Skip to main content

Advertisement

Log in

Evidence for benthic primary production support of an apex predator–dominated coral reef food web

  • Original Paper
  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Five hundred and ninety-nine primary producers and consumers in the Papahānaumokuākea Marine National Monument (PMNM) (22°N–30°N, 160°W–180°W) were sampled for carbon and nitrogen stable isotope composition to elucidate trophic relationships in a relatively unimpacted, apex predator–dominated coral reef ecosystem. A one-isotope (δ13C), two-source (phytoplankton and benthic primary production) mixing model provided evidence for an average minimum benthic primary production contribution of 65 % to consumer production. Primary producer δ15N values ranged from −1.6 to 8.0 ‰ with an average (2.1 ‰) consistent with a prevalence of N2 fixation. Consumer group δ15N means ranged from 6.6 ‰ (herbivore) to 12.1 ‰ (Galeocerdo cuvier), and differences between consumer group δ15N values suggest an average trophic enrichment factor of 1.8 ‰ Δ15N. Based on relative δ15N values, the larger G. cuvier may feed at a trophic position above other apex predators. The results provide baseline data for investigating the trophic ecology of healthy coral reef ecosystems.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

BMA:

Benthic macroalgae

BMI:

Benthic microalgae

C:

Carbon

FL:

Fork length

FFS:

French Frigate Shoals

HCl:

Hydrochloric acid

IRMS:

Isotope ratio mass spectrometer

Lu:

Ludox

PMNM:

Papahānaumokuākea Marine National Monument

N:

Nitrogen

SD:

Standard deviation

SI:

Stable isotope

TEF:

Trophic enrichment factor

TL:

Total length

TP:

Trophic position

VM:

Vertical migration

References

  • Allen GR, Steene R, Allen M (1998) A guide to angelfishes and butterflyfishes. Odyssey Publishing/Tropical Reef Research, Perth

    Google Scholar 

  • Atkinson MJ, Grigg RW (1984) Model of a coral-reef ecosystem. 2. Gross and net benthic primary production at French Frigate Shoals, Hawaii. Coral Reefs 3:13–22. doi:10.1007/bf00306136

    Article  CAS  Google Scholar 

  • Bearhop S, Adams CE, Waldron S, Fuller RA, Macleod H (2004) Determining trophic niche width: a novel approach using stable isotope analysis. J Anim Ecol 73:1007–1012. doi: 10.1111/j.0021-8790.2004.00861.x

    Article  Google Scholar 

  • Bond AL, Diamond AW (2011) Recent Bayesian stable-isotope mixing models are highly sensitive to variation in discrimination factors. Ecol Appl 21:1017–1023. doi:10.1890/09-2409.1

    Article  Google Scholar 

  • Bozec YM, Gascuel D, Kulbicki M (2004) Trophic model of lagoonal communities in a large open atoll (Ouvea, Loyalty islands, New Caledonia). Aquat Living Resour 17:151–162. doi:10.1051/alr:2004024

    Article  Google Scholar 

  • Carassou L, Kulbicki M, Nicola TJR, Polunin NVC (2008) Assessment of fish trophic status and relationships by stable isotope data in the coral reef lagoon of New Caledonia, southwest Pacific. Aquat Living Resour 21:1–12. doi:10.1051/alr:2008017

    Article  Google Scholar 

  • Carpenter EJ, Harvey HR, Fry B, Capone DG (1997) Biogeochemical tracers of the marine cyanobacterium Trichodesmium. Deep-Sea Res, Part I 44:27–38. doi:10.1016/s0967-0637(96)00091-x

    Article  CAS  Google Scholar 

  • Caut S, Angulo E, Courchamp F (2009) Variation in discrimination factors δ15N and δ13C: the effect of diet isotopic values and applications for diet reconstruction. J Appl Ecol 46:443–453. doi:10.1111/j.1365-2664.2009.01620.x

    Article  CAS  Google Scholar 

  • Cruz-Rivera E, Paul VJ (2006) Feeding by coral reef mesograzers: algae or cyanobacteria? Coral Reefs 25:617–627. doi:10.1007/s00338-006-0134-5

    Article  Google Scholar 

  • Currin CA, Levin LA, Talley TS, Michener R, Talley D (2011) The role of cyanobacteria in Southern California salt marsh food webs. Mar Ecol 32:346–363. doi:10.1111/j.1439-0485.2011.00476.x

    Article  Google Scholar 

  • Dale JJ, Meyer CG, Clark CE (2011) The ecology of coral reef top predators in the Papahānaumokuākea Marine National Monument. J Mar Biol 2011:1–14. doi:10.1155/2011/725602

    Google Scholar 

  • DeFelice RD, Parrish JD (2003) Importance of benthic prey for fishes in coral reef-associated sediments. Pac Sci 57:359–384

    Article  Google Scholar 

  • DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochim Cosmochim 45:341–351

    Article  CAS  Google Scholar 

  • Dore JE, Brum JR, Tupas LM, Karl DM (2002) Seasonal and interannual variability in sources of nitrogen supporting export in the oligotrophic subtropical North Pacific Ocean. Limnol Oceanogr 47:1595–1607

    Article  CAS  Google Scholar 

  • Fogel ML, Cifuentes LA (1993) Isotope fractionation during primary production. In: Engel MH, Macko SA (eds) Organic Geochemistry: Principles and applications. Plenum Publ, Corp, New York, pp 73–98

    Chapter  Google Scholar 

  • France RL (1995) Carbon-13 enrichment in benthic compared to planktonic algae: food web implications. Mar Ecol Prog Ser 124:307–312

    Article  Google Scholar 

  • France R, Holmquist J, Chandler M, Cattaneo A (1998) δ15N evidence for nitrogen fixation associated with macroalgae from a seagrass-mangrove coral reef system. Mar Ecol Prog Ser 167:297–299. doi:10.3354/meps167297

    Article  CAS  Google Scholar 

  • Friedlander AM, DeMartini EE (2002) Contrasts in density, size, and biomass of reef fishes between the northwestern and the main Hawaiian islands: the effects of fishing down apex predators. Mar Ecol Prog Ser 230:253–264

    Article  Google Scholar 

  • Friedlander A, Aeby G, Balwani S, Bowan B, Brainard R, Clark A, Kenyon J, Maragos J, Meyer C, Vroom PS, Zamzow J (2008) The state of coral reef ecosystems of the Northwestern Hawaiian islands. In: Wadell JE, Clarke AM (eds) The state of coral reef ecosystems of the United States and Pacific freely associated states NOAA Technical Memorandum NOS NCCOS 73. NOAA/NCCOS Center for Coastal Monitoring and Assessment’s Biogeography Team, Silver Spring, MD, pp 270–311

    Google Scholar 

  • Friedlander A, Kobayashi D, Bowen B, Meyers C, Papastamatiou Y, DeMartini E, Parrish F, Treml E, Currin C, Hilting A, Weiss J, Kelley C, O’Conner R, Parke M, Clark RG, Toonen RJ, Wedding L (2009) Connectivity and integrated ecosystem studies. NCCOS’s Biogegraphy Branch in cooperation with the Office of National Marine Sanctuaries Papahānaumokuākea Marine National Monument, Silver Spring, MD

    Google Scholar 

  • Froese R, Pauly D (2012) FishBase World Wide Web electronic publication. www.fishbase.org, version (02/2012)

  • Galván DE, Sweeting CJ, Polunin NVC (2012) Methodological uncertainty in resource mixing models for generalist fishes. Oecologia 169:1083–1093. doi:10.1007/s00442-012-2273-4

    Article  Google Scholar 

  • Greenwood NDW, Sweeting CJ, Polunin NVC (2010) Elucidating the trophodynamics of four coral reef fishes of the Solomon Islands using δ15N and δ13C. Coral Reefs 29:785–792. doi:10.1007/s00338-010-0626-1

    Article  Google Scholar 

  • Grigg RW, Polovina JJ, Friedlander AM, Rohmann SO (2008) Biology of Coral Reefs in the Northwestern Hawaiian Islands. In: Riegel BM, Dodge RE (eds) Coral Reefs of the USA. Springer, New York, pp 573–594

    Chapter  Google Scholar 

  • Hannides CCS, Popp BN, Landry MR, Graham BS (2009) Quantification of zooplankton trophic position in the North Pacific Subtropical Gyre using stable nitrogen isotopes. Limnol Oceanogr 54:50–61. doi:10.4319/lo.2009.54.1.0050

    Article  CAS  Google Scholar 

  • Harriott VJ, Banks SA (2002) Latitudinal variation in coral communities in eastern Australia: a qualitative biophysical model of factors regulating coral reefs. Coral Reefs 21:83–94. doi:10.1007/s00338-001-0201-x

    Google Scholar 

  • Heikoop JM, Dunn JJ, Risk MJ, Tomascik T, Schwarcz HP, Sandeman IM, Sammarco PW (2000) δ15N and δ13C of coral tissue show significant inter-reef variation. Coral Reefs 19:189–193

    Article  Google Scholar 

  • Hiatt RW, Strasburg DW (1960) Ecological relationships of the fish fauna on coral reefs of the Marshall Islands. Ecol Monogr 30:65–127. doi:10.2307/1942181

    Article  Google Scholar 

  • Hixon MA (2011) 60 years of coral reef fish ecology: past, present, future. Bull Mar Sci 87:727–765. doi:10.5343/bms.2010.1055

    Article  Google Scholar 

  • Hobson ES (1974) Feeding relationships of teleostean fishes on coral reefs in Kona Hawaii. Fish Bull 72:915–1031

    Google Scholar 

  • Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K, Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid climate change and ocean acidification. Science 318:1737–1742. doi:10.1126/science.1152509

    Article  CAS  Google Scholar 

  • Hoenisch B, Ridgwell A, Schmidt DN, Thomas E, Gibbs SJ, Sluijs A, Zeebe R, Kump L, Martindale RC, Greene SE, Kiessling W, Ries J, Zachos JC, Royer DL, Barker S, Marchitto TM Jr, Moyer R, Pelejero C, Ziveri P, Foster GL, Williams B (2012) The geological record of ocean acidification. Science 335:1058–1063. doi:10.1126/science.1208277

    Article  CAS  Google Scholar 

  • Hoey AS, Pratchett MS, Cvitanovic C (2011) High macroalgal cover and low coral recruitment undermines the potential resilience of the world’s southernmost coral reef assemblages. PLoS One 6(10):e25824. doi:10.1371/journal.pone.0025824

    Article  CAS  Google Scholar 

  • Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, Folke C, Grosberg R, Hoegh-Guldberg O, Jackson JBC, Kleypas J, Lough JM, Marshall P, Nystrom M, Palumbi SR, Pandolfi JM, Rosen B, Roughgarden J (2003) Climate change, human impacts, and the resilience of coral reefs. Science 301:929–933. doi:10.1126/science.1085046

    Article  CAS  Google Scholar 

  • Hughes TP, Graham NAJ, Jackson JBC, Mumby PJ, Steneck RS (2010) Rising to the challenge of sustaining coral reef resilience. Trends Ecol Evol 25:633–642. doi:10.1016/j.tree.2010.07.011

    Article  Google Scholar 

  • Kiehl J (2011) Lessons from Earth’s past. Science 331:158–159. doi:10.1126/science.1199380

    Article  CAS  Google Scholar 

  • Knowlton N, Jackson JBC (2008) Shifting baselines, local impacts, and global change on coral reefs. PLoS Biol 6:e54. doi:10.1371/journal.pbio.0060054

    Article  Google Scholar 

  • Kolasinski J, Rogers K, Cuet P, Barry B, Frouin P (2011) Sources of particulate organic matter at the ecosystem scale: a stable isotope and trace element study in a tropical coral reef. Mar Ecol Prog Ser 443:77–93. doi:10.3354/meps09416

    Article  CAS  Google Scholar 

  • Logan JM, Lutcavage ME (2010) Stable isotope dynamics in elasmobranch fishes. Hydrobiologia 644:231–244. doi:10.1007/s10750-010-0120-3

    Article  CAS  Google Scholar 

  • Lowe CG, Wetherbee BM, Crow GL, Tester AL (1996) Ontogenetic dietary shifts and feeding behavior of the tiger shark, Galeocerdo cuvier, in Hawaiian waters. Environ Biol Fishes 47:203–211. doi:10.1007/bf00005044

    Article  Google Scholar 

  • MacArthur LD, Phillips DL, Hyndes GA, Hanson CE, Vanderklift MA (2011) Habitat surrounding patch reefs influences the diet and nutrition of the western rock lobster. Mar Ecol Prog Ser 436:191–205. doi:10.3354/meps09256

    Article  Google Scholar 

  • Madigan D, Litvin S, Popp B, Carlisle AB, Farwell C, Block B (2012) Tissue turnover rates and isotopic trophic discrimination factors in the endothermic teleost, Pacific Bluefin Tuna (Thunnus orientalis). PLoS One 7:e49220. doi:10.1371/journal.pone.0049220

    Article  CAS  Google Scholar 

  • Marine Mammal Commission (2001) Annual Report to Congress 2000, Bethesda, Maryland, pp 1–253

  • Matich P, Heithaus MR, Layman CA (2011) Contrasting patterns of individual specialization and trophic coupling in two marine apex predators. J Anim Ecol 80:294–305. doi:10.1111/j.1365-2656.2010.01753.x

    Article  Google Scholar 

  • McClelland JW, Holl CM, Montoya JP (2003) Relating low δ15N values of zooplankton to N2-fixation in the tropical North Atlantic: insights provided by stable isotope ratios of amino acids. Deep-Sea Res, Part I 50:849–861. doi:10.1016/s0967-0637(03)00073-6

    Article  CAS  Google Scholar 

  • McCutchan JH, Lewis WM, Kendall C, McGrath CC (2003) Variation in trophic shift for stable isotope ratios of carbon, nitrogen and sulfur. Oikos 102:378–390

    Article  CAS  Google Scholar 

  • Moseman SM, Levin LA, Currin C, Forder C (2004) Colonization, succession, and nutrition of macrobenthic assemblages in a restored wetland at Tijuana Estuary, California. Estuar Coast Shelf Sci 60:755–770

    Article  Google Scholar 

  • Olson RJ, Popp BN, Graham BS, Lopez-Ibarra GA, Galvan-Magana F, Lennert-Cody CE, Bocanegra-Castillo N, Wallsgrove NJ, Gier E, Alatorre-Ramirez V, Ballance LT, Fry B (2010) Food-web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean. Prog Oceanogr 86:124–138. doi:10.1016/j.pocean.2010.04.026

    Article  Google Scholar 

  • O’Malley JM, Drazen JC, Popp BN, Gier E, Toonen RJ (2012) Spatial variability in the growth and prey availability of lobsters in the northwestern Hawaiian Islands. Mar Ecol Prog Ser 449:211–220. doi:10.3354/meps09533

    Article  Google Scholar 

  • O’Reilly CM, Hecky RE, Cohen AS, Plisnier PD (2002) Interpreting stable isotopes in food webs: recognizing the role of time averaging at different trophic levels. Limnol Oceanogr 47:306–309

    Article  Google Scholar 

  • Owens NJP (1987) Natural variations in 15N in the marine environment. Adv Mar Biol 24:389–451

    Article  Google Scholar 

  • Papastamatiou YP, Wetherbee BM, Lowe CG, Crow GL (2006) Distribution and diet of four species of carcharhinid shark in the Hawaiian Islands: evidence for resource partitioning and competitive exclusion. Mar Ecol Prog Ser 320:239–251. doi:10.3354/meps320239

    Article  Google Scholar 

  • Parrish FA, Boland RC (2004) Habitat and reef-fish assemblages of banks in the Northwestern Hawaiian Islands. Mar Biol 144:1065–1073. doi:10.1007/s00227-003-1288-0

    Article  Google Scholar 

  • Phillips DL, Newsome SD, Gregg JW (2005) Combining sources in stable isotope mixing models: alternative methods. Oecologia 144:520–527. doi:10.1007/s00442-004-1816-8

    Article  Google Scholar 

  • Piché J, Iverson SJ, Parrish FA, Dollar R (2010) Characterization of forage fish and invertebrates in the Northwestern Hawaiian Islands using fatty acid signatures: species and ecological groups. Mar Ecol Prog Ser 418:1–15. doi:10.3354/meps08814

    Article  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

    Article  Google Scholar 

  • Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83:703–718

    Article  Google Scholar 

  • Post DM, Layman CA, Arrington DA, Takimoto G, Quattrochi J, Montana CG (2007) Getting to the fat of the matter: models, methods and assumptions for dealing with lipids in stable isotope analyses. Oecologia 152:179–189. doi:10.1007/s00442-006-0630-x

    Article  Google Scholar 

  • Sandin SA, Smith JE, DeMartini EE, Dinsdale EA, Donner SD, Friedlander AM, Konotchick T, Malay M, Maragos JE, Obura D, Pantos O, Paulay G, Richie M, Rohwer F, Schroeder RE, Walsh S, Jackson JB, Knowlton N, Sala E (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS One 3:e1548. doi:10.1371/journal.pone.0001548

    Article  Google Scholar 

  • Stevenson C, Katz LS, Micheli F, Block B, Heiman KW, Perle C, Weng K, Dunbar R, Witting J (2007) High apex predator biomass on remote Pacific islands. Coral Reefs 26:47–51

    Article  Google Scholar 

  • Sweeting CJ, Jennings S, Polunin NVC (2005) Variance in isotopic signatures as a descriptor of tissue turnover and degree of omnivory. Funct Ecol 19:777–784. doi:10.1111/j.1365-2435.2005.01019.x

    Article  Google Scholar 

  • Vander Zanden MJ, Rasmussen JB (2001) Variation in δ15N and δ13C trophic fractionation: implications for aquatic food web studies. Limnol Oceanogr 46:2061–2066

    Article  CAS  Google Scholar 

  • Vanderklift MA, Ponsard S (2003) Sources of variation in consumer-diet δ15N enrichment: a meta-analysis. Oecologia 136:169–182. doi:10.1007/s00442-003-1270-z

    Article  Google Scholar 

  • Vroom PS, Braun CL (2010) Benthic composition of a healthy subtropical reef: baseline species-level cover, with an emphasis on algae, in the Northwestern Hawaiian Islands. PLoS One 5:e9733. doi:10.1371/journal.pone.0009733

    Article  Google Scholar 

  • Vroom PS, Page KN, Peyton KA, Kukea-Shultz JK (2005) Spatial heterogeneity of benthic community assemblages with an emphasis on reef algae at French Frigate Shoals, Northwestern Hawaiian Islands. Coral Reefs 24:574–581. doi:10.1007/s00338-005-0028-y

    Article  Google Scholar 

  • Wainright SC, Weinstein MW, Able KW, Currin CA (2000) Relative importance of benthic microalgae, phytoplankton and the detritus of smooth cordgrass Spartina alterniflora and the common reed Phragmites australis to brackish-marsh food webs. Mar Ecol Prog Ser 200:77–91

    Article  CAS  Google Scholar 

  • Wetherbee BM, Crow GL, Lowe CG (1996) Biology of the Galapagos shark, Carcharhinus galapagensis, in Hawai’i. Environ Biol Fishes 45:299–310. doi:10.1007/bf00003099

    Article  Google Scholar 

  • Wetherbee BM, Crow GL, Lowe CG (1997) Distribution, reproduction and diet of the gray reef shark Carcharhinus amblyrhynchos in Hawaii. Mar Ecol Prog Ser 151:181–189. doi:10.3354/meps151181

    Article  Google Scholar 

  • Wyatt ASJ, Waite AM, Humphries S (2010) Variability in isotope discrimination factors in coral reef fishes: implications for diet and food web reconstruction. PLoS One 5:e13682. doi:10.1371/journal.pone.0013682

    Article  Google Scholar 

  • Yamamuro M, Kayanne H, Minagawa M (1995) Carbon and nitrogen stable isotopes of primary producers in coral-reef ecosystems. Limnol Oceanogr 40:617–621

    Article  CAS  Google Scholar 

Download references

Acknowledgments

We thank R. Dollar, F. Parrish, and B. Popp for valuable discussions, E. Davenport for his technical expertise, E. Kehn for assistance with identification of macroalgal specimens, and H. Walsh, C. Meyer, Y. Papastamatiou, B. Bowen, and F. Parrish for sample collection. We thank the anonymous reviewers whose comments helped us significantly improve this paper. Funding was provided by NOAA’s Office of National Marine Sanctuaries, the Papahānaumokuākea Marine National Monument, and the National Ocean Service. A report based on data presented in this manuscript was included in Friedlander et al. (2009).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Anna K. Hilting.

Additional information

Communicated by C. Harrod.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 205 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hilting, A.K., Currin, C.A. & Kosaki, R.K. Evidence for benthic primary production support of an apex predator–dominated coral reef food web. Mar Biol 160, 1681–1695 (2013). https://doi.org/10.1007/s00227-013-2220-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00227-013-2220-x

Keywords

Navigation