Publications

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2016
Moseman-Valtierra, S, Levin LA, Martin RM.  2016.  Anthropogenic impacts on nitrogen fixation rates between restored and natural Mediterranean salt marshes. Marine Ecology-an Evolutionary Perspective. 37:370-379.   10.1111/maec.12289   AbstractWebsite

To test the effects of site and successional stage on nitrogen fixation rates in salt marshes of the Venice Lagoon, Italy, acetylene reduction assays were performed with Salicornia veneta- and Spartina townsendii-vegetated sediments from three restored (6-14years) and two natural marshes. Average nitrogen fixation (acetylene reduction) rates ranged from 31 to 343 mu mol C2H4.m(-2.)h(-1) among all marshes, with the greatest average rates being from one natural marsh (Tezze Fonde). These high rates are up to six times greater than those reported from Southern California Spartina marshes of similar Mediterranean climate, but substantially lower than those found in moister climates of the Atlantic US coast. Nitrogen fixation rates did not consistently vary between natural and restored marshes within a site (Fossei Est, Tezze Fonde, Cenesa) but were negatively related to assayed plant biomass within the acetylene reduction samples collected among all marshes. Highest nitrogen fixation rates were found at Tezze Fonde, the location closest to the city of Venice, in both natural and restored marshes, suggesting possible site-specific impacts of anthropogenic stress on marsh succession.

2015
Nordstrom, MC, Demopoulos AWJ, Whitcraft CR, Rismondo A, McMillan P, Gonzalez JP, Levin LA.  2015.  Food web heterogeneity and succession in created saltmarshes. Journal of Applied Ecology. 52:1343-1354.   10.1111/1365-2664.12473   AbstractWebsite

Ecological restoration must achieve functional as well as structural recovery. Functional metrics for re-establishment of trophic interactions can be used to complement traditional monitoring of structural attributes. In addition, topographic effects on food web structure provide added information within a restoration context; often, created sites may require spatial heterogeneity to effectively match structure and function of natural habitats. We addressed both of these issues in our study of successional development of benthic food web structure, with focus on bottom-up-driven changes in macroinvertebrate consumer assemblages in the saltmarshes of the Venice Lagoon, Italy. We combined quantified estimates of the changing community composition with stable isotope data (C-13:C-12 and N-15:N-14) to compare the general trophic structure between created (2-14years) marshes and reference sites and along topographic elevation gradients within saltmarshes. Macrofaunal invertebrate consumers exhibited local, habitat-specific trophic patterns. Stable isotope-based trophic structure changed with increasing marsh age, in particular with regard to mid-elevation (Salicornia) habitats. In young marshes, the mid-elevation consumer signatures resembled those of unvegetated ponds. The mid-elevation of older and natural marshes had a more distinct Salicornia zone food web, occasionally resembling that of the highest (Sarcocornia-dominated) elevation. In summary, this indicates that primary producers and availability of vascular plant detritus structure consumer trophic interactions and the flow of carbon. Functionally different consumers, subsurface-feeding detritivores (Oligochaeta) and surface grazers (Hydrobia sp.), showed distinct but converging trajectories of isotopic change over time, indicating that successional development may be asymmetric between brown' (detrital) guilds and green' (grazing) guilds in the food web.Synthesis and applications. Created marsh food webs converged into a natural state over about a decade, with successional shifts seen in both consumer community composition and stable isotope space. Strong spatial effects were noted, highlighting the utility of stable isotopes to evaluate functional equivalence in spatially heterogeneous systems. Understanding the recovery of functional properties such as food web support, and their inherent spatial variability, is key to planning and managing successful habitat restoration. Created marsh food webs converged into a natural state over about a decade, with successional shifts seen in both consumer community composition and stable isotope space. Strong spatial effects were noted, highlighting the utility of stable isotopes to evaluate functional equivalence in spatially heterogeneous systems. Understanding the recovery of functional properties such as food web support, and their inherent spatial variability, is key to planning and managing successful habitat restoration.

2014
Nordstrom, MC, Currin CA, Talley TS, Whitcraft CR, Levin LA.  2014.  Benthic food-web succession in a developing salt marsh. Marine Ecology Progress Series. 500:43-U69.   10.3354/meps10686   AbstractWebsite

Ecological succession has long been a focal point for research, and knowledge of underlying mechanisms is required if scientists and managers are to successfully promote recovery of ecosystem function following disturbance. We addressed the influence of bottom-up processes on successional assemblage shifts in salt marshes, ecosystems with strong physical gradients, and how these shifts were reflected in the trophic characteristics of benthic fauna. We tracked the temporal development of infaunal community structure and food-web interactions in a young, created salt marsh and an adjacent natural marsh in Mission Bay, California, USA (1996-2003). Macro faunal community succession in created Spartina foliosa habitats occurred rapidly, with infaunal densities reaching 70% of those in the natural marsh after 1 yr. Community composition shifted from initial dominance of insect larvae (surface-feeding microalgivores) to increased dominance of oligo chaetes (subsurface-feeding detritivores) within the first 7 yr. Isotopic labeling of microalgae, N-2-fixing cyanobacteria, S. foliosa and bacteria revealed direct links (or absence thereof) between these basal food sources and specific consumer groups. In combination with the compositional changes in the macroinvertebrate fauna, the trophic patterns indicated an increase in food-web complexity over time, reflecting resource-driven marsh succession. Natural abundance stable isotope ratios of salt marsh consumers (infaunal and epifaunal macroinvertebrates, and fish) initially reflected distinctions in trophic structure between the created and natural marsh, but these diminished during successional development. Our findings suggest that changing resource availability is one of the important drivers of succession in benthic communities of restored wetlands in Southern California.

2008
Whitcraft, CR, Levin LA, Talley D, Crooks JA.  2008.  Utilization of invasive tamarisk by salt marsh consumers. Oecologia. 158:259-272.   10.1007/s00442-008-1144-5   AbstractWebsite

Plant invasions of coastal wetlands are rapidly changing the structure and function of these systems globally. Alteration of litter dynamics represents one of the fundamental impacts of an invasive plant on salt marsh ecosystems. Tamarisk species (Tamarix spp.), which extensively invade terrestrial and riparian habitats, have been demonstrated to enter food webs in these ecosystems. However, the trophic impacts of the relatively new invasion of tamarisk into marine ecosystem have not been assessed. We evaluated the trophic consequences of invasion by tamarisk for detrital food chains in the Tijuana River National Estuarine Research Reserve salt marsh using litter dynamics techniques and stable isotope enrichment experiments. The observations of a short residence time for tamarisk combined with relatively low C:N values indicate that tamarisk is a relatively available and labile food source. With an isotopic ((15)N) enrichment of tamarisk, we demonstrated that numerous macroinvertebrate taxonomic and trophic groups, both within and on the sediment, utilized (15)N derived from labeled tamarisk detritus. Infaunal invertebrate species that took up no or limited (15)N from labeled tamarisk (A. californica, enchytraeid oligochaetes, coleoptera larvae) occurred in lower abundance in the tamarisk-invaded environment. In contrast, species that utilized significant (15)N from the labeled tamarisk, such as psychodid insects, an exotic amphipod, and an oniscid isopod, either did not change or occurred in higher abundance. Our research supports the hypothesis that invasive species can alter the trophic structure of an environment through addition of detritus and can also potentially impact higher trophic levels by shifting dominance within the invertebrate community to species not widely consumed.

2002
Levin, LA, Michener RH.  2002.  Isotopic evidence for chemosynthesis-based nutrition of macrobenthos: The lightness of being at Pacific methane seeps. Limnology and Oceanography. 47:1336-1345. AbstractWebsite

The importance of chemosynthetic nutritional pathways was examined for macrofaunal invertebrates (>300 mum) from methane seeps in the Gulf of Alaska (4,413-4,443 m), on the Oregon margin (590 m), and on the northern California slope [Eel River margin] (520 m) by use of natural abundance stable isotopic data. Seep macrofauna exhibited lighter delta(13)C and delta(15)N values than those in nonseep sediments, but isotopic signatures varied among seep sites. Macrofaunal isotopic signatures indicated chemosynthetically fixed carbon sources with a significant contribution from methane-derived carbon (MDC) in macrofauna from sediments of pogonophoran fields (average delta(13)C, -46.44parts per thousand, 32%-51% MDC) and Calyptogena phaseoliformis beds (average delta(13)C, -40.89parts per thousand, 12%-40% MDC) in the Gulf of Alaska and in microbial mat sediments on the Oregon margin (average delta(13)C, -43.80parts per thousand, 20%-44% MDC). Lesser influence of MDC was noted in macrofauna from sediments of Calyptogena pacifica beds on the Oregon (average delta(13)C, -33.38parts per thousand, 0%-27% MDC) and California (delta(13)C, -25.10parts per thousand, 0%-22% MDC) margins and from California microbial mat sediments (delta(13)C, -22.23%o, 0%-5% MDC). Although most macrofauna appeared to be heterotrophic, light delta(15)N and delta(13)C values together provided evidence for chemoautotrophic symbioses in selected taxa. Carbon isotopic signatures were consistent with consumption of methane-oxidizing archaea by some dorvilleid polychaetes (delta(13)C, -90.62parts per thousand and -73.80parts per thousand) and with grazing on filamentous sulfur bacteria by gastropods and polychaetes from the Oregon and California seeps. The importance of chemosynthetic trophic pathways varies regionally and among microhabitats, taxonomic groups, and feeding guilds.

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.

2000
Rathburn, AE, Levin LA, Held Z, Lohmann KC.  2000.  Benthic foraminifera associated with cold methane seeps on the northern California margin: Ecology and stable isotopic composition. Marine Micropaleontology. 38:247-266.   10.1016/s0377-8398(00)00005-0   AbstractWebsite

Release of methane from large marine reservoirs has been linked to climate change, as a causal mechanism and a consequence of temperature changes, during the Quaternary and the Paleocene. These inferred linkages are based primarily on variations in benthic foraminiferal stable isotope signatures. Few modem analog data exist, however, to assess the influence of methane flux on the geochemistry or faunal characteristics of benthic foraminiferal assemblages. Here we present analyses of the ecology and stable isotopic compositions of living (Rose Bengal stained) and dead (fossil) foraminifera (>150 mu m) from cold methane seeps on the slope off of the Eel River, northern California (500-525 m), and discuss potential applications for reconstructions of methane release in the past and present. Calcareous foraminiferal assemblages associated with Calyptogena clam bed seeps were comprised of species that are also found in organic-rich environments. Cosmopolitan, paleoceanographically important taxa were abundant; these included Uvigerina, Bolivina, Chilostomella, Globobulimina, and Nonionella. We speculate that seep foraminifera are attracted to the availability of food at cold seeps, and require no adaptations beyond those needed for life in organic-rich, reducing environments. Oxygen isotopic values of the tests of living foraminiferal assemblages from seeps had a high range (up to 0.69 parts per thousand) as did carbon isotopic values (up to 1.02 parts per thousand). Many living foraminiferal isotope values were within the range exhibited by the same or similar species in non-seep environments. Carbon isotopic values of fossil foraminifera found deeper in the sediments (18-20 cm), however, were 4.10 parts per thousand (U. peregrina) and 3.60 parts per thousand (B. subargentea) more negative than living delta(13)C values. These results suggest that delta(13)C values of foraminiferal tests reflect methane seepage and species-specific differences in isotopic composition, and can indicate temporal variations in seep activity. A better understanding of foraminiferal ecology and stable isotopic composition will enhance paleo-seep recognition, and improve interpretations of climatic and paleoceanographic change. (C) 2000 Elsevier Science B.V. All rights reserved.

Levin, LA, James DW, Martin CM, Rathburn AE, Harris LH, Michener RH.  2000.  Do methane seeps support distinct macrofaunal assemblages? Observations on community structure and nutrition from the northern California slope and shelf Marine Ecology-Progress Series. 208:21-39.   10.3354/meps208021   AbstractWebsite

Although the conspicuous epifauna of reducing environments are known to exhibit strong morphological, physiological, and nutritional adaptations for life in these habitats, it is less clear whether infaunal organisms do so as well. We examined metazoan macrofauna from methane-seep sediments on the northern California slope (500 to 525 m depth) and from seep and non-seep sediments at 3 locations on the shelf (31 to 53 m depth) to determine whether the community structure and nutritional sources of seep infauna were distinct from those in non-seep, margin sediments. Seep macrofauna consisted mainly of normal slope and shelf species found in productive settings. Several macrofaunal taxa, such as Capitella sp., Diastylopsis dawsoni, and Synidotea angulata, exhibited a preference for seeps. Other taxa, such as the amphipods Rhepoxynius abronius and R, daboius, avoided seeps. Species richness of shelf macrofauna, evaluated by rarefaction and diversity indices (H' and J'), generally did not differ in seep and non-seep sediments. Similarly, stable isotopic composition (delta C-13, delta N-15) Of active seep and non-seep macrofauna did not differ at the 3 shelf sites. Stable isotopic analyses of calcareous material confirmed the presence of methane-influenced pore waters at the slope study site. At one slope clam bed, macrofaunal delta C-13 signatures were lower and delta N-15 values were higher than at another clam bed, inactive slope sediments and shelf sites. However, only 1 of 14 macrofaunal taxa (a dorvilleid polychaete) exhibited isotopic evidence of chemosynthetic nutritional sources. At these sites, seep influence on the ecology of continental margin infauna appears spatially limited and relatively subtle. At their current level of activity, the northern California slope and shelf seeps appear to function as ephemeral, small-scale disturbances that are not sufficiently persistent to allow chemosynthesis-based trophic specialization by most infauna. Rather, we suggest that many of the infauna inhabiting these seep sediments are shelf and slope species preadapted to organic-rich, reducing environments.

1998
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.

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.