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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.

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.

Sato, KN, Powell J, Rudie D, Levin LA.  2018.  Evaluating the promise and pitfalls of a potential climate change-tolerant sea urchin fishery in southern California. Ices Journal of Marine Science. 75:1029-1041.   10.1093/icesjms/fsx225   AbstractWebsite

Marine fishery stakeholders are beginning to consider and implement adaptation strategies in the face of growing consumer demand and potential deleterious climate change impacts such as ocean warming, ocean acidification, and deoxygenation. This study investigates the potential for development of a novel climate change-tolerant sea urchin fishery in southern California based on Strongylocentrotus fragilis (pink sea urchin), a deep-sea species whose peak density was found to coincide with a current trap-based spot prawn fishery (Pandalus platyceros) in the 200-300-m depth range. Here we outline potential criteria for a climate change-tolerant fishery by examining the distribution, life-history attributes, and marketable qualities of S. fragilis in southern California. We provide evidence of seasonality of gonad production and demonstrate that peak gonad production occurs in the winter season. S. fragilis likely spawns in the spring season as evidenced by consistent minimum gonad indices in the spring/summer seasons across 4 years of sampling (2012-2016). The resiliency of S. fragilis to predicted future increases in acidity and decreases in oxygen was supported by high species abundance, albeit reduced relative growth rate estimates at water depths (485-510 m) subject to low oxygen (11.7-16.9 mmol kg similar to 1) and pHTotal (< 7.44), which may provide assurances to stakeholders and managers regarding the suitability of this species for commercial exploitation. Some food quality properties of the S. fragilis roe (e. g. colour, texture) were comparable with those of the commercially exploited shallow-water red sea urchin (Mesocentrotus franciscanus), while other qualities (e. g. 80% reduced gonad size by weight) limit the potential future marketability of S. fragilis. This case study highlights the potential future challenges and drawbacks of climate-tolerant fishery development in an attempt to inform future urchin fishery stakeholders.

Schaff, T, Levin L, Blair N, DeMaster D, Pope R, Boehme S.  1992.  Spatial heterogeneity of benthos on the Carolina continental slope: Large (100 km)-scale variation. Marine ecology progress series. Oldendorf. 88:143-160. AbstractWebsite

Large-scale spatial heterogeneity of macrofaunal and microbial communities was examined on the continental slope off North and South Carolina, USA, by comparing 3 sites, separated by 130 to 150 km and all at 850 m water depth. Significant variation was found among macrofaunal assemblages at all 3 sites, and between microbial counts at 2 sites. We investigated the hypothesis that 100 km scale heterogeneity was driven by variation in organic C flux to the sea floor. The northernmost site (Site III, off Cape Hatteras, NC) was found to have macrofaunal abundances (> 55,000 m super(-2)) higher than any previously recorded from this depth, and significantly higher than those at Site II (off Cape Lookout, NC) (21,319 m super(-2)) or Site I (off Charleston, SC) (9438 m super(-2)). Trends in macrofaunal abundance did not follow those of sediment TOC (total organic carbon), but agreed well with estimates of total carbon flux for the 3 sites. Mixing coefficients determined from profiles of naturally occurring super(234)Th (half life 24 d) indicate that the sediments at Site III are mixed 2 to 6 times faster than at the other 2 sites, which is consistent with the trends in macrofaunal abundance and biomass.

Schaff, TR, Levin LA.  1994.  Spatial heterogeneity of benthos associated with biogenic structures on the North Carolina continental slope. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 41:901-&.   10.1016/0967-0645(94)90053-1   AbstractWebsite

The objective of this study was to determine if biogenic features such as mounds, pits and tubes produce small-scale (0.1-100 m) spatial heterogeneity in macrofaunal community structure on the continental slope off North Carolina at 850 m. Macrofaunal and microbial communities associated with sediment mounds, pits and level areas were compared off Cape Lookout, North Carolina. No significant differences were found in sediment microbial counts or total macrofaunal distributions. One paraonid polychaete (Levensenia gracilis) was more abundant in pits than in the other samples, and infaunal anemones exhibited depressed densities in sediment mounds. At a second site, off Cape Hatteras, North Carolina, infaunal heterogeneity associated with the tube-building foraminiferan Bathysiphon filiformis was examined by comparing an area with high tube densities (93.8 m(-2)) with an area 100 m away without tubes. No significant differences were found in the distribution and abundances of bacteria between the two areas. The only significant difference found in infaunal densities was the presence of high numbers of reproductive oligochaetes in the 5-10 cm fraction beneath tube beds. One terebellid polychaete species (Nicolea sp.), which lives exclusively on B. filiformis tubes, was absent in the non-tube area. With a few exceptions, the biogenic structures examined at these two sites appeared to exert only minor influence on macrofaunal or microbial community structure. Within each site, slope assemblages examined in this study appeared to be homogeneous on the small scales examined.

Schander, C, Rapp HT, Kongsrud JA, Bakken T, Berge J, Cochrane S, Oug E, Byrkjedal I, Todt C, Cedhagen T, Fosshagen A, Gebruk A, Larsen K, Levin L, Obst M, Pleijel F, Stohr S, Waren A, Mikkelsen NT, Hadler-Jacobsen S, Keuning R, Petersen KH, Thorseth IH, Pedersen RB.  2010.  The fauna of hydrothermal vents on the Mohn Ridge (North Atlantic) *. Marine Biology Research. 6:155-171.: Taylor & Francis Group Ltd., 2 Park Square Oxford OX14 4RN UK   10.1080/17451000903147450   AbstractWebsite

not available.

Shankle, AM, Goericke R, Franks PJS, Levin LA.  2002.  Chlorin distribution and degradation in sediments within and below the Arabian Sea oxygen minimum zone. Deep-Sea Research Part I-Oceanographic Research Papers. 49:953-969.   10.1016/s0967-0637(01)00077-2   AbstractWebsite

The concentration of chlorophylla degradation products, i.e. chlorins, preserved in deep-sea sediments is a function of the amount of primary production input and the rate at which it is subsequently degraded. Sedimentary chlorins can be used as a proxy for paleoproductivity; however, our understanding of the factors controlling their preservation is limited. To study the effects of changes in export of primary production from the euphotic zone and of differences in depositional conditions on chlorin concentration in marine sediments, chlorins were analyzed by high pressure liquid chromatography from sediments taken within and below the oxygen minimum zone on the Oman margin in the Arabian Sea. Among five stations at water depths between 400 and 1250 m, variation in chlorin concentration in surface sediments (0-0.5 cm) was significantly related to water depth (used here as a proxy for chlorin fluxes to the sediments) and bottom-water oxygen concentration; the more important control on chlorin concentration of surficial sediments measured in this study is the amount of chlorins reaching the sediment. Chlorins decayed exponentially downcore (0-20 cm). The degradation of sedimentary chlorins was better described by a model in which chlorins decayed at different rates within and below the sediment mixed layer. The degradation rates within the mixed layer were 0.0280 +/- 0.0385 yr(-1) (t(1/2) = 73 yr). Below the mixed layer, degradation rates were one to two orders of magnitude less, ranging from 0.0022 +/- 0.0025 yr(-1) (t(1/2) = 680 yr). Many stations had subsurface chlorin concentration peaks between 6 and 10 cm depth. The most likely explanation for these peaks is a period of increased deposition of chlorins in the past. This could result from changes in local depositional environment or a more general increase in surface production resulting in an increased sedimentation of chlorins to the sediments 500-1000 years ago. Chlorins are a useful indicator of the magnitude of chlorin deposition; however their usage as indicators of paleoproductivity is more complicated. (C) 2002 Elsevier Science Ltd. All rights reserved.

Smith, CR, Levin LA, Hoover DJ, McMurtry G, Gage JD.  2000.  Variations in bioturbation across the oxygen minimum zone in the northwest Arabian Sea. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 47:227-257.   10.1016/s0967-0645(99)00108-3   AbstractWebsite

Oxygen minimum zones are expected to alter substantially the nature, rates and depths of bioturbation along continental margins, yet these effects remain poorly studied. Using excess (210)Pb profiles, sediment X-radiography and box-core samples for macrofauna, we examined bioturbation processes at six stations (400, 700, 850, 1000, 1250 and 3400 m deep) along a transect across the oxygen minimum zone (OMZ) on the Oman margin. Bottom-water oxygen concentrations ranged from similar to 0.13 mi l(-1) at 400 m to similar to 2.99 mi l(-1) at 3400 m. (210)Pb mixed-layer depth and bioturbation intensity (D(b)) exhibited high within-station variance, and means did not differ significantly among stations. However, the mean mixed-layer depth (4.6 cm) for pooled OMZ stations (400-1000 m depths, 0.13-0.27 mi l(-1) bottom-water oxygen) was half that for stations from similar water depths along well-oxygenated Atlantic and Pacific slopes (11.1 cm), suggesting that oxygen stress reduced (210)Pb mixing depth on the Oman margin. Modal burrow diameter and the diversity of burrow types at a station were highly correlated with bottom-water oxygen concentration from the edge to the core of the Oman OMZ (Spearman's rho greater than or equal to 0.89, p less than or equal to 0.02), suggesting that these parameters are useful proxies for bottom-water oxygen concentrations under dysaerobic conditions. In contrast, neither the maximum diameter and nor the maximum penetration depth of open burrows exhibited oxygen-related patterns along the transect. Reduced (210)Pb mixing depth within the Oman-margin OMZ appeared to result from a predominance of surface-deposit feeders and tube builders within this zone, rather than from simple changes in horizontal or vertical distributions of macrofaunal abundance or biomass. The number of burrow types per station was highly correlated with macrofaunal species diversity, suggesting that burrow diversity may be a good proxy for species diversity in paleo-dysaerobic assemblages. We conclude that bottom-water oxygen concentrations of 0.13-0.27 mi l(-1) substantially alter a number of bioturbation parameters of importance to diagenetic and biofacies models for continental margins. (C) 1999 Elsevier Science Ltd. All rights reserved.

Smith, CR, Levin LA, Mullineaux LS.  1998.  Deep-sea biodiversity: a tribute to Robert R. Hessler. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 45:1-11.   10.1016/s0967-0645(97)00088-x   AbstractWebsite

Through extraordinary research and training of graduate students, Robert R. Hessler has profoundly influenced our knowledge of biodiversity in the deep sea. This special volume honors his contributions and presents recent advances in the study of deep-sea biodiversity on a broad range of topics. (C) 1998 Elsevier Science Ltd. All rights reserved.

Sperling, EA, Frieder CA, Levin LA.  2016.  Biodiversity response to natural gradients of multiple stressors on continental margins. Proceedings of the Royal Society of London B: Biological Sciences. 283   10.1098/rspb.2016.0637   Abstract

Sharp increases in atmospheric CO2 are resulting in ocean warming, acidification and deoxygenation that threaten marine organisms on continental margins and their ecological functions and resulting ecosystem services. The relative influence of these stressors on biodiversity remains unclear, as well as the threshold levels for change and when secondary stressors become important. One strategy to interpret adaptation potential and predict future faunal change is to examine ecological shifts along natural gradients in the modern ocean. Here, we assess the explanatory power of temperature, oxygen and the carbonate system for macrofaunal diversity and evenness along continental upwelling margins using variance partitioning techniques. Oxygen levels have the strongest explanatory capacity for variation in species diversity. Sharp drops in diversity are seen as O2 levels decline through the 0.5–0.15 ml l−1 (approx. 22–6 µM; approx. 21–5 matm) range, and as temperature increases through the 7–10°C range. pCO2 is the best explanatory variable in the Arabian Sea, but explains little of the variance in diversity in the eastern Pacific Ocean. By contrast, very little variation in evenness is explained by these three global change variables. The identification of sharp thresholds in ecological response are used here to predict areas of the seafloor where diversity is most at risk to future marine global change, noting that the existence of clear regional differences cautions against applying global thresholds.

Sperling, EA, Frieder CA, Raman AV, Girguis PR, Levin LA, Knoll AH.  2013.  Oxygen, ecology, and the Cambrian radiation of animals. Proceedings of the National Academy of Sciences of the United States of America. 110:13446-13451.   10.1073/pnas.1312778110   AbstractWebsite

The Proterozoic-Cambrian transition records the appearance of essentially all animal body plans (phyla), yet to date no single hypothesis adequately explains both the timing of the event and the evident increase in diversity and disparity. Ecological triggers focused on escalatory predator-prey "arms races" can explain the evolutionary pattern but not its timing, whereas environmental triggers, particularly ocean/atmosphere oxygenation, do the reverse. Using modern oxygen minimum zones as an analog for Proterozoic oceans, we explore the effect of low oxygen levels on the feeding ecology of polychaetes, the dominant macrofaunal animals in deep-sea sediments. Here we show that low oxygen is clearly linked to low proportions of carnivores in a community and low diversity of carnivorous taxa, whereas higher oxygen levels support more complex food webs. The recognition of a physiological control on carnivory therefore links environmental triggers and ecological drivers, providing an integrated explanation for both the pattern and timing of Cambrian animal radiation.

Springer, AE, Stevens LE, Anderson DE, Partnell RA, Kreamer DK, Levin LA, Flora S.  2008.  A comprehensive springs classification system. Integrating geomorphic, hydrogeochemical, and ecological criteria. Aridland springs in North America: ecology and conservation. ( Stevens LE, Meretsky VJ, Eds.).:49-75., Tucson: University of Arizona Press and the Arizona-Sonora Desert Museum Abstract
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Stramma, L, Schmidtko S, Levin LA, Johnson GC.  2010.  Ocean oxygen minima expansions and their biological impacts. Deep-Sea Research Part I-Oceanographic Research Papers. 57:587-595.   10.1016/j.dsr.2010.01.005   AbstractWebsite

Climate models with biogeochemical components predict declines in oceanic dissolved oxygen with global warming. In coastal regimes oxygen deficits represent acute ecosystem perturbations Here, we estimate dissolved oxygen differences across the global tropical and subtropical oceans within the oxygen minimum zone (200-700-dbar depth) between 1960-1974 (an early period with reliable data) and 1990-2008 (a recent period capturing ocean response to planetary warming) In most regions of the tropical Pacific. Atlantic, and Indian Oceans the oxygen content in the 200-700-dbar layer has declined. Furthermore, at 200 dbar, the area with O(2) < 70 mu mol kg(-1) where some large mobile macro-organisms are unable to abide, has increased by 4.5 million km(2) The tropical low oxygen zones have expanded horizontally and vertically Subsurface oxygen has decreased adjacent to most continental shelves However, oxygen has increased in sonic regions in the subtropical gyres at the depths analyzed According to literature discussed below, fishing pressure is strong in the open ocean, which may make it difficult to isolate the impact of declining oxygen on fisheries At shallower depths we predict habitat compression will occur for hypoxia-intolerant taxa, with eventual loss of biodiversity. Should past trends in observed oxygen differences continue into the future, shifts in animal distributions and changes in ecosystem structure could accelerate (C) 2010 Elsevier Ltd. All rights reserved

Sweetman, AK, Thurber AR, Smith CR, Levin LA, Mora C, Wei CL, Gooday AJ, Jones DOB, Rex M, Yasuhara M, Ingels J, Ruhl HA, Frieder CA, Danovaro R, Wurzberg L, Baco A, Grupe BM, Pasulka A, Meyer KS, Dunlop KM, Henry LA, Roberts JM.  2017.  Major impacts of climate change on deep-sea benthic ecosystems. Elementa-Science of the Anthropocene. 5:1-23.   10.1525/elementa.203   AbstractWebsite

The deep sea encompasses the largest ecosystems on Earth. Although poorly known, deep seafloor ecosystems provide services that are vitally important to the entire ocean and biosphere. Rising atmospheric greenhouse gases are bringing about significant changes in the environmental properties of the ocean realm in terms of water column oxygenation, temperature, pH and food supply, with concomitant impacts on deep-sea ecosystems. Projections suggest that abyssal (3000-6000 m) ocean temperatures could increase by 1 degrees C over the next 84 years, while abyssal seafloor habitats under areas of deep-water formation may experience reductions in water column oxygen concentrations by as much as 0.03 mL L-1 by 2100. Bathyal depths (200-3000 m) worldwide will undergo the most significant reductions in pH in all oceans by the year 2100 (0.29 to 0.37 pH units). O-2 concentrations will also decline in the bathyal NE Pacific and Southern Oceans, with losses up to 3.7% or more, especially at intermediate depths. Another important environmental parameter, the flux of particulate organic matter to the seafloor, is likely to decline significantly in most oceans, most notably in the abyssal and bathyal Indian Ocean where it is predicted to decrease by 40-55% by the end of the century. Unfortunately, how these major changes will affect deep-seafloor ecosystems is, in some cases, very poorly understood. In this paper, we provide a detailed overview of the impacts of these changing environmental parameters on deep-seafloor ecosystems that will most likely be seen by 2100 in continental margin, abyssal and polar settings. We also consider how these changes may combine with other anthropogenic stressors (e.g., fishing, mineral mining, oil and gas extraction) to further impact deep-seafloor ecosystems and discuss the possible societal implications.