Transition probabilities help identify putative drivers of community change in complex systems.

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.

Long-term declines in an intertidal foundation species parallel shifts in community composition.

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.

A synthesis of genetic connectivity in deep-sea fauna and implications for marine reserve design.

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.

Into the deep: a phylogenetic approach to the bivalve subclass Protobranchia.

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.

Phylogeography of a pan-Atlantic abyssal protobranch bivalve: implications for evolution in the Deep Atlantic.

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), but much less is known about evolution in the more extensive abyssal regions (>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.

Shading facilitates sessile invertebrate dominance in the rocky subtidal Gulf of Maine.

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.

A strategy for the conservation of biodiversity on mid-ocean ridges from 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.

Population differentiation decreases with depth in deep-sea bivalves.

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.

A source-sink hypothesis for abyssal biodiversity.

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.

Population differentiation and species formation in the deep sea: the potential role of environmental gradients and depth.

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.

Elemental fingerprinting of mussel shells to predict population sources and redistribution potential in the Gulf of Maine.

As the climate warms, species that cannot tolerate changing conditions will only persist if they undergo range shifts. Redistribution ability may be particularly variable for benthic marine species that disperse as pelagic larvae in ocean currents. The blue mussel, Mytilus edulis, has recently experienced a warming-related range contraction in the southeastern USA and may face limitations to northward range shifts within the Gulf of Maine where dominant coastal currents flow southward. Thus, blue mussels might be especially vulnerable to warming, and understanding dispersal patterns is crucial given the species' relatively long planktonic larval period (>1 month). To determine whether trace elemental "fingerprints" incorporated in mussel shells could be used to identify population sources (i.e. collection locations), we assessed the geographic variation in shell chemistry of blue mussels collected from seven populations between Cape Cod, Massachusetts and northern Maine. Across this ∼500 km of coastline, we were able to successfully predict population sources for over two-thirds of juvenile individuals, with almost 80% of juveniles classified within one site of their collection location and 97% correctly classified to region. These results indicate that significant differences in elemental signatures of mussel shells exist between open-coast sites separated by ∼50 km throughout the Gulf of Maine. Our findings suggest that elemental "fingerprinting" is a promising approach for predicting redistribution potential of the blue mussel, an ecologically and economically important species in the region.

Bathymetric and geographic population structure in the pan-Atlantic deep-sea bivalve Deminucula atacellana (Schenck, 1939).

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 (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.

PHYSIOLOGICAL STRESS AND COLOR POLYMORPHISM IN THE INTERTIDAL SNAIL NUCELLA LAPILLUS.

The intertidal snail Nucella lapillus exhibits considerable variation in shell color both within and between populations differentially exposed to wave action. Populations from high-wave-energy shores tended to be highly polymorphic and were dominated by pigmented morphs (especially brown), while those at more sheltered locations exhibited less polymorphism and were predominantly white. Field and laboratory experiments were conducted to determine the role of physiological stress and selective predation in maintaining the observed distribution of color morphs. The results demonstrated that 1) physiological stress from high temperature and desiccation during periods of tidal emersion was greater on protected shores, 2) under similar natural conditions, brown morphs heated up faster, attained higher temperatures, desiccated more rapidly, and suffered greater mortality than did white morphs, and 3) when pairs of brown and white morphs were tethered intertidally there was virtually no mortality of either morph on the exposed shore or in shaded microhabitats on the protected shore, but brown morphs suffered much greater mortality in sunny microhabitats on the protected shore. These findings demonstrate that the interpopulation variation in shell color of N. lapillus is in part a response to a selective gradient in physiological stress. Selection for crypsis by visually hunting predators did not appear to play a prominent role; however, only adults were considered, and the predation experiments were conducted in the fall before shorebirds that prey on whelks had arrived from their summer feeding grounds. Further experimentation to quantify the effects of visual predators such as birds and fish, particularly on juvenile snails, is necessary to assess adequately the importance of predation.

ASYMMETRICAL DEVELOPMENTAL PLASTICITY IN AN INTERTIDAL SNAIL.

Field and laboratory experiments were used to investigate the variation and phenotypic plasticity in the adhesive abilities of the intertidal snail Nucella lapillus between high- and low-wave-energy environments. Whelks from an exposed coast produced a larger pedal surface area and were more resistant to dislodgement than were similar-sized individuals from a protected shore. Tenacity (g/cm2 ) was similar between individuals from exposed and protected shores, indicating that variation in resisting dislodgement was solely a function of pedal surface area. Whelks from exposed and protected shores did not differ in pedal surface area as they emerged from egg capsules or when reared in the laboratory under uniform conditions, suggesting that variation between populations does not represent genetic differentiation. Individuals from high-and low-wave-energy environments reared intertidally produced a larger pedal surface area than did those reared in the laboratory. The extent to which pedal surface area increased corresponded to the intensity of wave action. These findings suggest that pedal surface area is a highly plastic character modulated or induced by the water turbulence accompanying breaking waves. A reciprocal-transplant experiment confirmed this notion but revealed an asymmetry in the plasticity. Snails from the protected site transplanted to an exposed shore formed a much larger pedal surface area than did controls reared on the protected shore. In contrast, whelks from a wave-swept shore transplanted to a protected shore differed little from their controls reared on the exposed shore. The asymmetric response parallels a possible asymmetry in the risks of acclimating to a temporally unpredictable environmental cue, such as wave action.

The relationship between regional and local species diversity in marine benthic communities: a global perspective.

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 degrees S to 63 degrees 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.

BATHYMETRIC PATTERNS OF BODY SIZE IN DEEP-SEA GASTROPODS.

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.