Advertisement

Landscape Ecology

, Volume 33, Issue 8, pp 1273–1286 | Cite as

Habitat proximity exerts opposing effects on key ecological functions

  • Tyson S. H. MartinEmail author
  • Andrew D. Olds
  • Asier B. H. Olalde
  • Charlotte Berkström
  • Ben L. Gilby
  • Thomas A. Schlacher
  • Ian R. Butler
  • Nicholas A. Yabsley
  • Maria Zann
  • Rod M. Connolly
Research Article

Abstract

Context

Connectivity is an important property of landscapes that shapes populations and ecosystem functioning. We do not know, however, whether and how different types of spatial linkages combine to influence ecological functions, and this hampers their integration into conservation planning.

Objectives

We used coral reef seascapes in eastern Australia as a model system to test whether the proximity of other reefs (habitat proximity) or the proximity of other habitats (seascape proximity) exert stronger effects on two key ecological functions (herbivory and piscivory).

Methods

We measured rates of herbivory (on fleshy macroalgae) and piscivory (on prey fish) on reefs that differed in their proximity to both other reefs and nearby mangroves and seagrass.

Results

The extent of habitat proximity between reefs significantly influenced both ecological functions, but in different ways: isolated reefs supported high herbivory but low piscivory, whilst, conversely, reefs that were closer to other reefs supported high piscivory but low herbivory. This was not caused by herbivores avoiding their predators, as the dominant piscivores (small predatory snappers) were too small to consume the dominant herbivores (large rabbitfishes). Seascape proximity (e.g., distance to mangroves or seagrass) was less important in shaping ecological functions on reefs in this system.

Conclusions

We suggest that the effects of seascape configuration on ecological functions depends on the type of spatial linkage, and the ecological functions in question. To better integrate connectivity into conservation, we must develop a deeper understanding of how different spatial linkages combine to shape ecosystem functioning across landscapes.

Keywords

Seascape Predation Herbivory Fish Coral reefs Asymmetry Connectivity 

Notes

Acknowledgements

We thank A. Delaforce, A. Martin, K. Martin, C. Mapstone, R. Murphy and I. Pollard-Palmer for field assistance, and S. Engelhard, K. Gleeson and C. Henderson for helpful discussion of the manuscript. This study was funded by an Australian Postgraduate Award (TM). This research was carried out in accordance with Griffith University Ethics Guidelines under Ethics Approval ENV/02/16/AEC and conducted in accordance with Great Sandy Strait Marine Park Research Permit QS2016/GS065.

Supplementary material

10980_2018_680_MOESM1_ESM.docx (49 kb)
Supplementary material 1 (DOCX 49 kb)

References

  1. Baker R, Sheaves M (2007) Shallow-water refuge paradigm: conflicting evidence from tethering experiments in a tropical estuary. Mar Ecol Prog Ser 349:13–22CrossRefGoogle Scholar
  2. Beger M, Linke S, Watts M, Game E, Treml E, Ball I, Possingham HP (2010) Incorporating asymmetric connectivity into spatial decision making for conservation. Conserv Lett 3(5):359–368CrossRefGoogle Scholar
  3. Bélisle M (2005) Measuring landscape connectivity: the challenge of behavioural landscape ecology. Ecology 86(8):1988–1995CrossRefGoogle Scholar
  4. Bennett AF (1999) Linkages in the landscape: the role of corridors and connectivity in wildlife conservation. IUCN, NorwichGoogle Scholar
  5. Bennett S, Bellwood DR (2011) Latitudinal variation in macroalgal consumption by fishes on the Great Barrier Reef. Mar Ecol Prog Ser 426:241–252CrossRefGoogle Scholar
  6. Berkstrom C, Gullstrom G, Lindborg R, Mwandya AW, Yahya SA, Kautsky N, Nystrom M (2012) Exploring ‘knowns’ and ‘unknowns’ in tropical seascape connectivity with insights from East African coral reefs. Estuar Coast Shelf Sci 107:1–21CrossRefGoogle Scholar
  7. Berkstrom C, Lindborg R, Thyresson M, Gullstrom M (2013) Assessing connectivity in a tropical embayment: fish migrations and seascape ecology. Biol Conserv 166:43–53CrossRefGoogle Scholar
  8. Bernhardt JR, Leslie HM (2013) Resilience to climate change in coastal marine ecosystems. Annu Rev Mar Sci 5:371–392CrossRefGoogle Scholar
  9. Bosiger YJ, McCormick MI (2014) Temporal links in daily activity patterns between coral reef predators and their prey. PLoS ONE 9(10):e111723CrossRefPubMedPubMedCentralGoogle Scholar
  10. Bostrom C, Pittman SJ, Simenstad C, Kneib RT (2011) Seascape ecology of coastal biogenic habitats: advances, gaps, and challenges. Mar Ecol Prog Ser 427:191–217CrossRefGoogle Scholar
  11. Bregman TP, Lees AC, MacGregor HEA, Darski B, de Moura NG, Aleixo A, Barlow J, Tobias JA (2016) Using avian functional traits to assess the impact of land-cover change on ecosystem processes linked to resilience in tropical forests. Proc R Soc B.  https://doi.org/10.1098/rspb.2016.1289 CrossRefPubMedGoogle Scholar
  12. Brudvig LA, Damschen EI, Tewksbury JJ, Haddad NM, Levey DJ (2009) Landscape connectivity promotes plant biodiversity spillover into non-target habitats. Proc Natl Acad Sci USA 106:9328–9332CrossRefPubMedGoogle Scholar
  13. Burkholder DA, Heithaus MR, Fourqurean JW, Wirsing A, Dill LM (2013) Patterns of top-down control in a seagrass ecosystem: could a roving apex predator induce a behaviour-mediated trophic cascade? J Anim Ecol 82(6):1192–1202CrossRefPubMedGoogle Scholar
  14. Butler IR, Sommer B, Zann M, Zhao JX, Pandolfi JM (2013) The impacts of flooding on the high-latitude, terrigenoclastic influenced coral reefs of Hervey Bay, Queensland, Australia. Coral Reefs 32(4):1149–1163CrossRefGoogle Scholar
  15. Calabrese JM, Fagan WF (2004) A comparison-shopper's guide to connectivity metrics. Front Ecol Environ 2:529–536CrossRefGoogle Scholar
  16. Campbell SJ, McKenzie LJ (2004) Flood related loss and recovery of intertidal seagrass meadows in southern Queensland, Australia. Estuar Coast Shelf Sci 60:477–490CrossRefGoogle Scholar
  17. Christianen MJA, Herman PMJ, Bouma TJ, Lamers LPM, van Katwijk MM, van der Heide T, Mumby PJ, Silliman BR, Engelhard SL, van de Kerk M, Kiswara W, van de Koppel J (2014) Habitat collapse due to overgrazing threatens turtle conservation in marine protected areas. Proc R Soc B 281(1777):20132890CrossRefPubMedGoogle Scholar
  18. Crooks KR, Sanjayan M (2006) Connectivity conservation: maintaining connections for nature. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  19. Cumming GS (2011) Spatial resilience: integrating landscape ecology, resilience, and sustainability. Landscape Ecol 26(7):899–909CrossRefGoogle Scholar
  20. Davis JP, Pitt KA, Fry B, Olds AD, Connolly R (2014) Seascape-scale trophic links for fish on inshore coral reefs. Coral Reefs 33(4):897–907CrossRefGoogle Scholar
  21. Dorenbosch M, Grol MGG, de Groene A, van der Velde G, Nagelkerken I (2009) Piscivore assemblages and predation pressure affect relative safety of some back-reef habitats for juvenile fish in a Caribbean Bay. Mar Ecol Prog Ser 379:181–196CrossRefGoogle Scholar
  22. Downie RA, Babcock RC, Thomson DP, Vanderklift MA (2013) Density of herbivorous fish and intensity of herbivory are influenced by proximity to coral reefs. Mar Ecol Prog Ser 482:217–225CrossRefGoogle Scholar
  23. Dupuch A, Bertolo A, Magnan P, Dill LM (2014) Indirect effects of asymmetrical competition among top predators determine spatial patterns of predation risk for prey. Aquat Sci 76(4):543–552CrossRefGoogle Scholar
  24. Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. J Anim Ecol 77(4):802–813CrossRefPubMedGoogle Scholar
  25. Engelhard SL, Huijbers CM, Stewart-Koster B, Olds AD, Schlacher TA, Connolly RM (2017) Prioritising seascape connectivity in conservation using network analysis. J Appl Ecol.  https://doi.org/10.1111/1365-2664.12824 CrossRefGoogle Scholar
  26. Ferreras P (2001) Landscape structure and asymmetrical inter-patch connectivity in a metapopulation of the endangered Iberian lynx. Biol Conserv 100(1):125–136CrossRefGoogle Scholar
  27. Fox RJ, Bellwood DR (2008) Remote video bioassays reveal the potential feeding impact of the rabbitfish Siganus canaliculatus (f: Siganidae) on an inner-shelf reef of the Great Barrier Reef. Coral Reefs 27(3):605–615CrossRefGoogle Scholar
  28. Froese R, Pauly D (2000) FishBase 2000: concepts, design and data sources. ICLARM, Los Baños, p 344Google Scholar
  29. Gilby BL, Tibbetts IR, Stevens T (2017) Low functional redundancy and high variability in Sargassum browsing fish populations in a subtropical reef system. Mar Freshw Res 68:331–341CrossRefGoogle Scholar
  30. Grober-Dunsmore R, Frazer TK, Lindberg WJ, Beets J (2007) Reef fish and habitat relationships in a Caribbean seascape: the importance of reef context. Coral Reefs 26(1):201–216CrossRefGoogle Scholar
  31. Grober-Dunsmore R, Pittman SJ, Caldow C, Kendall MS, Frazer TK (2009) A landscape ecology approach for the study of ecological connectivity across tropical marine seascapes. In: Nagelkerken I (ed) Ecological connectivity among tropical coastal ecosystems. Springer, New York, pp 493–530CrossRefGoogle Scholar
  32. Hammerschlag N, Morgan AB, Serafy JE (2010) Relative predation risk for fishes along a subtropical mangrove-seagrass ecotone. Mar Ecol Prog Ser 401:259–267CrossRefGoogle Scholar
  33. Harrison HB, Williamson DH, Evans RD, Almany GR, Thorrold SR, Russ GR, Feldheim KA, van Herwerden L, Planes S, Srinivasan M, Berumen ML, Jones GP (2012) Larval export from marine reserves and the recruitment benefit for fish and fisheries. Curr Biol 22(11):1023–1028CrossRefPubMedGoogle Scholar
  34. Heithaus MR, Wirsing AJ, Dill LM (2012) The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem. Mar Freshw Res 63(11):1039–1050CrossRefGoogle Scholar
  35. Hoey AS, Bellwood DR (2010) Among-habitat variation in herbivory on Sargassum spp. on a mid-shelf reef in the northern Great Barrier Reef. Mar Biol 157(1):189–200CrossRefGoogle Scholar
  36. Hoey AS, Bellwood DR (2011) Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol Lett 14(3):267–273CrossRefPubMedGoogle Scholar
  37. Hosmer DW, Lemeshow S (2000) Introduction to the logistic regression model. In: Applied logistic regression. Wiley, Hoboken, p 1–30Google Scholar
  38. Igulu MM, Nagelkerken I, Dorenbosch M, Grol MGG, Harborne AR, Kimirei IA, Mumby PJ, Olds AD, Mgaya YD (2014) Mangrove habitat use by juvenile reef fish: meta-analysis reveals that tidal regime matters more than biogeographic region. PLoS ONE.  https://doi.org/10.1371/journal.pone.0114715 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Kleyheeg E, Treep J, de Jager M, Nolet BA, Soons MB (2017) Seed dispersal distributions resulting from landscape-dependent daily movement behaviour of a key vector species, Anas platyrhynchos. J Ecol.  https://doi.org/10.1111/1365-2745.12738 CrossRefGoogle Scholar
  40. Kool JT, Moilanen A, Treml EA (2013) Population connectivity: recent advances and new perspectives. Landscape Ecol 28(2):165–185CrossRefGoogle Scholar
  41. Krumme U (2009) Diel and tidal movements by fish and decapods linking tropical coastal ecosystems. In: Nagelkerken I (ed) Ecological connectivity among tropical coastal ecosystems. Springer, New York, pp 271–324CrossRefGoogle Scholar
  42. Kulbicki M, Guillemot N, Amand M (2005) A general approach to length–weight relationships for New Caledonian lagoon fishes. Cybium 29(3):235–252Google Scholar
  43. Lundberg J, Andersson E, Cleary G, Elmqvist T (2008) Linkages beyond borders: targeting spatial processes in fragmented urban landscapes. Landscape Ecol 23(6):717–726CrossRefGoogle Scholar
  44. Lundberg J, Moberg F (2003) Mobile link organisms and ecosystem functioning: implications for ecosystem resilience and management. Ecosystems 6(1):0087–0098CrossRefGoogle Scholar
  45. Madin EMP, Dill LM, Ridlon AD, Heithaus MR, Warner RR (2016) Human activities change marine ecosystems by altering predation risk. Glob Change Biol 22(1):44–60CrossRefGoogle Scholar
  46. Madin EMP, Madin JS, Booth DJ (2011) Landscape of fear visible from space. Sci Rep.  https://doi.org/10.1038/srep00014 PubMedPubMedCentralCrossRefGoogle Scholar
  47. Magris RA, Treml EA, Pressey RL, Weeks R (2016) Integrating multiple species connectivity and habitat quality into conservation planning for coral reefs. Ecography 39(7):649–664CrossRefGoogle Scholar
  48. Mantyka CS, Bellwood DR (2007) Macroalgal grazing selectivity among herbivorous coral reef fishes. Mar Ecol Prog Ser 352:177–185CrossRefGoogle Scholar
  49. Martin TSH, Olds AD, Pitt KA, Johnston AB, Butler IR, Maxwell PS, Connolly RM (2015) Effective protection of fish on inshore coral reefs depends on the scale of mangrove-reef connectivity. Mar Ecol Prog Ser 527:157–165CrossRefGoogle Scholar
  50. Massol F, Gravel D, Mouquet N, Cadotte MW, Fukami T, Leibold MA (2011) Linking community and ecosystem dynamics through spatial ecology. Ecol Lett 14(3):313–323CrossRefPubMedGoogle Scholar
  51. Michael PJ, Hyndes GA, Vanderklift MA, Vergés A (2013) Identity and behaviour of herbivorous fish influence large-scale spatial patterns of macroalgal herbivory in a coral reef. Mar Ecol Prog Ser 482:227–240CrossRefGoogle Scholar
  52. Moilanen A, Nieminen M (2002) Simple connectivity measures in spatial ecology. Ecology 83:1131–1145CrossRefGoogle Scholar
  53. Mueller T, Lenz J, Caprano T, Fiedler W, Böhning-Gaese K (2014) Large frugivorous birds facilitate functional connectivity of fragmented landscapes. J Appl Ecol 51(3):684–692CrossRefGoogle Scholar
  54. Nagelkerken I (2009) Evaluation of nursery function of mangroves and seagrass beds for tropical decapods and reef fishes: patterns and underlying mechanisms. In: Nagelkerken I (ed) Ecological connectivity among tropical coastal ecosystems. Springer, New York, pp 357–399CrossRefGoogle Scholar
  55. 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(2):362–371CrossRefGoogle Scholar
  56. Nystrom M, Folke C (2001) Spatial resilience of coral reefs. Ecosystems 4(5):406–417CrossRefGoogle Scholar
  57. Olds AD, Albert S, Maxwell PS, Pitt KA, Connolly RM (2013) Mangrove-reef connectivity promotes the effectiveness of marine reserves across the western Pacific. Glob Ecol Biogeogr 22(9):1040–1049CrossRefGoogle Scholar
  58. Olds AD, Connolly RM, Pitt KA, Maxwell PS (2012a) Habitat connectivity improves reserve performance. Conserv Lett 5(1):56–63CrossRefGoogle Scholar
  59. Olds AD, Connolly RM, Pitt KA, Maxwell PS (2012b) Primacy of seascape connectivity effects in structuring coral reef fish assemblages. Mar Ecol Prog Ser 462:191–203CrossRefGoogle Scholar
  60. Olds AD, Connolly RM, Pitt KA, Pittman SJ, Maxwell PS, Huijbers CM, Moore BR, Albert S, Rissik D, Babcock RC, Schlacher TA (2016) Quantifying the conservation value of seascape connectivity: a global synthesis. Glob Ecol Biogeogr 25(1):3–15CrossRefGoogle Scholar
  61. Olds AD, Nagelkerken I, Huijbers CM, Gilby BL, Schlacher TA (2017) Connectivity in coastal seascapes. In: Pittman SJ (ed) Seascape ecology: taking landscape ecology into the sea. Wiley, HobokenGoogle Scholar
  62. Olds AD, Pitt KA, Maxwell PS, Connolly RM (2012c) Synergistic effects of reserves and connectivity on ecological resilience. J Appl Ecol 49(6):1195–1203CrossRefGoogle Scholar
  63. Pagès JF, Gera A, Romero J, Alcoverro T (2014) Matrix composition and patch edges influence plant–herbivore interactions in marine landscapes. Funct Ecol 28(6):1440–1448CrossRefGoogle Scholar
  64. Paul V, Meyer K, Nelson S, Sanger H (1992) Deterrent effects of seaweed extracts and secondary metabolites on feeding by the rabbitfish Siganus spinus. In: Proceedings of the seventh international coral reef symposium, vol 2, p 867–874Google Scholar
  65. Pelicice FM, Latini JD, Agostinho AA (2015) Fish fauna disassembly after the introduction of a voracious predator: main drivers and the role of the invader’s demography. Hydrobiologia 746(1):271–283CrossRefGoogle Scholar
  66. Pérez-Hernández CG, Vergara PM, Saura S, Hernández J (2015) Do corridors promote connectivity for bird-dispersed trees? The case of Persea lingue in Chilean fragmented landscapes. Landscape Ecol 30(1):77–90CrossRefGoogle Scholar
  67. Peterson BJ, Valentine JF, Heck KL (2013) The snapper-grunt pump: habitat modification and facilitation of the associated benthic plant communities by reef-resident fish. J Exp Mar Biol Ecol 441:50–54CrossRefGoogle Scholar
  68. Pillans R, Franklin C, Tibbetts I (2004) Food choice in Siganus fuscescens: influence of macrophyte nutrient content and availability. J Fish Biol 64(2):297–309CrossRefGoogle Scholar
  69. Pittman SJ, Brown KA (2011) Multi-scale approach for predicting fish species distributions across coral reef seascapes. PLoS ONE.  https://doi.org/10.1371/journal.pone.0020583 CrossRefPubMedPubMedCentralGoogle Scholar
  70. Pittman SJ, Olds AD (2015) Seascape ecology of fishes on coral reefs. In: Mora C (ed) Ecology of fishes on coral reefs. Cambridge University Press, CambridgeGoogle Scholar
  71. Saura S, Pascual-Hortal L (2007) A new habitat availability index to integrate connectivity in landscape conservation planning: comparison with existing indices and application to a case study. Landsc Urban Plan 83:91–103CrossRefGoogle Scholar
  72. Sheaves M (2009) Consequences of ecological connectivity: the coastal ecosystem mosaic. Mar Ecol Prog Ser 391:107–115CrossRefGoogle Scholar
  73. Staddon P, Lindo Z, Crittenden PD, Gilbert F, Gonzalez A (2010) Connectivity, non-random extinction and ecosystem function in experimental metacommunities. Ecol Lett 13(5):543–552CrossRefPubMedGoogle Scholar
  74. Stuart-Smith RD, Barrett NS, Crawford CM, Frusher SD, Stevenson DG, Edgar GJ (2008) Spatial patterns in impacts of fishing on temperate rocky reefs: are fish abundance and mean size related to proximity to fisher access points? J Exp Mar Biol Ecol 365(2):116–125CrossRefGoogle Scholar
  75. Tewksbury JJ, Levey DJ, Haddad NM, Sargent S, Orrock JL, Weldon A, Danielson BJ, Brinkerhoff J, Damschen EI, Townsend P (2002) Corridors affect plants, animals, and their interactions in fragmented landscapes. Proc Natl Acad Sci USA 99:12923–12926CrossRefPubMedGoogle Scholar
  76. Tscharntke T, Tylianakis JM, Rand TA, Didham RK, Fahrig L, Batary P, Bengtsson J, Clough Y, Crist TO, Dormann CF, Ewers RM, Frund J, Holt RD, Holzschuh A, Klein AM, Kleijn D, Kremen C, Landis DA, Laurance W, Lindenmayer D, Scherber C, Sodhi N, Steffan-Dewenter I, Thies C, van der Putten WH, Westphal C (2012) Landscape moderation of biodiversity patterns and processes—eight hypotheses. Biol Rev 87(3):661–685CrossRefPubMedGoogle Scholar
  77. Valentine JF, Heck KL Jr, 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(6):1501–1515CrossRefPubMedGoogle Scholar
  78. Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH, Ballesteros E, Heck KL, Booth DJ, Coleman MA, Feary DA, Figueira W, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, van Sebille E, Gupta AS, Smale DA, Tomas F, Wernberg T, Wilson SK (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281(1789):20140846CrossRefPubMedGoogle Scholar
  79. Vuilleumier S, Possingham HP (2006) Does colonization asymmetry matter in metapopulations? Proc R Soc B 273(1594):1637–1642CrossRefPubMedGoogle Scholar
  80. White CA, Feller MC, Bayley S (2003) Predation risk and the functional response of elk–aspen herbivory. For Ecol Manag 181(1–2):77–97CrossRefGoogle Scholar
  81. 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(2):437–444CrossRefPubMedGoogle Scholar
  82. Zann M (2012) The use of remote sensing and field validation for mapping coral communities of Hervey Bay and the Great Sandy Strait and implications for coastal planning policy. Masters Thesis, The University of QueenslandGoogle Scholar
  83. Zann M, Phinn S, Done T, Roelfsema C (2017) Assessing coral reef conservation values and connectivity of Hervey Bay reefs, Hervey Bay, 2006–2011Google Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Tyson S. H. Martin
    • 1
    Email author
  • Andrew D. Olds
    • 2
  • Asier B. H. Olalde
    • 3
  • Charlotte Berkström
    • 3
    • 4
  • Ben L. Gilby
    • 2
  • Thomas A. Schlacher
    • 2
  • Ian R. Butler
    • 5
    • 6
  • Nicholas A. Yabsley
    • 2
  • Maria Zann
    • 7
  • Rod M. Connolly
    • 1
  1. 1.Australian Rivers Institute – Coast and Estuaries, and School of EnvironmentGriffith UniversityGold CoastAustralia
  2. 2.School of Science and EngineeringUniversity of the Sunshine CoastMaroochydoreAustralia
  3. 3.Department of Ecology, Environment & Plant SciencesStockholm UniversityStockholmSweden
  4. 4.Department of Aquatic ResourcesSwedish University of Agricultural SciencesÖregrundSweden
  5. 5.Research School of BiologyThe Australian National UniversityCanberraAustralia
  6. 6.CoraLogic Environmental ConsultingCookAustralia
  7. 7.Remote Sensing Research Centre, School Earth and Environmental SciencesThe University of QueenslandBrisbaneAustralia

Personalised recommendations