Hostname: page-component-586b7cd67f-t8hqh Total loading time: 0 Render date: 2024-11-23T18:20:42.610Z Has data issue: false hasContentIssue false
  • English
  • Français

Escalating herbivory and resulting adaptive trends in calcareous algal crusts

Published online by Cambridge University Press:  08 April 2016

Robert S. Steneck
Robert S. Steneck*
Affiliation:
Department of Paleobiology, Smithsonian Institution, Washington, D.C. 20560, and Department of Earth and Planetary Sciences, The Johns Hopkins University, Baltimore, Maryland 21218
Get access Rights & Permissions [Opens in a new window]

Abstract

Evolutionary changes in herbivore abundance, diversity, and ability to excavate calcareous substrata occurred independently in three major herbivore groups: mollusks, urchins, and fish. These changes in herbivory have escalated dramatically since the mid-Mesozoic Era to the extent that herbivory today is more intense than at any time in the past.

Today, calcareous red algal crusts (i.e., corallines) are a conspicuous and frequently dominant element of shallow marine communities. Corallines and their (assumed) parent taxon, solenopores, probably always required grazing to remain free of epiphytes. The large scale evolutionary trend toward increased grazing intensity may have given the corallines a distinct advantage over the more herbivore-susceptible solenopores. Four anatomical characters unique to corallines may have facilitated their rapid expansion into shallow reef environments and subsequently (more than 100 million years later) allowed them to withstand the more intense levels of grazing that evolved in those environments. Today corallines are the only algal form to thrive under, and often even require, intensive herbivory. The extinction of solenopores and the adaptive radiation of corallines parallel a gradient of escalating herbivory over time.

Herbivores capable of excavating calcareous substrate are also frequently capable of denuding, and preventing the establishment of, stands of large leathery (kelp-like) macrophytes. It is possible that large-scale increases in herbivory have caused large-scale reduction of algal biomass in benthic communities. The presence of algal forests especially in the Paleozoic and early Mesozoic Eras may be a new variable to consider in reconstructing paleoenvironments.

Type
Articles
Information
Paleobiology , Volume 9 , Issue 1 , Winter 1983 , pp. 44 - 61
Copyright
Copyright © The Paleontological Society 

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

Literature Cited

Abate, B., Catalano, R., D'Argenio, B., DiStefano, P., Riccobono, R. 1977. Relationships of algae with depositional environments and faunal assemblages of the Panormide platform, upper Triassic, Northwestern Sicily. Pp. 301–313. In: Flügel, E., ed. Fossil Algae. Springer-Verlag; New York.Google Scholar
Adey, W. H. 1973. Temperature control of reproduction and productivity in a subarctic coralline alga. Phycologia. 12:111–118.Google Scholar
Adey, W. H. and Sperapani, C. P. 1971. The biology of Kvaleya epilaeve a new parasitic genus and species of Corallinaceae. Phycologia. 10:29–42.CrossRefGoogle Scholar
Adey, W. H. and Johansen, H. W. 1972. Morphology and taxonomy of Corallinaceae with special reference to Clathromorphum, Mesophyllum and Neopolyporolithon gen. nov. Phycologia. 11:159–180.CrossRefGoogle Scholar
Adey, W. H. and Macintyre, I. G. 1973. Crustose coralline algae: a re-evaluation in the geological sciences. Geol. Soc. Am. Bull. 84:883–904.Google Scholar
Adey, W. H. and Vassar, J. M. 1975. Colonization, succession and growth rates of tropical crustose coralline algae (Rhodophyta, Cryptonemiales). Phycologia. 14:55–69.Google Scholar
Ausich, W. I. and Bottjer, D. J. 1982. Tiering in suspension-feeding communities on soft substrata throughout the Phanerozoic. Science. 216:173–174.Google Scholar
Bakker, R. T. 1977. Tetrapod mass extinctions: a model of the regulation of speciation rates and immigration by cycles of topographic diversity. Pp. 247–309. In: Hallman, A., ed. Patterns of Evolution, as Illustrated by the Fossil Record. Elsevier; Amsterdam.Google Scholar
Berg, L. S. 1940. Classification of fishes, both recent and fossil. Trav. Inst. Zool. Sic. URRS. 5:87–517.Google Scholar
Bergström, J. 1979. Morphology of fossil arthropods as a guide to phylogenetic relationships. Pp. 3–58. In: Gupta, A. P., ed. Arthropod Phylogeny. Van Nostrand Reinhold Co.; New York.Google Scholar
Bold, H. C. and Wynne, M. J. 1978. Introduction to the Algae. 706 pp. Prentice-Hall Inc.; Englewood Cliffs, New Jersey.Google Scholar
Brawley, S. H. and Adey, W. H. 1981. The effect of micro-grazers on algal community structure in a coral reef microcosm. Mar. Biol. 61:167–177.Google Scholar
Brock, R. E. 1979. An experimental study on the effects of grazing by parrotfishes and the role of refuges in benthic community structure. Mar. Biol. 51:381–388.Google Scholar
Bromley, R. G. 1975. Comparative analysis of fossil and recent echinoid bioerosion. Paleontology. 18:725–739.Google Scholar
Clavijo, I. E., Yntema, J. A., and Ogden, J. C. 1980. An Annotated List of the Fishes of St. Croix, U.S. Virgin Islands. 49 pp. West Indies Lab. Publ. St. Croix. U.S. Virgin Islands.Google Scholar
Conway Morris, S. 1979. Middle Cambrian polychaetes from the Burgess Shale of British Columbia. Phil. Trans. R. Soc., Ser. B. 285:227–274.Google Scholar
Dawkins, R. and Krebs, J. R. 1979. Arms races between and within species. Proc. R. Soc. Lond. Series B. 205:489–511.Google Scholar
Durham, J. W. Jr. 1966. Evolution among the Echinoidea. Biol. Rev. 41:368–391.Google Scholar
Durham, J. W. and Melville, R. V. 1957. A classification of echinoids. J. Paleontol. 31:242–272.Google Scholar
Elliott, G. F. 1964. Tertiary solenoporacean algae and the reproductive structures of the solenoporaceae. Paleontology. 7:695–702.Google Scholar
Elliott, G. F. 1973. A Miocene solenoporoid alga showing reproductive structures. Paleontology. 16:223–230.Google Scholar
Fischer, A. G. and Arthur, M. A. 1977. Secular variations in the pelagic realm. Tulsa, Okla., Soc. of Econ. Paleontol. and Mineral., Spec. Publ. 25:19–50.Google Scholar
Flügel, E. 1977. Environmental models for upper Paleozoic benthic calcareous algal communities. Pp. 314–343. In: Flügel, E., ed. Fossil Algae. Springer-Verlag; New York.Google Scholar
Fretter, V. and Graham, A. 1962. British Prosobranch Mollusca, their Functional Anatomy and Ecology. 548 pp. R. Soc.; London.Google Scholar
Garrett, P. 1970. Phanerozoic stromatolites: noncompetitive ecologic restriction by grazing and burrowing animals. Science. 169:171–173.Google Scholar
Glaessner, M. F. 1976. Early Phanerozoic annelid worms and their geological and biological significance. J. Geol. Soc. 132:259–275.Google Scholar
Glaessner, M. F. 1979. Precambrian. Pp. A79–A118. In: Robinson, R. A. and Teichert, C., eds. Treatise on Invertebrate Paleontology, Pt. A. Geol. Soc. Am. and Univ. Kansas Press; Lawrence, Kansas.Google Scholar
Gosline, W. A. 1971. Functional morphology and classification of teleostean fishes. 208 pp. Univ. Press Hawaii; Honolulu.Google Scholar
Gould, S. J. 1976. Paleontology plus ecology as paleobiology. Pp. 218–236. In: May, R., ed. Theoretical Ecology. W. B. Saunders Co.; Philadelphia.Google Scholar
Graham, A. 1973. The anatomical basis of function in the buccal mass of prosobranch and amphineuran molluscs. J. Zool. Lond. 169:317–348.Google Scholar
Hay, M. E. 1981. Spatial patterns of grazing intensity on a Caribbean barrier reef; herbivory and algal distribution. Aquat. Bot. 11:97–109.Google Scholar
Hiatt, R. W. and Strasburg, D. W. 1960. Ecological relationships of the fish fauna on coral reefs on the Marshall Islands. Ecol. Monogr. 30:65–127.CrossRefGoogle Scholar
Hobson, E. S. 1974. Feeding relationships of teleostean fishes on coral reefs in Kona, Hawaii. Fish. Bull. 72:915–1031.Google Scholar
Ishijima, W., Ozaki, H., and Nakamura, M. 1971. Upper Paleozoic calcareous algae from the limestone at Sakaishimachibun, Saitamaken. Bull. Nat. Sci., Mus. Tokyo. 14:97–136.Google Scholar
Johansen, H. W. 1981. Coralline algae, a first synthesis. 239 pp. CRC Press, Inc.; Boca Raton, Florida.Google Scholar
Johnson, J. H. 1960. Paleozoic Solenoporaceae and related red algae. Q. Colorado School of Mines. 55:1–77.Google Scholar
Johnson, J. H. 1961. Limestone-building algae and algal limestones. 143 pp. Johnson Publ. Co.; Boulder, Colorado.Google Scholar
Johnson, J. H. 1967. Bibliography of fossil algae, algal limestones, and the geological work of algae, 1956–1965. Q. Colorado School of Mines. 62:1–148.Google Scholar
Johnson, J. H. and Kaska, H. V. 1965. Fossil algae from Guatemala. Prof. Contrib. Colorado School of Mines. 1:1–152.Google Scholar
Johnson, J. H., Konishi, K., and Rezak, R. 1959. Studies of Silurian (Gotlandian) algae. Q. Colorado School of Mines. 51:1–171.Google Scholar
Jüch, P. J. W. and Boekschoten, G. J. 1980. Trace fossils and grazing traces produced by Littorina and Lepidochitons, Dutch Wadden Sea. Geologie en Mijbou. 59:33–42.Google Scholar
Kier, P. M. 1965. Evolutionary trends in Paleozoic echinoids. J. Paleontol. 39:436–465.Google Scholar
Kier, P. M. 1974. Evolutionary trends and their functional significance in the post-Paleozoic echinoids. J. Paleontol. 48:1–95.Google Scholar
Kier, P. M. 1977. The poor fossil record of the regular echinoid. Paleobiology. 3:168–174.Google Scholar
Kohn, A. J. and White, J. K. 1977. Polychaete annelids of an intertidal reef limestone platform at Tanguisson, Guam. Micronesica. 13:199–215.Google Scholar
Konishi, K. 1958. Devonian calcareous algae from Alberta, Canada. Q. Colorado School of Mines. 53:85–109.Google Scholar
Lawrence, J. M. 1975. On the relationships between marine plants and sea urchins. Oceanogr. Mar. Biol. Annu. Rev. 13:213–286.Google Scholar
Lemche, H. and Wingstrand, K. G. 1959. The anatomy of Neopilina galatheae Lemche, 1957 (Mollusca, Tryblidiacea), Galathea. Rep. 3:1–63.Google Scholar
Lowenstam, H. A. 1962. Geothite in radular teeth of recent marine gastropods. Science. 137:279–280.Google Scholar
Moore, R. C. 1964. Treatise on invertebrate paleontology. Part I. Mollusca. Vol. 1. Geol. Soc. Am., and Univ. Kansas Press; Boulder, Colo.Google Scholar
Moore, R. C. 1969. Treatise on invertebrate paleontology. Part R. Arthropoda 4. Vol. 1. Geol. Soc. Am. and Univ. Kansas Press; Boulder, Colo.Google Scholar
Ogden, J. C. and Lobel, P. S. 1978. The role of herbivorous fishes and urchins in coral reef communities. Evol. Biol. Fish. 3:19–63.Google Scholar
Paine, R. T. 1980. Food webs: linkage, interaction strength and community infrastructure. J. Anim. Ecol. 40:667–685.Google Scholar
Paine, R. T. and Vadas, R. L. 1969. The effect of grazing by sea urchins, Strongylocentrotus spp. on benthic algal populations. Limnol. and Oceanogr. 14:710–719.Google Scholar
Patterson, C. 1964. A review of Mesozoic Acanthopterygian fishes with special reference to those of the English chalk. Phil. Trans R. Soc. London, ser. B. 247:213–482.Google Scholar
Pelseneer, P. 1906. A Treatise on Zoology. In: Lankester, E. R., ed. V. Mollusca. 352 pp. A. C. Black; London.Google Scholar
Philip, G. M. 1965. Classification of echinoids. J. Paleontol. 39:45–62.Google Scholar
Poignant, A.-F. 1977. The Mesozoic red algae: a general survey. Pp. 177–189. In: Flügel, E., ed. Fossil Algae. Springer-Verlag; New York.CrossRefGoogle Scholar
Pojeta, J. Jr. and Runnegar, B. 1976. The paleontology of rostroconch mollusks and the early history of the phylum Mollusca. Geol. Surv. Prof. Pap. 968:1–47.Google Scholar
Randall, J. E. 1967. Food habits of reef fishes of the West Indies. Stud. Trop. Oceanogr. (Miami). 5:655–847.Google Scholar
Raup, D. M. and Gould, S. J. 1974. Stochastic simulation and evolution of morphology towards a nomothetic paleontology. Syst. Zool. 23:305–322.Google Scholar
Runnegar, B., Pojeta, J. Jr., Taylor, M. E., and Collins, D. 1979. New species of the Cambrian and Ordovician chitons Matthevia and Chelodes from Wisconsin and Queensland: evidence for the early history of polyplacophoran mollusks. J. Paleontol. 53:1374–1394.Google Scholar
Schopf, T. J. M. 1974. Permo-Triassic extinctions: relation to sea floor spreading. J. Geol. 82:525–542.Google Scholar
Schopf, W., Haugh, B., Molnar, R., and Satterthwaith, D. 1973. On the development of metaphytes and metazoans. J. Paleontol. 47:1–9.Google Scholar
Sepkoski, J. J. Jr. 1981. A factor analytic description of the Phanerozoic marine fossil record. Paleobiology. 7:36–53.Google Scholar
Stanley, S. M. 1974. What has happened to the articulate brachiopods? Geol. Soc. Am. Abstr. with Programs. 6:966–967.Google Scholar
Stanley, S. M. 1977. Trends, rates and patterns of evolution in the Bivalvia. Pp. 209–250. In: Hallam, A., ed. Patterns of Evolution, as Illustrated by the Fossil Record. Amsterdam; Elsevier.Google Scholar
Steneck, R. S. 1982a. A limpet-coralline alga association: adaptations and defenses between a selective herbivore and its prey. Ecology. 63:502–522.Google Scholar
Steneck, R. S. 1982b. Adaptive trends in the ecology and evolution of crustose coralline algae (Rhodophyta, Corallinaceae). Ph.D. Dissertation. The Johns Hopkins Univ. 253 pp.Google Scholar
Steneck, R. S. 1982c. Adaptive trends in branching crustose coralline algae: patterns in space and time. Geol. Soc. Am. Abstr. with Programs Bull. 14:86.Google Scholar
Steneck, R. S. and Watling, L. 1982. Feeding capabilities and limitations of herbivorous molluscs: a functional group approach. Mar. Biol. 68:299–319.Google Scholar
Steneck, R. S. and Adey, W. H. 1976. The role of environment in control of morphology in Lithophyllum congestum, a Caribbean algal ridge builder. Bot. Mar. 19:197–215.Google Scholar
Stevenson, W. and Searles, R. B. 1960. Experimental studies on the ecology of intertidal environments at Heron Island. I. Exclusion of fish from beach rock. Aust. J. Mar. Freshwater Res. 11:241–267.Google Scholar
Taylor, P. D. 1981. Bryozoa of British Portland beds (Upper Jurassic). Paleontology. 24:863–875.Google Scholar
Tedman, R. A. 1980. Comparative study of the cranial morphology of the labrids Choerodon venustus, Labroides dimidiatus and the scarid Scarus fasciatus (Pisces: Perciformes). II. Cranial morphology and feeding mechanisms. Aust. J. Mar. Freshwater Res. 31:351–372.Google Scholar
Thayer, C. W. 1979. Biological bulldozers and the evolution of marine benthic communities. Science. 203:458–461.Google Scholar
Vadas, R. L. 1977. Preferential feeding: an optimization strategy in sea urchins. Ecol. Monogr. 47:337–371.Google Scholar
van den Hoek, C. 1969. Algal vegetation—types along the open coasts of Curaçao, Netherlands Antilles I. Proc. K. Ned. Akad. Wet. Ser. Biol. Med. Sci. C. 72:537–577.Google Scholar
Vermeij, G. J. 1977. The Mesozoic marine revolution: evidence from snails, predators and grazers. Paleobiology. 3:245–258.Google Scholar
Vine, P. J. 1974. Effects of algal grazing and aggressive behavior of the fishes Pomacentrus lividus and Acanthurus sohal on coral reef ecology. Mar. Biol. 24:131–136.Google Scholar
Voight, E. 1973. Environmental conditions of bryozoan ecology of the hardground biotope of the Maastrichtian Tuff-Chalk, near Maastrick (Netherlands). Pp. 185–197. In: Larwood, G. P., ed. Living and Fossil Bryozoa: Recent Advances in Research. Academic Press; London.Google Scholar
Voight, E. 1977. On grazing traces produced by the radula of fossil and recent gastropods and chitons. Pp. 335–347. In: Crimes, T. P. and Harper, J., eds. Trace Fossils 2. Seel. House Press.Google Scholar
Wanders, J. B.W. 1977. The role of benthic algae in the shallow reef of Curaçao (Netherlands Antilles) III: the significance of grazing. Aquat. Bot. 3:357–390.Google Scholar
Wetherbee, R. 1979. “Transfer Connections”: specialized pathways for nutrient translocation in a red alga? Science. 204:856–858.Google Scholar
Wilson, J. L. 1975. Carbonate facies in geologic history. Springer-Verlag; New York.CrossRefGoogle Scholar
Wray, J. L. 1964. Archaeolithophyllum, an abundant calcareous alga in limestones of the Lansing group (Pennsylvanian), Southeastern Kansas. State Geol. Surv. Kansas Bull. 170:1–13.Google Scholar
Wray, J. L. 1968. Late Paleozoic phylloid algal limestones in the United States. Pp. 113–119. In: Genesis and Classification of Sedimentary Rocks. XXIII Int. Geol. Congress. Vol. 8.Google Scholar
Wray, J. L. 1969. Algae in reefs through time. Proc. North Am. Paleontol. Conv. Pp. 1358–1373.Google Scholar
Wray, J. L. 1972. Environmental distribution of calcareous algae in upper Devonian reef complexes. Geol. Rundschau. 61:578–584.Google Scholar
Wray, J. L. 1977. Late Paleozoic calcareous red algae. Pp. 167–177. In: Flügel, E., ed. Fossil Algae. Springer-Verlag; New York.Google Scholar
Wray, J. L. and Playford, P. E. 1970. Some occurrences of Devonian reef-building algae in Alberta. Bull. Can. Petrol. Geol. 18:544–555.Google Scholar
Yochelson, E. L. 1978. An alternative approach to the interpretation of the phylogeny of ancient mollusks. Malacologia. 17:165–191.Google Scholar
Adey, W. H. 1970. A revision of the Foslie crustose coralline herbarium. Skrifter. 1:1–46.Google Scholar
Babic, L., Gusic, I., and Zupanic, J. 1976. Paleocene reef-limestone in the region of Banija, Central Croatia. Geol. Vjestn. (Zagreb). 29:11–47.Google Scholar
Basson, W. and Edgell, H. S. 1971. Calcareous algae from the Jurassic and Cretaceous of Lebanon. Micropaleontology 17:411–433.Google Scholar
Branch, G. M. and Branch, M. L. 1980. Competition between Cellana tramoserica (Sowerby) (Gastropoda) and Patiriella exigua (Lamarck) (Asteroidea), and their influence on algal standing stocks. J. Exp. Mar. Biol. Ecol. 48:35–49.Google Scholar
Day, J. 1967. Polychaeta of southern Africa. Pt. I, Errantia; Brit. Mus. Nat. Hist.Google Scholar
Edhorn, A. S. 1976. Early Cambrian algal croppers. Can. J. Earth Sci. 14:1014–1021.Google Scholar
Graham, A. 1955. Molluscan diets. Proc. Malacol. Soc. London. 33:144–159.Google Scholar
Hartman, O. 1968. Atlas of Errantiate Polychaetous Annelids from California. Allen Hancock Foundation; Los Angeles.Google Scholar
Ijima, W. 1969. Tertiary and Pleistocene algae from Mindoro, the Philippines. Contrib. Geol. and Paleontol. of S.E. Asia. 6:277–291.Google Scholar
Howell, B. F. 1969. Worms. Pp. 144–177. In: Moore, R. C, ed. Treatise on Invertebrate Paleontology. Geol. Soc. of Am. and Kansas Univ. Press; Boulder, Colo.Google Scholar
Johnson, J. H. 1956. Archaeolithophyllum, a new genus of Paleozoic coralline algae. J. Paleontol. 30:53–55.Google Scholar
Johnson, J. H. 1957. Geology of Saipan Mariana Islands. Paleontology. 280:1–246.Google Scholar
Johnson, J. H. 1962. The algal genus Lithothamnium and its fossil representatives. Q. Colorado School of Mines. 57:1–111.Google Scholar
Johnson, J. H. 1963. The algal genus Archaeolithothamnium and its fossil representatives. J. Paleontol. 37:175–211.Google Scholar
Johnson, J. H. 1964. Paleocene calcareous red algae from northern Iraq. Micropaleontology. 10:207–216.Google Scholar
Johnson, J. H. 1964. The Jurassic algae. Q. Colorado School of Mines. 59:1–129.Google Scholar
Johnson, J. H. 1965. Coralline algae from the Cretaceous and Early Tertiary of Greece. J. Paleontol. 39:802–814.Google Scholar
Johnson, J. H. 1968. Lower Cretaceous algae from Texas. Prof. Contrib. Colorado School of Mines. 4:1–71.Google Scholar
Johnson, J. H. 1969. A review of the lower Cretaceous algae. Prof. Contrib. Colorado School of Mines. 6:1–180.Google Scholar
Johnson, J. H. and Ferris, B. J. 1948. Eocene algae from Florida. J. Paleontol. 22:764–766.Google Scholar
Johnson, J. H. and Tafur, I. A. 1952. Coralline algae from the Eocene Atascadero limestone. J. Paleontol. 26:537–543.Google Scholar
Johnson, J. H. and Konishi, K. 1956. Studies of Mississippian algae. Q. Colorado School of Mines. 51:1–132.Google Scholar
Johnson, J. H. and Høeg, O. A. 1961. Studies of Ordovician algae. Q. Colorado School of Mines. 56:1–120.Google Scholar
Johnson, J. H. and Adey, W. H. 1965. Studies of Lithophyllum and related algal genera. Q. Colorado School of Mines. 60:1–105.Google Scholar
Jumars, P. and Fauchald, K. 1977. Between community contrasts in successful polychaete feeding strategies. In: Coull, B. C, ed. Ecology of Marine Benthos. Univ. S. Carolina.Google Scholar
Manton, S. M. 1969. Introduction to classification of Arthropoda. Pp. 3–14. In: Moore, R. C, ed. Treatise on Invertebrate Paleontology. Part R. Arthropoda 4. Vol. 1. Geol. Soc. Am. and Univ. Kansas Press; Boulder, Colo.Google Scholar
Nicotri, M. E. 1977. Grazing effects of four marine intertidal herbivores on the microflora. Ecology. 58:1020–1032.Google Scholar
Purchon, R. D. 1977. The Biology of the Mollusca. Pergammon Press; Oxford.Google Scholar
Sinclair, G. W. 1956. Solenopora canadensis (Foord) and other algae from the Ordovician of Canada. Trans. R. Soc. Can. 50:65–81.Google Scholar
Southward, A. J. 1964. Limpet grazing and the control of vegetation on rocky shores. Pp. 265–273. In: Crisp, D. J., ed. Grazing in Terrestrial and Marine Environments. Blackwell Scientific Publ.; Oxford.Google Scholar
Wanders, J. B. W. 1976. The role of benthic algae in the shallow reef of Curaçao (Netherlands Antilles) II: primary productivity of the Sargassum beds on the north-east coast submarine plateau. Aquat. Bot. 2:327–335.Google Scholar