. Marine Ecology Progress Series 48, 305–308.Google Scholar
Ribeiro, PA (2008) Dispersal and connectivity of Northeastern Atlantic Patellid limpets: a multidisciplinary approach (PhD thesis). University of Southampton, Faculty of Medicine, Health and Life Sciences School of Biological Sciences.Google Scholar
Roberts, RD (2001) A review of settlement cues for larval abalone (Haliotis spp.). Journal of Shellfish Research 20, 571–586.Google Scholar
Roberts, RD, Barker, MF and Mladenov, P (2010) Is settlement of Haliotis iris larvae on coralline algae triggered by the alga or its surface biofilm? Journal of Shellfish Research 29, 671–678.Google Scholar
Rodriguez, SR, Ojedal, FP and Inestrosa, NC (1993) Settlement of benthic marine invertebrates. Marine Ecology Progress Series 97, 193–207.Google Scholar
Rowley, RJ (1989) Settlement and recruitment of sea urchins (Strongylocentrotus spp.) in a sea-urchin barren ground and a kelp bed: are populations regulated by settlement or post-settlement processes? Marine Biology 494, 485–494.Google Scholar
Rumrill, SS and Cameron, RA (1983) Effects of gamma-aminobutyric acid on the settlement of larvae of the black chiton Katharina tunicata. Marine Biology 72, 243–247.Google Scholar
Seabra, MI, Cruz, T, Espirito-Santo, C, Castro, JJ and Hawkins, SJ (in prep.) Rock-pools as nurseries for co-existing limpets: spatial and temporal patterns of limpet recruitment.Google Scholar
Sebens, KP (1983) Settlement and metamorphosis of a temperate soft-coral larva (Alcyonium siderium Verrill): induction by crustose algae. Biological Bulletin 165, 286–304.Google Scholar
Smaldon, PR and Duffus, JH (1984) The effects of temperature, pH and salinity on the maturation of gametes and fertilisation in Patella vulgata L. Journal of Molluscan Studies 50, 232–235.Google Scholar
Smith, FGW (1935) The development of Patella vulgata. Philosophical Transactions of the Royal Society of London Series B, Biological Sciences 225, 95–125.Google Scholar
Steneck, RS (1982) A limpet-coralline alga association: adaptations and defenses between a selective herbivore and its prey. Ecology 63, 507–522.Google Scholar
Strathmann, MF (1987) Reproduction and Development of Marine Invertebrates of the Northern Pacific Coast: Data and Methods for the Study of Eggs, Embryos, and Larvae. Seattle: University of Washington Press.Google Scholar
Tebben, J, Motti, CA, Siboni, N, Tapiolas, DM, Negri, AP, Schupp, PJ, Kitamura, M, Hatta, M, Steinberg, PD and Harder, T (2015) Chemical mediation of coral larval settlement by crustose coralline algae. Scientific Reports 5, 10803.Google Scholar
Thompson, JB (1979) Distribution and population dynamics of the limpet Patella aspera (Lamarck) in Bantry Bay. Journal of Experimental Marine Biology and Ecology 40, 115–135.Google Scholar
Underwood, AJ (2004) Landing on one's foot: small-scale topographic features of habitat and the dispersion of juvenile intertidal gastropods. Marine Ecology Progress Series 268, 173–182.Google Scholar
Vermeij, MJA (2005) Substrate composition and adult distribution determine recruitment patterns in a Caribbean brooding coral. Marine Ecology Progress Series 295, 123–133.Google Scholar
Wanninger, A, Ruthensteiner, B, Lobenwein, S, Salvenmoser, W, Dictus, WJ and Haszprunar, G (1999) Development of the musculature in the limpet Patella (Mollusca, Patellogastropoda). Development Genes and Evolution 209, 226–238.Google Scholar
Weber, LI and Hawkins, SJ (2005) Patella aspera and P. ulyssiponensis: genetic evidence of speciation in the North-east Atlantic. Marine Biology 147, 153–162.Google Scholar
Whalan, S, Webster, NS and Negri, AP (2012) Crustose coralline algae and a cnidarian neuropeptide trigger larval settlement in two coral reef sponges. PLoS ONE 7, e30386–e30386.Google Scholar