Abstract
To measure amounts of tissue lost in natural populations of the burrowing amphiurid ophiuroid Microphiopholis gracillima (Stimpson), individuals were collected from subtidal mud flats in North Inlet, South Carolina, USA, at monthly intervals between February 1985–February 1987 and December 1989–November 1990. Between 20 and 70% of all individuals were regenerating the disc, and 85% of the 2045 arms examined had regeneration scars; >50% had one scar and some arms had up to 4 scars. Fewer individuals were regenerating discs in warmer months, but there was no seasonality in arm-loss frequency. To quantify rates of arm regeneration in the field, individuals which had 1, 2, or 3 arms removed were placed in mud-filled cores in the field in late July and November 1988 and in March and May 1989, and recovered after periods of about one month. Another set of cores was held in a running seawater laboratory during the May 1989 experiment. No regeneration occurred during the cooler times of year (November and March), and rates of regeneration were slower in May (total: 0.13 mg/d; tissue: 0.03 mg/d) than July (total: 0.17 mg/d; tissue: 0.05 mg/d). These rates indicate complete replacement of lost tissue in 100 to 120 d during the growth season. Within experiments, per arm regeneration rates were similar regardless of the number of arms removed. This finding is complicated by small sample size, high variability and low statistical power, but in general individuals which lost 2 or 3 arms regenerated proportionally more tissue than individuals which lost 1 arm. Individuals held in the laboratory regenerated the same amount of tissue but 30% less skeleton than individuals in the field. Sublethal tissue loss is common in this population, and M. gracillima is capable of regenerating at least 50% (each arm=17% of total body weight x 3) of its standing crop in a single growing season. Burrowing brittlestars probably constitute a significant renewable energy source for higher trophic levels in areas where they occur in dense populations.
Similar content being viewed by others
References
Alva, V., Jangoux, M. (1990). Frequence et causes presumées de la regeneration brachiale chez Amphipholis squamata (Echinodermata: Ophiuroidea). In: De Ridder, C., Dubois, Ph., Lahaye, M.-C., Jangoux, M. (eds.) Echinoderm research. Balkema, Rotterdam, p. 147–153
Aronson, R. B. (1989). Brittlestar beds: low-predation anachronisms in the British Isles. Ecology 70: 856–865
Aronson, R. B. (1991) Predation, physical disturbance, and sublethal arm damage in ophiuroids: a Jurassic-Recent comparison. Mar. Ecol. Prog. Ser. 74: 91–97
Aronson, R. B. (1992). The effects of geography and hurricane disturbance on a tropical predator-prey interaction. J. exp. mar. Biol. Ecol. 162: 15–34
Aronson, R. B. (1993). Hurricane effects on back-reef echinoderms of the Caribbean. Coral Reefs (in press)
Aronson, R. B., Sues, H.-D. (1987). The paleoecological significance of an anachronistic ophiuroid community. In: Kerfoot, W. C., Sih, A. (eds.) Predation: direct and indirect impacts on aquatic communities. University Press of New England, Hanover, New Hampshire, p. 355–366
Barnard, J. L., Ziesenhenne, F. C. (1961). Ophiuroid communities of southern California coastal bottoms. Pacif. nat. 2: 131–152
Bourgoin, A. (1987). Ecologie et demographie d'Acrocnida brachiata (Montagu) (Echinodermata: Ophiuroidea) en Baie de Douarnenez (Bretagne). Ph. D. dissertation. Université de Bretagne Occidentale, Brest
Bowmer, T., Keegan, B. F. (1983). Field survey of the occurrence and significance of regeneration in Amphiura filiformis (Echinodermata: Ophiuroidea) from Galway Bay, west coast of Ireland. Mar. Biol. 74: 65–71
Buchanan, J. B. (1964) A comparative study of some features of the biology of Amphiura filiformis and Amphiura chiajei (Ophiuroidea) considered in relation to their distribution. J. mar. biol. Ass. U.K. 44:565–576
Bureau, F., Dubois, Ph., Ghyoot M., Jangoux M. (1991). Skeleton resorption in echinoderms: regression of pedicellarial stalks in Sphaerechinus granularis (Echinoidea). Zoomorphology 110: 217–226
Clements, L. A. J. (1985). Post-autotomy feeding behavior of Microphiopholis gracillima (Stimpson): implications for regeneration. In: Keegan, B. F., O'Connor, B. D. S. (eds.) Echinodermata. Proceedings of the Fifth International Echinoderms Conference, Galway, Ireland. Balkema, Rotterdam, p. 609–615
Clements, L. A. J., Bell, S. S., Kurdziel J. P. (1993). Secondary production from arm regeneration by the infaunal brittlestar Ophiophragmus filograneus (Echinodermata: Ophiuroidea) in natural and replanted seagrass beds. (in preparation)
Clements, L. A. J., Stancyk, S. E. (1984). Particle selection by the burrowing brittlestar Micropholis gracillima (Stimpson) (Echinodermata: Ophiuroidea). J. exp. mar. Biol. Ecol. 84: 1–13
Dafni, J. (1985) Effect of mechanical stress on the calcification pattern in regular echinoid skeletal plates. In: Keegan, B. F., O'Connor, B. D. S. (eds.) Echinodermata. Proceedings of the Fifth International Echinoderms Conference, Galway, Ireland. Balkema, Rotterdam, p. 233–236
Dobson, W. E. (1988). Studies of the process, mechanism and limiting factors affecting tissue regeneration after autotomy in the ophiuroid echinoderm Microphiopholis gracillima. Ph. D. dissertation. University of South Carolina, Columbia, South Carolina
Dobson, W. E., Stancyk, S. E., Clements, L. A., Showman, R. M. (1991). Nutrient translocation during early disc regeneration in the brittlestar Microphiopholis gracillima (Stimpson) (Echinodermata: Ophiuroidea). Biol. Bull. mar. biol. Lab., Woods Hole 180: 167–184
Dobson, W. E., Turner, R. L. (1989). Morphology and histology of the disc autotomy plane in Ophiophragmus filograneus (Echinodermata, Ophiuroidea). Zoomorphology 108: 323–332
Donachy, J. E., Watabe, N. (1986). Effects of salinity and calcium concentration on arm regeneration by Ophiothrix angulata (Echinodermata: Ophiuroidea). Mar. Biol. 91: 253–257
Dubois, P., Chen, C. P. (1989). Calcification in echinoderms. In: Jangoux, M., Lawrence, J. M. (eds.) Echinoderm studies Vol. 3. Balkema, Rotterdam, p. 109–178
Duineveld, G. C. A., Van Noort, G. J. (1986). Observations on the population dynamics of Amphiura filiformis (Ophiuroidea: Echinodermata) in the southern North Sea and its exploitation by the dab, Limanda limanda. Neth. J. Sea Res. 20: 85–94
Ebert, T. A. (1967). Negative growth and longevity in the purple sea urchin Strongylocentrotus purpuratus (Stimpson). Science, N.Y. 157: 557–358
Emson, R. H. (1985). Bone idle-a recipe for success? In: Keegan, B. F., O'Connor, B. D. S. (eds.) Echinodermata. Proceedings of the Fifth International Echinoderms Conference, Galway, Ireland. Balkema, Rotterdam, p. 25–30
Feder, H. M., Pearson, T. H. (1988). The benthic ecology of Loch Linnhe and Loch Eil, a sea-loch system on the west coast of Scotland. V. Biology of the dominant soft-bottom epifauna and their interaction with the infauna. J. exp. mar. Biol. Ecol. 116: 99–134
Fielman, K. T., Stancyk, S. E., Dobson, W. E., Clements, L. A. J. (1991). Effects of disc and arm loss on regeneration by Microphiopholis gracillima (Echinodermata: Ophiuroidea) in nutrient-free seawater. Mar. Biol. 111: 121–127
Gardner, L. R., Michener, W. K., Blood, E. R., Williams, T. M., Lipscomb, D. J., Jefferson, W. H. (1991) Ecological impact of Hurricane Hugo-salinization of a coastal forest. J. cstl Res., Fort Laude dale (Spec. Iss.) 8: 301–317
Golde, H. M. (1991). Respiration rates of regenerating Microphiopholis gracillima (Echinodermata: Ophiuroidea). M. S. thesis. University of South Carolina, Columbia, South Carolina
Goss, R. (1969). Principles of regeneration. Academic Press, New York
Grehan, A. (1982). Aspects of the biology and ecology of Amphiura filiformis (O. F. Müller) (Echinodermata: Ophiuroidea). B-Sc. thesis. University College, Galway, Ireland
Healy, D. K. (1991). The effect of physical disturbance on settlement and recruitment of the American oyster, Crassostrea virginica (Gmelin). M. S. thesis. University of South Carolina, Columbia, South Carolina
Jangoux, M. (1982). Digestive systems: Ophiuroidea. In: Jangoux, M., Lawrence, J. M. (eds.) Echinoderm nutrition. A. A. Balkema, Rotterdam, p. 273–279
Kirkwood, T. B. L. (1981). Repair and its evolution: survival versus reproduction. In: Townsend, C. R., Calow, P. (eds.) Physiological ecology: an evolutionary approach to resource use. Sinauer Assoc. Inc., Sunderland, Massachusetts, p. 165–189
Kunitzer, A. (1989). Factors affecting the population dynamic of Amphiura filiformis (Echinodermata: Ophiuroidea) and Mysella bidentata (Bivalvia: Galeommatacea) in the North Sea. In: Ryland, J., Tyler, P. (eds.) Reproduction, genetics and distributions of marine organisms. Olsen & Olsen, Fredensbork, Denmark, p. 395–406
Lawrence, J. M. (1985). The energetic echinoderm. In: Keegan, B. F., O'Connor, B. D. S. (eds.) Echinodermata. Proceedings of the Fifth International Echinoderms Conference, Galway, Ireland. Balkema, Rotterdam, p. 47–68
Lawrence, J. M. (1990). The effect of stress and disturbance on echinoderms. Zool. Sci. 7: 17–28
Lawrence, J. M. (1991). The analysis of characteristics of echinoderms associated with stress and disturbance. In: Yanagisawa, T., Yasumasu, I., Oguro, C., Suzuki, N., Motokawa, T. (eds.) Biology of Echinodermata. A. A. Balkema, Rotterdam, p. 11–26
Lawrence, J. M., Ellwood, A. (1991). Simultaneous allocation of resources to arm regeneration and to somatic and gonadal production in Luidia clathrata (Say) (Echinodermata: Asteroidea). In: Yanagisawa, T., Yasumasu, I., Oguro, C., Suzuki, N., Motokawa, T. (eds.) Biology of Echinodermata. A. A. Balkema, Rotterdam, p. 543–548
Lawrence, J. M., Klinger, T. S., McClintock, J. B., Watts, S. A., Chen, C. P., Marsh, A., Smith, L. (1986). Allocation of nutrient resources to body components by regenerating Luidia clathrata (Say) (Echinodermata: Asteroidea). J. exp. mar. Biol. Ecol. 102: 47–53
Levitan, D. R. (1991). Skeletal changes in the test and jaws of the sea urchin Diadema antillarum in response to food limitation. Mar. Biol. 111: 431–435
Lonsdale, D. J., Coull, B. C. (1977). Composition and seasonality of zooplankton in North Inlet, South Carolina. Chesapeake Sci. 18: 272–283
Michener, W. K., Blood, E. R., Gardner, L. R., Kjerfve, B., Cablk, M. E., Coleman, C. H., Jefferson, W. H., Karinshak, D. A., Spoon, F. D. (1991). GIS assessment of large-scale ecological disturbances (Hurricane Hugo, 1989). In: GIS/LIS Proceedings. Volume 1. 28 October-1 November 1991, Atlanta, Georgia. American Society for Photogrammetry and Remote Sensing, Bethesda, Maryland, p. 343–355
Mladenov, P. V. (1983). Rate of arm regeneration and potential causes of arm loss in the feather star Florometra serratissima (Echinodermata: Crinoidea). Can. J. Zool. 61: 2873–2879
Morgulis, S. (1909). Regeneration in the brittle-star Ophiocoma pumila, with special reference to the influence of the nervous system. Proc. Am. Acad. Arts Sci. 44: 655–659
Muus, K. (1981). Density and growth of juvenile Amphiura filiformis (Ophiuroidea) in the Oresund. Ophelia 20: 153–168
O'Connor, B., Bowmer, T., Grehan, A. (1983). Long-term assessment of the population dynamics of Amphiura filiformis (Echinodermata: Ophiuroidea) in Galway Bay (west coast of Ireland). Mar. Biol. 75: 279–286
O'Connor, B., Bowmer, T., McGrath, D., Raine, R. (1986). Energy flow through an Amphiura filiformis (Ophiuroidea: Echinodermata) population in Galway Bay, west coast of Ireland: A preliminary investigation. Ophelia 26: 351–357
O'Connor, B. D. S., McGrath, D. (1980). The population dynamics of Amphiura filiformis (O. F. Müller) in Galway Bay, west coast of Ireland. In: Jangoux, M. (ed.) Echinoderms: present and past. A. A. Balkema, Rotterdam, p. 219–222
Ogburn, M. V., Allen, D. M., Michener, W. K. (1988). Fishes, shrimps, and crabs of the North Inlet Estuary, SC: a four-year seine and trawl survey. Baruch Inst. tech. Rep. 88–1; 1–299 (University of South Carolina, Columbia)
Pearson, T. H., Josefson, A. B., Rosenberg, R. (1985). Petersen's benthic stations revisited. I. Is the Kattegat becoming eutrophic? J. exp. mar. Biol. Ecol. 92: 157–206
Petersen, C. G. J. (1913). Havets Bonitering. II. Om Havbundens Dyresamfund i Skagerak, Kristianiafjord og de danske Farvande. Beretn. Minist. Landbr. Fisk. dan. biol. stn 23: 5–26
Peterson, C. H., Quammen, M. L. (1982). Siphon nipping: its importance to small fishes and its impact on growth of the bivalve Protothaca staminea (Conrad). J. exp. mar. Biol. Ecol. 63: 249–268
Reichman, O. J. (1984). Evolution of regeneration capabilities. Am. Nat. 123: 752–763
Rosenberg, R., Gray, J. S., Josefson, A. B., Pearson, T. H. (1986). Petersen's benthic stations revisited. II. Is the Oslofjord and eastern Skagerrak enriched? J. exp. mar. Biol. Ecol. 105: 219–252
Salzwedel, H. (1974). Arm-regeneration bei Amphiura filiformis (Ophiuroidea). Veröff. Inst. Meeresforsch. Bremerh. 14: 161–167
SAS Institute Inc. (1988). SAS/STAT user's guide. Release 6.03 edn. SAS Institute Inc., Cary, North Carolina
Sellner, K. G., Zingmark, R. G., Miller, T. G. (1976). Interpretations of the 14C method of measuring the total annual production of phytoplankton in a South Carolina estuary. Botanica mar. 19: 119–125
Shuford, R. (1992). Spatial and temporal variability in abundance of the polychaete worm, Streblospio benedicti Webster, 1879. M.S. thesis. University of South Carolina, Columbia, South Carolina
Singletary, R. L. (1980). The biology and ecology of Amphioplus coniortodes, Ophionephthys limicola and Micropholis gracillima (Ophiuroidea: Amphiuridae). Caribb. J. Sci. 16: 39–55
Stancyk, S. E. (1974). Life history patterns of three estuarine ophiuroids at Cedar Key, Florida. Ph. D. dissertation. University of Florida, Gainesville, Florida
Steimle, F. W. (1990). Benthic macrofauna and habitat monitoring on the continental shelf of the northeastern United States. I. Biomass. NOAA natn. mar. Fish. Serv. tech. Rep. Circ. 86: 1–28
Thomas, L. P. (1966). A revision of the tropical American species of Amphipholis (Echinodermata: Ophiuroidea). Bull. mar. Sci. 16: 827–833
Thorson, G. (1957). Bottom communities. In: Hedgepeth, J. (ed.) Treatise on marine ecology and paleoecology. Vol. 1. Ecology. Geological Society of America, Washington, p. 461–534 (Mem. geol. Soc. Am. No. 67)
Trevallion, A. (1971). Studies on Tellina tenuis da Costa. III. Aspects of general biology and energy flow. J. exp. mar. Biol. Ecol. 7: 95–122
Turner, R. L. (1985). Microphiopholis, replacement name for Micropholis Thomas, 1966 (Ophiuroidea: Amphiuridae), non Huxley, 1859 (Amphibia: Dissorophidae). Proc. biol. Soc. Wash. 98: 1028–1029
Turner, R. L., Heatwole, D. G., Stancyk, S. E. (1982). Ophiuroid discs in stingray stomachs: evasive autotomy or partial consumption of prey? In: Lawrence, J. M. (ed.) Echinoderms. Proceedings of the International Conference, Tampa Bay. A. A. Balkema, Rotterdam, p. 331–335
Ursin, E. (1960). A quantitative investigation of the echinoderm fauna of the North Sea. Meddr Kommn Fisk.-og Havunders. (N.S.) 2: 1–204
Valentine, J. F. (1991). Temporal variation in populations of the brittlestars Hemipholis elongata (Say, 1825) and Microphiopholis atra (Stimpson, 1852) (Echinodermata: Ophiuroidea) in eastern Mississippi Sound. Bull. mar. Sci. 48: 597–605
Vermeij, G. J. (1978). Biogeography and adaptation: patterns of marine life. Harvard University Press, Cambridge, Mass.
Vlas, J. de. (1979a). Annual food intake by plaice and flounders in a tidal flat area in the Dutch Wadden Sea, with special reference to consumption of regenerating parts of macrobenthic prey. Neth. J. Sea Res. 13: 117–153
Vlas, J. de. (1979b). Secondary production by tail regeneration in a tidal flat population of lugworms (Arenicola morina), cropped by flatfish. Neth. J. Sea Res. 13: 362–393
Vlas, J. de. (1985). Secondary production by siphon regeneration in a tidal flat population of Macoma balthica. Neth. J. Sea Res. 19: 147–164
Warwick, R. M., Ruswahyuni (1987). Comparative study of the structure of some tropical and temperate marine soft-bottom macrobenthic communities. Mar. Biol. 95: 641–649
Wassenberg, T. J., Hill, B. J. (1987). Natural diet of the tiger prawns Penaeus esculentus and P. semisulcatus. Aust. J. mar. Freshwat. Res. 38: 169–182
Woodin, S. A. (1984). Effects of browsing predators: activity changes in infauna following tissue ioss. Biol. Bull. mar. biol. Lab., Woods Hole 166: 558–573
Woodley, J. D. (1975). The behavior of some amphiurid brittlestars. J. exp. mar. Biol. Ecol. 18: 29–46
Zajac, R. N. (1985). The effects of sublethal predation on reproduction in the spionid polychaete Polydora ligni Webster. J. exp. mar. Biol. Ecol. 88: 1–19
Zeleny, C. (1903). A study of the rate of regeneration of the arms in the brittle-star, Ophioglypha lacertosa. Biol. Bull. mar. biol. Lab., Woods Hole 6: 12–17
Zwarts, L., Wanink, J. (1989). Siphon size and burying depth in deposit-and suspension-feeding benthic bivalves. Mar. Biol. 100: 227–400
Author information
Authors and Affiliations
Additional information
Communicated by N. H. Marcus, Tallahassee
Rights and permissions
About this article
Cite this article
Stancyk, S.E., Golde, H.M., Pape-Lindstrom, P.A. et al. Born to lose. I. Measures of tissue loss and regeneration by the brittlestar Microphiopholis gracillima (Echinodermata: Ophiuroidea). Marine Biology 118, 451–462 (1994). https://doi.org/10.1007/BF00350302
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00350302