Skip to main content
SpringerLink
Log in

Investigating functional redundancy versus complementarity in Hawaiian herbivorous coral reef fishes

  • Community ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

Patterns of species resource use provide insight into the functional roles of species and thus their ecological significance within a community. The functional role of herbivorous fishes on coral reefs has been defined through a variety of methods, but from a grazing perspective, less is known about the species-specific preferences of herbivores on different groups of reef algae and the extent of dietary overlap across an herbivore community. Here, we quantified patterns of redundancy and complementarity in a highly diverse community of herbivores at a reef on Maui, Hawaii, USA. First, we tracked fish foraging behavior in situ to record bite rate and type of substrate bitten. Second, we examined gut contents of select herbivorous fishes to determine consumption at a finer scale. Finally, we placed foraging behavior in the context of resource availability to determine how fish selected substrate type. All species predominantly (73–100 %) foraged on turf algae, though there were differences among the types of macroalgae and other substrates bitten. Increased resolution via gut content analysis showed the composition of turf algae consumed by fishes differed across herbivore species. Consideration of foraging behavior by substrate availability revealed 50 % of herbivores selected for turf as opposed to other substrate types, but overall, there were variable foraging portfolios across all species. Through these three methods of investigation, we found higher complementarity among herbivorous fishes than would be revealed using a single metric. These results suggest differences across species in the herbivore “rain of bites” that graze and shape benthic community composition.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adam TC, Kelley M, Ruttenberg BI, Burkepile DE (2015) Resource partitioning along multiple niche axes drives functional diversity in parrotfishes on Caribbean coral reefs. Oecologia. doi:10.1007/s00442-015-3406-3

    PubMed  Google Scholar 

  • Adey W, Steneck RS (1985) Highly productive eastern Caribbean reefs: synergistic effects of biological, chemical, physical, and geological factors. In: Reaka M (ed) The ecology of deep and shallow coral reefs, 2nd edn. NOAA Undersea Research Program, Rockville, pp 163–187

    Google Scholar 

  • Aguilera MA, Navarrete SA (2012) Functional identity and functional structure change through succession in a rocky intertidal marine herbivore assemblage. Ecology 93:75–89. doi:10.1890/11-0434.1

    Article  PubMed  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E, Plymouth, UK

    Google Scholar 

  • Andrew MH (1988) Grazing impact in relation to livestock watering points. Trends Ecol Evol 3:336–339

    Article  CAS  PubMed  Google Scholar 

  • Arsenault R, Owen-Smith N (2002) Facilitation versus competition in grazing herbivore assemblages. Oikos 97:313–318

    Article  Google Scholar 

  • Barott K, Smith J, Dinsdale E et al (2009) Hyperspectral and physiological analyses of coral-algal interactions. PLoS One. doi:10.1371/journal.pone.0008043

    PubMed  PubMed Central  Google Scholar 

  • Bellwood DR (1994) A phylogenetic study of the parrotfish family Scaridae (Pisces: Labroidea), with a revision of genera. Rec Aust Museum Suppl 20:1–86. doi:10.3853/j.0812-7387.20.1994.51

    Article  Google Scholar 

  • Bellwood DR (1995) Direct estimate of bioerosion by two parrotfish species, Chlorurus gibbus and C. sordidus, on the Great Barrier Reef, Australia. Mar Biol 121:419–429. doi:10.1007/BF00349451

    Article  Google Scholar 

  • Bellwood DR, Choat JH (1990) A functional analysis of grazing in parrotfishes (family Scaridae): the ecological implications. Environ Biol Fishes 28:189–214. doi:10.1007/BF00751035

    Article  Google Scholar 

  • Bellwood DR, Hughes TP, Folke C, Nyström M (2004) Confronting the coral reef crisis. Nature 429:827–833. doi:10.1038/nature02691

    Article  CAS  PubMed  Google Scholar 

  • Brandl SJ, Bellwood DR (2014) Individual-based analyses reveal limited functional overlap in a coral reef fish community. J Anim Ecol. doi:10.1111/1365-2656.12171

    PubMed  Google Scholar 

  • Brandl SJ, Robbins WD, Bellwood DR (2015) Exploring the nature of ecological specialization in a coral reef fish community: morphology, diet and foraging microhabitat use. Proc R Soc B 282:20151147

    Article  PubMed  PubMed Central  Google Scholar 

  • Bruggemann JH, Kuyper MWM, Breeman AM (1994a) Comparative analysis of foraging and habitat use by the sympatric Caribbean parrotfish Scarus vetula and Sparisoma viride (Scaridae). Mar Ecol Ser 112:51–66

    Article  Google Scholar 

  • Bruggemann JH, Vanoppen MJH, Breeman AM (1994b) Foraging by the stoplight-parrotfish Sparisoma viride. 1. Food selection in different socially determined habitats. Mar Ecol Prog Ser 106:41–56. doi:10.3354/meps106041

    Article  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. doi:10.1073/pnas.0801946105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burkepile DE, Hay ME (2010) Impact of herbivore identity on algal succession and coral growth on a Caribbean reef. PLoS One 5:1–9. doi:10.1371/journal.pone.0008963

    Article  Google Scholar 

  • Burkepile DE, Hay ME (2011) Feeding complementarity versus redundancy among herbivorous fishes on a Caribbean reef. Coral Reefs 30:351–362. doi:10.1007/s00338-011-0726-6

    Article  Google Scholar 

  • Carpenter RC (1986) Partitioning herbivory and its effects on coral reef algal communities. Ecol Monogr 56:345–364

    Article  Google Scholar 

  • Chase JM, Leibold MA (2003) Ecological niches: linking classical and contemporary approaches. University of Chicago Press, Chicago, IL, 212 pp

    Book  Google Scholar 

  • Chesson J (1978) Measuring preference in selective predation. Ecology 59:211–215

    Article  Google Scholar 

  • Chesson J (1983) The estimation and analysis of preference and its relatioship to foraging models. Ecology 64:1297–1304. doi:10.2307/1937838

    Article  Google Scholar 

  • Choat JH, Clements KD, Robbins WD (2002) The trophic status of herbivorous fishes on coral reefs 1: dietary analyses. Mar Biol 140:613–623. doi:10.1007/s00227-001-0715-3

    Article  CAS  Google Scholar 

  • Choat JH, Robbins WD, Clements KD (2004) The trophic status of herbivorous fishes on coral reefs: II. Food processing modes and trophodynamics. Mar Biol 145:445–454. doi:10.1007/s00227-004-1341-7

    Article  Google Scholar 

  • Chong-Seng KM, Nash KL, Bellwood DR, Graham NAJ (2014) Macroalgal herbivory on recovering versus degrading coral reefs. Coral Reefs 33:409–419. doi:10.1007/s00338-014-1134-5

    Article  Google Scholar 

  • Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. PRIMER-E, Plymouth, UK, 192 pp

  • Clarke KR, Somerfield PJ, Chapman MG (2006) On resemblance measures for ecological studies, including taxonomic dissimilarities and a zero-adjusted Bray-Curtis coefficient for denuded assemblages. J Exp Mar Biol Ecol 330:55–80

    Article  Google Scholar 

  • Clements KD, Raubenheimer D, Choat JH (2009) Nutritional ecology of marine herbivorous fishes: 10 years on. Funct Ecol 23:79–92. doi:10.1111/j.1365-2435.2008.01524.x

    Article  Google Scholar 

  • Conklin EJ, Smith JE (2005) Abundance and spread of the invasive red algae, Kappaphycus spp., in Kane’ohe Bay, Hawai’i and an experimental assessment of management options. Biol Invasions 7:1029–1039. doi:10.1007/s10530-004-3125-x

    Article  Google Scholar 

  • Dailer ML, Knox RS, Smith JE et al (2010) Using ∂15 N values in algal tissue to map locations and potential sources of anthropogenic nutrient inputs on the island of Maui, Hawai’i, USA. Mar Pollut Bull 60:655–671. doi:10.1016/j.marpolbul.2009.12.021

    Article  CAS  PubMed  Google Scholar 

  • Du Toit JT, Cumming DHM (1999) Functional significance of ungulate diversity in African savannas and the ecological implications of the spread of pastoralism. Biodivers Conserv 8:1643–1661

    Article  Google Scholar 

  • Duffy JE, Macdonald KS, Rhode JM, Parker JD (2001) Grazer diversity, functional redundancy, and productivity in seagrass beds: an experimental test. Ecology 82:2417–2434

    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. doi:10.1098/rspb.2013.1835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Frank DA, McNaughton SJ, Tracy BF (1998) The ecology of the Earth’s grazing ecosystems. Bioscience 48:513–521

    Article  Google Scholar 

  • Green AL, Bellwood DR (2009) Monitoring functional groups of herbivorous reef fishes as indicators of coral reef resilience: a practical guide for coral reef managers in the Asia Pacific Region

  • Haas A, El-Zibdah M, Wild C (2010) Seasonal monitoring of coral-algae interactions in fringing reefs of the Gulf of Aqaba, Northern Red Sea. Coral Reefs 29:93–103. doi:10.1007/s00338-009-0556-y

    Article  Google Scholar 

  • Hamilton SL, Smith JE, Price NN, Sandin SA (2014) Quantifying patterns of fish herbivory on Palmyra Atoll (USA), an uninhabited predator-dominated central Pacific coral reef. Mar Ecol Prog Ser 501:141–155. doi:10.3354/meps10684

    Article  Google Scholar 

  • Harris JL, Lewis LS, Smith JE (2015) Quantifying scales of spatial variability in algal turf assemblages on coral reefs. Mar Ecol Prog Ser 532:41–57. doi:10.3354/meps11344

    Article  Google Scholar 

  • Hay ME, Taylor PR (1985) Competition between herbivourous fishes and urchins on Caribbean reefs. Oecologia 65:591–598. doi:10.1007/BF00379678

    Article  Google Scholar 

  • Hay ME, Fenical W, Gustafson K (1987) Chemical defense against diverse coral-reef herbivores 68:1581–1591

    CAS  Google Scholar 

  • Hoey AS, Bellwood DR (2009) Limited functional redundancy in a high diversity system: single species dominates key ecological process on coral reefs. Ecosystems 12:1316–1328. doi:10.1007/s10021-009-9291-z

    Article  Google Scholar 

  • Hurlbert SH, Lombardi CM (2009) Final collapse of the Neyman-Pearson decision theoretic framework and rise of the neoFisherian. Ann Zool Fennici 46:311–349. doi:10.5735/086.046.0501

    Article  Google Scholar 

  • Hurlbert SH, Lombardi CM (2012) Lopsided reasoning on lopsided tests and multiple comparisons. Aust New Zeal J Stat 54:23–42. doi:10.1111/j.1467-842X.2012.00652.x

    Article  Google Scholar 

  • Hutchinson GE (1959) Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat 93:145. doi:10.1086/282070

    Article  Google Scholar 

  • Isbell F, Calcagno V, Hector A et al (2011) High plant diversity is needed to maintain ecosystem services. Nature 477:199–202. doi:10.1038/nature10282

    Article  CAS  PubMed  Google Scholar 

  • Jackson JBC, Donovan MK, Cramer KL, Lam W (2014) Status and trends of Caribbean coral reefs: 1970–2012, vol 306. Global Coral Reef Moniting Network, IUCN, Gland Switz

    Google Scholar 

  • Jouffray J-B, Nyström M, Norström AV et al (2015) Identifying multiple coral reef regimes and their drivers across the Hawaiian archipelago. Phil Trans R Soc B 370:20130268. doi:10.1098/rstb.2013.0268

    Article  PubMed Central  Google Scholar 

  • Kartzinel TR, Chen PA, Coverdale TC et al (2015) DNA metabarcoding illuminates dietary niche partitioning by African large herbivores. Proc Natl Acad Sci 112:8019–8024. doi:10.1073/pnas.1503283112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Loreau M (2004) Does functional redundancy exist? Oikos 104:606–611. doi:10.1111/j.0030-1299.2004.12685.x

    Article  Google Scholar 

  • Mantyka CS, Bellwood DR (2007) Macroalgal grazing selectivity among herbivorous coral reef fishes. Mar Ecol Prog Ser 352:177–185. doi:10.3354/meps07055

    Article  Google Scholar 

  • McCook LJ, Jompa J, Diaz-Pulido G (2001) Competition between corals and algae on coral reefs: a review of evidence and mechanisms. Coral Reefs 19:400–417. doi:10.1007/s003380000129

    Article  Google Scholar 

  • McNaughton SJ (1984) Grazing lawns: animals in herds, plant form, and coevolution. Am Nat 124:863–886

    Article  Google Scholar 

  • Mumby PJ (2014) Stratifying herbivore fisheries by habitat to avoid ecosystem overfishing of coral reefs. Fish Fish. doi:10.1111/faf.12078

    Google Scholar 

  • Odum HT, Odum EP (1955) Trophic structure and productivity of a windward coral reef community on Eniwetok Atoll. Ecol Monogr 25:291–320

    Article  Google Scholar 

  • Ogden JC, Lobel PS (1978) The role of herbivorous fishes and urchins in coral reef communities. Environ Biol Fishes 3:49–63. doi:10.1007/BF00006308

    Article  Google Scholar 

  • Ong L, Holland KN (2010) Bioerosion of coral reefs by two Hawaiian parrotfishes: species, size differences and fishery implications. Mar Biol 157:1313–1323. doi:10.1007/s00227-010-1411-y

    Article  Google Scholar 

  • Ostfeld RS, Manson RH, Canham CD (1997) Effects of rodents on survival of tree seeds and seedlings invading old fields. Ecology 78:1531–1542. doi:10.1890/0012-9658(1997)078[1531:EOROSO]2.0.CO;2

    Article  Google Scholar 

  • Padilla DK, Allen BJ (2000) Paradigm lost: reconsidering functional form and group hypotheses in marine ecology. J Exp Mar Bio Ecol 250:207–221. doi:10.1016/S0022-0981(00)00197-0

    Article  PubMed  Google Scholar 

  • Pandolfi JM, Jackson JBC, Baron N et al (2005) Ecology. Are U.S. coral reefs on the slippery slope to slime? Science 307:1725–1726. doi:10.1126/science.1104258

    Article  CAS  PubMed  Google Scholar 

  • Polovina JJ (1984) Model of a coral reef ecosystem—I. The ECOPATH model and its application to French Frigate Shoals. Coral Reefs 3:1–11. doi:10.1007/BF00306135

    Article  Google Scholar 

  • Pringle RM, Goheen JR, Palmer TM et al (2014) Low functional redundancy among mammalian browsers in regulating an encroaching shrub (Solanum campylacanthum) in African savannah. Proc Biol Sci 281:20140390. doi:10.1098/rspb.2014.0390

    Article  PubMed  PubMed Central  Google Scholar 

  • Rasher DB, Hoey AS, Hay ME (2013) Consumer diversity interacts with prey defenses to drive ecosystem function. Ecology 94:1347–1358. doi:10.1890/12-0389.1

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodgers KS, Jokiel PL, Brown EK et al (2015) Over a decade of change in spatial and temporal dynamics of hawaiian coral reef communities. Pac Sci 69:1–13. doi:10.2984/69.1.1

    Article  Google Scholar 

  • Root RB (1967) The niche exploitation pattern of the blue-gray gnatcatcher. Ecol Monogr 37:317–350

    Article  Google Scholar 

  • Rosenfeld JS (2002) Functional redundancy in ecology and conservation. Oikos 98:156–162. doi:10.1034/j.1600-0706.2002.980116.x

    Article  Google Scholar 

  • Rudolf VHW, Rasmussen NL, Dibble CJ, Van Allen BG (2014) Resolving the roles of body size and species identity in driving functional diversity. Proc Biol Sci 281:20133203. doi:10.1098/rspb.2013.3203

    Article  PubMed  PubMed Central  Google Scholar 

  • Scheffer M, Vergnon R, van Nes EH et al (2015) The evolution of functionally redundant species; evidence from beetles. PLoS One. doi:10.1371/journal.pone.0137974

    Google Scholar 

  • Simberloff D, Dayan T (1991) The guild concept and the structure of ecological communities. Annu Rev Ecol Syst 22:115–143

    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. doi:10.1007/s00442-009-1546-z

    Article  PubMed  Google Scholar 

  • Smith JE, Brainard R, Carter A et al (2016) Re-evaluating the health of coral reef communities: baselines and evidence for human impacts across the central Pacific. Proc R Soc B 283:20151985

    Article  PubMed  Google Scholar 

  • Steneck RS (1988) Herbivory on coral reefs: A synthesis. In: Proceedings of 6th International Coral Reef Symposium 37–49

  • Steneck RS, Dethier MN (1994) A functional group approach to the structure of algal-dominated communities 3:476–498

    Google Scholar 

  • Stuercke B, McDermid KJ (2004) Variation in algal turf species composition and abundance on two Hawaiian shallow subtidal reefs. Cryptogam Algol 25:353–365

    Google Scholar 

  • Thibault KM, Ernest SKM, Brown JH (2010) Redundant or complementary? Impact of a colonizing species on community structure and function. Oikos 119:1719–1726. doi:10.1111/j.1600-0706.2010.18378.x

    Article  Google Scholar 

  • Williams SL, Carpenter RC (1990) Photosynthesis/photon flux relationships among components of coral reef algal turfs. J Phycol 26:36–40. doi:10.1111/j.0022-3646.1990.00036.x

    Article  Google Scholar 

  • Williams ID, Walsh WJ, Schroeder RE et al (2008) Assessing the importance of fishing impacts on Hawaiian coral reef fish assemblages along regional-scale human population gradients. Environ Conserv 35:261. doi:10.1017/S0376892908004876

    Article  Google Scholar 

Download references

Acknowledgments

We thank S. Sandin for discussions of data analysis and implications. Thanks to M. Dailer and D. White for ideas and field support, P. Dockry for logistical support, and K. Moses and N. Pederson for processing gut content samples. We also thank S. Kram, J. Harris, L. Lewis, M. Miller, D. Brown, J. Locke, and E. Keenan. A. Khen provided drawings used in figures. Funding was provided by NSF IGERT, Hawaii Coral Reef Initiative, Mia Tegner Fellowship, Women Divers Hall of Fame, Explorers Club Exploration Fund, the Sussman Fellowship, and the Oceanids Memorial Fellowship. Funding for benthic coral reef surveys came from the NOAA Coral Reef Conservation Program. We thank D. Burkepile, S. Brandl, and an anonymous reviewer for their constructive comments in improving the manuscript.

Author contribution statement

ELAK and JES conceived and designed the experiments. ELAK, SC, RT, IDW, and JES executed the field work and resulting additional research ideas. ELAK, SC, and MG analyzed samples in the lab. YE, ELAK, SC, MG and JES analyzed the data. ELAK wrote the manuscript with significant contributions and edits from all authors.

Author information

Authors and Affiliations

  1. Center for Marine Biodiversity and Conservation, Scripps Institution of Oceanography, University of California San Diego, 9500 Gilman Drive, La Jolla, CA, 92093, USA

    Emily L. A. Kelly, Yoan Eynaud, Samantha M. Clements, Molly Gleason & Jennifer E. Smith

  2. Department of Land and Natural Resources, Division of Aquatic Resources, Maui Office, 130 Mahalani Street, Wailuku, HI, 96768, USA

    Russell T. Sparks

  3. Coral Reef Ecosystem Program (CREP), Pacific Islands Fisheries Science Center (PIFSC), National Marine Fisheries Service, NOAA IRC, 1845 Wasp Blvd. Building 176, Honolulu, HI, 96818, USA

    Ivor D. Williams

Authors
  1. Emily L. A. Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yoan Eynaud
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Samantha M. Clements
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Molly Gleason
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Russell T. Sparks
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ivor D. Williams
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jennifer E. Smith
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emily L. A. Kelly.

Ethics declarations

Statement of animal rights

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Joel Trexler.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 385 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kelly, E.L.A., Eynaud, Y., Clements, S.M. et al. Investigating functional redundancy versus complementarity in Hawaiian herbivorous coral reef fishes. Oecologia 182, 1151–1163 (2016). https://doi.org/10.1007/s00442-016-3724-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-016-3724-0

Keywords

Search

Navigation