Phylogeography and Limited Genetic Connectivity in the Endangered Boring Giant Clam across the Coral Triangle

Abstract: The Coral Triangle is the global center of marine biodiversity; however, its coral reefs are critically threatened. Because of the bipartite life history of many marine species with sedentary adults and dispersive pelagic larvae, designing effective marine protected areas requires an understanding of patterns of larval dispersal and connectivity among geographically discrete populations. We used mtDNA sequence data to examine patterns of genetic connectivity in the boring giant clam (Tridacna crocea) in an effort to guide conservation efforts within the Coral Triangle. We collected an approximately 485 base pair fragment of mtDNA cytochrome c oxidase 1 (CO1) from 414 individuals at 26 sites across Indonesia. Genetic structure was strong between regions (φ_ST=0.549, p < 0.00001) with 3 strongly supported clades: one restricted to western Sumatra, another distributed across central Indonesia, and a third limited to eastern Indonesia and Papua. Even within the single largest clade, small but significant genetic structure was documented (φ_ST=0.069, p < 0.00001), which indicates limited gene flow within and among phylogeographic regions. Significant patterns of isolation by distance indicated an average dispersal distance of only 25–50 km, which is far below dispersal predictions of 406–708 km derived from estimates of passive dispersal over 10 days via surface currents. The strong regional genetic structure we found indicates potent limits to genetic and demographic connectivity for this species throughout the Coral Triangle and provides a regional context for conservation planning. The recovery of 3 distinct evolutionarily significant units within a well‐studied taxonomic group suggests that biodiversity in this region may be significantly underestimated and that Tridacna taxa may be more endangered than currently recognized.     

Effect of Macroalgal Expansion and Marine Protected Areas on Coral Recovery Following a Climatic Disturbance

Disturbance plays an important role in structuring marine ecosystems, and there is a need to understand how conservation practices, such as the designation of Marine Protected Areas (MPAs), facilitate postdisturbance recovery. We evaluated the association of MPAs, herbivorous fish biomass, substrate type, postdisturbance coral cover, and change in macroalgal cover with coral recovery on the fringing reefs of the inner Seychelle islands, where coral mortality after a 1998 bleaching event was extensive. We visually estimated benthic cover and fish biomass at 9 sites in MPAs where fishing is banned and at 12 sites where fishing is permitted in 1994, 2005, 2008, and 2011. We used analysis of variance to examine spatial and temporal variations in coral cover and generalized additive models to identify relations between coral recovery and the aforementioned factors that may promote recovery. Coral recovery occurred on all substrate types, but it was highly variable among sites and times. Between 2005 and 2011 the increase in coral cover averaged 1%/year across 21 sites, and the maximum increase was 4%/year. However, mean coral cover across the study area (14%) remained at half of 1994 levels (28%). Sites within MPAs had faster rates of coral recovery than sites in fished areas only where cover of macroalgae was low and had not increased over time. In MPAs where macroalgae cover expanded since 1998 there was no recovery. Where coral was recovering on granite reefs there was a shift in relative prevalence of colony life‐form from branching to encrusting species. This simplification of reef structure may affect associated reef fauna even if predisturbance levels of coral cover are attained. Efecto de la Expansión de Macroalgas y Áreas Marinas Protegidas sobre la Recuperación de Coral Después de una Perturbación Climática     

Wood Density as a Conservation Tool: Quantification of Disturbance and Identification of Conservation‐Priority Areas in Tropical Forests

Abstract: Inventories of tree species are often conducted to guide conservation efforts in tropical forests. Such surveys are time consuming, demanding of expertise, and expensive to perform and interpret. Approaches to make survey efforts simpler or more effective would be valuable. In particular, it would be good to be able to easily identify areas of old‐growth forest. The average density of the wood of a tree species is closely linked to its successional status. We used tree inventory data from eastern Borneo to determine whether wood density can be used to quantify forest disturbance and conservation importance. The average density of wood in a plot was significantly and negatively related to disturbance levels, with plots with higher wood densities occurring almost exclusively in old‐growth forests. Average wood density was unimodally related to the diversity of tree species, indicating that the average wood density in a plot might be a better indicator of old‐growth forest than species diversity. In addition, Borneo endemics had significantly heavier wood than species that are common throughout the Malesian region, and they were more common in plots with higher average wood density. We concluded that wood density at the plot level could be a powerful tool for identifying areas of conservation priority in the tropical rain forests of Southeast Asia.     

Combined Effects of Levels of Protection and Environmental Variables at Different Spatial Resolutions on Fish Assemblages in a Marine Protected Area

Abstract: The links between species–environment relations and species’ responses to protection are unclear, but the objectives of marine protected areas (MPAs) are most likely to be achieved when those relations are known and inform MPA design. The components of a species’ habitat vary with the spatial resolution of the area considered. We characterized areas at two resolutions: 250 m² (transect) and approximately 30,000 m² (seascape). We considered three categories of environmental variables: substrate type, bottom complexity, and depth. We sought to determine at which resolution habitat characteristics were a better predictor of abundance and species composition of fishes and whether the relations with environmental variables at either resolution affected species’ responses to protection. Habitat features accounted for a larger proportion of spatial variation in species composition and abundances than differences in protection status. This spatial variation was explained best by habitat characteristics at the seascape level than at the transect level. Species’ responses to protected areas were specific to particular seascape characteristics, primarily depth, and bottom complexity. Our method may be useful for prioritizing marine areas for protection, designing MPAs, and monitoring their effectiveness. It identified areas that provided natural shelter, areas acting as buffer zones, and areas where fish species were most responsive to protection. The identification of such areas is necessary for cost‐effective establishment and monitoring of MPAs.     

Effect of Rotational Shepherding on Demographic and Genetic Connectivity of Calcareous Grassland Plants

Response to habitat fragmentation may not be generalized among species, in particular for plant communities with a variety of dispersal traits. Calcareous grasslands are one of the most species‐rich habitats in Central Europe, but abandonment of traditional management has caused a dramatic decline of calcareous grassland species. In the Southern Franconian Alb in Germany, reintroduction of rotational shepherding in previously abandoned grasslands has restored species diversity, and it has been suggested that sheep support seed dispersal among grasslands. We tested the effect of rotational shepherding on demographic and genetic connectivity of calcareous grassland specialist plants and whether the response of plant populations to shepherding was limited to species dispersed by animals (zoochory). Specifically, we tested competing dispersal models and source and focal patch properties to explain landscape connectivity with patch‐occupancy data of 31 species. We fitted the same connectivity models to patch occupancy and nuclear microsatellite data for the herb Dianthus carthusianorum (Carthusian pink). For 27 species, patch connectivity was explained by dispersal by rotational shepherding regardless of adaptations to zoochory, whereas population size (16% species) and patch area (0% species) of source patches were not important predictors of patch occupancy in most species. [Correction made after online publication, February 25, 2014: Population size and patch area percentages were mistakenly inverted, and have now been fixed.] Microsite diversity of focal patches significantly increased the model variance explained by patch occupancy in 90% of the species. For D. carthusianorum, patch connectivity through rotational shepherding explained both patch occupancy and population genetic diversity. Our results suggest shepherding provides dispersal for multiple plant species regardless of their dispersal adaptations and thus offers a useful approach to restore plant diversity in fragmented calcareous grasslands. Efectos del Pastoreo Rotacional sobre la Conectividad Genética y Demográfica de Plantas de Pastizales Calcáreos     

Current Status of Marine Protected Areas in Latin America and the Caribbean

Abstract: Marine protected areas (MPAs), including no‐take marine reserves (MRs), play an important role in the conservation of marine biodiversity. We document the status of MPAs and MRs in Latin America and the Caribbean, where little has been reported on the scope of such protection. Our survey of protected area databases, published and unpublished literature, and Internet searches yielded information from 30 countries and 12 overseas territories. At present more than 700 MPAs have been established, covering more than 300,000 km² or 1.5% of the coastal and shelf waters. We report on the status of 3 categories of protection: MPAs (limited take throughout the area), MRs (no‐take throughout the area), and mixed‐use (a limited‐take MPA that contains an MR). The majority of protected areas in Latin America and the Caribbean are MPAs, which allow some or extensive extractive activities throughout the designated area. These 571 sites cover 51,505 km² or 0.3% of coastal and shelf waters. There are 98 MRs covering 16,862 km² or 0.1% of the coastal and shelf waters. Mixed‐use MPAs are the fewest in number (87), but cover the largest area (236,853 km², 1.2%). Across Latin America and the Caribbean, many biogeographic provinces are underrepresented in these protected areas. Large coastal regions remain unprotected, in particular, the southern Pacific and southern Atlantic coasts of South America. Our analysis reveals multiple opportunities to strengthen marine conservation in Latin America and the Caribbean by improving implementation, management, and enforcement of existing MPAs; adding new MPAs and MRs strategically to enhance connectivity and sustainability of existing protection; and establishing new networks of MPAs and MRs or combinations thereof to enhance protection where little currently exists.     

Use of Population Viability Analysis to Evaluate CITES Trade‐Management Options for Threatened Marine Fishes

Abstract: Achieving multiple conservation objectives can be challenging, particularly under high uncertainty. Having agreed to limit seahorse (Hippocampus) exports to sustainable levels, signatories to the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) were offered the option of a single 10‐cm minimum size limit (MSL) as an interim management measure for all Hippocampus species (≥34). Although diverse stakeholders supported the recommended MSL, its biological and socioeconomic implications were not assessed quantitatively. We combined population viability analysis, model sensitivity analysis, and economic information to evaluate the trade‐off between conservation threat to and long‐term cumulative income from these exploited marine fishes of high conservation concern. We used the European long‐snouted seahorse (Hippocampus guttulatus) as a representative species to compare the performance of MSLs set at alternative biological reference points. Our sensitivity analyses showed that in most of our scenarios, setting the MSL just above size at maturity (9.7 cm in H. guttulatus) would not prevent exploited populations from becoming listed as vulnerable. By contrast, the relative risk of decline and extinction were almost halved—at a cost of only a 5.6% reduction in long‐term catches—by increasing the MSL to the size reached after at least one full reproductive season. On the basis of our analysis, a precautionary increase in the MSL could be compatible with sustaining fishers' livelihoods and international trade. Such management tactics that aid species conservation and have minimal effects on long term catch trends may help bolster the case for CITES trade management of other valuable marine fishes.     

Incorporation of Spatial and Economic Analyses of Human‐Use Data in the Design of Marine Protected Areas

Abstract: Social, economic, and ecological criteria contribute to the successful design, implementation, and management of marine protected areas (MPAs). In the context of California's Marine Life Protection Act Initiative, we developed a set of methods for collecting, compiling, and analyzing data about the spatial extent and relative economic importance of commercial and recreational fishing. We interviewed 174 commercial fishers who represented the major fisheries in the initiative's north‐central coast region, which extends from Point Arena south to Pigeon Point. These fishers provided data that we used to map the extent of each of the fishing grounds, to weight the relative importance of areas within the grounds, to characterize the operating costs of each fishery, and to analyze the potential economic losses associated with proposed marine protected areas. A regional stakeholder group used the maps and impact analyses in conjunction with other data sets to iteratively identify economic and ecological trade‐offs in designations of different areas as MPAs at regional, port, and fishery extents. Their final proposed MPA network designated 20% of state waters as MPAs. Potential net economic loss ranged from 1.7% to 14.2% in the first round of network design and totaled 6.3% in the final round of design. This process is a case study in the application of spatial analysis to validate and integrate local stakeholder knowledge in marine planning.     

Phenological mismatch and the effectiveness of assisted gene flow

The persistence of narrowly adapted species under climate change will depend on their ability to migrate apace with their historical climatic envelope or to adapt in place to maintain fitness. This second path to persistence can only occur if there is sufficient genetic variance for response to new selection regimes. Inadequate levels of genetic variation can be remedied through assisted gene flow (AGF), that is the intentional introduction of individuals genetically adapted to localities with historic climates similar to the current or future climate experienced by the resident population. However, the timing of reproduction is frequently adapted to local conditions. Phenological mismatch between residents and migrants can reduce resident × migrant mating frequencies, slowing the introgression of migrant alleles into the resident genetic background and impeding evolutionary rescue efforts. Focusing on plants, we devised a method to estimate the frequency of resident × migrant matings based on flowering schedules and applied it in an experiment that mimicked the first generation of an AGF program with Chamaecrista fasciculata, a prairie annual, under current and expected future temperature regimes. Phenological mismatch reduced the potential for resident × migrant matings by 40–90%, regardless of thermal treatment. The most successful migrant sires were the most resident like in their flowering time, further biasing the genetic admixture between resident and migrant populations. Other loci contributing to local adaptation—heat‐tolerance genes, for instance—may be in linkage disequilibrium with phenology when residents and migrants are combined into a single mating pool. Thus, introgression of potentially adaptive migrant alleles into the resident genetic background is slowed when selection acts against migrant phenology. Successful AGF programs may require sustained high immigration rates or preliminary breeding programs when phenologically matched migrant source populations are unavailable.     

Effects of Management of Domestic Dogs and Recreation on Carnivores in Protected Areas in Northern California

Abstract: In developed countries dogs (Canis lupus familiaris) are permitted to accompany human visitors to many protected areas (e.g., >96% of protected lands in California, U.S.A.), and protected‐area management often focuses on regulating dogs due to concerns about predation, competition, or transmission of disease and conflicts with human visitors. In 2004 and 2005, we investigated whether carnivore species richness and abundance were associated with management of domestic dogs and recreational visitation in protected areas in northern California. We surveyed for mammalian carnivores and human visitors in 21 recreation areas in which dogs were allowed offleash or onleash or were excluded, and we compared our observations in the recreation areas with observations in seven reference sites that were not open to the public. Carnivore abundance and species richness did not differ among the three types of recreation areas, but native carnivore species richness was 1.7 times greater (p < 0.01) and the relative abundances of native coyotes (Canis latrans) and bobcats (Lynx rufus) were over four times greater (p < 0.01) in the reference sites. Abundances of bobcats and all carnivores declined as the number of visitors increased. The policy on domestic dogs did not appear to affect species richness and abundance of mammalian carnivores. But the number of dogs we observed was strongly associated with human visitation (R²= 0.54), so the key factors associated with recreational effects on carnivores appear to be the presence and number of human visitors to protected areas.     

Toward a Management Framework for Networks of Protected Areas in the Face of Climate Change

Abstract: Networks of sites of high importance for conservation of biological diversity are a cornerstone of current conservation strategies but are fixed in space and time. As climate change progresses, substantial shifts in species’ ranges may transform the ecological community that can be supported at a given site. Thus, some species in an existing network may not be protected in the future or may be protected only if they can move to sites that in future provide suitable conditions. We developed an approach to determine appropriate climate‐change adaptation strategies for individual sites within a network that was based on projections of future changes in the relative proportions of emigrants (species for which a site becomes climatically unsuitable), colonists (species for which a site becomes climatically suitable), and persistent species (species able to remain within a site despite the climatic change). Our approach also identifies key regions where additions to a network could enhance its future effectiveness. Using the sub‐Saharan African Important Bird Area (IBA) network as a case study, we found that appropriate conservation strategies for individual sites varied widely across sub‐Saharan Africa, and key regions where new sites could help increase network robustness varied in space and time. Although these results highlight the potential difficulties within any planning framework that seeks to address climate‐change adaptation needs, they demonstrate that such planning frameworks are necessary, if current conservation strategies are to be adapted effectively, and feasible, if applied judiciously.     

Comparison of Modern and Historical Fish Catches (AD 750–1400) to Inform Goals for Marine Protected Areas and Sustainable Fisheries

Abstract: We tested the unsustainable fishing hypothesis that species in assemblages of fish differ in relative abundance as a function of their size, growth rates, vagility, trophic level, and diet by comparing species composition in historical bone middens, modern fisheries, and areas closed to fishing. Historical data came from one of the earliest and most enduring Swahili coastal settlements (approximately AD 750–1400). Modern data came from fisheries near the archeological site and intensively harvested fishing grounds in southern Kenya. The areas we sampled that were closed to fishing (closures) were small (<28 km²) and permanent. The midden data indicated changes in the fish assemblage that are consistent with a weak expansion of fishing intensity and the unsustainable fishing hypothesis. Fishes represented in the early midden assemblages from AD 750 to 950 had longer life spans, older age at maturity, and longer generation times than fish assemblages after AD 950, when the abundance of species with longer maximum body lengths increased. Changes in fish life histories during the historical period were, however, one‐third smaller than differences between the historical and modern assemblages. Fishes in the modern assemblage had smaller mean body sizes, higher growth and mortality rates, a higher proportion of microinvertivores, omnivores, and herbivores, and higher rates of food consumption, whereas the historical assemblage had a greater proportion of piscivores and macroinvertivores. Differences in fish life histories between modern closures and modern fishing grounds were also small, but the life histories of fishes in modern closures were more similar to those in the midden before AD 950 because they had longer life spans, older age at maturity, and a higher proportion of piscivores and macroinvertivores than the modern fisheries. Modern closures and historical fish assemblages were considerably different, although both contained species with longer life spans.     

Quantitative Determination of Rarity of Freshwater Fishes and Implications for Imperiled‐Species Designations

Abstract: Conserving rare species and protecting biodiversity and ecosystem functioning depends on sound information on the nature of rarity. Rarity is multidimensional and has a variety of definitions, which presents the need for a quantitative classification scheme with which to categorize species as rare or common. We constructed such a classification for North American freshwater fishes to better describe rarity in fishes and provide researchers and managers with a tool to streamline conservation efforts. We used data on range extents, habitat specificities, and local population sizes of North American freshwater fishes and a variety of quantitative methods and statistical decision criteria, including quantile regression and a cost‐function algorithm to determine thresholds for categorizing a species as rare or common. Species fell into eight groups that conform to an established framework for rarity. Fishes listed by the American Fisheries Society (AFS) as endangered, threatened, or vulnerable were most often rare because their local population sizes were low, ranges were small, and they had specific habitat needs, in that order, whereas unlisted species were most often considered common on the basis of these three factors. Species with large ranges generally had few specific habitat needs, whereas those with small ranges tended to have narrow habitat specificities. We identified 30 species not designated as imperiled by AFS that were rare along all dimensions of rarity and may warrant further study or protection, and we found three designated species that were common along all dimensions and may require a review of their imperilment status. Our approach could be applied to other taxa to aid conservation decisions and serve as a useful tool for future revisions of listings of fish species.     

Birds as Suppliers of Seed Dispersal in Temperate Ecosystems: Conservation Guidelines from Real‐World Landscapes

Abstract: Seed dispersal by animals is considered a pivotal ecosystem function that drives plant‐community dynamics in natural habitats and vegetation recovery in human‐altered landscapes. Nevertheless, there is a lack of suitable ecological knowledge to develop basic conservation and management guidelines for this ecosystem service. Essential questions, such as how well the abundance of frugivorous animals predicts seeding function in different ecosystems and how anthropogenic landscape heterogeneity conditions the role of dispersers, remain poorly answered. In three temperate ecosystems, we studied seed dispersal by frugivorous birds in landscape mosaics shaped by human disturbance. By applying a standardized design across systems, we related the frequency of occurrence of bird‐dispersed seeds throughout the landscape to the abundance of birds, the habitat features, and the abundance of fleshy fruits. Abundance of frugivorous birds in itself predicted the occurrence of dispersed seeds throughout the landscape in all ecosystems studied. Even those landscape patches impoverished due to anthropogenic disturbance received some dispersed seeds when visited intensively by birds. Nonetheless, human‐caused landscape degradation largely affected seed‐deposition patterns by decreasing cover of woody vegetation or availability of fruit resources that attracted birds and promoted seed dispersal. The relative role of woody cover and fruit availability in seed dispersal by birds differed among ecosystems. Our results suggest that to manage seed dispersal for temperate ecosystem preservation or restoration one should consider abundance of frugivorous birds as a surrogate of landscape‐scale seed dispersal and an indicator of patch quality for the dispersal function; woody cover and fruit resource availability as key landscape features that drive seedfall patterns; and birds as mobile links that connect landscape patches of different degrees of degradation and habitat quality via seed deposition.