Skip to main content

Advertisement

Log in

Consumers decrease variability across space and turnover through time during coral reef succession

  • Original Research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Consumers play an integral role in mediating ecological succession—the change in community composition over time. As consumer populations are facing rapid decline in ecosystems around the world, understanding of their ecological role is becoming increasingly urgent. Increased understanding of how changes in consumer populations may influence community variability across space and turnover through time during succession is particularly important for coral reefs, which are among the most threatened ecosystems globally, and where fishes play vital roles in structuring benthic succession. Here, we examine how consumers influence coral reef succession by deploying 180 paired settlement tiles, caged (to exclude fishes larger than approximately 15 cm) and uncaged, within Palmyra Atoll, a remote marine wildlife refuge with previously documented high fish abundance, and monitored benthic community development one and three years after deployment. We found that excluding large fishes lead to lower alpha diversity and divergent community states across space (i.e.,, high beta diversity among caged tiles), suggesting that benthic fish feeding maintains local diversity but tends to homogenize community composition with dominance by crustose coralline algae. In addition, when fish were experimentally excluded, the developing benthic community exhibited a greater change in species composition over time (i.e., high temporal beta diversity), indicating that fish feeding tends to canalize community successional trajectories. Finally, the caged and uncaged tiles became more similar over time, suggesting that fish feeding plays a more important role during early succession. Our results demonstrate that the loss of large fishes, for example from overfishing, may result in benthic communities that are more variable across space and time. Increased variability could have important implications for ecosystem function and coral reef resilience in the face of escalating global stressors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of data and materials

All data are available at https://github.com/JamieMcDevittIrwin/McDevittIrwin_etal_PalmyraTileSuccession.

Code availability

All code for statistical analyses is available at https://github.com/JamieMcDevittIrwin/McDevittIrwin_etal_PalmyraTileSuccession.

References

  • Adam TC, Holbrook SJ, Burkepile DE et al (2022) Priority effects in coral-macroalgae interactions can drive alternate community paths in the absence of top–down control. Ecology. https://doi.org/10.1002/ecy.3831

    Article  PubMed  Google Scholar 

  • Albert S, Udy J, Tibbetts IR (2008) Responses of algal communities to gradients in herbivore biomass and water quality in Marovo Lagoon, Solomon Islands. Coral Reefs 27:73–82

    Article  Google Scholar 

  • Alberti J, Bakker ES, van Klink R et al (2017) Herbivore exclusion promotes a more stochastic plant community assembly in a natural grassland. Ecology 98:961–970

    Article  PubMed  Google Scholar 

  • Anderson KJ (2007) Temporal patterns in rates of community change during succession. Am Nat 169:780–793

    Article  PubMed  Google Scholar 

  • Arnold SN, Steneck RS, Mumby PJ (2010) Running the gauntlet: inhibitory effects of algal turfs on the processes of coral recruitment. Mar Ecol Prog Ser 414:91–105

    Article  Google Scholar 

  • Ashton GV, Freestone AL, Duffy JE et al (2022) Predator control of marine communities increases with temperature across 115 degrees of latitude. Science 376:1215–1219

    Article  CAS  PubMed  Google Scholar 

  • Baria MVB, Guest JR, Edwards AJ et al (2010) Caging enhances post-settlement survival of juveniles of the scleractinian coral Acropora tenuis. J Exp Mar Bio Ecol 394:149–153

    Article  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  • Belliveau SA, Paul VJ (2002) Effects of herbivory and nutrients on the early colonization of crustose coralline and fleshy algae. Mar Ecol Prog Ser 232:105–114

    Article  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833

    Article  CAS  PubMed  Google Scholar 

  • Berlow EL (1997) From canalization to contingency: historical effects in a successional rocky intertidal community. Ecol Monogr 67:435–460

    Article  Google Scholar 

  • Birrell CL, McCook LJ, Willis BL (2005) Effects of algal turfs and sediment on coral settlement. Mar Pollut Bull 51:408–414

    Article  CAS  PubMed  Google Scholar 

  • Bonaldo RM, Bellwood DR (2009) Dynamics of parrotfish grazing scars. Mar Biol 156:771–777

    Article  Google Scholar 

  • Burkepile DE, Hay ME (2006) Herbivore vs. nutrient control of marine primary producers: context-dependent effects. Ecology 87:3128–3139

    Article  PubMed  Google Scholar 

  • Burkepile DE, Hay ME (2008) Herbivore species richness and feeding complementarity affect community structure and function on a coral reef. Proc Natl Acad Sci USA 105:16201–16206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burkepile DE, Hay ME (2009) Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef. Mar Ecol Prog Ser 389:71–84

    Article  Google Scholar 

  • Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345–363

    Article  Google Scholar 

  • Ceccarelli DM, Jones GP, McCook LJ (2011) Interactions between herbivorous fish guilds and their influence on algal succession on a coastal coral reef. J Exp Mar Bio Ecol 399:60–67

    Article  Google Scholar 

  • Ceh J, Molis M, Dzeha TM, Wahl M (2005) Induction and reduction of anti-herbivore defenses in brown and red macroalgae off the Kenyan coast1. J Phycol 41:726–731

    Article  Google Scholar 

  • Chase JM, Biro EG, Ryberg WA, Smith KG (2009) Predators temper the relative importance of stochastic processes in the assembly of prey metacommunities. Ecol Lett 12:1210–1218

    Article  PubMed  Google Scholar 

  • Clements Frederic E (Frederic Edward) (1916) Plant succession; an analysis of the development of vegetation. No. 242(1916):56

  • Connell JH, Slatyer RO (1977) Mechanisms of succession in natural communities and their role in community stability and organization. Am Nat 111:1119–1144

    Article  Google Scholar 

  • De Cáceres M, Legendre P (2009) Associations between species and groups of sites: indices and statistical inference. Ecology 90:3566–3574

    Article  PubMed  Google Scholar 

  • Diaz-Pulido G, Harii S, McCook LJ, Hoegh-Guldberg O (2010) The impact of benthic algae on the settlement of a reef-building coral. Coral Reefs 29:203–208

    Article  Google Scholar 

  • Dijkstra JA, Westerman EL, Harris LG (2011) The effects of climate change on species composition, succession and phenology: a case study: climate Change Destabilizes Communities. Glob Chang Biol 17:2360–2369

    Article  Google Scholar 

  • Doropoulos C, Roff G, Bozec Y-M et al (2016) Characterizing the ecological trade-offs throughout the early ontogeny of coral recruitment. Ecol Monogr 86:20–44

    Article  Google Scholar 

  • Doropoulos C, Roff G, Visser M-S, Mumby PJ (2017) Sensitivity of coral recruitment to subtle shifts in early community succession. Ecology 98:304–314

    Article  PubMed  Google Scholar 

  • Dudgeon SR, Aronson RB, Bruno JF, Precht WF (2010) Phase shifts and stable states on coral reefs. Mar Ecol Prog Ser 413:201–216

    Article  Google Scholar 

  • Edwards CB, Friedlander AM, Green AG et al (2014) Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects. Proc Biol Sci 281:20131835

    CAS  PubMed  PubMed Central  Google Scholar 

  • Elmer F, Bell JJ, Gardner JPA (2018) Coral larvae change their settlement preference for crustose coralline algae dependent on availability of bare space. Coral Reefs 37:397–407

    Article  Google Scholar 

  • Estes JA, Terborgh J, Brashares JS et al (2011) Trophic downgrading of planet Earth. Science 333:301–306

    Article  CAS  PubMed  Google Scholar 

  • Evensen NR, Doropoulos C, Morrow KM (2019) Inhibition of coral settlement at multiple spatial scales by a pervasive algal competitor. Mar Ecol

  • Evensen NR, Vanwonterghem I, Doropoulos C et al (2021) Benthic micro- and macro-community succession and coral recruitment under overfishing and nutrient enrichment. Ecology 102:e03536

    Article  PubMed  Google Scholar 

  • Fox J, Weisberg S (2019) An R companion to applied regression

  • Fraser LH, Grime JP (1999) Interacting effects of herbivory and fertility on a synthesized plant community. J Ecol 87:514–525

    Article  Google Scholar 

  • Fukami T (2015) Historical contingency in community assembly: integrating niches, species pools, and priority effects. Annu Rev Ecol Evol Syst 46:1–23

    Article  Google Scholar 

  • Gleason HA (1926) The individualistic concept of the plant association. Bull Torrey Bot Club 53:7–26

    Article  Google Scholar 

  • Gouezo M, Golbuu Y, Fabricius K et al (2019) Drivers of recovery and reassembly of coral reef communities. Proc Biol Sci 286:20182908

    PubMed  PubMed Central  Google Scholar 

  • Higgins E, Scheibling RE, Desilets KM, Metaxas A (2019) Benthic community succession on artificial and natural coral reefs in the northern Gulf of Aqaba. Red Sea Plos One 14:e0212842

    Article  CAS  PubMed  Google Scholar 

  • Hixon MA, Brostoff WN (1996) Succession and herbivory: effects of differential fish grazing on hawaiian coral-reef algae. Ecol Monogr 66:67–90

    Article  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR et al (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933

    Article  CAS  PubMed  Google Scholar 

  • Hughes TP, Rodrigues MJ, Bellwood DR et al (2007) Phase shifts, herbivory, and the resilience of coral reefs to climate change. Curr Biol 17:360–365

    Article  CAS  PubMed  Google Scholar 

  • Jessen C, Roder C, Villa Lizcano JF et al (2013) In-situ effects of simulated overfishing and eutrophication on benthic coral reef algae growth, succession, and composition in the central red sea. PLoS One 8:e66992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koffel T, Boudsocq S, Loeuille N, Daufresne T (2018) Facilitation- vs. competition-driven succession: the key role of resource-ratio. Ecol Lett 21:1010–1021

    Article  PubMed  Google Scholar 

  • Kohler KE, Gill SM (2006) Coral point count with excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Comput Geosci 32:1259–1269

    Article  Google Scholar 

  • Legendre P (2019) A temporal beta-diversity index to identify sites that have changed in exceptional ways in space-time surveys. Ecol Evol 9:3500–3514

    Article  PubMed  PubMed Central  Google Scholar 

  • Leibold MA (1996) A graphical model of keystone predators in food webs: trophic regulation of abundance, incidence, and diversity patterns in communities. Am Nat 147:784–812

    Article  Google Scholar 

  • Lenth RV (2022) Estimated marginal means, aka least-squares means [R package emmeans version 1.7.4–1]

  • Levasseur M, Therriault J-C, Legendre L (1984) Hierarchical control of phytoplankton succession by physical factors. Mar Ecol Prog Ser 19:211–222

    Article  Google Scholar 

  • Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Monogr 56:183–200

    Article  Google Scholar 

  • Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci USA 100:12765–12770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Louette G, De Meester L (2007) Predation and priority effects in experimental zooplankton communities. Oikos 116:419–426

    Article  Google Scholar 

  • Lubchenco J (1978) Plant species diversity in a marine intertidal community: importance of herbivore food preference and algal competitive abilities. Am Nat 112:23–39

    Article  Google Scholar 

  • MacNeil MA, Graham NAJ, Cinner JE et al (2015) Recovery potential of the world’s coral reef fishes. Nature 520:341–344

    Article  CAS  PubMed  Google Scholar 

  • Marks KW, Lang JC (2005) AGRRA summary products version (08/2005). http://www.agrra.org

  • Makoto K, Wilson SD (2016) New multicentury evidence for dispersal limitation during primary succession. Am Nat 187:804–811

    Article  CAS  PubMed  Google Scholar 

  • McCauley DJ, Micheli F, Young HS et al (2010) Acute effects of removing large fish from a near-pristine coral reef. Mar Biol 157:2739–2750

    Article  PubMed  PubMed Central  Google Scholar 

  • McCauley DJ, Hoffmann E, Young HS, Micheli F (2012) Night shift: expansion of temporal niche use following reductions in predator density. PLoS One 7:e38871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCauley DJ, Gellner G, Martinez ND et al (2018) On the prevalence and dynamics of inverted trophic pyramids and otherwise top-heavy communities. Ecol Lett 21:439–454

    Article  PubMed  Google Scholar 

  • McDevitt-Irwin JM, McCauley DM, Brumbaugh DR et al (In Review). Temporally variable effects of fishes on coral recruitment patterns

  • Menge BA, Lubchenco J, Ashkenas LR, Ramsey F (1986) Experimental separation of effects of consumers on sessile prey in the low zone of a rocky shore in the Bay of Panama: direct and indirect consequences of food web complexity. J Exp Mar Bio Ecol 100:225–269

    Article  Google Scholar 

  • Mortensen B, Danielson B, Harpole WS et al (2018) Herbivores safeguard plant diversity by reducing variability in dominance. J Ecol 106:101–112

    Article  CAS  Google Scholar 

  • Mumby PJ (2009) Phase shifts and the stability of macroalgal communities on Caribbean coral reefs. Coral Reefs 28:761–773

    Article  Google Scholar 

  • Mumby PJ, Dahlgren CP, Harborne AR et al (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101

    Article  CAS  PubMed  Google Scholar 

  • Mumby PJ, Harborne AR, Williams J et al (2007) Trophic cascade facilitates coral recruitment in a marine reserve. Proc Natl Acad Sci 104:8362–8367

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Connor NE, Donohue I, Crowe TP, Emmerson MC (2011) Importance of consumers on exposed and sheltered rocky shores. Mar Ecol Prog Ser 443:65–75

    Article  Google Scholar 

  • Paine RT (1966) Food web complexity and species diversity. Am Nat 100:65–75

    Article  Google Scholar 

  • Plass-Johnson JG, Heiden JP, Abu N et al (2016) Experimental analysis of the effects of consumer exclusion on recruitment and succession of a coral reef system along a water quality gradient in the Spermonde Archipelago, Indonesia. Coral Reefs 35:229–243

    Article  Google Scholar 

  • Price N (2010) Habitat selection, facilitation, and biotic settlement cues affect distribution and performance of coral recruits in French Polynesia. Oecologia 163:747–758

    Article  PubMed  PubMed Central  Google Scholar 

  • Roff G, Doropoulos C, Zupan M et al (2015) Phase shift facilitation following cyclone disturbance on coral reefs. Oecologia 178:1193–1203

    Article  PubMed  Google Scholar 

  • Russ GR (2003) Grazer biomass correlates more strongly with production than with biomass of algal turfs on a coral reef. Coral Reefs 22:63–67

    Article  Google Scholar 

  • Sandin SA, Smith JE, Demartini EE et al (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS One 3:e1548

    Article  PubMed  PubMed Central  Google Scholar 

  • Smith J, Smith C, Hunter C (2001) An experimental analysis of the effects of herbivory and nutrient enrichment on benthic community dynamics on a Hawaiian reef. Coral Reefs 19:332–342

    Article  Google Scholar 

  • Smith JE, Hunter CL, Smith CM (2010) The effects of top-down versus bottom-up control on benthic coral reef community structure. Oecologia 163:497–507

    Article  PubMed  Google Scholar 

  • Sousa WP (1979) Experimental investigations of disturbance and ecological succession in a rocky intertidal algal community. Ecol Monogr 49:227–254

    Article  Google Scholar 

  • Speed JDM, Austrheim G, Mysterud A (2013) The response of plant diversity to grazing varies along an elevational gradient. J Ecol 101:1225–1236

    Article  Google Scholar 

  • Steneck RS, Arnold SN, Mumby PJ (2014) Experiment mimics fishing on parrotfish: insights on coral reef recovery and alternative attractors. Mar Ecol Prog Ser 506:115–127

    Article  Google Scholar 

  • Stevenson C, Katz LS, Micheli F, et al (2007) High apex predator biomass on remote Pacific islands. Coral Reefs

  • Stier AC, Hanson KM, Holbrook SJ et al (2014) Predation and landscape characteristics independently affect reef fish community organization. Ecology 95:1294–1307

    Article  PubMed  Google Scholar 

  • Terborgh JW (2015) Toward a trophic theory of species diversity. Proc Natl Acad Sci 112:11415–11422

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trapon ML, Pratchett MS, Hoey AS, Baird AH (2013) Influence of fish grazing and sedimentation on the early post-settlement survival of the tabular coral Acropora cytherea. Coral Reefs 32:1051–1059

    Article  Google Scholar 

  • Villar N, Siqueira T, Zipparro V et al (2020) The cryptic regulation of diversity by functionally complementary large tropical forest herbivores. J Ecol 108:279–290

    Article  Google Scholar 

  • Wakwella A, Mumby PJ, Roff G (2020) Sedimentation and overfishing drive changes in early succession and coral recruitment. Proc Biol Sci 287:20202575

    PubMed  PubMed Central  Google Scholar 

  • Williams I, Polunin N (2001) Large-scale associations between macroalgal cover and grazer biomass on mid-depth reefs in the Caribbean. Coral Reefs 19:358–366

    Article  Google Scholar 

  • Williams ID, Richards BL, Sandin SA et al (2010) Differences in reef fish assemblages between populated and remote reefs spanning multiple archipelagos across the central and western pacific. J Mar Biol. https://doi.org/10.1155/2011/826234

    Article  Google Scholar 

  • Williams ID, Baum JK, Heenan A et al (2015) Human, oceanographic and habitat drivers of central and western Pacific coral reef fish assemblages. PLoS One 10:e0120516

    Article  PubMed  PubMed Central  Google Scholar 

  • Yang LH (2020) Toward a more temporally explicit framework for community ecology. Ecol Res 35:445–462

    Article  Google Scholar 

  • Zander A, Gravel D, Bersier L-F, Gray SM (2016) Top predators affect the composition of naive protist communities, but only in their early-successional stage. Oecologia 180:519–528

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank Alan Nunez and Victoria Dubeau for help with CPCe classification and Sabina Perkins, Paul Leary and Ana Sofia Guerra for help in the field. We thank Tadashi Fukami for helpful discussion and feedback on statistical analyses and interpretation of results.

Funding

This work was supported through funding by the Reef Tomorrow Initiative, through a grant from the Gordon and Betty Moore Foundation and a National Sciences and Engineering Research Council of Canada Postgraduate Scholarship for JMI, and a grant from the Bertarelli Foundation.

Author information

Authors and Affiliations

Authors

Contributions

JMI wrote the initial draft and performed the analyses while DM, DB, FE, FF, FJ, TW, JW and FM collected the data and contributed to the writing.

Corresponding author

Correspondence to Jamie M. McDevitt-Irwin.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethics approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Additional information

Communicated by Jonathan Shurin.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (PDF 2673 KB)

Supplementary file2 (PDF 13165 KB)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

McDevitt-Irwin, J.M., McCauley, D.J., Brumbaugh, D.R. et al. Consumers decrease variability across space and turnover through time during coral reef succession. Oecologia 202, 431–443 (2023). https://doi.org/10.1007/s00442-023-05404-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-023-05404-y

Keywords

Navigation