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Evolution of large body size in abalones (Haliotis): patterns and implications

Published online by Cambridge University Press:  08 April 2016

James A. Estes ,
David R. Lindberg  and
Charlie Wray
James A. Estes
Affiliation:
U.S. Geological Survey and Department of Ecology and Evolutionary Biology, Long Marine Laboratory, 100 Shaffer Road, University of California, Santa Cruz, California 95060. E-mail: [email protected]
David R. Lindberg
Affiliation:
Department of Integrative Biology and Museum of Paleontology, University of California, Berkeley, California 94610-4780
Charlie Wray
Affiliation:
Mount Desert Island Biological Laboratory, Old Bar Harbor Road, Salisbury Cove, Maine 04672
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Abstract

Kelps and other fleshy macroalgae—dominant reef-inhabiting organisms in cool seas—may have radiated extensively following late Cenozoic polar cooling, thus triggering a chain of evolutionary change in the trophic ecology of nearshore temperate ecosystems. We explore this hypothesis through an analysis of body size in the abalones (Gastropoda; Haliotidae), a widely distributed group in modern oceans that displays a broad range of body sizes and contains fossil representatives from the late Cretaceous (60–75 Ma). Geographic analysis of maximum shell length in living abalones showed that small-bodied species, while most common in the Tropics, have a cosmopolitan distribution, whereas large-bodied species occur exclusively in cold-water ecosystems dominated by kelps and other macroalgae. The phylogeography of body size evolution in extant abalones was assessed by constructing a molecular phylogeny in a mix of large and small species obtained from different regions of the world. This analysis demonstrates that small body size is the plesiomorphic state and largeness has likely arisen at least twice. Finally, we compiled data on shell length from the fossil record to determine how (slowly or suddenly) and when large body size arose in the abalones. These data indicate that large body size appears suddenly at the Miocene/Pliocene boundary. Our findings support the view that fleshy-algal dominated ecosystems radiated rapidly in the coastal oceans with the onset of the most recent glacial age. We conclude with a discussion of the broader implications of this change.

Type
Articles
Information
Paleobiology , Volume 31 , Issue 4 , Fall 2005 , pp. 591 - 606
Copyright
Copyright © The Paleontological Society 

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References

Literature Cited

Barron, J. A. 1998. Late Neogene changes in diatom sedimentation in the North Pacific. Journal of Asian Earth Sciences 16:85–95.CrossRefGoogle Scholar
Barron, J. A. 2003. Planktonic marine diatom record of the past 18 My: appearances and extinctions in the Pacific and Southern Oceans. Diatom Research 18:203–224.Google Scholar
Barron, J. A., Larson, B., and Baldauf, J. C. 1991. Evidence for late Eocene to early Oligocene Antarctic glaciation and observations of late Neogene glacial history of Antarctica. Proceedings of the Ocean Drilling Program, Scientific Results 119:869–891.Google Scholar
Berta, A., and Morgan, G. S. 1986. A new sea otter (Carnivora: Mustelidae) from the Late Miocene and Early Pliocene (Hemphillian) of North America. Journal of Paleontology 59:809–819.Google Scholar
Branch, G. M. 1975. Mechanisms reducing intraspecific competition in Patella spp.: migration differentiation and territorial behavior. Journal of Animal Ecology 44:575–600.Google Scholar
Branch, G. M. 1976. Interspecific competition experienced by South African Patella species. Journal of Animal Ecology 45:507–529.CrossRefGoogle Scholar
Browning, J. V., Miller, K. G., Van Fossen, M., Liu, C., Aubry, M.-P., Pak, D. K., and Bybell, L. M. 1996. Lower to middle Eocene sequences of the New Jersey coastal plain and their significance for global climate change. Proceedings of the Ocean Drilling Program, Scientific Results 150:229–242.Google Scholar
Bustamante, R. H., and Branch, G. M. 1996. The dependence of intertidal consumers on kelp-derived organic matter on the west coast of South Africa. Journal of Experimental Marine Biology and Ecology 196:1–28.Google Scholar
Bustamante, R. H., Branch, G. M., and Eekhout, S. 1995. Maintenance of an exceptional intertidal grazer biomass in South Africa: subsidy by subtidal kelps. Ecology 76:2314–2329.Google Scholar
Carpenter, S. R., and Kitchell, J. F., eds. 1993. The trophic cascade in lakes. Cambridge University Press, New York.CrossRefGoogle Scholar
Castenholtz, R. W. 1961. The effect of grazing on marine littoral diatom populations. Ecology 42:783–794.Google Scholar
Castresana, J. 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17:540–552.Google Scholar
Cervato, C., and Burckle, L. 2003. Pattern of first and last appearance in diatoms: oceanic circulation and the position of polar fronts during the Cenozoic. Paleoceanography 18:1055.Google Scholar
Coleman, A. W., and Vacquier, V. D. 2002. Exploring the phylogenetic utility of ITS sequences for animals: a test case for abalone (Haliotis). Journal of Molecular Evolution 54:246–257.Google Scholar
Connor, V. M., and Quinn, J. F. 1984. Stimulation of food species growth by limpet mucus. Science 225:843–844.CrossRefGoogle ScholarPubMed
Creese, R. G., and Underwood, A. J. 1982. Analysis of inter- and intra-specific competition amongst intertidal limpets with different methods of feeding. Oecologia 53:337–347.CrossRefGoogle ScholarPubMed
Cubit, J. D. 1984. Herbivory and the seasonal abundance of algae on a high intertidal rocky shore. Ecology 65:1904–1917.CrossRefGoogle Scholar
DeConto, R. M., and Pollard, D. 2003. Rapid Cenozoic glaciation of Antarctica induced by declining atmospheric CO2 . Nature 421:245–249.Google Scholar
Domning, D. P. 1989. Kelp evolution: a comment. Paleobiology 15:53–56.CrossRefGoogle Scholar
Duffy, J. E., and Hay, M. E. 2001. The ecology and evolution of marine consumer-prey interactions. Pp. 131–157 in Bertness, M. D., Gaines, S. D., and Hay, M. E., eds. Marine community ecology. Sinauer, Sunderland, Mass. Google Scholar
Duggins, D. O., Simenstad, C. A., and Estes, J. A. 1989. Magnification of secondary production by kelp detritus in coastal marine ecosystems. Science 245:170–173.Google Scholar
Durham, J. W. 1979. California's Cretaceous Haliotis . Veliger 21:373–374.Google Scholar
Ebeling, A. W., Laur, D. R., and Rowley, R. J. 1985. Severe storm disturbances and reversal of community structure in a southern California kelp forest. Marine Biology 84:287–294.Google Scholar
Estes, J. A., and Duggins, D. O. 1995. Sea otters and kelp forests in Alaska: generality and variation in a community ecological paradigm. Ecological Monographs 65:75–100.Google Scholar
Estes, J. A., and Steinberg, P. D. 1988. Predation, herbivory, and kelp evolution. Paleobiology 14:19–36.Google Scholar
Estes, J. A., and Steinberg, P. D. 1989. Response to domning. Paleobiology 15:57–60.Google Scholar
Estes, J. A., and VanBlaricom, G. R. 1985. Sea otters and shell-fisheries. pp. 187–235 in Beverton, R. H., Lavigne, D., and Beddington, J., eds. Conflicts between marine mammals and fisheries. Allen and Unwin, London.Google Scholar
Fanshawe, S., VanBlaricom, G. R., and Shelly, A. A. 2003. Restored top carnivores as detriments to the performance of marine protected areas intended for fishery sustainability: a case study with red abalones and sea otters. Conservation Biology 17:273–283.Google Scholar
Gaines, S. D., and Lubchenco, J. 1982. A unified approach to marine plant-herbivore interactions. II. Biogeography. Annual Review of Ecology and Systematics 13:111–138.Google Scholar
Garland, C. D., Cooke, S. L., Grant, J. F., and McMeekin, T. A. 1985. Ingestion of the bacteria on the cuticle of crustose (non-articulated) coralline algae by post-larval and juvenile abalone (Haliotis ruber Leach) from Tasmanian waters. Journal of Experimental Marine Biology and Ecology 91:137–149.Google Scholar
Geiger, D. L. 1998. Recent genera and species of the family Haliotidae Rafinesque, 1815 (Gastropoda: Vetigastropoda). Nautilus 111:85–116.Google Scholar
Geiger, D. L. 2000. Distribution and biogeography of the Recent Haliotidae (Gastropoda: Vetigastropoda) world-wide. Bollettino Malacologico 35:57–120.Google Scholar
Geiger, D. L., and Groves, L. T. 1999. Review of fossil abalone (Gastropoda: Vetigastropoda: Haliotidae) with comparison to Recent species. Journal of Paleontology 73:872–885.CrossRefGoogle Scholar
Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41:95–98.Google Scholar
Harrold, C., and Reed, D. C. 1985. Food availability, sea urchin grazing, and kelp forest community structure. Ecology 66:1160–1169.Google Scholar
Hughes, T. P. 1994. Catastrophes, phase-shifts, and large-scale degradation of a Caribbean coral-reef. Science 265:1547–1551.Google Scholar
Hunter, M. D., and Price, P. W. 1992. Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in natural communities. Ecology 73:724–732.Google Scholar
Hutsell, K. C., Hutsell, L. L., and Pisor, D. L. 1999. Registry of world record size shells. Snail's Pace Productions, San Diego.Google Scholar
Jackson, J. B. C., Kirby, M. X., Berger, W. H., Bjorndal, K. A., Botsford, L. W., Bourque, B. J., Bradbury, R., Cooke, R., Estes, J. A., Hughes, T. P., Kidwell, S., Lange, C. B., Lenihan, H. S., Pandolfi, J. M., Peterson, C. H., Steneck, R. S., Tegner, M. J., and Warner, R. 2001. Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638.Google Scholar
Jacobs, D. K., Haney, T. A., and Louie, K. D. 2004. Genes, diversity, and geologic process on the Pacific coast. Annual Review of Ecology and Systematics 32:601–652.Google Scholar
Kawamura, T., Takami, H., Roberts, R. D., and Yamashita, Y. 2001. Radula development in abalone Haliotis discus hannai from larva to adult in relation to feeding transitions. Fisheries Science 67:596–605.Google Scholar
Konar, B. 2000. Seasonal inhibitory effects of marine plants on sea urchins: structuring communities the algal way. Oecologia 125:208–217.CrossRefGoogle ScholarPubMed
Konar, B., and Estes, J. A. 2003. The stability of boundary regions between kelp beds and deforested areas. Ecology 84:174–185.Google Scholar
Larson, B. R., Vadas, R. L., and Keser, M. 1980. Feeding and nutritional ecology of the sea urchin, Strongylocentrotus drobachiensis in Maine, USA. Marine Biology 59:49–62.Google Scholar
Lee, Y. H., and Vacquier, V. D. 1995. Evolution and systematics in Haliotidae (Mollusca: Gastropoda): inferences from DNA sequences of sperm lysin. Marine Biology 124:267–278.Google Scholar
Lindberg, D. R. 1991. Marine biotic interchange between the Northern and Southern Hemispheres. Paleobiology 17:308–324.Google Scholar
Lindberg, D. R. 1992. Evolution, distribution and systematics of Haliotidae. Pp 3–18 in Shepherd, S. A., Tegner, M., and Guzman, S. A., eds. Abalone of the world: biology, fisheries and culture. Blackwell Scientific, Oxford.Google Scholar
Lowry, L. F., and Pearse, J. S. 1973. Abalones and sea urchins in an area inhabited by sea otters. Marine Biology 23:213–219.Google Scholar
Maddison, W., and Maddison, D. 1992. MacClade: analysis of phylogeny and character evolution. Sinauer, Sunderland, Mass.Google Scholar
Mann, K. H., and Lazier, J. R. N. 1996. Dynamics of marine ecosystems: biological-physical interactions in the ocean, 2d ed. Blackwell Scientific, Boston.Google Scholar
McClenachan, L., Jackson, J. B. C., and Newman, M. J. H. 2005. Ecosystem consequences of historic range loss and decline of Caribbean marine megafauna. Proceedings of the National Academy of Sciences USA (in press).Google Scholar
Menge, B. A., Daley, B. A., Lubchenco, J., Sanford, E., Dahlhoff, E., Halpin, P. M., Hudson, G., and Burnaford, J. L. 1999. Top-down and bottom-up regulation of New Zealand rocky intertidal communities. Ecological Monographs 69:297–330.Google Scholar
Miller, R. 1985. Multiple comparisons. Pp. 679–689 in Kotz, S. and Johnson, N. L., eds. Encyclopedia of statistical sciences, Vol. 5. Wiley, New York.Google Scholar
Nelson, C. S., and Cooke, P. J. 2001. History of oceanic front development in the New Zealand sector of the Southern Ocean during the Cenozoic—a synthesis. New Zealand Journal of Geology and Geophysics 44:535–553.Google Scholar
Owen, B., Hanavan, S., and Hall, S. 2001. A new species of abalone (Haliotis) from Greece. Veliger 44:301–309.Google Scholar
Page, R. D. M. 1993. COMPONENT, Version 2: a computer program for analysing evolutionary trees. (http://taxonomy.zoology.gla.ac.uk/rod/cpw.html)Google Scholar
Page, R. D. M. 1996. TREEVIEW Version 1.6.6: an application to display phylogenetic trees on personal computers. Computer Applications in the Biosciences 12:357–358. (http://taxonomy.zoology.gla.ac.uk/rod/treeview.html)Google Scholar
Paine, R. T. 1980. Food webs: linkage, interaction strength, and community infrastructure. Journal of Animal Ecology 49:667–685.Google Scholar
Palmer, A. R. 1979. Fish predation and the evolution of gastropod shell structure: experimental and geographic evidence. Evolution 33:697–713.Google Scholar
Pandolfi, J. M., Bradbury, R. H., Sala, E., Hughes, T. P., Bjorndal, K. A., Cooke, R. G., McArdle, D., McClenachan, L., Newman, M. J. H., Paredes, G., Warner, R. R., and Jackson, J. B. C. 2003. Global trajectories of the long-term decline of coral reef ecosystems. Science 301:955–958.Google Scholar
Parker, B. C., and Dawson, E. Y. 1965. Non-calcareous marine algae from California Miocene deposits. Nova Hedwigia 10:273–295.Google Scholar
Plaganyi, E. E., and Branch, G. M. 2000. Does the limpet Patella cochlear fertilize its own algal garden? Marine Ecology Progress Series 194:113–122.Google Scholar
Polis, G. A., Anderson, W. B., and Holt, R. D. 1997. Towards an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annual Review of Ecology and Systematics 28:289–316.Google Scholar
Prince, J. D., Sellers, T. L., Ford, W. B., and Talbot, S. R. 1987. Experimental evidence for limited dispersal of haliotid larvae (genus Haliotis; Mollusca: Gastropoda). Journal of Experimental Marine Biology and Ecology 106:243–263.Google Scholar
Roberts, R. D., Kawamura, T., and Takami, H. 1999. Morphological changes in the radula of abalone (Haliotis iris) during post-larval development. Journal of Shellfish Research 18:637–644.Google Scholar
Shanks, A. L., Grantham, B. A., and Carr, M. H. 2003. Propagule dispersal distance and the size and spacing of marine reserves. Ecological Applications 13:S159–S169.CrossRefGoogle Scholar
Shepherd, S. A., and Steinberg, P. D. 1992. Food preferences of three Australian abalone species with a review of the algal food of abalone. Pp 169–181 in Shepherd, S. A., Tegner, M., and Guzman, S. A., eds. Abalone of the world: biology, fisheries and culture. Blackwell Scientific, Oxford.Google Scholar
Steinberg, P. D. 1989. Biogeographical variation in brown algal polyphenolics and other secondary metabolites: comparison between temperate Australasia and North America. Oecologia 78:373–382.CrossRefGoogle ScholarPubMed
Steinberg, P. D., Estes, J. A., and Winter, F. C. 1995. Evolutionary consequences of food chain length in kelp forest communities. Proceedings of the National Academy of Sciences USA 92:8145–8148.Google Scholar
Steneck, R. S. 1982. A limpet Acmaea testudinalis coralline alga Clathromorphum circumscriptum association: adaptations and defenses between a selective herbivore and its prey. Ecology 63:507–522.Google Scholar
Steneck, R. S., Graham, M. H., Bourque, B. J., Corbett, D., Erlandson, J. M., Estes, J. A., and Tegner, M. J. 2003. Kelp forest ecosystem: biodiversity, stability, resilience and future. Environmental Conservation 29:436–459.Google Scholar
Swofford, D. L. 1998. PAUP*. Phylogenetic analysis using parsimony (*and other methods), Version 4. Sinauer, Sunderland, Mass. Google Scholar
Tahil, A. S., and Juinio-Menez, M. A. 1999. Natural diet, feeding periodicity and functional response to food density of the abalone, Haliotis asinina L., (Gastropoda). Aquaculture Research 30:95–107.CrossRefGoogle Scholar
Thompson, J. D., Higgins, D. G., and Gibson, T. J. 1994. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position specific gap penalties and weight matrix choice. Nucleic Acids Research 22:4673–4680.Google Scholar
Tutschulte, T. C., and Connell, J. H. 1988. Reproductive biology of three species of abalone (Haliotis) in southern California. Veliger 23:195–206.Google Scholar
Vadas, R. L. 1977. Preferential feeding: an optimization strategy in sea urchins. Ecological Monographs 47:337–371.Google Scholar
Valentine, J. W. 1989. How good was the fossil record? Clues from the Californian Pleistocene. Paleobiology 15:83–94.Google Scholar
VanBlaricom, G. R. 1988. Effects of foraging by sea otters in mussel-dominated intertidal communities. Pp. 48–91 in VanBlaricom, G. R. and Estes, J. A., eds. The community ecology of sea otters. Springer, Berlin.CrossRefGoogle Scholar
Vermeij, G. J. 1978. Biogeography and adaptation: patterns of marine life. Harvard University Press, Cambridge.Google Scholar
Vermeij, G. J. 1992. Time of origin and biogeographical history of specialized relationships between northern marine plants and herbivorous molluscs. Evolution 46:657–664.Google Scholar
Vermeij, G. J. 2001. Community assembly in the sea: geologic history of the living shore biota. Pages 39–60 in Bertness, M. D., Gaines, S. D., and Hay, M. E., eds. Marine community ecology. Sinauer, Sunderland, Mass. Google Scholar
Winter, F. C., and Estes, J. A. 1992. Experimental evidence for the effects of polyphenolic compounds from Dictyoneurum californicum Ruprecht (Phaeophyta: Laminariales) on feeding rate and growth in the red abalone Haliotis rufescens Swainson. Journal of Experimental Marine Biology and Ecology 155:263–277.Google Scholar
Yoon, H. S., Lee, J. Y., Boo, S. M., and Bhattacharya, D. 2001. Phylogeny of Alariaceae, Laminariaceae, and Lessoniaceae (Phaeophyceae) based on plastid-encoded RuBisCo spacer and nuclear-encoded ITS sequence comparisons. Molecular Phylogenetics and Evolution 21:231–243.Google Scholar