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.
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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
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
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
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
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
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
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
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
Cooper WE (2000) Tradeoffs between predation risk and feeding in a lizard, the broad-headed skink (Eumeces laticeps). Behaviour 137:1175–1189
Dahlgren CP, Eggleston DB (2000) Ecological processes underlying ontogenetic habitat shifts in a coral reef fish. Ecology 81:2227–2240
Dill LM (1978) An energy-based model of optimal feeding-territory size. Theor Popul Biol 14:396–429
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
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
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
Eynaud Y, McNamara DE, Sandin SA (2016) Herbivore space use influences coral reef recovery. Royal Soc Open Sci. doi:10.1098/rsos.160262
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
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
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
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
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
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
Hay ME (1981) Spatial patterns of agrazing intensity on a caribbean barrier reef: herbivory and algal distribution. Aquat Bot 11:97–109
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
Helfman G (1989) Threat-sensitive predator avoidance in damselfish-trumpetfish interactions. Behav Ecol Sociobiol 24:47–58
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
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
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
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
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
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
Laegdsgaard P, Johnson C (2001) Why do juvenile fish utilise mangrove habitats? J Exp Mar Biol Ecol 257:229–253
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
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
Lendrem DW (1983) Predation risk and vigilance in the blue tit (Parus caeruleus). Behav Ecol Sociobiol 14:9–13
Lewis SM (1986) The role of herbivorous fishes in the organization of a Caribbean reef community. Ecol Monogr 56:183–200
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
Lima SL, Bednekoff PA (1999) Temporal variation in danger drives antipredator behavior: the predation risk allocation hypothesis. Am Nat 153:649–659
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
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
Madin EM, Gaines SD, Warner RR (2010b) Field evidence for pervasive indirect effects of fishing on prey foraging behavior. Ecology 91:3563–3571
Madin EM, Madin JS, Booth DJ (2011) Landscape of fear visible from space. Sci Rep 1:14. doi:10.1038/srep00014
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
Milinski M, Heller R (1978) Influence of a predator on the optimal foraging behaviour of sticklebacks (Gasterosteus aculeatus L.). Nature 275:642–644
Morse DH (1976) Variables affecting the density and territory size of breeding spruce-woods warblers. Ecology 57(2):290–301. doi:10.2307/1934817
Mumby PJ (2006) The impact of exploiting grazers (Scaridae) on the dynamics of Caribbean coral reefs. Ecol Appl 16:747–769
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
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
Mumby PJ et al (2006) Fishing, trophic cascades, and the process of grazing on coral reefs. Science 311:98–101
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
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
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
Parsons AJ, Dumont B (2003) Spatial heterogeneity and grazing processes. Anim Res 52:161–179. doi:10.1051/animres:2003013
Pöysä H (1987) Feeding-vigilance trade-off in the teal (Anas crecca): effects of feeding method and predation risk. Behaviour 103:108–122
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
Robertson DR (1996) Interspecific competition controls abundance and habitat use of territorial Caribbean damselfishes. Ecology 77(3):885–899. doi:10.2307/2265509
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
Sandin SA, McNamara DE (2012) Spatial dynamics of benthic competition on coral reefs. Oecologia 168:1079–1090. doi:10.1007/s00442-011-2156-0
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
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
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
Sommer U (2000) Benthic microalgal diversity enhanced by spatial heterogeneity of grazing. Oecologia 122:284–287
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
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
Taylor RJ (1988) Territory size and location in animals with refuges: influence of predation risk. Evol Ecol 2:95–101
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
Tricas TC (1989) Determinants of feeding territory size in the corallivorous butterflyfish, Chaetodon multicinctus. Anim Behav 37:830–841
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
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
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
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
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
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.
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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.
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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
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DOI: https://doi.org/10.1007/s00442-017-3857-9