Hostname: page-component-8448b6f56d-mp689 Total loading time: 0 Render date: 2024-04-25T00:25:14.870Z Has data issue: false hasContentIssue false
  • English
  • Français

Impact of wave exposure on seasonal morphological and reproductive responses of the intertidal limpet Fissurella crassa (Mollusca: Archaegastropoda)

Published online by Cambridge University Press:  28 March 2012

José Pulgar ,
Marcos Alvarez ,
Alejandro Delgadillo ,
Ines Herrera ,
Samanta Benitez ,
Juan Pablo Morales ,
Pilar Molina ,
Marcela Aldana  and
Victor Manuel Pulgar
José Pulgar*
Affiliation:
Universidad Andres Bello, Departamento de Ecología & Biodiversidad, República 470, SantiagoChile
Marcos Alvarez
Affiliation:
Universidad Andres Bello, Facultad de Ciencias Biológicas, República 217, Santiago, Chile
Alejandro Delgadillo
Affiliation:
Universidad Andres Bello, Departamento de Ecología & Biodiversidad, República 470, SantiagoChile Escuela de Ingeniería en Acuicultura, Universidad Andres Bello, República 440, Santiago, Chile
Ines Herrera
Affiliation:
Universidad Andres Bello, Departamento de Ecología & Biodiversidad, República 470, SantiagoChile
Samanta Benitez
Affiliation:
Universidad Andres Bello, Departamento de Ecología & Biodiversidad, República 470, SantiagoChile Universidad Andres Bello Escuela de Biología Marina, República 440, Santiago, Chile
Juan Pablo Morales
Affiliation:
Universidad Andres Bello, Facultad de Ciencias Biológicas, República 217, Santiago, Chile
Pilar Molina
Affiliation:
Pontificia Universidad Católica de Chile, Alameda 370, Santiago, Chile
Marcela Aldana
Affiliation:
Universidad Andres Bello, Departamento de Ecología & Biodiversidad, República 470, SantiagoChile Pontificia Universidad Católica de Chile, Alameda 370, Santiago, Chile Escuela de Pedagogía en Biología y Ciencias, Facultad de Ciencias de la Educación, Universidad Central de Chile,Santa Isabel 1278, Santiago
Victor Manuel Pulgar
Affiliation:
Center for Research in Obstetrics & Gynecology, Wake Forest School of Medicine and Biomedical Research Infrastructure Center, Winston-Salem State University, Winston-Salem NC, USA
*
Correspondence should be addressed to: J. Pulgar, Universidad Andres Bello, Departamento de Ecología & Biodiversidad, República 470, SantiagoChile email: jpulgar@unab.cl
Get access Rights & Permissions [Opens in a new window]

Abstract

Intertidal organisms have long been considered an ideal system to quantify how physical variations determine differential energy allocations in specimens inhabiting environmental gradients such as exposure to wave action. In habitats with differential intertidal wave exposure (sheltered, Sh; and exposed, E) seasonal gonadal and foot weight variations and their associations with exposure and food availability (algae abundance) were determined in the keyhole limpet Fissurella crassa. Gonadal weight is used as a measure of reproduction allocation whereas foot weight is an indirect indicator of energy allocation to survival. RNA:DNA ratio in limpets obtained from Sh and E habitats during the two different seasons was used as an indicator of biosynthetic capability. Our results indicate that algae abundance in E sites was higher in summer and lower in winter compared to Sh sites. In E sites the muscular foot weight of limpet was higher in summer in contrast to Sh sites where F. crassa muscular foot weight of limpet was higher in winter. Gonadal weight in Sh sites was higher in summer and remained constant in winter; whereas in E sites gonadal weight was lower in summer and higher in winter. RNA:DNA ratios indicate that regardless of intertidal wave exposure, F. crassa showed higher biosynthetic capability in summer. Energetic allocation in animals that inhabit sheltered intertidal habitats would support constant allocation towards reproduction. In contrast, animals that inhabit exposed habitats may favour seasonally reproduction allocation at expense of survival.

Keywords

shell morphologyRNA:DNA ratioenergetic trade-off
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 92 , Issue 7 , November 2012 , pp. 1595 - 1601
Copyright
Copyright © Marine Biological Association of the United Kingdom 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aguilera, M. (2011) The functional roles of the hervibores in the rocky intertidal systems in Chile: a review of food preferences and consumptive effects. Revista Chilena de Historia Natural 84, 241–261.Google Scholar
Astorga, M.P., Guiñez, R., Ortiz, J.C. and Castilla, J.C. (2002) Variación fenotípica y genética en el tunicado Pyura praeputialis (Heller, 1878) en el área Norte de la Bahía de Antofagasta, Chile. Revista Chilena de Historia Natural 75, 515–526.Google Scholar
Bretos, M. and Chihuailaf, R. (1993) Studies on the reproduction and gonadal parasites of Fissurella pulchra (Gastropoda: Prosobranchia). Veliger 36, 245–251.Google Scholar
Bretos, M., Tesorieri, I. and Alvarez, L. (1983) The biology of Fissurella maxima Sowerby (Mollusca: Archaeogastropoda) in northern Chile. 2. Notes on its reproduction. Biological Bulletin. Marine Biological Laboratory, Woods Hole 165, 559–568.Google Scholar
Bretos, M., Gutiérrez, J. and Espinoza, Z. (1988) Estudios biológicos para el manejo de Fissurella picta . Medio Ambiente 9, 28–34.Google Scholar
Brown, M.K. and Quinn, J.F. (1988) The effect of wave action on growth in three species of intertidal gastropods. Oecologia 75, 420–425.Google Scholar
Buckley, L.J. and Caldarone, E. (1999) RNA–DNA ratio and other nucleic acid-based indicators for growth and condition of marine fishes. Hydrobiologia 401, 265–277.Google Scholar
Caldarone, E.M., Onge-Burns, J.M. and Buckley, L.J. (2003) Relationship of RNA/DNA ratio and temperature to growth in larvae of Atlantic cod, Gadus morhua . Marine Ecology Progress Series 262, 229–421.Google Scholar
Carrington, E. (1990) Drag and dislodgment of an intertidal macroalga: consequences of morphological variation in Mastocarpus papillatus Kützing. Journal of Experimental Marine Biology and Ecology 139, 185–200.Google Scholar
Chícharo, M. and Chícharo, L. (2008) RNA:DNA ratio on other nucleic acid derived indices in marine ecology. International Journal of Molecular Science 9, 1453–1471.Google Scholar
Chícharo, L., Chícharo, M.A., Alves, F., Amaral, A., Pereira, A. and Regala, J. (2001) Diel variation of the RNA:DNA ratios in Crassostrea angulata (Lamarck) and Ruditapes decussates (Linnaeus 1758) (Mollusca, Bivalvia). Journal of Experimental Marine Biology and Ecology 259, 121–129.CrossRefGoogle Scholar
Chomczynski, P. (1993) A reagent for the single-step simultaneous isolation of RNA, DNA and proteins from cell and tissue samples. Bio-Techniques 15, 532–537.Google ScholarPubMed
Chomczynski, P. and Sacchi, N. (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Analytic Biochemistry 162, 156–159.Google Scholar
Chown, S.L. and Gaston, K.J. (1999) Exploring links between physiology and ecology at macro scales: the role of respiratory metabolism in insects. Biological Reviews 74, 87–120.Google Scholar
Chown, S.L. and Gaston, K.J. (2000) Areas, cradles and museums: the latitudinal gradient in species richness. Trends in Ecology and Evolution 8, 310–315.Google Scholar
Colman, J.S. (1933) The nature of the intertidal zonation of plants and animals. Journal of the Marine Biological Association of the United Kingdom 18, 435–476.Google Scholar
Dahlhoff, E.P. (2004) Biochemical indicators of stress and metabolism: applications for marine ecological studies. Annual Review of Physiology 66, 183–207.CrossRefGoogle ScholarPubMed
Dahlhoff, E.P., Stillman, J. and Menge, B. (2002) Physiological community ecology: variation in metabolic activity of ecologically important rocky intertidal invertebrates along environmental gradients. Integrative and Comparative Biology 42, 862–871.Google Scholar
Denny, M.W. (1988) Biology and the mechanics of the wave-swept environment. Princeton, NJ: Princeton University Press 329 pp.Google Scholar
Denny, M.W. (1999) Are there mechanical limits to size in wave-swept organisms? Journal of Experimental Biology 202, 3463–3467.Google Scholar
Denny, M.W. and Blanchette, C.A. (2000) Hydrodynamics, shall shape, behavior, and survivorship in the owl limpet, Lottia gigantea . Journal of Experimental Biology 203, 2623–2639.CrossRefGoogle Scholar
Dortch, Q., Roberts, T.L., Clayton, J.R. and Ahmed, S.I. (1983) RNA/DNA ratios and DNA concentrations as indicators of growth rate and biomass in planktonic organisms. Marine Ecology Progress Series 13, 61–71.CrossRefGoogle Scholar
Doty, M.S. (1971) Measurement of water movement in reference to benthic algal growth. Botánica Marina 14, 32–35.Google Scholar
Etter, R.J. (1988) Physiological stress and color polymorphism in the intertidal snail Nucella lapillus . Evolution 42, 660–680.CrossRefGoogle ScholarPubMed
Gaston, K. and Spicer, J. (1998) Do upper thermal tolerances differ in geographically separated populations of the beachflea Orchestia gammarellus (Crustacea: Amphipoda)? Journal of Experimental Marine Biology and Ecology 229, 256–276.CrossRefGoogle Scholar
Gaylord, B., Blanchette, C.A. and Denny, M.W. (1994) Mechanical consequences of size in wave-swept algae. Ecological Monographs 64, 287–313.CrossRefGoogle Scholar
Gerard, V. and Mann, K.H. (1979) Growth and production of Laminaria longicruris (Phaeophyta) populations exposed to different intensities of water movement. Phycology 15, 33–41.CrossRefGoogle Scholar
Guiñez, R. and Pacheco, C. (1999) Estimaciones de la velocidad máxima del oleaje en el intermareal rocoso de Chile Central, utilizando un dinamómetro prototipo. Revista Chilena de Historia Natural 72, 251–260.Google Scholar
Hammond, K.A. and Wunder, B.A. (1991) The role of diet quality and energy need in the nutritional ecology of a small herbivore: Microtus ochrogaster . Physiological Zoology 64, 541–567.Google Scholar
Helmuth, B. and Hofmann, G.E. (2001) Microhabitats, thermal heterogeneity, and patterns of physiological stress in the rocky intertidal zone. Biological Bulletin. Marine Biological Laboratory, Woods Hole 201, 374–384.Google Scholar
Hernandez, C.E., Neill, P.A., Pulgar, J.M., Ojeda, F.P. and Bozinovic, F. (2002) Water temperature fluctuations and territoriality in the intertidal zone: two possible explanations for the elevational distribution of body size in Graus nigra (Kyphosidae). Journal of Fish Biology 61, 472–488.Google Scholar
Hofmann, G.E. (2005) Patterns of Hsp gene expression in ectothermic marine organisms on small to large biogeographic scales. Integrative and Comparative Biology 45, 247–255.CrossRefGoogle ScholarPubMed
Ikeda, T., San, F., Yamaguchi, A. and Matsuishi, T. (2007) RNA:DNA ratios of calanoid copepods from the epipelagic through abyssopelagic zones of the North Pacific Ocean. Aquatic Biology 1, 99–108.Google Scholar
Jones, W.E. and Demetropoulos, A. (1968) Exposure to wave action: measurements of an important ecological parameter on rocky shores on Anglesey. Journal of Experimental Marine Biology and Ecology 2, 46–63.Google Scholar
Karasov, W.H. (1986) Energetics, physiology and vertebrate ecology. Trends in Ecology and Evolution 1, 101–104.Google Scholar
Lemos, D., Garcia-Carren, F.L., Hernández, P. and Toro, A.N. (2002) Ontogenetic variation in digestive proteinase activity, RNA and DNA content of larval and postlarval white shrimp Litopenaeus schmitti . Aquaculture 214, 363–380.Google Scholar
McLean, J.H. (1984) Systematics of Fissurella in the Peruvian and Magellanic faunal provinces (Gastropoda: Prosobranchia). Contributions in Science: Natural History Museum of Los Angeles County 354, 1–70.CrossRefGoogle Scholar
Moeser, G.M., Leba, H. and Carrington, E. (2006) Seasonal influence of wave action on thread production in Mytilus edulis . Journal of Experimental Biology 209, 881–890.CrossRefGoogle ScholarPubMed
Moore, P.G. and Seed, R. (1986) The ecology of rocky coasts. New York: Columbia University Press, 467 pp.Google Scholar
Newell, R.C. (1970) Biology of intertidal animals. Faversham, UK: Marine Ecological Survey, 556 pp.Google Scholar
Oliva, D. and Castilla, J. (1986) The effects of human exclosure on the population structure of key-hole limpets Fissurella crassa and Fissurella limbata in the coast of Central Chile. Marine Ecology 7, 201–217.Google Scholar
Oliva, D. and Castilla, J. (1992) Guía para el reconocimiento y morfometría de diez especies del género Fissurella Bruguière, 1789 (Mollusca:Gastropoda) comunes en la pesquería y conchales indígenas de Chile central y sur. Gayana Zoología 56, 77–108.Google Scholar
Olivares, A., Jofré, D., Alvarez, C. and Bustos, C. (2009). Hermafroditismo funcional de la gónada de Fissurella crassa (Mollusca: Fissurellidae). International Journal of Morphology 27, 509–514.Google Scholar
Palumbi, S.R. (2003) Ecological subsidies alter the structure of marine communities. Proceedings of the National Academy of Sciences of the United States of America 21, 11927–11928.CrossRefGoogle Scholar
Parmesan, C. and Yohe, G. (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42.Google Scholar
Pino, C., Oliva, D.P. and Castilla, J. (1994) Ritmos de actividad en lapas Fissurella crassa Lamarck 1822 y F. latimarginata Sowerby 1835: efectos del ciclo de marea y fotoperiodo. Revista de Biología Marina 29, 89–99.Google Scholar
Piersma, T. and Lindstrom, A. (1997) Rapid reversible changes in organ size as a component of adaptive behaviour. Trends in Ecology and Evolution 12, 134–138.CrossRefGoogle ScholarPubMed
Pulgar, J., Alvarez, M., Morales, J., Garcia-Huidobro, M., Aldana, M., Ojeda, F.P. and Pulgar, V.M. (2011) Impact of oceanic upwelling on morphometric and molecular indices of an intertidal fish Scarthichthys viridis (Blennidae). Marine and Freshwater Behaviour and Physiology 44, 33–42.CrossRefGoogle Scholar
Raffaelli, D. and Hawkins, S. (1996) Intertidal ecology. London: Chapman and Hall, 356 pp.Google Scholar
Ricklefs, R. and Wikelski, M. (2002) The physiology/life-history nexus. Trends in Ecology and Evolution 17, 462–468.Google Scholar
Roff, D.A. (2002) Life history evolution. Sunderland, MA: Sinauer Associates, 465 pp.Google Scholar
Sanford, E. (2002) Community responses to climate change: links between temperature and keystone predation in a rocky intertidal system. In Schneider, S.H. and Root, T.L. (eds) Wildlife responses to climate change: North American case studies. Covelo, CA: Island Press, pp. 165–200.Google Scholar
Sebens, K.P. (2002) Energetic constraint, size gradient, and size limits in benthic marine invertebrates. Integrative and Comparative Biology 142, 853–861.CrossRefGoogle Scholar
Serra, G., Chelazzi, G. and Castilla, J.C. (2001) Temporal and spatial activity of the key-hole limpet Fissurella crassa (Mollusca: Gastropoda) in the eastern Pacific. Journal of the Marine Biological Association of the United Kingdom 81, 485–490.Google Scholar
Sibly, R.M. (1991) The life-history approach to physiological ecology. Functional Ecology 5, 184–191.Google Scholar
Sibly, R.M. and Calow, P. (1986) Physiological ecology of animals: an evolutionary approach. Oxford: Blackwell Scientific Publications, 190 pp.Google Scholar
Smith, J.M., Green, S.J., Kelley, C.A., Prufert-Bebout, L. and Bebout, B.M. (2008) Shifts in methanogen community structure and function associated with long-term manipulation of sulfate and salinity in a hypersaline microbial mat. Environmental Microbiology 10, 386–394.Google Scholar
Somero, G.N. (2002) Thermal physiology of intertidal animals: optima, limits, and adaptive plasticity. Integrative and Comparative Biology 42, 780–789.Google Scholar
Spicer, J. and Gaston, K. (1999) Physiological diversity and its ecological implications. Oxford: Blackwell Scientific Publications, 240 pp.Google Scholar
Stearns, S.C. (1989) Trade-offs in life-history. Evolution 3 259–268.Google Scholar
Stearns, S.C. (1992) The evolution of life histories. Oxford: Oxford University Press, 249 pp.Google Scholar
Stickle, W.B. and Bayne, B.L. (1987) Energetics of the muricid gastropod Thais (Nucella) lapillus . Journal of Experimental Marine Biology and Ecology 107, 263–278.Google Scholar
Thorpe, J.E., Talbot, C. and Villarreal, C. (1982) Bimodality of growth and smolting in Atlantic salmon, Salmo salar L. Aquaculture 28, 123–132.Google Scholar
Tomanek, L. and Helmuth, B. (2002) Physiological ecology of rocky intertidal organisms: a synergy of concepts. Integrative and Comparative Biology 42, 771–775.Google Scholar
Truchot, J.P. and Duhanel-Jouve, A. (1980) Oxygen and carbon dioxide in the marine intertidal environments: diurnal and tide changes in rockpools. Respiration Physiology 39, 241–254.Google Scholar
Trussell, G.C., Johnson, A.S., Rudolph, S.G. and Gilfillan, E.S. (1993) Resistance to dislodgment: habitat and size-specific differences in morphology and tenacity in an intertidal snail. Marine Ecology Progress Series 100, 135–144.Google Scholar
Wagner, M., Durbin, E. and Buckley, L. (1998) RNA:DNA ratios as indicators of nutritional condition in the copepod Calanus finmarchicus . Marine Ecology Progress Series 162, 173–181.CrossRefGoogle Scholar
Warner, R.R. (1984) Deferred reproduction as a response to sexual selection in a coral reef fish: a test of the life historical consequences. Evolution 38, 148–162.Google Scholar
Wiener, J. (1992) Physiological limits to sustainable energy budgets in birds and mammals: ecological implications. Trends in Ecology and Evolution 7, 384–388.Google Scholar
Zar, J.H. (1996) Biostatistical analysis. 5th edition. Englewood Cliffs, NJ: Prentice-Hall, 622 pp.Google Scholar
Zera, A.J. and Harshman, L.G. (2001) Physiology of life history trade-offs in animals. Annual Review of Ecology, Evolutions, and Systematics 32, 95–106.CrossRefGoogle Scholar