Decadal shifts in traits of reef fish communities in marine reserves

Hadj-Hammou, J. and McClanahan, T.R. and Graham, N.A.J. (2021) Decadal shifts in traits of reef fish communities in marine reserves. Scientific Reports, 11 (1). ISSN 2045-2322

Full text not available from this repository.


Marine reserves are known to impact the biomass, biodiversity, and functions of coral reef fish communities, but the effect of protective management on fish traits is less explored. We used a time-series modelling approach to simultaneously evaluate the abundance, biomass, and traits of eight fish families over a chronosequence spanning 44 years of protection. We constructed a multivariate functional space based on six traits known to respond to management or disturbance and affect ecosystem processes: size, diet, position in the water column, gregariousness, reef association, and length at maturity. We show that biomass increased with a log-linear trend over the time-series, but abundance only increased after 20 years of closure, and with more variation among reserves. This difference is attributed to recovery rates being dependent on body sizes. Abundance-weighted traits and the associated multivariate space of the community change is driven by increased proportions over time of the trait categories: 7–15 cm body size; planktivorous; species low in the water column; medium-large schools; and species with high levels of reef association. These findings suggest that the trait compositions emerging after the cessation of fishing are novel and dynamic.

Item Type:
Journal Article
Journal or Publication Title:
Scientific Reports
Additional Information:
Export Date: 22 December 2021 Correspondence Address: Hadj-Hammou, J.; Lancaster University Environment Centre, United Kingdom; email: Funding details: John D. and Catherine T. MacArthur Foundation, JDCTMF Funding details: Natural Environment Research Council, NERC, NE/L002604/1 Funding details: Western Indian Ocean Marine Science Association, WIOMSA Funding text 1: Grants from the Western Indian Ocean Marine Science Association, the Tiffany, and John D. and Catherine T. MacArthur Foundations to the Wildlife Conservation Society supported the field work. Thanks to Kenya’s National Commission for Science and Innovation for clearance to do research in Kenya and Kenya Wildlife Services for permission to work in the parks. Research development was supported by a Doctoral Training Programme grant from NERC ENVISION (Grant Number: NE/L002604/1). We would also like to thank James Robinson for his help with the analysis and to the editor and two reviewers for their constructive suggestions. References: O’Leary, B.C., Effective coverage targets for ocean protection (2016) Conserv. Lett., 9, pp. 398-404; Edgar, G.J., Global conservation outcomes depend on marine protected areas with five key features (2014) Nature, 506, pp. 216-220. , COI: 1:CAS:528:DC%2BC2cXisValu78%3D, PID: 24499817; Lester, S.E., Biological effects within no-take marine reserves: A global synthesis (2009) Mar. Ecol. Prog. Ser., 384, pp. 33-46; Brandl, S.J., Emslie, M.J., Ceccarelli, D.M., Habitat degradation increases functional originality in highly diverse coral reef fish assemblages (2016) Ecosphere, 7; Ramírez-Ortiz, G., Reduced fish diversity despite increased fish biomass in a Gulf of California Marine Protected Area (2020) PeerJ, 2020; Miatta, M., Bates, A.E., Snelgrove, P.V.R., Incorporating biological traits into conservation (2021) Strategies; Coleman, M.A., Functional traits reveal early responses in marine reserves following protection from fishing (2015) Divers. Distrib., 21, pp. 876-887; Bellwood, D.R., Streit, R.P., Brandl, S.J., Tebbett, S.B., The meaning of the term ‘function’ in ecology: A coral reef perspective (2019) Funct. Ecol., 33, pp. 1365-2435; Brandl, S.J., Coral reef ecosystem functioning: Eight core processes and the role of biodiversity (2019) Front. Ecol. Environ.; McLean, M., Mouillot, D., Villéger, S., Graham, N.A.J., Auber, A., Interspecific differences in environmental response blur trait dynamics in classic statistical analyses (2019) Mar. Biol., 166, pp. 1-10; Hadj-Hammou, J., Mouillot, D., Graham, N.A.J., Response and effect traits of coral reef fish (2021) Front. Mar. Sci., 8, p. 640619; Griffin-Nolan, R.J., Trait selection and community weighting are key to understanding ecosystem responses to changing precipitation regimes (2018) Funct. Ecol., 32, pp. 1746-1756; Lefcheck, J.S., Tropical fish diversity enhances coral reef functioning across multiple scales (2019) Sci. Adv., 5, p. eaav6420. , PID: 30854434; McLean, M., A climate-driven functional inversion of connected marine ecosystems (2018) Curr. Biol., 28, pp. 3654-3660.e3. , COI: 1:CAS:528:DC%2BC1cXitFCgsb3M, PID: 30416056; Mouillot, D., Graham, N.A.J., Villéger, S., Mason, N.W.H., Bellwood, D.R., A functional approach reveals community responses to disturbances (2013) Trends Ecol. Evol., 28, pp. 167-177. , PID: 23141923; Harborne, A.R., Mumby, P.J., Novel ecosystems: Altering fish assemblages in warming waters (2011) Curr. Biol., 21, pp. R822-R824. , COI: 1:CAS:528:DC%2BC3MXhtlaqtL3I, PID: 21996508; Graham, N.A.J., Cinner, J.E., Norström, A.V., Nyström, M., Coral reefs as novel ecosystems: Embracing new futures (2014) Curr. Opin. Environ. Sustain., 7, pp. 9-14; Woodhead, A.J., Hicks, C.C., Norström, A.V., Williams, G.J., Graham, N.A.J., Coral reef ecosystem services in the Anthropocene (2019) Funct. Ecol., 33, pp. 1023-1034; Munday, P.L., Jones, G.P., The ecological implications of small body size among coral-reef fishes (1998) Oceanogr. Mar. Biol. Annu. Rev., 36, pp. 373-411; Babcock, R.C., Decadal trends in marine reserves reveal differential rates of change in direct and indirect effects (2010) Proc. Natl. Acad. Sci., 107, pp. 18256-18261. , COI: 1:CAS:528:DC%2BC3cXhtl2ktr7E, PID: 20176941; Robinson, J.P.W., Fishing degrades size structure of coral reef fish communities (2017) Glob. Change Biol., 23, pp. 1009-1022; Villéger, S., Brosse, S., Mouchet, M., Mouillot, D., Vanni, M.J., Functional ecology of fish: Current approaches and future challenges (2017) Aquat. Sci., 79, pp. 783-801; Cinner, J.E., Meeting fisheries, ecosystem function, and biodiversity goals in a human-dominated world (2020) Science (80-.), 368, pp. 307-311. , COI: 1:CAS:528:DC%2BB3cXntl2qurk%3D; McClanahan, T.R., Kenyan coral reef lagoon fish: Effects of fishing, substrate complexity, and sea urchins (1994) Coral Reefs, 13, pp. 231-241; McClanahan, T.R., Graham, N.A.J., Recovery trajectories of coral reef fish assemblages within Kenyan marine protected areas (2005) Mar. Ecol. Prog. Ser., 294, pp. 241-248; Graham, N.A.J., Changing role of coral reef marine reserves in a warming climate (2020) Nat. Commun., 111 (11), pp. 1-8; Greene, L.E., (1990) The Use of Discrete Group Censusing for Assessment and Monitoring of Reef Fish Assemblages, , PhD diss, Melbourne; McClanahan, T.R., Graham, N.A.J., Calnan, J.M., MacNeil, M.A., Toward pristine biomass: Reef fish recovery in coral reef marine protected areas in Kenya (2007) Ecol. Appl., 17, pp. 1055-1067. , PID: 17555218; McClanahan, T.R., Humphries, A.T., Differential and slow life-history responses of fishes to coral reef closures (2012) Mar. Ecol. Prog. Ser., 469, pp. 121-131; Kublicki, M., (2010) GASPAR General Approach to Species-Abundance Relationships in a Context of Global Change, Reef Fish Species as a Model; Froese, R., Pauly, D.F., (2019),, Available at, Accessed 23 May 2019; Thorson, J.T., Munch, S.B., Cope, J.M., Gao, J., Predicting life history parameters for all fishes worldwide (2017) Ecol. Appl., 27, pp. 2262-2276. , PID: 28746981; Rousseeuw, P., Finding Groups in Data (2018) Cluster Analysis Extended Rousseeuw Et Al. CRAN (Comprehensive R Archive Network (CRAN); Paradis, E., Package ‘ape (2019) Analyses of Phylogenetics and Evolution Depends R; Laliberté, E., Legendre, P.B.S., (2015) Package ‘FD’ Type Package Title Measuring Functional Diversity (FD) from Multiple Traits, and Other Tools for Functional Ecology; Lavorel, S., Assessing functional diversity in the field—Methodology matters! (2007) Funct. Ecol., 22, pp. 134-147; Fontoura, L., Climate-driven shift in coral morphological structure predicts decline of juvenile reef fishes (2020) Glob. Change Biol., 26, pp. 557-567; McClanahan, T., Coral reef fish communities, diversity, and their fisheries and biodiversity status in East Africa (2019) Mar. Ecol. Prog. Ser., 632, pp. 175-191; Selig, E.R., Casey, K.S., Bruno, J.F., New insights into global patterns of ocean temperature anomalies: Implications for coral reef health and management (2010) Glob. Ecol. Biogeogr., 19, pp. 397-411; Ye, H., Deyle, E.R., Gilarranz, L.J., Sugihara, G., Distinguishing time-delayed causal interactions using convergent cross mapping (2015) Sci. Rep., 5, p. 14750. , COI: 1:CAS:528:DC%2BC2MXhs1Sksr7J, PID: 26435402; Wilson, S.K., Influence of nursery microhabitats on the future abundance of a coral reef fish (2016) Proc. R. Soc. B Biol. Sci., 283, pp. 1-7; McClanahan, T.R., Decadal turnover of thermally stressed coral taxa support a risk-spreading approach to marine reserve design (2020) Coral Reefs; Yeager, L.A., Marchand, P., Gill, D.A., Baum, J.K., McPherson, J.M., Marine socio-environmental covariates: Queryable global layers of environmental and anthropogenic variables for marine ecosystem studies (2017) Ecology, 98, p. 1976. , PID: 28466482; Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A.G.M., (2009) Mixed Effects Models and Extensions in Ecology with R; Wood, S.N., (2017) Generalized Additive Models: An Introduction with R, , 2, CRC Press; Simpson, G.L., Modelling palaeoecological time series using generalised additive models (2018) Front. Ecol. Evol., 6, p. 149; Wood, S.N., Low-rank scale-invariant tensor product smooths for generalized additive mixed models (2006) Biometrics, 62, pp. 1025-1036. , PID: 17156276; Pedersen, E.J., Miller, D.L., Simpson, G.L., Ross, N., Hierarchical generalized additive models in ecology: An introduction with mgcv (2019) PeerJ, 2019; Pecuchet, L., From traits to life-history strategies: Deconstructing fish community composition across European seas (2017) Glob. Ecol. Biogeogr., 26, pp. 812-822; Dormann, F., Methods to account for spatial autocorrelation in the analysis of species distributional data: A review (2007) Ecography, 30, pp. 609-628; Schulp, C.J.E., Lautenbach, S., Verburg, P.H., Quantifying and mapping ecosystem services: Demand and supply of pollination in the European Union (2014) Ecol. Indic., 36, pp. 131-141; Warton, D.I., Hui, F.K.C., The arcsine is asinine: The analysis of proportions in ecology (2011) Ecology, 92, pp. 3-10. , PID: 21560670; (2020) A Language and Environment for Statistical Computing (R Foundation for Statistical Computing; MacNeil, M.A., Recovery potential of the world’s coral reef fishes (2015) Nature, 520, pp. 341-344. , COI: 1:CAS:528:DC%2BC2MXmt1Smtr8%3D; McClanahan, T.R., Ateweberhan, M., Muhando, C.A., Maina, J., Mohammed, M.S., Effects of climate and seawater temperature variation on coral bleaching and mortality (2007) Ecol. Monogr., 77, pp. 503-525; Chirico, A.A.D., McClanahan, T.R., Eklöf, J.S., Community- and government-managed marine protected areas increase fish size, biomass and potential value (2017) PLoS ONE, 12. , PID: 28806740; McClanahan, T.R., Friedlander, A.M., Graham, N.A.J., Chabanet, P., Bruggemann, J.H., Variability in coral reef fish baseline and benchmark biomass in the central and western Indian Ocean provinces (2020) Aquat. Conserv. Mar. Freshw. Ecosyst.; Mbaru, E.K., Graham, N.A.J., McClanahan, T.R., Cinner, J.E., Functional traits illuminate the selective impacts of different fishing gears on coral reefs (2019) J. Appl. Ecol.; Dulvy, N.K., Polunin, N.V.C., Mill, A.C., Graham, N.A.J., Size structural change in lightly exploited coral reef fish communities: Evidence for weak indirect effects (2004) Can. J. Fish. Aquat. Sci., 61, pp. 466-475; D’Agata, S., Marine reserves lag behind wilderness in the conservation of key functional roles (2016) Nat. Commun., 7, p. 12000. , PID: 27354026; Mbaru, E.K., McClanahan, T.R., Escape gaps in African basket traps reduce bycatch while increasing body sizes and incomes in a heavily fished reef lagoon (2013) Fish. Res., 148, pp. 90-99; Grime, J.P., Benefits of plant diversity to ecosystems: Immediate, filter and founder effects (1998) J. Ecol., 86, pp. 902-910; Campbell, S.J., Fishing restrictions and remoteness deliver conservation outcomes for Indonesia’s coral reef fisheries (2020) Conserv. Lett.; Heenan, A., Williams, G.J., Williams, I.D., Natural variation in coral reef trophic structure across environmental gradients (2020) Front. Ecol. Environ., 18, pp. 69-75; Morais, R.A., Bellwood, D.R., Pelagic subsidies underpin fish productivity on a degraded coral reef (2019) Curr. Biol., 29, pp. 1521-1527.e6. , COI: 1:CAS:528:DC%2BC1MXnslOqsL0%3D, PID: 31006572; González-Rivero, M., Linking fishes to multiple metrics of coral reef structural complexity using three-dimensional technology (2017) Sci. Rep., 7, pp. 1-15; Coker, D.J., Graham, N.A.J., Pratchett, M.S., Interactive effects of live coral and structural complexity on the recruitment of reef fishes (2012) Coral Reefs, 31, pp. 919-927; Benkwitt, C.E., Wilson, S.K., Graham, N.A.J., Seabird nutrient subsidies alter patterns of algal abundance and fish biomass on coral reefs following a bleaching event (2019) Glob. Change Biol., 25, pp. 2619-2632; Russ, G.R., Aller-Rojas, O.D., Rizzari, J.R., Alcala, A.C., Off-reef planktivorous reef fishes respond positively to decadal-scale no-take marine reserve protection and negatively to benthic habitat change (2017) Mar. Ecol., 38; Darling, E.S., McClanahan, T.R., Côté, I.M., Life histories predict coral community disassembly under multiple stressors (2013) Glob. Change Biol., 19, pp. 1930-1940; Strain, E.M.A., A global assessment of the direct and indirect benefits of marine protected areas for coral reef conservation (2019) Divers. Distrib., 25, pp. 9-20; Floeter, S.R., Bender, M.G., Siqueira, A.C., Cowman, P.F., Phylogenetic perspectives on reef fish functional traits (2018) Biol. Rev., 93, pp. 131-151. , PID: 28464469; Michael, P.J., Hyndes, G.A., Vanderklift, M.A., Vergés, A., Identity and behaviour of herbivorous fish influence large-scale spatial patterns of macroalgal herbivory in a coral reef (2013) Mar. Ecol. Prog. Ser., 482, pp. 227-240; Paijmans, K.C., Booth, D.J., Wong, M.Y.L., Predation avoidance and foraging efficiency contribute to mixed-species shoaling by tropical and temperate fishes (2020) J. Fish Biol., 96, pp. 806-814. , PID: 32031243; White, J.W., Warner, R.R., Behavioral and energetic costs of group membership in a coral reef fish (2007) Oecologia, 154, pp. 423-433. , PID: 17713786; van Kooten, T., Persson, L., de Roos, A.M., Population dynamical consequences of gregariousness in a size-structured consumer-resource interaction (2007) J. Theor. Biol., 245, pp. 763-774. , PID: 17240402; Kelley, J.L., Grierson, P.F., Collin, S.P., Davies, P.M., Habitat disruption and the identification and management of functional trait changes (2018) Fish Fish., 19, pp. 716-728; Rochet, M., Short-term effects of fishing on life history traits of fishes (1998) ICES J. Mar. Sci., 55, pp. 371-391; McClanahan, T.R., Global baselines and benchmarks for fish biomass: Comparing remote reefs and fisheries closures (2019) Mar. Ecol. Prog. Ser.; Jacob, U., The role of body size in complex food webs: A cold case (2011) Adv. Ecol. Res., 45, pp. 181-223; McClanahan, T.R., Graham, N.A.J., Marine reserve recovery rates towards a baseline are slower for reef fish community life histories than biomass (2015) Proc. Biol. Sci., 282, p. 20151938. , COI: 1:STN:280:DC%2BC28rlt1answ%3D%3D, PID: 26702040; Humphries, A.T., Algal turf consumption by sea urchins and fishes is mediated by fisheries management on coral reefs in Kenya (2020) Coral Reefs; Ward, T.J., Heinemann, D., Evans, N., The role of marine reserves as fisheries management tools. A review of concepts, evidence and international experience (2001) Bur. Rural Sci. Aust., 192, p. 105; Bergseth, B.J., Williamson, D.H., Russ, G.R., Sutton, S.G., Cinner, J.E., A social-ecological approach to assessing and managing poaching by recreational fishers (2017) Front. Ecol. Environ., 15, pp. 67-73; McClanahan, T.R., Recovery of functional groups and trophic relationships in tropical fisheries closures (2014) Mar. Ecol. Prog. Ser., 497, pp. 13-23; Mcclanahan, T.R., Omukoto, J.O., Comparison of modern and historical fish catches (AD 750–1400) to inform goals for marine protected areas and sustainable fisheries (2011) Conserv. Biol., 25, pp. 945-955. , PID: 21676028; Williams, G.J., Graham, N.A.J., Rethinking coral reef functional futures (2019) Funct. Ecol., 33, pp. 942-947
Uncontrolled Keywords:
ID Code:
Deposited By:
Deposited On:
05 Jan 2022 17:10
Last Modified:
17 Sep 2023 03:09