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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.

Levin, LA, Dayton PK.  2009.  Ecological theory and continental margins: where shallow meets deep. Trends in Ecology & Evolution. 24:606-617.   10.1016/j.tree.2009.04.012   AbstractWebsite

Continental margins, where land becomes ocean and plunges to the deep sea, provide valuable food and energy resources, and perform essential functions such as carbon burial and nutrient cycling. They exhibit remarkably high species and habitat diversity, but this is threatened by our increasing reliance on the resources that margins provide, and by warming, expanding hypoxia and acidification associated with climate change. Continental margin ecosystems, with environments, constituents and processes that differ from those in shallow water, demand a new focus, in which ecological theory and experimental methods are brought to bear on management and conservation practices. Concepts of disturbance, diversity-function relationships, top-down versus bottom-up control, facilitation and meta-dynamics offer a framework for studying fundamental processes and understanding future change.

Fodrie, FJ, Levin LA, Rathburn AE.  2009.  High densities and depth-associated changes of epibenthic megafauna along the Aleutian margin from 2000-4200 m. Journal of the Marine Biological Association of the United Kingdom. 89:1517-1527.   10.1017/s0025315409000903   AbstractWebsite

The Aleutian margin is a dynamic environment underlying a productive coastal ocean and subject to frequent tectonic disturbance. In July 2004, We used over 500 individual bottom images from towed camera transects to investigate patterns of epibenthic megafaunal density and community composition on the contiguous Aleutian margin (53 degrees N 163 degrees W) at depths of 2000 m, 3200 m and 4200 M. We also examined the influence of vertical isolation on the megafaunal assemblage across a topographic rise at 3200 m, located 30 km from the main margin and elevated 800 m above the surrounding seafloor. In comparison to previous reports from bathyal and abyssal depths, megafaunal densities along the Aleutian margin were remarkably high, averaging 5.38 +/- 0.43 (mean +/- 1 standard error), 0.32 +/- 0.02 to 0.43 +/- 0.03 and 0.27 +/- 0.01 individuals m(-2) at 2000 m, 3200 m and 4200 m, respectively. Diversity at 2000 M Was elevated by 15-30% over the deeper sites (3200-4200 m) depending on the metric, while evenness was depressed by similar to 10%. Levels of richness and evenness were similar among the three deeper sites. Echinoderms were the most abundant phylum at each depth; ophiuroids accounted for 89% of individuals in photographs at 2000 m, echinoids were dominant at 3200 M (39%), and holothurians dominated at 4200 m (47%). We observed a 26% reduction in megafaunal density across the summit of the topographic rise relative to that documented on the continental slope at the same depth. However, the two communities at 3200 m were very similar in composition. Together, these data support the modified 'archibenthal zone of transition' framework for slope community patterns with distinct communities along the middle and lower slope (the upper slope was not evaluated here). This study fills a geographical gap by providing baseline information for a relatively pristine, high-latitude, deep-sea benthic ecosystem. As pressures grow for drilling, fishing and mining on high-latitude margins, such data can serve as a reference point for much-needed studies on the ecology, long-term dynamics, and anthropogenically induced change of these habitats.

Blankenship, LE, Levin LA.  2007.  Extreme food webs: Foraging strategies and diets of scavenging amphipods from the ocean's deepest 5 kilometers. Limnology and Oceanography. 52:1685-1697.   10.4319/lo.2007.52.4.1685   AbstractWebsite

We explore hypotheses that alternate foraging strategies, diet, or nutrient partitioning could help explain the success of scavenging Lysianassoids (Amphipoda) in hadal oligotrophic trenches (depths of 6-11 km) by examining the nutritional strategies of four lysianassoid species ( Eurythenes gryllus, Scopelocheirus schellenbergi, Hirondellea dubia, and Uristes sp. nov.) collected with baited traps (6.3-10.8 km) from the oligotrophic Tonga and Kermadec Trenches (southwest Pacific Ocean). Diets and foraging strategies were examined by use of (1) the nascent DNA-based analysis of hindgut contents, which provides a 'snapshot' of recently ingested organisms, and (2) natural abundance isotopic signatures, which reflect the source of nutrition and relative trophic position. The scavenging guild exhibits remarkable trophic plasticity, and each amphipod species employs alternate foraging modes, including detrivory or predation, to supplement necrophagy. The nutritional strategies of some species appear to shift with age, depth, and even between trenches. Thus, there is no single ubiquitous hadal food web; rather it is influenced by depth and overlying surface productivity. Isotopic data suggest that coexisting species partition the dietary items, providing evidence of competition among members of the scavenging guild. The extreme foraging flexibility of scavenging amphipods may ultimately contribute to their success in severely food-limited hadal ecosystems.

Gallardo, VA, Palma M, Carrasco FD, Gutierrez D, Levin LA, Canete JI.  2004.  Macrobenthic zonation caused by the oxygen minimum zone on the shelf and slope off central Chile. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 51:2475-2490.   10.1016/j.dsr2.2004.07.028   AbstractWebsite

The relationship between macrobenthic (greater than or equal to 300 mum) zonation and the oxygen minimum zone (OMZ: O(2) < 0.5 ml L(-1)) was studied in shelf and slope sediments (122-840 m depth) off Concepcion Bay, central Chile. Four study sites were sampled during March-April 1999 for abiotic factors, macrofaunal density, biomass, mean individual size, and diversity. Within the OMZ (122-206 m), the macrofaunal density was high (16,478-21,381 individuals m(-2)) and 69-89% of the organisms were soft-bodied. Density was highest (21,381 individuals m(-2)), biomass lowest (16.95 g wet weight m-2), and individual size smallest (0.07 mg C individuals) at the shelf break site (206 m). Polychaete worms made up 71% of the total abundance, crustaceans 16%, and mollusks only 2%. Total abundance beneath the OMZ (mid-slope site, similar to840 m) was 49% crustaceans and 43% polychaetes. Although existing literature originally led to the hypothesis that both diversity and biomass within the OMZ would be lower than beneath the OMZ, in the present study this was only true for diversity. Biomass distribution, on the other hand, was concave along the depth gradient; the highest values were near the upper edge of (122 m) and beneath (840 m) the OMZ. Indices of the macrofaunal community structure varied in relation to bottom-water oxygen concentration, chlorophyll-alpha, phaeopigments, and sulfide concentration, but not in relation to grain size, C, N, mud, porosity, redox potential, a bottom-water temperature. (C) 2004 Published by Elsevier Ltd.

Levin, LA, Boesch DF, Covich A, Dahm C, Erseus C, Ewel KC, Kneib RT, Moldenke A, Palmer MA, Snelgrove P, Strayer D, Weslawski JM.  2001.  The function of marine critical transition zones and the importance of sediment biodiversity. Ecosystems. 4:430-451.   10.1007/s10021-001-0021-4   AbstractWebsite

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.

Gooday, AJ, Bernhard JM, Levin LA, Suhr SB.  2000.  Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 47:25-54.   10.1016/s0967-0645(99)00099-5   AbstractWebsite

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 412m within the oxygen minimum zone (OMZ) (O(2) = 0.13 ml l(-1)), the other located at 3350 m, well below the main OMZ (O(2) similar to 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-mu m fraction) than at the 3350-m site (625 indiv.10 cm(-2)). Species richness (E(S(100))), 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-mu 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 mu m fraction) in the Santa Barbara Basin (590 and 610m depth; O(2) = 0.05 and 0.15 ml(-1) respectively), and macrofaunal foraminifera(> 300 mu m) on the Peru margin (300-1250 m depth: O(2) = 0.02-1.60 mi l(-1)), matched those observed on the Oman margin. Tn particular, soft-shelled monothalamous taxa were rare and large agglutinated taxa were absent in the most oxygen-depleted ( < 0.20 mi l(-1)) stations. 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 mu 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 mu 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 In. 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. (C) 1999 Elsevier Science Ltd. All rights reserved.

Levin, LA, Gage JD, Martin C, Lamont PA.  2000.  Macrobenthic community structure within and beneath the oxygen minimum zone, NW Arabian Sea. Deep-Sea Research Part Ii-Topical Studies in Oceanography. 47:189-226.   10.1016/s0967-0645(99)00103-4   AbstractWebsite

Investigations of macrobenthos were carried out within and beneath the oxygen minimum zone (OMZ, < 0.5 ml l(-1)) during Fall 1994 on the Oman margin, NW Arabian Sea. Six stations (400, 700, 850, 1000, 1250 and 3400m) were characterized with respect to macrofaunal abundance, biomass, body size, taxonomic composition, diversity and lifestyles, and the relation of these parameters to environmental conditions. The OMZ (400-1000 m) was dominated by a dense (5818-19,183 ind m(-2)), soft-bodied assemblage consisting largely (86-99%) of surface-feeding polychaetes, Spionids and cirratulids dominated at the 400- and 700-m stations, paraonids and ampharetids at the 850- and 1000-m stations. Molluscs and most crustaceans were common only below the OMZ ( greater than or equal to 1250 m); a species of the amphipod Ampelisca was abundant within the OMZ, however. Both density and biomass were elevated within the OMZ relative to stations below but body size did not differ significantly among stations. The lower OMZ boundary (0.5 ml l(-1)) was not a zone of enhanced macrofaunal standing stock, as originally hypothesized. However, abundance maxima at 700-850m may reflect an oxygen threshold (0.15-0.20 ml l(-1)) above which macrofauna take advantage of organically enriched sediments. Incidence of burrowing and subsurface-deposit feeding increased below the OMZ, Species richness (E[S(100)]), diversity (H') and evenness (J') were lower and dominance (R1D) was higher within than beneath the OMZ. Within-station (between-boxcore) faunal heterogeneity increased markedly below the OMZ. Surface sediment pigment concentrations and oxygen together explained 96-99% of the variance in measures of E[S(100)], H' and J' across the transect; grain size and % TOC did not yield significant regressions. Pigments, assumed to reflect food availability and possibly oxygen effects on organic matter preservation, were negatively correlated with species richness and evenness, and positively correlated with dominance. The reverse was true for water depth. Macrobenthic patterns of calcification and lifestyle within the Oman margin OMZ (0.13-0.3 mi l(-1)) match the dysaerobic biofacies of paleo-environmental reconstruction models. (C) 1999 Elsevier Science Ltd. All rights reserved.

Thistle, D, Levin LA.  1998.  The effect of experimentally increased near-bottom flow on metazoan meiofauna at a deep-sea site, with comparison data on macrofauna. Deep-Sea Research Part I-Oceanographic Research Papers. 45:625-+.   10.1016/s0967-0637(97)00101-5   AbstractWebsite

It has been argued that strong near-bottom hows affect macrofauna and meiofauna in the deep sea, but the evidence comes largely from studies that compared sites separated geographically by hundreds to thousands of kilometers and in depth by hundreds of meters. In this paper, the results of the first experimental investigation of the effects of strong near-bottom flow on deep-sea metazoan meiofauna are presented. At a site (32 degrees 27.581' N, 127 degrees 47.839' W) at 583 m depth on the Fieberling Guyot summit plain, the submersible Alvin emplaced weirs designed to increase the near-bottom flow locally. After 6.5 weeks, sediments in the weirs and unmanipulated locations in the vicinity were sampled. The abundances of nematodes, harpacticoid copepods, ostracods, and kinorhynchs, considered collectively and as individual taxa, were significantly lower in the weir samples than in the background samples. Parallel responses were observed in total macrofaunal and mollusk abundances. Proportional declines in kinorhynchs and mollusks were observed as well. These results suggest that strong near-bottom flow can reduce the abundance of meiofauna and macrofauna in the deep sea and alter assemblage composition. (C) 1998 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.

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.

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.