Mapping habitats in a marine reserve showed how a 30-year trophic cascade altered ecosystem structure

Biological Conservation

Volumn 155, Issue , 2012, Pages 193-201

  Leleu, Kévin ^a,b,c   Remy Zephir, Brice ^a,d   Grace, Roger ^e   Costello, Mark J ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

^b IFREMER   (France)

^c AIX MARSEILLE UNIVERSITY   (France)

^d Gardline Marine Sciences Pty Limited Unit 2   (Australia)

^e Postal Distribution Centre   (New Zealand)

Author keywords

Ecosystem change; Fish; Kelp forest; Lobster; New Zealand; Predator release; Subtidal mapping; Time series; Urchin Barren

Indexed keywords

ABUNDANCE; ALGA; BIODIVERSITY; BIOTOPE; CETACEAN; ECHINODERM; ECOSYSTEM DYNAMICS; ECOSYSTEM STRUCTURE; FISHING; FOOD WEB; GRAZING; KELP FOREST; LOBSTER; MARINE PARK; PERCIFORM; POPULATION DISTRIBUTION; PREDATOR; SEAFLOOR MAPPING; SHARK; SUBTIDAL ENVIRONMENT; TIME SERIES; TROPHIC CASCADE;

NEW ZEALAND;

ALGAE; CETACEA; CHONDRICHTHYES; ECHINOIDEA; PALINURIDAE;

EID: 84864051826     PISSN: 00063207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biocon.2012.05.009     Document Type: Article

References (101)

1. Anderson M.J., Millar R.B. Spatial variation and effects of habitat on temperate reef fish assemblages in northeastern New Zealand. J. Exp. Mar. Biol. Ecol. 2004, 305:191-221.
2. Andrew N.L., Choat J.H. The influence of predation and conspecific adults on the abundance of juvenile Evechinus chloroticus (Echinoidea: Echinometridae). Oecologia 1982, 54:80-87.
3. Andrew N.L., Choat J.H. Habitat related differences in the survivorship and growth of juvenile sea urchins. Mar. Ecol. Prog. Ser. 1985, 27:155-161.
4. Andrew N.L., MacDiarmid A.B. Interrelations between sea urchins and spiny lobsters in northeastern New Zealand. Mar. Ecol. Prog. Ser. 1991, 70:211-222.
5. Appeltans, W., Bouchet, P., Boxshall, G.A., Fauchald, K., Gordon, D.P., Hoeksema, B.W., Poore, G.C.B., Van Soest, R.W.M., Stöhr, S., Walter, T.C., Costello, M.J., (Eds.), 2009. World Register of Marine Species. <> (accessed 20.11.09). http://www.marinespecies.org.
6. Ayling, A.M., 1978. Marine reserve survey. Bulletin 1. Leigh Laboratory, University of Auckland, New Zealand.
7. Ayling, A.M., Cumming, A., Ballantine, W.J., 1981. Map of shore and sub-tidal habitats of the Cape Rodney-Okakari Point Marine Reserve, North Island, New Zealand in 3 sheets, scale 1:2000. Department of Lands and Survey, Wellington, New Zealand.
8. Babcock R.C., Kelly S., Shears N.T., Walker J.W., Willis T.J. Changes in community structure in temperate marine reserves. Mar. Ecol. Prog. Ser. 1999, 189:125-134.
9. Babcock R.C., Shears N.T., Alcala A.C., Barrett N.S., Edgar G.J., Lafferty K.D., McClanahan T.R., Russ G.R. Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects. Proc. Natl. Acad. Sci. USA 2010, 107:18256-18261.
10. Ballantine W.J. Marine reserves: lessons from New Zealand. Progr. Underwater Sci. 1989, 13:1-14.
11. Barrett N., Buxton C., Gardner C. Rock lobster movement patterns and population structure within a Tasmanian Marine Protected Area inform fishery and conservation management. Mar. Freshwater Res. 2009, 60:417-425.
12. Barrett N., Buxton C., Edgar G.J. Changes in invertebrate and macroalgal populations in Tasmanian marine reserves in the decade following protection. J. Exp. Mar. Biol. Ecol. 2009, 370:104-119.
13. Childerhouse S., Gales N. Historical and modern distribution and abundance of the New Zealand sea lion Phocarctos hookeri. N.Z. J. Zool. 1998, 25:1-16.
14. Choat J.H., Schiel D.R. Patterns of distribution and abundance of large brown algae and invertebrate herbivores in subtidal regions of northern New Zealand. J. Exp. Mar. Biol. Ecol. 1982, 60:129-162.
15. Claudet J., Osenberg C.W., Benedetti-Cecchi L., Domenici P., Garcia-Charton J.-A., Pérez-Ruzafa Á., Badalamenti F., Bayle-Sempere J., Brito A., Bulleri F., Culioli J.-M., Dimech M., Falcón J.M., Guala I., Milazzo M., Sánchez-Meca J., Somerfield P.J., Stobart B., Vandeperre F., Valle C., Planes S. Marine reserves: size and age do matter. Ecol. Lett. 2008, 11:481-489.
16. Cole R.G., Ayling T.M., Creese R.G. Effects of marine reserve protection at Goat Island, northern New Zealand. N.Z. J. Mar. Freshwater Res. 1990, 24:197-210.
17. Cole R.G., Keuskamp D. Indirect effects of protection from exploitation: patterns from populations of Evechinus chloroticus (Echinoidea) in northeastern New Zealand. Mar. Ecol. Prog. Ser. 1998, 173:215-226.
18. Connor, D.W., Brazier, D.P., Hill, T.O., Northen, K.O., 1997a. Marine Nature Conservation Review: marine biotope classification for Britain and Ireland, vol. 1. Littoral biotopes. Version 97.06. Peterborough. Joint Nature Conservation Committee Report, No. 229.
19. Connor, D.W., Dalkin, M.J., Hill, T.O., Holt, R.H.F., Sanderson, W.G., 1997b. Marine Nature Conservation Review: marine biotope classification for Britain and Ireland, vol. 2. Sublittoral biotopes. Version 97.06. Peterborough. Joint Nature Conservation Committee Report, No. 230.
20. Congalton R., Green K. Assessing the accuracy of remotely sensed data: principles and practices 1999, Lewis Publishers, New York.
21. Cook K., Vanderklift M.A. Depletion of predatory fish by fishing in a temperate reef ecosystem leads to indirect effects on prey, but not lower trophic levels. Mar. Ecol. Prog. Ser. 2011, 432:195-205.
22. Costello M.J. Distinguishing marine habitat classification concepts for ecological data management. Mar. Ecol. Prog. Ser. 2009, 397:253-268.
23. Costello M.J., Emblow C. A classification of inshore marine biotopes. The Intertidal Ecosystem: The Value of Ireland's Shores 2005, 25-35. Royal Irish Academy, Dublin. J.G. Wilson (Ed.).
24. Costello M.J., McCrea M., Freiwald A., Lundalv T., Jonsson L., Bett B.J., Weering T.V., de Haas H., Roberts J.M., Allen D. Functional role of deep-sea cold-water Lophelia coral reefs as fish habitat in the north-eastern Atlantic. Cold-Water Corals and Ecosystems 2005, 771-805. Springer Verlag, Berlin, Heidelberg. A. Freiwald, J.M. Roberts (Eds.).
25. Cowles A., Hewitt J.E., Taylor R.B. Density, biomass and productivity of small mobile invertebrates in a wide range of coastal habitats. Mar. Ecol. Prog. Ser. 2009, 384:175-185.
26. Dalleau M., Andréfouët S., Wabnitz C.C., Payri C., Wantiez L., Pichon M., Friedman K., Vigliola L., Benzoni F. Use of habitats as surrogates of biodiversity for efficient coral reef conservation planning in Pacific ocean islands. Conserv. Biol. 2010, 24:541-552.
27. Denny C.M., Willis T.J., Babcock R.C. Rapid recolonisation of snapper Pagrus auratus: Sparidae within an offshore island marine reserve after implementation of no-take status. Mar. Ecol. Prog. Ser. 2004, 272:183-190.
28. De Ruiter P.C., Wolters V., Moore J.C., Winemiller K.O. Food web ecology: playing Jenga and beyond. Science 2005, 309:68-71.
29. Doak D.F., Estes J.A., Halpern B.S., Jacob U., Lindberg D.R., Lovvorn J., Monson D.H., Tinker M.T., Williams T.M., Wootton J.T., Carroll I., Emmerson M., Miocheli F., Novak M. Understanding and predicting ecological dynamics: are major surprises inevitable?. Ecology 2008, 89:952-961.
30. 14Carbon. Fish. Bull. 2003, 101:915-922.
31. Edgar G.J., Stuart-Smith R.D. Ecological effects of marine protected areas on rocky reef communities - a continental-scale analysis. Mar. Ecol. Prog. Ser. 2009, 388:51-62.
32. Egli D.P., Babcock R.C. Ultrasonic tracking reveals multiple behavioural modes of snapper (Pagrus auratus) in a temperate no-take marine reserve. ICES J. Mar. Sci. 2004, 61:1137-1143.
33. Eggleston D.B., Parsons D.M. Disturbance-induced 'spill-in' of Caribbean spiny lobster to marine reserves. Mar. Ecol. Prog. Ser. 2008, 371:213-220.
34. Estes J., Duggins D. Sea otters and kelp forests in Alaska. Ecol. Monogr. 1995, 65:75-100.
35. Fletcher W.J. Interactions among subtidal Australian sea urchins, gastropods, and algae: effects of experimental removals. Ecol. Monogr. 1987, 57:89-109.
36. Foster B., Rattenbury J., Marbrook J. A history of biology at the University of Auckland 1883-1983 1983, University of Auckland, Auckland.
37. Freeman D.J., MacDiarmid A.B., Taylor R.B. Habitat patches that cross marine reserve boundaries: consequences for the lobster Jasus edwardsii. Mar. Ecol. Prog. Ser. 2009, 388:159-167.
38. Grace, R., Kerr, V., 2005. Intertidal and subtidal habitats of Mimiwhangata Marine Park and adjacent shelf. Department of Conservation Research & Development Series, vol. 201. Wellington, New Zealand.
39. Gratwicke B., Speight M.R. The relationship between fish species richness, abundance and habitat complexity in a range of shallow tropical marine habitats. J. Fish Biol. 2005, 66:650-667.
40. Guidetti P., Bussoti S., Boero F. Evaluating the effects of protection on fish predators and sea urchins in shallow artificial rocky habitats: a case study in the northern Adriatic Sea. Mar. Environ. Res. 2004, 59(2005):333-348.
41. Haggitt T.R., Babcock R.C. The role of grazing by the lysianassid amphipod Orchomenella aahu in dieback of the kelp Ecklonia radiata in north-eastern New Zealand. Mar. Biol. 2003, 143:1201-1211.
42. Haggitt, T.R., Kelly, S., 2004. Cape Rodney to Okakari Point Marine Reserve lobster monitoring programme: 2004 survey. Department of Conservation, Auckland. <> (01.03.12). http://www.doc.govt.nz/upload/documents/conservation/marine-and-coastal/ marine-protected-areas/report-on-lobster-monitoring.pdf.
43. Halpern B.S. The impact of marine reserves: do reserves work and does reserve size matter?. Ecol. Appl. 2003, 13:S117-S137.
44. Harborne A.R., Mumby P.J., Kappel C.V., Dahlgren C.P., Micheli F., Holmes K.E., Sanchirico J.N., Broad K., Elliott I.A., Brumbaugh D.R. Reserve effects and natural variation in coral reef communities. J. Appl. Ecol. 2008, 45:1010-1018.
45. Harborne A.R., Mumby P.J., Kappel C.V., Dahlgren C.P., Micheli F., Holmes K.E., Brumbaugh D.R. Tropical coastal habitats as surrogates of fish community structure, grazing, and fisheries value. Ecol. Appl. 2008, 18:1689-1701.
46. Hughes T.P., Bellwood D.R., Folke C., Steneck R.S., Wilson J. New paradigms for supporting the resilience of marine ecosystems. Trends Ecol. Evol. 2005, 20:380-386.
47. Hutchings J.A. Collapse and recovery of marine fishes. Nature 2000, 406:882-885.
48. Jones, G.P., Cole, R.C., Battershill, C.N., 1993. Marine reserves: do they work? In: Battershill, et al., (Eds.), Proceedings of the Second International Temperate Reef Symposium, 7-10 January 1992, Auckland, New Zealand. NIWA, Wellington, pp. 29-45.
49. Kaiser M.J., Clarke K.R., Hinz H., Austen M.C.V., Somerfield P.J., Karakassis I. Global analysis of response and recovery of benthic biotoa to fishing. Mar. Ecol. Prog. Ser. 2006, 311:1-14.
50. Kelly S., MacDiarmid A.B. Movement patterns of mature spiny lobsters, Jasus edwardsii, from a marine reserve. N.Z. J. Mar. Freshwater Res. 2003, 37:149-158.
51. Kelly S., Scott D., MacDiarmid A.B., Babcock R.C. Spiny lobster, Jasus edwardsii, recovery in New Zealand marine reserves. Biol. Conserv. 2000, 92:359-369.
52. Lafferty K.D. Fishing for lobsters indirectly increases epidemics in sea urchins. Ecol. Appl. 2004, 14:1566-1573.
53. Lafferty K.D., Shaw J.C., Kuris A.M. Reef fishes have higher parasite richness at unfished Palmyra Atoll compared to fished Kirimati Island. EcoHealth 2008, 5:338-345.
54. Langlois T.J., Ballantine W.J. Marine ecological research in New Zealand: Developing predictive models through the study of no-take marine reserves. Conserv. Biol. 2005, 19:1763-1770.
55. Langlois T.J., Anderson M.J., Babcock R.C. Reef-associated predators influence adjacent soft-sediment communities. Ecology 2005, 86:1508-1519.
56. Langlois T.J., Anderson M.J., Babcock R.C. Inconsistent effects of reefs on different size classes of macrofauna in adjacent sand habitats. J. Exp. Mar. Biol. Ecol. 2006, 334:269-282.
57. Langlois T.J., Anderson M.J., Babcock R.C., Kato S. Marine reserves demonstrate trophic interactions across habitats. Oecologia 2006, 147:134-140.
58. Lester S.E., Halpern B.S., Groud-Colvert K., Lubchenco J., Ruttenberg B.I., Gaines S.D., Airame S., Warner R.R. Biological effects within no-take marine reserves: a global synthesis. Mar. Ecol. Prog. Ser. 2009, 384:33-46.
59. Matassa C.M. Purple sea urchins Strongylocentrotus purpuratus reduce grazing rates in response to risk cues from the spiny lobster Panulirus interruptus. Mar. Ecol. Prog. Ser. 2010, 400:283-288.
60. McGlone M.S. The Polynesian settlement of New Zealand in relation to environmental and biotic changes. N.Z. J. Ecol. 1989, 12:115-129.
61. Molloy P.P., McLean I.B., Côté I.M. Effects of marine reserve age on fish populations: a global meta-analysis. J. Appl. Ecol. 2009, 46:743-751.
62. Newcombe E.M., Taylor R.B. Trophic cascade in a seaweed-epifauna-fish food chain. Mar. Ecol. Prog. Ser. 2010, 408:161-167.
63. Ortiz D.M., Tissot B.N. Ontogenic patterns of habitat use by reef-fish in a Marine Protected Area network: a multiscaled remote sensing and in situ approach. Mar. Ecol. Prog. Ser. 2008, 365:217-232.
64. Pande A., MacDiarmid A.B., Smith P.J., Davidson R.J., Cole R.G., Freeman D., Kelly S., Gardner J.P.A. Marine reserves increase the abundance and size of blue cod and lobster. Mar. Ecol. Prog. Ser. 2008, 366:147-158.
65. Parnell P.E., Dayton P.K., Lennert-Cody C., Rasmussen L.L., Leichter J.J. Marine reserve design: optimal size, habitats, species affinities, diversity and ocean microclimate. Ecol. Appl. 2006, 16:945-962.
66. Parsons D.M., Babcock R.C., Hankin R.K.S., Willis T.J., Aitken J.P., O'Dor R.K., Jackson G.D. Snapper Pagrus auratus (Sparidae) home range dynamics: acoustic tagging studies in a marine reserve. Mar. Ecol. Prog. Ser. 2003, 262:253-265.
67. Parsons D.M., Shears N.T., Babcock R.C., Haggit T.R. Fine-scale habitat change in a marine reserve, mapped using radio-acoustically positioned video transects. Mar. Freshwater Res. 2004, 55:257-265.
68. Parsons D.M., Morrison M.A., Slater M.J. Responses to marine reserves: decreased dispersion of the sparid Pagrus auratus (snapper). Biol. Conserv. 2010, 143:2039-2048.
69. Pederson H.G., Johnson C.R. Predation of the sea urchin Heliocidaris erythrogramma by rock lobsters (Jasus edwardsii) in no-take marine reserves. J. Exp. Mar. Biol. Ecol. 2006, 336:120-134.
70. Phil L., Baden S., Kautsky N., Rönnback P., Söderqvist T., Troell M., Wennhage H. Shift in fish assemblage structure due to loss of seagrass Zostera marina habitats in Sweden. Estuar. Coast. Shelf Sci. 2006, 67:123-132.
71. Remy-Zephir B., Leleu K, Grace R., Costello M.J. 2012. Geographical Information System (GIS) files of seabed habitats and biotope maps from leigh marine reserve in 1977 and 2006. doi:10.5061/dryad.6vr28.
72. Russ G.R., Alcala A.C. Natural fishing experiments in marine reserves 1983-1993: community and trophic responses. Coral Reefs 1998, 17:383-397.
73. Russ G.R., Alcala A.C. Marine reserves: long-term protection is required for full recovery of predatory fish populations. Oecologia 2004, 138:622-627.
74. Sala E., Boudouresque C.F., Harmelin-Vivien M. Fishing, trophic cascades, and the structure of algal assemblages: evaluation of an old but untested paradigm. Oikos 1998, 82:425-439.
75. Salomon A.K., Shears N.T., Langlois T.J., Babcock R.C. Cascading effects of fishing can alter carbon flow through a temperate reef ecosystem. Ecol. Appl. 2008, 18:1874-1887.
76. Salomon A.K., Gaichas S.K., Shears N.T., Smith J.E., Madin E.M.P., Gaines S.D. Key features and context-dependence of fishery-induced trophic cascades. Conserv. Biol. 2010, 24:382-394.
77. Schiel D.R. Macroalgal assemblages in New Zealand: structure, interactions and demography. Hydrobiologia 1990, 192:59-76.
78. Schiel D.R., Hickford M. Biological structure of nearshore rocky subtidal habitats in southern New Zealand. Sci. Conserv. 2001, 182:54.
79. Shears N.T., Babcock R.C. Marine reserves demonstrate top-down control of community structure on temperate reefs. Oecologia 2002, 132:131-142.
80. Shears N.T., Babcock R.C. Continuing trophic cascade effects after 25years of no-take marine reserve protection. Mar. Ecol. Prog. Ser. 2003, 246:1-16.
81. Shears N.T., Babcock R.C. Community composition and structure of shallow subtidal reefs in northeastern New Zealand. Sci. Conserv. 2004, 245:65.
82. Shears N.T., Babcock R.C. Indirect effects of marine reserve protection on New Zealand's rocky coastal marine communities. Science Internal Series 2004, vol. 192. Department of Conservation, Wellington, New Zealand.
83. Shears N.T., Babcock R.C. Quantitative description of mainland New Zealand's shallow subtidal reef communities. Sci. Conserv. 2007, 280:126.
84. Shears N.T., Babcock R.C., Duffy C.A.J., Walker J.W. Validation of qualitative habitat descriptions commonly used to classify subtidal reef assemblages in north-eastern New Zealand. N.Z. J. Mar. Freshwater Res. 2004, 38. 743-742.
85. Shears N.T., Babcock R.C., Salomon A.K. Context dependent effects of fishing: variation in trophic cascades across environmental gradients. Ecol. Appl. 2008, 18:1860-1873.
86. Steneck, R.S., 1997. Fisheries induced biological changes to the structure and function of the Gulf of Maine ecosystem. In: Wallace, G.T., Braasch, E.F. (Eds.), Proceedings of the Gulf of Maine Ecosystem Dynamics Scientific Symposium and Workshop. Regional Association for Research on the Gulf of Maine, Hanover NH: RARGOM Report, 97-1, pp. 153-167.
87. Steneck R.S. Human influences on coastal ecosystems does overfishing create trophic cascades?. Trends Ecol. Evol. 1998, 13:429-430.
88. Stewart G.B., Kaiser M.J., Côté I.M., Halpern B.S., Lester S.E., Bayliss H.R., Pullin A.S. Temperate marine reserves: global ecological effects and guidelines for future networks. Conserv. Lett. 2009, 2:243-253.
89. Taylor R.B., Cole R.G. Mobile epifauna on subtidal brown seaweeds in northeastern New Zealand. Mar. Ecol. Prog. Ser. 1994, 115:271-282.
90. Taylor, R.B., Anderson, M.J., Egli, D., Usmar, N., Willis, T.J., 2005. Cape Rodney to Okakari Point Marine Reserve fish monitoring 2005: final report. Department of Conservation, Auckland. <> (01.03.12). http://www.doc.govt.nz/upload/documents/conservation/marine-and-coastal/ crop-fish-survey-2005.pdf.
91. Tegner M.J., Dayton P.K. Ecosystem effects of fishing in kelp forest communities. ICES J. Mar. Sci. 2000, 57:579-589.
92. Tetreault I., Ambrose R.F. Temperate marine reserves enhance targeted but not untargeted fishes in multiple no-take areas. Ecol. Appl. 2007, 17:2251-2267.
93. Thrush S.F., Hewitt J.E., Funnell G.A., Cummings V.J., Ellis J., Schultz, Talley D., Norkko A. Fishing disturbance and marine biodiversity: the role of habitat structure in simple soft-sediment systems. Mar. Ecol. Prog. Ser. 2001, 223:277-286.
94. Thrush S.F., Dayton P.K. Disturbance to marine benthic habitats by trawling and dredging: implications for marine biodiversity. Annu. Rev. Ecol. Syst. 2002, 33:449-473.
95. Tilman D., Reich P.B., Knops J.M.H. Biodiversity and ecosystem stability in a decade-long grassland experiment. Science 2006, 441:629-632.
96. Ward T.J., Vanderklift M.A., Nicholls A.O., Kenchington R.A. Selecting marine reserves using habitats and species assemblages as surrogates for biological diversity. Ecol. Appl. 1999, 9:691-698.
97. Willis T.J., Millar R.B., Babcock R.C. Detection of spatial variability in relative density of fishes: comparison of visual census, angling, and baited underwater video. Mar. Ecol. Prog. Ser. 2000, 198:249-260.
98. Willis T.J., Parsons D.M., Babcock R.C. Evidence for long-term site fidelity of snapper (Pagrus auratus) within a marine reserve. N.Z. J. Mar. Freshwater Res. 2001, 35:581-590.
99. Willis T.J., Millar R.B., Babcock R.C. Protection of exploited fish in temperate regions: high density and biomass of snapper Pagrus auratus (Sparidae) in northern New Zealand marine reserves. J. Appl. Ecol. 2003, 40:214-227.
100. Wood C.L., Byers J.E., Cottingham K.L., Altman I., Donahue M.J., Blakeslee A.M.H. Parasites alter community structure. Proc. Natl. Acad. Sci. USA 2007, 104:9335-9339.
101. Wood C.L., Lafferty K.D., Micheli F. Fishing out marine parasites? Impacts of fishing on rates of parasitism in the ocean. Ecol. Lett. 2010, 13:761-775.