Mikel A. Becerro

Global conservation outcomes depend on marine protected areas with five key features

In line with global targets agreed under the Convention on Biological Diversity, the number of marine protected areas (MPAs) is increasing rapidly, yet socio-economic benefits generated by MPAs remain difficult to predict and under debate. MPAs often fail to reach their full potential as a consequence of factors such as illegal harvesting, regulations that legally allow detrimental harvesting, or emigration of animals outside boundaries because of continuous habitat or inadequate size of reserve. Here we show that the conservation benefits of 87 MPAs investigated worldwide increase exponentially with the accumulation of five key features: no take, well enforced, old (>10 years), large (>100 km2), and isolated by deep water or sand. Using effective MPAs with four or five key features as an unfished standard, comparisons of underwater survey data from effective MPAs with predictions based on survey data from fished coasts indicate that total fish biomass has declined about two-thirds from historical baselines as a result of fishing. Effective MPAs also had twice as many large (>250 mm total length) fish species per transect, five times more large fish biomass, and fourteen times more shark biomass than fished areas. Most (59%) of the MPAs studied had only one or two key features and were not ecologically distinguishable from fished sites. Our results show that global conservation targets based on area alone will not optimize protection of marine biodiversity. More emphasis is needed on better MPA design, durable management and compliance to ensure that MPAs achieve their desired conservation value.

Integrating abundance and functional traits reveals new global hotspots of fish diversity

Species richness has dominated our view of global biodiversity patterns for centuries. The dominance of this paradigm is reflected in the focus by ecologists and conservation managers on richness and associated occurrence-based measures for understanding drivers of broad-scale diversity patterns and as a biological basis for management. However, this is changing rapidly, as it is now recognized that not only the number of species but the species present, their phenotypes and the number of individuals of each species are critical in determining the nature and strength of the relationships between species diversity and a range of ecological functions (such as biomass production and nutrient cycling). Integrating these measures should provide a more relevant representation of global biodiversity patterns in terms of ecological functions than that provided by simple species counts. Here we provide comparisons of a traditional global biodiversity distribution measure based on richness with metrics that incorporate species abundances and functional traits. We use data from standardized quantitative surveys of 2,473 marine reef fish species at 1,844 sites, spanning 133 degrees of latitude from all ocean basins, to identify new diversity hotspots in some temperate regions and the tropical eastern Pacific Ocean. These relate to high diversity of functional traits amongst individuals in the community (calculated using Rao’s Q), and differ from previously reported patterns in functional diversity and richness for terrestrial animals, which emphasize species-rich tropical regions only. There is a global trend for greater evenness in the number of individuals of each species, across the reef fish species observed at sites (‘community evenness’), at higher latitudes. This contributes to the distribution of functional diversity hotspots and contrasts with well-known latitudinal gradients in richness. Our findings suggest that the contribution of species diversity to a range of ecosystem functions varies over large scales, and imply that in tropical regions, which have higher numbers of species, each species contributes proportionally less to community-level ecological processes on average than species in temperate regions. Metrics of ecological function usefully complement metrics of species diversity in conservation management, including when identifying planning priorities and when tracking changes to biodiversity values.

Genetic diversity and population structure of the commercially harvested sea urchin Paracentrotus lividus (Echinodermata, Echinoidea)

The population structure of the edible Atlanto‐Mediterranean sea urchin Paracentrotus lividus is described by analysing sequence variation in a fragment of the mitochondrial gene cytochrome c oxidase subunit I in 127 individuals from 12 localities across south‐west Europe. The study revealed high levels of genetic diversity but low levels of genetic structure, suggesting a large degree of gene flow between populations and panmixis within each, the Mediterranean and Atlantic basins. However, we found significant genetic differentiation between the two basins probably due to restricted gene flow across the geographical boundary imposed by the area of the Strait of Gibraltar. Populations of P. lividus appeared to have experienced a recent demographic expansion in the late Pleistocene. We provide new evidence on the population structure of this commercial species, predicting a healthy stock of this sea urchin on the Mediterranean and Atlantic coasts.

ALLELOPATHIC INTERACTIONS BETWEEN SPONGES ON A TROPICAL REEF

Competition for space among organisms on tropical reefs has often been hypothesized to be mediated by allelopathic interactions, but the secondary metabolites involved in these interactions have rarely been identified. On Guam, the sponge Dysidea sp. overgrows the sponge Cacospongia sp. and causes necrosis. Using field assays, we tested the effects of crude organic extracts and a major sesquiterpene isolated from Dysidea, 7-deacetoxyolepupuane, on Cacospongia and on the production of the major terpenoid metabolites scalaradial and desacetylscalaradial by Cacospongia. We also tested whether the amounts of organic compounds produced by Dysidea differed in the presence or absence of Cacospongia. To determine whether 7-deacetoxyolepupuane had another ecological function, we tested the compound as a predator deterrent. In field experiments, crude extracts of Dysidea and pure 7-deacetoxyolepupuane both caused necrosis in Cacospongia when they were incorporated into agar strips and placed in contact with Cacospongia for 7 d. Organic extract, scalaradial, and desacetylscalaradial concentrations in Cacospongia were not affected by the overgrowth of Dysidea. However, a greater quantity of organic extract (but not scalaradial or desacetylscalaradial) was found in portions of Cacospongia covered by agar strips containing Dysidea organic extracts than in portions of Cacospongia covered by control agar strips. The production of 7-deacetoxyolepupuane by Dysidea occurring on rock substrates and on Cacospongia did not differ; thus, the production of this compound is not induced by the presence of competitors. In addition to its role in competition, 7-deacetoxyolepupuane deterred predation by a spongivorous fish, illustrating the multiple ecological roles that a single secondary metabolite may play.

Antimicrobial activity and surface bacterial film in marine sponges

The antimicrobial activity of three sponge species was tested against marine benthic bacteria and the presence of epibiotic bacteria on their surfaces was investigated. The aim of the present study was to determine whether there is a correlation between antimicrobial activities and the presence of a bacterial film. Seven benthic bacterial strains were isolated from the vicinity of the sponges and used as assay organisms. Gram-positive and Gram-negative bacteria were equally affected by all the sponge extracts. The encrusting sponge Crambe crambe featured the strongest antimicrobial activity in the assays and no bacteria were found on its surface. The other two sponges, Ircinia fasciculata and Spongia officinalis, featured lower antimicrobial activity than C. crambe and the number of bacteria found on their surfaces was of the same order of magnitude as that found on immersed glass slides used as controls. It was concluded that antimicrobial activities detected in laboratory assays were effective as mechanisms to combat microfouling in only some cases, and other possible interpretations are considered.

MULTIPLE FUNCTIONS FOR SECONDARY METABOLITES IN ENCRUSTING MARINE INVERTEBRATES

We used three chemical fractions (spanning a wide range of polarities) from the extracts of four marine invertebrates, the spongesCrambe crambe andHemimycale columella and the ascidiansCystodytes dellechiajei andPolysyncraton lacazei, to test inhibition of cell division, photosynthesis, and settlement. We used assay organisms from the same habitat, seeking to determine whether a species may display diverse, ecologically relevant bioac-tivities and, if so, whether the same types of compound may be responsible for such activities. Cell division was strongly inhibited by the spongeC. crambe. A dichloromethane fraction fromC. crambe prevented development of sea urchinParacentrotus lividus eggs at a concentration of 10 μg/ml, as did the butanolic fraction, but at higher concentrations (50 and 100 μg/ml). At 50 μg/ml, the aqueous fraction ofC. crambe allowed cell division but prevented eggs from developing beyond the gastrula stage. Similar results were recorded with the dichloromethane fraction ofP. lacazei and from the aqueous fraction ofH. columella. Photosynthesis was unaffected by any of the species at 50 μg/ml. Larval settlement was inhibited by one or another fraction from the four species surveyed at a concentration of 50 μg/ml, althoughC. crambe exhibited the greatest amount of activity. We therefore found that various fractions displayed the same type of bioactivity, while compounds from the same fraction were responsible for multiple activities, suggesting that secondary metabolites are multiple-purpose tools in nature, which is relevant to our understanding of species ecology and evolution. Moreover, results showed that the assessment of the role of chemical compounds is significantly influenced by the assay organism, fractionation procedure, concentration, and duration of experiments. All these factors should be carefully considered when testing ecological hypotheses of the roles of chemically-mediated bioactivities.

Distribution of brominated compounds within the sponge Aplysina aerophoba: coupling of X-ray microanalysis with cryofixation techniques.

Abstract. The major secondary metabolites of the sponge Aplysina aerophoba are brominated compounds. X-ray energy dispersive microanalysis was therefore used to locate secondary metabolites via the Br signal in energy emission spectra from sponge sections. To test the reliability of this method in the face of the loss or redistribution of metabolites during processing, we compared the results obtained by conventional aldehyde fixation with those obtained by cryofixation and cryosubstitution with and without cryoembedding. Bromine appeared to be concentrated in two sponge structures, viz. fibres and spherulous cells, when cryofixed material was examined. However, X-ray microanalysis failed to demonstrate the presence of bromine in spherulous cells in chemically fixed samples, showing the need for cryotechniques to avoid the loss of compounds. Cryofixation plus cryosubstitution methods performed best regarding structural preservation and the immobilization of metabolites. The presence of bromine in the spherulous cells suggests that this cell type is the producer of the secondary metabolites, as described for other sponge species. Nevertheless, the presence of bromine in sponge fibres indicates that they can accumulate metabolic substances, although we have been unable to assess whether the chemicals are in their original form or in a modified state within the fibres. A. aerophoba has both bacterial and cyanobacterial symbionts in its mesohyl; the absence of brominated compounds in them contrasts with previous findings in other sponges with prokaryote symbionts.

Silica deposition in Demosponges: spiculogenesis in Crambe crambe.

Abstract. Transmission electron-microscopy images coupled with dispersive X-ray analysis of the species Crambe crambe have provided information on the process of silica deposition in Demosponges. Sclerocytes (megasclerocytes) lie close to spicules or surround them at different stages of growth by means of long thin enveloping pseudopodia. Axial filaments occur free in the mesohyl, in close contact with sclerocytes, and are triangular in cross section, with an internal silicified core. The unit-type membrane surrounding the growing spicule coalesces with the plasmalemma. The axial filament of a growing spicule and that of a mature spicule contain 50%–70% Si and 30%–40% Si relative to that contained in the spicule wall, respectively. The extracellular space between the sclerocyte and the growing spicule contains 50%–65%. Mitochondria, vesicles and dense inclusions of sclerocytes exhibit less than 10%. The cytoplasm close to the growing spicule and that far from the growing spicule contain up to 50% and less than 10%, respectively. No Si has been detected in other parts of the sponge. The megascleres are formed extracellularly. Once the axial filament is extruded to the mesohyl, silicification is accomplished in an extracellular space formed by the enveloping pseudopodia of the sclerocyte. Si deposition starts at regularly distributed sites along the axial filament; this may be related to the highly hydroxylated zones of the silicatein-α protein. Si is concentrated in the cytoplasm of the sclerocyte close to the plasmalemma that surrounds the growing spicules. Orthosilicic acid seems to be pumped, both from the mesohyl to the sclerocyte and from the sclerocyte to the extra-cellular pocket containing the growing spicule, via the plasmalemma.

Finding the relevant scale: clonality and genetic structure in a marine invertebrate (Crambe crambe, Porifera)

Important changes in genetic relatedness may occur at extremely small scales in benthic invertebrates, providing key information about structuring processes in populations of these organisms. We performed a small‐scale study of the population structure of the sponge Crambe crambe, in which 177 individuals from the same rocky wall (interindividual distances from 0 to 7 m) were genotyped using six microsatellite markers. 101 sponges had unique genotypes and the remaining 76 individuals formed 24 groups of sponges sharing genotypes (clones). Mean intraclone distances were found to be c. 20 cm. Spatial autocorrelation analyses showed a drastic decrease in genetic relatedness over the first 100 cm of distance. If the contribution of clonality to this pattern was eliminated, the trend was attenuated, but remained a marked one and was still significant within the first distance classes (30–40 cm). Estimated mean dispersal distances per generation were c. 35 cm, and neighbourhood sizes were estimated at c. 33 sponges. Genetic similarities with sponges of the same locality, or from other Mediterranean localities, were within the same range as those found in sponges 2–7 m apart. It is concluded that asexual reproduction plays an important role in structuring populations in this species. However, over and above the effects of clonality, a strong fine‐scale genetic structure was present at distances in the range of tens of centimetres, probably as a result of short dispersal of larvae. This fine‐scale genetic structure may be common in invertebrates with lecitotrophic larvae.

Chemically-mediated interactions in benthic organisms: the chemical ecology of Crambe crambe (Porifera, Poecilosclerida)

We studied the chemically-mediated interactions of the encrusting sponge Crambe crambe, one of the most toxic and widespread species in rocky sublittoral habitats in the Northwestern Mediterranean. Guanidine alkaloids accounted for C. crambe’s toxicity, which seems to have multiple functions in nature, as evidence has been found for antifouling, antipredation, and space competition roles.