Blue mats: faunal composition and food web structure in colonial ciliate (Folliculinopsis sp.) mats at Northeast Pacific hydrothermal vents

Abstract

The present study provides a first description of the faunal composition and food web structure associated with blue mat ciliates (Folliculinopsis sp.) at hydrothermal vents on the Juan de Fuca and Explorer Ridges in the NE Pacific. Invertebrates associated with blue mats were identified, quantified and analyzed for stable carbon and nitrogen isotopes. In addition, fatty acid analyses of blue mats were performed. We found a recurrent assemblage of invertebrates associated with the blue mats, and, in all samples, meiofauna were numerically dominant. The harpacticoid copepod Amphiascus sp. was far more abundant than any other species within the folliculinid mats. While some of the invertebrates (including Amphiascus sp.) within this assemblage seem exclusively linked to blue mats, others are known from other nearby hydrothermal vent habitats. Folliculinopsis sp. ciliates were far more depleted in δ 13 C than invertebrates within the blue mat assemblage, indicating that the latter do not feed exclusively on the former. At least 2 trophic levels exist within this assemblage, with juvenile macrofauna, ostracod and nematode species occupying higher trophic levels. The lipid profiles indicate that 16:1ω7 and 18:1ω7 (typical of sulfur oxidizers) make up over half the blue mat fatty acids. Similar to tubeworm bushes at hydrothermal vents and mussel beds at cold seeps, blue mats may create a habitat within which meiofaunal and juvenile macrobenthic species can find shelter and food, thus playing an indirect but important role in the ecology of these organisms. KEY WORDS: Food web · Folliculinid · Hydrothermal vents · Stable isotopes · Fatty acid · Meiofauna · Macrofauna Resale or republication not permitted without written consent of the publisherMar Ecol Prog Ser 412: [93][94][95][96][97][98][99][100][101] 2010 length (Folliculinopsis sp.). These ciliate mats can cover extensive areas on basalt surfaces or patches on sulfide chimneys in some eastern Pacific Ocean hydrothermal vent fields and elsewhere (Tunnicliffe et al. 1985, Kouris et al. 2007). For example, in areas of widespread venting of 10 to 20 m 2 or more on the Juan de Fuca Ridge, blue mats occupied as much as 70% of the basaltic substratum (Kouris et al. 2007). At some vent sites, these folliculinid ciliates have also been reported attached to mobile invertebrates (Kouris et al. 2007), as well as on the tubes of the vestimentiferan Ridgeia piscesae (Bergquist et al. 2007, Gollner et al. 2007).To our knowledge, no other colonial ciliate has ever been reported to occupy such extensive areas in the marine environment. The ecological success of the blue mats, as evidenced by this abundance and widespread distribution around diffuse-flow vents, may be attributed to a recently proposed symbiosis involving prokaryotic symbionts hosted by these folliculinids. Abundant intra-cellular prokaryotes are apparent in transmission electron micrographs of the folliculinid cytoplasm and loricae (Kouris et al. 2007). These symbionts have also been the subject of 16S...

Colonial Tube-Dwelling Ciliates Influence Methane Cycling and Microbial Diversity within Methane Seep Ecosystems

“…Preliminary microscopy surveys revealed a variety of organisms attached to (e.g., filamentous bacteria and other sessile ciliates) and nestled between (e.g., nematodes) folliculinid lorica. These observations are consistent with the observed utilization of "blue mat" habitat by micro-and meiofaunal organisms at vents (Kouris et al, 2010). TEM observations also revealed a diversity of microorganisms attached to the folliculinid lorica.…”

“…This enrichment pattern was consistent in two independent stable isotope tracer experiments with folliculinids from seep regions that were 1480 kilometers apart. Folliculinids from hydrothermal vents also have a depleted carbon isotope signature (−32.8 ± 1.7‰ at Juan de Fuca, Kouris et al, 2010; −34‰ at Gorda Ridge, Goffredi and Orphan, unpublished) indicating the importance of folliculinid-associated chemoautotrophs may be more widespread across many types of chemosynthetic environments. While further work needs to be done to better understand the exact nature of this association, based on the natural carbon isotope signature of the folliculinids and 13 C-enrichment patterns in the isotope tracer experiments, we hypothesize that this specific association between folliculinid ciliates and "Deep sea-2" aerobic methanotrophs enables the ciliate to participate in ecosystem-level methane cycling.…”

“…These ciliates are found in non-chemosynthetic coastal marine habitats (e.g., Fauré-Fremiet, 1936;Das, 1949;Mathews, 1964Mathews, , 1968Ji et al, 2004) and are known to colonize a variety of substrates including oyster and mussel shells (Mathews, 1968;Toupoint et al, 2012), serpulid polychaete worm tubes (Mathews, 1964), crayfish (Jaszczolt and Szaniawsk, 2007), wood (Mathews, 1964), coral skeletons (Cróquer et al, 2006), and even artificial substrates (Ji et al, 2004). Their presence in chemosynthetic ecosystems was first discovered at hydrothermal vents in the 1980's (Tunnicliffe et al, 1985;Van Dover et al, 1988), but their abundance and ecological importance was only more recently recognized (Kouris et al, 2007(Kouris et al, , 2010. Folliculinids form dense "blue mat" colonies within hydrothermal vent fields, sometimes occupying 70% of mineralized substrate, influencing community composition and food web structure within these ecosystems (Kouris et al, 2010).…”

“…Their presence in chemosynthetic ecosystems was first discovered at hydrothermal vents in the 1980's (Tunnicliffe et al, 1985;Van Dover et al, 1988), but their abundance and ecological importance was only more recently recognized (Kouris et al, 2007(Kouris et al, , 2010. Folliculinids form dense "blue mat" colonies within hydrothermal vent fields, sometimes occupying 70% of mineralized substrate, influencing community composition and food web structure within these ecosystems (Kouris et al, 2010). Folliculinids have also been collected and documented from a methane seep in the Gulf of California (Lobban et al, 2007), but their ecological role in seep ecosystems has not been explored.…”

Hydrothermal vent protistan distribution along the Mariana arc suggests vent endemics may be rare and novel

“…To date, only one vent-endemic protist has been described, a sessile, colonial symbiont-bearing folliculinid ciliate that forms dense bright blue carpets at vent sites on the Juan de Fuca Ridge (Tunnicliffe et al, 1985;Kouris et al, 2007;Kouris et al, 2010). Additional hydrothermal vent endemism has been proposed based on previous culture-independent studies of protists, but most of these studies made no comparisons with protist communities in nearby non-vent-influenced habitats.…”