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2015
Levin, LA, Honisch B, Frieder CA.  2015.  Geochemical proxies for estimating faunal exposure to ocean acidification. Oceanography. 28:62-73.   10.5670/oceanog.2015.32   AbstractWebsite

Growing concern over the impacts of modern ocean acidification (OA) and interest in historical pH excursions have intensified the development of geochemical proxies for organism exposure to acidification and other components of the carbonate system. The use of carbonate structures produced by foraminifers, coccolithophores, corals, mollusks, brachiopods, echinoderms, ostracods, and fish for paleoreconstructions is an active area of study, and the resulting proxy development offers new opportunities for studying modern faunal exposures. Here we review information from field studies and laboratory experiments on carbonate system geochemical proxies in protists and metazoa. Geochemical proxy development for foraminifers and corals is most advanced; studies of fish and echinoderms are in their infancy. The most promising geochemical proxies are those with a mechanistic link to changes in seawater carbonate chemistry, such as boron isotopes (delta B-11), B/Ca, and U/Ca ratios recorded in skeletal hard parts. We also discuss indirect geochemical proxies (other trace elements and carbonate polymorphs) along with their potential uses and limitations due to modification by physiological processes, precipitation rate, and degree of calcification. Proxy measurements in modern skeletal structures, otoliths, statoliths, and other hard parts could reveal environmental exposures of organisms from larval through adult stages, and could advance inferences about effects of OA (and other stressors) on survival, growth, population connectivity, and other ecological attributes. Use of geochemical proxies in live, field-collected organisms is an underutilized and underdeveloped approach to studying OA consequences, but it may offer a powerful, complementary approach to laboratory observations.

2010
Buhl-Mortensen, L, Vanreusel A, Gooday AJ, Levin LA, Priede IG, Buhl-Mortensen P, Gheerardyn H, King NJ, Raes M.  2010.  Biological structures as a source of habitat heterogeneity and biodiversity on the deep ocean margins. Marine Ecology-an Evolutionary Perspective. 31:21-50.   10.1111/j.1439-0485.2010.00359.x   AbstractWebsite

Biological structures exert a major influence on species diversity at both local and regional scales on deep continental margins. Some organisms use other species as substrates for attachment, shelter, feeding or parasitism, but there may also be Mutual benefits from the association. Here, we highlight the structural attributes and biotic effects of the habitats that corals, sea pens, sponges and xenophyophores offer other organisms. The environmental setting of the biological structures influences their species composition. The importance of benthic species as substrates seems to increase with depth as the complexity of the surrounding geological substrate and food supply decline. There are marked differences in the degree of mutualistic relationships between habitat-forming taxa. This is especially evident for scleractinian corals, which have high numbers of facultative associates (commensals) and few obligate associates (mutualists), and gorgonians, with their few commensals and many obligate associates. Size, flexibility and architectural complexity of the habitat-forming organism are positively related to species diversity for both sessile and mobile species. This is mainly evident for commensal species sharing a facultative relationship with their host. Habitat complexity is enhanced by the architecture of biological structures, as well as by biological interactions. Colony morphology has a great influence on feeding efficiency for suspension feeders. Suspension feeding, habitat-forming organisms modify the environment to optimize their food uptake. This environmental advantage is also passed on to associated filter-feeding species. These effects are poorly understood but represent key points for understanding ecosystems and biodiversity on continental margins. In this paper we explore the contributions of organisms and the biotic structures they create (rather than physical modifications) to habitat heterogeneity and diversity on the deep continental margins.

2009
Woulds, C, Andersson JH, Cowie GL, Middelburg JJ, Levin LA.  2009.  The short-term fate of organic carbon in marine sediments: Comparing the Pakistan margin to other regions. Deep Sea Research (Part II, Topical Studies in Oceanography). 56:393-402., United Kingdom: Elsevier BV   10.1016/j.dsr2.2008.10.008   AbstractWebsite

Pulse-chase experiments with isotopically labelled phytodetritus conducted across the Pakistan margin reveal that the impact of biological activities on benthic C-cycling varies markedly among sites exhibiting different seafloor conditions. In this study, patterns of biological C-processing across the Pakistan margin oxygen minimum zone (OMZ) are compared with those observed in previous tracer studies. Variations in site environmental conditions are proposed to explain the considerable variations in C-processing patterns among this and previous studies. Three categories of C-processing pattern are identified: (1) respiration dominated, where respiration accounts for >75% of biological C-processing, and uptake by metazoan macrofauna, foraminifera and bacteria are relatively minor processes. These sites tend to show several (although not necessarily all) of the properties of being cold and deep, and having low inputs of organic carbon to the sediment and relatively low-biomass metazoan macrofaunal communities; (2) active faunal uptake, where respiration accounts for <75%, and metazoan macrofaunal, foraminiferal and bacterial uptake each account for 10-25% of biological C-processing. This type is further split into metazoan macrofaunal- and foraminiferal-dominated situations, dictated by oxygen availability; and (3) metazoan macrofaunal uptake dominated, characterised by metazoan macrofaunal uptake accounting for ~50% of biological C-processing, due to unusually large biomasses of the phytodetritus-consuming animals. Total respiration rates (of added C) on the Pakistan margin fell within the range of rates measured elsewhere in the deep sea (} .1-2.8mgCm super(-) super(2)h super(-) super(1)), and seem to be dominantly controlled by seafloor temperature. Rates of metazoan macrofaunal uptake of organic matter (OM) on the Pakistan margin are larger than those in most other studies, and this is attributed to the large and active metazoan macrofaunal communities in the lower OMZ, characteristic of OMZ boundaries. Finally, biological mixing of Pakistan margin sediments was reduced compared to that observed in comparable tracer studies on other margins. This probably reflects faunal feeding and burrowing strategies consistent with low oxygen concentrations and a relatively abundant supply of sedimentary OM.

2002
Levin, L, Gutierrez D, Rathburn A, Neira C, Sellanes J, Munoz P, Gallardo V, Salamanca M.  2002.  Benthic processes on the Peru margin: a transect across the oxygen minimum zone during the 1997-98 El Nino. Progress in Oceanography. 53:1-27.   10.1016/s0079-6611(02)00022-8   AbstractWebsite

Oxygen minimum zones (OMZs) are widespread features in the most productive regions of the world ocean. A holistic view of benthic responses to OMZ conditions will improve our ability to predict ecosystem-level consequences of climatic trends that influence oxygen availability, such as global warming or ENSO-related events. Four stations off Callao, Peru (-12'S, Station A, 305 m; Station B, 562 m; Station C, 830 nu and Station D, 1210 m) were sampled to examine the influence of the low bottom-water oxygen concentration and high organic-matter availability within the OMZ (O(2) < 0.5 ml L(-1)) on sediments, benthic communities, and bioturbation. Sampling took place during early January 1998, an intense El Ni (n) over tildeo period associated with higher-than-normal levels of O(2) on the shelf and upper slope. Peru slope sediments were highly heterogeneous. Sediment total organic carbon content exceeded 16%, lamination was present below 6 cm depth, and filamentous sulfur bacteria (Thioploca spp.) were present at Station A, (305 m, 0, < 0.02 ml L(-1)). Deeper sites contained phosphorite crusts or pellets and exhibited greater bottom-water oxygenation and lower content and quality of organic matter. X-radiographs and (210)Pb and (234)Th profiles suggested the dominance of lateral transport and bioturbation over pelagic sedimentation at the mid- and lower slope sites. Macrofauna, metazoan meiofauna and foraminifera exhibited coherence of density patterns across stations, with maximal densities (and for macrofauna, reduced diversity) at Station A, where bottom-water oxygen concentration was lowest and sediment labile organic matter content (LOC: sum of protein, carbohydrate and lipid carbon) was greatest. Metazoan and protozoan meiofaunal densities were positively correlated with sediment LOC. The taxa most tolerant of nearly anoxic, organic-rich conditions within the Peru OMZ were calcareous foraminifera, nematodes and gutless phallodrilinid (symbiont-bearing) oligochaetes. Agglutinated foraminifera, harpacticoid copepods, polychaetes and many other macrofaunal taxa increased in relative abundance below the OMZ. During the study (midpoint of the 1997-98 El Ni (n) over tildeo), the upper OMZ boundary exhibited a significant deepening (to 190 m) relative to 'normal', non-El Ni (n) over tildeo conditions (< 100 m), possibly causing a mild, transient oxygenation over the upper slope (200-300 m) and reduction of the organic particle flux to the seabed. Future sampling may determine whether the Peru margin system exhibits dynamic responses to changing ENSO-related conditions. (C) 2002 Elsevier Science Ltd. All rights reserved.

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.

Levin, LA.  1991.  Interactions between metazoans and large, agglutinating protozoans: implications for the community structure of deep-sea benthos. American Zoologist. 31:886-900. AbstractWebsite

Large, agglutinating protozoans belonging to the Foraminiferida (suborder Astrorhizina) and the Xenophyophorea are conspicuous, often dominant faunal elements in the deep sea. A review of known and suspected interactions between these forms and metazoans reveals a potentially significant role for the protozoans in structuring deep-sea metazoan assemblages. Direct interactions include provision to metazoans of (a) hard or stable substratum, (b) refuge from predators or physical disturbance, and (c) access to enhanced dietary resources. In some instances, rhizopod tests may provide a nursery function. Xenophyophore modification of flow regimes, particle flux, bottom skin friction and sediment characteristics appear likely and are believed to account for altered composition and abundance of meiofauna and macrofauna in the vicinity of rhizopod tests. Some analogous interactions are observed between metazoans and biogenic sediment structures in shallow water. However, metazoan-rhizopod associations are hypothesized to be more highly developed and complex in the deep sea than are comparable shallow-water associations, due to rhizopod abilities to enhance scarce food resources and to low rates of disturbance in much of the deep sea. Agglutinating rhizopods appear to be a significant source of heterogeneity on the deep-sea floor and large tests often represent 'hotspots' of metazoan activity. As such, they are hypothesized to have contributed to the origin and maintenance of metazoan diversity in the deep sea by providing distinct microenvironments in which species can specialize.