Abstract
Marine reserves are widely implemented worldwide to meet both conservation and fisheries management goals. This study examines the efficacy of Philippine marine reserves using meta-analysis by comparing variations in fish density (1) between reserves and adjacent fished reefs (spatial comparison), (2) within reserves before establishment relative to years following the establishment (temporal comparison), and (3) among reserves classified based on size, age, and enforcement capacity. A grand (total) mean of nineteen 22.3 ha coral reef reserves, protected for a mean duration of 8.2 years, were included in the meta-analyses. The overall density of fishes was higher in the reserves compared with the fished reefs and this difference was largely accounted for by exploited fishes. However, the overall density of fishes within the same reserves remained similar from the period before its establishment to several years following its establishment. Only the density of nonexploited fishes increased significantly during years subsequent to the establishment of the reserves. Neither age nor size of reserves correlated with pattern of change in fish density following the establishment of the reserves; however, fish density was consistently higher in larger and older reserves relative to smaller and younger reserves in the spatial comparison. Furthermore, well-enforced reserves had higher density of exploited fishes relative to less-enforced reserves in both spatial and temporal comparisons. In general, the magnitude and trajectory of change in fish density following the establishment of Philippine marine reserves are influenced by (1) functional groups of fishes under consideration, (2) size and age of the reserve, and (3) level of enforcement of the regulatory mechanisms necessary to sustain a marine reserve.
References
Alcala AC, Russ GR (2002) Status of Philippine coral reef fisheries. Asian Fish Sci 15:177–192
Alcala AC, Russ GR (2006) No-take marine reserves and reef fisheries management in the Philippines: a new people power revolution. Ambio 35:245–254
Alcala AC, Russ GR, Maypa AP, Calumpong HP (2005) A long-term, spatially replicated experimental test of the effect of marine reserves on local fish yields. Can J Fish Aquat Sci 62:98–108
Apistar DA, Diaz R, Lucas E, Raymundo D, Sabonsolin A, Tesch S (2006) Summary field report: reef monitoring survey in Gawi marine sanctuary and Sumilon island fish sanctuary, Oslob, Cebu, Philippines, 2006. The Coastal Conservation and Education Foundation Inc. (CCEF) and the Local Governance for Coastal Management Project (LGCMP), Cebu City, p 23
Apistar DA, Diaz R, Delizo D, Lucas E, Raymundo D, Sabonsolin A, Tesch S (2007) Summary field report: reef monitoring survey at Nalusuan island marine sanctuary, Cordova, Cebu, Philippines, 2007. CCEF and LGCMP, Cebu City, p 42
Arceo HO, Quibilan MC, Aliño PM, Lim G, Licuanan WY (2001) Coral bleaching in Philippine reefs: coincident evidences with mesoscale thermal anomalies. Bull Mar Sci 69:579–593
Arceo HO, Salmo SGIII, Aurellado EB, Alano HG (2005a) Balingasay marine protected area, Bolinao, Pangasinan. In: Miclat R, Sabater M, Quiblan MC, Tiquio GJ, Baria MV, Alonzo HK (eds) Reefs through time: 2004 biennial report on the status of Philippine coral reefs. Coral Reef Information Network of the Philippines (PHILREEFS) and the Marine Science Institute (MSI), University of the Philippines (UP), Diliman, Quezon City, pp 30–37
Arceo HO, Uychiaoco AJ, Nanola CL Jr (2005b) Cabacongan fish sanctuary, Loon, Bohol. In: Miclat R, Sabater M, Quiblan MC, Tiquio GJ, Baria MV, Alonzo HK (eds) Reefs through time: 2004 biennial report on the status of Philippine coral reefs. PHILREEFS and MSI, UP, Diliman, Quezon City, pp 139–144
Arceo HO, Uychiaoco AJ, Nanola CL Jr (2005c) Gilutongan marine sanctuary, Cordova, Cebu. In: Miclat R, Sabater M, Quiblan MC, Tiquio GJ, Baria MV, Alonzo HK (eds) Reefs through time: 2004 biennial report on the status of Philippine coral reefs. PHILREEFS and MSI, UP, Diliman, Quezon City, pp 79–84
Arceo HO, Uychiaoco AJ, Nanola CL Jr (2005d) Sibulan marine reserve, Sibulan, Negros oriental. In: Miclat R, Sabater M, Quiblan MC, Tiquio GJ, Baria MV, Alonzo HK (eds) Reefs through time: 2004 biennial report on the status of Philippine coral reefs. PHILREEFS and MSI, UP, Diliman, Quezon City, pp 105–109
Arceo HO, Alino PM, Gonzales RM (2008) Where are we now with marine protected areas? In: Alino PM, Geronimo RC, Mamauag SS, Gonzales RM (eds) Reefs through time 2008: initiating the state of the coasts reports. PHILREEFS, MPA Support Network, Marine Environment and Resources Foundation, Inc. (MERF) and UP-MSI, Diliman, Quezon City, pp 145–152
Barrett NS, Edgar GJ, Buxton CD, Haddon M (2007) Changes in fish assemblages following 10 years of protection in Tasmanian marine protected areas. J Exp Mar Biol Ecol 345:141–157
Botsford LW, Micheli F, Hastings A (2003) Principles for the design of marine reserves. Ecol Appl 13:S25–S31
Carpenter KE, Springer VG (2005) The center of the center of marine shore fish biodiversity: the Philippine islands. Environ Biol Fish 72:467–480
Christie P, White AT (2007) Best practices for improved governance of coral reef marine protected areas. Coral Reefs 26:1047–1056
Christie P, White A, Deguit E (2002) Starting point or solution? Community-based marine protected areas in the Philippines. J Environ Manag 66:441–454
Claudet J, Osenberg CW, Benedetti-Cecchi L, Domenici P, García-Charton JA, Perez-Ruzafa A, Badalamenti F, Bayle-Sempere J, Brito A, Bulleri F (2008) Marine reserves: size and age do matter. Ecol Lett 11:481–489
Côté IM, Mosqueira I, Reynolds JD (2001) Effects of marine reserve characteristics on the protection of fish populations: a meta-analysis. J Fish Biol 59:178–189
Edgar GJ, Barrett NS (1999) Effects of the declaration of marine reserves on Tasmanian reef fishes, invertebrates and plants. J Exp Mar Biol Ecol 242:107–144
Edgar GJ, Bustamante RH, Fariña JM, Calvopiña M, Martíez C, Toral-Granda MV (2004) Bias in evaluating the effects of marine protected areas: the importance of baseline data for the Galapagos marine reserve. Environ Conserv 31:212–218
English S, Wilkinson C, Baker V (1997) Survey manual for tropical marine resources. Australian Institute of Marine Science, Townsville, Australia
Fazey I, Salisbury JG, Lindenmayer DB, Maindonald J, Douglas R (2004) Can methods applied in medicine be used to summarize and disseminate conservation research? Environ Conserv 31:190–198
Fernandez-Duque E (1997) Comparing and combining data across studies: alternatives to significance testing. Oikos 79:616–618
Francini-Filho RB, Moura RL (2008) Evidence for spillover of reef fishes from a no-take marine reserve: an evaluation using the before-after control-impact (BACI) approach. Fish Res 93:346–356
Fretwell SD, Lucas HL Jr (1970) On territorial behaviour and other factors influencing habitat distribution in birds. I. Theoretical development. Acta Biotheor 19:16–36
Friedlander AM, Brown EK, Jokiel PL, Smith WR, Rodgers KS (2003) Effects of habitat, wave exposure, and marine protected area status on coral reef fish assemblages in the Hawaiian archipelago. Coral Reefs 22:291–305
Froese R, Pauly D (eds) (2008) FishBase. World Wide Web electronic publication. www.fishbase.org, version 02/2008
Galal N, Ormond RFG, Hassan O (2002) Effect of a network of no-take reserves in increasing catch per unit effort and stocks of exploited reef fish at Nabq, South Sinai, Egypt. Mar Freshw Res 53:199–206
Gell FR, Roberts CM (2003) Benefits beyond boundaries: the fishery effects of marine reserves. Trends Ecol Evol 18:448–455
Graham NAJ, Evans RD, Russ GR (2003) The effects of marine reserve protection on the trophic relationships of reef fishes on the Great Barrier Reef. Environ Conserv 30:200–208
Graham NAJ, McClanahan TR, MacNeil MA, Wilson SK, Polunin NVC, Jennings S, Chabanet P, Clark S, Spalding MD, Letourneur Y, Bigot L, Galzin R, Öhman M, Garpe KC, Edwards AJ, Sheppard CRC (2008) Climate warming, marine protected areas and the ocean-scale integrity of coral reef ecosystems. PLoS ONE 3(8):e3039
Guidetti P, Sala E (2007) Community-wide effects of marine reserves in the Mediterranean Sea. Mar Ecol Prog Ser 335:43–56
Guidetti P, Milazzo M, Bussotti S, Molinari A, Murenu M, Pais A, Spano N, Balzano R, Agardy T, Boero F, Carrada G, Cattaneo-Vietti R, Cau A, Chemello R, Greco S, Manganaro A, Notarbartolo di Sciara G, Russo GF, Tunesi L (2008) Italian marine reserve effectiveness: does enforcement matter? Biol Conserv 141:699–709
Halpern BS (2003) The impact of marine reserves: do reserves work and does reserve size matter? Ecol Appl 13:S117–S137
Halpern BS, Warner RR (2002) Marine reserves have rapid and lasting effects. Ecol Lett 5:361–366
Harborne AR, Mumby PJ, Kappel CV, Dahlgren CP, Micheli F, Holmes KE, Sanchirico JN, Broad K, Elliott IA, Brumbaugh DR (2008) Reserve effects and natural variation in coral reef communities. J Appl Ecol 45:1010–1018
Hastings A, Botsford LW (2003) Comparing designs of marine reserves for fisheries and for biodiversity. Ecol Appl 13:65–70
Hedges LV, Olkin I (1985) Statistical methods for meta-analysis. Academic Press, San Diego
Hutchings JA (2000) Collapse and recovery of marine fishes. Nature 406:882–885
Jennings S (2001) Patterns and prediction of population recovery in marine reserves. Rev Fish Biol Fish 10:209–231
Kulbicki M, Sarramégna S, Letourneur Y, Wantiez L, Galzin R, Mou-Tham G, Chauvet C, Thollot P (2007) Opening of an MPA to fishing: natural variations in the structure of a coral reef fish assemblage obscure changes due to fishing. J Exp Mar Biol Ecol 353:145–163
Maliao RJ, Webb EL, Jensen KR (2004) A survey of stock of the donkey’s ear abalone, Haliotis asinina L. in the Sagay marine reserve, Philippines: evaluating the effectiveness of marine protected area enforcement. Fish Res 66:343–353
Maliao RJ, Turingan RG, Lin J (2008) Phase-shift in coral reef communities in the Florida Keys National Marine Sanctuary (FKNMS), USA. Mar Biol 154:841–853
Maliao RJ, Pomeroy RS, Turingan RG (2009) Performance of community-based coastal resource management (CBCRM) programs in the Philippines: a meta-analysis. Mar Policy 33:818–825
Marcus JE, Samoilys MA, Meeuwig JJ, Villongco ZAD, Vincent ACJ (2007) Benthic status of near-shore fishing grounds in the central Philippines and associated seahorse densities. Mar Pollut Bull 54:1483–1494
McClanahan TR (2000) Recovery of a coral reef keystone predator, Balistapus undulatus, in East African marine parks. Biol Conserv 94:191–198
McClanahan TR, Graham NAJ, Calnan JM, MacNeil MA (2007) Toward pristine biomass: reef fish recovery in coral reef marine protected areas in Kenya. Ecol Appl 17:1055–1067
Micheli F, Halpern BS, Botsford LW, Warner RR (2004) Trajectories and correlates of community change in no-take marine reserves. Ecol Appl 14:1709–1723
Molloy PP, Reynolds JD, Gage MJG, Mosqueira I, Côté IM (2007) Links between sex change and fish densities in marine protected areas. Biol Conserv 14:187–197
Mora C, Andrefouet S, Costello MJ, Kranenburg C, Rollo A, Veron J, Gaston KJ, Myers RA (2006) Coral reefs and the global network of marine protected areas. Science 312:1750–1751
Mosquera I, Côté IM, Jennings S, Reynolds JD (2000) Conservation benefits of marine reserves for fish populations. Anim Conserv 3:321–332
Munday PL, Jones GP (1998) The ecological implications of small body size among coral-reef fishes. Ocean Mar Biol Ann Rev 36:373–411
Nanola CL, Arceo HO, Uychiaoco AJ (2005) Port Barton marine park, San Vicente, Palawan. In: Miclat R, Sabater M, Quiblan MC, Tiquio GJ, Baria MV, Alonzo HK (eds) Reefs through time: 2004 biennial report on the status of Philippine coral reefs. PHILREEFS and MSI, UP, Diliman, Quezon City, pp 62–67
Pauly D, Christensen V, Dalsgaard J, Froese R, Torres F Jr (1998) Fishing down marine food webs. Science 279:860
Pinnegar JK, Polunin NVC, Francour P, Badalamenti F, Chemello R, Harmelin-Vivien ML, Hereu B, Milazzo M, Zabala M, D’Anna G (2002) Trophic cascades in benthic marine ecosystems: lessons for fisheries and protected-area management. Environ Conserv 27:179–200
Pomeroy RS, Watson LM, Parks JE, Cid GA (2005) How is your MPA doing? A methodology for evaluating the management effectiveness of marine protected areas. Ocean Coast Manage 48:485–502
PROCESS (2003) Kawasihan marine sanctuary fish assessment. Participatory, Research, Organization of Communities and Education Towards Struggle for Self-Reliance (PROCESS)-Bohol Inc, Bohol
Raymundo DJC (2008) 2007 biophysical monitoring surveys in Southeast Cebu, Philippines. CCEF, Cebu City, p 14
Roberts CM (1995) Rapid build-up of fish biomass in a Caribbean marine reserve. Conserv Biol 9:815–826
Roberts CM (1997) Ecological advice for the global fisheries crisis. Trends Ecol Evol 12:35–38
Rosenberg MS, Adams DC, Gurevitch J (2000) MetaWin 2.0: statistical software for meta-analysis. Sinauer Associates, Massachusetts
Russ GR (2006) Yet another review of marine reserves as reef fishery management tools. In: Sale PF (ed) Coral reef fishes: dynamics and diversity in a complex ecosystem. Academic Press, San Diego, pp 421–443
Russ GR, Alcala AC (1996) Do marine reserves export adult fish biomass? Evidence from Apo Island, Central Philippines. Mar Ecol Prog Ser 132:1–9
Russ GR, Alcala AC (2003) Marine reserves: rates and patterns of recovery and decline of predatory fish, 1983–2000. Ecol Appl 13:1553–1565
Russ GR, Alcala AC (2004) Marine reserves: long-term protection is required for full recovery of predatory fish populations. Oecologia 138:622–627
Russ GR, Alcala AC, Maypa AP (2003) Spillover from marine reserves: the case of Naso vlamingii at Apo Island, the Philippines. Mar Ecol Prog Ser 264:15–20
Russ GR, Stockwell B, Alcala AC (2005) Inferring versus measuring rates of recovery in no-take marine reserves. Mar Ecol Prog Ser 292:1–12
Sale PF, Cowen RK, Danilowicz BS, Jones GP, Kritzer JP, Lindeman KC, Planes S, Polunin NVC, Russ GR, Sadovy YJ (2005) Critical science gaps impede use of no-take fishery reserves. Trends Ecol Evol 20:74–80
Salmo SG III, Arceo H, Pacifico KP, Aurellado EB, Alano HG (2005) Marine protected areas of Anda, Pangasinan. In: Miclat R, Sabater M, Quiblan MC, Tiquio GJ, Baria MV, Alonzo HK (eds) Reefs through time: 2004 biennial report on the status of Philippine coral reefs. PHILREEFS and MSI, UP, Diliman, Quezon City, pp 21–29
Samoilys MA, Martin-Smith KM, Giles BG, Cabrera B, Anticamara JA, Brunio EO, Vincent ACJ (2007) Effectiveness of five small Philippines’ coral reef reserves for fish populations depends on site-specific factors, particularly enforcement history. Biol Conserv 136:584–601
Underwood AJ (1994) On beyond BACI: sampling designs that might reliably detect environmental disturbances. Ecol Appl 4:3–15
Walmsley SF, White AT (2003) Influence of social, management and enforcement factors on the long-term ecological effects of marine sanctuaries. Environ Conserv 30:388–407
Wantiez L, Thollot P, Kulbicki M (1997) Effects of marine reserves on coral reef fish communities from five islands in New Caledonia. Coral Reefs 16:215–224
Webb EL, Maliao RJ, Siar SV (2004) Using local user perceptions to evaluate outcomes of protected area management in the Sagay marine reserve, Philippines. Environ Conserv 31:138–148
White AT, Vogt HP, Arin T (2000) Philippine coral reefs under threat: the economic losses caused by reef destruction. Mar Pollut Bull 40:598–605
White AT, Christie P, Apurado J, Meneses A, Ovenden M, Tesch S, White E (2002) Summary field report: coral reef monitoring in Cebu, Negros and Siquijor, Philippines, March 23–31, 2002. CCEF and the Coastal Resource Management Project (CRMP), Cebu City, p 126
White AT, Stockwell B, Meneses A, Ovenden M, Tesch S, Apurado J, White E (2003) Summary field report: coral reef monitoring in Bohol and Siquijor, Philippines, April 11–30, 2003. CCEF and CRMP, Cebu City, p 126
White AT, Meneses AT, Ovenden MF (2004) Management rating system for marine protected areas: an important tool to improve management. In: DA-BFAR (Department of Agriculture-Bureau of Fisheries, Aquatic Resources) (ed) In turbulent seas: the status of Philippine marine fisheries. CRMP, Cebu City, pp 226–231
White AT, Maypa A, Tesch S, Stockwell B, Meneses A, White E, Mueller TJ (2005) Summary field report: coral reef monitoring expedition to Mabini and Tingloy, Batangas, Philippines, March 19–27, 2005. CCEF and the Fisheries Improved for Sustainable Harvest (FISH) Project, Cebu City, p 117
White AT, Meneses A, Tesch S, Maypa A, Stockwell B, White E, Martinez R (2007) Summary field report: coral reef monitoring in Bohol, Philippines, March 26–April 3, 2007. CCEF and FISH, Cebu City, p 111
Willis TJ, Millar RB, Babcock RC, Tolimieri N (2003a) Burdens of evidence and the benefits of marine reserves: putting Descartes before des horse? Environ Conserv 30:97–103
Willis TJ, Millar RB, Babcock RC (2003b) 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 40:214–227
Acknowledgments
R. J. Maliao and A. P. Maypa are supported by the Fulbright-Philippines Agriculture Scholarship Program. Key persons contributing to the Saving Philippine Reefs project annual coral reef monitoring expeditions of the CCEF are A. P. Maypa, B. Stockwell, S. Tesch, A. Meneses, E. White, and the volunteer divers that have supported the expeditions. Thanks to A. Uychiaoco, M. Vergara, and T. Dacles for providing copies of the reports from Reefs Through Time, a biennial report on the status of Philippine coral reefs. Comments of R. van Woesik, J. Lin, E. Webb, B. Polohan, J. Kerfoot, and M. Wittenrich on earlier drafts of this manuscript are gratefully acknowledged. We are thankful to the four anonymous reviewers for their valuable comments and recommendations to improve the quality of the manuscript.
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Maliao, R.J., White, A.T., Maypa, A.P. et al. Trajectories and magnitude of change in coral reef fish populations in Philippine marine reserves: a meta-analysis. Coral Reefs 28, 809–822 (2009). https://doi.org/10.1007/s00338-009-0532-6
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DOI: https://doi.org/10.1007/s00338-009-0532-6