Publications

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2015
Neira, C, Mendoza G, Porrachia M, Stransky C, Levin LA.  2015.  Macrofaunal recolonization of copper-contaminated sediments in San Diego Bay. Marine Pollution Bulletin. 101:794-804.   10.1016/j.marpolbul.2015.09.023   AbstractWebsite

Effects of Cu-loading on macrofaunal recolonization were examined in Shelter Island Yacht Basin (San Diego Bay, California). Sediments with high and low Cu levels were defaunated and Cu-spiked, translocated, and then placed back into the environment These demonstrated that the alteration observed in benthic communities associated with Cu contamination occurs during initial recolonization. After a 3-month exposure to sediments with varying Cu levels, two primary colonizing communities were identified: (1) a "mouth assemblage" resembling adjacent background fauna associated with low-Cu levels that was more diverse and predominantly dominated by surface- and subsurface-deposit feeders, burrowers, and tube builders, and (2) a "head assemblage" resembling adjacent background fauna associated with high-Cu concentrations, with few dominant species and an increasing importance of carnivores and mobile epifauna. Cu loading can cause reduced biodiversity and lower structural complexity that may last several months if high concentrations persist, with a direct effect on community functioning. (C) 2015 Elsevier Ltd. All rights reserved.

2014
Sapir, A, Dillman AR, Connon SA, Grupe BM, Ingels J, Mundo-Ocampo M, Levin LA, Baldwin JG, Orphan VJ, Sternberg PW.  2014.  Microsporidia-nematode associations in methane seeps reveal basal fungal parasitism in the deep sea. Frontiers in Microbiology. 5   10.3389/fmicb.2014.00043   AbstractWebsite

The deep sea is Earth's largest habitat but little is known about the nature of deep-sea parasitism. In contrast to a few characterized cases of bacterial and protistan parasites, the existence and biological significance of deep-sea parasitic fungi is yet to be understood. Here we report the discovery of a fungus-related parasitic microsporidium, Nematocenator marisprofundi n. gen. n. sp. that infects benthic nematodes at methane seeps on the Pacific Ocean floor. This infection is species-specific and has been temporally and spatially stable over 2 years of sampling, indicating an ecologically consistent host-parasite interaction. A high distribution of spores in the reproductive tracts of infected males and females and their absence from host nematodes' intestines suggests a sexual transmission strategy in contrast to the fecal-oral transmission of most microsporidia. N. mansprofundi targets the host's body wall muscles causing cell lysis, and in severe infection even muscle filament degradation. Phylogenetic analyses placed N. marisprofundi in a novel and basal clade not closely related to any described microsporidia clade, suggesting either that microsporidia-nematode parasitism occurred early in microsporidia evolution or that host specialization occurred late in an ancient deep-sea microsporidian lineage. Our findings reveal that methane seeps support complex ecosystems involving interkingdom interactions between bacteria, nematodes, and parasitic fungi and that microsporidia parasitism exists also in the deep-sea biosphere.

2011
Neira, C, Mendoza G, Levin LA, Zirino A, Delgadillo-Hinojosa F, Porrachia M, Deheyn DD.  2011.  Macrobenthic community response to copper in Shelter Island Yacht Basin, San Diego Bay, California. Marine Pollution Bulletin. 62:701-717.   10.1016/j.marpolbul.2011.01.027   AbstractWebsite

We examined Cu contamination effects on macrobenthic communities and Cu concentration in invertebrates within Shelter Island Yacht Basin, San Diego Bay, California. Results indicate that at some sites, Cu in sediment has exceeded a threshold for "self defense" mechanisms and highlight the potential negative impacts on benthic faunal communities where Cu accumulates and persists in sediments. At sites with elevated Cu levels in sediment, macrobenthic communities were not only less diverse but also their total biomass and body size (individual biomass) were reduced compared to sites with lower Cu. Cu concentration in tissue varied between species and within the same species, reflecting differing abilities to "regulate" their body load. The spatial complexity of Cu effects in a small marina such as SIYB emphasizes that sediment-quality criteria based solely on laboratory experiments should be used with caution, as they do not necessarily reflect the condition at the community and ecosystem levels. (C) 2011 Elsevier Ltd. All rights reserved.

2009
Cowie, GL, Levin LA.  2009.  Benthic biological and biogeochemical patterns and processes across an oxygen minimum zone (Pakistan margin, NE Arabian Sea). Deep-Sea Research Part Ii-Topical Studies in Oceanography. 56:261-270.   10.1016/j.dsr2.2008.10.001   AbstractWebsite

Oxygen minimum zones (OMZs) impinging on continental margins present sharp gradients ideal for testing environmental factors thought to influence C cycling and other benthic processes, and for identifying the roles that biota play in these processes. Here we introduce the objectives and initial results of a multinational research program designed to address the influences of water depth, the OMZ (similar to 150-1300 m), and organic matter (OM) availability on benthic communities and processes across the Pakistan Margin of the Arabian Sea. Hydrologic, sediment, and faunal characterizations were combined with in-situ and shipboard experiments to quantify and compare biogeochemical processes and fluxes, OM burial efficiency, and the contributions of benthic communities, across the OMZ. In this introductory paper, we briefly review previous related work in the Arabian Sea, building the rationale for integrative biogeochemical and ecological process studies. This is followed by a summary of individual volume contributions and a brief synthesis of results. Five primary stations were studied, at 140, 300, 940,1200 and 1850 m water depth, with sampling in March-May (intermonsoon) and August-October (late-to-postmonsoon) 2003. Taken together, the contributed papers demonstrate distinct cross-margin gradients, not only in oxygenation and sediment OM content, but in benthic community structure and function, including microbial processes, the extent of bioturbation, and faunal roles in C cycling. Hydrographic studies demonstrated changes in the intensity and extent of the OMZ during the SW monsoon, with a shoaling of the upper OMZ boundary that engulfed the previously oxygenated 140-m site. Oxygen profiling and microbial process rate determinations demonstrated dramatic differences in oxygen penetration and consumption across the margin, and in the relative importance of anaerobic processes, but surprisingly little seasonal change. A broad maximum in sediment OM content occurred on the upper slope, roughly coincident with the OMZ; but the otherwise poor correlation with bottom-water oxygen concentrations indicated that other factors are important in determining sediment OM distributions. Downcore profiles generally showed little clear evidence of in-situ OM alteration, and there was little sign of OM enrichment resulting from the southwest monsoon in sediments collected in the late-to-postmonsoon sampling. This is interpreted to be due to rapid cycling of labile OM. Organic geochemical studies confirmed that sediment OM is overwhelmingly of marine origin across the margin, but also that it is heavily altered, with only small changes in degradation state across the OMZ. More negative stable C isotopic compositions in surficial sediments at hypoxic sites within the OMZ core are attributed to a chemosynthetic bacterial imprint. Dramatic changes in benthic community structure occurred across the lower OMZ transition, apparently related to OM availability and quality as well as to DO concentrations. High-resolution sampling, biomarkers and isotope tracer studies revealed that oxygen availability appears to exert threshold-type controls on benthic community structure and early faunal C processing. Biomarker studies also provided evidence of faunal influence on sediment OM composition. Together, the results offer strong evidence that benthic fauna at sites across the margin play important roles in the early cycling of sediment OM through differential feeding and bioturbation activities. (C) 2008 Published by Elsevier Ltd.

2006
Neira, C, Grosholz ED, Levin LA, Blake R.  2006.  Mechanisms generating modification of benthos following tidal flat invasion by a Spartina hybrid. Ecological Applications. 16:1391-1404.   10.1890/1051-0761(2006)016[1391:mgmobf]2.0.co;2   AbstractWebsite

Many coastal habitats are being substantially altered by introduced plants. In San Francisco Bay,, California, USA, a hybrid form of the eastern cordgrass Spartina alterniflora is rapidly invading open mudflats in southern and central sections of the Bay, altering habitat, reducing macrofaunal densities, and shifting species composition. The invasion has resulted in significant losses of surface-feeding amphipods, bivalves, and cirratulid polychaetes, while subsurface feeding groups such as tubificid oligochaetes and capitellid polychaetes have been unaffected. In the present paper, we document the causes and mechanisms underlying the changes observed. Through a series of in situ manipulative experiments we examined the influence of hybrid Spartina canopy on a range of physical, chemical, and biological properties. The hybrid Spartina canopy exerted a strong influence on. the hydrodynamic regime, triggering a series of physical, chemical, and biological changes in the benthic system. Relative to tidal flats, water velocity was reduced in hybrid patches, promoting deposition of fine-grained, organic-rich particles. The resulting changes in the sediment environment included increased porewater sulfide concentrations and anoxia, which led to poor survivorship. of surface feeders such as, bivalves, amphipods, and polychaetes. These are key taxa that support higher trophic levels including migratory shorebirds that feed on tidal flats. Altered flow in the Spartina canopy further contributed to changes in barnacle recruitment and resuspension of adult benthic invertebrates. Increased crab-induced predation pressure associated with Spartina invasion also contributed to changes in benthic invertebrate communities. Our results suggest that multiple physical, chemical, biotic, and trophic impacts of the Spartina invasion have resulted in substantial changes in benthic communities that are likely to have important effects on the entire ecosystem.

1999
Thistle, D, Levin LA, Gooday AJ, Pfannkuche O, Lambshead PJD.  1999.  Physical reworking by near-bottom flow alters the metazoan meiofauna of Fieberling Guyot (northeast Pacific). Deep-Sea Research Part I-Oceanographic Research Papers. 46:2041-2052.   10.1016/s0967-0637(99)00040-0   AbstractWebsite

Although much of the deep sea is physically tranquil, some regions experience near-bottom flows that rework the surficial sediment. During periods of physical reworking, animals in the reworked layer risk being suspended, which can have both positive and negative effects. Reworking can also change the sediment in ecologically important ways, so the fauna of reworked sites should differ from that of quiescent locations. We combined data from two reworked, bathyal sites on the summit of Fieberling Guyot (32 degrees 27.631'N, 127 degrees 49.489'W; 32 degrees 27.581'N, 127 degrees 47.839'W) and compared the results with those of more tranquil sites. We tested for differences in the following parameters, which seemed likely to be sensitive to the direct or indirect effects of reworking: (1) the vertical distribution of the meiofauna in the sea bed, (2) the relative abundance of surface-living harpacticoids, (3) the proportion of the fauna consisting of interstitial harpacticoids, (4) the ratio of harpacticoids to nematodes. We found that the vertical distributions of harpacticoid copepods, ostracods, and kinorhynchs were deeper on Fieberling. In addition, the relative abundance of surface-living harpacticoids was less, the proportion of interstitial harpacticoids was greater, and the ratio of harpacticoids to nematodes was greater on Fieberling. These differences between Fieberling and the comparison sites suggest that physical reworking affects deep-sea meiofauna and indicate the nature of some of the effects. (C) 1999 Elsevier Science Ltd. AII rights reserved.

1997
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.

1991
Levin, LA, Childers SE, Smith CR.  1991.  Epibenthic, agglutinating foraminiferans in the Santa Catalina Basin and their response to disturbance. Deep-Sea Research Part a-Oceanographic Research Papers. 38:465-483.   10.1016/0198-0149(91)90047-j   AbstractWebsite

There are five common species of large (0.5-6 cm long) epibenthic, agglutinating foraminiferans in the Santa Catalina Basin (1200-1350 m). This paper describes their basic ecology and response to mound disturbance. Combined, the five species attain mean densities of 200-300 individuals per m2 and their protoplasm has an average biomass of 199.5 mg m-2. Individual species occur at densities ranging from 7 to 100 m-2, and each species has a different population size structure. Protoplasm comprises < 2% of test volumes. Analysis of excess Th-234 revealed no indication of particle sequestering within tests, and acridine orange direct counts of bacteria provided no evidence of microbial gardening or enhancement associated with tests. Twenty-five per cent of tests examined had metazoan associates; approximately half of these were polychaetes. Experiments were carried out to investigate the response of the epibenthic foraminiferal assemblage to disturbance from large, biogenic mounds, a common feature on the Santa Catalina Basin floor. Three branched forms, Pelosina cf. arborescens, P. cf. cylindrica and a mud-walled astrorhizinid, were most abundant on background sediments, less common on natural mounds and absent from artificially-created mounds exposed for 10.5 months. Two spherical species, Oryctoderma sp. and a different mud-walled astrorhizinid, were present at similar densities on artificial mounds (9.5-10.5 months old), natural mounds and undisturbed sediments, but Oryctoderma sp. attained largest sizes on mounds. These two species appear to be opportunistic taxa that can colonize and grow rapidly on mound sediments. This study suggests that disturbance, in this case that by sediment mound builders, is an important source of spatial heterogeneity in deep-water foraminiferal communities. Where sediment mounds occur, foraminiferal assemblages will experience disequilibrium dynamics.