Animals are central to numerous ecological processes that shape the structure and function of ecosystems. It follows that species that are strongly linked to specific functions can represent these functions spatially and hence be useful in conservation planning. Here we test this notion of ‘functional species surrogacy’ for the conservation of seagrass meadows that have been impacted by stressors. We measured algal herbivory and herbivorous fish assemblages across a range of seagrass meadows in the Moreton Bay Marine Park, Queensland, Australia. We determined the suitability of herbivorous fish to act as a surrogate for the function of algal herbivory and modelled the abundance of this surrogate, and thus herbivory, in seagrass meadows to compare the spatial distribution of this function within existing reserves. We used underwater video systems to determine the abundance of all herbivorous fish species in seagrass meadows. The abundance of the dusky rabbitfish (Siganus fuscescens) was the best predictor of algal herbivory in seagrass meadows, supporting the suitability of this species as a functional surrogate. The distribution of dusky rabbitfish, and therefore the ecological function of herbivory, was not well represented in the Moreton Bay Marine Park protected areas. Only 7% of the equivalent area of seagrass meadows protected in marine reserves were found to have high abundances of dusky rabbitfish. We demonstrate that the abundance of functionally important herbivores can be suitable as a surrogate for herbivory in seagrass conservation. Our findings show that data on the spatial distribution of ecological functions can alter priorities for reserve design, and we suggest that our functional approach to species surrogacy is likely to improve conservation performance in seagrass ecosystems.
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Althaus F, Williams A, Alderslade P, Schlacher TA. 2017. Conservation of marine biodiversity on a very large deep continental margin: how representative is a very large offshore reserve network for deep-water octocorals? Divers Distrib 23:90–103.
Aragones L, Marsh H. 2000. Impact of Dugong grazing and turtle cropping on tropical seagrass communities. Pac Conserv Biol 5:277–88.
Atwood TB, Connolly RM, Ritchie EG, Lovelock CE, Heithaus MR, Hays GC, Fourqurean JW, Macreadie PI. 2015. Predators help protect carbon stocks in blue carbon ecosystems. Nat Clim Chang 5:1038–45.
Bartoń K. 2013. MuMIn: multi-model inference. R package version 1.9. 13. The comprehensive R archive network (CRAN). Vienna, Austria.
Beger M, McGowan J, Treml EA, Green AL, White AT, Wolff NH, Klein CJ, Mumby PJ, Possingham HP. 2015. Integrating regional conservation priorities for multiple objectives into national policy. Nat Commun 6:8208.
Bell JD, Steffe AS, Westoby M. 1988. Location of seagrass beds in estuaries: effects on associated fish and decapods. J Exp Mar Biol Ecol 122:127–46.
Bennett J, Fisk G, Abal E, Stevens TF, Connolly R, Schlacher TA, Udy N, Rissik D, Zeller B, Winning M, Deacon G. 2009. Towards understanding the ecological health and character of Moreton Bay. In: 2nd Queensland Coastal Conference. Gold Coast, Australia.
Best RJ, Stachowicz JJ. 2012. Trophic cascades in seagrass meadows depend on mesograzer variation in feeding rates, predation susceptibility, and abundance. Mar Ecol Prog Ser 456:29–42.
Brown CJ, Mumby PJ. 2014. Trade-offs between fisheries and the conservation of ecosystem function are defined by management strategy. Front Ecol Environ 12:324–9.
Capper A, Tibbetts IR, O’Neil JM, Shaw GR. 2006. Feeding preference and deterrence in rabbitfish Siganus fuscescens for the cyanobacterium Lyngbya majuscula in Moreton Bay, south-east Queensland, Australia. J Fish Biol 68:1589–609.
Cardinale BJ, Srivastava DS, Duffy JE, Wright JP, Downing AL, Sankaran M, Jouseau C. 2006. Effects of biodiversity on the functioning of trophic groups and ecosystems. Nature 443:989–92.
Caro T. 2010. Conservation by proxy: indicator, umbrella, keystone, flagship, and other surrogate species. Washington: Island Press.
Carwardine J, Klein CJ, Wilson KA, Pressey RL, Possingham HP. 2009. Hitting the target and missing the point: target-based conservation planning in context. Conserv Lett 2:4–11.
Chelsky Budarf A, Burfeind DD, Loh WKW, Tibbetts IR. 2011. Identification of seagrasses in the gut of a marine herbivorous fish using DNA barcoding and visual inspection techniques. J Fish Biol 79:112–21.
Connolly RM, Hindell JS. 2006. Review of nekton patterns and ecological processes in seagrass landscapes. Estuar Coast Shelf Sci 68:433–44.
Cullen-Unsworth LC, Nordlund LM, Paddock J, Baker S, McKenzie LJ, Unsworth RK. 2014. Seagrass meadows globally as a coupled social–ecological system: Implications for human wellbeing. Mar Pollut Bull 83:387–97.
Davis JP, Pitt KA, Fry B, Olds AD, Connolly RM. 2014. Seascape-scale trophic links for fish on inshore coral reefs. Coral Reefs 33:897–907.
Duffy JE, Reynolds PL, Boström C, Coyer JA, Cusson M, Donadi S, Douglass JG, Eklöf JS, Engelen AH, Eriksson BK. 2015. Biodiversity mediates top–down control in eelgrass ecosystems: a global comparative-experimental approach. Ecol Lett 18:696–705.
Ebrahim A, Olds AD, Maxwell PS, Pitt KA, Burfeind DD, Connolly RM. 2014. Herbivory in a subtropical seagrass ecosystem: separating the functional role of different grazers. Mar Ecol Prog Ser 511:83–91.
Edwards HJ, Elliott IA, Pressey RL, Mumby PJ. 2010. Incorporating ontogenetic dispersal, ecological processes and conservation zoning into reserve design. Biol Conserv 143:457–70.
EHMP. 2016. Healthy waterways and catchments: ecosystem health monitoring program. Available at: http://healthywaterways.org.
Estes JA, Terborgh J, Brashares JS, Power ME, Berger J, Bond WJ, Carpenter SR, Essington TE, Holt RD, Jackson JB. 2011. Trophic downgrading of planet earth. Science 333:301–6.
Fourqurean JW, Duarte CM, Kennedy H, Marbà N, Holmer M, Mateo MA, Apostolaki ET, Kendrick GA, Krause-Jensen D, McGlathery KJ. 2012. Seagrass ecosystems as a globally significant carbon stock. Nat Geosci 5:505–9.
Gibbes B, Grinham A, Neil D, Olds A, Maxwell P, Connolly R, Weber T, Udy N, Udy J. 2014. Moreton Bay and its estuaries: a sub-tropical system under pressure from rapid population growth. In: Wolanski E, Ed. Estuaries of Australia in 2050 and beyond. Estuaries of the World. Dordrecht: Springer.
Gilby B, Henderson C, Tibbetts I, Burfeind D. 2016a. Quantifying the influence of small omnivorous fishes on seagrass epiphyte load. J Fish Biol 89:1905–12.
Gilby BL, Maxwell PS, Tibbetts IR, Stevens T. 2015. Bottom-up factors for algal productivity outweigh no-fishing marine protected area effects in a marginal coral reef system. Ecosystems 18:1–14.
Gilby BL, Olds AD, Yabsley NA, Connolly RM, Maxwell PS, Schlacher TA. 2017a. Enhancing the performance of marine reserves in estuaries: just add water. Biol Conserv 210:1–7.
Gilby BL, Tibbetts IR, Olds AD, Maxwell PS, Stevens T. 2016b. Seascape context and predators override water quality effects on inshore coral reef fish communities. Coral Reefs 35:1–12.
Gilby BL, Tibbetts IR, Stevens T. 2017b. Low functional redundancy and high variability in Sargassum browsing fish populations in a subtropical reef system. Mar Freshw Res 68:331–41.
Gullström M, Berkström C, Öhman M, Bodin M, Dahlberg M. 2011. Scale-dependent patterns of variability of a grazing parrotfish (Leptoscarus vaigiensis) in a tropical seagrass-dominated seascape. Mar Biol 158:1483–95.
Harvey ES, Cappo M, Butler JJ, Hall N, Kendrick GA. 2007. Bait attraction affects the performance of remote underwater video stations in assessment of demersal fish community structure. Mar Ecol Prog Ser 350:245–54.
Heck K, Hays G, Orth RJ. 2003. Critical evaluation of the nursery role hypothesis for seagrass meadows. Mar Ecol Prog Ser 253:123–36.
Heck K, Valentine J. 2007. The primacy of top-down effects in shallow benthic ecosystems. Estuar Coasts 30:371–81.
Heck KL, Valentine JF. 2006. Plant–herbivore interactions in seagrass meadows. J Exp Mar Biol Ecol 330:420–36.
Henderson CJ, Gilby BL, Lee SY, Stevens T. 2017a. Contrasting effects of habitat complexity and connectivity on biodiversity in seagrass meadows. Mar Biol 164:117–25.
Henderson CJ, Olds AD, Lee SY, Gilby BL, Maxwell PS, Connolly RM, Stevens T. 2017b. Marine reserves and seascape context shape fish assemblages in seagrass ecosystems. Mar Ecol Prog Ser 566:135–44.
Hoey AS, Bellwood DR. 2011. Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol Lett 14:267–73.
Hughes AR, Williams SL, Duarte CM, Heck KL, Waycott M. 2009. Associations of concern: declining seagrasses and threatened dependent species. Front Ecol Environ 7:242–6.
Hunter M Jr, Westgate M, Barton P, Calhoun A, Pierson J, Tulloch A, Beger M, Branquinho C, Caro T, Gross J, Heino J, Lane P, Longo C, Martin K, McDowell WH, Mellin C, Salo H, Lindenmayer D. 2016. Two roles for ecological surrogacy: Indicator surrogates and management surrogates. Ecol Indic 63:121–5.
Klein C, Wilson K, Watts M, Stein J, Berry S, Carwardine J, Smith MS, Mackey B, Possingham H. 2009. Incorporating ecological and evolutionary processes into continental-scale conservation planning. Ecol Appl 19:206–17.
Lentini PE, Wintle BA. 2015. Spatial conservation priorities are highly sensitive to choice of biodiversity surrogates and species distribution model type. Ecography 38:1101–11.
Leslie HM. 2005. A synthesis of marine conservation planning approaches. Conserv Biol 19:1701–13.
Lindenmayer D, Pierson J, Barton P, Beger M, Branquinho C, Calhoun A, Caro T, Greig H, Gross J, Heino J, Hunter M, Lane P, Longo C, Martin K, McDowell WH, Mellin C, Salo H, Tulloch A, Westgate M. 2015. A new framework for selecting environmental surrogates. Sci Total Environ 538:1029–38.
Ling S, Johnson C, Frusher S, Ridgway K. 2009. Overfishing reduces resilience of kelp beds to climate-driven catastrophic phase shift. Proc Natl Acad Sci 106:22341–5.
Lowenstein DM, Matteson KC, Minor ES. 2015. Diversity of wild bees supports pollination services in an urbanized landscape. Oecologia 179:811–21.
Lundberg J, Andersson E, Cleary G, Elmqvist T. 2008. Linkages beyond borders: targeting spatial processes in fragmented urban landscapes. Landsc Ecol 23:717.
Lundberg J, Moberg F. 2003. Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6:87–98.
Mace GM. 2014. Whose conservation? Science 345:1558–60.
Maxwell PS, Eklöf JS, van Katwijk MM, O’brien KR, de la Torre-Castro M, Boström C, Bouma TJ, Krause-Jensen D, Unsworth RK, van Tussenbroek BI. 2017. The fundamental role of ecological feedback mechanisms for the adaptive management of seagrass ecosystems—a review. Biol Rev 92:1521–38.
Maxwell PS, Pitt KA, Burfeind DD, Olds AD, Babcock RC, Connolly RM. 2014. Phenotypic plasticity promotes persistence following severe events: physiological and morphological responses of seagrass to flooding. J Ecol 102:54–64.
Maxwell PS, Pitt KA, Olds AD, Rissik D, Connolly RM. 2015. Identifying habitats at risk: simple models can reveal complex ecosystem dynamics. Ecol Appl 25:573–87.
McCauley DJ, Young HS, Dunbar RB, Estes JA, Semmens BX, Micheli F. 2012. Assessing the effects of large mobile predators on ecosystem connectivity. Ecol Appl 22:1711–17.
Mellin C, Aaron MacNeil M, Cheal AJ, Emslie MJ, Julian Caley M. 2016. Marine protected areas increase resilience among coral reef communities. Ecol Lett 19:629–37.
Mumby PJ, Dahlgren CP, Harborne AR, Kappel CV, Micheli F, Brumbaugh DR, Holmes KE, Mendes JM, Broad K, Sanchirico JN, Buch K, Box S, Stoffle RW, Gill AB. 2006. Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101.
Nagelkerken I. 2009. Ecological connectivity among tropical coastal ecosystems. Berlin: Springer.
Nagelkerken I, Sheaves M, Baker R, Connolly RM. 2015. The seascape nursery: a novel spatial approach to identify and manage nurseries for coastal marine fauna. Fish Fish 16:362–71.
Olds AD, Connolly RM, Pitt KA, Maxwell PS. 2012a. Habitat connectivity improves reserve performance. Conserv Lett 5:56–63.
Olds AD, Connolly RM, Pitt KA, Maxwell PS. 2012b. Primacy of seascape connectivity effects in structuring coral reef fish assemblages. Mar Ecol Prog Ser 462:191–203.
Olds AD, Connolly RM, Pitt KA, Maxwell PS, Aswani S, Albert S. 2014. Incorporating surrogate species and seascape connectivity to improve marine conservation outcomes. Conserv Biol 28:982–91.
Olds AD, Nagelkerken I, Huijbers CM, Gilby BL, Pittman SJ, Schlacher TA. 2017. Connectivity in coastal seascapes. Seascape ecology. Hoboken: John Wiley & Sons.
Olds AD, Pitt KA, Maxwell PS, Connolly RM. 2012c. Synergistic effects of reserves and connectivity on ecological resilience. J Appl Ecol 49:1195–203.
Orth RJ, Carruthers TJ, Dennison WC, Duarte CM, Fourqurean JW, Heck KL, Hughes AR, Kendrick GA, Kenworthy WJ, Olyarnik S. 2006. A global crisis for seagrass ecosystems. BioScience 56:987–96.
Pages J, Gera A, Romero J, Alcoverro T. 2014. Matrix composition and patch edges influence plant–herbivore interactions in marine landscapes. Funct Ecol 28:1440–8.
Pillans R, Franklin C, Tibbetts I. 2004. Food choice in Siganus fuscescens: influence of macrophyte nutrient content and availability. J Fish Biol 64:297–309.
Poore AG, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA. 2012. Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–22.
Possingham HP, Franklin J, Wilson K, Regan TJ. 2005. The roles of spatial heterogeneity and ecological processes in conservation planning. Ecosystem function in heterogeneous landscapes. New York: Springer. pp 389–406.
Prado P, Farina S, Tomas F, Romero J, Alcoverro T. 2008. Marine protection and meadow size alter fish herbivory in seagrass ecosystems. Mar Ecol Prog Ser 371:11–21.
Pressey B, McCauley DJ, Morgan L, Possingham H, White L, Darling E. 2014. A to-do list for the world’s parks. Nature 515:28–31.
Ripple WJ, Estes JA, Beschta RL, Wilmers CC, Ritchie EG, Hebblewhite M, Berger J, Elmhagen B, Letnic M, Nelson MP. 2014. Status and ecological effects of the world’s largest carnivores. Science 343:1241484.
Rodrigues AS, Brooks TM. 2007. Shortcuts for biodiversity conservation planning: the effectiveness of surrogates. Ann Rev Ecol Evol Syst 38:713–37.
Roelfsema CM, Lyons M, Kovacs EM, Maxwell P, Saunders MI, Samper-Villarreal J, Phinn SR. 2014. Multi-temporal mapping of seagrass cover, species and biomass: A semi-automated object based image analysis approach. Remote Sens Environ 150:172–87.
Saunders MI, Bode M, Atkinson S, Klein CJ, Metaxas A, Beher J, Beger M, Mills M, Giakoumi S, Tulloch V, Possingham HP. 2017. Simple rules can guide whether land- or ocean-based conservation will best benefit marine ecosystems. PLoS Biol 15:e2001886.
Schlacher TA, Schoeman DS, Jones AR, Dugan JE, Hubbard DM, Defeo O, Peterson CH, Weston MA, Maslo B, Olds AD. 2014. Metrics to assess ecological condition, change, and impacts in sandy beach ecosystems. J Environ Manag 144:322–35.
Schlacher TA, Weston MA, Lynn D, Schoeman DS, Huijbers CM, Olds AD, Masters S, Connolly RM. 2015. Conservation gone to the dogs: when canids rule the beach in small coastal reserves. Biodivers Conserv 24:493–509.
Skilleter GA, Loneragan NR, Olds A, Zharikov Y, Cameron B. 2017. Connectivity between seagrass and mangroves influences nekton assemblages using nearshore habitats. Mar Ecol Prog Ser 573:25–43.
Stephens PA, Pettorelli N, Barlow J, Whittingham MJ, Cadotte MW. 2015. Management by proxy? The use of indices in applied ecology. J Appl Ecol 52:1–6.
Stevens T, Connolly RM. 2005. Local-scale mapping of benthic habitats to assess representation in a marine protected area. Mar Freshw Res 56:111–23.
Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batary P, Bengtsson J, Clough Y, Crist TO, Dormann CF. 2012. Landscape moderation of biodiversity patterns and processes-eight hypotheses. Biol Rev 87:661–85.
Unsworth RK, Cullen LC. 2010. Recognising the necessity for Indo-Pacific seagrass conservation. Conserv Lett 3:63–73.
Unsworth RK, Taylor JD, Powell A, Bell JJ, Smith DJ. 2007. The contribution of scarid herbivory to seagrass ecosystem dynamics in the Indo-Pacific. Estuar Coast Shelf Sci 74:53–62.
Unsworth RKF, Collier CJ, Waycott M, McKenzie LJ, Cullen-Unsworth LC. 2015. A framework for the resilience of seagrass ecosystems. Mar Pollut Bull 100:34–46.
Unsworth RKF, Salinas De León P, Garrard SL, Jompa J, Smith DJ, Bell JJ. 2008. High connectivity of Indo-Pacific seagrass fish assemblages with mangrove and coral reef habitats. Mar Ecol Prog Ser 353:213–24.
Valentine JF, Heck K, Blackmon D, Goecker ME, Christian J, Kroutil RM, Peterson BJ, Vanderklift MA, Kirsch KD, Beck M. 2008. Exploited species impacts on trophic linkages along reef-seagrass interfaces in the Florida Keys. Ecol Appl 18:1501–15.
Valentine JF, Heck KL, Busby J Jr, Webb D. 1997. Experimental evidence that herbivory increases shoot density and productivity in a subtropical turtlegrass (Thalassia testudinum) meadow. Oecologia 112:193–200.
Vergés A, Tomas F, Cebrian E, Ballesteros E, Kizilkaya Z, Dendrinos P, Karamanlidis AA, Spiegel D, Sala E. 2014. Tropical rabbitfish and the deforestation of a warming temperate sea. J Ecol 102:1518–27.
Waycott M, Duarte CM, Carruthers TJ, Orth RJ, Dennison WC, Olyarnik S, Calladine A, Fourqurean JW, Heck KL, Hughes AR. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proc Natl Acad Sci 106:12377–81.
Whalen MA, Duffy JE, Grace JB. 2013. Temporal shifts in top-down vs. bottom-up control of epiphytic algae in a seagrass ecosystem. Ecology 94:510–20.
Willis TJ, Babcock RC. 2000. A baited underwater video system for the determination of relative density of carnivorous reef fish. Mar Freshw Res 51:755–63.
Wood S. 2012. gamm4: generalized additive mixed models using mgcv and lme4. R package version 0.1-6.
Yabsley NA, Olds AD, Connolly RM, Martin TSH, Gilby BL, Maxwell PS, Huijbers CM, Schoeman DS, Schlacher TA. 2016. Resource type influences the effects of reserves and connectivity on ecological functions. J Anim Ecol 85:437–44.
Zuur AF, Ieno EN, Walker NJ, Saveliev AA, Smith GM. 2009. Mixed effects modelling for nested data. Mixed effects models and extensions in ecology with R. New York: Springer. pp 101–42.
We thank the three anonymous reviewers and the editor for their comments on this manuscript. We thank the staff of the Moreton Bay Research Station and K. Finlayson, E. Bell, N. Harcla-Goody, and B. Meteyard for field assistance. The Australian Rivers Institute and the Griffith University School of Environment funded the project.
Data for this paper are archived in the University of the Sunshine Coast Research Bank.
CH, TS, SYL, BG, PM, and AO conceived the idea; CH and BG performed the research; CH, TS, SYL, BG, and JW analysed the data; and CH, TS, SYL, BG, TS, RC, and AO wrote the paper.
Data for this article can be found at https://zenodo.org/record/2535950#.XDZ22vxx3OR.
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Henderson, C.J., Stevens, T., Lee, S.Y. et al. Optimising Seagrass Conservation for Ecological Functions. Ecosystems 22, 1368–1380 (2019). https://doi.org/10.1007/s10021-019-00343-3
- coastal ecosystems
- conservation prioritisation
- surrogate species