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In intertidal communities, consumers (especially carnivorous gastropods) have historically been thought to exert strong top-down control on community composition by regulating competitively dominant mussels and barnacles. This paradigm was formulated based on wire mesh cage exclusion experiments, which have well-known artifacts such as altering hydrodynamics and excluding non-target, but potentially important, consumer species. Recent research highlights the potential importance of multiple consumers that are often subtle and transient, as well as the modifications of consumer pressure by spatial and temporal environmental variability and bottom-up processes. Manipulative experiments that target individual taxa will be essential to more clearly identify their roles in complex ecological communities. The predatory gastropod Nucella lapillus has long been considered an important consumer controlling the structure and dynamics of intertidal communities in the Gulf of Maine. To test the role of N. lapillus in shaping community structure, we manually reduced its densities for 2.33 years. Species composition, stable stage community composition (based on a Markov model), and transition probabilities (as measures of ecological pathway strength) were compared between treatments (control vs. density reductions), and among seasons (spring, summer, fall, winter). In contrast to previous studies, exclusions had no effect on community composition or long-term Markov model predictions of stable stage community structure. Reducing N. lapillus abundance increased the persistence and reduced the mortality of the barnacle Semibalanus balanoides in the model, but did not affect blue mussels, Mytilus edulis , in a similar way. Reducing N. lapillus abundance had additional indirect effects of increasing Ralfsia spp. mortality and increasing hydroid persistence. Despite differences in transition probabilities among treatments, compensatory changes in direct and indirect pathways led to communities that converged over the long-term. Our results contrast previous estimates of the role of N. lapillus in intertidal communities and might reflect low mussel recruitment, predation by alternate consumers (e.g., C. maenas , C. borealis , Tautogolabrus adspersus , birds), or spatial and/or temporal environmental variation that influenced the role of N. lapillus in structuring these communities. The role of N. lapillus may be more limited, or variable, than often assumed in the Gulf of Maine, and the methods manipulating broad functional groups such as “consumers”, though useful in developing basic conceptual models, blur the effects of individual species in community assembly and dynamics.

With anthropogenic impacts rapidly advancing into deeper waters, there is growing interest in establishing deep-sea marine protected areas (MPAs) or reserves. Reserve design depends on estimates of connectivity and scales of dispersal for the taxa of interest. Deep-sea taxa are hypothesized to disperse greater distances than shallow-water taxa, which implies that reserves would need to be larger in size and networks could be more widely spaced; however, this paradigm has not been tested. We compiled population genetic studies of deep-sea fauna and estimated dispersal distances for 51 studies using a method based on isolation-by-distance slopes. Estimates of dispersal distance ranged from 0.24 km to 2028 km with a geometric mean of 33.2 km and differed in relation to taxonomic and life-history factors as well as several study parameters. Dispersal distances were generally greater for fishes than invertebrates with the Mollusca being the least dispersive sampled phylum. Species that are pelagic as adults were more dispersive than those with sessile or sedentary lifestyles. Benthic species from soft-substrate habitats were generally less dispersive than species from hard substrate, demersal or pelagic habitats. As expected, species with pelagic and/or feeding (planktotrophic) larvae were more dispersive than other larval types. Many of these comparisons were confounded by taxonomic or other life-history differences (e.g. fishes being more dispersive than invertebrates) making any simple interpretation difficult. Our results provide the first rough estimate of the range of dispersal distances in the deep sea and allow comparisons to shallow-water assemblages. Overall, dispersal distances were greater for deeper taxa, although the differences were not large (0.3-0.6 orders of magnitude between means), and imbalanced sampling of shallow and deep taxa complicates any simple interpretation. Our analyses suggest the scales of dispersal and connectivity for reserve design in the deep sea might be comparable to or slightly larger than those in shallow water. Deep-sea reserve design will need to consider the enormous variety of taxa, life histories, hydrodynamics, spatial configuration of habitats and patterns of species distributions. The many caveats of our analyses provide a strong impetus for substantial future efforts to assess connectivity of deep-sea species from a variety of habitats, taxonomic groups and depth zones.

An international initiative takes conservation planning into the deep ocean to inform environmental management of deep-sea mining., Mineral exploitation has spread from land to shallow coastal waters and is now planned for the offshore, deep seabed. Large seafloor areas are being approved for exploration for seafloor mineral deposits, creating an urgent need for regional environmental management plans. Networks of areas where mining and mining impacts are prohibited are key elements of these plans. We adapt marine reserve design principles to the distinctive biophysical environment of mid-ocean ridges, offer a framework for design and evaluation of these networks to support conservation of benthic ecosystems on mid-ocean ridges, and introduce projected climate-induced changes in the deep sea to the evaluation of reserve design. We enumerate a suite of metrics to measure network performance against conservation targets and network design criteria promulgated by the Convention on Biological Diversity. We apply these metrics to network scenarios on the northern and equatorial Mid-Atlantic Ridge, where contractors are exploring for seafloor massive sulfide (SMS) deposits. A latitudinally distributed network of areas performs well at (i) capturing ecologically important areas and 30 to 50% of the spreading ridge areas, (ii) replicating representative areas, (iii) maintaining along-ridge population connectivity, and (iv) protecting areas potentially less affected by climate-related changes. Critically, the network design is adaptive, allowing for refinement based on new knowledge and the location of mining sites, provided that design principles and conservation targets are maintained. This framework can be applied along the global mid-ocean ridge system as a precautionary measure to protect biodiversity and ecosystem function from impacts of SMS mining.

Little is known about how larvae disperse in deep ocean currents despite how critical estimates of population connectivity are for ecology, evolution and conservation. Estimates of connectivity can provide important insights about the mechanisms that shape patterns of genetic variation. Strong population genetic divergence above and below about 3000 m has been documented for multiple protobranch bivalves in the western North Atlantic. One possible explanation for this congruent divergence is that the Deep Western Boundary Current (DWBC), which flows southwestward along the slope in this region, entrains larvae and impedes dispersal between the upper/middle slope and the lower slope or abyss. We used Lagrangian particle trajectories based on an eddy-resolving ocean general circulation model (specifically FLAME – Family of Linked Atlantic Model Experiments) to estimate the nature and scale of dispersal of passive larvae released near the sea floor at 4 depths across the continental slope (1500, 2000, 2500 and 3200 m) in the western North Atlantic and to test the potential role of the DWBC in explaining patterns of genetic variation on the continental margin. Passive particles released into the model DWBC followed highly complex trajectories that led to both onshore and offshore transport. Transport averaged about 1 km d−1 with dispersal kernels skewed strongly right indicating that some larvae dispersed much greater distances. Offshore transport was more likely than onshore and, despite a prevailing southwestward flow, some particles drifted north and east. Dispersal trajectories and estimates of population connectivity suggested that the DWBC is unlikely to prevent dispersal among depths, in part because of strong cross-slope forces induced by interactions between the DWBC and the deeper flows of the Gulf Stream. The strong genetic divergence we find in this region of the Northwest Atlantic is therefore likely driven by larval behaviors and/or mortality that limit dispersal, or local selective processes (both pre and post-settlement) that limit recruitment of immigrants from some depths.

Understanding the role of larger-scale processes in modulating the assembly, structure, and dynamics of communities is critical for forecasting the effects of climate-change and managing ecosystems. Developing this comprehensive perspective is difficult though, because species interactions are complex, interdependent, and dynamic through space and time. Typically, experiments focus on tractable subsets of interactions that will be most critical to investigate and explain shifts in communities, but qualitatively base these choices on experience, natural history, and theory. One quantitative approach to identify the putative forces regulating communities, without reducing system complexity, is estimating transition probabilities among species occupying space (i.e., multispecies Markov chain models). Although not mechanistic, these models estimate the relative frequency and importance of ecological pathways in community assembly and dynamics, and can serve as a framework to identify how pathways change across large scales and which are most important to investigate further. Here, we demonstrate this method in the Gulf of Maine (GOM) intertidal zone, where research has largely focused on the local-scale processes that influence communities, while the mechanisms responsible for more regional shifts in communities are less clear. Transition probabilities of faunal elements were quantified bimonthly for ~2.5 yr in local intertidal communities at three replicate sites in the southern, mid-coast, and northern GOM. Transitions related to mortality, colonization, and replacement by mussels, barnacles, red algae, and encrusting corallines differed regionally, suggesting specific pathways related to consumer pressure and recruitment vary across the GOM with shifting intertidal community structure. Combined with species abundance data and insights from previous research, we develop and evaluate the pathways by which communities likely change in the GOM. Species interactions in local communities can be complex, and this complexity should be incorporated into hypothesis building, experiments, theory, interpretations, and forecasts in ecology. Such a comprehensive approach will be critical to understand how regional shifts in local interactions can drive large-scale community change.

The ability to accurately estimate population connectivity and larval dispersal among mussel populations in the Gulf of Maine is important to better understand ongoing declines in blue mussel abundances. Such efforts are crucial for crafting conservation strategies targeting important spawning and settlement sites necessary to support threatened local shellfisheries, and to mitigate the potential effects of rapid climate change on larval dispersal and survivorship. Trace element fingerprints can be used to infer larval dispersal and population connectivity, but require a reference map of geographic variation in elemental fingerprints to infer natal sites of settled mussels. Previous work has suggested rearing mussel larvae in situ to create a reference map because biomineralization differs between larval and post-metamorphic mussels, which might lead to differences in trace element fingerprints. To test whether elemental fingerprints differed between larval and juvenile (post-metamorphic) mussels ( Mytilus edulis ), we reared them in situ and under controlled laboratory conditions. Trace element concentrations in larval and juvenile shell matrices were quantified using laser ablation inductively coupled plasma mass spectrometry (LA-ICPMS). The majority of trace element concentrations, normalized to calcium, differed between larval and juvenile mussels, resulting in elemental fingerprints that were consistently distinct between age classes. Larval and juvenile fingerprints differed consistently whether they were reared in the lab or field, probably reflecting age-specific differences in biomineralization. To use trace element fingerprints to estimate larval dispersal and population connectivity, our results suggest that a spatial map of elemental fingerprints should be created by rearing larval, not juvenile, mussels at potential source populations. Our results are consistent with what has been found for other mussels and thus may be true for all mussels, and likely true for any bivalves with age-specific differences in biomineralization.

The deep ocean supports a highly diverse and mostly endemic fauna, yet little is known about how or where new species form in this remote ecosystem. How speciation occurs is especially intriguing in the deep sea because few obvious barriers exist that would disrupt gene flow. Geographic and bathymetric patterns of genetic variation can provide key insights into how and where new species form. We quantified the population genetic structure of a protobranch bivalve, Neilonella salicensis, along a depth gradient (2200‐3800 m) in the western North Atlantic using both nuclear (28S and calmodulin intron) and mitochondrial (cytochrome c oxidase subunit I) loci. A sharp genetic break occurred for each locus between populations above 2800 m and below 3200 m, defining two distinct clades with no nuclear or mitochondrial haplotypes shared between depth regimes. Bayesian phylogenetic analyses provided strong support for two clades, separated by depth, within N. salicensis. Although no morphological divergence was apparent, we suggest that the depth-related population genetic and phylogenetic divergence is indicative of a cryptic species. The frequent occurrence of various stages of divergence associated with species formation along bathymetric gradients suggests that depth, and the environmental gradients that attend changes in depth, probably play a fundamental role in the diversification of marine organisms, especially in deep water. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, ••, ••‐••.

The Pleistocene and post-Pleistocene evolutionary history of many North Atlantic intertidal invertebrate species is well known, but the evolutionary history of the deep North Atlantic fauna is poorly understood, specifically whether colonization of the deep North Atlantic paralleled the patterns observed in shallow water. Contemporary pan-Atlantic species distributions could result from several colonization pathways that connected different regions of the Atlantic at different times (e.g. Arctic, Antarctic or Panamanian pathways). To test potential colonization pathways we quantified geographic variation in nuclear and mitochondrial markers from Atlantic samples ofNucula atacellana, a pan-Atlantic deep-sea protobranch bivalve, usingN. profundorumin the eastern central Pacific as an outgroup. We combined existing 16S data from North and South Atlantic populations ofN. atacellanawith new sequences of 16S, COI, and an intron of calmodulin from those populations, and newly sampled populations near Iceland. Population genetic analyses indicated a subtropical expansion via the Central American Seaway. We found no evidence for Transarctic migration to the Atlantic inN. atacellana, which suggests that colonization pathways may differ significantly between shallow- and deep-water fauna.

A molecular phylogeny of Protobranchia, the subclass of bivalve mollusks sister to the remaining Bivalvia, has long proven elusive, because many constituent lineages are deep-sea endemics, which creates methodological challenges for collecting and preserving genetic material. We obtained 74 representatives of all 12 extant protobranch families and investigated the internal phylogeny of this group using sequence data from five molecular loci (16S rRNA, 18S rRNA, 28S rRNA, cytochrome c oxidase subunit I, and histone H3). Model-based and dynamic homology parsimony approaches to phylogenetic reconstruction unanimously supported four major clades of Protobranchia, irrespective of treatment of hypervariable regions in the nuclear ribosomal genes 18S rRNA and 28S rRNA. These four clades correspond to the superfamilies Nuculoidea (excluding Sareptidae), Nuculanoidea (including Sareptidae), Solemyoidea, and Manzanelloidea. Salient aspects of the phylogeny include (1) support for the placement of the family Sareptidae with Nuculanoidea; (2) the non-monophyly of the order Solemyida (Solemyidae + Nucinellidae); (3) and the non-monophyly of most nuculoid and nuculanoid genera and families. In light of this first family-level phylogeny of Protobranchia, we present a revised classification of the group. Estimation of divergence times in concert with analyses of diversification rates demonstrate the signature of the end-Permian mass extinction in the phylogeny of extant protobranchs.

The earth is in the midst of a biodiversity crisis, and projections indicate continuing and accelerating rates of global changes. Future alterations in communities and ecosystems may be precipitated by changes in the abundance of strongly interacting species, whose disappearance can lead to profound changes in abundance of other species, including an increase in extinction rate for some. Nearshore coastal communities are often dependent on the habitat and food resources provided by foundational plant (e.g., kelp) and animal (e.g., shellfish) species. We quantified changes in the abundance of the blue mussel (Mytilus edulis), a foundation species known to influence diversity and productivity of intertidal habitats, over the past 40 years in the Gulf of Maine, USA, one of the fastest warming regions in the global ocean. Using consistent survey methods, we compared contemporary population sizes to historical data from sites spanning >400 km. The results of these comparisons showed that blue mussels have declined in the Gulf of Maine by >60% (range: 29-100%) at the site level since the earliest benchmarks in the 1970s. At the same time as mussels declined, community composition shifted: at the four sites with historical community data, the sessile community became increasingly algal dominated. Contemporary (2013-2014) surveys across 20 sites showed that sessile species richness was positively correlated to mussel abundance in mid to high intertidal zones. These results suggest that declines in a critical foundation species may have already impacted the intertidal community. To inform future conservation efforts, we provide a database of historical and contemporary baselines of mussel population abundance and dynamics in the Gulf of Maine. Our results underscore the importance of anticipating not only changes in diversity but also changes in the abundance and identity of component species, as strong interactors like foundation species have the potential to drive cascading community shifts.

Most metazoan species have strict maternal inheritance of the mitochondrial genome. In bivalves, a unique inheritance pattern called doubly uniparental inheritance (DUI) occurs in at least seven bivalve families. In this system of mitochondrial inheritance, males inherit and carry mtDNA from both parents, while females only carry mtDNA from the mother. Here, we present evidence of mitochondrial heteroplasmy in deep-sea protobranch bivalves. Divergent 16S rRNA and cytochrome b sequences were obtained within individuals of Ledella ultima. Ledella sublevis also exhibited divergent 16S sequences. Levels of divergence between 16S sequences within individuals were 27 and 15 % for each species, respectively. Ratios of homoplasmic to heteroplasmic individuals were not significantly different from 1:1, in agreement with sex ratios in protobranchs. The results provide the first evidence for mitochondrial heteroplasmy in the protobranchs and suggest DUI might have evolved much earlier in the evolution of the Bivalvia than previously thought.

We describe PCR primers and amplification protocols developed to obtain introns from conserved nuclear genes in deep-sea protobranch bivalves. Because almost no sequence data for protobranchs are publically available, mollusk and other protostome sequences from GenBank were used to design degenerate primers, making these loci potentially useful in other invertebrate taxa. Amplification and sequencing success varied across the test group of 30 species, and we present five loci spanning this range of outcomes. Intron presence in the targeted regions also varied across genes and species, often within single genera; for instance, the calmodulin and β-tubulin loci contained introns with high frequency, whereas the triose phosphate isomerase locus never contained an intron. In introns for which we were able to obtain preliminary estimates of polymorphism levels in single species, polymorphism was greater than traditional mitochondrial loci. These markers will greatly increase the ability to assess population structure in the ecologically important protobranchs, and may prove useful in other taxa as well.

The physical orientation of rocky substrate profoundly affects subtidal marine commu- nities of sessile organisms. Anecdotal descriptions of dramatic differences between communities on rock walls and adjacent horizontal rocky bottoms abound in the literature and are common knowl- edge among scuba divers, yet these differences have rarely been quantified by ecologists. We sam- pled rock walls and adjacent horizontal rock bottoms at 8 subtidal sites across the Gulf of Maine. Spe- cies richness and abundance, in percent cover, of sessile invertebrates on vertical walls averaged 4 times higher than that on horizontal platforms, whereas abundance of macroalgae on horizontal rock was about 3 times that on vertical walls. Both macroalgae and sessile invertebrates were less abundant, particularly on horizontal surfaces, at sites with high sea urchin densities. The consistency of sessile invertebrate domination of vertical walls versus macroalgal domination of horizontal rock, combined with previous experimental results, suggests that competition for space between autotro- phic and heterotrophic organisms drives this pattern. The partitioning of autotrophs (macroalgae) and heterotrophs (sessile invertebrates) between horizontal and vertical surfaces respectively implies that topographic heterogeneity plays an important role in the structure, composition and function of rocky subtidal ecosystems.

The deep sea is a vast and essentially continuous environment with few obvious barriers to gene flow. How populations diverge and new species form in this remote ecosystem is poorly understood. Phylogeographical analyses have begun to provide some insight into evolutionary processes at bathyal depths ( 3000 m). Here, we quantify geographical and bathymetric patterns of genetic variation (16S rRNA mitochondrial gene) in the protobranch bivalve Ledella ultima, which is one of the most abundant abyssal protobranchs in the Atlantic with a broad bathymetric and geographical distribution. We found virtually no genetic divergence within basins and only modest divergence among eight Atlantic basins. Levels of population divergence among basins were related to geographical distance and were greater in the South Atlantic than in the North Atlantic. Ocean-wide patterns of genetic variation indicate basin-wide divergence that exceeds what others have found for abyssal organisms, but considerably less than bathyal protobranchs across similar geographical scales. Populations on either side of the Mid-Atlantic Ridge in the North Atlantic differed, suggesting the Ridge might impede gene flow at abyssal depths. Our results indicate that abyssal populations might be quite large (cosmopolitan), exhibit only modest genetic structure and probably provide little potential for the formation of new species.

Dramatic shifts in community composition occur between vertical and horizontal rocky surfaces in subtidal environments worldwide, yet the forces mediating this transition are poorly understood. Vertical rock walls are often covered by lush, diverse communities of sessile suspension-feeding invertebrates, while adjacent horizontal substrates are dominated by algae, or corals in the tropics. Multiple factors, including light, sedimentation, water flow, and predation have been proposed to explain this pattern, but experimental tests of these hypotheses are lacking. We manipulated light level and predation to test whether variation in these mechanisms could be responsible for the shift in composition of sessile communities between vertical and horizontal surfaces in the rocky subtidal Gulf of Maine. Shaded horizontally oriented granite plots were dominated by invertebrates (e.g., ascidians, barnacles, bryozoans) after 25 months. Unshaded plots were dominated by macroalgae, which was virtually absent in shaded plots. Exclusion of grazers with cages had no effect on percent cover of invertebrates or algae. Preferential settlement of invertebrate larvae to shaded plots, due to larval behaviors such as negative phototaxis, did not seem to play a role. Shading likely affects post-settlement mortality of invertebrates by alleviating competition for space with algae, although greater abundance of micropredators in algal- dominated communities could also be important. Communities on shaded plots lacked many taxa present on natural wall communities, likely due to greater disturbance on horizontal substrates and/or lack of sufficient time for colonization of these taxa. These results suggest that light plays a key role in controlling the structure, composition, and function of shallow subtidal communities.

The relationship between surface production and benthic standing stock is fundamental to understanding biogeography in the deep sea. While much has been learned about the complex oceanographic processes involved in energy transfer to the benthos on local scales, the correspondence of overhead production to benthic community structure on regional scales remains poorly characterized. We compiled a database on the biomass and abundance of deep-sea macrobenthos in the western North Atlantic collected from 1961 to 1985. Using SeaWiFS satellite color imagery, we calculated POC from surface chlorophyll a concentrations (from 1997 to 2001), and estimated POC flux to the seafloor by using the empirically derived Pace et al. [1987. Primary production, new production and vertical flux in the eastern Pacific Ocean. Nature 325, 803–804] algorithm. The standing stock and surface production data are not concurrent, but their basic geographic trends at these very large spatial scales appear to be relatively stable over the time scales of measurement. Estimated POC flux at depth accounts for 62–67% of the variance ðPo0:0001Þ in benthic standing stock, suggesting that macroecological studies of the relationship between satellite-derived surface production and deep-sea community structure may be possible. r 2007 Elsevier Ltd. All rights reserved.

Gastropod shells are important antipredator structures that vary morphologically in response to predation risk, often increasing in thickness when the risk of predation is greater. Because the shell is composed of different microstructures that vary in energetic cost and strength, shell thickness may be increased in different ways. We tested whether the common intertidal snail Nucella lapillus differs in microstructure between shores with different predation risk, and whether any differences in microstructure affect shell strength. Predation risk varies with degree of wave exposure, so we compared shell microstructure and strength between snails from different exposure regimes. N. lapillus shells are made of a strong but energetically expensive crossed lamellar microstructure and a weaker but less energetically expensive homogeneous microstructure. Inde- pendent of exposure regime, the homogeneous microstructure was used to thicken the shell as snails increase in size. The thickness of the stronger crossed-lamellar microstructure changes little with snail size or predator risk. Whelks from wave-protected shores, where predation risk is high, have much thicker shells than conspecifics from exposed shores, where predation risk is low. The greater thickness is largely due to a disproportionate increase in the thickness of the homogeneous layer, and this increase translates into a much stronger shell. The advantage of using the weaker microstructure may lie in the fact that it is energetically cheaper and can be deposited more quickly, allowing snails to grow more rapidly to a size refuge. Reinforcing the shell with weaker and energetically cheaper materials that allow rapid growth to a size refuge may be a more important strategy for reducing the risk of predation than simply maximizing strength.

We present the first global-scale analy- sis of standing stock (abundance and biomass) for 4 major size classes of deep-sea biota: bacteria, meta- zoan meiofauna, macrofauna and megafauna. The community standing stock decreases with depth; this is a universal phenomenon that involves a com- plex transition in the relative importance of the different size groups. Bacterial abundance and biomass show no decline with depth. All 3 animal size groups experience significant exponential de- creases in both abundance and biomass. The abun- dance of larger animals is significantly lower and decreases more rapidly than for smaller groups. The resulting drop in average body size with depth con- firms Thiel's size-structure hypothesis on very large spatial scales. In terms of their proportion of total community biomass, smaller size classes replace larger size classes. The upper continental slope is dominated by macrofaunal biomass, and the abyss by bacterial and meiofaunal biomass. The dramatic decrease in total community standing stock and the ascendancy of smaller organisms with depth has important implications for deep-sea biodiversity. The bathyal zone (200 to 4000 m) affords more eco- logical and evolutionary opportunity in the form of energy availability for larger organisms, and conse- quently supports higher macrofaunal and mega- faunal species diversity than the abyss (> 4000 m).

The deep-sea soft-sediment environment hosts a diverse and highly endemic fauna of uncertain origin. We know little about how this fauna evolved because geographic patterns of genetic variation, the essential information for inferring patterns of population differentiation and speciation are poorly understood. Using formalin-fixed specimens from archival collections, we quantify patterns of genetic variation in the protobranch bivalve Deminucula atacellana, a species widespread throughout the Atlantic Ocean at bathyal and abyssal depths. Samples were taken from 18 localities in the North American, West European and Argentine basins. A hypervariable region of mitochondrial 16S rDNA was amplified by polymerase chain reaction (PCR) and sequenced from 130 individuals revealing 21 haplotypes. Except for several important exceptions, haplotypes are unique to each basin. Overall gene diversity is high ( h = 0.73) with pronounced population structure (Φ ST = 0.877) and highly significant geographic associations ( P < 0.0001). Sequences cluster into four major clades corresponding to differences in geography and depth. Genetic divergence was much greater among populations at different depths within the same basin, than among those at similar depths but separated by thousands of kilometres. Isolation by distance probably explains much of the interbasin variation. Depth-related divergence may reflect historical patterns of colonization or strong environmental selective gradients. Broadly distributed deep-sea organisms can possess highly genetically divergent populations, despite the lack of any morphological divergence.

Geometric constraints represent a class of null models that describe how species diversity may vary between hard boundaries that limit geographic distributions. Recent studies have suggested that a number of large scale biogeographic patterns of diversity (e.g. latitude, altitude, depth) may reflect boundary constraints. However, few studies have rigorously tested the degree to which mid-domain null predictions match empirical patterns or how sensitive the null models are to various assumptions. We explore how variation in the assumptions of these models alter null depth ranges and consequently bathymetric variation in diversity, and test the extent to which bathymetric patterns of species diversity in deep sea gastropods, bivalves, and polychaetes match null predictions based on geometric constraints. Range–size distributions and geographic patterns of diversity produced by these null models are sensitive to the relative position of the hard boundaries, the specific algorithms used to generate range sizes, and whether species are continuously or patchily distributed between range end points. How well empirical patterns support null expectations is highly dependent on these assumptions. Bathymetric patterns of species diversity for gastropods, bivalves and polychaetes differ substantially from null expectations suggesting that geometric constraints do not account for diversity–depth patterns in the deep sea benthos.

The number of species coexisting in ecological communities must be a consequence of processes operating on both local and regional scales. Although a great deal of experimental work has been devoted to local causes of diversity, little is known about the effects of regional processes on local diversity and how they contribute to global diversity patterns in marine systems. We tested the effects of latitude and the richness of the regional species pool on the species richness of local epifaunal invertebrate communities by sampling the diversity of local sites in 12 independent biogeographic regions from 62°S to 63°N latitude. Both regional and local species richness displayed significant unimodal patterns with latitude, peaking at low latitudes and decreasing toward high latitudes. The latitudinal diversity gradient was represented at the scale of local sites because local species richness was positively and linearly related to regional species richness. The richness of the regional species pool explained 73-76% of local species richness. On a global scale, the extent of regional influence on local species richness was nonrandom—the proportion of regional biota represented in local epifaunal communities increased significantly from low to high latitudes. The strong effect of the regional species pool implies that patterns of local diversity in temperate, tropical, and high-latitude marine benthic communities are influenced by processes operating on larger spatiotemporal scales than previously thought.

With the development of new methods to sequence DNA from preserved organisms, existing archival collections can be used to document the population genetic structure of deep-sea species. This has made possible the first direct inferences about patterns of evolutionary diversification in the soft-sediment macrofauna. Here we report protocols and success rates for amplifying and sequencing regions of the mitochondrial 16S rDNA, Cytochrome oxidase I (COI), and Cytochrome b (cytb) genes from formalin-fixed protobranch bivalves and gastropods, major components of the deep-sea benthos. DNA was extracted from 1532 individuals of 12 common bathyal and abyssal species that had been fixed in formalin and preserved in alcohol for up to 36 years. DNA was also extracted from 53 individuals that were dried upon collection, some of which were collected more than 100 years ago. The overall success rate for amplification by PCR was 44%, but this varied considerably among species, stations, and cruises. When DNA amplified, sequencing success was generally high, averaging 85% and ranging from 19% to 100%. The reliability of amplification and sequencing depend strongly on how samples are treated during collection and storage. Amplification success was similar among samples collected from the same station and samples collected on the same cruise. We provide recommendations on strategies for primer design, PCR, and sample selection to improve success rates for genetic analysis of preserved deep-sea organisms. The success rates from different collections, sampling stations, and cruises provide important guidance for selecting material for future genetic work on deep-sea collections examined here.

The deep sea supports a diverse and highly endemic invertebrate fauna, the origin of which remains obscure. Little is known about geographic variation in deep-sea organisms or the evolutionary processes that promote population-level differentiation and eventual speciation. Sequence variation at the 16 S rDNA locus was examined in formalin-preserved specimens of the common upper bathyal rissoid Frigidoalvania brychia (Verrill, 1884) to examine its population genetic structure. The specimens came from trawl samples taken over 30 years ago at depths of 457–1,102 m at stations in the Northwest Atlantic south of Woods Hole, Massachusetts, USA. Near the upper boundary of its bathymetric range (500 m), extremely divergent haplotypes comprising three phylogenetically distinct clades (average uncorrected sequence divergence among clades ~23%, ~3% within clades) were found at stations separated by a maximum distance of ~80 km, suggesting the presence of high levels of intraspecific divergence or the possibility of morphologically cryptic species. Only one of these clades was found at two stations in the mid- to lower part of F. brychia's depth distribution (800–1,100 m), suggesting lower clade diversity with increasing depth, although among-sample divergence, with a single exception, was minimal. One station was genetically divergent from all others sampled, containing a unique suite of haplotypes including two found only at this site. Steep vertical selective gradients, major oceanographic changes during the late Cenozoic, and habitat fragmentation by submarine canyons might have contributed to an upper bathyal region that is highly conducive to evolutionary change.

▪ Abstract Most of our knowledge of biodiversity and its causes in the deep-sea benthos derives from regional-scale sampling studies of the macrofauna. Improved sampling methods and the expansion of investigations into a wide variety of habitats have revolutionized our understanding of the deep sea. Local species diversity shows clear geographic variation on spatial scales of 100–1000 km. Recent sampling programs have revealed unexpected complexity in community structure at the landscape level that is associated with large-scale oceanographic processes and their environmental consequences. We review the relationships between variation in local species diversity and the regional-scale phenomena of boundary constraints, gradients of productivity, sediment heterogeneity, oxygen availability, hydrodynamic regimes, and catastrophic physical disturbance. We present a conceptual model of how these interdependent environmental factors shape regional-scale variation in local diversity. Local communities in the deep sea may be composed of species that exist as metapopulations whose regional distribution depends on a balance among global-scale, landscape-scale, and small-scale dynamics. Environmental gradients may form geographic patterns of diversity by influencing local processes such as predation, resource partitioning, competitive exclusion, and facilitation that determine species coexistence. The measurement of deep-sea species diversity remains a vital issue in comparing geographic patterns and evaluating their potential causes. Recent assessments of diversity using species accumulation curves with randomly pooled samples confirm the often-disputed claim that the deep sea supports higher diversity than the continental shelf. However, more intensive quantitative sampling is required to fully characterize the diversity of deep-sea sediments, the most extensive habitat on Earth. Once considered to be constant, spatially uniform, and isolated, deep-sea sediments are now recognized as a dynamic, richly textured environment that is inextricably linked to the global biosphere. Regional studies of the last two decades provide the empirical background necessary to formulate and test specific hypotheses of causality by controlled sampling designs and experimental approaches.

We have developed cellular automaton models for two species competing in a patchy environment. We have modeled three common types of competition: facilitation (in which the winning species can colonize only after the losing species has arrived) inhibition (in which either species is able to prevent the other from colonizing) and tolerance (in which the species most tolerant of reduced resource levels wins). The state of a patch is defined by the presence or absence of each species. State transition probabilities are determined by rates of disturbance, competitive exclusion, and colonization. Colonization is restricted to neighboring patches. In all three models, disturbance permits regional persistence of species that are excluded by competition locally. Persistence, and hence diversity, is maximized at intermediate disturbance frequencies. If disturbance and dispersal rates are sufficiently high, the inferior competitor need not have a dispersal advantage to persist. Using a new method for measuring the spatial patterns of nominal data, we show that none of these competition models generates patchiness at equilibrium. In the inhibition model, however, transient patchiness decays very slowly. We compare the cellular automaton models to the corresponding mean-field patch-occupancy models, in which colonization is not restricted to neighboring patches and depends on spatially averaged species frequencies. The patch-occupancy model does an excellent job of predicting the equilibrium frequencies of the species and the conditions required for coexistence, but not of predicting transient behavior.

Our knowledge of deep-sea biodiversity is based almost entirely on morphological distinctions at the species level. Here, we use haplotype variations in the mitochondrial 16S ribosomal gene to assess biodiversity at the genome level in four deep-sea molluscan morphospecies. Genetic divergence levels among populations of the morphospecies fall within the range of interspecific divergence found in coastal marine and aquatic molluscan genera. Results indicate a rich population structure at the genetic level in deep-sea mollusks, and suggest the possibility that some seemingly coherent morphospecies are composed of cryptic species.

The origin of the deep-sea benthic fauna is poorly understood and represents an enormous gap in our understanding of basic evolutionary phenomena. One obstacle to studying evolutionary patterns in the deep sea has been the technical difficulty of measuring genetic variation in species that are typically minute, rare, and must be recovered from extreme depths. We used molecular genetic techniques to quantify variation in the 16S rRNA mitochondrial gene within and among populations of the common protobranch bivalve Deminucula atacellana (Schenck, 1939). We analyzed 89 individuals from nine samples collected in the 1960s along a depth gradient from 1100 to 3800 m in the western North Atlantic. Genetic variability within populations is much lower than between populations, and peak haplotype numbers occur near the center of its depth distribution. Continental slope ( 2500 m) populations were genetically distinct despite the lack of any obvious topographic or oceanographic features that would impede gene flow. These findings indicate that the deep-sea macrofauna can have strong population structure over small (134 km) spatial scales, similar to that observed in shallow-water and terrestrial organisms. This surprisingly high biodiversity at the genetic level affords the potential for adaptation and evolutionary diversification, the ultimate historical causes of high species diversity in the deep-sea benthos.

The evolution of body size is a problem of fundamental interest, and one that has an important bearing on community structure and conservation of biodiversity. The most obvious and pervasive characteristic of the deep-sea benthos is the small size of most species. The numerous attempts to document and explain geographic patterns of body size in the deep-sea benthos have focused on variation among species or whole faunal components, and have led to conflicting and contradictory results. It is important to recognize that studying size as an adaptation to the deep-sea environment should include analyses within species using measures of size that are standardized to common growth stages. An analysis within eight species of deep-sea benthic gastropods presented here reveals a clear trend for size to increase with depth in both larval and adult shells. An ANCOVA with multiple comparison tests showed that, in general, size–depth relationships for both adult and larval shells are more pronounced in the bathyal region than in the abyss. This result reinforces the notion that steepness of the bathymetric selective gradient decreases with depth, and that the bathyal region is an evolutionary hotspot that promotes diversification. Bathymetric size clines in gastropods support neither the predictions of optimality models nor earlier arguments based on tradeoffs among scaling factors. As in other environments, body size is inversely related to both abundance and species density. We suggest that the decrease in nutrient input with depth may select for larger size because of its metabolic or competitive advantages, and that larger size plays a role in limiting diversity. Adaptation is an important evolutionary driving force of biological diversity, and geographic patterns of body size could help unify ecological and historical theories of deep-sea biodiversity.

Growth rates of intertidal snails vary among populations differentially exposed to wave action; individuals from sheltered habitats typically grow more quickly than do those from more exposed coasts. A series of field and laboratory experiments were conducted to separate the genetic and phenotypic components of this variation in Nucella lapillus (L.) and to investigate the extent to which prey type and foraging time, which also vary across the wave-exposure gradient, affect growth. Juvenile and adult whelks were reciprocally transplanted between an exposed and a protected shore and subsequent growth followed. Independent of origin, whelks grew more on the sheltered shore. By contrast, growth rates for snails from exposed and protected shores were similar when reared under uniform conditions in the laboratory. Together these findings suggest that the variation observed in nature does not represent genetic differentiation, but reflects the influence of proximal factors that depress growth on wave-swept shores. Growth rates of juveniles from exposed and protected shores maintained in the laboratory on a diet of an overabundance of (1) barnacles, (2) mussels, (3) both, and (4) both, but only 67% of the time, indicated that prey type and foraging time affect growth. Whelks grew best on a diet of mussels, either singly or in combination with barnacles, grew less on barnacles alone, and least when foraging time was restricted. Because growth rates on specific prey in the laboratory were opposite the observed trend in nature, variation in prey across the exposure gradient cannot be invoked to account for the difference in growth between N. lapillus from exposed and protected shores. The slower growth rates when foraging time was restricted are consistent with the notion that wave energies on exposed coasts depress growth by limiting foraging time or by reducing foraging efficiency.

Ecological speciation probably plays a more prominent role in diversification than previously thought, particularly in marine ecosystems where dispersal potential is great and where few obvious barriers to gene flow exist. This may be especially true in the deep sea where allopatric speciation seems insufficient to account for the rich and largely endemic fauna. Ecologically driven population differentiation and speciation are likely to be most prevalent along environmental gradients, such as those attending changes in depth. We quantified patterns of genetic variation along a depth gradient (1600-3800m) in the western North Atlantic for a protobranch bivalve ( Nuculaatacellana ) to test for population divergence. Multilocus analyses indicated a sharp discontinuity across a narrow depth range, with extremely low gene flow inferred between shallow and deep populations for thousands of generations. Phylogeographical discordance occurred between nuclear and mitochondrial loci as might be expected during the early stages of species formation. Because the geographic distance between divergent populations is small and no obvious dispersal barriers exist in this region, we suggest the divergence might reflect ecologically driven selection mediated by environmental correlates of the depth gradient. As inferred for numerous shallow-water species, environmental gradients that parallel changes in depth may play a key role in the genesis and adaptive radiation of the deep-water fauna.

The evolutionary processes that have generated the rich and highly endemic deep-sea benthic invertebrate fauna remain largely unstudied. Patterns of geographic variation constitute the most basic and essential information for understanding speciation and adaptive radiation. Here we present a multivariate analysis of phenotypic distance to quantify geographic variation in shell form among populations of eight deep-sea gastropod species distributed along a depth gradient in the western North Atlantic. Our primary aim is to identify regions within the deep sea that may promote population differentiation. The degree of interpopulation divergence is highest at the shelf-slope transition (200 m), and then decreases dramatically with increasing depth across the bathyal region (200–4000 m) to the abyssal plain (>4000 m). Phenotypic change parallels faunal change along the depth gradient, suggesting that the selective regime becomes more uniform with increasing depth. Results indicate that the potential for gastropod radiation within the deep-sea environment (>200 m) varies geographically and is highest in the narrow upper bathyal region.

Benthomangelia antonia and Benthonella tenella are the most abundant benthic gastropod species living at continental rise and abyssal depths south of New England, and are widely distributed in the deep sea of the Atlantic. Both species have planktotrophic development with ontogenetic vertical migration and the potential for large-scale dispersal. A multivariate analysis of shell form in the two species revealed only weak population differentiationon bathymetric scales of about a thousand meters and horizontal separation of hundreds of kilometers in the North American Basin. The degree of differentiation is considerably less than that observed in upper bathyal and coastal snails on much smaller spatial scales. Population differentiation in deep-dwelling snails like B. antonia and B. tenella may be constrained by both their potential for gene flow and the more spatially uniform selective regime at great depths. Lower bathyal and especially abyssal regions may not be as conducive to population differentiation in deep-sea snails as the continental slope.

Extensive boxcore sampling in the Atlantic Continental Slope and Rise study permitted the first precise measurement of gastropod density in the bathyal region of the deep sea. Gastropod density decreases significantly and exponentially with depth (250–3494 m), and density-depth regression lines do not differ significantly in either slope or elevatiob over horizontal scales of approximately 1000 km. The subclasses Prosobranchia and Opisthobranchia both show significant decreases in density with depth. Predatory taxa (neogastropods and opisthobranchs) exhibit significantly steeper declines in density with depth than do taxa dominated by deposit feeders (archaeogastropods and mesogastropods). Members of upper trophic levels may be more sensitive to the reduction in nutrient input with increased depth because of the energy loss between trophic levels in the food chain. A comparison of density estimates of gastropods from boxcore, grab and anchor-dredge samples taken in the same region revealed no significant differences in density-depth relationships among the sampling methods. A synthesis of data from 777 boxcore samples collected from the Atlantic, Caribbean and Pacific over a depth range of 250–7298 m indicates that the decline in gastropod density with depth is a global trend with only moderate inter-regional variation.

Histidine-rich Glycoprotein (HRG) is a metal-binding protein described from the blood plasma of a pteriomorph bivalve, the marine mussel Mytilus edulis L. We demonstrate here, using Cd-Immobilized Metal Affinity Chromatography (IMAC), SDS-PAGE, Western Blotting, and ELISA, that HRG is present in three additional pteriomorphs and two heterodont bivalves. ELISA indicates that HRG is the predominant blood plasma protein in all six species (41 to 61% of total plasma proteins by weight). Thus, HRG appears to be a widespread metal-binding protein in the plasma of bivalves.

The deep-sea soft-sediment environment hosts a diverse and highly endemic fauna of uncertain origin. We know little about how this fauna evolved because geographic patterns of genetic variation, the essential information for inferring patterns of population differentiation and speciation are poorly understood. Using formalin-fixed specimens from archival collections, we quantify patterns of genetic variation in the protobranch bivalve Deminucula atacellana, a species widespread throughout the Atlantic Ocean at bathyal and abyssal depths. Samples were taken from 18 localities in the North American, West European and Argentine basins. A hypervariable region of mitochondrial 16S rDNA was amplified by polymerase chain reaction (PCR) and sequenced from 130 individuals revealing 21 haplotypes. Except for several important exceptions, haplotypes are unique to each basin. Overall gene diversity is high (h = 0.73) with pronounced population structure (Phi(ST) = 0.877) and highly significant geographic associations (P0.0001). Sequences cluster into four major clades corresponding to differences in geography and depth. Genetic divergence was much greater among populations at different depths within the same basin, than among those at similar depths but separated by thousands of kilometres. Isolation by distance probably explains much of the interbasin variation. Depth-related divergence may reflect historical patterns of colonization or strong environmental selective gradients. Broadly distributed deep-sea organisms can possess highly genetically divergent populations, despite the lack of any morphological divergence.

The deep sea is the largest ecosystem on Earth. Recent exploration has revealed that it supports a highly diverse and endemic benthic invertebrate fauna, yet the evolutionary processes that generate this remarkable species richness are virtually unknown. Environmental heterogeneity, topographic complexity, and morphological divergence all tend to decrease with depth, suggesting that the potential for population differentiation may decrease with depth. To test this hypothesis, we use mitochondrial DNA (16S rRNA gene) to examine patterns of population differentiation in four species of protobranch bivalves (Nuculoma similis, Deminucula atacellana, Malletia abyssorum, and Ledella ultima) distributed along a depth gradient in the western North Atlantic. We sequenced 268 individuals from formalin-fixed samples and found 45 haplotypes. The level of sequence divergence among haplotypes within species was similar, but shifted from between populations at bathyal depths to within populations at abyssal depths. Levels of population structure as measured by phiST were considerably greater in the upper bathyal species (N. similis = 0.755 and D. atacellana = 0.931; 530-3834 m) than in the lower bathyal/abyssal species (M. abyssorum = 0.071 and L. ultima = 0.045; 2864-4970 m). Pairwise genetic distances among the samples within each species also decreased with depth. Population trees (UPGMA) based on modified coancestry coefficients and nested clade analysis both indicated strong population-level divergence in the two upper bathyal species but little for the deeper species. The population genetic structure in these protobranch bivalves parallels depth-related morphological divergence observed in deep-sea gastropods. The higher level of genetic and morphological divergence, coupled with the strong biotic and abiotic heterogeneity at bathyal depths, suggests this region may be an active area of species formation. We suggest that the steep, topographically complex, and dynamic bathyal zone, which stretches as a narrow band along continental margins, plays a more important role in the evolutionary radiation of the deep-sea fauna than the much more extensive abyss.

Bathymetric gradients of biodiversity in the deep-sea benthos constitute a major class of large-scale biogeographic phenomena. They are typically portrayed and interpreted as variation in alpha diversity (the number of species recovered in individual samples) along depth transects. Here, we examine the depth ranges of deep-sea gastropods and bivalves in the eastern and western North Atlantic. This approach shows that the abyssal molluscan fauna largely represents deeper range extensions for a subset of bathyal species. Most abyssal species have larval dispersal, and adults live at densities that appear to be too low for successful reproduction. These patterns suggest a new explanation for abyssal biodiversity. For many species, bathyal and abyssal populations may form a source-sink system in which abyssal populations are regulated by a balance between chronic extinction arising from vulnerabilities to Allee effects and immigration from bathyal sources. An increased significance of source-sink dynamics with depth may be driven by the exponential decrease in organic carbon flux to the benthos with increasing depth and distance from productive coastal systems. The abyss, which is the largest marine benthic environment, may afford more limited ecological and evolutionary opportunity than the bathyal zone.

Temporal and spatial patterns of phenotypic variation have traditionally been thought to reflect genetic differentiation produced by natural selection. Recently, however, there has been growing interest in how natural selection may shape the genetics of phenotypic plasticity to produce patterns of geographic variation and phenotypic evolution. Because the covariance between genetic and environmental influences can modulate the expression of phenotypic variation, a complete understanding of geographic variation requires determining whether these influences covary in the same (cogradient variation) or in opposing (countergradient variation) directions. We focus on marine snails from rocky intertidal shores as an ideal system to explore how genetic and plastic influences contribute to geographic and historical patterns of phenotypic variation. Phenotypic plasticity in response to predator cues, wave action, and water temperature appear to exert a strong influence on small and large-scale morphological variation in marine snails. In particular, plasticity in snail shell thickness: (i) may contribute to phenotypic evolution, (ii) appears to have evolved across small and large spatial scales, and (iii) may be driven by life history trade-offs tied to architectural constraints imposed by the shell. The plasticity exhibited by these snails represents an important adaptive strategy to the pronounced heterogeneity of the intertidal zone and undoubtedly has played a key role in their evolution.

The shift to smaller body size in marine invertebrates at the deep-sea threshold and size-depth clines within the deep-sea ecosystem are global biogeographic phenomena that remain poorly understood. We present the first standardized measurements of larval and adult size among ecologically and phylogenetically similar species across a broad and continuous depth range, using the largest family of deep-sea gastropods (the Turridae). Size at all life stages increases significantly with depth from the upper bathyal region to the abyssal plain. These consistent clines may result from selection favoring larger size at greater depths because of its metabolic and competitive advantages. The unusually small size of deep-sea mollusks, in general, may represent an independent evolutionary process that favors invasion by inshore taxa composed of small organisms.

The ecological theory of species interactions rests largely on the competition and predatorprey models of Lotka, Volterra, Nicholson, and Gause (e.g., May 1973). These models neglect spatial structure in general, and patchiness in particular. In this paper we introduce cellular automata (CA) as a new class of models for population interactions in space. We will discuss the relations between CA models and the more familiar reaction-diffusion and patch-occupancy formulations, and compare the results of a simple CA competition model to the corresponding Markov chain patch-occupancy model. This comparison reveals some of the factors that determine when simple patch-occupancy models are successful approximations, and when spatially explicit CA models are more appropriate.