Lisa A. Levin

Recent progress in understanding larval dispersal: new directions and digressions

Larvae have been difficult to study because their small size limits our ability to understand their behavior and the conditions they experience. Questions about larval transport focus largely on (a) where they go [dispersal] and (b) where they come from [connectivity]. Mechanisms of transport have been intensively studied in recent decades. As our ability to identify larval sources develops, the consequences of connectivity are garnering more consideration. Attention to transport and connectivity issues has increased dramatically in the past decade, fueled by changing motivations that now include management of fisheries resources, understanding of the spread of invasive species, conservation through the design of marine reserves, and prediction of climate-change effects. Current progress involves both technological advances and the integration of disciplines and approaches. This review focuses on insights gained from physical modeling, chemical tracking, and genetic approaches. I consider how new findings are motivating paradigm shifts concerning (1) life-history consequences; (2) the openness of marine populations, self-recruitment, and population connectivity; (3) the role of behavior; and (4) the significance of variability in space and time. A challenge for the future will be to integrate methods that address dispersal on short (intragenerational) timescales such as elemental fingerprinting and numerical simulations with those that reflect longer timescales such as gene flow estimates and demographic modeling. Recognition and treatment of the continuum between ecological and evolutionary timescales will be necessary to advance the mechanistic understanding of larval and population dynamics.

ECOLOGY OF COLD SEEP SEDIMENTS: INTERACTIONS OF FAUNA WITH FLOW, CHEMISTRY AND MICROBES

Cold seeps occur in geologically active and passive continental margins, where pore waters enriched in methane are forced upward through the sediments by pressure gradients. The advective supply of methane leads to dense microbial communities with high metabolic rates. Anaerobic methane oxidation presumably coupled to sulphate reduction facilitates formation of carbonates and, in many places, generates extremely high concentrations of hydrogen sulphide in pore waters. Increased food supply, availability of hard substratum and high concentrations of methane and sulphide supplied to free-living and symbiotic bacteria provide the basis for the complex ecosystems found at these sites. This review examines the structures of animal communities in seep sediments and how they are shaped by hydrologic, geochemical and microbial processes. The full size range of biota is addressed but emphasis is on the mid-size sediment-dwelling infauna (foraminiferans, metazoan meiofauna and macrofauna), which have received less attention than megafauna or microbes. Megafaunal biomass at seeps, which far exceeds that of surrounding non-seep sediments, is dominated by bivalves (mytilids, vesicomyids, lucinids and thyasirids) and vestimentiferan tube worms, with pogonophorans, cladorhizid sponges, gastropods and shrimp sometimes abundant. In contrast, seep sediments at shelf and upper slope depths have infaunal densities that often differ very little from those in ambient sediments. At greater depths, seep infauna exhibit enhanced densities, modified composition and reduced diversity relative to background sediments. Dorvilleid, hesionid and ampharetid polychaetes, nematodes, and calcareous foraminiferans are dominant. There is extensive spatial heterogeneity of microbes and higher organisms at seeps. Specialized infaunal communities are associated with different seep habitats (microbial mats, clam beds, mussel beds and tube worms aggregations) and with different vertical zones in the sediment. Whereas fluid flow and associated porewater properties, in particular sulphide concentration, appear to regulate the distribution, physiological adaptations and sometimes behaviour of many seep biota, sometimes the reverse is true. Animal-microbe interactions at seeps are complex and involve symbioses, heterotrophic nutrition, geochemical feedbacks and habitat structure. Nutrition of seep fauna varies, with thiotrophic and methanotrophic symbiotic bacteria fueling most of the megafaunal forms but macrofauna and most meiofauna are mainly heterotrophic. Macrofaunal food sources are largely photosynthesis-based at shallower seeps but reflect carbon fixation by chemosynthesis and considerable incorporation of methane-derived C at deeper seeps. Export of seep carbon appears to be highly localized based on limited studies in the Gulf of Mexico. Seep ecosystems remain one of the oceans true frontiers. Seep sediments represent some of the most extreme marine conditions and offer unbounded opportunities for discovery in the realms of animal-microbe-geochemical interactions, physiology, trophic ecology, biogeography, system-atics and evolution.

Man and the Last Great Wilderness: Human Impact on the Deep Sea

The deep sea, the largest ecosystem on Earth and one of the least studied, harbours high biodiversity and provides a wealth of resources. Although humans have used the oceans for millennia, technological developments now allow exploitation of fisheries resources, hydrocarbons and minerals below 2000 m depth. The remoteness of the deep seafloor has promoted the disposal of residues and litter. Ocean acidification and climate change now bring a new dimension of global effects. Thus the challenges facing the deep sea are large and accelerating, providing a new imperative for the science community, industry and national and international organizations to work together to develop successful exploitation management and conservation of the deep-sea ecosystem. This paper provides scientific expert judgement and a semi-quantitative analysis of past, present and future impacts of human-related activities on global deep-sea habitats within three categories: disposal, exploitation and climate change. The analysis is the result of a Census of Marine Life – SYNDEEP workshop (September 2008). A detailed review of known impacts and their effects is provided. The analysis shows how, in recent decades, the most significant anthropogenic activities that affect the deep sea have evolved from mainly disposal (past) to exploitation (present). We predict that from now and into the future, increases in atmospheric CO2 and facets and consequences of climate change will have the most impact on deep-sea habitats and their fauna. Synergies between different anthropogenic pressures and associated effects are discussed, indicating that most synergies are related to increased atmospheric CO2 and climate change effects. We identify deep-sea ecosystems we believe are at higher risk from human impacts in the near future: benthic communities on sedimentary upper slopes, cold-water corals, canyon benthic communities and seamount pelagic and benthic communities. We finalise this review with a short discussion on protection and management methods.

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

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

Rapid subduction of organic matter by maldanid polychaetes on the North Carolina slope

In situ tracer experiments conducted on the North Carolina continental slope reveal that tube-building worms (Polychaeta: Maldanidae) can, without ingestion, rapidly subduct freshly deposited, algal carbon ( 13 C-labeled diatoms) and inorganic materials (slope sediment and glass beads) to depths of 10 cm or more in the sediment column. Transport over 1.5 days appears to be nonselective but spatially patchy, creating localized, deep hotspots. As a result of this transport, relatively fresh organic matter becomes available soon after deposition to deep-dwelling microbes and other infauna, and both aerobic and anaerobic processes may be enhanced. Comparison of tracer subduction with estimates from a diffusive mixing model using 234 Th-based coefficients, suggests that maldanid subduction activities, within 1.5 d of particle deposition, could account for 25-100% of the mixing below 5 cm that occurs on 100-day time scales. Comparisons of community data from the North Carolina slope for different places and times indicate a correlation between the abundance of deep-dwelling maldanids and the abundance and the dwelling depth in the sediment column of other infauna. Pulsed inputs of organic matter occur frequently in margin environments and maldanid polychaetes are a common component of continental slope macrobenthos. Thus, the activities we observe are likely to be widespread and significant for chemical cycling (natural and anthropogenic materials) on the slope. We propose that species like maldanids, that rapidly redistribute labile organic matter within the seabed, probably function as keystone resource modifiers. They may exert a disproportionately strong influence (relative to their abundance) on the structure of infaunal communities and on the timing, location and nature of organic matter diagenesis and burial in continental margin sediments.

Demographic Responses of Estuarine Polychaetes to Pollutants: Life Table Response Experiments

Capitella sp. I and Streblospio benedicti are infaunal, deposit-feeding polychaetes that occur in estuaries and littoral wetlands throughout much of the United States. Life table response experiments (sensu Caswell 1989a) were carried out in the laboratory to compare the demographic responses of these species to three common sources of estuarine contamination or enrichment: sewage (Milorganite), blue-green algae (Spirulina sp.), and hydrocarbons (No. 2 fuel oil). Life table data were used to generate two population projection models (a fully age-classified model and a simple two-stage model) for each species in each treatment and in a salt marsh sediment control. These models were used to quantify the effects of treatments on survival, reproduction, and age at maturity, and hence on population growth rate. For both species, survival was high in all treatments except the blue-green algae treatment, where oxygen depletion (to <1 mL/L) occurred. Treatments had dramatic effects on age at maturity, fertility, and generation time, which differed between species and among contaminants. Population growth rates (X) were higher in Capitella sp. I than in S. benedicti for all treatments, primarily due to earlier maturation and a fertility advantage exhibited by Capitella during the first few weeks of reproduction. In Capitella sp. I, explosive increases in X were seen in the sewage (X = 5.31) and algae (X = 2.81) enrichments relative to the control (X = 1.86) and the hydrocarbon treatments (X = 1.67). Reduced maturation time and increases in age-specific fertility associated with rapid growth and large body size were responsible. Hydrocarbons reduced X primarily through delayed maturation and reduced age-specific fertility. Population growth rates of S. benedicti in the hydrocarbon treatment (X = 1.11) and algae treatment (X = 1.09) were reduced relative to the control (X = 1.46) and sewage treatments (X = 1.41). The hydrocarbon reduction resulted from delayed maturity and reduced fertility, whereas the algal effects were caused by reductions in both juvenile survival and fertility. Our analyses revealed that Capitella sp. Is population growth rate was less sensitive than that of S. benedicti to these three common forms of estuarine contamination, that different sources of organic enrichment (sewage and blue-green algae) introduced at the same C and N levels could have varying demographic effects, and that when two contaminants (hydrocarbons and blue-green algae) caused similar reductions in population growth rate in a species (Streblospio), the underlying mechanisms may have differed. For both species all demographically important effects of contaminants occurred early in life, suggesting a need to focus on juveniles and young adults in field and laboratory testing. The experiments performed here demonstrated the sensitivity of polychaete demo- graphic properties to the condition of estuarine sediments. This sensitivity may be exploited to evaluate organic enrichment and hydrocarbon contamination in field settings.

Complex larval connectivity patterns among marine invertebrate populations

Based on the belief that marine larvae, which can spend days to months in the planktonic stage, could be transported considerable distances by ocean currents, it has long been assumed that populations of coastal species with a planktonic larval stage are demographically open and highly “connected.” Such assumptions about the connectivity of coastal populations govern approaches to managing marine resources and shape our fundamental understanding of population dynamics and evolution, yet are rarely tested directly due to the small size and high mortality of marine larvae in a physically complex environment. Here, we document a successful application of elemental fingerprinting as a tracking tool to determine sources of settled invertebrates and show that coastal mussel larvae, previously thought to be highly dispersed, can be retained within 20–30 km of their natal origin. We compare two closely related and co-occurring species, Mytilus californianus and Mytilus galloprovincialis, and determine that, despite expected similarities, they exhibit substantially different connectivity patterns. Our use of an in situ larval culturing technique overcomes the previous challenge of applying microchemical tracking methods to species with completely planktonic development. The exchange of larvae and resulting connectivities among marine populations have fundamental consequences for the evolution and ecology of species and for the management of coastal resources.

Taking the “Waste” Out of “Wastewater” for Human Water Security and Ecosystem Sustainability

Humans create vast quantities of wastewater through inefficiencies and poor management of water systems. The wasting of water poses sustainability challenges, depletes energy reserves, and undermines human water security and ecosystem health. Here we review emerging approaches for reusing wastewater and minimizing its generation. These complementary options make the most of scarce freshwater resources, serve the varying water needs of both developed and developing countries, and confer a variety of environmental benefits. Their widespread adoption will require changing how freshwater is sourced, used, managed, and priced.

Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas

Previous work has shown that some foraminiferal species thrive in organically enriched, oxygen-depleted environments. Here, we compare ‘live’ (stained) faunas in multicorer samples (0–1 cm layer) obtained at two sites on the Oman margin, one located at 412 m within the oxygen minimum zone (OMZ) (O2=0.13 ml l?1), the other located at 3350 m, well below the main OMZ (O2~3.00 ml l?1). While earlier studies have focused on the hard-shelled (predominantly calcareous) foraminifera, we consider complete stained assemblages, including poorly known, soft-shelled, monothalamous forms. Densities at the 412-m site were much higher (16,107 individuals.10 cm?2 in the >63-m fraction) than at the 3350-m site (625 indiv.10 cm?2). Species richness (E(S100)), diversity (H?, Fishers Alpha index) and evenness (J?) were much lower, and dominance (R1D) was higher, at 412 m compared with 3350 m. At 412 m, small calcareous foraminifera predominated and soft-shelled allogromiids and sacamminids were a minor faunal element. At 3350 m, calcareous individuals were much less common and allogromiids and saccamminids formed a substantial component of the fauna. There were also strong contrasts between the foraminiferal macrofauna (>300-m fraction) at these two sites; relatively small species of Bathysiphon, Globobulimina and Lagenammina dominated at 412 m, very large, tubular, agglutinated species of Bathysiphon, Hyperammina, Rhabdammina and Saccorhiza were important at 3350 m. Our observations suggest that, because they contain fewer soft-shelled and agglutinated foraminifera, a smaller proportion of bathyal, low-oxygen faunas is lost during fossilization compared to faunas from well-oxygenated environments. Trends among foraminifera (>63 m fraction) in the Santa Barbara Basin (590 and 610 m depth; O2=0.05 and 0.15 ml l?1 respectively), and macrofaunal foraminifera (>300 m) on the Peru margin (300–1250 m depth; O2=0.02–1.60 ml l?1), matched those observed on the Oman margin. In particular, soft-shelled monothalamous taxa were rare and large agglutinated taxa were absent in the most oxygen-depleted ( Foraminifera often outnumber metazoans (both meiofaunal and macrofaunal) in bathyal oxygen-depleted settings. However, although phylogenetically distant, foraminifera and metazoans exhibit similar population responses to oxygen depletion; species diversity decreases, dominance increases, and the relative abundance of the major taxa changes. The foraminiferal macrofauna (>300 m) were 5 times more abundant than the metazoan macrofauna at 412 m on the Oman margin but 16 times more abundant at the 3350 m site. Among the meiofauna (63–300 m), the trend was reversed; foraminifera were 17 times more abundant than metazoan taxa at 412 m but only 1.4 times more abundant at 3350 m. An abundance of food combined with oxygen levels which are not depressed sufficiently to eliminate the more tolerant taxa, probably explains why foraminifera and macrofaunal metazoans flourished at the 412-m site, perhaps to the detriment of the metazoan meiofauna.

THE ROLE OF BENTHIC FORAMINIFERA IN DEEP-SEA FOOD WEBS AND CARBON CYCLING

Benthic foraminifers are a major element in deep-sea sediment and hard-substrate communities, sometimes accounting for 50% or more of eukaryotic biomass. They feed at a low trophic level, consuming mainly planktonic and other detritus and bacteria. Some species have metabolic adaptations enabling them to respond quickly to pulsed detrital inputs with rapid rates of reproduction and growth. These foraminifers probably assist microorganisms in the breakdown of fresh detrital material, while others are deposit feeders which convert more refractory organic substances into biomass. DOM uptake may be important, although no data exist as yet to substantiate this. Foraminifers are consumed by a wide variety of organisms, including selective and non-selective deposit feeders and specialised predators, and probably represent an important link between lower and higher levels of deep-sea food webs. A variety of non-trophic interactions between metazoans and foraminifers, for example, the provision of physical substrates, may facilitate access to enhanced food supplies. Thus, foraminifera playa largely unquantified but potentially significant role in deep-sea carbon cycling