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

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.

Decadal-scale response of detritivorous surgeonfishes (family Acanthuridae) to no-take marine reserve protection and changes in benthic habitat.

No-take marine reserves (NTMR) are increasingly being implemented to mitigate the effects of fishing on coral reefs, yet determining the efficacy of NTMRs depends largely on partitioning the effects of fishing from the effect of benthic habitat. Species of coral-reef fishes typically decline in density when subjected to fishing or benthic disturbances, but this is not always the case. This study documents the long-term (8-31 years) response of six species of detritivorous surgeonfishes (family Acanthuridae) to NTMR protection and benthic habitat change at four islands (Apo, Sumilon, Mantigue, Selinog) in the central Philippines, each island with a NTMR and a monitored fished site. Despite being subject to moderate fishing pressure, these species did not increase in density with NTMR protection. However, density of these surgeonfishes had a strong negative relationship with cover of live hard coral and a strong positive relationship with cover of dead substratum (sand, rubble, hard dead substratum). These surgeonfishes typically feed over dead substrata and thus probably increase in density following large environmental disturbances that substantially reduce live hard coral cover. Here, we describe effects of environmental disturbance events (e.g., use of explosives, typhoons) that reduced live hard-coral cover and subsequent large increases (up to 25 fold) in surgeonfish densities, which then slowly (over 5-15 years) decreased in density as live hard coral recovered. Density of these functionally important surgeonfish species was influenced more by changes to benthic cover than by NTMR protection. Thus, we highlight the greater importance of bottom-up controls (i.e., benthic changes to food availability) than top-down control (i.e., fishing) on a functionally important group of coral-reef fishes.

Phylogeographic patterns in the Philippine archipelago influence symbiont diversity in the bobtail squid-Vibrio mutualism.

Marine microbes encounter a myriad of biotic and abiotic factors that can impact fitness by limiting their range and capacity to move between habitats. This is especially true for environmentally transmitted bacteria that cycle between their hosts and the surrounding habitat. As geologic history, biogeography, and other factors such as water temperature, salinity, and physical barriers can inhibit bacterial movement to novel environments, we chose to examine the genetic architecture of Euprymna albatrossae (Mollusca: Cephalopoda) and their Vibrio fischeri symbionts in the Philippine archipelago using a combined phylogeographic approach. Eleven separate sites in the Philippine islands were examined using haplotype estimates that were examined via nested clade analysis to determine the relationship between E. albatrossae and V. fischeri populations and their geographic location. Identical analyses of molecular variance (AMOVA) were used to estimate variation within and between populations for host and symbiont genetic data. Host animals demonstrated a significant amount of variation within island groups, while symbiont variation was found within individual populations. Nested clade phylogenetic analysis revealed that hosts and symbionts may have colonized this area at different times, with a sudden change in habitat. Additionally, host data indicate restricted gene flow, whereas symbionts show range expansion, followed by periodic restriction to genetic flow. These differences between host and symbiont networks indicate that factors "outside the squid" influence distribution of Philippine V. fischeri. Our results shed light on how geography and changing environmental factors can impact marine symbiotic associations at both local and global scales.

Partitioning no-take marine reserve (NTMR) and benthic habitat effects on density of small and large-bodied tropical wrasses.

No-take marine reserves (NTMRs) are increasingly implemented for fisheries management and biodiversity conservation. Yet, assessing NTMR effectiveness depends on partitioning the effects of NTMR protection and benthic habitat on protected species. Such partitioning is often difficult, since most studies lack well-designed sampling programs (i.e. Before-After-Control-Impact-Pair designs) spanning long-term time scales. Spanning 31 years, this study quantifies the effects of NTMR protection and changes to benthic habitat on the density of tropical wrasses (F. Labridae) at Sumilon and Apo Islands, Philippines. Five species of wrasse were studied: two species of large-bodied (40-50 cm TL) Hemigymnus that were vulnerable to fishing, and three species of small-bodied (10-25 cm TL) Thalassoma and Cirrhilabrus that were not targeted by fishing. NTMR protection had no measurable effect on wrasse density, irrespective of species or body size, over 20 (Sumilon) and 31 (Apo) years of protection. However, the density of wrasses was often affected strongly by benthic cover. Hemigymnus spp. had a positive association with hard coral cover, while Thalassoma spp. and Cirrhilabrus spp. had strong positive associations with cover of rubble and dead substratum. These associations were most apparent after environmental disturbances (typhoons, coral bleaching, crown of thorns starfish (COTS) outbreaks, use of explosives and drive nets) reduced live hard coral cover and increased cover of rubble, dead substratum and sand. Disturbances that reduced hard coral cover often reduced the density of Hemigymnus spp. and increased the density of Thalassoma spp. and Cirrhilabrus spp. rapidly (1-2 years). As hard coral recovered, density of Hemigymnus spp. often increased while density of Thalassoma spp. and Cirrhilabrus spp. often decreased, often on scales of 5-10 years. This study demonstrates that wrasse population density was influenced more by changes to benthic cover than by protection from fishing.

The amphibians and reptiles of Mindanao Island, southern Philippines, II: the herpetofauna of northeast Mindanao and adjacent islands.

We summarize all available amphibian and reptile species distribution data from the northeast Mindanao faunal region, including small islands associated with this subcenter of endemic vertebrate biodiversity. Together with all publicly available historical information from biodiversity repositories, we present new data from several major herpetological surveys, including recently conducted inventories on four major mountains of northeast Mindanao, and adjacent islands of Camiguin Sur, Dinagat, and Siargao. We present species accounts for all taxa, comment on unresolved taxonomic problems, and provide revisions to outdated IUCN conservation status assessments in cases where our new data significantly alter earlier classification status summaries. Together, our comprehensive analysis of this fauna suggests that the greater Mindanao faunal region possesses distinct subcenters of amphibian and reptile species diversity, and that until this area is revisited and its fauna and actually studied, with on-the-ground field work including targeted surveys of species distributions coupled to the study their natural history, our understanding of the diversity and conservation status of southern Philippine herpetological fauna will remain incomplete. Nevertheless, the northeast Mindanao geographical area (Caraga Region) appears to have the highest herpetological species diversity (at least 126 species) of any comparably-sized Philippine faunal subregion.

Enhanced biodiversity beyond marine reserve boundaries: the cup spillith over.

Overfishing can have detrimental effects on marine biodiversity and the structure of marine ecosystems. No-take marine reserves (NTMRs) are much advocated as a means of protecting biodiversity and ecosystem structure from overharvest. In contrast to terrestrial protected areas, NTMRs are not only expected to conserve or recover biodiversity and ecosystems within their boundaries, but also to enhance biodiversity beyond their boundaries by exporting species richness and more complex biological communities. Here we show that species richness of large predatory reef fish increased fourfold and 11-fold inside two Philippine no-take marine reserves over 14 and 25 years, respectively. Outside one reserve (Apo) the species richness also increased. This increase beyond the Apo reserve boundary was 78% higher closer to the boundary (200-250 m) than farther from it (250-500 m). The increase in richness beyond the boundary could not be explained by improvements over time in habitat or prey availability. Furthermore, community composition of predatory fish outside but close to (200-250 m) the Apo reserve became very similar to that inside the reserve over time, almost converging with it in multivariate space after 26 years of reserve protection. This is consistent with the suggestion that, as community composition inside Apo reserve increased in complexity, this complexity spilled over the boundary into nearby fished areas. Clearly, the spillover of species richness and community complexity is a direct consequence of the spillover of abundance of multiple species. However, this spillover of species richness and community complexity demonstrates an important benefit of biodiversity and ecosystem export from reserves, and it provides hope that reserves can help to reverse the decline of marine ecosystems and biodiversity.

Phylogeny of Philippine slender skinks (Scincidae: Brachymeles) reveals underestimated species diversity, complex biogeographical relationships, and cryptic patterns of lineage diversification.

The spectacular, virtually endemic radiation of Philippine semi-fossorial skinks of the genus Brachymeles represent one of the few radiations of scincid lizards to possess both fully limbed and limbless species. And yet, nothing is known of the phylogenetic relationships of this exceptional group. Morphologically similar body plans have made it difficult to assess species-level diversity, and the genus has long been recognized as one of the more modest radiations of southeast Asian lizards. However, recent large-scale survey efforts have resulted in the discovery of numerous new species, and taxonomic studies indicate that the diversity within the genus Brachymeles is grossly underestimated. In this study we provide the first robust estimate of phylogenetic relationships within the genus Brachymeles using a multi-locus dataset and nearly complete taxonomic sampling. We provide statistical tests of monophyly for all polytypic species and two widespread limb-reduced species and our results indicate wholesale deviations from past summaries and taxonomic evaluations of the genus. With few exceptions, we are able to reject the monophyly of all polytypic and widespread species, thereby validating the need for large-scale taxonomic revisions. Our results reveal that the limbless, monotypic, genus Davewakeum is nested within Brachymeles. Mapping of body form on our preferred phylogenetic tree suggests that limb-reduction and digit loss has occurred on multiple occasions in the history of the genus. A Bayesian reconstruction of ancestral areas indicates strong statistical support for a minimum of five major dispersal events that have given rise to a major component of the observed species diversity on separate Pleistocene aggregate island platforms of the archipelago.

Decadal-scale rebuilding of predator biomass in Philippine marine reserves.

No-take marine reserves (NTMRs) provide hope that local carrying capacity may be partially restored if reserves are protected long enough. How long is long enough? We assess the duration of protection required for populations of large predatory reef fish in marine reserves to attain new steady states. We monitored biomass of large predatory fish in two marine reserves at Sumilon and Apo Islands, Philippines, almost annually for 26 years (1983-2009), and fit a logistic model to the data. As duration of reserve protection increased, biomass of predatory fish approached an asymptote, although the models suggest that 20-40 years of protection is required to attain new steady states. Thus, for local carrying capacity to be rebuilt, no-take protection must be effective on decadal timescales.

Effectiveness of marine protected areas in the Philippines for biodiversity conservation.

Quantifying the extent to which existing reserves meet conservation objectives and identifying gaps in coverage are vital to developing systematic protected-area networks. Despite widespread recognition of the Philippines as a global priority for marine conservation, limited work has been undertaken to evaluate the conservation effectiveness of existing marine protected areas (MPAs). Targets for MPA coverage in the Philippines have been specified in the 1998 Fisheries Code legislation, which calls for 15% of coastal municipal waters (within 15 km of the coastline) to be protected within no-take MPAs, and the Philippine Marine Sanctuary Strategy (2004), which aims to protect 10% of coral reef area in no-take MPAs by 2020. We used a newly compiled database of nearly 1000 MPAs to measure progress toward these targets. We evaluated conservation effectiveness of MPAs in two ways. First, we determined the degree to which marine bioregions and conservation priority areas are represented within existing MPAs. Second, we assessed the size and spacing patterns of reserves in terms of best-practice recommendations. We found that the current extent and distribution of MPAs does not adequately represent biodiversity. At present just 0.5% of municipal waters and 2.7-3.4% of coral reef area in the Philippines are protected in no-take MPAs. Moreover, 85% of no-take area is in just two sites; 90% of MPAs are <1 km(2). Nevertheless, distances between existing MPAs should ensure larval connectivity between them, providing opportunities to develop regional-scale MPA networks. Despite the considerable success of community-based approaches to MPA implementation in the Philippines, this strategy will not be sufficient to meet conservation targets, even under a best-case scenario for future MPA establishment. We recommend that implementation of community-based MPAs be supplemented by designation of additional large no-take areas specifically located to address conservation targets.

No-take marine reserves and reef fisheries management in the Philippines: a new people power revolution.

The marine-conservation and reef fisheries-management program that exists today in the Philippines had humble beginnings in the 1970s at Sumilon and Apo islands. These islands have produced some of the best evidence available that no-take reserves, protected and managed by local communities, can play a key role in biodiversity conservation and fisheries management. Perhaps more importantly, they served as models for an extraordinary expansion of no-take reserves nationally in the Philippines in the past 2 decades. This expansion contributed substantially to a major shift in national policy of management of marine resources. This policy shift partially devolved responsibility from a centralized government bureaucracy to local governments and local communities. Local governments now comanage, along with the national government, marine resources out to 15 km from the coast. Giving some responsibility for management of marine resources to coastal people dependent upon those resources represents, in a very real sense, another "people power revolution" in the Philippines.

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.