Skip to main content

Advertisement

Log in

Effects of sea urchin disease on coastal marine ecosystems

  • Review, Concept, and Synthesis
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Outbreaks of disease in herbivorous sea urchins have led to ecosystem phase shifts from urchin barrens to kelp beds (forests) on temperate rocky reefs, and from coral to macroalgal-dominated reefs in the tropics. We analyzed temporal patterns in epizootics that cause mass mortality of sea urchins, and consequent phase shifts, based on published records over a 42-year period (1970–2012). We found no evidence for a general increase in disease outbreaks among seven species of ecologically important and intensively studied sea urchins. Periodic waves of recurrent amoebic disease of Strongylocentrotus droebachiensis in Nova Scotia coincide with periods when the system was in a barrens state and appear to have increased in frequency. In contrast, following a major epizootic that decimated Diadema antillarum throughout the Caribbean in 1983, subsequent outbreaks of disease were highly localized and none have been reported since 1991. Epizootics of Strongylocentrotus in the NW Atlantic and NE Pacific, and Paracentrotus and Diadema in the eastern Atlantic, have been linked to climate change and overfishing of sea urchin predators. The spatial extent of recurrent disease outbreaks in these species, and the frequency of phase shifts associated with these epizootics, has decreased over time due to the expansion of the macroalgal state and its stabilization through positive feedback mechanisms. Longitudinal studies to monitor disease outbreaks in sea urchin populations and improved techniques to identify causative agents are needed to assess changes in the frequency and extent of epizootics, which can profoundly affect the structure and functioning of coastal marine ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agatsuma Y (2013) Ecology of Strongylocentrotus intermedius. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 437–448

    Google Scholar 

  • Alves FMA, Chícharo LM, Serrão E, Abreu AD (2001) Algal cover and sea urchin spatial distribution at Maderia Island (NE Atlantic). Sci Mar 65:383–392

    Google Scholar 

  • Alves FMA, Chícharo LM, Serrão E, Abreu AD (2003) Grazing by Diadema antillarum (Philippi) upon algal communities on rocky substrate. Sci Mar 67:307–311

    Google Scholar 

  • Aronson RB, Precht WF (2001a) Evolutionary paleoecology of Caribbean coral reefs. In: Allmon WD, Bottjer DL (eds) Evolutionary paleoecology: the ecological context of macro-evolutionary change. Columbia University Press, New York, pp 171–233

    Google Scholar 

  • Aronson RB, Precht WF (2001b) White-band disease and the changing face of Caribbean coral reefs. Hydrobiologia 460:25–38

    Google Scholar 

  • Aronson RB, Precht WF (2006) Conservation, precaution, and Caribbean reefs. Coral Reefs 25:441–450

    Google Scholar 

  • Azzolina JF (1987) Evolution à long terme des populations de l’oursin comestible Paracentrotus lividus dans la baie de Port-Cros (Var, France). In: Colloque international sur Paracentrotus lividus et les oursins comestibles. GIS Posidonie Publ., Marseille, pp 257–269

  • Bally M, Garrabou J (2007) Thermodependent bacterial pathogens and mass mortalities in temperate benthic communities: a new case of emerging disease linked to climate change. Glob Change Biol 13:2078–2088

    Google Scholar 

  • Bates AE, Hilton BJ, Harley CDG (2009) Effects of temperature, season and locality on wasting disease in the keystone predatory sea star Pisaster ochraceus. Dis Aquat Org 86:245–251

    Google Scholar 

  • Becker PT, Egea E, Eeckhaut I (2008) Characterization of the bacterial communities associated with the bald sea urchin disease of the echinoid Paracentrotus lividus. J Invert Pathol 98:136–147

    CAS  Google Scholar 

  • Benítez-Villalobos F, Domínguez y Gómez MT, López Pérez RA (2008) Changes in population densities of Diadema mexicanum at Bahias de Huatulco, Western Mexico. Rev Biol Trop 56:255–263

    Google Scholar 

  • Benítez-Villalobos F, Díaz Martinez JP, Martínez-García M (2009) Mass mortality of the sea urchin Diadema mexicanum in La Entrega at Bahias de Huatulco, Western Mexico. Coral Reefs 28:1017

    Google Scholar 

  • Boudouresque CF, Verlaque M (2013) Paracentrotus lividus. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 297–328

    Google Scholar 

  • Boudouresque CF, Nedelec H, Shepherd SA (1980) The decline of a population of the sea urchin Paracentrotus lividus in the Bay of Port-Cros (Var, France). Travaux Scientifique du Parc National de Port-Cros 6:243–251

    Google Scholar 

  • Brady SM, Scheibling RE (2005) Repopulation of the shallow subtidal zone by green sea urchins (Strongylocentrotus droebachiensis) following mass mortality in Nova Scotia, Canada. J Mar Biol Ass UK 85:1511–1517

    Google Scholar 

  • Burge CA, Eakin CM, Friedman CS, Froelich B, Hershberger PK, Hofmann EE, Petes LF, Prager KC, Weil E, Willis BL, Ford SE, Harvell CD (2014) Climate change influences on marine infectious diseases: implications for management and society. Annu Rev Mar Sci 6:249–277

    Google Scholar 

  • Byrne M, Andrew NL (2013) Centrostephanus rodgersii. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 243–256

    Google Scholar 

  • Caraguel CGB, O’Kelly CJ, Legendre P, Frasca S Jr, Gast RJ, Després BM, Cawthorn RJ, Greenwood SJ (2007) Microheterogeneity and coevolution: an examination of rDNA sequence characteristics in Neoparamoeba pemaquidensis and its prokinetoplastid endosymbiont. J Eukaryot Microbiol 54:418–426

    CAS  Google Scholar 

  • Carpenter RC (1990) Mass mortality of Diadema antillarum I. Long-term effects on sea urchin population-dynamics and coral reef algal communities. Mar Biol 104:67–77

    Google Scholar 

  • Carpenter RC, Edmunds PJ (2006) Local and regional scale recovery of Diadema promotes recruitment of scleractinian corals. Ecol Lett 9:271–280

    Google Scholar 

  • Chiappone M, Rutten LM, Miller SL, Swanson DW (2013) Recent trends (1999–2011) in population density and size of the echinoid Diadema antillarum in the Florida keys. Fla Sci 76:23–35

    Google Scholar 

  • Christie H, Leinaas HP, Skadsheim A (1995) Local patterns in mortality of the green sea urchin, Strongylocentrotus droebachiensis, at the Norwegian coast. In: Skjoldal HR, Hopkins C, Erikstad KE, Leinaas HP (eds) Ecology of fjords and coastal waters. Elsevier, Amsterdam, pp 573–584

    Google Scholar 

  • Clemente S, Hernández JC, Rodríguez A, Brito A (2010) Identifying keystone predators and the importance of preserving functional diversity in sublittoral rocky-bottom areas. Mar Ecol Prog Ser 413:55–67

    Google Scholar 

  • Dayton PK, Tegner MJ, Parnell PE, Edwards PB (1992) Temporal and spatial patterns of disturbance and recovery in a kelp forest community. Ecol Monogr 62:421–445

    Google Scholar 

  • Duggins DO (1980) Kelp beds and sea otters: an experimental approach. Ecology 61:447–453

    Google Scholar 

  • Dyková I, Lorenzo-Morales J, Kostka M, Valladares B, Pecková H (2011) Neoparamoeba branchiphila infections in moribund sea urchins Diadema aff. antillarum in Tenerife, Canary Islands, Spain. Dis Aquat Org 95:225–231

    Google Scholar 

  • Eckert GL, John ME, Kushner DJ (2000) Sea star disease and population declines at the Channel Islands. Proceedings of the fifth California Islands symposium. US Minerals Management Service

  • Edmunds PJ, Carpenter RC (2001) Recovery of Diadema antillarum reduces macroalgal cover and increases abundance of juvenile corals on a Caribbean reef. Proc Natl Acad Sci USA 98:5067–5071

    CAS  Google Scholar 

  • Edwards HJ, Elliott IA, Eakin C, Irikawa A, Madin JS, McField M, Morgan JA, van Woesik R, Mumby PJ (2011) How much time can herbivore protection buy for coral reefs under realistic regimes of hurricanes and coral bleaching? Glob Change Biol 17:2033–2048

    Google Scholar 

  • Estes JA, Peterson CH, Steneck RS (2010) Some effects of apex predators in higher-latitude coastal oceans. In: Terborgh J, Estes JA (eds) Trophic cascades: predators, prey, and the changing dynamics of nature. Island Press, Washington, pp 37–53

    Google Scholar 

  • Fagerli CW, Norderhaug KM, Christie HC (2013) Lack of sea urchin settlement may explain kelp forest recovery in overgrazed areas in Norway. Mar Ecol Prog Ser 488:119–132

    Google Scholar 

  • Fagerli CW, Norderhaug KM, Christie H, Pedersen MF, Fredriksen S (2014) Predators of the destructive sea urchin Strongylocentrotus droebachiensis on the Norwegian coast. Mar Ecol Prog Ser 502:207–218

    Google Scholar 

  • Feehan CJ, Scheibling RE (2014) Disease as a control of sea urchin populations in Nova Scotian kelp beds. Mar Ecol Prog Ser 500:149–158

    Google Scholar 

  • Feehan C, Scheibling RE, Lauzon-Guay JS (2012) An outbreak of sea urchin disease associated with a recent hurricane: support for the ‘killer storm hypothesis’ on a local scale. J Exp Mar Biol Ecol 413:159–168

    Google Scholar 

  • Feehan CJ, Johnson-Mackinnon J, Scheibling RE, Lauzon-Guay JS, Simpson AG (2013) Validating the identity of Paramoeba invadens, the causative agent of recurrent mass mortality of sea urchins in Nova Scotia, Canada. Dis Aquat Organ 103:209–227

    Google Scholar 

  • Filbee-Dexter K, Scheibling RE (2014) Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar Ecol Prog Ser 495:1–25

    Google Scholar 

  • Forcucci D (1994) Population density, recruitment and 1991 mortality event of Diadema antillarum in the Florida keys. Bull Mar Sci 54:917–928

    Google Scholar 

  • Ford SE, Smolowitz R (2007) Infection dynamics of an oyster parasite in its newly expanded range. Mar Biol 151:119–133

    Google Scholar 

  • Fung T, Seymour RM, Johnson CR (2011) Alternative stable states and phase shifts in coral reefs under anthropogenic stress. Ecology 92:967–982

    Google Scholar 

  • Gagnon P, Himmelman JH, Johnson LE (2004) Temporal variation in community interfaces: kelp-bed boundary dynamics adjacent to persistent urchin barrens. Mar Biol 144:1191–1203

    Google Scholar 

  • Gilles KW, Pearse JS (1986) Disease in sea urchin Strongylocentrotus purpuratus: experimental infection and bacterial virulence. Dis Aquat Org 1:105–114

    Google Scholar 

  • Girard D, Clemente S, Toledo-Guedes K, Brito A, Hernández JC (2012) A mass mortality of subtropical intertidal populations of the sea urchin Paracentrotus lividus: analysis of potential links with environmental conditions. Mar Ecol 33:377–385

    Google Scholar 

  • Granéli E, Ferreira CEL, Yasumoto T, Rodrigues EM, Neves B (2002) Sea urchins poisoning by the benthic dinoflagellate Ostreopsis ovata on the Brazilian Coast. In: Steidinger KA (ed) Xth Int Conf on Harmful Algae, St. Pete Beach, Florida, p 113, Book of Abstracts

  • Hagen NT (1987) Sea urchin outbreaks and nematode epizootics in Vestfjorden, northern Norway. Sarsia 72:213–229

    Google Scholar 

  • Hagen NT (1992) Macroparasitic epizootic disease: a potential mechanism for the termination of sea urchin outbreaks in Northern Norway? Mar Biol 114:469–478

    Google Scholar 

  • Hagen NT (1996) Parasitic castration of the green echinoid Strongylocentrotus droebachiensis by the nematode endoparasite Echinomermella matsi: reduced reproductive potential and reproductive death. Dis Aquat Org 24:215–226

    Google Scholar 

  • Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstein PR, Grimes DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM, Porter JW, Smith GW, Vasta GR (1999) Emerging marine diseases–climate links and anthropogenic factors. Science 285:1505–1510

    CAS  Google Scholar 

  • Harvell CD, Mitchell CE, Ward JR, Altizer S, Dobson AP, Ostfeld RS, Samuel MD (2002) Climate warming and disease risks for terrestrial and marine biota. Science 296:2158–2162

    CAS  Google Scholar 

  • Harvell D, Jordan-Dahlgren E, Merkel S, Rosenberg E, Raymundo L, Smith G, Weil E, Willis B (2007) Coral disease, environmental drivers, and the balance between coral and microbial associates. Oceanography 20:172–195

    Google Scholar 

  • Hereu B, Linares C, Sala E, Garrabou J, Garcia-Rubies A, Diaz D, Zabala M (2012) Multiple processes regulate long-term population dynamics of sea urchins on Mediterranean rocky reefs. PLoS ONE 7:E36901

    CAS  Google Scholar 

  • Hernández JC, Sangil C, Clemente S (2013) Sea urchins, natural events and benthic ecosystem functioning in the Canary Islands. In: Fernández-Palocios JM, Nascimiento LD, Hernández JC, Clemente S, González A, Diaz-González JP (eds) Climate change: perspectives from the Atlantic: past, present and future. Servicio de Publicaciones de la Universidad de La Laguna, Tenerife, pp 487–512

    Google Scholar 

  • Hobaus E, Fenaux L, Hignette M (1981) Premières observations sur les lèsions provoquèes par une maladie affectant le test des oursins en Mèditerrannèe occidentale. Rapp Comm Int Mer Medit 27:221–222

    Google Scholar 

  • Hughes TP (1989) Community structure and diversity of coral reefs: the role of history. Ecology 70:275–279

    Google Scholar 

  • Hughes TP (1994) Catastrophes, phase shifts, and large-scale degradation of a Caribbean coral reef. Science 265:1547–1551

    CAS  Google Scholar 

  • Hughes TP, Reed DC, Boyle MJ (1987) Herbivory on coral reefs: community structure following mass mortalities of sea urchins. J Exp Mar Biol Ecol 113:39–59

    Google Scholar 

  • Hughes TP, Graham NA, Jackson JB, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642

    Google Scholar 

  • Jackson JB, Kirby MX, Berger WH, Bjorndal KA, Botsford LW, Bourque BJ, Bradbury R, Cooke R, Erlandson J, Estes JA, Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM, Peterson CH, Steneck RS, Tegner MJ, Warner R (2001) Historical overfishing and the recent collapse of coastal ecosystems. Science 293:629–638

    CAS  Google Scholar 

  • Johnson PT (1971) Studies on diseased urchins from Point Loma. Kelp Habitat Improvement Project, Annual Report, 1970–1971, pp 82–90, Calif Inst Technol, Pasadena

  • Jones GM (1985) Paramoeba invadens n. sp. (Amoebidae, Paramoebidae) a pathogenic amoeba from the sea urchin, Strongylocentrotus droebachiensis, in eastern Canada. J Protozool 32:346–369

    Google Scholar 

  • Jones GM, Hagen NT (1987) Echinomermella matsi sp. n., an endoparasitic nematode from the sea urchin Strongylocentrotus droebachiensis in northern Norway. Sarsia 72:203–212

    Google Scholar 

  • Keats DW, South GR, Steele DH (1991) The effects of an experimental reduction in grazing by green sea urchins on a benthic macroalgal community in eastern Newfoundland. Mar Ecol Prog Ser 68:181–193

    Google Scholar 

  • Keesing JK (2013) Heliocidaris erythrogramma. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 369–380

    Google Scholar 

  • Kushner DR, Walder L, Gorodezky D, Lerma Richards DV (1995a) Kelp Forest Monitoring, 1993 Annual Report. Technical Report CHIS-95-02

  • Kushner DJ, Lerma DL, Richards DV (1995b) Kelp Forest Monitoring, 1994 Annual Report. Technical Report CHIS-95-03

  • Kushner DJ, Lerma D, Mondrgon J, Morgan J (1997a) Kelp forest monitoring, 1995 annual report. Technical Report-CHIS-97-01

  • Kushner DJ, Morgan J, Mondragon J, Lerma D (1997b) Kelp forest monitoring, 1996 annual report. Technical Report-CHIS-97-04

  • Kushner DJ, Morgan J, Mondragon J, Lerma D (1998) Kelp forest monitoring, 1997 annual report. Technical Report-CHIS-98-05

  • Kushner DJ, Lerma D, Alesandrini S, Shaffer J (2000) Kelp forest monitoring, 1998 annual report. Technical Report-CHIS-99-01

  • Kushner DJ, Lerma D, Shaffer J, Hajduczek B (2001a) Kelp forest monitoring, 1999 annual report. Technical Report-CHIS-01-05

  • Kushner DJ, Lerma D, Donahue M (2001b) Kelp forest monitoring, 2000 annual report. Technical Report-CHIS-01-07

  • Kushner DJ, Lerma D, Ugoretz K (2004) Kelp forest monitoring, 2001 annual report. Technical Report-CHIS-03-02

  • Kushner DJ, Lerma D, Rich P (2007a) Kelp forest monitoring, 2002 annual report. Technical Report-CHIS-07-01

  • Kushner DJ, Lerma D, Rich P (2007b) Kelp forest monitoring, 2003 annual report. Technical Report-CHIS-07-02

  • Kushner DJ, Moss M, Sprague JL, Moore KJ (2012) Channel Islands National Park kelp forest monitoring program: Annual report 2005. Natural Resource Data Series NPS/MEDN/NRDS—2012/376. National Park Service, Fort Collins, Colorado

  • Kushner DJ, Moss M, Sprague JL, Moore KJ (2013a) Kelp forest monitoring: annual report 2006. Natural Resource Data Series NPS/CHIS/NRDS—2013/478. National Park Service, Fort Collins, Colorado

  • Kushner DJ, Moore KJ, Mooney EA, Ibarra S, Grunden JR, Metzger JR (2013b) Channel Islands National Park Kelp Forest Monitoring Program: Annual report 2009. Natural Resource Data Series NPS/CHIS/NRDS—2013/581. National Park Service, Fort Collins, Colorado

  • Kushner DJ, Rassweiler A, McLaughlin JP, Lafferty KD (2013c) A multi-decade time series of kelp forest community structure at the California Channel Islands. Ecology 94:2655

    Google Scholar 

  • Lafferty KD (2004) Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol Appl 14:1566–1573

    Google Scholar 

  • Lafferty KD, Porter JW, Ford SE (2004) Are diseases increasing in the ocean? Annu Rev Ecol Evol Syst 35:31–54

    Google Scholar 

  • Lessios HA (1988a) Mass mortality of Diadema antillarum in the Caribbean: what have we learned? Ann Rev Ecol Syst 19:371–393

    Google Scholar 

  • Lessios HA (1988b) Population dynamics of Diadema antillarum (Echinodermata: Echinoidea) following mass mortality in Panama. Mar Biol 99:515–526

    Google Scholar 

  • Lessios HA (2005) Diadema antillarum populations in Panama twenty years following mass mortality. Coral Reefs 24:125–127

    Google Scholar 

  • Lessios HA, Robertson DR, Cubit JD (1984) Spread of Diadema mass mortality through the Caribbean. Science 226:335–337

    CAS  Google Scholar 

  • Lester SE, Tobin ED, Behrens MD (2007) Disease dynamics and the potential role of thermal stress in the sea urchin, Strongylocentrotus purpuratus. Can J Fish Aquat Sci 64:314–323

    Google Scholar 

  • Levitan DR (1988) Algal-urchin biomass responses following mass mortality of Diadema antillarum Philippi at Saint John, U.S. Virgin Islands. J Exp Mar Biol Ecol 119:167–178

    Google Scholar 

  • Liddel WD, Ohlhorst SL (1986) Changes in benthic community composition following the mass mortality of Diadema at Jamaica. J Exp Mar Biol Ecol 95:271–278

    Google Scholar 

  • Lyons DA, Scheibling RE (2008) Context-dependant survival of the invasive seaweed Codium fragile ssp. tomentosoides in kelp beds and urchin barrens off Nova Scotia. Aquat Biol 2:17–27

    Google Scholar 

  • Maes P, Jangoux M (1984) The bald sea urchin disease: a biopathological approach. Helgol Meeresunters 37:217–222

    Google Scholar 

  • Mann KH (1982) Ecology of coastal waters: a systems approach. In: Pitelka FA, Anderson DJ, Greig-Smith P (eds) Studies in ecology. University of California Press, Berkeley, pp 1–322

    Google Scholar 

  • Maynard JA, Anthony KRN, Harvell CD, Burgman MA, Beeden R, Sweatman H, Heron SF, Lamb JB, Willis BL (2011) Predicting outbreaks of a climate-driven coral disease in the Great Barrier Reef. Coral Reefs 30:485–495

    Google Scholar 

  • Miller RJ (1985) Succession in sea urchin and seaweed abundance in Nova Scotia, Canada. Mar Biol 84:275–286

    Google Scholar 

  • Miller RJ, Colodey AG (1983) Widespread mass mortalities of the green sea urchin in Nova Scotia, Canada. Mar Biol 73:263–267

    Google Scholar 

  • Miller RJ, Nolan SC (2000) Management of the Nova Scotia sea urchin fishery: a nearly successful habitat based management regime. Fisheries and Oceans Science, Canadian Stock Assessment Secretariat, Ottawa

  • Miner CM, Altstatt JM, Raimondi PT, Minchinton TE (2006) Recruitment failure and shifts in community structure following mass mortality limit recovery prospects of black abalone. Mar Ecol Prog Ser 327:107–117

    Google Scholar 

  • Moore KJ, Kushner DJ, Sprague JL, Moss M (2013) Channel Islands National Park Kelp Forest Monitoring Program: annual report 2007. Natural Resource Data Series NPS/MEDN/NRDS—2013/547. National Park Service, Fort Collins, Colorado

  • Muelhstein L (1989) Perspectives on the wasting disease of eelgrass Zostera marina. Dis Aquat Org 7:211–221

    Google Scholar 

  • Mullen TE, Russell S, Tucker MT, Maratea JL et al (2004) Paramoebiasis associated with mass mortality of American lobster Homarus americanus in Long Island Sound, USA. J Aquat Anim Health 16:29–38

    Google Scholar 

  • Mumby PJ, Hastings A, Edwards HJ (2007) Thresholds and the resilience of Caribbean coral reefs. Nature 450:98–101

    CAS  Google Scholar 

  • Muthiga NA, McClanahan TR (2013) Diadema. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 257–274

    Google Scholar 

  • Norderhaug KM, Christie HC (2009) Sea urchin grazing and kelp re-vegetation in the NE Atlantic. Mar Biol Res 5:515–528

    Google Scholar 

  • North WJ, Pearse JS (1970) Sea urchin population explosion in southern California coastal waters. Science 167:209

    CAS  Google Scholar 

  • Nugues MM, Bak RPM (2008) Long-term dynamics of the brown macroalga Lobophora variegata on deep reefs in Curacao. Coral Reefs 27:389–393

    Google Scholar 

  • Ostrander GK, Armstrong KM, Knobbe ET, Gerace D, Scully EP (2000) Rapid transition in the structure of a coral reef community: the effects of coral bleaching and physical disturbance. Proc Natl Acad Sci USA 97:5297–5302

    CAS  Google Scholar 

  • Pearse JS, Hines AH (1979) Expansion of a central California kelp forest following the mass mortality of sea urchins. Mar Biol 51:83–91

    Google Scholar 

  • Pearse JS, Costa DP, Yellin MB, Agegian CR (1977) Localized mass mortality of red sea urchin, Strongylocentrotus franciscanus, near Santa Cruz, California. Fish Bull US 53:645–648

    Google Scholar 

  • Richards DV, Kushner D (1994) Kelp Forest Monitoring, 1992 annual report. Channel Islands National Park, Ventura, California. Technical Report-CHIS-94-01

  • Robblee MB, Barber TR, Carlson PR Jr, Durako MJ, Fourqurean JW, Muehlstein LK, Porter D, Yarbro LA, Zieman RT, Zieman JC (1991) Mass mortality of the tropical seagrass Thalassia testudium in Florida Bay (USA). Mar Ecol Prog Ser 71:297–299

    Google Scholar 

  • Rodríguez M, Barquín J, Pérez-Dionis G (2001) Eulimid gastropods (Caenogastropoda: Eulimidae) of the Canary Islands. Part I. Species parasiting sea urchins. Iberus 19:7–24

    Google Scholar 

  • Rodríguez A, Hernández JC, Clemente S, Coppard SE (2013) A new species of Diadema (Echinodermata: Echinodea: Diadematidae) from the eastern Atlantic Ocean and a neotype designation of Diadema antillarum (Philippi, 1984). Zootaxa 3636:144–170

    Google Scholar 

  • Rogers-Bennett L (2013) Strongylocentrotus franciscanus and Strongylocentrotus purpuratus. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 413–436

    Google Scholar 

  • Ross PS (2002) The role of immunotoxic environmental contaminants in facilitating the emergence of infectious disease in marine mammals. Hum Ecol Risk Assess 8:277–292

    Google Scholar 

  • Sala E, Boudouresque CF, Harmelin-Vivien M (1998) Fishing, trophic cascades and the structure of algal assemblages; evaluation of an old but untested paradigm. Oikos 82:425–439

    Google Scholar 

  • Sammarco PW (1982) Effects of grazing by Diadema antillarum Philippi (Echinodermata: Echinoidea) on algal diversity and community structure. J Exp Mar Biol Ecol 65:83–105

    Google Scholar 

  • Sangil C, Clemente S, Martín-García L, Hernández JC (2012) No-take areas as an effective tool to restore urchin barrens on subtropical rocky reefs. Est Coast Shelf Sci 112:207–215

    Google Scholar 

  • Scheibling RE (1984) Echinoids, epizootics and ecological stability in the rocky subtidal off Nova Scotia, Canada. Helgol Meeresunters 37:233–242

    Google Scholar 

  • Scheibling RE (1986) Increased macroalgal abundance following mass mortalities of sea urchins (Strongylocentrotus droebachiensis) along the Atlantic coast of Nova Scotia. Oecol 68:186–198

    Google Scholar 

  • Scheibling RE (1988) Microbial control of sea urchins: Achilles’ Heel or Pandora’s Box? In: Burke RD, Mladenov PV, Lambert P, Parsley RL (eds) Proc 6th Intl Echinoderms Conf, Victoria, BC, 22–28 Aug 1987. Balkema, Rotterdam, pp 745–754

    Google Scholar 

  • Scheibling RE, Hatcher BG (2013) Ecology of Strongylocentrotus droebachiensis. In: Lawrence JM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 353–392

    Google Scholar 

  • Scheibling RE, Hennigar AW (1997) Recurrent outbreaks of disease in sea urchins Strongylocentrotus droebachiensis in Nova Scotia: evidence for a link with large- scale meteorologic and oceanographic events. Mar Ecol Prog Ser 152:155–165

    Google Scholar 

  • Scheibling RE, Lauzon-Guay JS (2010) Killer storms: North Atlantic hurricanes and disease outbreaks in sea urchins. Limnol Oceanogr 556:2331–2338

    Google Scholar 

  • Scheibling RE, Stephenson RL (1984) Mass mortality of Strongylocentrotus droebachiensis (Echinodermata: Echinoidea) off Nova Scotia, Canada. Mar Biol 78:153–164

    Google Scholar 

  • Scheibling RE, Hennigar AW, Balch T (1999) Destructive grazing, epiphytism, and disease: the dynamics of sea urchin–kelp interactions in Nova Scotia. Can J Fish Aquat Sci 56:2300–2314

    Google Scholar 

  • Scheibling RE, Feehan C, Lauzon-Guay J-S (2010) Disease outbreaks associated with recent hurricanes cause mass mortality of sea urchins in Nova Scotia. Mar Ecol Prog Ser 408:109–116

    Google Scholar 

  • Scheibling RE, Feehan CJ, Lauzon-Guay JS (2013) Climate change, disease and the dynamics of a kelp-bed ecosystem in Nova Scotia. In: Fernández-Palocios JM, Nascimiento LD, Hernández JC, Clemente S, González A, Diaz-González JP (eds) Climate change: perspectives from the Atlantic: past, present and future. Servicio de Publicaciones de la Universidad de La Laguna, Tenerife, pp 361–387

    Google Scholar 

  • Shears NT, Ross PM (2009) Blooms of benthic dinoflagellates of the genus Ostreopsis; an increasing and ecologically important phenomenon on temperate reefs in New Zealand and worldwide. Harmful Algae 8:916–925

    Google Scholar 

  • Short FT, Muehlstein LK, Porter D (1987) Eelgrass wasting disease: cause and recurrence of a marine epidemic. Biol Bull 173:557–562

    Google Scholar 

  • Sivertsen K (1996) Incidence, occurrence and distribution of the nematode Echinomermella matsi in its echinoid host, Strongylocentrotus droebachiensis, in northern Norway. Mar Biol 126:703–7146

    Google Scholar 

  • Skadsheim A, Christie H, Leinaas HP (1995) Population reductions of Strongylocentrotus droebachiensis (Echinodermata) in Norway and the distribution of its endoparasite Echinomermella matsi (Nematoda). Mar Ecol Prog Ser 119:199–209

    Google Scholar 

  • Smale DA, Burrows MT, Moore P, O’Connor N, Hawkins SJ (2013) Threats and knowledge gaps for ecosystem services provided by kelp forests. A northeast Atlantic perspective. Ecol Evol 3:4016–4038

    Google Scholar 

  • Sonnenholzner JI, Lafferty KD, Ladah LB (2011) Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagenis in the Galapágos. Ecology 92:2276–2284

    Google Scholar 

  • Sprague JL, Moore KJ, Grunden JR, Ibarra SN, Mooney EA, Scheer G, Kushner DJ (2012) Channel Islands National Park kelp forest monitoring program: annual report 2010. Natural Resource Data Series NPS/CHIS/NRDS—2012/334. National Park Service, Fort Collins, Colorado

  • Sprague JL, Kushner DJ, Moore KJ (2013a) Channel Islands National Park Kelp Forest Monitoring Program: Annual report 2008. Natural Resource Data Series NPS/MEDN/NRDS—2013/572. National Park Service, Fort Collins, Colorado

  • Sprague JL, Kushner DJ, Moore KJ (2013b) Channel Islands National Park Kelp Forest Monitoring Program: annual report 2008. Natural Resource Data Series NPS/MEDN/NRDS—2013/572. National Park Service, Fort Collins, Colorado

  • Sprague JL, Traiger SB, Grunden JR, Ibarra SN, Mooney EA, Moore KJ, Kushner DJ (2013c) Channel Islands National Park kelp forest monitoring program: annual report 2011. Natural Resource Data Series NPS/MEDN/NRDS—2013/480. National Park Service, Fort Collins, Colorado

  • Sprague JL, Civiello MA, Kushner DJ, Moore KJ, Carter SN, Centoni JJ, Fejtek SM (2013d) Channel Islands National Park kelp forest monitoring program: annual report 2012. Natural Resource Data Series NPS/MEDN/NRDS—2013/479. National Park Service, Fort Collins, Colorado

  • Steneck RS (1997) Fisheries-induced biological changes to the structure and function of the Gulf of Maine ecosystem. In: Wallace GT, Braasch EF (eds) Proceedings of the Gulf of Maine ecosystem dynamics scientific symposium and workshop. Regional Association for Research on the Gulf of Maine, Hanover, pp 151–165

    Google Scholar 

  • Steneck RS, Graham MH, Bourque BJ, Corbett D, Erlandson JM, Estes JA, Tegner MJ (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459

    Google Scholar 

  • Steneck RS, Vavrinec J, Leland AV (2004) Accelerating trophic-level dysfunction in kelp forests ecosystems of the Western North Atlantic. Ecosystems 7:323–332

    Google Scholar 

  • Stien A (1999) Effects of the parasite nematode Echinomermella matsi on growth and survival of its host, the sea urchin Strongylocentrotus droebachiensis. Can J Zool 77:139–147

    Google Scholar 

  • Stien A, Halvorsen O, Leinaas HP (1995) No evidence of Echinomermella matsi (Nematoda) as a mortality factor in a local mass mortality of Strongylocentrotus droebachiensis (Echinoidea). In: Skjoldal HR, Hopkins C, Erikstad KE, Leinaas HP (eds) Ecology of fjords and coastal waters. Troms, Norway, pp 585–592

    Google Scholar 

  • Stien A, Leinaas HP, Halvorsen O, Christie H (1998) Population dynamics of the Echinomermella matsi (Nematoda)—Strongylocentrotus droebachiensis (Echinoida) system: effects on host fecundity. Mar Ecol Prog Ser 163:193–201

    Google Scholar 

  • Tegner MJ, Dayton PK (2000) Ecosystem effects of fishing in kelp forest communities. ICES J Mar Sci 57:579–589

    Google Scholar 

  • Tuya F, Boyra A, Sanchez-Jerez P, Barbera C, Haroun R (2004) Can one species determine the structure of the benthic community on a temperate rocky reef? The case of the long-spined sea-urchin Diadema antillarum (Echinodermata: Echinodea) in the eastern Atlantic. Hydrobiologia 519:211–214

    Google Scholar 

  • Tuya F, Haroun RJ, Boyra A, Sanchez-Jerez P (2005) Sea urchin Diadema antillarum: different functions in the structure and dynamics of reefs on both sides of the Atlantic. Mar Ecol Prog Ser 302:307–310

    Google Scholar 

  • Uthicke S, Schaffelke B, Byrne M (2009) A boom and bust phylum? Ecological and evolutionary consequences of density variations in echinoderms. Ecol Monogr 79:3–24

    Google Scholar 

  • Wang YN, Chang YQ, Lawrence JM (2013) Disease in sea urchins. In: Lawrence LM (ed) Edible sea urchins: biology and ecology. Elsevier, Amsterdam, pp 179–186

    Google Scholar 

  • Ward JR, Lafferty KD (2004) The elusive baseline of marine disease: are diseases in ocean ecosystems increasing? PLoS Biol 2:E120

    Google Scholar 

  • Watson J, Estes JA (2011) Stability, resilience, and phase shifts in rocky subtidal communities along the west coast of Vancouver Island, Canada. Ecol Monogr 81:215–239

    Google Scholar 

  • Wharton WG, Mann KH (1981) Relationship between destructive grazing by the sea urchin, Strongylocentrotus droebachiensis, and the abundance of American lobster, Homarus americanus, on the Atlantic coast of Nova Scotia. Can J Fish Aquat Sci 38:1339–1349

    Google Scholar 

  • Zann L, Brodie J, Vuki V (1990) History and dynamics of the crown-of-thorns starfish Acanthaster planci (L.) in the Suva area, Fiji. Coral Reefs 9:135–144

    Google Scholar 

Download references

Acknowledgments

We thank A. Metaxas, C. DiBacco, T. Romanuk, J.S. Lauzon-Guay, K. Filbee-Dexter, and K. Krumhansl for helpful comments on the manuscript. This research was funded by a Discovery Grant to RES from the Natural Sciences and Engineering Research Council (NSERC) of Canada. CJF was supported by a Dalhousie University Graduate Scholarship and an NSERC Canada Graduate Scholarship.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Colette J. Feehan.

Additional information

Communicated by M. Byrne.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Feehan, C.J., Scheibling, R.E. Effects of sea urchin disease on coastal marine ecosystems. Mar Biol 161, 1467–1485 (2014). https://doi.org/10.1007/s00227-014-2452-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-014-2452-4

Keywords

Navigation