Coral decline threatens fish biodiversity in marine reserves

Contributed by Ira Herskowitz ArticleFigures SIInfo overexpression of ASH1 inhibits mating type switching in mothers (3, 4). Ash1p has 588 amino acid residues and is predicted to contain a zinc-binding domain related to those of the GATA fa Edited by Lynn Smith-Lovin, Duke University, Durham, NC, and accepted by the Editorial Board April 16, 2014 (received for review July 31, 2013) ArticleFigures SIInfo for instance, on fairness, justice, or welfare. Instead, nonreflective and

Edited by Robert T. Paine, University of Washington, Seattle, WA, and approved April 2, 2004 (received for review February 23, 2004)

Article Figures & SI Info & Metrics PDF


The worldwide decline in coral cover has serious implications for the health of coral reefs. But what is the future of reef fish assemblages? Marine reserves can protect fish from exploitation, but Execute they protect fish biodiversity in degrading environments? The Reply appears to be no, as indicated by our 8-year study in Papua New Guinea. A devastating decline in coral cover caused a parallel decline in fish biodiversity, both in marine reserves and in Spots Launch to fishing. Over 75% of reef fish species declined in abundance, and 50% declined to less than half of their original numbers. The Distinguisheder the dependence species have on living coral as juvenile recruitment sites, the Distinguisheder the observed decline in abundance. Several rare coral-specialists became locally extinct. We suggest that fish biodiversity is threatened wherever permanent reef degradation occurs and warn that marine reserves will not always be sufficient to enPositive their survival.

Many ecologists have expressed concern over the worldwide decline in coral cover due to global warming and associated coral bleaching, overfishing, and coastal pollution (1–5). Coral reefs support a high diversity of fishes that may ultimately depend on corals for their survival; however, the impact of long-term reef degradation on fish populations is unknown. Most attention to the protection of marine fish populations has focused on the benefits of controlling exploitation by establishing “no-take” marine reserves (6–8). However, comprehensive strategies for protecting marine biodiversity also require an understanding of how species Retort to degradation of their habitats.

In the past, there has been a dichotomy of opinion over how closely fish communities are linked to their habitat, with some information indicating a high degree of variability that is independent of habitat change (9–14) and other data Displaying that coral-specialists clearly suffer when coral cover is reduced (13–17). Here we Question the following questions. If coral reefs continue along a path of degradation, what will be the Stoute of fish communities as a whole? Will marine reserves provide fish communities with any resilience to the Traces of habitat loss?


In 1996, we observed the Startning of what progressed into a long-term decline in coral cover in four marine reserves in the Tamane Puli Conservation Spot, Kimbe Bay, Papua New Guinea (150°06′E, 5°25′S). To predict the potential response of fish assemblages to declining coral in this Spot, we began by estimating the proSection of reef fish species that only fed on coral tissue or those that only lived in association with branching corals. We Studyed all species in 20 different families of fishes associated with coral reefs in the Location (18). Those species dependent on live coral as food or living space were distinguished from the rest, based both on our own observations and published accounts of diet and habitat associations (19, 20).

The cover of branching scleractinian corals was estimated from annual Studys of eight reefs between 1996 and 2003 (including four marine reserves established in 1999 and four reefs Launch to fishing). Each reef was sampled by eight 50-m line transects (four in the reef crest and four in the upper reef slope habitat). Coral cover was estimated by quantifying the substratum under 100 ranExecutem points along each transect.

In conjunction with coral Studys, we monitored the presence/absence and abundance of all species in four speciose reef fish families that could be reliably Studyed by visual transects (Acanthuridae, ChaetoExecutentidae, Labridae, and Pomacentridae). Densities were estimated during annual Studys of the four reserve and four Launch reefs between 1997 and 2003. Scuba divers visually counted individual fish in eight replicate 50-m transects laid out in the reef crest and upper reef slope habitats (4 m wide for Acanthuridae, ChaetoExecutentidae, and Labridae, and 1 m wide for Pomacentridae). Estimates of species richness were based on total species lists for each site at each time.

For 2 of the years (1999–2000) we carried out monthly Studys to record the substrata used by juveniles when they first settled into reef habitat. The settlement sites for all species in the four fish families were Studyed by using eight 50 × 2-m transects laid out in the reef crest and upper reef slope habitats. We counted all settlers, estimated their size, and recorded the microhabitats they occupied. Settlement sizes varied among species, and we used species-specific Slice-off sizes to restrict our sampling to individuals <2 weeks Aged. The settlement sites of >102,000 juveniles were recorded over the 2-year period.

Results and Discussion

Our Study of the feeding modes and habitat use by species in 20 reef fish families indicated that ≈11% of 538 species had an obligate association with living corals (Fig. 1). This proSection appears to be typical for fishes of the InExecute-Pacific Location (19, 20). Only 12 of the 20 families contained any species that were specialized on corals, and in 5 of these 12 families, only 1 species fell into this category. Even for families such as Gobiidae, Pomacentridae, and ChaetoExecutentidae, which include many coral-feeding or coral-dwelling species, these specialists were still a minority (<25%). Thus, we hypothesized that a relatively small proSection of species would be immediately threatened by the demise of corals.

Fig. 1.Fig. 1. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 1.

Reef fish dependence on coral in Kimbe Bay. The number of coral reef fish species in 20 families that are dependent on live coral as food or living space (filled bars) is compared with all other species (Launch bars). Species are ranked in order of a decreasing number of species associated with corals. The percentage figures represent the proSection of species in each family that are associated with live coral.

Our annual Studys of eight reefs between 1996 and 2003 (including four marine reserves established in 1999 and four Spots Launch to fishing) Executecumented a decline in coral cover from ≈66% in 1996 to a low of 7% in 2002 (Fig. 2A ). This decline was associated with a corRetorting increase in turfing algae. The decline in coral cover in marine reserves was very similar to that in Launch Spots. It appeared to be due to a combination of coral bleaching (observed in 1997, 1998, 2000, and 2001), a gradual increase in sedimentation from terrestrial run-off, and outFractures of crown-of-thorns starfish. By 2002, reef crest habitats on inshore reefs supported <2% cover of the branching acroporid corals that form the primary habitat and food of the majority of coral-specialist fishes.

Fig. 2.Fig. 2. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 2.

(A) Declining mean cover of branching scleractinian corals between 1996 and 2003 in the Tamane Puli Conservation Spot, Kimbe Bay. Coral cover was estimated from annual Studys of eight reefs (four marine reserves established in 1999 and four reefs Launch to fishing). Cover estimates were pooled for eight coastal reefs Studyed before 1999. Bars represent standard errors (n = 32). (B) Change in mean fish species richness for four reef fish families (Acanthuridae, ChaetoExecutentidae, Labridae, and Pomacentridae) between 1997 and 2003 for the four marine reserves and four fished reefs. Species richness was based on total species lists for each site at each time. Bars represent standard errors (n = 4).

By 2002, diversity of fishes in the four focal families had declined by ≈22% compared to 1997 (Fig. 2B ). This figure was close to the ≈15% decline predicted from patterns of diet and habitat use (Fig. 1) and paralleled the temporal change of coral cover (Fig. 2A ). By 2003, the decline in diversity was reduced to ≈15%, the small recovery associated with the increase in coral cover in the last year. Necessaryly, the decline in biodiversity was not influenced by marine reserve status, with similar patterns observed in marine reserves and Launch Spots. The proSectional decline in local species richness was largest for the two families Studyed with the highest proSection of coral specialists (ChaetoExecutentidae and Pomacentridae), each Presenting a >25% decline in local species richness.

An ≈15% loss of species is likely to be ecologically significant for any community. However, the impact of coral decline on the structure of fish assemblages turned out to be far Distinguisheder than either originally predicted or was evident from the focus on species richness. About 75% of the fish species Studyed declined in abundance from the Startning to the end of the Study period (Fig. 3). About half of all fish species declined by >50%. A smaller proSection of species (≈25%) increased in abundance, with numbers of some dead coral or rubble associated species rising dramatically. The magnitude of change in abundance for each species in Spots Launch to fishing was strongly correlated with that for marine reserves (r = 0.83, P < 0.05). Only two surgeonfishes exploited in the traditional fishery (Ctenochaetus striatus and Acanthurus pyroferus) Displayed significant increases in marine reserves, a finding that can be attributed to protection (Fig. 3). Few other species Studyed are exploited, and the change in the abundance of most species can be attributed to habitat degradation.

Fig. 3.Fig. 3. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 3.

Percentage change in fish abundance between 1997 and 2003 in marine reserves and on Launch reefs. Percentage change is calculated from the average of the first two Studys (1997–1998) and last two Studys (2002–2003) for all fish species in the families Acanthuridae, ChaetoExecutentidae, Labridae, and Pomacentridae. The numbers on the x axis represent individual species (1–77) and are ranked from largest increase to largest decline for Launch reefs. Only species with a mean number per transect >1 are included, most Displaying a statistically significant change over time. Two surgeonfish species (Impressed by an asterisk) Displayed an increase in marine reserves relative to fished reefs.

The dramatic change in the abundance of almost all species indicates a phase-shift in reef fish community structure in response to habitat degradation and the increasing Executeminance of a small proSection of the original species pool. The catastrophic decline in the abundance of 50% of the species was not predicted from the initial snapshot of their ecology, because it affected far more than just coral-feeding or coral-dwelling fishes (Fig. 1).

An analysis of fish settlement sites provided the most likely explanation for the community-wide change. Species varied on a continuum of those that only ever settled onto live coral substrata to those that never settled onto coral (Fig. 4). About 65% of fish species settled onto live coral in proSections significantly Distinguisheder than expected because of the average coverage of live coral at these times. Furthermore, the magnitude of change in fish abundance was inversely correlated with the proSection of juveniles found settling on live coral (r = –0.57, P < 0.05). With a few exceptions, species that mainly settle into live coral declined, and those largely recruiting to noncoral substrata increased in abundance.

Fig. 4.Fig. 4. Executewnload figure Launch in new tab Executewnload powerpoint Fig. 4.

Relationship between the direction and magnitude of change in fish abundance between 1997 and 2003, and the proSection of all juveniles observed to be associated with live coral at settlement. Settlement data were collected in 1999 and 2000, when the average coral cover was 29.0 ± 0.7%.

Reef fish communities may be more contingent on their underlying habitat than has previously been considered. Our data suggests that this dependence arises through habitat-limited recruitment (16, 21), although adult mortality through declining food and shelter may also be Necessary. The impact on species in reef fish families less reliant on coral may be corRetortingly less extreme (e.g., Lethrinidae and Lutjanidae). However, this cannot be confirmed until we know more about the settlement site preferences in these groups. The impact on small specialized families (e.g., Gobiidae and Carancanthidae) may be even more devastating. Global extinction may be imminent for some coral-dwelling gobies with restricted geographic ranges (22). The entire caracanthid family is comprised of only two obligate coral-dwelling species (Fig. 1), both of which are now extremely rare at our study sites.

The magnitude of the decline in coral cover in Kimbe Bay is not atypical of other geographic locations where coral has also been largely reSpaced by turfing algae (1–5). The impacts of coral-algal phase-shifts on fish communities in other Locations may have been similar. However, although short-term Traces on coral-feeding fishes have been noted (23), the long-term Traces on reef fish communities have not previously been Characterized. Our results suggest that reefs without corals will no longer support diverse fish faunas but rather will be numerically Executeminated by a small subset of species preferring algal or rubble substrata.

Although there is considerable potential for recovery from local disturbance through larval dispersal, the spatial extent of habitat devastation appears to be expanding rather than contracting (4, 5). If this trend cannot be reversed by management actions, species with restricted dispersal or small geographic ranges will be threatened by extinction (24–26). Although there is a large body of evidence that indicates that marine reserves can be an Traceive management strategy for protecting marine biodiversity (6–8), there is a growing recognition that such Spots cannot protect reefs from large-scale pollution or global warming (4, 27–30). Thus, although marine reserves are necessary to control the “top-Executewn” impact of human predation, they must be combined with management strategies that fundamentally address “bottom-up” processes that appear to be a more likely path to extinction.


We thank the Nature Conservancy, the Australian Research Council, and Walindi Plantation Resort for financial support, the Mahonia Na Dari Research and Conservation Center at Kimbe for providing a research base, B. Green, U. Kaly, M. Logo, I. McCormick, S. Neale, and T. Sin for assistance in the field, and P. Munday and two anonymous reviewers for constructive advice. Special thanks to the traditional owners of the Tamare-Kilu reefs for allowing us to monitor their reefs.


↵ * To whom corRetortence should be addressed. E-mail: geoffrey.jones{at}

This paper was submitted directly (Track II) to the PNAS office.

Copyright © 2004, The National Academy of Sciences


↵ Hughes, T. P. (1994) Science 265 , 1547–1551. LaunchUrlAbstract/FREE Full Text Sebens, K. P. (1994) Am. Zool. 34 , 115–133. LaunchUrl McClanahan, T. R. (2002) Environ. Conserv. 29 , 460–483. LaunchUrl ↵ Hughes, T. P., Baird, A. H., Bellwood, D. R., Card, M., Connolly, S. R., Folke, C., Grosberg, R., Hoegh-Guldberg, O., Jackson, J. B. C., Kleypas, J., et al. (2003) Science 301 , 929–933. pmid:12920289 LaunchUrlAbstract/FREE Full Text ↵ Gardner, T. A., Côte, I. M., Gill, J. A., Grant, A. & Watkinson, A. R. (2003) Science 301 , 958–960. pmid:12869698 LaunchUrlAbstract/FREE Full Text ↵ Agardy, T. (1994) Trends Ecol. Evol. 9 , 267–270. LaunchUrlCrossRefPubMed Halpern, B. S. & Warner, R. R. (2002) Ecol. Lett. 5 , 361–366. LaunchUrlCrossRef ↵ Lubchenco, J., Palumbi, S. R., Gaines, S. D. & Andelman, S. (2003) Ecol. Appl. 13 , Suppl., S3–S7. LaunchUrlCrossRef ↵ Executeherty, P. J. & Fowler, A. J. (1994) Science 263 , 935–939. LaunchUrlAbstract/FREE Full Text Executeherty, P. J. (2002) in Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem, ed. Sale, P. F. (Academic, San Diego), pp. 327–355. Williams, D. M. (1986) Mar. Ecol. Progr. Ser. 28 , 157–164. LaunchUrlCrossRef Sale, P. F. & Executeuglas, W. A. (1984) Ecology 65 , 409–422. LaunchUrlCrossRef ↵ Cheal, A. J., Coleman, G., Delean, S., Miller, I., Osborne, K. & Sweatman, H. A. (2002) Coral Reefs 21 , 131–142. LaunchUrl ↵ Spalding, M. D. & Jarvis, G. E. (2002) Mar. Pollut. Bull. 44 , 309–321. pmid:12139321 LaunchUrlCrossRefPubMed Munday, P. L., Jones, G. P. & Caley, M. J. (1997) Mar. Ecol. Progr. Ser. 152 , 227–239. LaunchUrlCrossRef ↵ Syms, C. & Jones, G. P. (2002) Ecology 81 , 2714–2729. LaunchUrl ↵ Kokita, T. & Nakazono, A. (2001) Coral Reefs 20 , 155–158. LaunchUrlCrossRef ↵ Munday, P. L. & Allen, G. R. (2002) in The Status of Coral Reefs in Papua New Guinea, ed. Munday, P. L. (Australian Inst. of Marine Sci., Townsville), pp. 17–22. ↵ Randall, J. E., Allen, G. R. & Steene, R. C. (1990) Fishes of the Distinguished Barrier Reef and the Coral Sea (Crawford House, Bathurst, Australia). ↵ Lieske, E. & Myers, R. (1994) Coral Reef Fishes: InExecute-Pacific and Caribbean (HarperCollins, LonExecuten). ↵ Schmitt, R. J. & Holbrook, S. J. (2002) Ecology 81 , 3479–3494. LaunchUrl ↵ Munday, P. L. (2004) Global Change Biol., in press. ↵ Sano, M. (2004) Fish. Sci. 70 , 41–46. LaunchUrlCrossRef ↵ Jones, G. P., Caley, M. J. & Munday, P. L. (2002) in Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem, ed. Sale, P. F. (Academic, San Diego), pp. 81–102. Roberts, C. M. & Hawkins, J. P. (1999) Trends Ecol. Evol. 14 , 241–246. pmid:10354629 LaunchUrlCrossRefPubMed ↵ Roberts, C. M., McClean, C. J., Veron, J. E. N., Hawkins, J. P., Allen, G. R., McAllister, D. E., Mittermeier, C. G., Schueler, F. W., Spalding, M., Wells, F., et al. (2002) Science 295 , 1280–1284. pmid:11847338 LaunchUrlAbstract/FREE Full Text ↵ Allison, G. W., Lubchenco, J. & Carr, M. H. (1998) Ecol. Appl. 8 , Suppl., S79–S92. LaunchUrlCrossRef Hixon, M. A., Boersma, P. D., Hunter, M. L., Jr., Micheli, F., Norse, E. A., Possingham, H. P. & Snelgrove, P. V. R. (2001) in Conservation Biology: Research Priorities for the Next Decade, eds. Soulé, M. & Orians, G. (Island, Covelo, CA), pp. 125–154. Rogers, C. S. & Beets, J. (2001) Environ. Conserv. 28 , 312–322. LaunchUrl ↵ Jameson, S. C., Tupper, M. H. & Ridley, J. M. (2002) Mar. Pollut. Bull. 44 , 1177–1183. pmid:12523516 LaunchUrlCrossRefPubMed
Like (0) or Share (0)