Skip to main content
Log in

Predation risk influences feeding rates but competition structures space use for a common Pacific parrotfish

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

Abstract

In terrestrial systems it is well known that the spatial patterns of grazing by herbivores can influence the structure of primary producer communities. On coral reefs, the consequences of varied space use by herbivores on benthic community structure are not well understood, nor are the relative influences of bottom-up (resource abundance and quality), horizontal (competition), and top-down (predation risk) factors in affecting spatial foraging behaviors of mobile herbivorous fishes. In the current study we quantified space use and feeding rates of the parrotfish, Chlorurus spilurus, across a strong gradient of food resources and predator and competitor abundance across two islands with drastically different fisheries management schemes. We found evidence that while feeding rates of this species are affected by direct interference competition and chronic predation risk, space use appears to be primarily related to exploitative competition with the surrounding herbivore community. We found no evidence that predation risk influences diurnal foraging space use in this small bodied parrotfish species. Additionally, we found the influence of chronic predation risk on feeding rates of this species to be less dramatic than the results of recent studies that used model predators to measure acute behavioral responses of other species of herbivorous fishes. Our results indicate that the non-consumptive effects of predators on the foraging behaviors of coral reef herbivores may be less dramatic than previously thought.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Adler P, Raff D, Lauenroth W (2001) The effect of grazing on the spatial heterogeneity of vegetation. Oecologia 128:465–479. doi:10.1007/s004420100737

    Article  Google Scholar 

  • Heenan A et al (2014) Ecological monitoring 2012–2013: reef fishes and benthic habitats of the main Hawaiian Islands, American Samoa, and Pacific Remote Island Areas. PIFSC Data Report DR-14-003

  • Ripley B et al (2015) Package ‘MASS’. Retrieved from CRAN: http://cran.r-project.org/web/packages/MASS/MASS.pdf

  • Benhamou S (2011) Dynamic approach to space and habitat use based on biased random bridges. PLoS One 6:e14592

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Box SJ, Mumby PJ (2007) Effect of macroalgal competition on growth and survival of juvenile Caribbean corals. Mar Ecol Prog Ser 342:139–149. doi:10.3354/meps342139

    Article  Google Scholar 

  • Brooks A (2015) MCR LTER: Coral Reef: Long-term Population and Community Dynamics: Fishes, ongoing since 2005. knb-lter-mcr.6.54 doi:10.6073/pasta/d688610e536f54885a3c59d287f6c4c3

  • 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 82:1192–1202. doi:10.1111/1365-2656.12097

    Article  PubMed  Google Scholar 

  • Calenge C (2006) The package “adehabitat” for the R software: a tool for the analysis of space and habitat use by animals. Ecol Model 197:516–519. doi:10.1016/j.ecolmodel.2006.03.017

    Article  Google Scholar 

  • Carlson PM, Davis K, Warner RR, Caselle JE (in revision) Bottom-up rescource dynamics drive dramatic differences in the fine scale feeding behavior of a large coral reef herbivore

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

    Article  Google Scholar 

  • Catano LB et al (2016) Reefscapes of fear: predation risk and reef hetero-geneity interact to shape herbivore foraging behaviour. J Anim Ecol 85:146–156. doi:10.1111/1365-2656.12440

    Article  PubMed  Google Scholar 

  • Clements KD, German DP, Piché J, Tribollet A, Choat JH (2016) Integrating ecological roles and trophic diversification on coral reefs: multiple lines of evidence identify parrotfishes as microphages. Biol J Linn, Soc

    Google Scholar 

  • Cooper WE (2000) Tradeoffs between predation risk and feeding in a lizard, the broad-headed skink (Eumeces laticeps). Behaviour 137:1175–1189

    Article  Google Scholar 

  • Dahlgren CP, Eggleston DB (2000) Ecological processes underlying ontogenetic habitat shifts in a coral reef fish. Ecology 81:2227–2240

    Article  Google Scholar 

  • Dill LM (1978) An energy-based model of optimal feeding-territory size. Theor Popul Biol 14:396–429

    Article  CAS  PubMed  Google Scholar 

  • Dubin RE, Baker JD (1982) 2 types of cover-seeking behavior at sunset by the princess parrotfish, scarus-taeniopterus, at Barbados West-Indies. Bull Mar Sci 32:572–583

    Google Scholar 

  • Edwards CB 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 

  • Evans MR (1996) Nectar and flower production of Lobelia telekii inflorescences, and their influence on territorial behaviour of the scarlet-tufted malachite sunbird (Nectarinia johnstoni). Biol J Linn Soc 57:89–105

    Google Scholar 

  • Eynaud Y, McNamara DE, Sandin SA (2016) Herbivore space use influences coral reef recovery. Royal Soc Open Sci. doi:10.1098/rsos.160262

    Google Scholar 

  • Ferrari MCO, Elvidge CK, Jackson CD, Chivers DP, Brown GE (2010) The responses of prey fish to temporal variation in predation risk: sensory habituation or risk assessment? Behav Ecol 21:532–536. doi:10.1093/beheco/arq023

    Article  Google Scholar 

  • Fortin D, Beyer HL, Boyce MS, Smith DW, Duchesne T, Mao JS (2005) Wolves influence elk movements: behavior shapes a trophic cascade in Yellowstone National Park. Ecology 86:1320–1330

    Article  Google Scholar 

  • Gallagher AJ, Creel S, Wilson RP, Cooke SJ (2016) Energy landscapes and the landscape of fear. Trends Ecol Evol 32(2):88–96. doi:10.1016/j.tree.2016.10.010

    Article  PubMed  Google Scholar 

  • Gil MA, Zill J, Ponciano JM (2016) Context-dependent landscape of fear: algal density elicits risky herbivory in a coral reef. Ecology 98(2):534–544. doi:10.1002/ecy.1668

    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. In: IUCN working group on climate change and coral reefs. IUCN, Gland, Switzerland, p 70

  • Grömping U (2006) Relative importance for linear regression in R: the package relaimpo. J Stat Softw 17:1–27

    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 

  • Hay ME (1981) Spatial patterns of agrazing intensity on a caribbean barrier reef: herbivory and algal distribution. Aquat Bot 11:97–109

    Article  Google Scholar 

  • Heithaus MR et al (2007) State-dependent risk-taking by green sea turtles mediates top-down effects of tiger shark intimidation in a marine ecosystem. J Anim Ecol 76:837–844. doi:10.1111/j.1365-2656.2007.01260.x

    Article  PubMed  Google Scholar 

  • Helfman G (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58

    Article  Google Scholar 

  • Hernández L, Laundré JW (2005) Foraging in the ‘landscape of fear’ and its implications for habitat use and diet quality of elk Cervus elaphus and bison Bison bison. Wildl. Biol. 11:215–220. doi:10.2981/0909-6396(2005)11[215:fitlof]2.0.co;2

  • Hirsch B (2002) Social monitoring and vigilance behavior in brown capuchin monkeys (Cebus apella). Behav Ecol Sociobiol 52:458–464. doi:10.1007/s00265-002-0536-5

    Article  Google Scholar 

  • Hixon MA (1980) Food production and competitor density as the determinants of feeding territory size. Am Nat 115(4):510–530. doi:10.1086/283577

    Article  Google Scholar 

  • Hixon MA, Brostoff WN (1996) Succession and herbivory: effects of differential fish grazing on Hawaiian coral-reef algae. Ecol Monogr 66(1):67–90. doi:10.2307/2963481

    Article  Google Scholar 

  • Hoey AS, Bellwood DR (2007) Cross-shelf variation in the role of parrotfishes on the great barrier reef. Coral Reefs 27:37–47. doi:10.1007/s00338-007-0287-x

    Article  Google Scholar 

  • Howard KG, Claisse JT, Clark TB, Boyle K, Parrish JD (2013) Home range and movement patterns of the Redlip Parrotfish (Scarus rubroviolaceus) in Hawaii. Mar Biol 160:1583–1595. doi:10.1007/s00227-013-2211-y

    Article  Google Scholar 

  • Jackson J, Donovan M, Cramer K, Lam V (2014) Status and trends of Caribbean coral reefs: 1970–2012. Global Coral Reef Monitoring Network

  • Kotler BP, Brown J, Mukherjee S, Berger-Tal O, Bouskila A (2010) Moonlight avoidance in gerbils reveals a sophisticated interplay among time allocation, vigilance and state-dependent foraging. Proc Biol Sci 277:1469–1474. doi:10.1098/rspb.2009.2036

    Article  PubMed  PubMed Central  Google Scholar 

  • Laegdsgaard P, Johnson C (2001) Why do juvenile fish utilise mangrove habitats? J Exp Mar Biol Ecol 257:229–253

    Article  CAS  PubMed  Google Scholar 

  • Laundré JW, Hernandez L, Ripple WJ (2010) The landscape of fear: ecological implications of being afraid. Open Ecol J 3:1–7. doi:10.2174/1874213001003030001

    Article  Google Scholar 

  • Leenhardt P, Moussa RM, Galzin R (2012) Reef and lagoon fisheries yields in Moorea: a summary of data collected. Secr Pac Community Fish Newsl 137:27–35

    Google Scholar 

  • Lendrem DW (1983) Predation risk and vigilance in the blue tit (Parus caeruleus). Behav Ecol Sociobiol 14:9–13

    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 

  • Licht T (1989) Discriminating between Hungry and Satiated Predators: the Response of Guppies (Poecilia reticulata) from High and Low Predation Sites. Ethology 82:238–243

    Article  Google Scholar 

  • Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659

    Article  Google Scholar 

  • Lirman D (2001) Competition between macroalgae and corals: effects of herbivore exclusion and increased algal biomass on coral survivorship and growth. Coral Reefs 19:392–399. doi:10.1007/s003380000125

    Article  Google Scholar 

  • Madin EM, Gaines SD, Madin JS, Warner RR (2010a) Fishing indirectly structures macroalgal assemblages by altering herbivore behavior. Am Nat 176:785–801. doi:10.1086/657039

    Article  PubMed  Google Scholar 

  • Madin EM, Gaines SD, Warner RR (2010b) Field evidence for pervasive indirect effects of fishing on prey foraging behavior. Ecology 91:3563–3571

    Article  PubMed  Google Scholar 

  • Madin EM, Madin JS, Booth DJ (2011) Landscape of fear visible from space. Sci Rep 1:14. doi:10.1038/srep00014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Madin EM et al (2012) Do behavioral foraging responses of prey to predators function similarly in restored and pristine foodwebs? PLoS One 7:e32390. doi:10.1371/journal.pone.0032390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Milinski M, Heller R (1978) Influence of a predator on the optimal foraging behaviour of sticklebacks (Gasterosteus aculeatus L.). Nature 275:642–644

    Article  Google Scholar 

  • Morse DH (1976) Variables affecting the density and territory size of breeding spruce-woods warblers. Ecology 57(2):290–301. doi:10.2307/1934817

    Article  Google Scholar 

  • Mumby PJ (2006) The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecol Appl 16:747–769

    Article  PubMed  Google Scholar 

  • Mumby PJ (2009) Herbivory versus corallivory: are parrotfish good or bad for Caribbean coral reefs? Coral Reefs 28:683–690. doi:10.1007/s00338-009-0501-0

    Article  Google Scholar 

  • Mumby PJ, Wabnitz CC (2002) Spatial patterns of aggression, territory size, and harem size in five sympatric Caribbean parrotfish species. Environ Biol Fishes 63:265–279

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Nash KL, Graham NAJ, Januchowski-Hartley FA, Bellwood DR (2012) Influence of habitat condition and competition on foraging behaviour of parrotfishes. Mar Ecol Prog Ser 457:113–124. doi:10.3354/meps09742

    Article  Google Scholar 

  • Palmer S, Gordon I, Hester A, Pakeman R (2005) Introducing spatial grazing impacts into the prediction of moorland vegetation dynamics. Landscape Ecol 19:817–827

    Article  Google Scholar 

  • Papastamatiou YP, Friedlander AM, Caselle JE, Lowe CG (2010) Long-term movement patterns and trophic ecology of blacktip reef sharks (Carcharhinus melanopterus) at Palmyra Atoll. J Exp Mar Biol Ecol 386:94–102. doi:10.1016/j.jembe.2010.02.009

    Article  Google Scholar 

  • Parsons AJ, Dumont B (2003) Spatial heterogeneity and grazing processes. Anim Res 52:161–179. doi:10.1051/animres:2003013

    Article  Google Scholar 

  • Pöysä H (1987) Feeding-vigilance trade-off in the teal (Anas crecca): effects of feeding method and predation risk. Behaviour 103:108–122

    Article  Google Scholar 

  • Rizzari JR, Frisch AJ, Hoey AS, McCormick MI (2014) Not worth the risk: apex predators suppress herbivory on coral reefs. Oikos 123:829–836. doi:10.1111/oik.01318

    Article  Google Scholar 

  • Robertson DR (1996) Interspecific competition controls abundance and habitat use of territorial Caribbean damselfishes. Ecology 77(3):885–899. doi:10.2307/2265509

    Article  Google Scholar 

  • Robertson DR, Gaines SD (1986) Interference competition structures habitat use in a local assemblage of coral reef surgeonfishes. Ecology 67(5):1372–1383. doi:10.2307/1938693

    Article  Google Scholar 

  • Sandin SA, McNamara DE (2012) Spatial dynamics of benthic competition on coral reefs. Oecologia 168:1079–1090. doi:10.1007/s00442-011-2156-0

    Article  PubMed  Google Scholar 

  • Sandin SA et al (2008) Baselines and degradation of coral reefs in the Northern Line Islands. PLoS One 3:e1548. doi:10.1371/journal.pone.0001548

    Article  PubMed  PubMed Central  Google Scholar 

  • Seastedt T, MacLean S (1979) Territory size and composition in relation to resource abundance in Lapland Longspurs breeding in arctic Alaska. The Auk 131–142

  • Smith JE et al (2006) Indirect effects of algae on coral: algae-mediated, microbe-induced coral mortality. Ecol Lett 9:835–845. doi:10.1111/j.1461-0248.2006.00937.x

    Article  PubMed  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 

  • Sommer U (2000) Benthic microalgal diversity enhanced by spatial heterogeneity of grazing. Oecologia 122:284–287

    Article  CAS  PubMed  Google Scholar 

  • Stenger J (1958) Food habits and available food of ovenbirds in relation to territory size. The Auk 75(3):335–346. doi:10.2307/4081979

    Article  Google Scholar 

  • Stimson J (1973) The role of the territory in the ecology of the intertidal limpet Lottia gigantea (Gray). Ecology 54(5):1020–1030. doi:10.2307/1935568

    Article  Google Scholar 

  • Taylor RJ (1988) Territory size and location in animals with refuges: influence of predation risk. Evol Ecol 2:95–101

    Article  Google Scholar 

  • Thacker R, Ginsburg D, Paul V (2014) Effects of herbivore exclusion and nutrient enrichment on coral reef macroalgae and cyanobacteria. Coral Reefs 19:318–329. doi:10.1007/s003380000122

    Article  Google Scholar 

  • Tricas TC (1989) Determinants of feeding territory size in the corallivorous butterflyfish, Chaetodon multicinctus. Anim Behav 37:830–841

    Article  Google Scholar 

  • van Rooij JM, Kroon FJ, Videler JJ (1996) The social and mating system of the herbivorous reef fish Sparisoma viride: one-male versus multi-male groups. Environ Biol Fishes 47:353–378

    Article  Google Scholar 

  • Walker BLE, Robinson MA (2009) Economic development, marine protected areas and gendered access to fishing resources in a Polynesian lagoon. Gender, Place Culture 16:467–484. doi:10.1080/09663690903003983

    Article  Google Scholar 

  • Warner R (1991) The use of phenotypic plasticity in coral reef fishes as tests of theory in evolutionary ecology. The ecology of fishes on coral reefs. Academic Press, San Diego, pp 387–398

  • Weber GE, Jeltsch F, Van Rooyen N, Milton SJ (1998) Simulated long-term vegetation response to grazing heterogeneity in semi-arid rangelands. J Appl Ecol 35(5):687–699. doi:10.1046/j.1365-2664.1998.355341.x

    Article  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. doi:10.1007/s003380000121

    Article  Google Scholar 

  • Wirsing AJ, Heithaus MR, Frid A, Dill LM (2008) Seascapes of fear: evaluating sublethal predator effects experienced and generated by marine mammals. Mar Mamm Sci 24:1–15. doi:10.1111/j.1748-7692.2007.00167.x

    Article  Google Scholar 

Download references

Acknowledgements

This work was made possible by The Nature Conservancy, US Fish and Wildlife Service, the Palmyra Atoll Research Consortium, Richard B. Gump South Pacific Research Station, and the Mo’orea Coral Reef Long Term Ecological Research Program (National Science Foundation Grant OCE1637396). Funding was provided by the Gordon and Betty Moore Foundation as a part of the Reefs Tomorrow Initiative, The Marisla Foundation, and the American Academy of Underwater Sciences. We thank J. Schem and J. Eurich for field assistance; staff at Palmyra Station and Gump Station; C. Lowe, D. McCauley, and S. Hamilton for valuable discussion and comments on the manuscript; and the three reviewers and handling editor for advice and insight on improvements to the original manuscript. This is Contribution Number PARC-0134 from the Palmyra Atoll Research Consortium.

Author information

Authors and Affiliations

Authors

Contributions

KD, PMC, and JEC conceived of and designed the study. All authors performed fieldwork. KD performed analysis and wrote the manuscript. All authors provided editorial advice.

Corresponding author

Correspondence to Kathryn Davis.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Stuart Sandin.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 7895 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Davis, K., Carlson, P.M., Bradley, D. et al. Predation risk influences feeding rates but competition structures space use for a common Pacific parrotfish. Oecologia 184, 139–149 (2017). https://doi.org/10.1007/s00442-017-3857-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-017-3857-9

Keywords

Navigation