Hostname: page-component-7c8c6479df-p566r Total loading time: 0 Render date: 2024-03-28T22:26:06.450Z Has data issue: false hasContentIssue false

Sediment preference, salinity tolerance and COX-1 genetic differences in two purportive species of Luidia (Echinodermata: Asteroidea)

Published online by Cambridge University Press:  28 November 2014

M.P. Cortes
Affiliation:
Department of Biology, University of West Florida, 11000 University Parkway, Pensacola, Florida 32514, USA
H.-M. Chung
Affiliation:
Department of Biology, University of West Florida, 11000 University Parkway, Pensacola, Florida 32514, USA
C.M. Pomory*
Affiliation:
Department of Biology, University of West Florida, 11000 University Parkway, Pensacola, Florida 32514, USA
*
Correspondence should be addressed to: Christopher Pomory, Department of Biology, University of West Florida, 11000, University Parkway, Pensacola, Florida 32514, USA email: cpomory@uwf.edu

Abstract

Specimens collected in or near Pensacola Bay, Florida matching the descriptions of Luidia lawrencei and Luidia clathrata (the congener from which L. lawrencei was recently split) were compared to determine whether their recent taxonomic separation is supported by differences in sediment preference, salinity tolerance and COX-1 mtDNA sequences. Luidia clathrata has a preference for smaller grain sizes, while no statistically significant preference was found for Luidia lawrencei, and no significant difference was found between the species. Luidia clathrata is more tolerant of lower salinity based on the righting response than Luidia lawrencei, especially at salinities lower than 25 g kg−1. The COX-1 comparison returned over 99% homology among individuals of the two species. While sediment preference and salinity tolerance results indicate differences in response to habitat dissimilarities, the COX-1 genetic result is strong evidence against the recently proposed separation of the species. In light of the COX-1 result, we interpret the sediment and salinity results as long-term acclimation responses.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2014 

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

Anderson, R.W. and Darling, D.A. (1954) A test of goodness of fit. Journal of the American Statistical Association 49, 765769.Google Scholar
Barker, M.F. and Russell, M.P. (2007) The distribution and behaviour of Patiriella mortenseni and P. regularis in the extreme hyposaline conditions of the southern New Zealand Fiords. Journal of Experimental Marine Biology and Ecology 355, 7684.Google Scholar
Berger, V.J. and Kharazova, A.D. (1997) Mechanisms of salinity adaptations in marine mollusks. Hydrobiologia 355, 115126.Google Scholar
Binyon, J. (1961) Salinity tolerance and permeability to water of the starfish Asterias rubens. Journal of the Marine Biological Association of the United Kingdom 41, 161174.Google Scholar
Boos, K., Gutow, L., Mundry, R. and Franke, H.D. (2010) Sediment preference and burrowing behavior in the sympatric brittlestars Ophiura albida (Forbes, 1839) and Ophiura ophiura (Linnaeus, 1758) (Ophiuroidea, Echinodermata). Journal of Experimental Marine Biology and Ecology 393, 176181.Google Scholar
Boyer, T., Levitus, S., Garcia, H., Locarnini, R.A., Stephens, C. and Antonov, J. (2005) Objective analyses of annual, seasonal, and monthly temperature and salinity for the world ocean on a 0.25° grid. International Journal of Climatology 25, 931945.Google Scholar
Brown, M.B. and Forsythe, A.B. (1974) Robust tests for equality of variances. Journal of the American Statistical Association 69, 364367.Google Scholar
Bush, G.L. (1975) Modes of animal speciation. Annual Review of Ecology, Evolution, and Systematics 6, 339364.Google Scholar
Clements, L.A. (1988) Substrate selection by the burrowing brittlestar Microphiopholis gracillima (Stimpson) (Echinodermata: Ophiuroidea). Marine and Freshwater Behaviour and Physiology 13, 239255.Google Scholar
Conover, W.J., Johnson, M.E. and Johnson, M.M. (1981) A comparative study of tests for homogeneity of variances, with applications to the outer continental shelf bidding data. Technometrics 23, 351361.Google Scholar
D'Agostino, R.B., Belanger, A. and D'Agostino, R.B. Jr (1990) A suggestion for using powerful and informative tests of normality. American Statistician 44, 316321.Google Scholar
Ellington, W.R. and Lawrence, J.M. (1974) Coelomic fluid volume regulation and isosmotic intracellular regulation by Luidia clathrata (Echinodermata: Asteroidea) in response to hypoosmotic stress. Biological Bulletin 146, 2031.Google Scholar
Etter, R.J. and Grassle, J.F. (1992) Patterns of species diversity in the deep-sea as a function of sediment particle size. Nature 360, 576578.Google Scholar
Ferber, I. and Lawrence, J.M. (1976) Distribution, substratum preference and burrowing behaviour of Lovenia elongata (Gray) (Echinoidea: Spatangoida) in the Gulf of Elat ('Aqaba), Red Sea. Journal of Experimental Marine Biology and Ecology 22, 207225.Google Scholar
Folmer, O., Black, O., Hoeh, W., Lutz, R. and Vrijenhoek, R. (1993) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294299.Google Scholar
Forcucci, D. and Lawrence, J.M. (1986) Effect of low salinity on the activity, feeding, growth and absorption of Luidia clathrata (Echinodermata: Asteroidea). Marine Biology 91, 315321.Google Scholar
Franz, D.R., Worley, E.K. and Merrill, A.S. (1981) Distribution patterns of common seastars of the Middle Atlantic continental shelf of the northwest Atlantic (Gulf of Maine to Cape Hatteras). Biological Bulletin 160, 394418.Google Scholar
Gray, J.S. and Elliott, M. (2009) Ecology of marine sediments: from science to management. Oxford: Oxford University Press.Google Scholar
Gunter, G. (1961) Some relations of estuarine organisms to salinity. Limnology and Oceanography 6, 182190.Google Scholar
Hagy, J.D., Lehrter, J.C. and Murrell, M.C. (2006) Effects of hurricane Ivan on water quality in Pensacola Bay, Florida. Estuaries Coasts 29, 919925.Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. and deWaard, J.R. (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B 270, 313321.Google Scholar
Hebert, P.D.N., Ratnasingham, S. and deWaard, J.R. (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London, Series B 270, S96S99.Google Scholar
Held, M.B.E. and Harley, C.D.G. (2009) Responses to low salinity by the sea star Pisaster ochraceus. Invertebrate Biology 128, 381390.Google Scholar
Hendler, G., Miller, J.E., Pawson, D.L. and Kier, P.M. (1995) Sea stars, sea urchins and allies. Washington, DC: Smithsonian Institution Press.Google Scholar
Himmelman, J.H. and Dutil, C. (1991) Distribution, population size-structure and feeding of subtidal seastars in the northern Gulf of St. Lawrence. Marine Ecology Progress Series 76, 6172.Google Scholar
Himmelman, J.H., Guderley, H., Vignault, G., Drouin, G. and Wells, P.G. (1984) Response of the sea urchin Strongylocentrotus droebachiensis to reduced salinities: importance of size, acclimation and interpopulation differences. Canadian Journal of Zoology 62, 10151021.Google Scholar
Hintz, J.L. and Lawrence, J.M. (1994) Acclimation of gametes to reduced salinity prior to spawning in Luidia clathrata (Echinodermata: Asteroidea). Marine Biology 120, 443446.Google Scholar
Holm, S. (1979) A simple sequentially rejective multiple test procedure. Scandinavian Journal of Statistics 6, 6570.Google Scholar
Hopkins, T.S. and Knott, K.E. (2010) The establishment of a neotype for Luidia clathrata (Say, 1825) and a new species within the genus Luidia (Asteroida: Paxillosida: Luidiidae). In Harris, L.G., Böttger, S.A., Walker, C.W. and Lesser, M.P. (eds) Echinoderms: Durham: Proceedings of The12th International Echinoderm Conference. London: CRC Press, pp. 207212.Google Scholar
Hopkins, T.S., Thompson, L.E., Knott, K.E. and Tingle, T.A. (1999) A study of Luidia clathrata (Say): further evidence for two species rather than one on the mid-western inner continental shelf of the Atlantic Ocean and the Gulf of Mexico. In Carnevali, C. and Bonasoro, F. (eds) Echinoderm research 1998. Rotterdam: A.A. Balkema, pp. 487490.Google Scholar
Kaack, K.E. and Pomory, C.M. (2011) Salinity effects on arm regeneration in Luidia clathrata (Echinodermata: Asteroidea). Marine and Freshwater Behaviour and Physiology 446, 359374.Google Scholar
Kashenko, S.D. (2003) The reaction of the starfish Asterias amurensis and Patiria pectinifera (Asteroidea) from Vostok Bay (Sea of Japan) to a salinity decrease. Russian Journal of Marine Biology 29, 110114.Google Scholar
Kinne, O. (1971) Salinity: animals–invertebrates. In Kinne, O. (ed.) Marine ecology 1. Environmental factors part 2. London: Wiley-Interscience, pp. 820995.Google Scholar
Klinger, T.S. (1978) A study of sediment preference and its effect on distribution in Luidia clathrata Say (Echinodermata: Asteroidea). MS thesis. University of South Florida, Tampa, FL.Google Scholar
Knott, K.E. and Hopkins, T.S. (1998) Morphological and biochemical variation in two color morphs of Luidia clathrata. In Mooi, R. and Telford, M. (eds) Echinoderms: San Francisco: Proceedings of the 9th International Echinoderm Conference. Rotterdam: A.A. Balkema, pp. 923929.Google Scholar
Knott, K.E. and Wray, G.A. (2000) Controversy and consensus in asteroid systematics: new insights to ordinal and familial relationships. American Zoologist 40, 382392.Google Scholar
Lau, D.C., Lau, S.C., Qian, P.Y. and Qiu, J.W. (2009) Morphological plasticity and resource allocation in response to food limitation and hyposalinity in a sea urchin. Journal of Shellfish Research 28, 383388.Google Scholar
Lawrence, J.M., Cobb, J.C. and Talbot-Oliver, T. (2012) Density and dispersion of Luidia clathrata (Echinodermata: Asteroidea) in old Tampa Bay. Marine and Freshwater Behavior and Physiology 45, 101109.Google Scholar
Lawrence, J.M. and Cowell, B.C. (1996) The righting response as an indication of stress in Stichaster striatus (Echinodermata: Asteroidea). Marine and Freshwater Behaviour and Physiology 27, 239248.Google Scholar
Lawrence, J.M., Durán-González, A., Solís-Marín, F.A. and Herrera, J. (2013) Distribution of Luidia clathrata and Luidia lawrencei (Echinodermata: Asteroidea) along the coast of the western Atlantic Ocean, the Gulf of Mexico and the Caribbean Sea. Cahiers de Biologie Marine 54, 525529.Google Scholar
Lehmann, E.L. and Romano, J.P. (2005) Generalizations of the familywise error rate. Annals of Statistics 33, 11381154.Google Scholar
Loosanoff, V.L. (1945) Effects of sea water of reduced salinities upon starfish, A. forbesi, of Long Island Sound. Transactions of the Connecticut Academy of Arts and Sciences 36, 813835.Google Scholar
Matsubara, M., Komatsu, M., Araki, T., Asakawa, S., Yokobori, S., Watanabe, K. and Wada, H. (2005) The phylogenetic status of Paxillosida (Asteroidea) based on complete mitochondrial DNA sequences. Molecular Phylogenetics and Evolution 36, 598605.Google Scholar
McLusky, D.S. and Michael, E. (2004) The estuarine ecosystem: ecology, threats and management. Oxford: Oxford University Press.Google Scholar
McManus, J. (1998) Temporal and spatial variations in estuarine sedimentation. Estuaries 21, 622634.Google Scholar
Nosil, P. (2008) Ernst Mayr and the integration of geographic and ecological factors in speciation. Biological Journal of the Linnean Society 95, 2646.Google Scholar
Palumbi, S.R. (1994) Genetic divergence, reproductive isolation, and marine speciation. Annual Review of Ecology, Evolution and Systematics 25, 547572.Google Scholar
Pomory, C.M. (2006) A note on calculating P values from 0.15–0.005 for the Anderson-Darling normality test using the F distribution. Journal of Applied Statistics 33, 461462.Google Scholar
Pomory, C.M. and Lares, M. (2000) Rate of regeneration of two arms in the field and its effect on body components in Luidia clathrata (Echinodermata: Asteroidea). Journal of Experimental Marine Biology and Ecology 254, 211220.Google Scholar
Roberts, D. (1979) Deposit feeding mechanisms and resource partitioning in tropical holothurians. Journal of Experimental Marine Biology and Ecology 15, 6980.Google Scholar
Russell, M.P. (2013) Echinoderm responses to variation in salinity. In Lesser, M. (ed.) Advances in marine biology. Volume 66. Burlington: Academic Press, pp. 172212.Google Scholar
Shirley, T.C. and Stickle, W.B. (1982) Responses of Leptasterias hexactis (Echinodermata: Asteroidea) to low salinity. I. Survival Activity, feeding, growth, and absorption efficiency. Marine Biology 169, 147154.Google Scholar
Smith, P.J., Rae, D.S., Manderscheid, R.W. and Silbergeld, S. (1981) Approximating the moments and distribution of the likelihood ratio statistic for multinomial goodness of fit. Journal of the American Statistical Association 76, 737740.Google Scholar
Stickle, W.B. and Diehl, W.J. (1987) Effects of salinity on echinoderms. In Jangoux, M. and Lawrence, J.M. (eds) Echinoderm studies. Rotterdam: A.A. Balkema, pp. 235285.Google Scholar
Stoner, A.W. and Ottmar, M.L. (2003) Relationship between size-specific sediment preferences and burial capabilities in juveniles of two Alaska flatfishes. Journal of Experimental Marine Biology and Ecology 282, 85101.Google Scholar
Swift, D.J.P., Oertel, G.F., Tillman, R.W. and Thorne, J.A. (1991) Shelf sand and sandstone bodies. Geometry, facies and sequence stratigraphy. Special publication number 14 of the International Association of Sedimentologists. Oxford: Blackwell.Google Scholar
Tang, S. and Huang, T. (2010) Characterization of mitochondrial DNA heteroplasmy using a parallel sequencing system. BioTechniques 48, 287296.Google Scholar
Telesh, I.V. and Khlebovich, V.V. (2010) Principal processes within the estuarine salinity gradient: a review. Marine Pollution Bulletin 61, 149155.Google Scholar
Vaughan, W.C., Griggs, K.B., Kim, J-W., Bianchi, T.S. and Smith, R.W. (2009) Storm-generated sediment distribution along the northwest Florida inner continental shelf. IEEE Journal of Oceanic Engineering 34, 495515.Google Scholar
Virstein, R. (1979) Predation on estuarine infauna: response patterns of component species. Estuaries 2, 6986.Google Scholar
Waters, J.M., O'Loughlin, P.M. and Roy, M.S. (2004) Cladogenesis in a starfish species complex from southern Australia: evidence for vicariant speciation? Molecular Phylogenetics and Evolution 32, 236245.Google Scholar
Watts, S.A. and Lawrence, J.M. (1990a) The effect of reproductive state, temperature, and salinity on DNA and RNA levels and activities of metabolic enzymes of the pyloric enzymes of the pyloric ceca in the sea star Luidia clathrata (Say). Physiological Zoology 63, 11961215.Google Scholar
Watts, S.A. and Lawrence, J.M. (1990b) The effects of temperature and salinity interactions on righting, feeding, and growth in the sea star Luidia clathrata (Say). Marine Behaviour and Physiology 17, 159165.Google Scholar
Whitlack, R.B. (1981) Animal-sediment relationships in intertidal marine benthic habitats: some determinants of deposit-feeding species diversity. Journal of Experimental Marine Biology and Ecology 53, 3145.Google Scholar
Williams, S.J., Flocks, J., Jenkins, C., Khalil, S. and Moya, J. (2012) Offshore sediment character and sand resource assessment of the northern Gulf of Mexico, Florida to Texas. Journal of Coastal Research 60, 3044.Google Scholar
Xiao, N., Liu, R., Yuan, S. and Sha, Z. (2013) A preliminary phylogenetic analysis of Luidia (Paxillosida: Luidiidae) from Chinese waters with cytochrome oxidase subunit I (COI) sequences. Journal Ocean University China (Oceanic and Coastal Sea Research) 12, 459468.Google Scholar
Zar, J.H. (2010) Biostatistical analysis. 5th edition. Upper Saddle River, NJ: Prentice Hall.Google Scholar
Zhang, X., Leung, F.C., Chan, D.K., Chen, Y. and Wu, C. (2002) Comparative analysis of allozyme, random amplified polymorphic DNA, and microsatellite polymorphism on Chinese native chickens. Poultry Science 81, 10931098.Google Scholar
Zimmerman, K.M., Stancyk, S.E. and Clements, L.A.J. (1988) Substrate selection by the burrowing brittlestar Microphiopholis gracillima (Stimpson) (Echinodermata: Ophiuroidea). Marine Behaviour and Physiology 13, 239255.Google Scholar