Paul V. R. Snelgrove

The function of marine critical transition zones and the importance of sediment biodiversity

Estuaries and coastal wetlands are critical transition zones (CTZs) that link land, freshwater habitats, and the sea. CTZs provide essential ecological functions, including decomposition, nutrient cycling, and nutrient production, as well as regulation of fluxes of nutrients, water, particles, and organisms to and from land, rivers, and the ocean. Sediment-associated biota are integral to these functions. Functional groups considered essential to CTZ processes include heterotrophic bacteria and fungi, as well as many benthic invertebrates. Key invertebrate functions include shredding, which breaks down and recycles organic matter; suspension feeding, which collects and transports sediments across the sediment–water interface; and bioturbating, which moves sediment into or out of the seabed. In addition, macrophytes regulate many aspects of nutrient, particle, and organism dynamics above- and belowground. Animals moving within or through CTZs are vectors that transport nutrients and organic matter across terrestrial, freshwater, and marine interfaces. Significant threats to biodiversity within CTZs are posed by anthropogenic influences; eutrophication, nonnutrient pollutants, species invasions, overfishing, habitat alteration, and climate change affect species richness or composition in many coastal environments. Because biotic diversity in marine CTZ sediments is inherently low whereas their functional significance is great, shifts in diversity are likely to be particularly important. Species introductions (from invasion) or loss (from overfishing or habitat alteration) provide evidence that single-species changes can have overt, sweeping effects on CTZ structure and function. Certain species may be critically important to the maintenance of ecosystem functions in CTZs even though at present there is limited empirical evidence that the number of species in CTZ sediments is critical. We hypothesized that diversity is indeed important to ecosystem function in marine CTZs because high diversity maintains positive interactions among species (facilitation and mutualism), promoting stability and resistance to invasion or other forms of disturbance. The complexity of interactions among species and feedbacks with ecosystem functions suggests that comparative (mensurative) and manipulative approaches will be required to elucidate the role of diversity in sustaining CTZ functions.

Global patterns in marine dispersal estimates: the influence of geography, taxonomic category and life history

We examine estimates of dispersal in a broad range of marine species through an analysis of published values, and evaluate how well these values represent global patterns through a comparison with correlates of dispersal. Our analysis indicates a historical focus in dispersal studies on low-dispersal/low-latitude species, and we hypothesize that these studies are not generally applicable and representative of global patterns. Large-scale patterns in dispersal were examined using a database of correlates of dispersal such as planktonic larval duration (PLD, 318 species) and genetic differentiation (FST, 246 species). We observed significant differences in FST (p<0.001) and PLD (p<0.001) between taxonomic groups (e.g. fishes, cnidarians, etc.). Within marine fishes (more than 50% of datasets), the prevalence of demersal eggs was negatively associated with PLD (R2=0.80, p<0.001) and positively associated with genetic structure (R2=0.74, p<0.001). Furthermore, dispersal within marine fishes (i.e. PLD and FST) increased with latitude, adult body size and water depth. Of these variables, multiple regression identified latitude and body size as persistent predictors across taxonomic levels. These global patterns of dispersal represent a first step towards understanding and predicting species-level and regional differences in dispersal, and will be improved as more comprehensive data become available.

The biodiversity of macrofaunal organisms in marine sediments

Marine sediments cover most of the ocean bottom, and the organisms that reside in these sediments therefore constitute the largest faunal assemblage on Earth in areal coverage. The biomass in these sediments is dominated by macrofauna, a grouping of invertebrate polychaetes, molluscs, crustaceans and other phyla based on size. Globally, only a small portion of marine habitats have been sampled for macrofauna, but sampled areas have led to global estimates of macrofaunal species number ranging from 500,000 to 10,000,000. Most of these species are undescribed, and global syntheses of patterns of individual taxa and biodiversity are few and based on limited samples. The significance of biodiversity in marine sediments to ecosystem processes is poorly understood, but individual species and functional groups are known to carry out activities that have global importance. Macrofaunal activity impacts global carbon, nitrogen and sulphur cycling, transport, burial and metabolism of pollutants, secondary production including commercial species, and transport of sediments. Documented extinctions of marine macrofauna are few, but the ramifications of species loss through habitat shrinkage and undocumented extinctions are unknown. Limited data suggest there is substantial functional redundancy in macrofauna within trophic groups but whether this redundancy is sufficient to allow species loss without significantly altering ecosystem processes is unknown. Sorely needed are experiments that test specific hypotheses on biodiversity, redundancy, and ecosystem processes as they relate to marine macrofauna.

Parallel adaptive evolution of Atlantic cod on both sides of the Atlantic Ocean in response to temperature

Despite the enormous economic and ecological importance of marine organisms, the spatial scales of adaptation and biocomplexity remain largely unknown. Yet, the preservation of local stocks that possess adaptive diversity is critical to the long-term maintenance of productive stable fisheries and ecosystems. Here, we document genomic evidence of range-wide adaptive differentiation in a broadcast spawning marine fish, Atlantic cod (Gadus morhua), using a genome survey of single nucleotide polymorphisms. Of 1641 gene-associated polymorphisms examined, 70 (4.2%) tested positive for signatures of selection using a Bayesian approach. We identify a subset of these loci (n = 40) for which allele frequencies show parallel temperature-associated clines (p < 0.001, r2 = 0.89) in the eastern and western north Atlantic. Temperature associations were robust to the statistical removal of geographic distance or latitude effects, and contrasted ‘neutral’ loci, which displayed no temperature association. Allele frequencies at temperature-associated loci were significantly correlated, spanned three linkage groups and several were successfully annotated supporting the involvement of multiple independent genes. Our results are consistent with the evolution and/or selective sweep of multiple genes in response to ocean temperature, and support the possibility of a new conservation paradigm for non-model marine organisms based on genomic approaches to resolving functional and adaptive diversity.

Genomic islands of divergence and their consequences for the resolution of spatial structure in an exploited marine fish

As populations diverge, genomic regions associated with adaptation display elevated differentiation. These genomic islands of adaptive divergence can inform conservation efforts in exploited species, by refining the delineation of management units, and providing genomic tools for more precise and effective population monitoring and the successful assignment of individuals and products. We explored heterogeneity in genomic divergence and its impact on the resolution of spatial population structure in exploited populations of Atlantic cod, Gadus morhua, using genome wide expressed sequence derived single nucleotide polymorphisms in 466 individuals sampled across the range. Outlier tests identified elevated divergence at 5.2% of SNPs, consistent with directional selection in one‐third of linkage groups. Genomic regions of elevated divergence ranged in size from a single position to several cM. Structuring at neutral loci was associated with geographic features, whereas outlier SNPs revealed genetic discontinuities in both the eastern and western Atlantic. This fine‐scale geographic differentiation enhanced assignment to region of origin, and through the identification of adaptive diversity, fundamentally changes how these populations should be conserved. This work demonstrates the utility of genome scans for adaptive divergence in the delineation of stock structure, the traceability of individuals and products, and ultimately a role for population genomics in fisheries conservation.

Hydrodynamic enhancement of larval settlement in the bivalve Mulinia lateralis (Say) and the polychaete Capitella sp. I in microdepositional environments

To test whether larval settlement patterns of the opportunistic bivalve Mulinia lateralis (Say) and the opportunistic polychaete Capitella sp. I are influenced by near-bottom flow, laboratory still-water and flume-flow experiments were conducted using a sediment-filled array consisting of depressions and compartments flush with the flume bottom. Compartments were filled with organic-rich mud or a low-organic, glass-bead mixture of a comparable grain size. Previous flume experiments have shown that larvae of both species settle in greater numbers in mud compared with glass beads. Depressions create a hydrodynamic environment that traps passive particles, permitting tests of the relative importance of active selection versus passive deposition of larvae in regions of microtopography. In both flow and still water, Capitella sp. I larvae consistently selected organic-rich mud over glass beads, regardless of whether treatments were flush or depressions. Settlement was higher, however, in depressions (3.8 cm in diameter and 2.8 cm deep) for a given sediment treatment, particularly in glass bead treatments in flow. In flow and still-water experiments, M. lateralis larvae also chose mud over glass beads but, in some instances, higher settlement occurred in glass bead depressions (a “poor” choice) compared to flush mud (a “good” choice). These results suggest that near-bottom flow influences settlement distributions of both species (i.e. settlement enhancement in depressions), but the effect may be greater for M. lateralis larvae. Higher settlement generally observed in mud depressions compared with glass bead depressions suggests that larvae of both species may have been able to “escape” from depressions if the substratum was unsuitable, although M. lateralis larvae were poorer swimmers than Capitella sp. I larvae and were more vulnerable to passive entrainment and retention in depressions. Similar experiments with smaller depressions (9 mm in diameter and 9 mm deep) showed no settlement enhancement in depressions for Capitella sp. I and enhancement in only one of two flow experiments with M. lateralis larvae, suggesting that the hydrodynamic, trapping effect may be scale dependent for both species.

Managing Critical Transition Zones

Ecosystems that function as critical transition zones (CTZs) among terrestrial, freshwater, and marine habitats are closely connected to the ecosystems adjacent to them and are characterized by a rapid flux of materials and organisms. CTZs play various roles, including mediating water flows, accumulating sediments and organic matter, processing nutrients, and providing opportunities for recreation. They are particularly difficult to manage because they tend to be small, albeit important, components of large watersheds, and managers may not have control over the entire landscape. Moreover, they are often the focus of intensive human activity. Consequently, CTZs are critically important zones, and their preservation and protection are likely to require unique collaboration among scientists, managers, and stakeholders. Scientists can learn a great deal from the study of these ecosystems, taking advantage of small size and the importance of fluxes, but a good understanding of adaptive management strategies is needed to establish a dialogue with managers and stakeholders on technical and management issues. An understanding of risk analysis is also important to help set meaningful goals and establish logical strategies that include all of the interested parties. Successful restoration of a CTZ is the best test of the quality of knowledge about its structure and function. Much has already been learned about coastal CTZs through restoration projects, and the large number of such projects involving riparian CTZs in particular suggests that there is considerable opportunity for fruitful collaborations between scientists and managers.

Macrofaunal response to artificial enrichments and depressions in a deep-sea habitat

To test whether colonizing macrofauna specialize on different types of small-scale patches of food and disturbance in the deep sea, sediment tray and artificial depression colonization experiments were conducted on the deep-sea floor at 900-m depth, south of St. Croix, U.S. Virgin Islands. Trays and depressions were unenriched (Unenriched Controls) or enriched with either Thalassiosira sp. or Sargassum sp. Concurrent deployment of different types of enrichment and disturbance made it possible to evaluate whether macrofauna specialize on different patches, and thus avoid species interactions that might lead to competitive exclusion. Depressions create a hydrodynamic regime that traps passive particles, allowing tests of the relative importance of active selection of different patch types versus passive deposition for abundant colonizers. After 23 d, total densities and densities of the four abundant colonizers (Capitella spp., Nereimyra punctata, Cumella sp. and Nebalia sp.) were extremely high in enriched trays, despite relatively low ambient densities. Densities in Unenriched Control Trays were very low, and did not attain ambient densities. After 24 d, total densities in all depression treatments were considerably lower than in enriched tray treatments, and only Sargassum Depression densities exceeded those in the ambient environment. Lower densities of organisms in depression treatments compared with trays and differences in densities among depression treatments suggest that the dominant colonizers were highly active and selective, and were not passively entrained in depressions. Fauna1 analysis indicated that trays and depressions were very different, and Sargassum Depression fauna was very different from other depression types. A strong difference was not observed between fauna in ambient sediments and Thalassiosira sp. or Unenriched Control Depressions, perhaps because Thalassiosira sp. was dropped in depressions on the sediment surface and may have been more readily available to consumers and more rapidly consumed than in trays. Thalassiosira Trays were colonized by a lower diversity fauna than Sargassum Trays, and Unenriched Control Trays were colonized by very low densities of a fauna that was comparable in diversity to the ambient community. Diversity in Sargassum Depressions was higher than in enriched trays but lower than in other artificial depressions and the ambient fauna. Thalassiosira Depressions and Unenriched Control Depressions were comparable in diversity to ambient fauna and natural depressions, which were highly diverse. These experiments suggest that fauna may respond quickly and selectively to artificial food patches and disturbance, and this fauna is different from that observed in the ambient sediment. Thus, a patch mosaic may be part of the 1. Biology Department, Woods Hole Oceanographic Institution, Woods Hole, Massachusetts, 02543, USA. 2. Present address: Institute of Marine and Coastal Sciences, Rutgers University, P.O. Box 231, New Brunswick, New Jersey, 08903, USA. 345 346 Journal of Marine Research [52,2 reason for the high species diversity that is observed in deep-sea ecosystems. The different, highly diverse, fauna observed in natural depressions compared with flat ambient sediment suggests that natural analogs of these experiments have unique faunas that may contribute to the species richness of deep-sea habitats.

Hydrodynamic enhancement of invertebrate larval settlement in microdepositional environments: colonization tray experiments in a muddy habitat

To test whether the distribution of settling larvae in muddy habitats is influenced by near-bed hydrodynamics, colonization trays with different trapping characteristics were deployed flush with the ocean bottom at 20-m depth in Buzzards Bay, Massachusetts. The goal of these experiments was to determine whether different densities of settling larvae would be collected under different hydrodynamic conditions. Before deployment, trays were filled with pre-frozen, muddy sediment collected from the site; some trays (Flush Trays) were filled so that the sediment surface would be flush with that of the ocean bottom when in situ, and other deeper trays (Depression Trays) were filled with a similar volume of sediment so that the sediment surface was a 8 cm below that of the surrounding ocean bottom when deployed. This latter treatment created a hydrodynamic regime that would trap passive particles, permitting a test of whether settling larvae at the site would be entrained like passive particles, and thus occur in higher densities in Depression Trays compared with Flush Trays. Experiments were deployed at five different times during the summer of 1990, and were recovered after 3 or 4 days depending on the sampling date. Total densities of organisms were higher in Depression Trays compared with Flush Trays on each sampling date, and of the five taxa that were consistently abundant, four were significantly more abundant in Depression Trays (bivalve larvae, gastropod larvae, juvenile Mediomastus ambiseta (Hartman) polychaetes, and nemerteans). Juvenile spionid polychaetes were abundant on only one date, and on that date they were significantly more abundant in Depression Trays. The only abundant taxon that was not significantly more abundant in Depression Trays was Capitella spp. polychaetes. To determine whether higher numbers in Depression Trays was an active response by settling larvae to elevated organic matter that is often associated with trapping environments such as depressions, some Flush Trays were enriched with Thalassiosira sp. on one of the sampling dates. Densities of organisms in Thalassiosira Trays were either comparable to or lower than those in Flush Trays, suggesting that higher levels of organic matter do not necessarily promote larval settlement of dominant colonizers at this site over the time scale of these experiments. Furthermore, several of the taxa that were more abundant in Depression Trays are common at the site and might therefore be expected to find Flush Trays a suitable environment in which to settle. Thus, the most parsimonious explanation for these results is that larvae were passively entrained in Depression Trays. These field experiments are consistent with results from earlier flume studies suggesting that the microdepositional environment of small depressions may result in passive entrainment of settling larvae, indicating that hydrodynamic, as well as behavioral, factors may determine where larvae in muddy habitats initially settle.

Biodiversity links above and below the marine sediment–water interface that may influence community stability

Linkages across the sediment–water interface (SWI) between biodiversity and community stability appear to exist but are very poorly studied. Processes by which changes in biodiversity could affect stability on the other side of the SWI include carbon transfer during feeding, decomposition of organic matter, nutrient recycling, organism recruitment and structural stabilisation of sediments. The importance of these processes will clearly vary among habitats. Direct disturbance to communities on one side of the SWI, such as created by overfishing, habitat destruction, and species invasions, has the potential to impact communities on the other side of the SWI through the many functional links. Hypotheses are proposed to suggest further areas of research to fill the large gaps in our knowledge concerning the nature and intensity of such linkages. The linkage between benthic and pelagic diversity is likely to be tighter where there is a close energetic connection between the domains, such as polar and shallow coastal waters, and where communities are dominated by selective detritivores. The quantity of carbon reserves in the sediment and the predominant mode of larval development of sediment communities probably influence the stability of below SWI communities in the face of changes in above SWI diversity. The organisms, including hyperbenthos, that are found at the SWI may be of crucial importance to the linkage and stability of above and below SWI communities.