Michael A. Rex

Global Patterns and Predictions of Seafloor Biomass Using Random Forests

A comprehensive seafloor biomass and abundance database has been constructed from 24 oceanographic institutions worldwide within the Census of Marine Life (CoML) field projects. The machine-learning algorithm, Random Forests, was employed to model and predict seafloor standing stocks from surface primary production, water-column integrated and export particulate organic matter (POM), seafloor relief, and bottom water properties. The predictive models explain 63% to 88% of stock variance among the major size groups. Individual and composite maps of predicted global seafloor biomass and abundance are generated for bacteria, meiofauna, macrofauna, and megafauna (invertebrates and fishes). Patterns of benthic standing stocks were positive functions of surface primary production and delivery of the particulate organic carbon (POC) flux to the seafloor. At a regional scale, the census maps illustrate that integrated biomass is highest at the poles, on continental margins associated with coastal upwelling and with broad zones associated with equatorial divergence. Lowest values are consistently encountered on the central abyssal plains of major ocean basins The shift of biomass dominance groups with depth is shown to be affected by the decrease in average body size rather than abundance, presumably due to decrease in quantity and quality of food supply. This biomass census and associated maps are vital components of mechanistic deep-sea food web models and global carbon cycling, and as such provide fundamental information that can be incorporated into evidence-based management.

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 α 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.

Deep-Sea Species Diversity: Decreased Gastropod Diversity at Abyssal Depths

Gastropod species diversity is low on the continental shelf, high on the continental slope and abyssal rise, and then decreases with increasing distance out onto the abyssal plain. Increased diversity below the continental shelf has been attributed to increased environmental stability. Decreased diversity on the abyss may result from extremely low productivity.

LARGE-SCALE BIOGEOGRAPHIC PATTERNS IN MARINE MOLLUSKS: A CONFLUENCE OF HISTORY AND PRODUCTIVITY?

Large-scale biogeographic patterns in marine systems are considerably less well documented and understood than those in terrestrial systems. Here, we synthesize recent evidence on latitudinal and bathymetric gradients of species diversity in benthic mollusks, one of the most diverse and intensively studied marine taxa. Latitudinal gradients in coastal faunas show poleward declines in diversity, but the patterns are highly asymmetrical between hemispheres, and irregular both within and among regions. The extensive fossil record of mollusks reveals that latitudinal gradients have become steeper during the Neogene, partly because of a rapid diversification in tropical coral reefs and their associated biotas. Much of the inter-regional variation in contemporary latitudinal trends depends on the longitudinal distribution of reefs and major Neogene vicariant events. Thus, coastal faunas reveal a strong evolutionary–historical legacy. Bathymetric and latitudinal gradients in the deep ocean suggest that molluscan diversity is a function of the rate of nutrient input from surface production. Diversity may be depressed at abyssal depths because of extremely low rates of organic carbon flux, and at upper bathyal depths and high latitudes by pulsed nutrient loading. While the deep-sea environment is not conducive to fossilization, relationships between local and regional diversity, and the distribution and age of higher taxa indicate an evolutionary signal in present-day diversity gradients. Marine invertebrate communities offer tremendous potential to determine the relative importance of history and ecological opportunity in shaping large-scale patterns of species diversity.

POPULATION DIFFERENTIATION DECREASES WITH DEPTH IN DEEP-SEA BIVALVES

Abstract 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 differentiationin four species of protobranch bivalves (Nuculoma similis, Deminucula atacellana, Malletia abyssorum, and Ledellaultima) distributed along a depth gradient in the western North Atlantic. We sequenced 268 individuals from formalinfixed 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 ST 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 heterogeneityal 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.

Biotic and Human Vulnerability to Projected Changes in Ocean Biogeochemistry over the 21st Century

Mora and colleagues show that ongoing greenhouse gas emissions are likely to have a considerable effect on several biogeochemical properties of the worlds oceans, with potentially serious consequences for biodiversity and human welfare.

Bathymetric patterns of body size: implications for deep-sea biodiversity

Abstract 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.

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 (ΦST = 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.

Population differentiation decreases with depth in deep-sea gastropods

Abstract 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.

A genetic dimension to deep-sea biodiversity

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.