Date Published: October 13, 2015
Publisher: Public Library of Science
Author(s): German A. Soler, Graham J. Edgar, Russell J. Thomson, Stuart Kininmonth, Stuart J. Campbell, Terence P. Dawson, Neville S. Barrett, Anthony T. F. Bernard, David E. Galván, Trevor J. Willis, Timothy J. Alexander, Rick D. Stuart-Smith, Dennis M. Higgs.
Marine Protected Areas (MPAs) offer a unique opportunity to test the assumption that fishing pressure affects some trophic groups more than others. Removal of larger predators through fishing is often suggested to have positive flow-on effects for some lower trophic groups, in which case protection from fishing should result in suppression of lower trophic groups as predator populations recover. We tested this by assessing differences in the trophic structure of reef fish communities associated with 79 MPAs and open-access sites worldwide, using a standardised quantitative dataset on reef fish community structure. The biomass of all major trophic groups (higher carnivores, benthic carnivores, planktivores and herbivores) was significantly greater (by 40% – 200%) in effective no-take MPAs relative to fished open-access areas. This effect was most pronounced for individuals in large size classes, but with no size class of any trophic group showing signs of depressed biomass in MPAs, as predicted from higher predator abundance. Thus, greater biomass in effective MPAs implies that exploitation on shallow rocky and coral reefs negatively affects biomass of all fish trophic groups and size classes. These direct effects of fishing on trophic structure appear stronger than any top down effects on lower trophic levels that would be imposed by intact predator populations. We propose that exploitation affects fish assemblages at all trophic levels, and that local ecosystem function is generally modified by fishing.
Marine protected area (MPA) networks represent an experimental set of ecological plots with reduced human extraction pressure. As such, MPAs provide an ideal focus for improved understanding of broad-scale effects of protection through comparison of differences in fished and protected areas . Effective MPAs also provide a reference benchmark as undisturbed ecosystems for comparison with sites with high human impact . Nevertheless, many MPAs do not appear to be effectively achieving conservation goals [3–6].
Marine ecological survey data were collected worldwide through the Reef Life Survey program (RLS: http://www.reeflifesurvey.org) from September 2006 until November 2012 (see Edgar and Stuart-Smith  for details). The following authorities gave permission for field studies: Australia Department of Environment, Costa Rica Sistema Nacional de Areas de Conservacion, Galapagos National Parks Service, NSW Department of Primary Industries, New Zealand Department of Conservation, Panama Autoridad Nacional del Ambiente, Parks Victoria, Parques Nacionales Naturales de Colombia, Rottnest Island Authority, South Australia Department of Environment Water and Natural Resources, Tasmania Parks and Wildlife Service, United States Fish and Wildlife Service, United States National Park Service, Western Australia Department of Parks and Wildlife. Data covered 1,844 rocky and coral reef sites in 11 realms and 74 ecoregions  (Fig 1). The level of protection from fishing of each site was classed as no-take (no fishing allowed), restricted fishing (some form of fishery restrictions in place), or open-access. The ecological effectiveness of MPAs also depends on compliance with regulations and time since declaration . Here we considered no-take zones to be effective if they exhibited a medium to high level of enforcement and had been established for at least five years prior to the fish survey (S1 Table). MPAs at which limited fishing was allowed, where enforcement of regulations was poor, and/or less than five years had elapsed since creation were considered less effective. Sites were assessed for effective protection using information on zoning in management plans, patrolling capacity, and infractions observed while in the field undertaking surveys, as described in Edgar et al. . Open-access sites lay outside MPAs, or inside MPAs in zones with no restrictions on fishing other than national regulations (e.g. no explosives). A total of 79 MPAs were investigated, including some with multiple zones of differing effectiveness. A total of 405 sites within 50 MPAs were classified as effective no-take areas, 509 sites within 54 MPA were classified as low effectiveness, and 930 sites were open-access.
The population index was used as a proxy for human pressure, and had a significant negative effect on biomass of higher and benthic carnivores (Fig 2). The three environmental covariates, SST mean, SST range and PAR-mean, also had significant effects on fish biomass. However, only SST mean was significant for all four trophic groups (Fig 2). PAR-mean had a significant positive effect for biomass of planktivores and herbivores. SST range had a significant negative effect on biomass of higher carnivores, planktivores and herbivores (Fig 2).
Our results show clear differences in fish community structure due to protection from fishing in effective MPAs (i.e. no-take, with medium to high enforcement and over 5 years old). Higher biomass of large predatory species was particularly marked, while the biomass of all other trophic groups was either greater or equal in effective MPAs compared with open-access sites. Thus, none of the trophic or size groups had negative biomass ratios in MPAs compared with open-access sites that would indicate patterns for top-down control of the fish community in the presence of greater biomass of predatory fishes. This result was consistent even when considering only the MPAs identified as most effective and having the five attributes of protection outlined in Edgar et al.  and known to have elevated biomass of the major groups of predatory and exploited species. This does not imply that cascading trophic interactions have not occurred in effective MPAs, as our study did not look at individual species, but rather at the scale of whole trophic size groups. However it does present two clear, novel outcomes with respect to general MPA effects: (1) that protection from fishing appears to favor all trophic groups, some much more than might be expected (e.g. medium-sized planktivores); and (2) that regardless of whether cascading trophic interactions occur within MPAs, the disparity in the biomass ratios between MPAs and open access sites for the different size-classes of trophic groups implies a trophic re-organisation that is likely to have substantial consequences for ecological functions.