Multiple Stressors and the Functioning of Coral Reefs

Annual Review of Marine Science

Volumn 9, Issue 1, 2017, Pages 445-468

  Harborne, Alastair R ^a,b   Rogers, Alice ^b   Bozec, Yves Marie ^b   Mumby, Peter J ^b  

^a FLORIDA INTERNATIONAL UNIVERSITY   (United States)

^b UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

Climate change; Ecological uncertainty; Ecosystem functioning; Ecosystem service; Fishing; Water quality

Indexed keywords

ECOSYSTEMS; FISHERIES; FISHING (OIL WELLS); REEFS; UNCERTAINTY ANALYSIS; WATER QUALITY;

COASTAL COMMUNITIES; CUMULATIVE EFFECTS; ECOLOGICAL UNCERTAINTY; ECOSYSTEM FUNCTIONING; ECOSYSTEM FUNCTIONS; ECOSYSTEM SERVICES; ECOSYSTEM STABILITY; PREDATOR-PREY INTERACTION;

CLIMATE CHANGE;

CLIMATE CHANGE; CORAL REEF; ECOLOGICAL STABILITY; ECOSYSTEM FUNCTION; ECOSYSTEM SERVICE; FISHING; FUNCTIONAL GROUP; PREDATOR-PREY INTERACTION; QUALITATIVE ANALYSIS; UNCERTAINTY ANALYSIS; WATER QUALITY;

ANTHOZOA;

ANIMAL; ANTHOZOA; CLIMATE CHANGE; CORAL REEF; ECOSYSTEM; FISH;

ANIMALS; ANTHOZOA; CLIMATE CHANGE; CORAL REEFS; ECOSYSTEM; FISHES;

EID: 85008870835     PISSN: 19411405     EISSN: 19410611     Source Type: Journal    
DOI: 10.1146/annurev-marine-010816-060551     Document Type: Review

References (150)

1. Aalto EA, Baskett ML. 2013. Quantifying the balance between bycatch and predator or competitor release for nontarget species. Ecol. Appl. 23:972-83
2. Ainsworth TD, Vega Thurber R, Gates RD. 2010. The future of coral reefs: a microbial perspective. Trends Ecol. Evol. 25:233-40
3. Albright R. 2011. Reviewing the effects of ocean acidification on sexual reproduction and early life history stages of reef-building corals. J. Mar. Biol. 2011:473615
4. Alvarez-Filip L, Dulvy NK, Gill JA, Coté IM, Watkinson AR. 2009. Flattening of Caribbean coral reefs: region-wide declines in architectural complexity. Proc. R. Soc. B 276:3019-25
5. Anthony KRN, Fabricius KE. 2000. Shifting roles of heterotrophy and autotrophy in coral energetics under varying turbidity. J. Exp. Mar. Biol. Ecol. 252:221-53
6. Anthony KRN, Kline DI, Diaz-Pulido G, Dove S, Hoegh-Guldberg O. 2008. Ocean acidification causes bleaching and productivity loss in coral reef builders. PNAS 105:17442-46
7. Ateweberhan M, Feary DA, Keshavmurthy S, Chen A, Schleyer MH, Sheppard CRC. 2013. Climate change impacts on coral reefs: synergies with local effects, possibilities for acclimation, and management implications. Mar. Pollut. Bull. 74:526-39
8. Ault JS, Bohnsack JA, Meester GA. 1998. A retrospective (1979-1996) multispecies assessment of coral reef fish stocks in the Florida Keys. Fish. Bull. 96:395-414
9. Baird AH, Marshall PA. 2002. Mortality, growth and reproduction in scleractinian corals following bleaching on the Great Barrier Reef. Mar. Ecol. Prog. Ser. 237:133-41
10. Ban SS, Graham NAJ, Connolly SR. 2014. Evidence for multiple stressor interactions and effects on coral reefs. Glob. Change Biol. 20:681-97
11. Bascompte J,Melián CJ, Sala E. 2005. Interaction strength combinations and the overfishing of a marine food web. PNAS 102:5443-47
12. Beardall J, Beer S, Raven JA. 1998. Biodiversity of marine plants in an era of climate change: some predictions based on physiological performance. Bot. Mar. 41:113-23
13. Behrenfeld MJ, O'Malley RT, Siegel DA, McClain CR, Sarmiento JL, et al. 2006. Climate-driven trends in contemporary ocean productivity. Nature 444:752-55
14. Bell PRF, Elmetri I,Uwins P. 1999. Nitrogen fixation by Trichodesmium spp. in theCentral andNorthernGreat Barrier Reef Lagoon: relative importance of the fixed-nitrogen load. Mar. Ecol. Prog. Ser. 186:119-26
15. Bellwood DR, Hoey AS, Hughes TP. 2012. Human activity selectively impacts the ecosystem roles of parrotfishes on coral reefs. Proc. R. Soc. B 279:1621-29
16. Bender D, Champ CM, Kline D, Diaz-Pulido G, Dove S. 2015. Effects of "reduced" and "business-as-usual" CO2 emission scenarios on the algal territories of the damselfish Pomacentrus wardi (Pomacentridae). PLOS ONE 10:e0131442
17. Birkeland C, Dayton PK. 2005. The importance in fishery management of leaving the big ones. Trends Ecol. Evol. 20:356-58
18. Birrell CL, McCook LJ, Willis BL. 2005. Effects of algal turfs and sediment on coral settlement. Mar. Pollut. Bull. 51:408-14
19. Boyce DG, LewisMR,WormB. 2010. Global phytoplankton decline over the past century. Nature 466:591-96
20. Boyer KE, Fong P, Armitage AR, Cohen RA. 2004. Elevated nutrient content of tropical macroalgae increases rates of herbivory in coral, seagrass, and mangrove habitats. Coral Reefs 23:530-38
21. Bozec YM, Yakob L, Bejarano S, Mumby PJ. 2013. Reciprocal facilitation and non-linearity maintain habitat engineering on coral reefs. Oikos 122:428-40
22. Buck BH, Rosenthal H, Saint-Paul U. 2002. Effect of increased irradiance and thermal stress on the symbiosis of Symbiodinium microadriaticum and Tridacna gigas. Aquat. Living Resour. 15:107-17
23. Burkepile DE, Hay ME. 2006. Herbivore versus nutrient control of marine primary producers: contextdependent effects. Ecology 87:3128-39
24. Burkepile DE, HayME. 2009. Nutrient versus herbivore control of macroalgal community development and coral growth on a Caribbean reef. Mar. Ecol. Prog. Ser. 389:71-84
25. Cacciapaglia C, van Woesik R. 2016. Climate-change refugia: shading reef corals by turbidity. Glob. Change Biol. 22:1145-54
26. Campbell JE, Fisch J, Langdon C, Paul VJ. 2016. Increased temperature mitigates the effects of ocean acidification in calcified green algae (Halimeda spp). Coral Reefs 35:357-68
27. Cardini U, Bednarz VN, Foster RA,Wild C. 2014. Benthic N2 fixation in coral reefs and the potential effects of human-induced environmental change. Ecol. Evol. 4:1706-27
28. Carpenter RC. 1990. Mass mortality of Diadema antillarum. I. Long-term effects on sea urchin populationdynamics and coral reef algal communities. Mar. Biol. 104:67-77
29. Carreiro-SilvaM,McClanahan TR. 2001. Echinoid bioerosion and herbivory on Kenyan coral reefs: the role of protection from fishing. J. Exp. Mar. Biol. Ecol. 262:133-53
30. Catano LB, RojasMC, Malossi RJ, Peters JR, Heithaus MR, et al. 2016. Reefscapes of fear: predation risk and reef heterogeneity interact to shape herbivore foraging behaviour. J. Anim. Ecol. 85:146-56
31. Ceccarelli DM, Hughes TP, McCook LJ. 2006. Impacts of simulated overfishing on the territoriality of coral reef damselfish. Mar. Ecol. Prog. Ser. 309:255-62
32. Chan NCS, Connolly SR. 2013. Sensitivity of coral calcification to ocean acidification: a meta-analysis. Glob. Change Biol. 19:282-90
33. Chazottes V, Campion-Alsumard T, Peyrot-Clausade M, Cuet P. 2002. The effects of eutrophicationrelated alterations to coral reef communities on agents and rates of bioerosion (Reunion Island, Indian Ocean). Coral Reefs 21:375-90
34. Cheung WWL, Sarmiento JL, Dunne J, Fr olicher TL, Lam VWY, et al. 2013. Shrinking of fishes exacerbates impacts of global ocean changes on marine ecosystems. Nat. Clim. Change 3:254-58
35. Chong-Seng KM, Nash KL, Bellwood DR, Graham NAJ. 2014. Macroalgal herbivory on recovering versus degrading coral reefs. Coral Reefs 33:409-19
36. Coker DJ, Pratchett MS, Munday PL. 2009. Coral bleaching and habitat degradation increase susceptibility to predation for coral-dwelling fishes. Behav. Ecol. 20:1204-10
37. Coker DJ, Wilson SK, Pratchett MS. 2014. Importance of live coral habitat for reef fishes. Rev. Fish Biol. Fish. 24:89-126
38. Comeau S, Lantz CA, Edmunds PJ, Carpenter RC. 2016. Framework of barrier reefs threatened by ocean acidification. Glob. Change Biol. 22:1225-34
39. Connell JH. 1978. Diversity in tropical rain forests and coral reefs. Science 199:1302-10
40. D'Angelo C, Wiedenmann J. 2014. Impacts of nutrient enrichment on coral reefs: new perspectives and implications for coastal management and reef survival. Curr. Opin. Environ. Sustain. 7:82-93
41. Dambacher JM, Luh HK, Li HW, Rossignol PA. 2003. Qualitative stability and ambiguity in model ecosystems. Am. Nat. 161:876-88
42. de Groot RS, Wilson MA, Boumans RMJ. 2002. A typology for the classification, description and valuation of ecosystem functions, goods and services. Ecol. Econ. 41:393-408
43. De'ath G, Lough JM, Fabricius KE. 2009. Declining coral calcification on the Great Barrier Reef. Science 323:116-19
44. DeCarlo TM, Cohen AL, BarkleyHC, CobbanQ, Young C, et al. 2015. Coralmacrobioerosion is accelerated by ocean acidification and nutrients. Geology 43:7-10
45. Delgado O, Lapointe BE. 1994. Nutrient-limited productivity of calcareous versus fleshy macroalgae in a eutrophic, carbonate-rich tropical marine environment. Coral Reefs 13:151-59
46. DeMartini EE, Friedlander AM, Sandin SA, Sala E. 2008. Differences in fish-assemblage structure between fished and unfished atolls in the northern Line Islands, central Pacific. Mar. Ecol. Prog. Ser. 365:199-215
47. Díaz S, Demissew S, Carabias J, Joly C, Lonsdale M, et al. 2015. The IPBES Conceptual Framework-connecting nature and people. Curr. Opin. Environ. Sustain. 14:1-16
48. Diaz-Pulido G, Gouezo M, Tilbrook B, Dove S, Anthony KRN. 2011. High CO2 enhances the competitive strength of seaweeds over corals. Ecol. Lett. 14:156-62
49. Diaz-Pulido G, McCook LJ. 2003. Relative roles of herbivory and nutrients in the recruitment of coral-reef seaweeds. Ecology 84:2026-33
50. Diaz-Pulido G, McCook LJ, Larkum AWD, Lotze HK, Raven JA, et al. 2007. Vulnerability of macroalgae of the Great Barrier Reef to climate change. In Climate Change and the Great Barrier Reef: A Vulnerability Assessment, ed. J Johnson, P Marshall, pp. 151-92. Townsville, Aust.: Great Barrier Reef Mar. Park Auth. and Aust. Greenh. Off
51. Dixson DL, Abrego D, HayME. 2014. Chemically mediated behavior of recruiting corals and fishes: a tipping point that may limit reef recovery. Science 345:892-97
52. Donelson JM. 2015. Development in a warm future ocean may enhance performance in some species. J. Exp. Mar. Biol. Ecol. 472:119-25
53. Donelson JM, Munday PL, McCormick MI, Pankhurst NW, Pankhurst PM. 2010. Effects of elevated water temperature and food availability on the reproductive performance of a coral reef fish. Mar. Ecol. Prog. Ser. 401:233-43
54. Eakin CM, Morgan JA, Heron SF, Smith TB, Liu G, et al. 2010. Caribbean corals in crisis: record thermal stress, bleaching, and mortality in 2005. PLOS ONE 5:e13969
55. Edwards CB, Friedlander AM, Green AG, Hardt MJ, Sala E, et al. 2014. Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects. Proc. R. Soc. B 281:20131835
56. Enochs IC. 2012. Motile cryptofauna associated with live and dead coral substrates: implications for coral mortality and framework erosion. Mar. Biol. 159:709-22
57. Fabricius KE. 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs: review and synthesis. Mar. Pollut. Bull. 50:125-46
58. Fabricius KE, De'ath G, Noonan S, Uthicke S. 2014. Ecological effects of ocean acidification and habitat complexity on reef-associated macroinvertebrate communities. Proc. R. Soc. B 281:20132479
59. Fabricius KE, Okaji K, De'ath G. 2010. Three lines of evidence to link outbreaks of the crown-of-thorns seastar Acanthaster planci to the release of larval food limitation. Coral Reefs 29:593-605
60. Feary DA, McCormick MI, Jones GP. 2009. Growth of reef fishes in response to live coral cover. J. Exp. Mar. Biol. Ecol. 373:45-49
61. Ferrari MCO, McCormick MI, Munday PL, Meekan MG, Dixson DL, et al. 2011. Putting prey and predator into the CO2 equation-qualitative and quantitative effects of ocean acidification on predator-prey interactions. Ecol. Lett. 14:1143-48
62. Ferrari R, Gonzalez-RiveroM,Mumby PJ. 2012. Size matters in competition between corals and macroalgae. Mar. Ecol. Prog. Ser. 467:77-88
63. Furnas M, Mitchell A, Skuza M, Brodie J. 2005. In the other 90%: phytoplankton responses to enhanced nutrient availability in the Great Barrier Reef Lagoon. Mar. Pollut. Bull. 51:253-65
64. GaoKS, HelblingEW,Häder DP,Hutchins DA. 2012. Responses ofmarine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar. Ecol. Prog. Ser. 470:167-89
65. Gardiner NM, Munday PL, Nilsson GE. 2010. Counter-gradient variation in respiratory performance of coral reef fishes at elevated temperatures. PLOS ONE 5:e13299
66. Gilmour JP, Smith LD, Heyward AJ, Baird AH, PratchettMS. 2013. Recovery of an isolated coral reef system following severe disturbance. Science 340:69-71
67. Goatley CHR, Bellwood DR. 2012. Sediment suppresses herbivory across a coral reef depth gradient. Biol. Lett. 8:1016-18
68. Goatley CHR, Bellwood DR. 2013. Ecological consequences of sediment on high-energy coral reefs. PLOS ONE 8:e77737
69. Graham NAJ, Nash KL. 2013. The importance of structural complexity in coral reef ecosystems. Coral Reefs 32:315-26
70. Grigg RW. 1994. Effects of sewage discharge, fishing pressure and habitat complexity on coral ecosystems and reef fishes in Hawaii. Mar. Ecol. Prog. Ser. 103:25-34
71. Hawkins JP, Roberts CM. 2003. Effects of fishing on sex-changing Caribbean parrotfishes. Biol. Conserv. 115:213-26
72. Head CEI, Bonsall MB, Koldewey H, Pratchett MS, Speight M, Rogers AD. 2015. High prevalence of obligate coral-dwelling decapods on dead corals in the Chagos Archipelago, central Indian Ocean. Coral Reefs 34:905-15
73. Hoey AS, Bellwood DR. 2011. Suppression of herbivory by macroalgal density: a critical feedback on coral reefs? Ecol. Lett. 14:267-73
74. Houk P, RhodesK,Cuetos-Bueno J, Lindfield S, Fread V, McIlwain JL. 2012. Commercial coral-reef fisheries across Micronesia: a need for improving management. Coral Reefs 31:13-26
75. Hughes TP, Baird AH, Bellwood DR, Card M, Connolly SR, et al. 2003. Climate change, human impacts, and the resilience of coral reefs. Science 301:929-33
76. Hunter CL, Evans CW. 1995. Coral reefs in Kaneohe Bay, Hawaii: two centuries of western influence and two decades of data. Bull. Mar. Sci. 57:501-15
77. Hutchings P, Peyrot-Clausade M, Osnorno A. 2005. Influence of land runoff on rates and agents of bioerosion of coral substrates. Mar. Pollut. Bull. 51:438-47
78. Jax K. 2005. Function and "functioning" in ecology: What does it mean? Oikos 111:641-48
79. Johansen JL, JonesGP. 2011. Increasing ocean temperature reduces themetabolic performance and swimming ability of coral reef damselfishes. Glob. Change Biol. 17:2971-79
80. Johansen JL, Messmer V, Coker DJ, Hoey AS, Pratchett MS. 2014. Increasing ocean temperatures reduce activity patterns of a large commercially important coral reef fish. Glob. Change Biol. 20:1067-74
81. Johansen JL, Pratchett MS, Messmer V, Coker DJ, Tobin AJ, Hoey AS. 2015. Large predatory coral trout species unlikely to meet increasing energetic demands in a warming ocean. Sci. Rep. 5:13830
82. Johnson MD, Carpenter RC. 2012. Ocean acidification and warming decrease calcification in the crustose coralline alga Hydrolithon onkodes and increase susceptibility to grazing. J. Exp. Mar. Biol. Ecol. 434:94-101
83. Jompa J,McCook LJ. 2002. The effects of nutrients and herbivory on competition between a hard coral (Porites cylindrica) and a brown alga (Lobophora variegata). Limnol. Oceanogr. 47:527-34
84. Jones GP, McCormick MI, Srinivasan M, Eagle JV. 2004. Coral decline threatens fish biodiversity in marine reserves. PNAS 101:8251-53
85. Knutson TR, McBride JL, Chan J, Emanuel K, Holland G, et al. 2010. Tropical cyclones and climate change. Nat. Geosci. 3:157-63
86. Koch M, Bowes G, Ross C, Zhang XH. 2013. Climate change and ocean acidification effects on seagrasses and marine macroalgae. Glob. Change Biol. 19:103-32
87. Koop K, Booth D, Broadbent A, Brodie J, Bucher D, et al. 2001. ENCORE: the effect of nutrient enrichment on coral reefs. Synthesis of results and conclusions. Mar. Pollut. Bull. 42:91-120
88. Kramer MJ,Bellwood DR,Bellwood O. 2014. Large-scale spatial variation in epilithic algal matrix cryptofaunal assemblages on the Great Barrier Reef. Mar. Biol. 161:2183-90
89. Kramer MJ, Bellwood O, Fulton CJ, Bellwood DR. 2015. Refining the invertivore: diversity and specialisation in fish predation on coral reef crustaceans. Mar. Biol. 162:1779-86
90. Kroeker KJ, Kordas RL, Crim R, Hendriks IE, Ramajo L, et al. 2013a. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19:1884-96
91. Kroeker KJ, Micheli F,Gambi MC. 2013b.Ocean acidification causes ecosystem shifts via altered competitive interactions. Nat. Clim. Change 3:156-59
92. Lamb JB,WilliamsonDH, Russ GR,Willis BL. 2015. Protected areas mitigate diseases of reef-building corals by reducing damage from fishing. Ecology 96:2555-67
93. Lessios HA. 2016. The great Diadema antillarum die-off: 30 years later. Annu. Rev. Mar. Sci. 8:267-83
94. Letourneur Y, Harmelin-VivienM, Galzin R. 1993. Impact of hurricane Firinga on fish community structure on fringing reefs of Reunion Island, S.W. Indian Ocean. Environ. Biol. Fishes 37:109-20
95. Lohrer AM, Hewitt JE, Thrush SF. 2006. Assessing far-field effects of terrigenous sediment loading in the coastal marine environment. Mar. Ecol. Prog. Ser. 315:13-18
96. López-Victoria M, Zea S. 2004. Storm-mediated coral colonization by an excavating Caribbean sponge. Clim. Res. 26:251-56
97. Lough JM, Cantin NE. 2014. Perspectives on massive coral growth rates in a changing ocean. Biol. Bull. 226:187-202
98. Lucas JS. 1994. The biology, exploitation, and mariculture of giant clams (Tridacnidae). Rev. Fish. Sci. 2:181-223
99. Madin EMP, Gaines SD, Warner RR. 2010. Field evidence for pervasive indirect effects of fishing on prey foraging behavior. Ecology 91:3563-71
100. Manzello DP, Kleypas JA, Budd DA, Eakin CM, Glynn PW, Langdon C. 2008. Poorly cemented coral reefs of the eastern tropical Pacific: possible insights into reef development in a high-CO2 world. PNAS 105:10450-55
101. McClanahan TR, Graham NAJ, Darling ES. 2014. Coral reefs in a crystal ball: predicting the future from the vulnerability of corals and reef fishes to multiple stressors. Curr. Opin. Environ. Sustain. 7:59-64
102. McCormick MI. 2012. Lethal effects of habitat degradation on fishes through changing competitive advantage. Proc. R. Soc. B 279:3899-904
103. McCormick MI,Watson S-A,Munday PL. 2013. Ocean acidification reverses competition for space as habitats degrade. Sci. Rep. 3:3280
104. McManus JW, Reyes RB, Nanola CL. 1997. Effects of some destructive fishing methods on coral cover and potential rates of recovery. Environ. Manag. 21:69-78
105. Moberg F, Folke C. 1999. Ecological goods and services of coral reef ecosystems. Ecol. Econ. 29:215-33
106. Mora C. 2008. A clear human footprint in the coral reefs of the Caribbean. Proc. R. Soc. B 275:767-73
107. MumbyPJ, BroadK,Brumbaugh DR,DahlgrenCP, Harborne AR, et al. 2008. Coral reef habitats as surrogates of species, ecological functions, and ecosystem services. Conserv. Biol. 22:941-51
108. Mumby PJ, Hastings A, Edwards HJ. 2007. Thresholds and the resilience of Caribbean coral reefs. Nature 450:98-101
109. Mumby PJ, Steneck RS, Edwards AJ, Ferrari R, Coleman R, et al. 2012. Fishing down a Caribbean food web relaxes trophic cascades. Mar. Ecol. Prog. Ser. 445:13-24
110. Mumby PJ, van Woesik R. 2014. Consequences of ecological, evolutionary and biogeochemical uncertainty for coral reef responses to climatic stress. Curr. Biol. 24:R413-23
111. Munday PL, Crawley NE, Nilsson GE. 2009a. Interacting effects of elevated temperature and ocean acidification on the aerobic performance of coral reef fishes. Mar. Ecol. Prog. Ser. 388:235-42
112. Munday PL, Dixson DL, Donelson JM, Jones GP, Pratchett MS, et al. 2009b. Ocean acidification impairs olfactory discrimination and homing ability of a marine fish. PNAS 106:1848-52
113. Munday PL, Dixson DL, McCormick MI, Meekan M, Ferrari MCO, Chivers DP. 2010. Replenishment of fish populations is threatened by ocean acidification. PNAS 107:12930-34
114. Munday PL, Leis JM, Lough JM, Paris CB, Kingsford MJ, et al. 2009c. Climate change and coral reef connectivity. Coral Reefs 28:379-95
115. Munday PL, McCormick MI, Nilsson GE. 2012. Impact of global warming and rising CO2 levels on coral reef fishes: what hope for the future? J. Exp. Biol. 215:3865-73
116. Nagelkerken I, Munday PL. 2016. Animal behaviour shapes the ecological effects of ocean acidification and warming: moving from individual to community-level responses. Glob. Change Biol. 22:974-89
117. Nilsson GE, Östlund-Nilsson S, Munday PL. 2010. Effects of elevated temperature on coral reef fishes: loss of hypoxia tolerance and inability to acclimate. Comp. Biochem. Physiol. A 156:389-93
118. Nugues MM, Roberts CM. 2003. Coral mortality and interaction with algae in relation to sedimentation. Coral Reefs 22:507-16
119. O'Connor JJ, Lecchini D, Beck HJ, Cadiou G, Lecellier G, et al. 2016. Sediment pollution impacts sensory ability and performance of settling coral-reef fish. Oecologia 180:11-21
120. O'Connor MI, Bruno JF, Gaines SD, Halpern BS, Lester SE, et al. 2007. Temperature control of larval dispersal and the implications for marine ecology, evolution, and conservation. PNAS 104:1266-71
121. Pacala SW, Kinzig AP. 2001. Introduction to theory and the common ecosystem model. In The Functional Consequences of Biodiversity: Empirical Progress and Theoretical Extensions, ed. D Tilman, AP Kinzig, SW Pacala, pp. 169-74. Princeton, NJ: Princeton Univ. Press
122. Paddack MJ, Reynolds JD, Aguilar C, Appeldoorn RS, Beets J, et al. 2009. Recent region-wide declines in Caribbean reef fish abundance. Curr. Biol. 19:590-95
123. Pandolfi JM. 2015. Incorporating uncertainty in predicting the future response of coral reefs to climate change. Annu. Rev. Ecol. Evol. Syst. 46:281-303
124. Perry CT, Smithers SG, Gulliver P, Browne NK. 2012. Evidence of very rapid reef accretion and reef growth under high turbidity and terrigenous sedimentation. Geology 40:719-22
125. Pistevos JCA, Nagelkerken I, Rossi T, Olmos M, Connell SD. 2015. Ocean acidification and global warming impair shark hunting behaviour and growth. Sci. Rep. 5:16293
126. Pratchett MS, Wilson SK, Berumen ML, McCormick MI. 2004. Sublethal effects of coral bleaching on an obligate coral feeding butterflyfish. Coral Reefs 23:352-56
127. Przeslawski R, Ahyong S, Byrne M, Worheide G, Hutchings P. 2008. Beyond corals and fish: the effects of climate change on noncoral benthic invertebrates of tropical reefs. Glob. Change Biol. 14:2773-95
128. Puccia CJ, Levins R. 1985. Qualitative Modeling of Complex Systems. Cambridge, MA: Harvard Univ. Press
129. Rhyne A, Rotjan R, Bruckner A, Tlusty M. 2009. Crawling to collapse: ecologically unsound ornamental invertebrate fisheries. PLOS ONE 4:e8413
130. Rogers A, Blanchard JL, Mumby PJ. 2014. Vulnerability of coral reef fisheries to a loss of structural complexity. Curr. Biol. 24:1000-5
131. Rogers A, Harborne AR, Brown CJ, Bozec YM, Castro C, et al. 2015. Anticipative management for coral reef ecosystem services in the 21st century. Glob. Change Biol. 21:504-14
132. Rogers CS. 1990. Responses of coral reefs and reef organisms to sedimentation. Mar. Ecol. Prog. Ser. 62:185-202
133. Ruttenberg BI, Hamilton SL,Walsh SM, Donovan MK, Friedlander A, et al. 2011. Predator-induced demographic shifts in coral reef fish assemblages. PLOS ONE 6:e21062
134. Sotka EE, Hay ME. 2009. Effects of herbivores, nutrient enrichment, and their interactions on macroalgal proliferation and coral growth. Coral Reefs 28:555-68
135. Sotka EE, Thacker RW. 2005. Do some corals like it hot? Trends Ecol. Evol. 20:59-62
136. Srivastava DS, Vellend M. 2005. Biodiversity-ecosystem function research: Is it relevant to conservation? Annu. Rev. Ecol. Evol. Syst. 36:267-94
137. Stallings CD. 2008. Indirect effects of an exploited predator on recruitment of coral-reef fishes. Ecology 89:2090-95
138. Steneck RS. 1997. Crustose corallines, other algal functional groups, herbivores and sediments: complex interactions along reef productivity gradients. In Proceedings of the 8th International Coral Reef Symposium, Vol. 1, ed. HA Lessios, IG Macintyre, pp. 695-700. Balboa, Panama: Smithson. Trop. Res. Inst
139. Tissot BN, Hallacher LE. 2003. Effects of aquarium collectors on coral reef fishes in Kona, Hawaii. Conserv. Biol. 17:1759-68
140. UmarMJ, McCook LJ, Price IR. 1998. Effects of sediment deposition on the seaweed Sargassum on a fringing coral reef. Coral Reefs 17:169-77
141. Vega Thurber RL, Burkepile DE, Fuchs C, Shantz AA, McMinds R, Zaneveld JR. 2014. Chronic nutrient enrichment increases prevalence and severity of coral disease and bleaching. Glob. Change Biol. 20:544-54
142. Ward-Paige CA, Risk MJ, Sherwood OA, Jaap WC. 2005. Clionid sponge surveys on the Florida Reef Tract suggest land-based nutrient inputs. Mar. Pollut. Bull. 51:570-79
143. Watson S-A, Lefevre S, McCormick MI, Domenici P, Nilsson GE, Munday PL. 2014. Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels. Proc. R. Soc. B 281:20132377
144. Wenger AS, Johansen JL, Jones GP. 2012. Increasing suspended sediment reduces foraging, growth and condition of a planktivorous damselfish. J. Exp. Mar. Biol. Ecol. 428:43-48
145. Wenger AS, McCormick MI, Endo GGK, McLeod IM, Kroon FJ, Jones GP. 2014. Suspended sediment prolongs larval development in a coral reef fish. J. Exp. Biol. 217:1122-28
146. Wenger AS, McCormick MI, McLeod IM, Jones GP. 2013. Suspended sediment alters predator-prey interactions between two coral reef fishes. Coral Reefs 32:369-74
147. Wild C, Hoegh-Guldberg O, Naumann MS, Colombo-Pallotta MF, Ateweberhan M, et al. 2011. Climate change impedes scleractinian corals as primary reef ecosystem engineers. Mar. Freshw. Res. 62:205-15
148. Williams DM, Hatcher AI. 1983. Structure of fish communities on outer slopes of inshore, mid-shelf and outer shelf reefs of the Great Barrier Reef. Mar. Ecol. Prog. Ser. 10:239-50
149. Wilson SK, Babcock RC, Fisher R, Holmes TH, Moore JAY, Thomson DP. 2012. Relative and combined effects of habitat and fishing on reef fish communities across a limited fishing gradient at Ningaloo. Mar. Environ. Res. 81:1-11
150. Wisshak M, Schonberg CHL, Form A, Freiwald A. 2012. Ocean acidification accelerates reef bioerosion. PLOS ONE 7:e45124