(seaweeds) to overgrow corals and dominate reefs
(Jackson et al., 2001). This is a hypothesis about local,
intrinsic processes responding to extrinsic disturbances
(if fishing is considered extrinsic). The scenario is incorrect in this strict form because (1) direct observations
showed macroalgal overgrowth of corals to have made
a minor contribution to reef degradation (Aronson and
Precht, 2006) and (2) contrary to popular opinion among
coral reef scientists, the majority of Caribbean reefs are
not dominated by macroalgae (Bruno et al., 2009). In
a modified version, extrinsic disturbances such as
cyclones, which kill corals and open space for algal
colonization, interacted with overfishing of herbivores
and the loss of Diadema to promote a macroalgaedominated state (Hughes, 1994). This version is also not
entirely correct, because sufficient levels of coral mortality can lead to macroalgal dominance even without reductions of herbivores (Ostrander et al., 2000; Williams et al.,
2001). In such instances, widespread coral mortality overwhelms the capacity of populations of herbivores
to respond sufficiently to forestall macroalgal dominance.
More realistic scenarios of reef degradation emphasize
the primary (but not exclusive) role of extrinsic factors,
especially infectious coral diseases, thermally induced
coral bleaching, and their interactors, in causing coral
mortality, with or without ensuing shifts to macroalgal
dominance (Hoegh-Guldberg, 1999; Aronson and Precht,
2001, 2006; Hughes et al., 2003). Even remote, quasipristine reefs in the Indo-Pacific have been affected by
temperature-induced bleaching (Alling et al., 2007;
Sandin et al., 2008), emphasizing the now-overriding
importance of large-scale, extrinsic influences related to
human activities, especially climate change. Intensifying
ocean acidification and rising eustatic sea levels are additional, extrinsic effects of climate change that likely will
have negative impacts on coral populations in the
not-too-distant future (Kleypas et al., 1999; WBGU
2006; Hoegh-Guldberg et al., 2007).
Nutrient loading, whether viewed as intrinsic or extrinsic, appears to be a relatively minor driver of coral and
algal dynamics in most cases (Hughes et al., 1999;
Aronson and Precht, 2000), but the relationship between
top-down consumption (predation and herbivory) and
bottom-up, nutrient-driven production is complex
(Burkepile and Hay, 2006; Littler et al., 2006). The new
consensus on (reduced) herbivory is that its contribution
to algal dominance was overstated; however, by controlling macroalgae, herbivorous fish and echinoids can facilitate the recruitment and recovery of coral populations
(Bythell et al., 2000; Hughes et al., 2003; Carpenter and
Edmunds, 2006; Idjadi et al., 2006; Birrell et al., 2008;
Mumby and Harborne, 2010).
Summary
Coral populations and their recovery from stresses and
disturbances will continue to be driven by combinations
of factors, but categorizing them as intrinsic or extrinsic
is not as useful as understanding the scales on which they
operate. The process or interaction of processes that exerts
the strongest influence will by logical necessity be the limiting factor to corals. Addressing regional and global problems such as greenhouse-gas emissions and species
introductions will leave local factors to limit coral
populations, and vice versa. Simultaneous action on
anthropogenic drivers at multiple scales is the only way
to mitigate and, hopefully, reverse the degradation of coral
reefs.
Bibliography
Alling, A., Doherty, O., Logan, H., Feldman, L., and Dustan, P.,
2007. Catastrophic coral mortality in the remote central Pacific
Ocean: Kiribati, Phoenix islands. Atoll Research Bulletin, 551,
1–19.
Aronson, R. B., and Precht, W. F., 2000. Herbivory and algal
dynamics on the coral reef at Discovery Bay, Jamaica.
Limnology and Oceanography, 45, 251–255.
Aronson, R. B., and Precht, W. F., 2001. White-band disease and the
changing face of Caribbean coral reefs. Hydrobiologia, 460,
25–38.
Aronson, R. B., and Precht, W. F., 2006. Conservation, precaution,
and Caribbean reefs. Coral Reefs, 25, 441–450.
Aronson, R. B., Precht, W. F., and Macintyre, I. G., 1998. Extrinsic
control of species replacement on a Holocene reef in Belize: the
role of coral disease. Coral Reefs, 17, 223–230.
Aronson, R. B., Precht, W. F., Murdoch, T. J. T., and Robbart, M. L.,
2005. Long-term persistence of coral assemblages on the flower
garden banks, northwestern Gulf of Mexico: implications for science and management. Gulf of Mexico Science, 23, 84–94.
Birrell, C. L., McCook, L. J., Willis, B. L., and Diaz-Pulido, G. A.,
2008. Effects of benthic algae on the replenishment of corals and
the implications for the resilience of coral reefs. Oceanography
and Marine Biology: An Annual Review, 46, 25–63.
Bruno, J. F., and Selig, E. R., 2007. Regional decline of coral cover
in the Indo-Pacific: timing, extent, and subregional comparisons.
PLoS ONE, 2, e711, doi:10.1371/journal.pone.0000711.
Bruno, J. F., Sweatman, H., Precht, W. F., Selig, E. R., and Schutte,
V. G. W., 2009. Assessing evidence of phase shifts from coral to
macroalgal dominance on coral reefs. Ecology, 90, 1478–1484.
Burkepile, D. E., and Hay, M. E., 2006. Herbivore vs. nutrient control of marine primary producers: context-dependent effects.
Ecology, 87, 3128–3139.
Bythell, J. C., Hillis-Starr, Z., and Rogers, C. S., 2000. Local
cariability but landscape stability in coral reef communities following repeated hurricane impacts. Marine Ecology Progress
Series, 204, 93–100.
Carpenter, R. C., and Edmunds, P. J., 2006. Local and regional scale
recovery of diadema promotes recruitment of scleractinian
corals. Ecology Letters, 9, 271–280.
Connell, J. H., 1978. Diversity in tropical rainforests and coral reefs.
Science, 199, 1302–1310.
Done, T. J., 1999. Coral community adaptability to environmental
change at the scales of regions, reefs, and reef zones. American
Zoologist, 39, 66–79.
Gardner, T. A., Côté, I. M., Gill, J. A., Grant, A., and Watkinson,
A. R., 2003. Long-term region-wide declines in Caribbean coral
reefs. Science, 301, 958–960.
Hoegh-Guldberg, O., 1999. Climate change, coral bleaching and the
future of the world’s coral reefs. Marine and Freshwater
Research, 50, 839–866.
Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S.,
Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F.,
INTRINSIC AND EXTRINSIC DRIVERS ON CORAL REEFS
611
(Jackson et al., 2001). This is a hypothesis about local,
intrinsic processes responding to extrinsic disturbances
(if fishing is considered extrinsic). The scenario is incorrect in this strict form because (1) direct observations
showed macroalgal overgrowth of corals to have made
a minor contribution to reef degradation (Aronson and
Precht, 2006) and (2) contrary to popular opinion among
coral reef scientists, the majority of Caribbean reefs are
not dominated by macroalgae (Bruno et al., 2009). In
a modified version, extrinsic disturbances such as
cyclones, which kill corals and open space for algal
colonization, interacted with overfishing of herbivores
and the loss of Diadema to promote a macroalgaedominated state (Hughes, 1994). This version is also not
entirely correct, because sufficient levels of coral mortality can lead to macroalgal dominance even without reductions of herbivores (Ostrander et al., 2000; Williams et al.,
2001). In such instances, widespread coral mortality overwhelms the capacity of populations of herbivores
to respond sufficiently to forestall macroalgal dominance.
More realistic scenarios of reef degradation emphasize
the primary (but not exclusive) role of extrinsic factors,
especially infectious coral diseases, thermally induced
coral bleaching, and their interactors, in causing coral
mortality, with or without ensuing shifts to macroalgal
dominance (Hoegh-Guldberg, 1999; Aronson and Precht,
2001, 2006; Hughes et al., 2003). Even remote, quasipristine reefs in the Indo-Pacific have been affected by
temperature-induced bleaching (Alling et al., 2007;
Sandin et al., 2008), emphasizing the now-overriding
importance of large-scale, extrinsic influences related to
human activities, especially climate change. Intensifying
ocean acidification and rising eustatic sea levels are additional, extrinsic effects of climate change that likely will
have negative impacts on coral populations in the
not-too-distant future (Kleypas et al., 1999; WBGU
2006; Hoegh-Guldberg et al., 2007).
Nutrient loading, whether viewed as intrinsic or extrinsic, appears to be a relatively minor driver of coral and
algal dynamics in most cases (Hughes et al., 1999;
Aronson and Precht, 2000), but the relationship between
top-down consumption (predation and herbivory) and
bottom-up, nutrient-driven production is complex
(Burkepile and Hay, 2006; Littler et al., 2006). The new
consensus on (reduced) herbivory is that its contribution
to algal dominance was overstated; however, by controlling macroalgae, herbivorous fish and echinoids can facilitate the recruitment and recovery of coral populations
(Bythell et al., 2000; Hughes et al., 2003; Carpenter and
Edmunds, 2006; Idjadi et al., 2006; Birrell et al., 2008;
Mumby and Harborne, 2010).
Summary
Coral populations and their recovery from stresses and
disturbances will continue to be driven by combinations
of factors, but categorizing them as intrinsic or extrinsic
is not as useful as understanding the scales on which they
operate. The process or interaction of processes that exerts
the strongest influence will by logical necessity be the limiting factor to corals. Addressing regional and global problems such as greenhouse-gas emissions and species
introductions will leave local factors to limit coral
populations, and vice versa. Simultaneous action on
anthropogenic drivers at multiple scales is the only way
to mitigate and, hopefully, reverse the degradation of coral
reefs.
Bibliography
Alling, A., Doherty, O., Logan, H., Feldman, L., and Dustan, P.,
2007. Catastrophic coral mortality in the remote central Pacific
Ocean: Kiribati, Phoenix islands. Atoll Research Bulletin, 551,
1–19.
Aronson, R. B., and Precht, W. F., 2000. Herbivory and algal
dynamics on the coral reef at Discovery Bay, Jamaica.
Limnology and Oceanography, 45, 251–255.
Aronson, R. B., and Precht, W. F., 2001. White-band disease and the
changing face of Caribbean coral reefs. Hydrobiologia, 460,
25–38.
Aronson, R. B., and Precht, W. F., 2006. Conservation, precaution,
and Caribbean reefs. Coral Reefs, 25, 441–450.
Aronson, R. B., Precht, W. F., and Macintyre, I. G., 1998. Extrinsic
control of species replacement on a Holocene reef in Belize: the
role of coral disease. Coral Reefs, 17, 223–230.
Aronson, R. B., Precht, W. F., Murdoch, T. J. T., and Robbart, M. L.,
2005. Long-term persistence of coral assemblages on the flower
garden banks, northwestern Gulf of Mexico: implications for science and management. Gulf of Mexico Science, 23, 84–94.
Birrell, C. L., McCook, L. J., Willis, B. L., and Diaz-Pulido, G. A.,
2008. Effects of benthic algae on the replenishment of corals and
the implications for the resilience of coral reefs. Oceanography
and Marine Biology: An Annual Review, 46, 25–63.
Bruno, J. F., and Selig, E. R., 2007. Regional decline of coral cover
in the Indo-Pacific: timing, extent, and subregional comparisons.
PLoS ONE, 2, e711, doi:10.1371/journal.pone.0000711.
Bruno, J. F., Sweatman, H., Precht, W. F., Selig, E. R., and Schutte,
V. G. W., 2009. Assessing evidence of phase shifts from coral to
macroalgal dominance on coral reefs. Ecology, 90, 1478–1484.
Burkepile, D. E., and Hay, M. E., 2006. Herbivore vs. nutrient control of marine primary producers: context-dependent effects.
Ecology, 87, 3128–3139.
Bythell, J. C., Hillis-Starr, Z., and Rogers, C. S., 2000. Local
cariability but landscape stability in coral reef communities following repeated hurricane impacts. Marine Ecology Progress
Series, 204, 93–100.
Carpenter, R. C., and Edmunds, P. J., 2006. Local and regional scale
recovery of diadema promotes recruitment of scleractinian
corals. Ecology Letters, 9, 271–280.
Connell, J. H., 1978. Diversity in tropical rainforests and coral reefs.
Science, 199, 1302–1310.
Done, T. J., 1999. Coral community adaptability to environmental
change at the scales of regions, reefs, and reef zones. American
Zoologist, 39, 66–79.
Gardner, T. A., Côté, I. M., Gill, J. A., Grant, A., and Watkinson,
A. R., 2003. Long-term region-wide declines in Caribbean coral
reefs. Science, 301, 958–960.
Hoegh-Guldberg, O., 1999. Climate change, coral bleaching and the
future of the world’s coral reefs. Marine and Freshwater
Research, 50, 839–866.
Hoegh-Guldberg, O., Mumby, P. J., Hooten, A. J., Steneck, R. S.,
Greenfield, P., Gomez, E., Harvell, C. D., Sale, P. F.,
INTRINSIC AND EXTRINSIC DRIVERS ON CORAL REEFS
611