Advertisement

Ecosystems

pp 1–13 | Cite as

Optimising Seagrass Conservation for Ecological Functions

  • Christopher J. HendersonEmail author
  • Tim Stevens
  • Shing Y. Lee
  • Ben L. Gilby
  • Thomas A. Schlacher
  • Rod M. Connolly
  • Jan Warnken
  • Paul S. Maxwell
  • Andrew D. Olds
Article
  • 41 Downloads

Abstract

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.

Keywords

coastal ecosystems conservation prioritisation herbivory seagrass surrogate species fish 

Notes

Acknowledgements

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 Accessibility

Data for this paper are archived in the University of the Sunshine Coast Research Bank.

Supplementary material

10021_2019_343_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 20 kb)
10021_2019_343_MOESM2_ESM.docx (13 kb)
Supplementary material 2 (DOCX 12 kb)

References

  1. 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.CrossRefGoogle Scholar
  2. Aragones L, Marsh H. 2000. Impact of Dugong grazing and turtle cropping on tropical seagrass communities. Pac Conserv Biol 5:277–88.CrossRefGoogle Scholar
  3. 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.CrossRefGoogle Scholar
  4. Bartoń K. 2013. MuMIn: multi-model inference. R package version 1.9. 13. The comprehensive R archive network (CRAN). Vienna, Austria.Google Scholar
  5. 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.CrossRefGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.Google Scholar
  8. 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.CrossRefGoogle Scholar
  9. 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.CrossRefGoogle Scholar
  10. 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.CrossRefGoogle Scholar
  11. 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.CrossRefGoogle Scholar
  12. Caro T. 2010. Conservation by proxy: indicator, umbrella, keystone, flagship, and other surrogate species. Washington: Island Press.Google Scholar
  13. 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.CrossRefGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. Connolly RM, Hindell JS. 2006. Review of nekton patterns and ecological processes in seagrass landscapes. Estuar Coast Shelf Sci 68:433–44.CrossRefGoogle Scholar
  16. 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.CrossRefGoogle Scholar
  17. 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.CrossRefGoogle Scholar
  18. 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.CrossRefGoogle Scholar
  19. 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.CrossRefGoogle Scholar
  20. 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.CrossRefGoogle Scholar
  21. EHMP. 2016. Healthy waterways and catchments: ecosystem health monitoring program. Available at: http://healthywaterways.org.
  22. 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.CrossRefGoogle Scholar
  23. 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.CrossRefGoogle Scholar
  24. 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.Google Scholar
  25. 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.CrossRefGoogle Scholar
  26. 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.CrossRefGoogle Scholar
  27. 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.CrossRefGoogle Scholar
  28. 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.CrossRefGoogle Scholar
  29. 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.CrossRefGoogle Scholar
  30. 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.CrossRefGoogle Scholar
  31. 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.CrossRefGoogle Scholar
  32. Heck K, Hays G, Orth RJ. 2003. Critical evaluation of the nursery role hypothesis for seagrass meadows. Mar Ecol Prog Ser 253:123–36.CrossRefGoogle Scholar
  33. Heck K, Valentine J. 2007. The primacy of top-down effects in shallow benthic ecosystems. Estuar Coasts 30:371–81.CrossRefGoogle Scholar
  34. Heck KL, Valentine JF. 2006. Plant–herbivore interactions in seagrass meadows. J Exp Mar Biol Ecol 330:420–36.CrossRefGoogle Scholar
  35. 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.CrossRefGoogle Scholar
  36. 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.CrossRefGoogle Scholar
  37. Hoey AS, Bellwood DR. 2011. Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol Lett 14:267–73.CrossRefGoogle Scholar
  38. 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.CrossRefGoogle Scholar
  39. 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.CrossRefGoogle Scholar
  40. 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.CrossRefGoogle Scholar
  41. 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.CrossRefGoogle Scholar
  42. Leslie HM. 2005. A synthesis of marine conservation planning approaches. Conserv Biol 19:1701–13.CrossRefGoogle Scholar
  43. 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.CrossRefGoogle Scholar
  44. 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.CrossRefGoogle Scholar
  45. Lowenstein DM, Matteson KC, Minor ES. 2015. Diversity of wild bees supports pollination services in an urbanized landscape. Oecologia 179:811–21.CrossRefGoogle Scholar
  46. Lundberg J, Andersson E, Cleary G, Elmqvist T. 2008. Linkages beyond borders: targeting spatial processes in fragmented urban landscapes. Landsc Ecol 23:717.CrossRefGoogle Scholar
  47. Lundberg J, Moberg F. 2003. Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6:87–98.CrossRefGoogle Scholar
  48. Mace GM. 2014. Whose conservation? Science 345:1558–60.CrossRefGoogle Scholar
  49. 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.CrossRefGoogle Scholar
  50. 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.CrossRefGoogle Scholar
  51. 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.CrossRefGoogle Scholar
  52. 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.CrossRefGoogle Scholar
  53. 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.CrossRefGoogle Scholar
  54. 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.CrossRefGoogle Scholar
  55. Nagelkerken I. 2009. Ecological connectivity among tropical coastal ecosystems. Berlin: Springer.CrossRefGoogle Scholar
  56. 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.CrossRefGoogle Scholar
  57. Olds AD, Connolly RM, Pitt KA, Maxwell PS. 2012a. Habitat connectivity improves reserve performance. Conserv Lett 5:56–63.CrossRefGoogle Scholar
  58. 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.CrossRefGoogle Scholar
  59. 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.CrossRefGoogle Scholar
  60. Olds AD, Nagelkerken I, Huijbers CM, Gilby BL, Pittman SJ, Schlacher TA. 2017. Connectivity in coastal seascapes. Seascape ecology. Hoboken: John Wiley & Sons.Google Scholar
  61. Olds AD, Pitt KA, Maxwell PS, Connolly RM. 2012c. Synergistic effects of reserves and connectivity on ecological resilience. J Appl Ecol 49:1195–203.CrossRefGoogle Scholar
  62. 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.CrossRefGoogle Scholar
  63. 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.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. 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.CrossRefGoogle Scholar
  66. 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.CrossRefGoogle Scholar
  67. 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.CrossRefGoogle Scholar
  68. 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.CrossRefGoogle Scholar
  69. 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.CrossRefGoogle Scholar
  70. Rodrigues AS, Brooks TM. 2007. Shortcuts for biodiversity conservation planning: the effectiveness of surrogates. Ann Rev Ecol Evol Syst 38:713–37.CrossRefGoogle Scholar
  71. 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.CrossRefGoogle Scholar
  72. 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.CrossRefGoogle Scholar
  73. 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.CrossRefGoogle Scholar
  74. 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.CrossRefGoogle Scholar
  75. 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.CrossRefGoogle Scholar
  76. 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.CrossRefGoogle Scholar
  77. 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.CrossRefGoogle Scholar
  78. 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.CrossRefGoogle Scholar
  79. Unsworth RK, Cullen LC. 2010. Recognising the necessity for Indo-Pacific seagrass conservation. Conserv Lett 3:63–73.CrossRefGoogle Scholar
  80. 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.CrossRefGoogle Scholar
  81. 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.CrossRefGoogle Scholar
  82. 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.CrossRefGoogle Scholar
  83. 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.CrossRefGoogle Scholar
  84. 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.CrossRefGoogle Scholar
  85. 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.CrossRefGoogle Scholar
  86. 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.CrossRefGoogle Scholar
  87. 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.CrossRefGoogle Scholar
  88. 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.CrossRefGoogle Scholar
  89. Wood S. 2012. gamm4: generalized additive mixed models using mgcv and lme4. R package version 0.1-6.Google Scholar
  90. 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.CrossRefGoogle Scholar
  91. 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.Google Scholar

Copyright information

© Springer Science+Business Media, LLC, part of Springer Nature 2019

Authors and Affiliations

  • Christopher J. Henderson
    • 1
    • 2
    • 3
    Email author
  • Tim Stevens
    • 1
  • Shing Y. Lee
    • 1
    • 4
  • Ben L. Gilby
    • 2
    • 3
  • Thomas A. Schlacher
    • 2
    • 3
  • Rod M. Connolly
    • 1
  • Jan Warnken
    • 1
  • Paul S. Maxwell
    • 5
  • Andrew D. Olds
    • 2
    • 3
  1. 1.Australian Rivers Institute—Coasts and Estuaries and Griffith School of EnvironmentGriffith UniversitySouthportAustralia
  2. 2.School of Science and EngineeringUniversity of the Sunshine CoastMaroochydoreAustralia
  3. 3.The ANIMAL Centre—Health, Ecology and Conservation ResearchUniversity of the Sunshine CoastMaroochydoreAustralia
  4. 4.Simon FS Li Marine Science Laboratory, School of Life Sciences, and Earth System Science ProgrammeThe Chinese University of Hong KongShatinChina
  5. 5.Healthy Land and WaterBrisbaneAustralia

Personalised recommendations