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Levin, L, Blair N, DeMaster D, Plaia G, Fornes W, Martin C, Thomas C.  1997.  Rapid subduction of organic matter by maldanid polychaetes on the North Carolina slope. Journal of Marine Research. 55:595-611.   10.1357/0022240973224337   AbstractWebsite

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 (C-13-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 Th-234-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.

Levin, LA, Huggett D, Myers P, Bridges T, Weaver J.  1993.  Rare earth tagging methods for the study oflarval dispersal by marine invertebrates. Limnology and Oceanography. 38:346-360. AbstractWebsite

Rare-earth elements (REEs) are proposed as a label for invertebrate larvae (clams, barnacles, and polychaetes) and passive larval mimics (polystyrene spheres) to be used in field studies of larval dispersal. Different elements, their uptake levels, retention times, and effects on larval survivorship were examined to assess suitability of REEs as larval tags. Lu, Sm, and Eu were selected for labeling work based on extremely low levels in natural plankton and seawater and due to the high sensitivity of neutron activation analysis to these elements. Adequate label retention occurs on time scales of hours to days in both larvae and microspheres. Combined use of Eu-labeled microspheres and Lu- and Sm-labeled larvae in release-recapture mode offers a highly sensitive method for studying trajectories and behavior of larvae in natural settings. However, dilution factors may limit experimentation to small and intermediate spatial scales (meters to kilometers) in the field.

Levin, LA.  2006.  Recent progress in understanding larval dispersal: new directions and digressions. Integrative and Comparative Biology. 46:282-297.   10.1093/icb/024   AbstractWebsite

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.

Levin, LA, Ziebis W, Mendoza GF, Growney-Cannon V, Walther S.  2006.  Recruitment response of methane-seep macrofauna to sulfide-rich sediments: An in situ experiment. Journal of Experimental Marine Biology and Ecology. 330:132-150.   10.1016/j.jembe.2005.12.022   AbstractWebsite

Hydrodynamically unbiased colonization trays were deployed for 6 months (Oct. 2000 to April 2001) on the northern California margin (Eel R. region; 525 m) to examine macrofaunal colonization rates at methane seeps. The influence of sulfide on recruitment and survival was examined by deploying sediments with and without sulfide added; effect of seep proximity was evaluated by placing trays inside and outside seeps. The trays contained a two-layer system mimicking vesicomyid clam bed habitat geochemistry, with 89 9 mM sulfide in a lower agar layer at the start of the experiment. After 6 month on the seabed, the lower agar layer contained 2-4 mM H2S. We observed rapid macrofaunal colonization equivalent to 50% of initial non-seep ambient densities. There was no difference in total colonizer densities, number of species, or rarefaction diversity among 3 treatments: (1) controls (no sulfide added) placed outside seeps, (2) trays with sulfide added placed outside seeps and (3) trays with sulfide added placed inside seep patches. Colonization trays with sulfide placed at seeps had different species composition from trays without sulfide place outside seeps; there were more amphipods (non-ampeliscid) and cumaceans in the seep/sulfide treatment and more nemerteans, Nephtys cornuta and tanaids in the non-seep/no-sulfide treatment. Outside seeps, annelids comprised <15% of tray colonists; within seep patches, annelids comprised 5 of the top 10 dominant colonizing taxa (24% of the total). The polychaetes Mediomastus sp., Aphelochaeta sp., Paraonidae sp., and Nerillidae sp. exhibited significantly higher densities in sulfide additions. Tanaids, echinoderms, and N. cornuta exhibited sulfide avoidance. At least 6 dorvilleid polychaete species colonized the experiments. Of these, 4 species occurred exclusively in trays with sulfide added and 80% of all dorvilleid individuals were found in trays with sulfide placed inside seep sediments. Counts of large sulfur bacterial filaments were positively correlated with maximum sulfide concentration in each tray, and with proximity of sulfide to the sediment surface. However, total macrofaunal densities were not correlated with tray sulfide concentrations. As a group, tray assemblages achieved some but not all characteristics of ambient seep assemblages after 6-month exposure on the sea floor. Distinctive colonization patterns at methane seeps contribute to the dynamic mosaic of habitat patches that characterize the eastern Pacific continental margin. Overall, proximity of seep habitats had at least as great an influence on macrofaunal colonization as tray sulfide concentrations. Taxa characteristic of seep sediments were more likely to settle into trays placed inside rather than outside seep patches. Whether this is due to limited dispersal ability or local geochemical cues remains to be determined. (C) 2005 Elsevier B.V. All rights reserved.

Whitcraft, CR, Levin LA.  2007.  Regulation of benthic algal and animal communities by salt marsh plants: Impact of shading. Ecology. 88:904-917.   10.1890/05-2074   AbstractWebsite

Plant cover is a fundamental feature of many coastal marine and terrestrial systems and controls the structure of associated animal communities. Both natural and human-mediated changes in plant cover influence abiotic sediment properties and thus have cascading impacts on the biotic community. Using clipping ( structural) and light ( shading) manipulations in two salt marsh vegetation zones ( one dominated by Spartina foliosa and one by Salicornia virginica), we tested whether these plant species exert influence on abiotic environmental factors and examined the mechanisms by which these changes regulate the biotic community. In an unshaded ( plant and shade removal) treatment, marsh soils exhibited harsher physical properties, a microalgal community composition shift toward increased diatom dominance, and altered macrofaunal community composition with lower species richness, a larger proportion of insect larvae, and a smaller proportion of annelids, crustaceans, and oligochaetes compared to shaded ( plant removal, shade mimic) and control treatment plots. Overall, the shaded treatment plots were similar to the controls. Plant cover removal also resulted in parallel shifts in microalgal and macrofaunal isotopic signatures of the most dynamic species. This suggests that animal responses are seen mainly among microalgae grazers and may be mediated by plant modi. cation of microalgae. Results of these experiments demonstrate how light reduction by the vascular plant canopy can control salt marsh sediment communities in an arid climate. This research facilitates understanding of sequential consequences of changing salt marsh plant cover associated with climate or sea level change, habitat degradation, marsh restoration, or plant invasion.

Levin, LA, Gage JD.  1998.  Relationships between oxygen, organic matter and the diversity of bathyal macrofauna. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 45:129-163.   10.1016/s0967-0645(97)00085-4   AbstractWebsite

The relationships of environmental factors with measures of macrobenthic community diversity were examined for the total fauna, and for polychaetes only, from 40 bathyal stations in the North Atlantic, eastern Pacific and Indian Oceans (154-3400 m). Stepwise multiple regression revealed that depth, latitude, sediment organic-carbon content and bottom-water oxygen concentration are significant factors that together explained 52-87% of the variation in macrobenthic species richness (E[s(100)]), the Shannon-Wiener index (H'), dominance (D), and evenness (J'). Percent sand and percent clay were not significant factors. After removal of depth and latitudinal effects, oxygen and organic-carbon concentrations combined accounted for 47, 67, 52 and 32% of residual variation in macrobenthic E(s(100)), H', D, and J', respectively. Organic carbon exhibited a stronger relationship than oxygen to measures of community evenness, and appeared to have more explanatory power for polychaetes than total macrobenthos. When only stations with oxygen < 1mll(-1) were considered, oxygen concentration became the dominant parameter after depth. Results suggest existence of an oxygen threshold ( < 0.45 mi l(-1)), above which oxygen effects on macrobenthic diversity are minor relative to organic matter influence, but below which oxygen becomes a critical factor. Our regression results lead us to hypothesize that for bathyal faunas, oxygen at low concentrations has more influence on species richness, while organic carbon regulates the distribution of individuals among species (community evenness). Examination of rarefaction curves for Indo-Pacific stations reveals that total macrobenthos, polychaetes, crustaceans and molluscs all exhibit reduced species richness within oxygen minimum zones (OMZs). However, representation under conditions of hypoxia varies among taxa, with polychaetes being most tolerant. Molluscs and crustaceans often (but not always) exhibit few individuals and species in OMZs, and sometimes disappear altogether, contributing to reduced macrobenthic diversity and elevated dominance in these settings. The linear negative relationship observed between bathyal species richness and sediment organic-carbon content (used here as a proxy for food availability) may represent the right side (more productive half) of the hump-shaped, diversity-productivity curve reported in other systems. These analyses suggest then are potentially strong influences of organic matter and oxygen on the diversity and composition of bathyal macrobenthos, especially in the Indo-Pacific Ocean. (C) 1998 Elsevier Science Ltd. All rights reserved.

Blair, NE, Plaia GR, Boehme SE, Demaster DJ, Levin LA.  1994.  The remineralization of organic carbon on the North Carolina continental slope. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 41:755-766.   10.1016/0967-0645(94)90046-9   AbstractWebsite

The sources and fates of metabolizable organic carbon were examined at three sites on the North Carolina slope positioned offshore of Cape Fear, Cape Lookout and Cape Hatteras. The C-13/C-12 compositions (delta(13)C) of the solid phase organic matter, and the dissolved inorganic carbon (Sigma CO2) produced during its oxidation, suggested that the labile fraction was predominantly marine in origin. The Sigma CO2 concentration gradient across the sediment-water interface, and by inference the Sigma CO2 flux and production rate, increased northward from Cape Fear to Cape Hatteras. Methane distributions and Sigma CO2 delta(13)C values suggest that the rate of anaerobic diagenesis increased northward as well. The differences in sedimentary biogeochemistry are most likely driven by an along-slope gradient of reactive organic carbon flux to the seabed. This trend in reactive organic carbon flux correlates well with macrofaunal densities previously observed at the three sites. Proximity to the shelf and the transport of particulate material by surface boundary currents may control the deposition of metabolizable material on the Carolina slope. Evidence for methanogenesis was found only on the Cape Hatteras slope. The methane, which was produced at a depth of approximately 1 m in the seabed, was consumed nearly quantitatively in the biologically mixed layer as it diffused upward. Irrigation of the sediments by infauna may have provided the necessary oxidant for the consumption of the methane.

Carson, HS, Lopez-Duarte PC, Rasmussen L, Wang DX, Levin LA.  2010.  Reproductive timing alters population connectivity in marine metapopulations. Current Biology. 20:1926-1931.   10.1016/j.cub.2010.09.057   AbstractWebsite

Populations of most marine organisms are connected by the dispersal of larval stages, with profound implications for marine conservation [1]. Because of the extreme effort needed to empirically measure larval exchange, multispecies conservation efforts must estimate connectivity by extrapolation using taxonomy, adult distribution, life history, behavior, or phenology. Using a 6-year record of connectivity realized through trace-elemental fingerprinting of larval shells, we document the seasonal and interannual variability of larval exchange for two congeneric mussel species with overlapping but distinct distribution, life history, and reproduction timing. We reveal consistent autumn poleward movement and spring equatorward movement for both species, coincident with near-shore surface currents. However, because the major reproductive seasons differ, the dominant source-sink dynamics of these two congeneric species are nearly opposite. Consideration of present and future reproductive timing as altered by climate change is crucial to marine connectivity and conservation, especially for the numerous coastal areas subject to seasonal current reversals.

Levin, LA, Smith CR.  1984.  Response of background fauna to disturbance and enrichment in the deep sea: a sediment tray experiment. Deep-Sea Research Part a-Oceanographic Research Papers. 31:1277-&.   10.1016/0198-0149(84)90001-3   AbstractWebsite

Free-vehicle sediment trays were deployed on the floor of the Santa Catalina Basin (1300 m) to study the response of deep-sea infauna to defaunation and algal enrichment. We recovered three trays that had been filled with frozen basin sediment: one otherwise untreated, one enriched with 20 g of powdered Macrocystis pyrifera (kelp) and containing oxidized sediment, and one kelp-enriched and anoxic. After 4.7 months on the basin floor, macrofaunal density in the unenriched tray was 10% () of that in the surrounding sea floor. Most colonists belonged to species dominant in the background basin community. Juveniles and mature individuals were present, suggesting short maturation times or post-larval dispersal ability in some species. The kelp-enriched (oxidized) tray contained a single macrofaunal mite (Arachnida:Acarina), suggesting avoidance of kelp-enriched sediment by available colonists. The anoxic, kelp-enriched tray contained two dorvilleid polychaetes apparently adapted to high sulphide environments.As in other deep-sea studies, we obtained slower colonization of sediment trays than in shallow water experiments. The primary tray respondents, however, were dominants of the background community, in contrast to previous deep-sea experiments. The findings are consistent with the hypothesis that disturbance is important to the ecology of the dominant species in the Santa Catalina Basin.

Sato, KN, Andersson AJ, Day JMD, Taylor JRA, Frank MB, Jung JY, McKittrick J, Levin LA.  2018.  Response of sea urchin fitness traits to environmental gradients across the Southern California oxygen minimum zone. Frontiers in Marine Science. 5   10.3389/fmars.2018.00258   AbstractWebsite

Marine calcifiers are considered to be among the most vulnerable taxa to climate-forced environmental changes occurring on continental margins with effects hypothesized to occur on microstructural, biomechanical, and geochemical properties of carbonate structures. Natural gradients in temperature, salinity, oxygen, and pH on an upwelling margin combined with the broad depth distribution (100-1,100 m) of the pink fragile sea urchin, Strongylocentrotus (formerly Allocentrotus) fragilis, along the southern California shelf and slope provide an ideal system to evaluate potential effects of multiple climate variables on carbonate structures in situ. We measured, for the first time, trait variability across four distinct depth zones using natural gradients as analogues for species-specific implications of oxygen minimum zone (OMZ) expansion, deoxygenation and ocean acidification. Although S. fragilis may likely be tolerant of future oxygen and pH decreases predicted during the twenty-first century, we determine from adults collected across multiple depth zones that urchin size and potential reproductive fitness (gonad index) are drastically reduced in the OMZ core (450-900 m) compared to adjacent zones. Increases in porosity and mean pore size coupled with decreases in mechanical nanohardness and stiffness of the calcitic endoskeleton in individuals collected from lower pH(Total) (7.57-7.59) and lower dissolved oxygen (13-42 mu mol kg(-1)) environments suggest that S. fragilis may be potentially vulnerable to crushing predators if these conditions become more widespread in the future. In addition, elemental composition indicates that S. fragilis has a skeleton composed of the low Mg-calcite mineral phase of calcium carbonate (mean Mg/Ca = 0.02 mol mol(-1)), with Mg/Ca values measured in the lower end of values reported for sea urchins known to date. Together these findings suggest that ongoing declines in oxygen and pH will likely affect the ecology and fitness of a dominant echinoid on the California margin.

Levin, LA.  1990.  A review of methods for labeling and tracking marine invertebrate larvae. Ophelia. 32:115-144.   10.1080/00785236.1990.10422028   AbstractWebsite

Methods for marking invertebrate larvae for use in dispersal studies include staining, tagging with calcium replacements, radiotracers and rare elements, and use of genetic, morphological, and parasite markers. The mark, release and recapture method provides a valuable approach to the study of larval movements but has been attempted only rarely, in part because of difficulties with larval recovery. Methodological and instrumentational advances may improve the feasibility of release and recovery efforts. Additional approaches to tracking larvae include visual tracking, use of isolated or point sources, Lagrangian and Eulerian methods, energetic calculations, hydro-graphic modeling and simulations. Recent emphases on physical transport mechanisms, and on the interrelationship of behavior and passive transport can be considered in the context of tracking methods. Newly-developed and recently-conceived techniques offer promise of considerable advance in our understanding of larval dispersal phenomena.

Gooday, AJ, Levin LA, Linke P, Heeger T.  1992.  The role of benthic foraminifera in Deep-sea food webs and carbon cycling. Deep-sea food chains and the global carbon cycle. ( Rowe GT, Pariente V, Eds.).:63-91., Dordrecht ; Boston: Kluwer Academic Publishers Abstract
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Currin, CA, Levin LA, Talley TS, Michener R, Talley D.  2011.  The role of cyanobacteria in Southern California salt marsh food webs. Marine Ecology. 32:346-363.: Blackwell Publishing Ltd   10.1111/j.1439-0485.2011.00476.x   AbstractWebsite

Understanding wetland food webs is critical for effective habitat management, restoration and conservation. Microalgae are recognized as key food sources for marsh invertebrates but the importance of different groups under various conditions is rarely examined. We tested the hypothesis that faunal utilization of microalgae, and cyanobacteria in particular, is significant in Southern California created and natural salt marshes but varies with habitat type (creek bank versus marsh interior) and season (spring versus autumn). We used stable isotope analysis and mixing models (IsoSource) to compare food webs in adjacent young (created) and mature (natural) salt marshes. Isotopic values of some primary producers, macrofauna, epifauna, and fish demonstrated significant differences between the adjacent salt marshes. δ13C and δ34S values of the benthic microalgal community varied with taxonomic composition (diatoms versus cyanobacteria) and to a lesser extent with season. Depleted δ15N values of benthic diatoms and macroalgae indicated that N2 fixed within algal mats was recycled within the benthic algal community. Marsh fauna, including most major macrofauna taxal, Cerithidea, and Fundulus, also exhibited seasonal differences in isotopic composition, and Cerithidea and selected macrofauna (oligochaetes, polychaetes) from the marsh interior were more enriched in 13C and depleted in 15N than those from the creek bank. In the young marsh, the cyanobacteria contributed a minimum of 17–100% of the primary production in food webs supporting macrofauna, and cyanobacteria contributed at least 40% of the primary production included in Cerithidea and Fundulus food webs. A wider range of primary producers contributed to food webs in the mature marsh. Cyanobacteria were a greater source of trophic support for macrofauna from the marsh interior than the creek bank, whereas Spartina was a more important food source for creek bank macrofauna in both marshes. Insect larvae largely consumed cyanobacteria, whereas polychaetes exhibited greater utilization of Spartina. Phytoplankton was the primary food resource for mussels in both marshes. Although the spatial and temporal complexity of food webs has traditionally been collapsed into the study of relatively simplified food webs, isotope signatures reveal fine-scale patterns in food web structure that may be used to make more accurate assessments of ecosystem state. Accurate interpretation of marsh trophic structure using natural abundance stable isotopes requires fine-scale resolution in space and time, a large number of samples, and a high level of taxonomic resolution.