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Effectiveness of small locally-managed marine protected areas for coral reef fisheries management in the Philippines
Ocean and Coastal Management 179 (2019) 104831
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Effectiveness of small locally-managed marine protected areas for coral reef fisheries management in the Philippines
T
Richard N. Muallila,∗, Melchor R. Deocadezb, Renmar Jun S. Martinezb,c, Wilfredo L. Camposd, Samuel S. Mamauagb, Cleto L. Nañola Jr.e, Porfirio M. Aliñob,c Mindanao State University – Tawi-Tawi College of Technology and Oceanography, 7500, Bongao, Tawi-Tawi, Philippines Marine Environment and Resources Foundation, Inc., Marine Science Institute, University of the Philippines Diliman, 1101, Quezon City, Philippines c Marine Science Institute, University of the Philippines Diliman, 1101, Quezon City, Philippines d Division of Biological Sciences, College of Arts and Science University of the Philippines Visayas, Iloilo City, Philippines e University of the Philippines Mindanao, Mintal, Tugbok District, Davao City, Philippines a
b
A R T I C LE I N FO
A B S T R A C T
Keywords: Marine protected area Coral reef fishes Sustainable fishery Fish biomass Coral triangle
The Philippines has more than 1600 locally managed marine protected areas (MPAs), the most in the world. However, their effectiveness for coral reef fisheries management is often questionable because most of these MPAs are small and ineffectively managed. In this study, we assessed the fish biomass of commercially important coral reef fishes (e.g. surgeonfish (family Acanthuridae), parrotfish (subfamily Scarinae), snapper (family Lutjanidae), grouper (subfamily Epinephelinae), sweetlips (family Haemulidae), goatfish (Mullidae) and emperor (family Lethrinidae)) in 57 locally managed MPAs in the Philippines. We used the fish biomass level at the nationally managed, large (332.0 km2), remote, old and well enforced (i.e. strictly protected for > 20 years) Tubbataha Reefs National Marine Park (TRNMP) as a proxy for “unfished” ecosystems (Bo). We considered fish biomass levels between 25 and 50% of Bo as biomass within the maximum sustainable yield for multi-species coral reef fisheries (BMMSY) (McClanahan et al., 2014). Results showed that fish biomass levels in 7%, 25% and 68% of the surveyed MPAs were “above BMMSY”, “within BMMSY” and “below BMMSY”, respectively. None of the reefs outside MPAs was “above BMMSY”. About 86% were “below BMMSY” and the rest of the 14% of the sites outside MPAs were “within BMMSY” (14%). The mean ( ± S.E.) fish biomass levels on reefs inside and outside MPAs were only about 20.4 ± 2.2% and 10.9 ± 1.3%, respectively, of the TRNMP level. Neither size nor age of MPAs was significantly associated with fish biomass. Overall, our study showed that the current locally managed MPAs are not effective enough for coral reef fisheries management but, nonetheless, better than having no MPA at all.
1. Introduction The Philippines is situated within the Coral Triangle region, which is a major hotspot for coral reef biodiversity (Roberts et al., 2002; Halpern et al., 2008; Burke et al., 2012). The Philippines has the highest concentration of fish species per unit area and is considered as the center of the center of marine shore-fish diversity (Carpenter and Springer, 2005). Unfortunately, anthropogenic disturbances from an expanding and highly resource dependent population are seriously threatening the rich biodiversity of coral reef ecosystems (Burke et al., 2012; Cabral et al., 2013, Muallil et al., 2014a and 2014b). Habitat destruction and signs of overfishing such as local extinctions (Nañola et al., 2011), disappearance of large predatory fishes from catches (Lavides et al., 2010), severe reduction in catch per unit effort (Muallil ∗
et al., 2014b), and very low to zero catches (Muallil et al., 2014a) have been increasingly reported in the country. Establishment of marine protected areas (MPAs) has been among the major initiatives for coral reef conservation and fisheries management in the Philippines (Russ, 2002; White et al., 2014). An MPA is a “generic term for a defined area of the sea established and set aside by law, administrative regulation, or any other effective means, in order to conserve and protect a part of or the entire enclosed environment, through the establishment of management guidelines” (White et al., 2014). In the Philippines, MPAs can be generally classified, based on governance levels, into nationally managed MPAs (established through the Republic Act 7586 or National Integrated Protected Area System (NIPAS) Act of 1992) and locally managed MPAs (established through the Republic Act 8550 or the Fisheries Code of 1998). There are at least
Corresponding author. E-mail address: [email protected] (R.N. Muallil).
https://doi.org/10.1016/j.ocecoaman.2019.104831 Received 12 January 2019; Received in revised form 19 May 2019; Accepted 21 May 2019 0964-5691/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. Map of the Philippines showing the six biogeographic regions of the Pilippines, the Tubbataha Reef National Marine Park (TRNMP) and the 57 study sites (municipality/city).
28 nationally managed MPAs, covering about 14,500 km2 and 1600 locally managed MPAs, covering about 240 km2 (White et al., 2014) in the country. Roughly, the average size of each MPA is about 518.86 km2 for nationally managed MPAs and 0.15 km2 for locally managed MPAs. In this study, we assessed the effectiveness of the small locally managed MPAs for coral reef fisheries management by comparing them to the well-protected nationally managed Tubbataha Reef National Marine Park (TRNMP).
0.57.0 ( ± 0.07) km2, mostly with less than 0.10 km2 no take zone), relatively new (mean age, 10 years old) and located in populated areas where fishing is a major source of livelihood (Muallil et al., 2014a) (see Table 1). 2.2. Data collection A modified non-destructive fish visual census (FVC) (English et al., 1997) was conducted on 4–12 10 m × 50 m belt transects for the locally managed MPAs, half of which were established inside MPAs and the other half on adjacent reefs outside MPAs, which were at least 200 m away from the boundaries of MPAs. Thirty-three transects with the same dimension were surveyed for the nationally managed TRNMP. The transects were established on upper reef slope, mostly with depths ranging from 5 to 10 m. FVC was performed by swimming slowly and stopping every 5 m to record all the fish within a 10 m - wide belt. Surveys were conducted by six professional divers who have been actively performing FVC surveys in the Philippines for more than a decade already. All surveys were conducted from 2010 to 2014 for the locally managed MPAs and 2006–2009 for TRNMP between 9:00–16:00 h. All the fish were counted, identified to the species level and total length (TL) estimated to the nearest centimeter. Some fishes were identifiable to genus level only. Fish biomass was estimated using the relationship between length (L) and weight (W) with equation W = aLb.
2. Materials and methods 2.1. Study sites The surveys were conducted on coral reefs in 58 sites from 57 coastal municipalities/cities and 20 provinces covering all the six biogeographic regions of the Philippines (Fig. 1; Table 1). Only the Tubbataha Reef National Marine Park (TRNMP), was managed by the national government. The rest were co-managed by the local communities and their respective Local Government Units (LGUs). The TRNMP is an offshore reef located in the middle of the Sulu Sea and far from human settlements. It is also a large coral reef complex with a total area 332.0 km2 and has been strictly protected by the government for over 20 years already (White and Ovenden, 2007). On the other hand, the locally-managed MPAs were generally small (i.e. mean ( ± SE) of 2
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Table 1 The study sites showing the size and age of the MPAs and the number of transects surveyed in each site. No.
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58
Municipality/City
San Fernando City Alaminos City Bolinao Candelaria Masinloc Calatagan Mabini Tingloy Puerto Galera El Nido Dipaculao San Luis Siruma Tinambac Tigaon Sagnay Caramoan Bacacay Gubat Matnog Hinunangan San Francisco Cantilan Lanuza Cortes Lianga Marihatag Mati City Roxas Bulalacao Siaton Bongao Panglima Sugala Simunul Calapan City Naujan Pola Gloria Bongabong Mansalay Bulan Ayungon Bindoy Amlan San Francisco Pilar Boljoon Ubay Inabanga Tagbilaran City Panabo City IGACOS IGACOS Dumalinao Tabina Tukuran Ipil Cagayancillo
Province
La Union Pangasinan Pangasinan Zambales Zambales Batangas Batangas Batangas Oriental Mindoro Palawan Aurora Aurora Camarines Sur Camarines Sur Camarines Sur Camarines Sur Camarines Sur Albay Sorsogon Sorsogon Leyte Leyte Surigao del Sur Surigao del Sur Surigao del Sur Surigao del Sur Surigao del Sur Davao Oriental Palawan Oriental Mindoro Negros Oriental Tawi-Tawi Tawi-Tawi Tawi-Tawi Oriental Mindoro Oriental Mindoro Oriental Mindoro Oriental Mindoro Oriental Mindoro Oriental Mindoro Sorsogon Negros Oriental Negros Oriental Negros Oriental Cebu Cebu Cebu Bohol Bohol Bohol Davao del Norte Davao del Norte Davao del Norte Zamboanga del Sur Zamboanga del Sur Zamboanga del Sur Zamboanga Sibugay Palawan
Size (km2)
Name of MPA
Kasay Telbang Balingasay Sinacaban-Malimanga San Salvador Pyramid Twin Rocks Pulang Buli Clam Shell Tres Marias Mabuno Kabulonan Sapinetan Caloco Tigaon Atulayan Gata Uson Bagacay Subic San Pablo Punta Ayoke Lanuza Uba Cagana Umangon Tamisan Caramay Balatasan Andulay Pababag Batu-Batu Kulape Doh Tong Harka Piloto Masaguing St. John the Baptish Agsalin Masaguisi Palaypay Butag Iniban Mantalip Tandayag Santiago Pilar Arbor Sinandigan Hambongan Mabaw Cagangohan Dapia Sanipaan Bibilik Tambunan Sugod Tagulo Buluan TRNMP
0.30 0.34 0.24 1.90 1.27 0.60 0.23 0.03 2.50 0.08 0.58 0.80 0.57 0.50 0.18 0.70 0.38 0.45 0.40 1.38 0.35 0.10 0.23 0.50 0.30 0.44 1.50 0.11 1.00 1.79 0.06 0.69 0.52 0.45 0.37 0.30 0.49 0.80 0.21 0.83 0.40 0.28 0.46 0.06 0.19 0.11 0.09 0.52 0.14 0.02 0.53 0.22 1.58 0.20 1.04 1.60 0.82 332.00
Year Established
2006 1993 1997 2003 1989 1999 1991 2002 2006 2007 2005 1998 1994 2006 2009 1993 2011 2002 2012 2005 2003 1997 2005 2002 2005 2002 2001 2005 2004 1993 1996 2005 2005 2005 2003 2006 2010 2003 2003 2006 1999 2008 2006 1996 2006 2007 2001 2004 1999 2000 2003 2010 2010 2002 2003 2003 2004 1988
Year surveyed
2013 2013 2012 2011 2010 2013 2013 2013 2014 2011 2010 2010 2012 2012 2012 2012 2012 2012 2012 2013 2012 2012 2012 2012 2012 2012 2012 2012 2012 2014 2013 2010 2010 2010 2014 2014 2014 2014 2014 2014 2013 2012 2012 2012 2012 2012 2012 2012 2012 2012 2012 2012 2012 2010 2011 2011 2012 2006–2009
No. of transects Surveyed (n) Inside MPAs
Outside MPA
4 5 4 6 4 5 4 4 3 4 2 2 5 5 3 5 4 4 5 4 5 5 4 5 5 5 4 5 4 3 4 3 3 3 3 3 3 3 3 3 5 5 5 5 5 5 5 5 5 5 4 5 5 2 4 4 5 33
4 5 4 6 4 5 4 4 3 4 2 2 5 5 3 5 4 4 5 4 5 5 4 5 5 5 4 5 4 3 4 3 3 3 3 3 3 3 3 3 5 5 5 5 5 5 5 5 5 5 4 5 5 2 4 4 5 NA
These fish families constitute the major coral reef demersal fish caught by small-scale fishers in the Philippines (Muallil et al., 2014a). We opted to use this simple classification since fishers in the Philippines have been increasingly becoming less selective in their target species, which makes it difficult to classify each species as commercially important or not (Muallil et al., 2014b). The date of establishment and size of MPAs were gathered from the local records of the respective LGU or management body. These data are also available in the MPA database which is maintained by the Marine Science Institute, University of the Philippines Diliman (Cabral
Species specific a and b values were gathered from published records (Froese and Pauly, 2011; Kulbicki et al., 2005). The a and b values used for fishes identified to the genus level only were the average values for the genus. Classification of fish was based on Muallil et al. (2015), wherein only the surgeonfish (family Acanthuridae excluding genus Zebrasoma), parrotfish (subfamily Scarinae, family Labridae), snapper (family Lutjanidae), grouper (subfamily Epinephelinae, family Serranidae), goatfish (family Mullidae), sweetlips (family Haemulidae) and emperor (family Lethrinidae) were considered as commercially important fishes. 3
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biomass on reefs inside MPAs. Moreover, the estimate can still be conservative as the overall fish biomass of about 106.5 mt/km2 recorded in the TRNMP, which was used as the proxy for unfished biomass (Bo), is lower than the estimated 120 mt/km2 fish biomass for pristine reefs in the Indo-Pacific (McClanahan et al., 2014). The extent of overfishing in Philippine coral reef fisheries as shown in this study is much worse than previously estimated (Muallil et al., 2014a) where only about 68% of coastal fishing grounds in the country are overfished. The previous study was based on a bioeconomic model using data from interviews that did not account for IUU (illegal, unreported and unregulated) fishing which is still rampant in many areas in the Philippines (Muallil et al., 2014a, 2014b). Our study supports the findings that many fisheries worldwide have already been severely depleted where fish stocks have been reduced to less than 10% of the unfished levels (Green et al., 2003; Myers and Worm, 2003; Worm et al., 2006). Age and size of the MPAs were not significantly correlated with fish biomass levels which contradict the results of some studies showing higher fish biomass in older and bigger MPAs. For example, Maliao et al., (2009) showed higher fish density in older and larger MPAs based on the metaanalysis of 19 MPAs in the country. However, their study included only well enforced MPAs (e.g. at least level 2 or established/ fair) in central Philippines. On the contrary, the management levels of most of the MPAs in our study were still at level 0 or have not been assessed at all at the time of the study. There are also studies which showed increased in fish biomass in small locally managed MPAs after decades of strict enforcement (Russ and Alcala, 2003; Abesamis et al., 2006) but these are rather exceptional cases as most of the MPAs in the country are not effectively managed (Arceo et al., 2008; Maypa et al., 2012; PhilReefs, 2014). Generally, the MPAs in the Philippines are too small and fishing pressure from the highly fishery-dependent coastal ommunities is high and increasing (Weeks et al., 2010; Edgar et al., 2014; Green et al., 2014; Muallil et al., 2014a). The mean ( ± SE) size of about 0.57 ± 0.07 km2 of the MPAs in this study is much smaller than the suggested size of at least 10.0 km2 for an MPA to be effective for coral reef fishes conservation (Weeks et al., 2010). Fishing pressure alone from the almost two million small-scale fishers could easily deplete the coastal fisheries (Newton et al., 2007; Muallil et al., 2014a). In addition, the prevalence of blast, poison and other forms of illegal fishing practices in many areas in the country could further worsen the impact of overfishing and hamper fish stocks recovery (Muallil et al., 2014a, 2014b). Management effectiveness and the level of compliance play an important role in successful MPAs (Bergseth et al., 2015). Unfortunately, the sustainability of MPA management in the Philippines is a major problem due to lack of sustainable financing (Senga, 2001; Maypa et al., 2012). Reefbase (2015) reported that more than half (54%) of the MPAs had not progressed beyond the implementation phase. Many of the MPAs in the country benefit from the generous support of non-government organizations (NGOs), particularly in terms of technical and logistical support, including livelihood programs for the displaced fishers, that usually last for 3–5 years. The Philippine law as per RA 8550 or the Fisheries Code of 1998, which has been recently ammended to RA 10654, devolved the management of municipal waters, i.e., the area from the shore up to 15 km seaward, and all the coastal ecosystems within it to the local government units (LGUs). The LGUs are required to protect at least 15% of the municipal waters. However, the LGUs often have limited resources and the technical capability to do the job. In addition, many LGUs do not have the political will to strictly enforce MPA laws because of fear of being not voted for in the election by the affected community. Thus, without external support, the LGU-managed MPAs are often not sustainable and eventually become mere “paper” MPAs in the long run (De Jesus et al., 2013; Reefbase, 2015).
et al., 2014). 2.3. Analyses Shapiro-Wilk's test for normality revealed that the fish biomass data were not normally distributed (P < 0.001) (Annex 1). Fish biomass values were square root transformed and the generalized linear mixed model with gaussian distribution family was used to compare fish biomass levels between reefs inside and outside MPAs, with study sites as the random factor. Fish biomass levels were also assessed using the modified exploitation levels proposed by McClanahan et al. (2014) for multi-species coral reef fisheries. Here, fish biomass (B) levels between 25 and 50% of the unfished levels (Bo) was considered as the biomass within the multi-species maximum sustainable yield (BMMSY) level. In our study, we used three levels of exploitation, namely, (i) “above BMMSY” (B > 50% of BO), (ii) “within BMMSY” (B = 25–50% of BO), and (iii) “below BMMSY” (B < 25% of BO). Due to unavailability of baseline information, we opted to use the biomass level of coral reefs at the Tubbataha Reefs National Marine Park (TRNMP), which is arguably the most effectively managed MPA in the country, as the proxy for “unfished” ecosystems (BO). We further determined whether fish biomass is influenced by size or age of MPAs using a generalized linear model with fish biomass as the dependent variable and size and age of MPAs as independent variables. Statistical analyses were implemented using RStudio statistical analysis software version 1.2.1335 (2009–2019 RStudio, Inc). 3. Results Overall, the highest fish biomass was recorded at the TRNMP which had a mean ( ± S.E.) biomass of 106.5 ± 16.2 mt/km2. The seven commercially important coral reef fish groups considered in the study had a biomass of 55.1 ± 7.5 mt/km2 which constituted about 51.7% of the overall fish biomass. Using the fish biomass at the TRNMP as the proxy for “unfished” coral reefs, only four of the 57 (7.0%) of surveyed MPAs had fish biomass of “above BMMSY”, i.e. more than 50% of the TRNMP level (Fig. 2 ). Fish biomass in 13 of the MPAs (22.8%) were “within BMMSY”, i.e. 25–50% of the TRNMP level, and fish biomass in the remaining 40 MPAs (70.2%) were “below BMMSY”, i.e. less than 25% of the TRNMP level. None of the reefs outside MPAs had fish biomass “above BMMSY”. Fish biomass levels in six sites (10.5%) were “within BMMSY” while the other 51 sites (89.5%) outside MPA were all “below BMMSY”. The mean ( ± S.E.) fish biomass levels on reefs inside and outside MPAs were only about 20.4 ± 2.2% and 10.9 ± 1.3%, respectively, of the TRNMP level. Surgeonfish (family Acanthuridae), followed by parrotfish (subfamily Scarinae) and snappers (family Lutjanidae) had the highest fish biomass both inside and outside MPAs (Fig. 3). Surgeonfish and parrotfish consistently had the highest fish biomass but their proportion relative to other fish groups decreased as overall fish biomass level increased from overfished to unfished or pristine level (Fig. 3). Except for the sweetlips (family Haemulidae) (P = 0.07), the biomass levels of other fish groups studies were significantly higher inside MPAs than outside MPAs (P < 0.05) (Annex 2). Neither size nor age of MPAs showed a significant relationship with fish biomass inside MPAs (Annexes 3 and 4). 4. Discussion Fish biomass of commercially important coral reef fishes is generally very low indicating the highly overfished state of Philippine coral reefs. Using the biomass thresholds proposed by McClanahan et al. (2014) for coral reef fisheries, our study showed that overfishing is evident even inside MPAs, which has a fish biomass of only about 20.4% of the TRNMP level. Coral reefs outside MPAs had only about half of the fish 4
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Fig. 2. Levels of exploitation rate based on fish biomass levels on reefs in the Philippines relative to the TRNMP level, which was used as the proxy for unfished level. A. inside MPA and B. outside MPAs. Blue, “above BMMSY” where B > 50% of TRNMP; Green, “within BMMSY” where B = 25–50% of TRNMP); Red, “below BMMSY” where B < 25% of TRNMP. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
5. CONCULUSION and recommendations
2014) which means that more than 95% of the coral reefs in the country are at high risk of further exploitation from the nearly two million fishers in the country. Other complementary initiatives aside from MPAs that are geared towards reducing fishing pressure and eliminating IUU fishing are needed for effective coral reef fisheries management in the Philippines. As pointed out in Muallil et al. (2015), the current MPAs in the country may, at best, work in delaying fast extirpation of commercially important coral reef fishes. Nonetheless, the higher fish biomass on reefs inside than outside MPAs indicate that having MPAs is better than
Our study showed the highly overfished state of the Philippine coral reef fisheries which coroborate the results of various localized studies conducted independently in the country (PhilReefs, 2008 and 2014). Generally, fish biomass is slightly better inside MPAs but still fell within the overfished state indicating that the existing MPAs, which are mostly small and ineffectively managed, are not working well as far as coral reef fisehries management is concern. Moreover, the MPAs cover only less than 5% of the total coral reef area in the country (White et al.,
Fig. 3. Patterns in community assemblages of commercially important coral reef fishes across total biomass range (i.e. from overfished to unfished levels). Fish assemblages inside and outside MPAs are also shown. 5
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having no MPAs at all. With the increasing coastal population and the advancement in fishing technology (Anticamara et al., 2001; Teh et al., 2013), effectively enforced MPAs may be among the few remaining unfished areas left in the Philippines that can sustain coral reef fisheries through the spillover effect of adult fishes or through the recruitment effect as a source of fish larvae (Abesamis et al., 2017). The study though was mainly based on McClanahan et al. (2014) which assumes that fish biomass levels reflect the level of fishing intensity. However, environmental factors such as island geomorphologies (Sandin et al., 2008), benthic characteristics (Taylor et al., 2015; Russ et al., 2015), water quality and productivity (Sandin et al., 2008) and connectivity with adjacent habitats (Olds et al., 2012) are also known to affect reef fish assemblages. Our study covers all the six biogeographic regions of the Philippines where other factors aside from fishing vary among the study sites. With climate change, the impact of environmental factors is expected to become increasingly more important in driving coral reef fisheries (Munday et al., 2008). Thus, future studies need to investigate how different factors apart from fishing drive coral reef fisheries in order to better understand and ensure its long-term sustainability which supports the livelihood of millions of people living in coastal areas in the country.
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Ethical statement All authors have contributed to this study. Below are the specific contributions of each author: Richard N. Muallil: Designed the study, Analysed the data, Wrote the manuscript. Melchor R. Deocadez: Collected the data, Analysed the data, Provided inputs to the manuscript. Renmar Jun S. Martinez: Collected the data, Analysed the data, Provided inputs to the manuscript. Wilfredo L. Campos: Designed the study, Provided inputs to the manuscript. Samuel S. Mamauag, Designed the study, Provided inputs to the manuscript. Cleto L. Nañola Jr.: Provided inputs to the manuscript. Porfirio Aliño: Designed the study, Wrote the manuscript. Acknowledgements This study is an output of various projects of the Coral Reefs and Community Ecology (COMECO) laboratory at the Marine Science Institute of the University of the Philippines conducted from 2006 to 2014. These projects were funded by the United States Agency for International Development, The Deutsche Gesellschaft für Internationale Zusammenarbeit (GIZ), the Department of Environment and Natural Resources (DENR) of the Philippines and the Department of Science and Tecnology (DOST) of the Philippines. We would also like to thank the two anonymous reviewers who provided valuable comments that greatly improved our manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.lwt.2019.05.053. References Abesamis, R.A., Russ, G.R., Alcala, A.C., 2006. Gradients of abundance of fish across no‐take marine reserve boundaries: evidence from Philippine coral reefs. Aquat. Conserv. 16 (4), 349–371. Abesamis, R.A., Saenz-Agudelo, P., Berumen, M.L., Bode, M., Jadloc, C.R.L., Solera, L.A., Villanoy, C.L., Bernardo, L.P.C., Alcala, A.C., Russ, G.R., 2017. Reef-fish larval dispersal patterns validate no-take marine reserve network connectivity that links human communities. Coral Reefs 36 (3), 791–801. Arceo, H.O., Aliño, P.M., Gonzales, R.O.M., 2008. Where are we now with marine protected areas? In: Reefs through Time: Initiating the State of the Coasts Reports. Coral Reef Information Network of the Philippines (PhilReefs), MPA Support Network. Marine Environment & Resources Foundation, Inc. and the Marine Science Institute, University of the Philippines, Quezon City, pp. 145–152. Anticamara, J.A., Watson, R., Gelchu, A., Pauly, D., 2001. Global fishing effort (19502010): trends, gaps, and implications. Fish. Res. 107, 131–136.
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parrotfish communities. Ecography 38 (5), 520–530. Teh, L.S., Teh, L.C., Sumaila, U.R., 2013. A global estimate of the number of coral reef Fishers. PLoS One 8 (6) e65397. Weeks, R., Russ, G.R., Alcala, A.C., White, A.T., 2010. Effectiveness of marine protected areas in the Philippines for biodiversity conservation. Conserv. Biol. 24 (2), 531–540. White, A.T., Aliño, P.M., Cros, A., Fatan, N.A., Green, A.L., Teoh, S.J., et al., 2014. Marine protected areas in the Coral Triangle: progress, issues, and options. Coast. Manag. 42 (2), 87–106. White, A.T., Ovenden, M., 2007. Tubbataha Reef National Marine Park in Palawan. Philippine Coral Reefs through Time. pp. 144. Worm, B., Barbier, E.B., Beaumont, N., Duffy, J.E., Folke, C., Halpern, B.S., et al., 2006. Impacts of biodiversity loss on ocean ecosystem services. Science 314, 787–790.
Tools. Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem. Academic Press, San Diego, California, USA, pp. 421–443. Russ, G.R., Alcala, A.C., 2003. Marine reserves: rates and patterns of recovery and decline of predatory fish, 1983–2000. Ecol. Appl. 13 (6), 1553–1565. Russ, G.R., Miller, K.I., Rizzari, J.R., Alcala, A.C., 2015. Long-term no-take marine reserve and benthic habitat effects on coral reef fishes. Mar. Ecol. Prog. Ser. 29, 233–248. Sandin, S.A., Vermeij, M.J., Hurlbert, A.H., 2008. Island biogeography of Caribbean coral reef fish. Glob. Ecol. Biogeogr. 17 (6), 770–777. Senga, R.G., 2001. Establishing protected areas in the Philippines: emerging trends, challenges and prospects. George Wright Forum 18 (2), 56–65. Taylor, B.M., Lindfield, S.J., Choat, J.H., 2015. Hierarchical and scale‐dependent effects of fishing pressure and environment on the structure and size distribution of
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Contents lists available at ScienceDirect
Ocean and Coastal Management journal homepage: www.elsevier.com/locate/ocecoaman
Effectiveness of small locally-managed marine protected areas for coral reef fisheries management in the Philippines
T
Richard N. Muallila,∗, Melchor R. Deocadezb, Renmar Jun S. Martinezb,c, Wilfredo L. Camposd, Samuel S. Mamauagb, Cleto L. Nañola Jr.e, Porfirio M. Aliñob,c Mindanao State University – Tawi-Tawi College of Technology and Oceanography, 7500, Bongao, Tawi-Tawi, Philippines Marine Environment and Resources Foundation, Inc., Marine Science Institute, University of the Philippines Diliman, 1101, Quezon City, Philippines c Marine Science Institute, University of the Philippines Diliman, 1101, Quezon City, Philippines d Division of Biological Sciences, College of Arts and Science University of the Philippines Visayas, Iloilo City, Philippines e University of the Philippines Mindanao, Mintal, Tugbok District, Davao City, Philippines a
b
A R T I C LE I N FO
A B S T R A C T
Keywords: Marine protected area Coral reef fishes Sustainable fishery Fish biomass Coral triangle
The Philippines has more than 1600 locally managed marine protected areas (MPAs), the most in the world. However, their effectiveness for coral reef fisheries management is often questionable because most of these MPAs are small and ineffectively managed. In this study, we assessed the fish biomass of commercially important coral reef fishes (e.g. surgeonfish (family Acanthuridae), parrotfish (subfamily Scarinae), snapper (family Lutjanidae), grouper (subfamily Epinephelinae), sweetlips (family Haemulidae), goatfish (Mullidae) and emperor (family Lethrinidae)) in 57 locally managed MPAs in the Philippines. We used the fish biomass level at the nationally managed, large (332.0 km2), remote, old and well enforced (i.e. strictly protected for > 20 years) Tubbataha Reefs National Marine Park (TRNMP) as a proxy for “unfished” ecosystems (Bo). We considered fish biomass levels between 25 and 50% of Bo as biomass within the maximum sustainable yield for multi-species coral reef fisheries (BMMSY) (McClanahan et al., 2014). Results showed that fish biomass levels in 7%, 25% and 68% of the surveyed MPAs were “above BMMSY”, “within BMMSY” and “below BMMSY”, respectively. None of the reefs outside MPAs was “above BMMSY”. About 86% were “below BMMSY” and the rest of the 14% of the sites outside MPAs were “within BMMSY” (14%). The mean ( ± S.E.) fish biomass levels on reefs inside and outside MPAs were only about 20.4 ± 2.2% and 10.9 ± 1.3%, respectively, of the TRNMP level. Neither size nor age of MPAs was significantly associated with fish biomass. Overall, our study showed that the current locally managed MPAs are not effective enough for coral reef fisheries management but, nonetheless, better than having no MPA at all.
1. Introduction The Philippines is situated within the Coral Triangle region, which is a major hotspot for coral reef biodiversity (Roberts et al., 2002; Halpern et al., 2008; Burke et al., 2012). The Philippines has the highest concentration of fish species per unit area and is considered as the center of the center of marine shore-fish diversity (Carpenter and Springer, 2005). Unfortunately, anthropogenic disturbances from an expanding and highly resource dependent population are seriously threatening the rich biodiversity of coral reef ecosystems (Burke et al., 2012; Cabral et al., 2013, Muallil et al., 2014a and 2014b). Habitat destruction and signs of overfishing such as local extinctions (Nañola et al., 2011), disappearance of large predatory fishes from catches (Lavides et al., 2010), severe reduction in catch per unit effort (Muallil ∗
et al., 2014b), and very low to zero catches (Muallil et al., 2014a) have been increasingly reported in the country. Establishment of marine protected areas (MPAs) has been among the major initiatives for coral reef conservation and fisheries management in the Philippines (Russ, 2002; White et al., 2014). An MPA is a “generic term for a defined area of the sea established and set aside by law, administrative regulation, or any other effective means, in order to conserve and protect a part of or the entire enclosed environment, through the establishment of management guidelines” (White et al., 2014). In the Philippines, MPAs can be generally classified, based on governance levels, into nationally managed MPAs (established through the Republic Act 7586 or National Integrated Protected Area System (NIPAS) Act of 1992) and locally managed MPAs (established through the Republic Act 8550 or the Fisheries Code of 1998). There are at least
Corresponding author. E-mail address: [email protected] (R.N. Muallil).
https://doi.org/10.1016/j.ocecoaman.2019.104831 Received 12 January 2019; Received in revised form 19 May 2019; Accepted 21 May 2019 0964-5691/ © 2019 Elsevier Ltd. All rights reserved.
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Fig. 1. Map of the Philippines showing the six biogeographic regions of the Pilippines, the Tubbataha Reef National Marine Park (TRNMP) and the 57 study sites (municipality/city).
28 nationally managed MPAs, covering about 14,500 km2 and 1600 locally managed MPAs, covering about 240 km2 (White et al., 2014) in the country. Roughly, the average size of each MPA is about 518.86 km2 for nationally managed MPAs and 0.15 km2 for locally managed MPAs. In this study, we assessed the effectiveness of the small locally managed MPAs for coral reef fisheries management by comparing them to the well-protected nationally managed Tubbataha Reef National Marine Park (TRNMP).
0.57.0 ( ± 0.07) km2, mostly with less than 0.10 km2 no take zone), relatively new (mean age, 10 years old) and located in populated areas where fishing is a major source of livelihood (Muallil et al., 2014a) (see Table 1). 2.2. Data collection A modified non-destructive fish visual census (FVC) (English et al., 1997) was conducted on 4–12 10 m × 50 m belt transects for the locally managed MPAs, half of which were established inside MPAs and the other half on adjacent reefs outside MPAs, which were at least 200 m away from the boundaries of MPAs. Thirty-three transects with the same dimension were surveyed for the nationally managed TRNMP. The transects were established on upper reef slope, mostly with depths ranging from 5 to 10 m. FVC was performed by swimming slowly and stopping every 5 m to record all the fish within a 10 m - wide belt. Surveys were conducted by six professional divers who have been actively performing FVC surveys in the Philippines for more than a decade already. All surveys were conducted from 2010 to 2014 for the locally managed MPAs and 2006–2009 for TRNMP between 9:00–16:00 h. All the fish were counted, identified to the species level and total length (TL) estimated to the nearest centimeter. Some fishes were identifiable to genus level only. Fish biomass was estimated using the relationship between length (L) and weight (W) with equation W = aLb.
2. Materials and methods 2.1. Study sites The surveys were conducted on coral reefs in 58 sites from 57 coastal municipalities/cities and 20 provinces covering all the six biogeographic regions of the Philippines (Fig. 1; Table 1). Only the Tubbataha Reef National Marine Park (TRNMP), was managed by the national government. The rest were co-managed by the local communities and their respective Local Government Units (LGUs). The TRNMP is an offshore reef located in the middle of the Sulu Sea and far from human settlements. It is also a large coral reef complex with a total area 332.0 km2 and has been strictly protected by the government for over 20 years already (White and Ovenden, 2007). On the other hand, the locally-managed MPAs were generally small (i.e. mean ( ± SE) of 2
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Table 1 The study sites showing the size and age of the MPAs and the number of transects surveyed in each site. No.
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58
Municipality/City
San Fernando City Alaminos City Bolinao Candelaria Masinloc Calatagan Mabini Tingloy Puerto Galera El Nido Dipaculao San Luis Siruma Tinambac Tigaon Sagnay Caramoan Bacacay Gubat Matnog Hinunangan San Francisco Cantilan Lanuza Cortes Lianga Marihatag Mati City Roxas Bulalacao Siaton Bongao Panglima Sugala Simunul Calapan City Naujan Pola Gloria Bongabong Mansalay Bulan Ayungon Bindoy Amlan San Francisco Pilar Boljoon Ubay Inabanga Tagbilaran City Panabo City IGACOS IGACOS Dumalinao Tabina Tukuran Ipil Cagayancillo
Province
La Union Pangasinan Pangasinan Zambales Zambales Batangas Batangas Batangas Oriental Mindoro Palawan Aurora Aurora Camarines Sur Camarines Sur Camarines Sur Camarines Sur Camarines Sur Albay Sorsogon Sorsogon Leyte Leyte Surigao del Sur Surigao del Sur Surigao del Sur Surigao del Sur Surigao del Sur Davao Oriental Palawan Oriental Mindoro Negros Oriental Tawi-Tawi Tawi-Tawi Tawi-Tawi Oriental Mindoro Oriental Mindoro Oriental Mindoro Oriental Mindoro Oriental Mindoro Oriental Mindoro Sorsogon Negros Oriental Negros Oriental Negros Oriental Cebu Cebu Cebu Bohol Bohol Bohol Davao del Norte Davao del Norte Davao del Norte Zamboanga del Sur Zamboanga del Sur Zamboanga del Sur Zamboanga Sibugay Palawan
Size (km2)
Name of MPA
Kasay Telbang Balingasay Sinacaban-Malimanga San Salvador Pyramid Twin Rocks Pulang Buli Clam Shell Tres Marias Mabuno Kabulonan Sapinetan Caloco Tigaon Atulayan Gata Uson Bagacay Subic San Pablo Punta Ayoke Lanuza Uba Cagana Umangon Tamisan Caramay Balatasan Andulay Pababag Batu-Batu Kulape Doh Tong Harka Piloto Masaguing St. John the Baptish Agsalin Masaguisi Palaypay Butag Iniban Mantalip Tandayag Santiago Pilar Arbor Sinandigan Hambongan Mabaw Cagangohan Dapia Sanipaan Bibilik Tambunan Sugod Tagulo Buluan TRNMP
0.30 0.34 0.24 1.90 1.27 0.60 0.23 0.03 2.50 0.08 0.58 0.80 0.57 0.50 0.18 0.70 0.38 0.45 0.40 1.38 0.35 0.10 0.23 0.50 0.30 0.44 1.50 0.11 1.00 1.79 0.06 0.69 0.52 0.45 0.37 0.30 0.49 0.80 0.21 0.83 0.40 0.28 0.46 0.06 0.19 0.11 0.09 0.52 0.14 0.02 0.53 0.22 1.58 0.20 1.04 1.60 0.82 332.00
Year Established
2006 1993 1997 2003 1989 1999 1991 2002 2006 2007 2005 1998 1994 2006 2009 1993 2011 2002 2012 2005 2003 1997 2005 2002 2005 2002 2001 2005 2004 1993 1996 2005 2005 2005 2003 2006 2010 2003 2003 2006 1999 2008 2006 1996 2006 2007 2001 2004 1999 2000 2003 2010 2010 2002 2003 2003 2004 1988
Year surveyed
2013 2013 2012 2011 2010 2013 2013 2013 2014 2011 2010 2010 2012 2012 2012 2012 2012 2012 2012 2013 2012 2012 2012 2012 2012 2012 2012 2012 2012 2014 2013 2010 2010 2010 2014 2014 2014 2014 2014 2014 2013 2012 2012 2012 2012 2012 2012 2012 2012 2012 2012 2012 2012 2010 2011 2011 2012 2006–2009
No. of transects Surveyed (n) Inside MPAs
Outside MPA
4 5 4 6 4 5 4 4 3 4 2 2 5 5 3 5 4 4 5 4 5 5 4 5 5 5 4 5 4 3 4 3 3 3 3 3 3 3 3 3 5 5 5 5 5 5 5 5 5 5 4 5 5 2 4 4 5 33
4 5 4 6 4 5 4 4 3 4 2 2 5 5 3 5 4 4 5 4 5 5 4 5 5 5 4 5 4 3 4 3 3 3 3 3 3 3 3 3 5 5 5 5 5 5 5 5 5 5 4 5 5 2 4 4 5 NA
These fish families constitute the major coral reef demersal fish caught by small-scale fishers in the Philippines (Muallil et al., 2014a). We opted to use this simple classification since fishers in the Philippines have been increasingly becoming less selective in their target species, which makes it difficult to classify each species as commercially important or not (Muallil et al., 2014b). The date of establishment and size of MPAs were gathered from the local records of the respective LGU or management body. These data are also available in the MPA database which is maintained by the Marine Science Institute, University of the Philippines Diliman (Cabral
Species specific a and b values were gathered from published records (Froese and Pauly, 2011; Kulbicki et al., 2005). The a and b values used for fishes identified to the genus level only were the average values for the genus. Classification of fish was based on Muallil et al. (2015), wherein only the surgeonfish (family Acanthuridae excluding genus Zebrasoma), parrotfish (subfamily Scarinae, family Labridae), snapper (family Lutjanidae), grouper (subfamily Epinephelinae, family Serranidae), goatfish (family Mullidae), sweetlips (family Haemulidae) and emperor (family Lethrinidae) were considered as commercially important fishes. 3
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biomass on reefs inside MPAs. Moreover, the estimate can still be conservative as the overall fish biomass of about 106.5 mt/km2 recorded in the TRNMP, which was used as the proxy for unfished biomass (Bo), is lower than the estimated 120 mt/km2 fish biomass for pristine reefs in the Indo-Pacific (McClanahan et al., 2014). The extent of overfishing in Philippine coral reef fisheries as shown in this study is much worse than previously estimated (Muallil et al., 2014a) where only about 68% of coastal fishing grounds in the country are overfished. The previous study was based on a bioeconomic model using data from interviews that did not account for IUU (illegal, unreported and unregulated) fishing which is still rampant in many areas in the Philippines (Muallil et al., 2014a, 2014b). Our study supports the findings that many fisheries worldwide have already been severely depleted where fish stocks have been reduced to less than 10% of the unfished levels (Green et al., 2003; Myers and Worm, 2003; Worm et al., 2006). Age and size of the MPAs were not significantly correlated with fish biomass levels which contradict the results of some studies showing higher fish biomass in older and bigger MPAs. For example, Maliao et al., (2009) showed higher fish density in older and larger MPAs based on the metaanalysis of 19 MPAs in the country. However, their study included only well enforced MPAs (e.g. at least level 2 or established/ fair) in central Philippines. On the contrary, the management levels of most of the MPAs in our study were still at level 0 or have not been assessed at all at the time of the study. There are also studies which showed increased in fish biomass in small locally managed MPAs after decades of strict enforcement (Russ and Alcala, 2003; Abesamis et al., 2006) but these are rather exceptional cases as most of the MPAs in the country are not effectively managed (Arceo et al., 2008; Maypa et al., 2012; PhilReefs, 2014). Generally, the MPAs in the Philippines are too small and fishing pressure from the highly fishery-dependent coastal ommunities is high and increasing (Weeks et al., 2010; Edgar et al., 2014; Green et al., 2014; Muallil et al., 2014a). The mean ( ± SE) size of about 0.57 ± 0.07 km2 of the MPAs in this study is much smaller than the suggested size of at least 10.0 km2 for an MPA to be effective for coral reef fishes conservation (Weeks et al., 2010). Fishing pressure alone from the almost two million small-scale fishers could easily deplete the coastal fisheries (Newton et al., 2007; Muallil et al., 2014a). In addition, the prevalence of blast, poison and other forms of illegal fishing practices in many areas in the country could further worsen the impact of overfishing and hamper fish stocks recovery (Muallil et al., 2014a, 2014b). Management effectiveness and the level of compliance play an important role in successful MPAs (Bergseth et al., 2015). Unfortunately, the sustainability of MPA management in the Philippines is a major problem due to lack of sustainable financing (Senga, 2001; Maypa et al., 2012). Reefbase (2015) reported that more than half (54%) of the MPAs had not progressed beyond the implementation phase. Many of the MPAs in the country benefit from the generous support of non-government organizations (NGOs), particularly in terms of technical and logistical support, including livelihood programs for the displaced fishers, that usually last for 3–5 years. The Philippine law as per RA 8550 or the Fisheries Code of 1998, which has been recently ammended to RA 10654, devolved the management of municipal waters, i.e., the area from the shore up to 15 km seaward, and all the coastal ecosystems within it to the local government units (LGUs). The LGUs are required to protect at least 15% of the municipal waters. However, the LGUs often have limited resources and the technical capability to do the job. In addition, many LGUs do not have the political will to strictly enforce MPA laws because of fear of being not voted for in the election by the affected community. Thus, without external support, the LGU-managed MPAs are often not sustainable and eventually become mere “paper” MPAs in the long run (De Jesus et al., 2013; Reefbase, 2015).
et al., 2014). 2.3. Analyses Shapiro-Wilk's test for normality revealed that the fish biomass data were not normally distributed (P < 0.001) (Annex 1). Fish biomass values were square root transformed and the generalized linear mixed model with gaussian distribution family was used to compare fish biomass levels between reefs inside and outside MPAs, with study sites as the random factor. Fish biomass levels were also assessed using the modified exploitation levels proposed by McClanahan et al. (2014) for multi-species coral reef fisheries. Here, fish biomass (B) levels between 25 and 50% of the unfished levels (Bo) was considered as the biomass within the multi-species maximum sustainable yield (BMMSY) level. In our study, we used three levels of exploitation, namely, (i) “above BMMSY” (B > 50% of BO), (ii) “within BMMSY” (B = 25–50% of BO), and (iii) “below BMMSY” (B < 25% of BO). Due to unavailability of baseline information, we opted to use the biomass level of coral reefs at the Tubbataha Reefs National Marine Park (TRNMP), which is arguably the most effectively managed MPA in the country, as the proxy for “unfished” ecosystems (BO). We further determined whether fish biomass is influenced by size or age of MPAs using a generalized linear model with fish biomass as the dependent variable and size and age of MPAs as independent variables. Statistical analyses were implemented using RStudio statistical analysis software version 1.2.1335 (2009–2019 RStudio, Inc). 3. Results Overall, the highest fish biomass was recorded at the TRNMP which had a mean ( ± S.E.) biomass of 106.5 ± 16.2 mt/km2. The seven commercially important coral reef fish groups considered in the study had a biomass of 55.1 ± 7.5 mt/km2 which constituted about 51.7% of the overall fish biomass. Using the fish biomass at the TRNMP as the proxy for “unfished” coral reefs, only four of the 57 (7.0%) of surveyed MPAs had fish biomass of “above BMMSY”, i.e. more than 50% of the TRNMP level (Fig. 2 ). Fish biomass in 13 of the MPAs (22.8%) were “within BMMSY”, i.e. 25–50% of the TRNMP level, and fish biomass in the remaining 40 MPAs (70.2%) were “below BMMSY”, i.e. less than 25% of the TRNMP level. None of the reefs outside MPAs had fish biomass “above BMMSY”. Fish biomass levels in six sites (10.5%) were “within BMMSY” while the other 51 sites (89.5%) outside MPA were all “below BMMSY”. The mean ( ± S.E.) fish biomass levels on reefs inside and outside MPAs were only about 20.4 ± 2.2% and 10.9 ± 1.3%, respectively, of the TRNMP level. Surgeonfish (family Acanthuridae), followed by parrotfish (subfamily Scarinae) and snappers (family Lutjanidae) had the highest fish biomass both inside and outside MPAs (Fig. 3). Surgeonfish and parrotfish consistently had the highest fish biomass but their proportion relative to other fish groups decreased as overall fish biomass level increased from overfished to unfished or pristine level (Fig. 3). Except for the sweetlips (family Haemulidae) (P = 0.07), the biomass levels of other fish groups studies were significantly higher inside MPAs than outside MPAs (P < 0.05) (Annex 2). Neither size nor age of MPAs showed a significant relationship with fish biomass inside MPAs (Annexes 3 and 4). 4. Discussion Fish biomass of commercially important coral reef fishes is generally very low indicating the highly overfished state of Philippine coral reefs. Using the biomass thresholds proposed by McClanahan et al. (2014) for coral reef fisheries, our study showed that overfishing is evident even inside MPAs, which has a fish biomass of only about 20.4% of the TRNMP level. Coral reefs outside MPAs had only about half of the fish 4
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Fig. 2. Levels of exploitation rate based on fish biomass levels on reefs in the Philippines relative to the TRNMP level, which was used as the proxy for unfished level. A. inside MPA and B. outside MPAs. Blue, “above BMMSY” where B > 50% of TRNMP; Green, “within BMMSY” where B = 25–50% of TRNMP); Red, “below BMMSY” where B < 25% of TRNMP. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)
5. CONCULUSION and recommendations
2014) which means that more than 95% of the coral reefs in the country are at high risk of further exploitation from the nearly two million fishers in the country. Other complementary initiatives aside from MPAs that are geared towards reducing fishing pressure and eliminating IUU fishing are needed for effective coral reef fisheries management in the Philippines. As pointed out in Muallil et al. (2015), the current MPAs in the country may, at best, work in delaying fast extirpation of commercially important coral reef fishes. Nonetheless, the higher fish biomass on reefs inside than outside MPAs indicate that having MPAs is better than
Our study showed the highly overfished state of the Philippine coral reef fisheries which coroborate the results of various localized studies conducted independently in the country (PhilReefs, 2008 and 2014). Generally, fish biomass is slightly better inside MPAs but still fell within the overfished state indicating that the existing MPAs, which are mostly small and ineffectively managed, are not working well as far as coral reef fisehries management is concern. Moreover, the MPAs cover only less than 5% of the total coral reef area in the country (White et al.,
Fig. 3. Patterns in community assemblages of commercially important coral reef fishes across total biomass range (i.e. from overfished to unfished levels). Fish assemblages inside and outside MPAs are also shown. 5
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having no MPAs at all. With the increasing coastal population and the advancement in fishing technology (Anticamara et al., 2001; Teh et al., 2013), effectively enforced MPAs may be among the few remaining unfished areas left in the Philippines that can sustain coral reef fisheries through the spillover effect of adult fishes or through the recruitment effect as a source of fish larvae (Abesamis et al., 2017). The study though was mainly based on McClanahan et al. (2014) which assumes that fish biomass levels reflect the level of fishing intensity. However, environmental factors such as island geomorphologies (Sandin et al., 2008), benthic characteristics (Taylor et al., 2015; Russ et al., 2015), water quality and productivity (Sandin et al., 2008) and connectivity with adjacent habitats (Olds et al., 2012) are also known to affect reef fish assemblages. Our study covers all the six biogeographic regions of the Philippines where other factors aside from fishing vary among the study sites. With climate change, the impact of environmental factors is expected to become increasingly more important in driving coral reef fisheries (Munday et al., 2008). Thus, future studies need to investigate how different factors apart from fishing drive coral reef fisheries in order to better understand and ensure its long-term sustainability which supports the livelihood of millions of people living in coastal areas in the country.
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Ethical statement All authors have contributed to this study. Below are the specific contributions of each author: Richard N. Muallil: Designed the study, Analysed the data, Wrote the manuscript. Melchor R. Deocadez: Collected the data, Analysed the data, Provided inputs to the manuscript. Renmar Jun S. Martinez: Collected the data, Analysed the data, Provided inputs to the manuscript. Wilfredo L. Campos: Designed the study, Provided inputs to the manuscript. Samuel S. Mamauag, Designed the study, Provided inputs to the manuscript. Cleto L. Nañola Jr.: Provided inputs to the manuscript. Porfirio Aliño: Designed the study, Wrote the manuscript. Acknowledgements This study is an output of various projects of the Coral Reefs and Community Ecology (COMECO) laboratory at the Marine Science Institute of the University of the Philippines conducted from 2006 to 2014. These projects were funded by the United States Agency for International Development, The Deutsche Gesellschaft für Internationale Zusammenarbeit (GIZ), the Department of Environment and Natural Resources (DENR) of the Philippines and the Department of Science and Tecnology (DOST) of the Philippines. We would also like to thank the two anonymous reviewers who provided valuable comments that greatly improved our manuscript. Appendix A. Supplementary data Supplementary data to this article can be found online at https:// doi.org/10.1016/j.lwt.2019.05.053. References Abesamis, R.A., Russ, G.R., Alcala, A.C., 2006. Gradients of abundance of fish across no‐take marine reserve boundaries: evidence from Philippine coral reefs. Aquat. Conserv. 16 (4), 349–371. Abesamis, R.A., Saenz-Agudelo, P., Berumen, M.L., Bode, M., Jadloc, C.R.L., Solera, L.A., Villanoy, C.L., Bernardo, L.P.C., Alcala, A.C., Russ, G.R., 2017. Reef-fish larval dispersal patterns validate no-take marine reserve network connectivity that links human communities. Coral Reefs 36 (3), 791–801. Arceo, H.O., Aliño, P.M., Gonzales, R.O.M., 2008. Where are we now with marine protected areas? In: Reefs through Time: Initiating the State of the Coasts Reports. Coral Reef Information Network of the Philippines (PhilReefs), MPA Support Network. Marine Environment & Resources Foundation, Inc. and the Marine Science Institute, University of the Philippines, Quezon City, pp. 145–152. Anticamara, J.A., Watson, R., Gelchu, A., Pauly, D., 2001. Global fishing effort (19502010): trends, gaps, and implications. Fish. Res. 107, 131–136.
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Tools. Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem. Academic Press, San Diego, California, USA, pp. 421–443. Russ, G.R., Alcala, A.C., 2003. Marine reserves: rates and patterns of recovery and decline of predatory fish, 1983–2000. Ecol. Appl. 13 (6), 1553–1565. Russ, G.R., Miller, K.I., Rizzari, J.R., Alcala, A.C., 2015. Long-term no-take marine reserve and benthic habitat effects on coral reef fishes. Mar. Ecol. Prog. Ser. 29, 233–248. Sandin, S.A., Vermeij, M.J., Hurlbert, A.H., 2008. Island biogeography of Caribbean coral reef fish. Glob. Ecol. Biogeogr. 17 (6), 770–777. Senga, R.G., 2001. Establishing protected areas in the Philippines: emerging trends, challenges and prospects. George Wright Forum 18 (2), 56–65. Taylor, B.M., Lindfield, S.J., Choat, J.H., 2015. Hierarchical and scale‐dependent effects of fishing pressure and environment on the structure and size distribution of
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