Electronic Supplementary Material: S.D. Ling et al. Global regime shift dynamics of catastrophic sea urchin overgrazing
Table S1. Summary of correlative databetween percent ‘landscape’ cover (%) of macroalgal canopy formers and sea urchin biomass (grams. m-2) for 13 regions worldwide. Where required, conversion of macroalgal abundance to % Cover was based only on large canopy-forming adults where data sets split abundance or biomass estimates by life-history stages. For sea urchins, biomass (grams wet weight) was calculated using allometric conversion of TD (Test Diameter in mm) to biomass where individual sea urchin test diameters were recorded; else an average individual biomass of sea urchins was estimated for particular regions.
Macroalgal canopy cover / Sea urchin abundance# / Hemisphere / Region / Sites / Spatial extent (km) / n / Year sampled / Dominant genera / Quadrat scale (m) / % Cover / conversion / Dominant genera / Quadrat
scale (m) / Biomass (B, grams)
1 / Southern / Australia -Tas/NSW / 164 / 1,500 / 5,264 / 2001-2008 / Ecklonia / 5x1 / Direct measure / Centrostephanus / 5x1 / B=0.0106(TD)2.2319
2 / Southern / Australia – Tas/Vic / 37 / 500 / 628 / 2001-2013 / Ecklonia / 5x1 / Direct measure / Heliocidaris / 5x1 / B=0.0014(TD)2.668
3 / Southern / New Zealand / 165 / 2,000 / 642 / 1999-2003 / Ecklonia / 1x1 / % Cover=8.92ln(biomass) +2.29 / Evechinus / 1x1 / B=0.000843(TD)2.8288
4 / Southern / Chile / 4 / 400 / 511 / 2012 / Lessonia / 1x1 / Morphometric scaling:
Lessonia canopy area =
pi*(3.5*individ. holdfast radius)2 / Tetrapygus / 1x1 / B= 298g. individ.-1
[Individual holdfast diameter measured in situ]
5 / Southern / South Africa / 6 / 100 / 162 / 1988/89,2001/05-06 / Ecklonia/ Laminaria / 1x1 / % Cover= 0.1432(biomass) + 5.518 / Parechinus / 1x1 / B= 27.5g.Individ.-1
6 / Northern / Nova Scotia / 2 / 100 / 115 / 1992-1993 / Sacharrina/ Laminaria / 1x1 / Direct measure / Strongylocentrotus / 1x1 / Direct measure
7 / Northern / Gulf of St.Lawrence / 18 / 100 / 157 / 2011 / Sacharrina/ Laminaria / 0.5x0.5 / Direct measure / Strongylocentrotus / 0.5x0.5 / B = 0.0007(TD)2.8539
8 / Northern / Norway / 51 / 1,000 / 1,025 / 2007-2012 / Sacharrina/ Laminaria / 0.5x0.5 / Direct measure / Strongylocentrotus / 0.5x0.5 / B= 0.0007(TD)2.8539
9 / Northern / Canary Islands / 125 / 500 / 800 / 2001-2004 / Lobophora/ Cystoseira / 0.5x0.5 / Direct measure / Diadema / 5 x 4 / B=0.0008(TD)2.8941
10 / Northern / California / 11 / 250 / 581 / 2001-2012 (annually) / Macrocysits / 20x2 / %Cover to Stipe Count (SC): / Strongylocentrotus / 3x1 / B=0.0499(TD) + 0.0019
Laminaria / Macrocystis; %Cover=3.77*SC
Pterygophora / Eisenia; %Cover=8.98*SC
Eisenia / Pterygophora; %Cover=2.23*SC
Laminaria; %Cover=0.89*SC
11 / Northern / British Columbia / 8 / 250 / 161 / 2012 / Nereocystis/ / 1x1 / Morphometric scaling: / Strongylocentrotus / 1 x 1 / S.franciscanus:
B=0.0005*(TD)2.9572;
Laminaria / Genus %Cover of 1m2/individ.
Nereocystis 100 / S. purpuratusB=0.0005*(TD)2.9598
Cymathere 25
Costeria 21
Alaria 20
Laminaria 16
Saccharina 15
Pterygophora 7
Eisenia 2
12 / Northern / Mediterranean / 6 / 2 / 278 / 1999 / Cystoseira / 1x1 / Direct measure / Paracentrotus / 1 x 1 / B=0.00319(TD)2.479
13 / Northern / Japan / 1 / 1 / 320 / 2013 / Eisenia/ Saccharina / 1x1 / Direct measure / Strongylocentrotus / 1 x 1 / B= 79g.individ.-1
/ Undaria
1
Electronic Supplementary Material: S.D. Ling et al. Global regime shift dynamics of catastrophic sea urchin overgrazing
Table S2. Summary of observational and manipulative experiments detailing the magnitude and directional response of macroalgal habitat (both forward and reverse regime shifts) following change in sea urchin abundance. Studies were included if stated magnitudes in themacroalgalresponse and sea urchin abundance could be standardized as percentage cover (%) for macroalgaeand biomass(grams. m-2) for sea urchins respectively. Experiments involved sudden changes in urchin biomass density between “Start” & “End”: experimenters either reduced or increased urchins to a target density; or in the case of observational studies, either disease (reverse shifts) or local aggregation (forward shifts) also caused sudden change in urchin density. But see exception (study #43) in footnote below.
# / Hemisphere / Region / Experiment / Regimeshiftdirection / Urchin biomass
Start (g.m-2) / Urchin biomass
End (g.m-2) / Urchin density end
(individ. m-2) / % Cover canopy macroalgae start / % Cover canopy macroalgae end / % Cover canopy macroalgae loss/gain / Duration of response (months) / Source
1 / Northern / New England / Observational / Fwd / 0 / 12,228 / 280 / 100 / 0 / 100 / 3 / Witman, 1985
2 / Southern / Australia / Manipulation / Fwd / 0 / 7,767 / 90 / 55 / 7 / 48 / 7 / Wright et al 2005
3 / Southern / Australia / Manipulation / Fwd / 932 / 6,136 / 80 / 60 / 0 / 60 / 4 / Wright et al 2005
4 / Northern / British Columbia / Observational / Fwd / 5,770 / 5,770 / 322 / 39 / 1 / 38 / 11 / Foreman 1977
5 / Southern / Australia / Manipulation / Fwd / 0 / 3,107 / 40 / 68 / 37 / 30 / 7 / Wright et al 2005
6 / Southern / Australia / Manipulation / Fwd / 0 / 2,535 / 10 / 95 / 20 / 75 / 5 / Hill et al 2003
7 / Northern / California / Observational / Fwd / 1,246 / 1,246 / 7 / 38 / 8 / 30 / 3 / Dean et al 1984
8 / Southern / Australia / Manipulation / Fwd / 1,162 / 1,162 / 4 / 71 / 12 / 58 / 6 / Strain & Johnson 2009
9 / Southern / Australia / Manipulation / Fwd / 0 / 1,014 / 4 / 95 / 70 / 25 / 5 / Hill et al 2003
10 / Northern / Nova Scotia / Manipulation / Fwd / 0 / 883 / 34 / 98 / 0 / 98 / 3 / Johnson & Mann 1990
11 / Northern / Nova Scotia / Observational / Fwd / 691 / 691 / 120 / 20 / 0 / 20 / 24 / Miller 1985
12 / Northern / Nova Scotia / Observational / Fwd / 667 / 667 / 93 / 84 / 0 / 83 / 1 / Scheilbling et al 1999
13 / Southern / Australia / Manipulation / Fwd / 581 / 581 / 2 / 71 / 23 / 47 / 6 / Strain & Johnson 2009
14 / Southern / Australia / Manipulation / Fwd / 0 / 507 / 2 / 95 / 70 / 25 / 5 / Hill et al 2003
15 / Northern / Nova Scotia / Observational / Fwd / 233 / 233 / 32 / 79 / 0 / 78 / 3 / Scheilbling et al 1999
16 / Northern / Canary Islands / Manipulation / Fwd / 27 / 210 / 7 / 54 / 12 / 42 / 6 / Hernández et al. unpub. data
17 / Northern / Canary Islands / Manipulation / Fwd / 9 / 150 / 8 / 85 / 0 / 85 / 9 / Hernández et al. unpub. data
18 / Northern / Nova Scotia / Manipulation / Rev / 804 / 0 / 0 / 0 / 59 / 59 / 4 / Johnson & Mann 1990
19 / Northern / Alaska / Manipulation / Rev / 3,506 / 0 / 0 / 0 / 100 / 100 / 12 / Duggins 1980
20 / Southern / Australia / Manipulation / Rev / 464 / 0 / 0 / 0 / 100 / 100 / 6 / Kriegisch et al. unpub. data
21 / Southern / New Zealand / Manipulation / Rev / 2,261 / 0 / 0 / 0 / 12 / 12 / 10 / Shears & Babcock 2002
22 / Southern / Australia / Manipulation / Rev / 1,057 / 0 / 0 / 0 / 93 / 93 / 18 / Ling 2008
23 / Southern / Australia / Manipulation / Rev / 559 / 0 / 0 / 0 / 78 / 77 / 18 / Ling 2008
24 / Southern / Australia / Manipulation / Rev / 401 / 0 / 0 / 0 / 37 / 37 / 18 / Ling 2008
25 / Southern / Australia / Manipulation / Rev / 757 / 0 / 0 / 0 / 92 / 92 / 18 / Ling unpub. 2008-2011
26 / Southern / Australia / Manipulation / Rev / 456 / 0 / 0 / 0 / 91 / 91 / 18 / Ling unpub. 2008-2011
27 / Southern / Australia / Manipulation / Rev / 2,535 / 0 / 0 / 0 / 48 / 48 / 18 / Andrew & Underwood 1993
28 / Southern / Australia / Manipulation / Rev / 1,521 / 0 / 0 / 0 / 30 / 30 / 18 / Andrew et al 1998
29 / Southern / Australia / Manipulation / Rev / 1,014 / 0 / 0 / 0 / 28 / 28 / 5 / Hill et al 2003
30 / Southern / New Zealand / Manipulation / Rev / 912 / 0 / 0 / 0 / 28 / 27 / 18 / Andrew & Choat 1982
31 / Southern / New Zealand / Manipulation / Rev / 912 / 0 / 0 / 0 / 42 / 42 / 18 / Andrew & Choat 1982
32 / Northern / British Columbia / Observational / Rev / 2,900 / 0 / 0 / 0 / 100 / 100 / 72 / Watson & Estes 2011
33 / Northern / British Columbia / Observational / Rev / 4,579 / 0 / 0 / 0 / 100 / 100 / 12 / Watson & Estes 2011
34 / Southern / Australia / Observational / Rev / 2,317 / 0 / 0 / 0 / 88 / 88 / 20 / Andrew 1991
35 / Northern / New England / Manipulation / Rev / 4,673 / 0 / 0 / 0 / 100 / 100 / 25 / Witman 1987
36 / Northern / Nova Scotia / Observational / Rev / 1208 / 0 / 0 / 0 / 100 / 100 / 36 / Scheibling, 1986
37 / Southern / Australia / Manipulation / Rev / 191 / 0 / 0 / 0 / 52 / 52 / 13 / Strain & Johnson 2013
38 / Northern / Nova Scotia / Observational / Rev / 480 / 5 / 0.5 / 0 / 100 / 100 / 33 / Miller & Colodey 1983
39 / Northern / British Columbia / Observational / Rev / 2,198 / 15 / 0.1 / 0.3 / 100 / 100 / 12 / Watson & Estes 2011
40 / Northern / Nova Scotia / Observational / Rev / 201 / 18 / 15 / 0 / 25 / 25 / 21 / Miller 1985
41 / Northern / California / Manipulation / Rev / 1,254 / 25 / 0.1 / 0 / 22 / 22 / 8 / Cowen et al 1982
42 / Northern / Newfoundland / Manipulation / Rev / 413 / 41 / 3 / 0 / 9 / 9 / 10 / Keats et al 1990
43 / Southern / New Zealand / Manipulation / Rev / 635 / 70 / 0.5 / 2 / 50 / 48 / 300* / Shears & Babcock 2003
44 / Northern / British Columbia / Observational / Rev / 2,314 / 76 / 0.3 / 0 / 100 / 100 / 24 / Watson & Estes 2011
45 / Southern / Australia / Manipulation / Rev / 581 / 79 / 0.5 / 0 / 25 / 25 / 12 / Ling et al 2010
46 / Northern / California / Observational / Rev / 623 / 89 / 0.5 / 0 / 100 / 100 / 12 / Pearse & Hines 1979
47 / Northern / Nova Scotia / Manipulation / Rev / 2,200 / 102 / 13 / 0 / 26 / 26 / 23 / Himmelman et al 1983
48 / Northern / Nova Scotia / Observational / Rev / 128 / 128 / 24 / 0 / 90 / 90 / 19 / Schielbling et al 1999
49 / Southern / Australia / Manipulation / Rev / 1,521 / 254 / 1 / 0 / 30 / 30 / 18 / Andrew et al 1998
50 / Northern / Norway / Manipulation / Rev / 1,388 / 324 / 6 / 0 / 95 / 95 / 36 / Leinass & Christie 1996
51 / Northern / Canary Islands / Manipulation / Rev / 112 / 0 / 0 / 17 / 46 / 29 / 12 / Ortega-Borges et al 2009
52 / Northern / Mediterranean / Manipulation / Rev / 208 / 5 / 0.2 / 0 / 41 / 41 / 16 / Bendetti-cecchi et al 1998
53 / Northern / Mediterranean / Manipulation / Rev / 231 / 5 / 0.2 / 2 / 54 / 52 / 18 / Bulleri et al 1999
54 / Northern / Canary Islands / Manipulation / Rev / 185 / 12 / 0.5 / 0 / 54 / 54 / 6 / Hernández et al. unpub. data
55 / Northern / Mediterranean / Manipulation / Rev / 336 / 19 / 1 / 0 / 70 / 70 / 48 / Hereu 2004
56 / Northern / Canary Islands / Manipulation / Rev / 170 / 20 / 1 / 0 / 85 / 85 / 10 / Hernández et al. unpub. data
57 / Northern / Canary Islands / Manipulation / Rev / 150 / 57 / 2 / 0 / 54 / 54 / 6 / Hernández et al. unpub. data
*Note that for purposes of calculating an average time for macroalgae recovery once urchin abundance falls below the critical reverse-shift threshold, the long-term recovery of macroalgae observed inside the Leigh Marine Reserve over 25 years (300 months) was excluded given the long lag times involved in the re-establishment of functional urchin predators and ultimately reduction in urchin abundance (Shears & Babcock 2003).
Fig. S1. Example images of alternative macroalgal bed and grazed sea urchin barren states of rocky reef systems worldwide. Red arrows indicate the forward-shift caused by sea urchin overgrazing from macroalgal dominated to urchin dominated barrens; blue arrows indicate the reverse-shift from urchin barrens back to macroalgal habitat once grazing pressure is alleviated. Dominant macroalgal and barrens-forming sea urchin species are listed respectively - photographic credits are given in square brackets: Northern Hemisphere systems, a.) Nova Scotia (SaccharinalatissimaStrogylocentrotusdroebachiensis[by Scott Ling]), b.) British Columbia(NereocystisluetkeanaS. franciscanus[by Mark Wunsch], c.) California (Pterygophoracalifornica [by Alejandro Perez-Matus] & S. franciscanus plus S. purpuratus [by Scott Ling], d) Japan (Saccharina japonicaS. nudus [by Daisuke Fujita]), e) Mediterranean (CystoseirabalearicaParacentrotuslividus [by BernatHereu]), f) Canary Islands (LobophoravariegataDiademaafricanum [by Scott Ling]); Southern Hemisphere systems, g) Australia (EckloniaradiataHeliocidariserythrogramma [by Scott Ling] - for images of Australian urchin barrens formed by Centrostephanusrodgersii - see Ling & Johnson 2012; Ling 2013), h) New Zealand (E.radiataEvechinuschloriticus [by Nick Shears], i) Chile (LessoniatrabeculataTetrapygusniger [by Alejandro Perez-Matus]), j) South Africa, Ecklonia maxima and Laminariapallida [by Rob Tarr] & Parechinusangulosus [by Rob Tarr]).
Fig. S2.Map showing the 13 globally representative temperate rocky reef systems known to occur as algal bed or urchin barrens states (temperate zones encapsulated by dotted lines within each hemisphere; equator is shown as dash-dot line). Ordered west to east from Northern to Southern Hemispheres, the representative reef systems covered 11 regions: 1. British Columbia (Gulf of Alaska, NE Pacific); 2.California (NE Pacific); 3.Nova Scotia (NW Atlantic); 4.Gulf of St. Lawrence (NW Atlantic); 5.Canary Is. (NE Atlantic); 6.Norway (Norwegian Sea, NE Atlantic); 7.Mediterranean (Mediterranean Sea, NE Atlantic); 8. Japan (NW Pacific); 9.Chile (SE Pacific); 10.South Africa (W Indian); 11.Victoria (SE Australia, SW Pacific); 12.Tasmania (SE Australia, SW Pacific); 13. New Zealand (SW Pacific Ocean). Refer to Fig. S1 for particular sea urchin and macroalgal species occurring within each reef system.
Supplementary References
Table 1
S1.Estes, J.A. and D.O. Duggins, Sea otters and kelp forests in Alaska: generality and variation in a community ecological paradigm. Ecological Monographs, 1995. 65(1): p. 75-100.
S2.Shears, N.T. and R.C. Babcock, Continuing trophic cascade effects after 25 years of no take marine reserve protection. Marine Ecology Progress Series, 2003. 246: p. 1-16.
S3.Pederson, H.G. and C.R. Johnson, Predation of the sea urchin< i> Heliocidaris erythrogramma</i> by rock lobsters (< i> Jasus edwardsii</i>) in no-take marine reserves. Journal of Experimental Marine Biology and Ecology, 2006. 336(1): p. 120-134.
S4.Ling, S., et al., Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proceedings of the National Academy of Sciences, 2009. 106(52): p. 22341-22345.
S5.Clemente, S., et al., Identifying keystone predators and the importance of preserving functional diversity in sublittoral rocky-bottom areas. Marine Ecology Progress Series, 2010. 413: p. 55-67.
S6.Ling, S. and C. Johnson, Marine reserves reduce risk of climate-driven phase shift by reinstating size-and habitat-specific trophic interactions. Ecological Applications, 2012. 22(4): p. 1232-1245.
S7.Bonaviri, C., et al., Micropredation on sea urchins as a potential stabilizing process for rocky reefs. Journal of Sea Research, 2012. 73: p. 18-23.
S8.Estes, J.A., et al., Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science, 1998. 282: p. 473-476.
S9.Steneck, R.S. Fisheries-induced biological changes to the structure and function of the Gulf of Maine ecosystem. in Proceedings of the Gulf of Maine ecosystem dynamics scientific symposium and workshop. 1997. Regional Association for Research on the Gulf of Maine Hanover, NH.
S10.Britton-Simmons, K.H., G. Foley, and D. Okamoto, Spatial subsidy in the subtidal zone: utilization of drift algae by a deep subtidal sea urchin. Aquat Biol, 2009. 5(3): p. 233-243.
S11.Kelly, J.R., K.A. Krumhansl, and R.E. Scheibling, Drift algal subsidies to sea urchins in low-productivity habitats. Marine Ecology Progress Series, 2012. 452: p. 145-157.
S12.Connell, S.D. and A.D. Irving, Integrating ecology with biogeography using landscape characteristics: a case study of subtidal habitat across continental Australia. Journal of Biogeography, 2008. 35(9): p. 1608-1621.
S13.Keats, D., G. South, and D. Steele, The effects of an experimental reduction in grazing by green sea urchins on a benthic macroalgal community in eastern Newfoundland. Marine Ecology Progress Series, 1990. 68: p. 181-193.
S14.Kawamata, S., Inhibitory effects of wave action on destructive grazing by sea urchins: a review. Bulletin of Fisheries Research Agency, 2010 32(95-102).
S15.Konar, B., Limited effects of a keystone species: trends of sea otters and kelp forests at the Semichi Islands, Alaska. Marine Ecology Progress Series, 2000. 199: p. 271-280.
S16.Kelly, J.R., R.E. Scheibling, and T. Balch, Invasion-mediated shifts in the macrobenthic assemblage of a rocky subtidal ecosystem. Mar Ecol Prog Ser, 2011. 437: p. 69-78.
S17.Dayton, P.K., et al., Sliding baselines, ghosts, and reduced expectations in kelp forest communities. Ecological Applications [Ecol. Appl.]. 1998. 8(2): p. 309-322.
S18.Hart, M.W. and R.E. Scheibling, Heat waves, baby booms, and the destruction of kelp beds by sea urchins. Marine Biology, 1988. 99: p. 167-176.
S19.Sivertsen, K. Overgrazing of kelp beds along the coast of Norway. in Eighteenth International Seaweed Symposium. 2007. Springer.
S20.Tegner, M.J., et al., Sea urchin cavitation of giant kelp (Macrocystis pyriferaC. Agardh) holdfasts and its effects on kelp mortality across a large California forest. Journal of Experimental Marine Biology and Ecology, 1995. 191: p. 83-99.
S21.Harrold, C. and D.C. Reed, Food availability, sea urchin grazing and kelp forest community structure. Ecology, 1985. 66(4): p. 1160-1169.
S22.Ling, S., et al., Reproductive potential of a marine ecosystem engineer at the edge of a newly expanded range. Global Change Biology, 2008. 14(4): p. 907-915.
S23.Johnson, C.R. and K.H. Mann, The importance of plant defence abilities to the structure of subtidal seaweed communities: The kelp< i> Laminaria longicruris</i> de la Pylaie survives grazing by the snail< i> Lacuna vincta</i>(Montagu) at high population densities. Journal of Experimental Marine Biology and Ecology, 1986. 97(3): p. 231-267.
S24.Fletcher, W.J., Interactions among subtidal Australian sea urchins, gastropods, and algae: effects of experimental removals. Ecological Monographs, 1987. 57(1): p. 89-109.
S25.Clemente, S., J. Hernández, and A. Brito, Context-dependent effects of marine protected areas on predatory interactions. Mar Ecol Prog Ser, 2011. 437: p. 119-133.
S26.Watson, J. and J.A. Estes, Stability, resilience, and phase shifts in rocky subtidal communities along the west coast of Vancouver Island, Canada. Ecological Monographs, 2011. 81(2): p. 215-239.
S27.Sangil, C., et al., No-take areas as an effective tool to restore urchin barrens on subtropical rocky reefs. Estuarine, Coastal and Shelf Science, 2012. 112: p. 207-215.
S28.Jones, N. and J. Kain, Subtidal algal colonization following the removal of Echinus. Helgoländ Wiss Meer, 1967. 15: p. 460-466.
S29.Lauzon-Guay, J.-S. and R.E. Scheibling, Seasonal variation in movement, aggregation and destructive grazing of the green sea urchin (Strongylocentrotus droebachiensis) in relation to wave action and sea temperature. Marine Biology, 2007. 151(6): p. 2109-2118.
S30.Gagnon, P., J. Himmelman, and L. Johnson, Temporal variation in community interfaces: kelp-bed boundary dynamics adjacent to persistent urchin barrens. Marine Biology, 2004. 144(6): p. 1191-1203.
S31.Tegner, M. and P. Dayton, Sea urchins, El Ninos, and the long term stability of Southern California kelp forest communities. Marine ecology progress series. Oldendorf, 1991. 77(1): p. 49-63.
S32.Lang, C. and K. Mann, Changes in sea urchin populations after the destruction of kelp beds. Marine Biology, 1976. 36(4): p. 321-326.
S33.Hernández, J.C., et al., Effect of temperature on settlement and postsettlement survival in a barrens-forming sea urchin. Marine Ecology Progress Series, 2010. 413(6).
S34.Byrne, M., et al., Reproduction in the diadematoid sea urchin Centrostephanus rodgersii in contrasting habitats along the coast of New South Wales, Australia. Marine Biology, 1998. 132: p. 305-318.
S35.Eurich, J., R. Selden, and R. Warner, California spiny lobster preference for urchins from kelp forests: implications for urchin barren persistence. MARINE ECOLOGY PROGRESS SERIES, 2014. 498: p. 217-225.
S36.Tegner, M.J. and P.K. Dayton, Sea urchin recruitment patterns and implications of commerical fishing. Science, 1976: p. 324-326.
S37.Tegner, M.J. and P.K. Dayton, Population structure, recruitment and mortality of two sea urchins (Stronglyocentrotus franciscanus and S. purpuratus) in a kelp forest. Marine Ecology Progress Series, 1981. 5: p. 255-268.
S38.Zhang, Z., et al., Recruitment patterns and juvenile–adult associations of red sea urchins in three areas of British Columbia. Fisheries Research, 2011. 109(2): p. 276-284.
S39.Hereu, B., et al., Multiple processes regulate long-term population dynamics of sea urchins on Mediterranean rocky reefs. PloS one, 2012. 7(5): p. e36901.
S40.Scheibling, R.E. and A.W. Hennigar, Recurrent outbreaks of disease in sea urchins Stronglyocentrotus droebachiensis in Nova Scotia: evidence for a link with large-scale meteorologic and ceanographic events. Marine Ecology Progress Series, 1997. 152: p. 155-165.
S41.Pearse, J. and A. Hines, Expansion of a central California kelp forest following the mass mortality of sea urchins. Marine Biology, 1979. 51: p. 83-91.
S42.Scheibling, R.E., A.W. Hennigar, and T. Balch, Destructive grazing, epiphytism, and disease: the dynamics of sea urchin-kelp interactions in Nova Scotia. Canadian Journal of Fisheries and Aquatic Sciences, 1999. 56(12): p. 2300-2314.
S43.Scheibling, R.E. and J.-S. Lauzon-Guay, Killer storms: North Atlantic hurricanes and disease outbreaks in sea urchins. Limnology and Oceanography, 2010. 55(6): p. 2331-2338.
S44.Andrew, N.L., Changes in subtidal habitat following mass mortality of sea urchins in Botany Bay, New South Wales. Australian Journal of Ecology, 1991. 16: p. 353-362.
S45.Scheibling, R., Feehan CJ, and L.-G. JS, Climate change, disease and the dynamics of a kelp-bed ecosystem in Nova Scotia, in Climate Change: past, present and future perspectives, a global synthesis from the Atlantic. Servicio de Publicaciones de la Universidad de La Laguna, Tenerife, Fernández-Palocios JM, et al., Editors. 2013. p. 41−81.
S46.Fagerli, C.W., K.M. Norderhaug, and H.C. Christie, Lack of sea urchin settlement may explain kelp forest recovery in overgrazed areas in Norway. Marine Ecology Progress Series, 2013. 488: p. 119-132.
S47.Fagerli CW, et al., Predators of the destructive sea urchin grazer Strongylocentrotus droebachiensis on the Norwegian coast Marine Ecology Progress Series, 2014. 502: p. 207-218.
Supplementary References
Table S2
Andrew NL (1991) Changes in subtidal habitat following mass mortality of sea urchins in Botany Bay, New South Wales. Australian Journal of Ecology 16: 353-362
Andrew NL, Choat JH (1982) The influence of predation and conspecific adults on the abundance of juvenile Evechinuschloroticus (Echinoidea: Echinometridae). Oecologia54: 80-87
Andrew NL, Underwood AJ (1993) Density-dependent foraging in the sea urchin Centrostephanusrodgersii on shallow subtidal reefs in New South Wales, Australia. Marine Ecology Progress Series99: 89-98
Andrew NL, Worthington DG, Brett PA, Bentley N, Chick RC, Blount C (1998) Interactions between the abalone fishery and sea urchins in New South Wales. inFRDC Final Report, ed. 1993/102 PN
Benedetti-Cecchi, L, Bulleri, F, Cinelli, F. (1998) Density dependent foraging of sea urchins in shallow subtidal reefs on the west coast of Italy (western Mediterranean).Marine Ecology Progress Series163: 203-211
Bulleri F, Benedetti-CecchiL, Cinelli F (1999) Grazing by the sea urchinsArbacialixulaL. and ParacentrotuslividusLam. in the Northwest Mediterranean. Journal of Experimental Marine Biology and Ecology 241: 81-95
Cowen, Robert K., Catherine R. Agegian, Foster MS (1982) The maintenance of community structure in a central California giant kelp forest. Journal of Experimental Marine Biology and Ecology 64: 189-201
Dean TA, Schroeter SC, Dixon JD (1984) Effects of grazing by two species of sea urchins (Strongylocentrotusfranciscanusand Lytechinusanamesus) on recruitment and survival of two species of kelp(Macrocystispyrifera and Pterygophoracalifornica). Marine Biology 78, 301-313
Duggins DO (1980) Kelp beds and sea otters: An experimental approach.Ecology 61:447-453
Foreman RE (1977) Benthic community modification and recovery following intensive grazing by Strongylocentrotusdroebachiensis. Helgoland Wiss Meer 30:468-484
Hereu, B (2004) The role of trophic interactions between fishes, sea urchins and algae in the northwest Meditterannean rocky infralittotal. PhD Thesis, Department d’Ecologia, Universitat de Barcelona.
Hill NA, Blount C, Poore AGB, Worthington D, Steinberg PD (2003) Grazing effects of the sea urchin Centrostephanusrodgersii in two contrasting rocky reef habitats: effects of urchin density and its implications for the fishery. Marine & Freshwater Research54: 691-700
Himmelman JH, Cardinal A, Bourget E (1983) Community development following removal of urchins, Strongylocentrotusdroebachiensis, from the rocky subtidal zone of the St. Lawrence Estuary, Eastern Canada. Oecologia 59:27-39
Johnson CR, Mann KH (1993) Rapid succession in subtidal understorey seaweeds during recovery from overgrazing by sea urchins in eastern Canada. Botanica Marina 36: 63-77
Keats DW, South GR, Steele DH (1990) The effects of an experimental reduction in grazing by green sea urchins on a benthic macroalgal community in eastern Newfoundland. Marine Ecology Progress Series68:181-193
Leinaas HP, Christie H (1996) Effects of removing sea urchins (Strongylocentrotusdroebachiensis): stability of the barren state and succession of kelp forest recovery in the east Atlantic. Oecologia 105:524-536
Ling SD (2008) Range expansion of a habitat-modifying species leads to loss of taxonomic diversity: a new and impoverished reef state. Oecologia156:883-894
Ling SD, Ibbott S, Sanderson JC (2010) Recovery of canopy-forming macroalgae following removal of the enigmatic grazing sea urchin Heliocidariserythrogramma.Journal of Experimental Marine Biology and Ecology 395:135-146
Miller RJ (1985) Succession in sea urchin and seaweed abundance in Nova Scotia, Canada. Mar Biol 84:275-286