Highly structured populations of copepods at risk to deep-sea mining: Integration of genomic data with demogenetic and biophysical modelling.

Copepoda is the most abundant taxon in deep-sea hydrothermal vents, where hard substrate is available. Despite the increasing interest in seafloor massive sulphides exploitation, there have been no population genomic studies conducted on vent meiofauna, which are known to contribute over 50% to metazoan biodiversity at vents. To bridge this knowledge gap, restriction-site-associated DNA sequencing, specifically 2b-RADseq, was used to retrieve thousands of genome-wide single-nucleotide polymorphisms (SNPs) from abundant populations of the vent-obligate copepod Stygiopontius lauensis from the Lau Basin. SNPs were used to investigate population structure, demographic histories and genotype-environment associations at a basin scale. Genetic analyses also helped to evaluate the suitability of tailored larval dispersal models and the parameterization of life-history traits that better fit the population patterns observed in the genomic dataset for the target organism. Highly structured populations were observed on both spatial and temporal scales, with divergence of populations between the north, mid, and south of the basin estimated to have occurred after the creation of the major transform fault dividing the Australian and the Niuafo'ou tectonic plate (350 kya), with relatively recent secondary contact events (<20 kya). Larval dispersal models were able to predict the high levels of structure and the highly asymmetric northward low-level gene flow observed in the genomic data. These results differ from most studies conducted on megafauna in the region, elucidating the need to incorporate smaller size when considering site prospecting for deep-sea exploitation of seafloor massive sulphides, and the creation of area-based management tools to protect areas at risk of local extinction, should mining occur.

Endosymbionts escape dead hydrothermal vent tubeworms to enrich the free-living population.

Theory predicts that horizontal acquisition of symbionts by plants and animals must be coupled to release and limited dispersal of symbionts for intergenerational persistence of mutualisms. For deep-sea hydrothermal vent tubeworms (Vestimentifera, Siboglinidae), it has been demonstrated that a few symbiotic bacteria infect aposymbiotic host larvae and grow in a newly formed organ, the trophosome. However, whether viable symbionts can be released to augment environmental populations has been doubtful, because (i) the adult worms lack obvious openings and (ii) the vast majority of symbionts has been regarded as terminally differentiated. Here we show experimentally that symbionts rapidly escape their hosts upon death and recruit to surfaces where they proliferate. Estimating symbiont release from our experiments taken together with well-known tubeworm density ranges, we suggest a few million to 1.5 billion symbionts seeding the environment upon death of a tubeworm clump. In situ observations show that such clumps have rapid turnover, suggesting that release of large numbers of symbionts may ensure effective dispersal to new sites followed by active larval colonization. Moreover, release of symbionts might enable adaptations that evolve within host individuals to spread within host populations and possibly to new environments.

Highly structured populations of deep-sea copepods associated with hydrothermal vents across the Southwest Pacific, despite contrasting life history traits.

Hydrothermal vents are extreme environments, where abundant communities of copepods with contrasting life history traits co-exist along hydrothermal gradients. Here, we discuss how these traits may contribute to the observed differences in molecular diversity and population genetic structure. Samples were collected from vent locations across the globe including active ridges and back-arc basins and compared to existing deep-sea hydrothermal vent and shallow water data, covering a total of 22 vents and 3 non-vent sites. A total of 806 sequences of mtDNA from the Cox1 gene were used to reconstruct the phylogeny, haplotypic relationship and demography within vent endemic copepods (Dirivultidae, Stygiopontius spp.) and non-vent-endemic copepods (Ameiridae, Miraciidae and Laophontidae). A species complex within Stygiopontius lauensis was studied across five pacific back-arc basins at eight hydrothermal vent fields, with cryptic species being restricted to the basins they were sampled from. Copepod populations from the Lau, North Fiji and Woodlark basins are undergoing demographic expansion, possibly linked to an increase in hydrothermal activity in the last 10 kya. Highly structured populations of Amphiascus aff. varians 2 were also observed from the Lau to the Woodlark basins with populations also undergoing expansion. Less abundant harpacticoids exhibit little to no population structure and stable populations. This study suggests that similarities in genetic structure and demography may arise in vent-associated copepods despite having different life history traits. As structured meta-populations may be at risk of local extinction should major anthropogenic impacts, such as deep-sea mining, occur, we highlight the importance of incorporating a trait-based approach to investigate patterns of genetic connectivity and demography, particularly regarding area-based management tools and environmental management plans.

Restoration experiments in polymetallic nodule areas.

Deep-seabed polymetallic nodule mining can have multiple adverse effects on benthic communities, such as permanent loss of habitat by removal of nodules and habitat modification of sediments. One tool to manage biodiversity risks is the mitigation hierarchy, including avoidance, minimization of impacts, rehabilitation and/or restoration, and offset. We initiated long-term restoration experiments at sites in polymetallic nodule exploration contract areas in the Clarion-Clipperton Zone that were (i) cleared of nodules by a preprototype mining vehicle, (ii) disturbed by dredge or sledge, (iii) undisturbed, and (iv) naturally devoid of nodules. To accommodate for habitat loss, we deployed >2000 artificial ceramic nodules to study the possible effect of substrate provision on the recovery of biota and its impact on sediment biogeochemistry. Seventy-five nodules were recovered after eight weeks and had not been colonized by any sessile epifauna. All other nodules will remain on the seafloor for several years before recovery. Furthermore, to account for habitat modification of the top sediment layer, sediment in an epibenthic sledge track was loosened by a metal rake to test the feasibility of sediment decompaction to facilitate soft-sediment recovery. Analyses of granulometry and nutrients one month after sediment decompaction revealed that sand fractions are proportionally lower within the decompacted samples, whereas total organic carbon values are higher. Considering the slow natural recovery rates of deep-sea communities, these experiments represent the beginning of a ~30-year study during which we expect to gain insights into the nature and timing of the development of hard-substrate communities and the influence of nodules on the recovery of disturbed sediment communities. Results will help us understand adverse long-term effects of nodule removal, providing an evidence base for setting criteria for the definition of "serious harm" to the environment. Furthermore, accompanying research is needed to define a robust ecosystem baseline in order to effectively identify restoration success. Integr Environ Assess Manag 2022;18:682-696. © 2021 The Authors. Integrated Environmental Assessment and Management published by Wiley Periodicals LLC on behalf of Society of Environmental Toxicology & Chemistry (SETAC).

Deep-Sea Misconceptions Cause Underestimation of Seabed-Mining Impacts.

Scientific misconceptions are likely leading to miscalculations of the environmental impacts of deep-seabed mining. These result from underestimating mining footprints relative to habitats targeted and poor understanding of the sensitivity, biodiversity, and dynamics of deep-sea ecosystems. Addressing these misconceptions and knowledge gaps is needed for effective management of deep-seabed mining.

Resilience of benthic deep-sea fauna to mining activities.

With increasing demand for mineral resources, extraction of polymetallic sulphides at hydrothermal vents, cobalt-rich ferromanganese crusts at seamounts, and polymetallic nodules on abyssal plains may be imminent. Here, we shortly introduce ecosystem characteristics of mining areas, report on recent mining developments, and identify potential stress and disturbances created by mining. We analyze species' potential resistance to future mining and perform meta-analyses on population density and diversity recovery after disturbances most similar to mining: volcanic eruptions at vents, fisheries on seamounts, and experiments that mimic nodule mining on abyssal plains. We report wide variation in recovery rates among taxa, size, and mobility of fauna. While densities and diversities of some taxa can recover to or even exceed pre-disturbance levels, community composition remains affected after decades. The loss of hard substrata or alteration of substrata composition may cause substantial community shifts that persist over geological timescales at mined sites.

Mitochondrial DNA Analyses Indicate High Diversity, Expansive Population Growth and High Genetic Connectivity of Vent Copepods (Dirivultidae) across Different Oceans.

Communities in spatially fragmented deep-sea hydrothermal vents rich in polymetallic sulfides could soon face major disturbance events due to deep-sea mineral mining, such that unraveling patterns of gene flow between hydrothermal vent populations will be an important step in the development of conservation policies. Indeed, the time required by deep-sea populations to recover following habitat perturbations depends both on the direction of gene flow and the number of migrants available for re-colonization after disturbance. In this study we compare nine dirivultid copepod species across various geological settings. We analyze partial nucleotide sequences of the mtCOI gene and use divergence estimates (FST) and haplotype networks to infer intraspecific population connectivity between vent sites. Furthermore, we evaluate contrasting scenarios of demographic population expansion/decline versus constant population size (using, for example, Tajima's D). Our results indicate high diversity, population expansion and high connectivity of all copepod populations in all oceans. For example, haplotype diversity values range from 0.89 to 1 and FST values range from 0.001 to 0.11 for Stygiopontius species from the Central Indian Ridge, Mid Atlantic Ridge, East Pacific Rise, and Eastern Lau Spreading Center. We suggest that great abundance and high site occupancy by these species favor high genetic diversity. Two scenarios both showed similarly high connectivity: fast spreading centers with little distance between vent fields and slow spreading centers with greater distance between fields. This unexpected result may be due to some distinct frequency of natural disturbance events, or to aspects of individual life histories that affect realized rates of dispersal. However, our statistical performance analyses showed that at least 100 genomic regions should be sequenced to ensure accurate estimates of migration rate. Our demography parameters demonstrate that dirivultid populations are generally large and continuously undergoing population growth. Benthic and pelagic species abundance data support these findings.

Size matters at deep-sea hydrothermal vents: different diversity and habitat fidelity patterns of meio- and macrofauna.

Species with markedly different sizes interact when sharing the same habitat. Unravelling mechanisms that control diversity thus requires consideration of a range of size classes. We compared patterns of diversity and community structure for meio- and macrofaunal communities sampled along a gradient of environmental stress at deep-sea hydrothermal vents on the East Pacific Rise (9° 50' N) and neighboring basalt habitats. Both meio- and macrofaunal species richnesses were lowest in the high-stress vent habitat, but macrofaunal richness was highest among intermediate-stress vent habitats. Meiofaunal species richness was negatively correlated with stress, and highest on the basalt. In these deep-sea basalt habitats surrounding hydrothermal vents, meiofaunal species richness was consistently higher than that of macrofauna. Consideration of the physiological capabilities and life history traits of different-sized animals suggests that different patterns of diversity may be caused by different capabilities to deal with environmental stress in the 2 size classes. In contrast to meiofauna, adaptations of macrofauna may have evolved to allow them to maintain their physiological homeostasis in a variety of hydrothermal vent habitats and exploit this food-rich deep-sea environment in high abundances. The habitat fidelity patterns also differed: macrofaunal species occurred primarily at vents and were generally restricted to this habitat, but meiofaunal species were distributed more evenly across proximate and distant basalt habitats and were thus not restricted to vent habitats. Over evolutionary time scales these contrasting patterns are likely driven by distinct reproduction strategies and food demands inherent to fauna of different sizes.

Ecology and biogeography of free-living nematodes associated with chemosynthetic environments in the deep sea: a review.

BACKGROUND: Here, insight is provided into the present knowledge on free-living nematodes associated with chemosynthetic environments in the deep sea. It was investigated if the same trends of high standing stock, low diversity, and the dominance of a specialized fauna, as observed for macro-invertebrates, are also present in the nematodes in both vents and seeps. METHODOLOGY: This review is based on existing literature, in combination with integrated analysis of datasets, obtained through the Census of Marine Life program on Biogeography of Deep-Water Chemosynthetic Ecosystems (ChEss). FINDINGS: Nematodes are often thriving in the sulphidic sediments of deep cold seeps, with standing stock values ocassionaly exceeding largely the numbers at background sites. Vents seem not characterized by elevated densities. Both chemosynthetic driven ecosystems are showing low nematode diversity, and high dominance of single species. Genera richness seems inversely correlated to vent and seep fluid emissions, associated with distinct habitat types. Deep-sea cold seeps and hydrothermal vents are, however, highly dissimilar in terms of community composition and dominant taxa. There is no unique affinity of particular nematode taxa with seeps or vents. CONCLUSIONS: It seems that shallow water relatives, rather than typical deep-sea taxa, have successfully colonized the reduced sediments of seeps at large water depth. For vents, the taxonomic similarity with adjacent regular sediments is much higher, supporting rather the importance of local adaptation, than that of long distance distribution. Likely the ephemeral nature of vents, its long distance offshore and the absence of pelagic transport mechanisms, have prevented so far the establishment of a successful and typical vent nematode fauna. Some future perspectives in meiofauna research are provided in order to get a more integrated picture of vent and seep biological processes, including all components of the marine ecosystem.

Advances in taxonomy, ecology, and biogeography of Dirivultidae (copepoda) associated with chemosynthetic environments in the deep sea.

BACKGROUND: Copepoda is one of the most prominent higher taxa with almost 80 described species at deep-sea hydrothermal vents. The unique copepod family Dirivultidae with currently 50 described species is the most species rich invertebrate family at hydrothermal vents. METHODOLOGY/PRINCIPAL FINDINGS: We reviewed the literature of Dirivultidae and provide a complete key to species, and map geographical and habitat specific distribution. In addition we discuss the ecology and origin of this family. CONCLUSIONS/SIGNIFICANCE: Dirivultidae are only present at deep-sea hydrothermal vents and along the axial summit trough of midocean ridges, with the exception of Dirivultus dentaneus found associated with Lamellibrachia species at 1125 m depth off southern California. To our current knowledge Dirivultidae are unknown from shallow-water vents, seeps, whale falls, and wood falls. They are a prominent part of all communities at vents and in certain habitat types (like sulfide chimneys colonized by pompei worms) they are the most abundant animals. They are free-living on hard substrate, mostly found in aggregations of various foundation species (e.g. alvinellids, vestimentiferans, and bivalves). Most dirivultid species colonize more than one habitat type. Dirivultids have a world-wide distribution, but most genera and species are endemic to a single biogeographic region. Their origin is unclear yet, but immigration from other deep-sea chemosynthetic habitats (stepping stone hypothesis) or from the deep-sea sediments seems unlikely, since Dirivultidae are unknown from these environments. Dirivultidae is the most species rich family and thus can be considered the most successful taxon at deep-sea vents.

Diversity of meiofauna from the 9°50'N East Pacific rise across a gradient of hydrothermal fluid emissions.

BACKGROUND: We studied the meiofauna community at deep-sea hydrothermal vents along a gradient of vent fluid emissions in the axial summit trought (AST) of the East Pacific Rise 9°50'N region. The gradient ranged from extreme high temperatures, high sulfide concentrations, and low pH at sulfide chimneys to ambient deep-sea water conditions on bare basalt. We explore meiofauna diversity and abundance, and discuss its possible underlying ecological and evolutionary processes. METHODOLOGY/PRINCIPAL FINDINGS: After sampling in five physico-chemically different habitats, the meiofauna was sorted, counted and classified. Abundances were low at all sites. A total of 52 species were identified at vent habitats. The vent community was dominated by hard substrate generalists that also lived on bare basalt at ambient deep-sea temperature in the axial summit trough (AST generalists). Some vent species were restricted to a specific vent habitat (vent specialists), but others occurred over a wide range of physico-chemical conditions (vent generalists). Additionally, 35 species were only found on cold bare basalt (basalt specialists). At vent sites, species richness and diversity clearly increased with decreasing influence of vent fluid emissions from extreme flow sulfide chimney (no fauna), high flow pompei worm (S: 4-7, H'(loge): 0.11-0.45), vigorous flow tubeworm (S: 8-23; H'(loge): 0.44-2.00) to low flow mussel habitats (S: 28-31; H'(loge): 2.34-2.60). CONCLUSIONS/SIGNIFICANCE: Our data suggest that with increasing temperature and toxic hydrogen sulfide concentrations and increasing amplitude of variation of these factors, fewer species are able to cope with these extreme conditions. This results in less diverse communities in more extreme habitats. The finding of many species being present at sites with and without vent fluid emissions points to a non endemic deep-sea hydrothermal vent meiofaunal community. This is in contrast to a mostly endemic macrofauna but similar to what is known for meiofauna from shallow-water vents.

A new species of deep-sea Tegastidae (Crustacea: Copepoda: Harpacticoida) from 9°50'N on the East Pacific Rise, with remarks on its ecology.

Both male and female of the new deep-sea species Smacigastes barti sp. nov. (Tegastidae, Sars) are described in detail. Copepoda is one of the most diversified taxa at deep-sea hydrothermal vents, but only one species of the family Tegastidae has been described from this habitat and other deep-sea environments. Smacigastes barti is the second species of the genus SmacigastesIvanenko & Defaye, 2004, and was found in artificial substrates deployed in the vicinity of and 0.5 m from tubeworm aggregations at the 9°50'N region on the East Pacific Rise at 2500 meters depth. The derived character states of the new species are the lack of coxal endites on the maxilla, and 2-segmented exopods of swimming legs 2 and 3, the latter being the result of the fusion of the 2 proximal segments. An identification key to all known genera of Tegastidae is provided. Interestingly, the distribution of S. barti showed that it does not tolerate elevated temperatures and/or the presence of hydrogen sulfide or oxygen fluctuations, although both species of this genus were found in deep-sea chemosynthetic environments.