Coral cover a stronger driver of reef fish trophic biomass than fishing

Abstract

An influential paradigm in coral reef ecology is that fishing causes trophic cascades through reef fish assemblages, resulting in reduced herbivory and thus benthic phase shifts from coral to algal dominance. Few long-term field tests exist of how fishing affects the trophic structure of coral reef fish assemblages, and how such changes affect the benthos. Alternatively, benthic change itself may drive the trophic structure of reef fish assemblages. Reef fish trophic structure and benthic cover were quantified almost annually from 1983 to 2014 at two small Philippine islands (Apo, Sumilon). At each island a No-Take Marine Reserve (NTMR) site and a site open to subsistence reef fishing were monitored. Thirteen trophic groups were identified. Large planktivores often accounted for >50% of assemblage biomass. Significant NTMR effects were detected at each island for total fish biomass, but for only 2 of 13 trophic components: generalist large predators and large planktivores. Fishing-induced changes in biomass of these components had no effect on live hard coral (HC) cover. In contrast, HC cover affected biomass of 11 of 13 trophic components significantly. Positive associations with HC cover were detected for total fish biomass, generalist large predators, piscivores, obligate coral feeders, large planktivores, and small planktivores. Negative associations with HC cover were detected for large benthic foragers, detritivores, excavators, scrapers, and sand feeders. These associations of fish biomass to HC cover were most clear when environmental disturbances (e.g., coral bleaching, typhoons) reduced HC cover, often quickly (1-2 yr), and when HC recovered, often slowly (5-10 yr). As HC cover changed, the biomass of 11 trophic components of the fish assemblage changed. Benthic and fish assemblages were distinct at all sites from the outset, remaining so for 31 yr, despite differences in fishing pressure and disturbance history. HC cover alone explained ~30% of the variability in reef fish trophic structure, whereas fishing alone explained 24%. Furthermore, HC cover affected more trophic groups more strongly than fishing. Management of coral reefs must include measures to maintain coral reef habitats, not just measures to reduce fishing by NTMRs.

Keywords: Philippines; coral cover; coral reef fish; environmental disturbances; fishing effects; no-take marine reserves; trophic biomass.

Fig. 1

Location of the study sites in the central Philippines. Inset (a) Sumilon Island. Inset (b) Apo Island. Cross‐hatch indicates marine reserve area and black rectangles indicate approximate positions of permanent 50 × 20 m replicate transects for fish and benthic surveys.

Fig. 2

Long‐term (1983–2014) temporal trends in (a) total reef fish biomass and (b) live hard coral cover (HC) vs. years of protection by no‐take marine reserve (NTMR) status at Apo Island (top panels of a and b) and Sumilon Island (bottom panels of a and b). (c) Total reef fish biomass vs. chronological time (1983–2014) at Sumilon NTMR (top panel) and Sumilon fished site (bottom panel). Arrows in c indicate times when fishing starts (black), stops (white), or was restricted to hook and line fishing only (gray). Data points are means, trend lines are sixth order polynomials, and shading represents 95% confidence intervals. NTMR sites are shown in green and fished sites in blue. Note that the y‐axis for hard coral is percent cover, not biomass. Note y‐axis ranges differ among panels.

Fig. 3

Long‐term (1983–2014) temporal trends in biomass of three trophic groups vs. years of protection by no‐take marine reserve (NTMR) status at Apo (upper panels) and Sumilon (lower panels) Islands. These three trophic groups had the clearest evidence of direct NTMR effects. Data points are means, trend lines are sixth‐order polynomials, and shading represents 95% confidence intervals. NTMR sites shown in green and fished sites in blue. Note y‐axis ranges differ among panels.

Fig. 4

Long‐term (1983–2014) temporal trends in total reef fish biomass (left y‐axis) and hard coral cover (HC) (right y‐axis) at Apo NTMR and Apo fished sites (left column) and Sumilon NTMR and fished site (right column). Data points are means, trend lines are sixth‐order polynomials, and shading represents 95% confidence intervals. Fish biomass is purple and live hard coral is brown. Note y‐axis ranges differ among panels. Environmental disturbances (red brackets) are coral bleaching (1998) at all four sites, local storm (2010) and back‐to‐back typhoons (2011–2012) at Apo NTMR, destructive fishing (1984) at Sumilon NTMR, and typhoon (2012) at Sumilon fished site.

Fig. 5

Long‐term (1983–2014) temporal trends in biomass (left y‐axis) of four trophic groups of reef fish and live hard coral cover (HC; right y‐axis) at Apo NTMR (first column), Apo fished site (second column), Sumilon NTMR (third column), and Sumilon fished site (fourth column). These are examples of trophic groups that had a generally positive relationship with HC. Data points are means, trend lines are sixth‐order polynomials, and shading represents 95% confidence intervals. Fish biomass is purple and live hard coral is brown. Note y‐axis ranges differ among panels. Environmental disturbances (red brackets) are coral bleaching (1998) at all four sites, local storm (2010) and back‐to‐back typhoons (2011–2012) at Apo NTMR, destructive fishing (1984) at Sumilon NTMR, and typhoon (2012) at Sumilon fished site.

Fig. 6

Long‐term (1983–2014) temporal trends in biomass (left y‐axis) of four trophic groups of reef fish and live hard coral cover (HC) (right y‐axis) at Apo NTMR (first column), Apo fished site (second column), Sumilon NTMR (third column), and Sumilon fished site (fourth column). These are examples of trophic groups that had a generally negative relationship with HC. Data points are means, trend lines are sixth‐order polynomials, and shading represents 95% confidence intervals. Fish biomass is purple and live hard coral is brown. Note y‐axis ranges differ among panels. Environmental disturbances (red brackets) are coral bleaching (1998) at all four sites, local storm (2010) and back‐to‐back typhoons (2011–2012) at Apo NTMR, destructive fishing (1984) at Sumilon NTMR, and typhoon (2012) at Sumilon fished site.

Fig. 7

Nonmetric multidimensional scaling (NMDS) analysis performed on distance matrices for (a) benthic cover of hard coral and dead substrate and duration of NTMR protection (yr) and (b) the biomass of reef fish trophic groups. Apo fished sites are dark blue, Apo NTMR sites are dark green, Sumilon fished sites are light blue, and Sumilon NTMR sites are light green. Dotted circles (benthos) and ellipses (fish) represent years when typhoons hit Apo NTMR and the Sumilon fished site, and when Sumilon NTMR was opened to fishing in 1984 and 1992. Numbers adjacent to NTMR sites (dark and light green) indicate the duration of NTMR protection in years. Vectors represent Pearson correlations between the original variables ([a] hard coral, dead substrate, duration of NTMR protection; [b] biomass of reef fish trophic groups). Lengths of the vectors are proportional to the squared multiple correlation coefficient.