Marine reserves: long-term protection is required for full recovery of predatory fish populations

No-take marine reserves are advocated widely as a potential solution to the loss of marine biodiversity and ecosystem structure, and to over-fishing. We assess the duration of protection required for unfished populations of large predatory reef fish to attain natural states. We have monitored two marine reserves at Sumilon and Apo Islands, Philippines, regularly for 17 years (1983–2000). The biomass of large predatory fish was still increasing exponentially after 9 and 18 years of protection at Sumilon and Apo reserves, respectively. There was little evidence that the rate of accumulation of biomass inside the reserves was slowing down even after so many years of protection. This suggests that the length of time to full recovery will be considerable. We made two assumptions in order to estimate this period. Firstly, that biomass growth will follow the logistic model. Secondly, the conservative assumption that biomass had already attained 90% of the local carrying capacity of the environments in the reserves. We conclude that the time required for full recovery will be 15 and 40 years at Sumilon and Apo reserves, respectively. Such durations of recovery appear consistent with known life history characteristics of these fish, and with empirical data on recovery rates of heavily exploited fish stocks. By the time the full fisheries or ecosystem benefits from such reserves are apparent, human populations and impacts will have doubled in much of the developing world. Thus, networks of such reserves need to be implemented immediately. Furthermore, the management mechanisms for the reserves need to be successful over timescales of human generations.     

The intrinsic vulnerability to fishing of coral reef fishes and their differential recovery in fishery closures

Coral reef fishes differ in their intrinsic vulnerability to fishing and rates of population recovery after cessation of fishing. We reviewed life history-based predictions about the vulnerability of different groups of coral reef fish and examined the empirical evidence for different rates of population recovery inside no-take marine reserves to (1) determine if the empirical data agree with predictions about vulnerability and (2) show plausible scenarios of recovery within fully protected reserves and periodically-harvested fishery closures. In general, larger-bodied carnivorous reef fishes are predicted to be more vulnerable to fishing while smaller-bodied species lower in the food web (e.g., some herbivores) are predicted to be less vulnerable. However, this prediction does not always hold true because of the considerable diversity of life history strategies in reef fishes. Long-term trends in reef fish population recovery inside no-take reserves are consistent with broad predictions about vulnerability, suggesting that moderately to highly vulnerable species will require a significantly longer time (decades) to attain local carrying capacity than less vulnerable species. We recommend: (1) expanding age-based demographic studies of economically and ecologically important reef fishes to improve estimates of vulnerability; (2) long term (20–40 years), if not permanent, protection of no-take reserves to allow full population recovery and maximum biomass export; (3) strict compliance to no-take reserves to avoid considerable delays in recovery; (4) carefully controlling the timing and intensity of harvesting periodic closures to ensure long-term fishery benefits; (5) the use of periodically-harvested closures together with, rather than instead of, permanent no-take reserves.     

Spatial and temporal variation of abundance,biomass and diversity within marine reserves in the Philippines

Aim The objective of this study was to investigate the influence of protection duration (years of fishing closure) and location (distance from shore) on reef fish diversity. Location Danajon Double Barrier Reef, Bohol, Philippines. Methods Reef fish abundance and size structure, by species, were obtained monthly using replicated underwater visual belt transects (n = 8; 70 × 5‐m belt transects) over 3 years (2002–2005) at eight sites that included six marine reserves and two unprotected reef areas. We analysed species accumulation curves, diversity indices and abundance–biomass comparison (ABC) curves within and across the study sites to assess the influence of protection duration and location. Results Analyses showed that longer protection duration impacted reef fish diversity at both inshore and offshore sites by shifting ABC curves from higher abundance than biomass curves at fished sites to higher biomass than abundance curves at most of the protected sites. Protection duration did not significantly influence either the rate of species accumulation within sites or the 12 diversity indices measured across the study sites. The offshore sites consistently showed higher rates of species accumulation and diversity indices values than inshore sites with similar protection duration. One protected offshore young marine reserve site that has been assessed as the least well‐managed showed patterns more consistent with the fished sites. Main conclusions Analyses showed that protection duration mainly impacted diversity by increasing the dominance of large‐bodied species and enhancing total biomass. Besides protection duration, reserve location influenced species accumulation curves and diversity indices.     

Ecological guidelines for designing networks of marine reserves in the unique biophysical environment of the Gulf of California

No-take marine reserves can be powerful management tools, but only if they are well designed and effectively managed. We review how ecological guidelines for improving marine reserve design can be adapted based on an area’s unique evolutionary, oceanic, and ecological characteristics in the Gulf of California, Mexico. We provide ecological guidelines to maximize benefits for fisheries management, biodiversity conservation and climate change adaptation. These guidelines include: representing 30% of each major habitat (and multiple examples of each) in marine reserves within each of three biogeographic subregions; protecting critical areas in the life cycle of focal species (spawning and nursery areas) and sites with unique biodiversity; and establishing reserves in areas where local threats can be managed effectively. Given that strong, asymmetric oceanic currents reverse direction twice a year, to maximize connectivity on an ecological time scale, reserves should be spaced less than 50–200 km apart depending on the planktonic larval duration of target species; and reserves should be located upstream of fishing sites, taking the reproductive timing of focal species in consideration. Reserves should be established for the long term, preferably permanently, since full recovery of all fisheries species is likely to take?>?25 years. Reserve size should be based on movement patterns of focal species, although marine reserves?>?10 km long are likely to protect?~?80% of fish species. Since climate change will affect species’ geographic range, larval duration, growth, reproduction, abundance, and distribution of key recruitment habitats, these guidelines may require further modifications to maintain ecosystem function in the future.     

Evidence of artisanal fishing impacts and depth refuge in assemblages of Fijian reef fish

Protection from fishing generally results in an increase in the abundance and biomass of species targeted by fisheries within marine reserve boundaries. Natural refuges such as depth may also protect such species, yet few studies in the Indo Pacific have investigated the effects of depth concomitant with marine reserves. We studied the effects of artisanal fishing and depth on reef fish assemblages in the Kubulau District of Vanua Levu Island, Fiji, using baited remote underwater stereo-video systems. Video samples were collected from shallow (5–8 m) and deep (25–30 m) sites inside and outside of a large old marine reserve (60.6 km², 13 years old) and a small new marine reserve (4.25 km², 4 years old). Species richness tended to be greater in the shallow waters of the large old reserve when compared to fished areas. In the deeper waters, species richness appeared to be comparable. The difference in shallow waters was driven by species targeted by fisheries, indicative of a depth refuge effect. In contrast, differences in the abundance composition of the fish assemblage existed between protected and fished areas for deep sites, but not shallow. Fish species targeted by local fisheries were 89% more abundant inside the large old reserve than surrounding fished areas, while non-targeted species were comparable. We observed no difference in the species richness or abundance of species targeted by fisheries inside and outside of the small new reserve. This study suggests that artisanal fishing impacts on the abundance and species richness of coral reef fish assemblages and effects of protection are more apparent with large reserves that have been established for a long period of time. Observed effects of protection also vary with depth, highlighting the importance of explicitly incorporating multiple depth strata in studies of marine reserves.     

Extinction, survival or recovery of large predatory fishes

Large predatory fishes have long played an important role in marine ecosystems and fisheries. Overexploitation, however, is gradually diminishing this role. Recent estimates indicate that exploitation has depleted large predatory fish communities worldwide by at least 90% over the past 50-100 years. We demonstrate that these declines are general, independent of methodology, and even higher for sensitive species such as sharks. We also attempt to predict the future prospects of large predatory fishes. (i) An analysis of maximum reproductive rates predicts the collapse and extinction of sensitive species under current levels of fishing mortality. Sensitive species occur in marine habitats worldwide and have to be considered in most management situations. (ii) We show that to ensure the survival of sensitive species in the northwest Atlantic fishing mortality has to be reduced by 40-80%. (iii) We show that rapid recovery of community biomass and diversity usually occurs when fishing mortality is reduced. However, recovery is more variable for single species, often because of the influence of species interactions. We conclude that management of multi-species fisheries needs to be tailored to the most sensitive, rather than the more robust species. This requires reductions in fishing effort, reduction in bycatch mortality and protection of key areas to initiate recovery of severely depleted communities.     

Effects of marine reserves versus nursery habitat availability on structure of reef fish communities

No-take marine fishery reserves sustain commercial stocks by acting as buffers against overexploitation and enhancing fishery catches in adjacent areas through spillover. Likewise, nursery habitats such as mangroves enhance populations of some species in adjacent habitats. However, there is lack of understanding of the magnitude of stock enhancement and the effects on community structure when both protection from fishing and access to nurseries concurrently act as drivers of fish population dynamics. In this study we test the separate as well as interactive effects of marine reserves and nursery habitat proximity on structure and abundance of coral reef fish communities. Reserves had no effect on fish community composition, while proximity to nursery habitat only had a significant effect on community structure of species that use mangroves or seagrass beds as nurseries. In terms of reef fish biomass, proximity to nursery habitat by far outweighed (biomass 249% higher than that in areas with no nursery access) the effects of protection from fishing in reserves (biomass 21% lower than non-reserve areas) for small nursery fish (≤ 25 cm total length). For large-bodied individuals of nursery species (>25 cm total length), an additive effect was present for these two factors, although fish benefited more from fishing protection (203% higher biomass) than from proximity to nurseries (139% higher). The magnitude of elevated biomass for small fish on coral reefs due to proximity to nurseries was such that nursery habitats seem able to overrule the usually positive effects on fish biomass by reef reserves. As a result, conservation of nursery habitats gains importance and more consideration should be given to the ecological processes that occur along nursery-reef boundaries that connect neighboring ecosystems.     

Marine reserves indirectly affect fine‐scale habitat associations,but not overall densities,of small benthic fishes

Many large, fishery‐targeted predatory species have attained very high relative densities as a direct result of protection by no‐take marine reserves. Indirect effects, via interactions with targeted species, may also occur for species that are not themselves targeted by fishing. In some temperate rocky reef ecosystems, indirect effects have caused profound changes in community structure, notably the restoration of predator–urchin–macroalgae trophic cascades. Yet, indirect effects on small benthic reef fishes remain poorly understood, perhaps because of behavioral associations with complex, refuge‐providing habitats. Few, if any, studies have evaluated any potential effects of marine reserves on habitat associations in small benthic fishes. We surveyed densities of small benthic fishes, including some endemic species of triplefin (Tripterygiidae), along with fine‐scale habitat features in kelp forests on rocky reefs in and around multiple marine reserves in northern New Zealand over 3 years. Bayesian generalized linear mixed models were used to evaluate evidence for (1) main effects of marine reserve protection, (2) associations with habitat gradients, including complexity, and (3) differences in habitat associations inside versus outside reserves. No evidence of overall main effects of marine reserves on species richness or densities of fishes was found. Both richness and densities showed strong associations with gradients in habitat features, particularly habitat complexity. In addition, some species exhibited reserve‐by‐habitat interactions, having different associations with habitat gradients inside versus outside marine reserves. Two species (Ruanoho whero and Forsterygion flavonigrum) showed stronger positive associations with habitat complexity inside reserves. These results are consistent with the presence of a behavioral risk effect, whereby prey fishes are more strongly attracted to habitats that provide refuge from predation in areas where predators are more abundant. This work highlights the importance of habitat structure and the potential for fishing to affect behavioral interactions and the interspecific dynamic attributes of community structure beyond simple predator–prey consumption and archetypal trophic cascades.     

Mesophotic depths as refuge areas for fishery-targeted species on coral reefs

Coral reefs are subjected to unprecedented levels of disturbance with population growth and climate change combining to reduce standing coral cover and stocks of reef fishes. Most of the damage is concentrated in shallow waters (<30 m deep) where humans can comfortably operate and where physical disturbances are most disruptive to marine organisms. Yet coral reefs can extend to depths exceeding 100 m, potentially offering refuge from the threats facing shallower reefs. We deployed baited remote underwater stereo-video systems (stereo-BRUVs) at depths of 10–90 m around the southern Mariana Islands to investigate whether fish species targeted by fishing in the shallows may be accruing benefits from being at depth. We show that biomass, abundance and species richness of fishery-targeted species increased from shallow reef areas to a depth of 60 m, whereas at greater depths, a lack of live coral habitat corresponded to lower numbers of fish. The majority of targeted species were found to have distributions that ranged from shallow depths (10 m) to depths of at least 70 m, emphasising that habitat, not depth, is the limiting factor in their vertical distribution. While the gradient of abundance and biomass versus depth was steepest for predatory species, the first species usually targeted by fishing, we also found that fishery-targeted herbivores prevailed in similar biomass and species richness to 60 m. Compared to shallow marine protected areas, there was clearly greater biomass of fishery-targeted species accrued in mesophotic depths. Particularly some species typically harvested by depth-limited fishing methods (e.g., spearfishing), such as the endangered humphead wrasse Cheilinus undulatus, were found in greater abundance on deeper reefs. We conclude that mesophotic depths provide essential fish habitat and refuge for fishery-targeted species, representing crucial zones for fishery management and research into the resilience of disturbed coral reef ecosystems.     

Large recovery of fish biomass in a no-take marine reserve

No-take marine reserves are effective management tools used to restore fish biomass and community structure in areas depleted by overfishing. Cabo Pulmo National Park (CPNP) was created in 1995 and is the only well enforced no-take area in the Gulf of California, Mexico, mostly because of widespread support from the local community. In 1999, four years after the establishment of the reserve, there were no significant differences in fish biomass between CPNP (0.75 t ha(-1) on average) and other marine protected areas or open access areas in the Gulf of California. By 2009, total fish biomass at CPNP had increased to 4.24 t ha(-1) (absolute biomass increase of 3.49 t ha(-1), or 463%), and the biomass of top predators and carnivores increased by 11 and 4 times, respectively. However, fish biomass did not change significantly in other marine protected areas or open access areas over the same time period. The absolute increase in fish biomass at CPNP within a decade is the largest measured in a marine reserve worldwide, and it is likely due to a combination of social (strong community leadership, social cohesion, effective enforcement) and ecological factors. The recovery of fish biomass inside CPNP has resulted in significant economic benefits, indicating that community-managed marine reserves are a viable solution to unsustainable coastal development and fisheries collapse in the Gulf of California and elsewhere.     

The diets and parasites of larval and 0+ juvenile twaite shad in the lower reaches and estuaries of the rivers Wye,Usk and Towy,UK

Aquatic predators and habitat permanence can jointly affect benthic invertebrate biomass and community composition. In 2006 I sampled fish and invertebrates in ten ponds embedded in a seasonal wetland before and after a natural drought. Drought reduced fish biomass and density leaving some ponds in a fishless condition when rains returned in July. In July, large aquatic insects and crayfish colonized and reproduced in the ponds, but did not colonize all of the ponds equally. Using measurements of fish abundance and other environmental parameters of the ponds, I conducted linear regression analyses to explore potential drivers of variable invertebrate biomass in July. Fish biomass had a negative effect on invertebrate biomass and it explained more of the variation in total invertebrate biomass and total non-shrimp biomass than fish abundance (number of fish caught). Dissolved oxygen and pond depth were both correlated with fish biomass, but were poorer predictors of invertebrate biomass. Ponds with few or no fish had 20× greater total biomass and 200× more non-shrimp biomass than ponds with high fish biomass. Shrimp dominated the invertebrate composition, and were only found in the two deepest ponds with the highest fish biomass; predatory insects and crayfish dominated the other eight ponds. When taxa were analyzed separately, fish biomass explained a large portion of the variation for predatory insects (Coleoptera, Hemiptera, and Odonata) and crayfish (Procambarus alleni), but dissolved oxygen was the best predictor of larval stratiomyid (order Diptera) biomass. These results are generally consistent with studies demonstrating negative effects of fish on large predatory invertebrates, but also suggest that more severe local droughts can seasonally enhance insect and crayfish populations by generating fishless or nearly fishless conditions. Handling editor: J. Trexler     

Changes in fish assemblages following 10 years of protection in Tasmanian marine protected areas

Most studies examining effects of marine protected areas (MPAs) on fish assemblages are potentially confounded, either because they are once off comparisons between fished and unfished locations, or because they are snapshot studies over a fixed period. Here we compare long-term changes within fully protected Tasmanian marine reserves with changes at external reference sites on an annual basis over the first ten years of protection. The results highlight the importance of long-term datasets for differentiating changes occurring over differing time scales. Notable results include a statistically significant increase in abundance of Latridopsis forsteri and large fish (> 300 mm) when examined across all reserves relative to controls, and a 10-fold increase in the abundance of large fish and a doubling of per site species richness of large fish within the Tinderbox Marine Reserve relative to controls. Short-term resident species that recruit sporadically show very different patterns in reserves compared to those that recruit regularly and have long-term age-class storage. While several recent reviews have suggested size of MPAs and duration of protection has little influence on the extent of recovery, our results suggest this is not the case and that responses can be slow, complex and species-specific. The extent of localised fishing pressure appeared to have a substantial influence on the degree of change detected, potentially confounding meta-analyses of recovery rates in MPAs if overlooked as a relevant parameter.     

Fiji’s largest marine reserve benefits reef sharks

To provide more information about whether sharks benefit from no-take marine reserves, we quantified the relative abundance and biomass of reef sharks inside and outside of Namena, Fiji’s largest reserve (60.6 km²). Using stereo baited remote underwater video systems (stereo-BRUVs), we found that the abundance and biomass of sharks was approximately two and four times greater in shallow and deep locations, respectively, within the Namena reserve compared to adjacent fished areas. The greater abundance and biomass of reef sharks inside Namena is likely a result of greater prey availability rather than protection from fishing. This study demonstrates that marine reserves can benefit sharks.     

The structure of Mediterranean rocky reef ecosystems across environmental and human gradients, and conservation implications

Historical exploitation of the Mediterranean Sea and the absence of rigorous baselines makes it difficult to evaluate the current health of the marine ecosystems and the efficacy of conservation actions at the ecosystem level. Here we establish the first current baseline and gradient of ecosystem structure of nearshore rocky reefs at the Mediterranean scale. We conducted underwater surveys in 14 marine protected areas and 18 open access sites across the Mediterranean, and across a 31-fold range of fish biomass (from 3.8 to 118 g m(-2)). Our data showed remarkable variation in the structure of rocky reef ecosystems. Multivariate analysis showed three alternative community states: (1) large fish biomass and reefs dominated by non-canopy algae, (2) lower fish biomass but abundant native algal canopies and suspension feeders, and (3) low fish biomass and extensive barrens, with areas covered by turf algae. Our results suggest that the healthiest shallow rocky reef ecosystems in the Mediterranean have both large fish and algal biomass. Protection level and primary production were the only variables significantly correlated to community biomass structure. Fish biomass was significantly larger in well-enforced no-take marine reserves, but there were no significant differences between multi-use marine protected areas (which allow some fishing) and open access areas at the regional scale. The gradients reported here represent a trajectory of degradation that can be used to assess the health of any similar habitat in the Mediterranean, and to evaluate the efficacy of marine protected areas.     

Trajectories and magnitude of change in coral reef fish populations in Philippine marine reserves: a meta-analysis

Marine reserves are widely implemented worldwide to meet both conservation and fisheries management goals. This study examines the efficacy of Philippine marine reserves using meta-analysis by comparing variations in fish density (1) between reserves and adjacent fished reefs (spatial comparison), (2) within reserves before establishment relative to years following the establishment (temporal comparison), and (3) among reserves classified based on size, age, and enforcement capacity. A grand (total) mean of nineteen 22.3 ha coral reef reserves, protected for a mean duration of 8.2 years, were included in the meta-analyses. The overall density of fishes was higher in the reserves compared with the fished reefs and this difference was largely accounted for by exploited fishes. However, the overall density of fishes within the same reserves remained similar from the period before its establishment to several years following its establishment. Only the density of nonexploited fishes increased significantly during years subsequent to the establishment of the reserves. Neither age nor size of reserves correlated with pattern of change in fish density following the establishment of the reserves; however, fish density was consistently higher in larger and older reserves relative to smaller and younger reserves in the spatial comparison. Furthermore, well-enforced reserves had higher density of exploited fishes relative to less-enforced reserves in both spatial and temporal comparisons. In general, the magnitude and trajectory of change in fish density following the establishment of Philippine marine reserves are influenced by (1) functional groups of fishes under consideration, (2) size and age of the reserve, and (3) level of enforcement of the regulatory mechanisms necessary to sustain a marine reserve.     

Effects of marine reserve characteristics on the protection of fish populations: a meta-analysis

Meta-analyses of published data for 19 marine reserves reveal that marine protected areas enhance species richness consistently, but their effect on fish abundance is more variable. Overall, there was a slight (11%) but significant increase in fish species number inside marine reserves, with all reserves sharing a common effect. There was a substantial but non-significant increase in overall fish abundance inside marine reserves compared to adjacent, non-reserve areas. When only species that are the target of fisheries were considered, fish abundance was significantly higher (by 28%) within reserve boundaries. Marine reserves vary significantly in the extent and direction of their response. This variability in relative abundance was not attributable to differences in survey methodology among studies, nor correlated with reserve characteristics such as reserve area, years since protection, latitude nor species diversity. The effectiveness of marine reserves in enhancing fish abundance may be largely related to the intensity of exploitation outside reserve boundaries and to the composition of the fish community within boundaries. It is recommended that studies of marine reserve effectiveness should routinely report fishing intensity, effectiveness of enforcement and habitat characteristics.     

Modelling spatial and temporal scales for spill-over and biomass exportation from MPAs and their potential for fisheries enhancement

Marine protected areas (MPAs) are considered as a tool for marine conservation and sustainable fishery resource management. Improvements in fishery yields should take place via the spill-over of individuals from the reserve. In general, it has been demonstrated that MPAs affect the density and biomass of the organisms within them, however, little evidence has been found in order to assess the exportation of individuals across their boundaries. In this study, a simple model involving population growth, harvest, and the diffusion coefficient for individuals was used to explore the effects of protection on populations inside the reserve and the spill-over of individuals to the fished area. The model showed that biological responses inside marine reserves appear to develop quickly, reaching mean levels within a short (1–5 year) time period. Mean population abundance is always higher inside the reserve and highlights the effectiveness of protection, particularly when there is strong fishing pressure outside the reserve. However, reserves smaller than 2000 m radius show significantly lower levels of abundance inside than larger sites. Large MPAs (i.e. about 2000 m in radius) offer nearly the maximum capacity for recovery (close to 100% of the system carrying capacity) and nearly the maximum flux of individuals per unit boundary length. Very large MPAs (i.e. larger than 6000 m in radius) could be a guaranteed means of providing resilience in order to prevent population crises, with the added advantage that the flux of individuals is slightly higher at larger distances from the boundary. However, in practice they provide no further advantage towards increasing the density of individuals or the exportation of biomass, and a network of smaller MPAs could be more beneficial, both from the point of view of conservation and of benefits to fisheries.     

Spillover of fish naïveté from marine reserves

Spillover of adult fish biomass is an expected benefit from no‐take marine reserves to adjacent fisheries. Here, we show fisher‐naïve behaviour in reef fishes also spills over from marine reserves, potentially increasing access to fishery benefits by making fishes more susceptible to spearguns. The distance at which two targeted families of fishes began to flee a potential fisher [flight initiation distance (FID)] was lower inside reserves than in fished areas, and this reduction extended outside reserve boundaries. Reduced FID persisted further outside reserves than increases in fish biomass. This finding could help increase stakeholder support for marine reserves and improve current models of spillover by informing estimates for spatial changes in catchability. Behavioural changes of fish could help explain differences between underwater visual census and catch data in quantifying the spatial extent of spillover from marine reserves, and should be considered in the management of adjacent fisheries.     

Changes in Fish Assemblages following the Establishment of a Network of No-Take Marine Reserves and Partially-Protected Areas

Networks of no-take marine reserves and partially-protected areas (with limited fishing) are being increasingly promoted as a means of conserving biodiversity. We examined changes in fish assemblages across a network of marine reserves and two different types of partially-protected areas within a marine park over the first 5 years of its establishment. We used Baited Remote Underwater Video (BRUV) to quantify fish communities on rocky reefs at 20–40 m depth between 2008–2011. Each year, we sampled 12 sites in 6 no-take marine reserves and 12 sites in two types of partially-protected areas with contrasting levels of protection (n = 4 BRUV stations per site). Fish abundances were 38% greater across the network of marine reserves compared to the partially-protected areas, although not all individual reserves performed equally. Compliance actions were positively associated with marine reserve responses, while reserve size had no apparent relationship with reserve performance after 5 years. The richness and abundance of fishes did not consistently differ between the two types of partially-protected areas. There was, therefore, no evidence that the more regulated partially-protected areas had additional conservation benefits for reef fish assemblages. Overall, our results demonstrate conservation benefits to fish assemblages from a newly established network of temperate marine reserves. They also show that ecological monitoring can contribute to adaptive management of newly established marine reserve networks, but the extent of this contribution is limited by the rate of change in marine communities in response to protection.