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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.

Levin, LA, Mendoza GF.  2007.  Community structure and nutrition of deep methane-seep macrobenthos from the North Pacific (Aleutian) Margin and the Gulf of Mexico (Florida Escarpment). Marine Ecology-an Evolutionary Perspective. 28:131-151.   10.1111/j.1439-0485.2006.00131.x   AbstractWebsite

Methane seeps occur at depths extending to over 7000 m along the world's continental margins, but there is little information about the infaunal communities inhabiting sediments of seeps deeper than 3000 m. Biological sampling was carried out off Unimak Island (3200-3300 m) and Kodiak Island (4500 m) on the Aleutian margin, Pacific Ocean and along the Florida Escarpment (3300 m) in the Gulf of Mexico to investigate the community structure and nutrition of macrofauna at these sites. We addressed whether there are characteristic infaunal communities common to the deep-water seeps or to the specific habitats (clam beds, pogonophoran fields, and microbial mats) studied here, and ask how these differ from background communities or from shallow-seep settings sampled previously. We also investigated, using stable isotopic signatures, the utilization of chemosynthetically fixed and methane-derived organic matter by macrofauna from different regions and habitats. Within seep sites, macrofaunal densities were the greatest in the Florida microbial mats (20,961 +/- 11,618 ind(.)m(2)), the lowest in the Florida pogonophoran fields (926 +/- 132 ind(.)m(2)), and intermediate in the Unimak and Kodiak seep habitats. Seep macrofaunal densities differed from those in nearby non-seep sediments only in Florida mat habitats, where a single, abundant species of hesionid polychaete comprised 70% of the macrofauna. Annelids were the dominant taxon (> 60%) at all sites and habitats except in Florida background sediments (33%) and Unimak pogonophoran fields (27%). Macrofaunal diversity (H') was lower at the Florida than the Alaska seeps, with a trend toward reduced richness in clam bed relative to pogonophoran field or non-seep sediments. Community composition differences between seep and non-seep sediments were evident in each region except for the Unimak margin, but pogonophoran and clam bed macrofaunal communities did not differ from one another in Alaska. Seep VC and delta N-15 signatures were lighter for seep than non-seep macrofauna in all regions, indicating use of chemosynthetically derived carbon. The lightest delta C-13 values (average of species' means) were observed at the Florida escarpment (-42.87 parts per thousand). We estimated that on average animal tissues had up to 55% methane-derived carbon in Florida mats, 3144% in Florida clam beds and Kodiak clam beds and pogonophoran fields, and 9-23% in Unimak seep habitats. However, some taxa such as hesionid and capitellid polychaetes exhibited tremendous intraspecific 613C variation (> 307.0) between patch types. Overall we found few characteristic communities or features common to the three deep-water seeps (> 3000 m), but common properties across habitats (mat, clam bed, pogonophorans), independent of location or water depth. In general, macrofaunal densities were lower (except at Florida microbial mats), community structure was similar, and reliance on chemosynthesis was greater than observed in shallower seeps off California and Oregon.

Levin, LA, Ziebis W, Mendoza GF, Growney-Cannon V, Walther S.  2006.  Recruitment response of methane-seep macrofauna to sulfide-rich sediments: An in situ experiment. Journal of Experimental Marine Biology and Ecology. 330:132-150.   10.1016/j.jembe.2005.12.022   AbstractWebsite

Hydrodynamically unbiased colonization trays were deployed for 6 months (Oct. 2000 to April 2001) on the northern California margin (Eel R. region; 525 m) to examine macrofaunal colonization rates at methane seeps. The influence of sulfide on recruitment and survival was examined by deploying sediments with and without sulfide added; effect of seep proximity was evaluated by placing trays inside and outside seeps. The trays contained a two-layer system mimicking vesicomyid clam bed habitat geochemistry, with 89 9 mM sulfide in a lower agar layer at the start of the experiment. After 6 month on the seabed, the lower agar layer contained 2-4 mM H2S. We observed rapid macrofaunal colonization equivalent to 50% of initial non-seep ambient densities. There was no difference in total colonizer densities, number of species, or rarefaction diversity among 3 treatments: (1) controls (no sulfide added) placed outside seeps, (2) trays with sulfide added placed outside seeps and (3) trays with sulfide added placed inside seep patches. Colonization trays with sulfide placed at seeps had different species composition from trays without sulfide place outside seeps; there were more amphipods (non-ampeliscid) and cumaceans in the seep/sulfide treatment and more nemerteans, Nephtys cornuta and tanaids in the non-seep/no-sulfide treatment. Outside seeps, annelids comprised <15% of tray colonists; within seep patches, annelids comprised 5 of the top 10 dominant colonizing taxa (24% of the total). The polychaetes Mediomastus sp., Aphelochaeta sp., Paraonidae sp., and Nerillidae sp. exhibited significantly higher densities in sulfide additions. Tanaids, echinoderms, and N. cornuta exhibited sulfide avoidance. At least 6 dorvilleid polychaete species colonized the experiments. Of these, 4 species occurred exclusively in trays with sulfide added and 80% of all dorvilleid individuals were found in trays with sulfide placed inside seep sediments. Counts of large sulfur bacterial filaments were positively correlated with maximum sulfide concentration in each tray, and with proximity of sulfide to the sediment surface. However, total macrofaunal densities were not correlated with tray sulfide concentrations. As a group, tray assemblages achieved some but not all characteristics of ambient seep assemblages after 6-month exposure on the sea floor. Distinctive colonization patterns at methane seeps contribute to the dynamic mosaic of habitat patches that characterize the eastern Pacific continental margin. Overall, proximity of seep habitats had at least as great an influence on macrofaunal colonization as tray sulfide concentrations. Taxa characteristic of seep sediments were more likely to settle into trays placed inside rather than outside seep patches. Whether this is due to limited dispersal ability or local geochemical cues remains to be determined. (C) 2005 Elsevier B.V. All rights reserved.

Levin, LA, Neira C, Grosholz ED.  2006.  Invasive cordgrass modifies wetland trophic function. Ecology. 87:419-432.   10.1890/04-1752   AbstractWebsite

Vascular plants strongly control belowground environments in most ecosystems. Invasion by vascular plants in coastal wetlands, and by cordgrasses (Spartina spp.) in particular, are increasing in incidence globally, with dramatic ecosystem-level consequences. We examined the trophic consequences of' invasion by a Spartina hybrid (S. alterniflora X S. foliosa) in San Francisco Bay (USA) by documenting differences in biomass and trophic structure of benthic communities between sediments invaded by Spartina and uninvaded sediments. We found the invaded system shifted from all algae-bascd to a detritus-based food web. We then tested for a relationship between diet and tolerance to invasion, hypothesizing that species that consume Spartina detritus are more likely to inhabit invaded sediments than those that consume surface algae. Infaunal diets were initially examined with natural abundance stable isotope analyses and application of mixing models, but these yielded an ambiguous picture of food sources. Therefore, we conducted isotopic enrichment experiments by providing N-15-labeled Spartina detritus both on and below the sediment surface in areas that either contained Spartina or were unvegetated. Capitellid and nereid polychaetes, and oligochaetes, groups shown to persist following Spartina invasion of San Francisco Bay tidal flats, took up N-15 from labeled native and invasive Spartina detritus. In contrast, We found that amphipods, bivalves, and other taxa less tolerant to invasion consumed primarily surficial algae, based oil C-13 enrichment experiments. Habitat (Spartina vs. unvegetated patches) and location of' detritus (on or within sediments) did not affect N-15 uptake from cletritus. Our investigations support a "trophic shift" model for ecosystem response to wetland plant invasion and preview loss of key trophic support for fishes and migratory birds by shifting dominance to species not widely consumed by species at higher trophic levels.

Neira, C, Levin LA, Grosholz ED.  2005.  Benthic macrofaunal communities of three sites in San Francisco Bay invaded by hybrid Spartina, with comparison to uninvaded habitats. Marine Ecology-Progress Series. 292:111-126.   10.3354/meps292111   AbstractWebsite

A hybrid cordgrass, formed from a cross between Spartina alterniflora (Atlantic cordgrass) and S. foliosa (Pacific cordgrass), has recently spread within the intertidal zone of south San Francisco Bay. Sediment properties and macroinfaunal community structure were compared in patches invaded by Spartina hybrid and adjacent uninvaded patches at 3 sites in San Francisco Bay (2 tidal flats and 1 Salicornia marsh). We hypothesized that (1) sediments vegetated by Spartina hybrid would have reduced sediment grain size, higher organic matter content, lower redox potential, lower salinity and reduced microalgal biomass relative to adjacent unvegetated tidal flat sediments, and (2) that differences in the sediment environment would correspond to changes in the infaunal invertebrate community structure and feeding modes. We observed 75 % lower total macro-faunal density and lower species richness in Spartina-vegetated sediments at Elsie Roemer (30 yr old invasion) than in an adjacent unvegetated tidal flat. This was due to lower densities of surface-feeding amphipods, bivalves, cirratulid and spionid polychaetes. The proportional representation of subsurface-deposit feeders was greater in Spartina patches than in unvegetated sediments. At a more recently invaded site (Roberts Landing; 15 yr invasion), Spartina patches differed from tidal flat sediments in composition, but not in abundance. Native (Salicornia) and Spartina patches exhibited similar sediment properties at San Mateo, where the Spartina hybrid invaded 8 to 10 yr earlier. No differences were detected in densities or proportions of surface- or subsurface-deposit feeders, but the proportion of carnivores/omnivores and grazers increased in the hybrid-invaded patches. These studies suggest that the invasive Spartina hybrid in south San Francisco Bay can have differing effects on sediment ecosystems, possibly depending on the location, age, or type of habitats involved.

Moseman, SM, Levin LA, Currin C, Forder C.  2004.  Colonization, succession, and nutrition of macrobenthic assemblages in a restored wetland at Tijuana Estuary, California. Estuarine Coastal and Shelf Science. 60:755-770.   10.1016/j.ecss.2004.03.013   AbstractWebsite

Modes of colonization, the successional trajectory, and trophic recovery of a macrofaunal community were analyzed over 19 months in the Friendship marsh, a 20-acre restored wetland in Tijuana Estuary, California. Traditional techniques for quantifying macrofaunal communities were combined with emerging stable isotopic approaches for evaluation of trophic recovery, making comparisons with a nearby natural Spartina foliosa habitat. Life history-based predictions successfully identified major colonization modes, although most taxa employed a variety of tactics for colonizing the restored marsh. The presence of S.foliosa did not seem to affect macrofaunal colonization or succession at the scale of this study. However, soil organic matter content in the restored marsh was positively correlated with insect densities, and high initial salinities may have limited the success of early colonists. Total macrofaunal densities recovered to natural marsh levels after 14 months and diversity, measured as species richness and the Shannon index (H'), was comparable to the natural marsh by 19 months. Some compositional disparities between the natural and created communities persisted after 19 months, including lower percentages of surface-feeding polychaetes (Polydora spp.) and higher percentages of dipteran insects and turbellarians in the Friendship marsh. As surficial structural similarity of infaunal communities between the Friendship and natural habitat was achieved, isotopic analyses revealed a simultaneous trajectory towards recovery of trophic structure. Enriched delta(13)C signatures of benthic microalgae and infauna, observed in the restored marsh shortly after establishment compared to natural Spartina habitat, recovered after 19 months. However, the depletion in delta(15)N signatures of macrofauna in the Friendship marsh indicated consumption of microalgae, particularly nitrogen-fixing cyanobacteria, while macroalgae and Spartina made a larger contribution to macrofaunal diets in the natural habitat. Future successional studies must continue to develop and employ novel combinations of techniques for evaluating structural and functional recovery of disturbed and created habitats. (C) 2004 Elsevier Ltd. All rights reserved.

Levin, LA, Talley TS.  2002.  Natural and manipulated sources of heterogeneity controlling early faunal development of a salt marsh. Ecological Applications. 12:1785-1802.   10.2307/3099938   AbstractWebsite

Ecosystem recovery following wetland restoration offers exceptional opportunities to study system structure, function, and successional processes in salt marshes. This study used observations of natural variation and large-scale manipulative experiments to test the influence of vascular vegetation and soil organic matter on the rate and trajectory of macrofaunal recovery in a southern California created salt marsh, the Crown Point Mitigation Site. During the first three years following marsh establishment, macrofaunal density and species richness recovered rapidly within the Spartina foliosa (cordgrass) zone; densities in the created marsh were 50% of those in the natural marsh after 16 mo and 97% after 28 mo. However, the early successional assemblage had a lower proportion of tubificid and enchytraeid oligochaetes, and a higher proportion of chironomids and other insect larvae than did the mature natural marsh. Most of the colonizers arrived by rafting on sea grass and algae rather than by larval dispersal. Initial planting of S. foliosa had no influence on macrofaunal recovery, perhaps because of variable transplant survival. However, subsequently, both positive and negative correlations were observed between densities of some macrofaunal taxa and shoot densities of S. foliosa or Salicornia spp. (pickleweed). Salinity and measures of soil organics (belowground biomass, combustible organic matter, and chlorophyll a) also were correlated with macrofaunal densities and taxon richness. Of foul added soil amendments (kelp, alfalfa, peat, and Milorganite), Milorganite (a sewage product) and kelp both promoted macrofaunal colonization during year 1, but effects were short lived. The most significant sources of heterogeneity in the recovering marsh were associated with site history and climate variation. Faunal recovery was most rapid in highly localized, organic-rich marsh sediments that were remnants of the historical wetland. Elevated sea level during the 1998 El Nino corresponded with similarity of macrofaunal communities in the created and natural marshes. The large spatial scale and multi-year duration of this study revealed that natural sources of spatial and temporal heterogeneity may exert stronger influence on faunal succession in California wetlands than manipulation of vegetation or soil properties.

Talley, TS, Levin LA.  1999.  Macrofaunal succession and community structure in Salicornia marshes of southern California. Estuarine Coastal and Shelf Science. 49:713-731.   10.1006/ecss.1999.0553   AbstractWebsite

Lack of basic understanding of ecosystem structure and function forms a major impediment to successful conservation of coastal ecosystems. This paper provides a description of the fauna and examines faunal succession in Salicornia-vegetated sediments of southern California. Environmental attributes (vegetation and sediment properties) and macrofaunal (animals greater than or equal to 0.3 mm) community structure were examined in sediments of five natural, southern California Salicornia spp. marshes (Tijuana Estuary, San Diego Bay, Mission Bay, Upper Newport Bay and Anaheim Bay) and in created Salicornia marshes 16 months to 10 years in age, located within four of the bays. Oligochaetes and insects were the dominant taxa in both natural (71 to 98% of total fauna) and created (91 to 97%) marshes. In San Diego, Newport and Anaheim Bays, macrofaunal densities were generally higher in the created marshes (88 000 to 290 000 ind m(-2)) than in their natural counterparts (26 000 to 50 000 ind m(-2)). In the youngest system, Mission Bay, the reverse was true (natural: 113 000 vs created: 28 000 ind m-2). Similar species numbers were recorded from the created and adjacent natural marshes. Insects, especially chironomids, dolichopodids, and heleids, as well as the naidid oligochaete, Paranais litoralis, characterize early successional stages. Enchytraeid and tubificid oligochaetes reflect later succession evident in natural and older created marshes. Sediment organic matter (both combustible and below-ground plant biomass) was the environmental variable most commonly associated with densities of various macrofaunal taxa. These relationships were generally negative in the natural marshes and positive in the created marshes. Within-bay comparisons of macrofauna from natural Salicornia- vs Spartina-vegetated habitat in San Diego and Mission Bays revealed lower macrofaunal density (San Diego Bay only), proportionally fewer oligochaetes and more insects, and no differences in species richness in the Salicornia habitat. The oldest created Salicornia marsh (San Diego Bay) exhibited an assemblage intermediate in composition between those of the natural Salicornia- and Spartina-vegetated marshes. These results suggest: (a) faunal recovery following Salicornia marsh creation can require 10 or more years, (b) high macrofaunal variability among bays requires marsh creation reference site selection from within the same bay, and (c) Spartina-based research should not be used for Salicornia marsh management decisions. (C) 1999 Academic Press.