A leading argument for no-take marine protected area (marine reserve) establishment is their contribution to the conservation of biodiversity, but the impacts of reserves on ecosystem functioning have seldom been quantified. This is unusual given the value of services provided by ocean ecosystems to human well-being. While no single index can describe ecosystem function, a set of life-history attributes possessed by taxa can be used to infer differences in ecosystem function across space and time. In this study, we use biological trait analysis to determine whether the attributes of invertebrate taxa differ between inside of six no-take marine reserves and outside, in fished areas in the Central Philippines. Using permutational multivariate analyses, we found that the composition of traits and taxa were significantly different between reserve and non-reserve areas. Habitat use, morphology and mobility traits were the biggest contributors to dissimilarity, indicating that reserves can have community-wide effects that change the functional composition of invertebrate assemblages. Notably, traits associated with coral habitat use, bearing a shell, lacking mobility and filter feeding are the most important traits associated with differences in community structure between reserve and non-reserve areas. At the taxa composition level, small shrimps, three families of bivalve, two families of burrowing snails and brittle stars are the most important contributors to differences in taxonomic community composition. The addition of organismal attributes to traditional taxa composition approaches provides richer insight into how ecosystems respond to protection and has the potential to inform practitioners on conserving for ecosystem traits.
This is a preview of subscription content, log in to check access.
Buy single article
Instant access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Anderson SC, Flemming JM, Watson R, Lotze HK (2011) Rapid global expansion of invertebrate fisheries: trends, drivers, and ecosystem effects. PLoS ONE 6:e14735. https://doi.org/10.1371/journal.pone.0014735
Anticamara JA, Zeller D, Vincent ACJ (2010) Spatial and temporal variation of abundance, biomass and diversity within marine reserves in the Philippines. Divers Distrib 16:529–536
Bengtsson J (1998) Which species? What kind of diversity? Which ecosystem function? Some problems in studies of relations between biodiversity and ecosystem function. Appl Soil Ecol 10:191–199
Berkes F, Folke C, Colding J (2000) Linking social and ecological systems: management practices and social mechanisms for building resilience. Cambridge University Press, Cambridge
Bertrand Y, Pleijel F, Rouse GW (2006) Taxonomic surrogacy in biodiversity assessments, and the meaning of Linnaean ranks. Syst Biodivers 4:149–159
Bremner J, Frid CLJ, Rogers SI (2003) Assessing marine ecosystem health: the long-term effects of fishing on functional biodiversity in North Sea benthos. Aquat Ecosyst Health Manag 6:131–137
Bremner J, Rogers SI, Frid CLJ (2006a) Methods for describing ecological functioning of marine benthic assemblages using biological traits analysis (BTA). Ecol Indic 6:609–622. https://doi.org/10.1016/j.ecolind.2005.08.026
Bremner J, Rogers SI, Frid CLJ (2006b) Matching biological traits to environmental conditions in marine benthic ecosystems. J Mar Syst 60:302–316
Cardinale BJ, Duffy JE, Gonzalez A et al (2012) Biodiversity loss and its impact on humanity. Nature 486:59–67
Carpenter KE, Springer VG (2005) The center of the center of marine shore fish biodiversity: the Philippine Islands. Environ Biol Fishes 72:467–480. https://doi.org/10.1007/s10641-004-3154-4
Castella E, Speight MCD (1996) Knowledge representation using fuzzy coded variables: an example based on the use of Syrphidae (Insecta, Diptera) in the assessment of riverine wetlands. Ecol Model 85:13–25
Cesar CP, Frid CLJ (2009) Effects of experimental small-scale cockle (Cerastoderma edule L.) fishing on ecosystem function. Mar Ecol 30:123–137
Chevene F, Doleadec S, Chessel D (1994) A fuzzy coding approach for the analysis of long-term ecological data. Freshw Biol 31:295–309. https://doi.org/10.1111/j.1365-2427.1994.tb01742.x
Clarke K, Gorley R (2015) PRIMER v7: user manual/tutorial. PRIMER-E, Plymouth
Clarke KR, Green RH (1988) Statistical design and analysis for a “biological effects” study. Mar Ecol Prog Ser 46:213–226
Coleman MA, Bates AE, Stuart-Smith RD et al (2015) Functional traits reveal early responses in marine reserves following protection from fishing. Divers Distrib 21:876–887
Collie JS, Hall SJ, Kaiser MJ, Poiner IR (2000) A quantitative analysis of fishing impacts on shelf-sea benthos. J Anim Ecol 69:785–798
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
de Bakker DM, van Duyl FC, Bak RPM et al (2017) 40 Years of benthic community change on the Caribbean reefs of Curaçao and Bonaire: the rise of slimy cyanobacterial mats. Coral Reefs. https://doi.org/10.1007/s00338-016-1534-9
Dıaz S, Cabido M (2001) Vive la difference: plant functional diversity matters to ecosystem processes. Trends Ecol Evol 16:646–655
Donaldson M, Burnett N, Braun D et al (2016) Taxonomic bias and international biodiversity conservation research. FACETS 1:105–113
Dulvy NK, Sadovy Y, Reynolds JD (2003) Extinction vulnerability in marine populations. Fish Fish 4:25–64
Dumas P, Jimenez H, Peignon C et al (2013) Small-scale habitat structure modulates the effects of no-take marine reserves for coral reef macroinvertebrates. PLoS ONE 8:e58998
Eddy TD, Lotze HK, Fulton EA et al (2017) Ecosystem effects of invertebrate fisheries. Fish Fish 18:40–53
Frid CLJ, Paramor OAL, Brockington S, Bremner J (2008) Incorporating ecological functioning into the designation and management of marine protected areas. Challenges to marine ecosystems. Springer, Berlin, pp 69–79
Gagic V, Bartomeus I, Jonsson T et al (2015) Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proc R Soc B Biol Sci 282:20142620
Giller PS, Hillebrand H, Berninger U et al (2004) Biodiversity effects on ecosystem functioning: emerging issues and their experimental test in aquatic environments. Oikos 104:423–436
Halpern BS, Warner RR (2002) Marine reserves have rapid and lasting effects. Ecol Lett 5:361–366
Halpern BS, Warner RR (2003) Matching marine reserve design to reserve objectives. Proc R Soc B Biol Sci 270:1871
Hughes TP, Bellwood DR, Folke C et al (2005) New paradigms for supporting the resilience of marine ecosystems. Trends Ecol Evol 20:380–386
Jackson J, Donovan M, Cramer K, Lam V (2014) Status and trends of Caribbean coral reefs: 1970–2012. Global Coral Reef Monitoring Network
Jimenez H, Dumas P, Bigot L et al (2010) Taxonomic resolution needed to describe invertebrate assemblages and to detect harvesting effects on coral reef ecosystems. Mar Ecol Prog Ser 406:211–222
Jimenez H, Dumas P, Bigot L, Ferraris J (2015a) Harvesting effects on tropical invertebrate assemblages in New Caledonia. Fish Res 167:75–81
Jimenez H, Dumas P, Mouillot D et al (2015b) Harvesting effects on functional structure and composition of tropical invertebrate assemblages. ICES J Mar Sci J du Cons. https://doi.org/10.1093/icesjms/fsv179
Kaiser MJ, Spence FE, Hart PJB (2000) Fishing-gear restrictions and conservation of benthic habitat complexity. Conserv Biol 14:1512–1525
Kleiber D, Harris LM, Vincent ACJ (2014) Gender and small-scale fisheries: a case for counting women and beyond. Fish Fish. https://doi.org/10.1111/faf.12075
Knowlton N, Jackson JBC (2008) Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6:e54
Lasiak TA, Field JG (1995) Community-level attributes of exploited and non-exploited rocky infratidal macrofaunal assemblages in Transkei. J Exp Mar Biol Ecol 185:33–53
Lavorel S, Garnier E (2002) Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct Ecol 16:545–556. https://doi.org/10.1046/j.1365-2435.2002.00664.x
Lester SE, Halpern BS, Grorud-Colvert K et al (2009) Biological effects within no-take marine reserves: a global synthesis. Mar Ecol Prog Ser 384:33–46
Levin SA, Lubchenco J (2008) Resilience, robustness, and marine ecosystem-based management. Bioscience 58:27–32
McClanahan TR (2014) Recovery of functional groups and trophic relationships in tropical fisheries closures. Mar Ecol Prog Ser 497:13–23. https://doi.org/10.3354/meps10605
McClanahan TR, Graham NAJ (2015) Marine reserve recovery rates towards a baseline are slower for reef fish community life histories than biomass. Proc R Soc London B Biol Sci 282:20141817
McClanahan TR, Shafir SH (1990) Causes and consequences of sea urchin abundance and diversity in Kenyan coral reef lagoons. Oecologia 83:362–370
McCook L, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417
Mumby PJ, Dahlgren CP, Harborne AR et al (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101
Naeem S (2004) How biodiversity loss affects the health of ecosystems
Newell RIE (1988) Ecological changes in Chesapeake Bay: are they the result of overharvesting the American oyster, Crassostrea virginica. Underst Estuary Adv Chesap Bay Res 129:536–546
Olsgard F, Somerfield PJ (2000) Surrogates in marine benthic investigations-which taxonomic unit to target? J Aquat Ecosyst Stress Recover 7:25–42
Pikitch EK, Santora C, Babcock EA et al (2004) Ecosystem-based fishery management. Science 305:346–347
Powell A, Smith DJ, Hepburn LJ et al (2014) Reduced diversity and high sponge abundance on a sedimented Indo-Pacific Reef System: implications for future changes in environmental quality. PLoS ONE 9:e85253. https://doi.org/10.1371/journal.pone.0085253
QGIS Development Team (2014) QGIS Geographic Information System
Ricard D, Minto C, Jensen OP, Baum JK (2012) Examining the knowledge base and status of commercially exploited marine species with the RAM Legacy Stock Assessment Database. Fish Fish 13:380–398
Sainsbury KJ, Campbell RA, Lindholm R, Whitelaw AW (1997) Experimental management of an Australian multispecies fishery: examining the possibility of trawl-induced habitat modification. Glob trends Fish Manag 20:107–112
Sala E, Aburto-Oropeza O, Paredes G et al (2002) A general model for designing networks of marine reserves. Science 298:1991–1993
Tillin HM, Hiddink JG, Jennings S, Kaiser MJ (2006) Chronic bottom trawling alters the functional composition of benthic invertebrate communities on a sea-basin scale. Mar Ecol Prog Ser 318:31–45
Travis J, Coleman FC, Auster PJ et al (2013) Integrating the invisible fabric of nature into fisheries management. Proc Natl Acad Sci. https://doi.org/10.1073/pnas.1305853111
Vanderklift MA, Ward TJ, Phillips JC (1998) Use of assemblages derived from different taxonomic levels to select areas for conserving marine biodiversity. Biol Conserv 86:307–315
White AT, Courtney CA, Salamanca A (2002) Experience with marine protected area planning and management in the Philippines. Coast Manag 30:1–26. https://doi.org/10.1080/08920750252692599
White AT, Aliño PM, Meneses ABT (2006) Creating and managing marine protected areas in the Philippines. Fisheries Improved for Sustainable Harvest Project
White AT, Aliño PM, Cros A et al (2014) Marine protected areas in the coral triangle: progress, issues, and options. Coast Manag 42:87–106
Yasue M, Kaufman L, Vincent ACJ (2010) Assessing ecological changes in and around marine reserves using community perceptions and biological surveys. Aquat Conserv Mar Freshw Ecosyst 20:407–418. https://doi.org/10.1002/aqc.1090
Zuur AF, Ieno EN, Elphick CS (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol 1:3–14
This is a contribution from Project Seahorse. We thank the people of Danajon Bank for their commitment to marine conservation and their engagement with our collective work. Many other members of the Project Seahorse Foundation for Marine Conservation, ZSL Philippines and Project Seahorse international teams have made important contributions over the years that have led to this project. We are also grateful to G. Sucano, R. Pechoko, E. Alibo for critical support during field work and A. Nellas, E. Jong, R. Apurado for providing logistical support and guidance in the Philippines. Two anonymous reviewers, provided very helpful suggestions and comments on this manuscript. Statistical guidance was provided by I. Côté.
KMG and ACJV were supported by a Grant from The Natural Sciences and Engineering Research Council (Canada; Grant Number 18430-12), and funds from Guylian Chocolates Belgium and The Ocean Charitable Trust. KMG was also supported by awards from The University of British Columbia Departments of Zoology, and Graduate and Post-Doctoral Studies, and a Natural Sciences and Engineering Research Council funded Ocean Leaders Fellowship.
All organisms sampled in this study are invertebrates and do not fall under consideration of The UBC Animal Care and Use Program. While collecting data for this study we followed animal care and use protocols previously approved for use in similar coral reef fish studies.
Conflict of interest
The authors declare that they have no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article belongs to the Topical Collection: Coastal and marine biodiversity.
Communicated by Peter Bridgewater.
About this article
Cite this article
Gillespie, K.M., Vincent, A.C.J. Marine reserves drive both taxonomic and functional change in coral reef invertebrate communities. Biodivers Conserv 28, 921–938 (2019). https://doi.org/10.1007/s10531-019-01702-1
- Coral reef
- Biological trait analysis
- Marine protected area
- Ecosystem services