Publications

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2012
Thornhill, DJ, Struck TH, Ebbe B, Lee RW, Mendoza GF, Levin LA, Halanych KM.  2012.  Adaptive radiation in extremophilic Dorvilleidae (Annelida): diversification of a single colonizer or multiple independent lineages? Ecology and Evolution. 2:1958-1970.   10.1002/ece3.314   AbstractWebsite

Metazoan inhabitants of extreme environments typically evolved from forms found in less extreme habitats. Understanding the prevalence with which animals move into and ultimately thrive in extreme environments is critical to elucidating how complex life adapts to extreme conditions. Methane seep sediments along the Oregon and California margins have low oxygen and very high hydrogen sulfide levels, rendering them inhospitable to many life forms. Nonetheless, several closely related lineages of dorvilleid annelids, including members of Ophryotrocha, Parougia, and Exallopus, thrive at these sites in association with bacterial mats and vesicomyid clam beds. These organisms are ideal for examining adaptive radiations in extreme environments. Did dorvilleid annelids invade these extreme environments once and then diversify? Alternatively, did multiple independent lineages adapt to seep conditions? To address these questions, we examined the evolutionary history of methane-seep dorvilleids using 16S and Cyt b genes in an ecological context. Our results indicate that dorvilleids invaded these extreme habitats at least four times, implying preadaptation to life at seeps. Additionally, we recovered considerably more dorvilleid diversity than is currently recognized. A total of 3 major clades (designated "Ophryotrocha,""Mixed Genera" and "Parougia") and 12 terminal lineages or species were encountered. Two of these lineages represented a known species, Parougia oregonensis, whereas the remaining 10 lineages were newly discovered species. Certain lineages exhibited affinity to geography, habitat, sediment depth, and/or diet, suggesting that dorvilleids at methane seeps radiated via specialization and resource partitioning.

2007
Neira, C, Levin LA, Grosholz ED, Mendoza G.  2007.  Influence of invasive Spartina growth stages on associated macrofaunal communities. Biological Invasions. 9:975-993.   10.1007/s10530-007-9097-x   AbstractWebsite

In coastal wetlands, invasive plants often act as ecosystem engineers altering flow, light and sediments which, in turn, can affect benthic animal communities. However, the degree of influence of the engineer will vary significantly as it grows, matures and senesces, and surprisingly little is known about how the influence of an ecosystem engineer varies with ontogeny. We address this issue on the tidal flats of San Francisco Bay where hybrid Spartina (foliosa x alterniflora) invaded 30 years ago. The invasion has altered the physico-chemical properties of the sediment habitat, which we predicted should cause changes in macrofaunal community structure and function. Through mensurative and manipulative approaches we investigated the influence of different growth stages of hybrid Spartina on macrobenthos and the underlying mechanisms. Cross-elevation sampling transects were established covering 5 zones (or stages) of the invasion, running from the tidal flat (pre-invasion) to an unvegetated dieback zone. Additionally, we experimentally removed aboveground plant structure in the mature (inner) marsh to mimic the 'unvegetated areas'. Our results revealed four distinct faunal assemblages, which reflected Spartina-induced changes in the corresponding habitat properties along an elevation gradient: a pre-invaded tidal flat, a leading edge of immature invasion, a center of mature invasion, and a senescing dieback area. These stages of hybrid Spartina invasion were accompanied by a substantial reduction in macrofaunal species richness and an increase in dominance, as well as a strong shift in feeding modes, from surface microalgal feeders to subsurface detritus/Spartina feeders (mainly tubificid oligochaetes and capitellid polychaetes). Knowledge of the varying influence of plant invaders on the sediment ecosystem during different phases of invasion is critical for management of coastal wetlands.

2004
Robinson, CA, Bernhard JM, Levin LA, Mendoza GF, Blanks JK.  2004.  Surficial hydrocarbon seep infauna from the Blake Ridge (Atlantic Ocean, 2150 m) and the Gulf of Mexico (690-2240 m). Marine Ecology-Pubblicazioni Della Stazione Zoologica Di Napoli I. 25:313-336.   10.1111/j.1439-0485.2004.00034.x   AbstractWebsite

Infauna, including foraminifera and metazoans, were enumerated and identified from five types of seep habitats and two adjacent non-seep habitats. Collections were made with the deep submergence research vessel 'Alvin' from three areas of active seepage in the Gulf of Mexico (Alaminos Canyon [2220 m], Atwater Canyon [1930 m], and Green Canyon lease block 272 [700 m]) and on the Blake Ridge Diapir [2250 m], which is located off the southeastern coast of the United States. The seep habitats sampled included four types of microbial mats (Beggiatoa, Thioploca, thin and thick Arcobacter) and the periphery of a large mussel bed. Sediments under large rhizopod protists, xenophyophores, were sampled adjacent to the mussel bed periphery. A non-seep site, which was >1 km away from active seeps, was also sampled for comparison. Densities of most taxa were higher in the Gulf of Mexico seeps than in Blake Ridge samples, largely because densities in the thick microbial mats of Blake Ridge were significantly lower. Diversity was higher in the Thioploca mats compared to other microbial-mat types. Within an ocean basin (i.e., Atlantic, Gulf of Mexico) we did not observe significant differences in meiofaunal or macrofaunal composition in Beggiatoa versus Thioploca mats or thin versus thick Arcobacter mats. Foraminifera represented up to 16% of the seep community, a proportion that is comparable to their contribution at adjacent non-seep communities. In general, the observed densities and taxonomic composition of seep sites at the genus level was consistent with previous observations from seeps (e.g., the foraminifers Bolivina and Fursenkoina, the dorvilleid polychaete Ophryotrocha).

2000
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.