Joan M. Bernhard

Foraminifera of oxygen-depleted environments

In summary, certain benthic Foraminifera from various water depths inhabit oxygen-poor and even anoxic environments. It is established that at least some foraminiferal species survive anoxia and even sulfidic conditions for periods up to a few weeks, but the tolerance of most species to oxygen depletion is unknown. Furthermore, the physiological mechanisms enabling foraminiferal species to survive exposure to anoxia and/or sulfidic conditions are not yet identified. The available data suggest, however, that all Foraminifera are aerobic for at least part of their life, and, in all likelihood, some species are facultative anaerobes. Obligate anaerobes have not been identified among foraminiferal species. The information necessary to understand the diverse aspects of foraminiferal adaptation to oxygen-depleted environments must come from experimental studies. Only with such biological information, it will be possible to construct more accurate databases for use in other disciplines such as paleoecology and paleoceanography.

Foraminifera in the Arabian Sea oxygen minimum zone and other oxygen-deficient settings: taxonomic composition, diversity, and relation to metazoan faunas

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 412 m within the oxygen minimum zone (OMZ) (O2=0.13 ml l?1), the other located at 3350 m, well below the main OMZ (O2~3.00 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-m fraction) than at the 3350-m site (625 indiv.10 cm?2). Species richness (E(S100)), 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-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 m fraction) in the Santa Barbara Basin (590 and 610 m depth; O2=0.05 and 0.15 ml l?1 respectively), and macrofaunal foraminifera (>300 m) on the Peru margin (300–1250 m depth; O2=0.02–1.60 ml l?1), matched those observed on the Oman margin. In particular, soft-shelled monothalamous taxa were rare and large agglutinated taxa were absent in the most oxygen-depleted ( 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 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 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 m. 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.

Benthic foraminiferal population fluctuations related to anoxia: Santa Barbara Basin

The pore-water geochemistry and benthic foraminiferal assemblages of sediments from two slope sites and within the central portion of the Santa Barbara Basin were characterized between February 1988 and July 1989. The highest foraminiferal numerical densities (1197 cm−3 as determined by an ATP assay) occurred at a slope site in June 1988 (550 m) in partially laminated sediments. In continuously laminated sediments from the central basin, foraminifera were found living (as determined by ATP assay) in October 1988 to depths of 4 cm, and specimens prepared for transmission electron microscopy were found with intact organelles to 3 cm, indicating their inhabitation of anoxic pore waters. Ultrastructural data from Nonionella stella is consistent with the hypothesis that this species can survive by anaerobic respiration. However, the benthic foraminifera appear unable to survive prolonged anoxia. The benthic foraminiferal population was completely dead in July 1989 when bottom water O2 was undetectable.

Blake Ridge methane seeps: characterization of a soft-sediment, chemosynthetically based ecosystem

Observations from the first submersible reconnaissance of the Blake Ridge Diapir provide the geological and ecological contexts for chemosynthetic communities established in close association with methane seeps. The seeps mark the loci of focused venting of methane from the gas hydrate reservoir, and, in one location (Hole 996D of the Ocean Drilling Program), methane emitted at the seafloor was observed forming gas hydrate on the underside of a carbonate overhang. Megafaunal elements of a chemosynthetically based community mapped onto dive tracks provide a preliminary overview of faunal distributions and habitat heterogeneity. Dense mussel beds were prominent and covered 20 � 20 m areas. The nearly non-overlapping distributions of mussels and clams indicate that there may be local (meter-scale) variations in fluid flux and chemistry within the seep site. Preliminary evidence suggests that the mussels are host to two symbiont types (sulfide-oxidizing thiotrophs and methanotrophs), while the clams derive their nutrition only from thiotrophic bacteria. Invertebrate biomass is dominated by mussels (Bathymodiolus heckerae) that reach lengths of up to 364 mm and, to a lesser extent, by small (22 mm length) vesicomyid clams (Vesicomya cf. venusta). Taking into account biomass distributions among taxa, symbiont characteristics of the bivalves, and stable-isotope analyses, the relative importance of methanotrophic vs thiotrophic bacteria in the overall nutrition of the invertebrate

Benthic foraminiferal distribution and biomass related to pore-water oxygen content: central California continental slope and rise

Benthic foraminiferal distributions and biomass were investigated with respect to bottom-water and pore-water dissolved oxygen concentrations and sedimentary organic carbon content at nine stations (624–3728 m) along two transects perpendicular to the central California coast. These stations were selected to intersect the oxygen minimum zone (OMZ) as it impinges on the seafloor. Foraminiferal numerical densities were determined at selected depths within the uppermost 9 cm of box cores, using either an adenosine triphosphate (ATP) assay or a Rose Bengal vital staining technique. Foraminiferal abundances from surficial sediments, as determined by the staining technique, varied considerably and were negatively correlated to bottom-water oxygen concentration. Maximal numerical densities occurred at a depth of 998 m, which is within the OMZ; values ranged from 0 to 11.8 individuals cm−3 (determined by the ATP method) in surficial sediments. Six of nine cores exhibited subsurface maxima in foraminiferal abundance, and seven of the cores had subsurface foraminiferal biomass maxima. Results indicate that certain species are infaunal while others only live in the surface sediment interval, an important observation for paleoceanographic studies utilizing stable isotopic analyses of deep-sea benthic foraminifera.

Benthic foraminifera of dysoxic sediments: chloroplast sequestration and functional morphology

Abstract Our recent surveys of dysoxic and anoxic sites reveal that many of the common foraminiferal inhabitants sequester chloroplasts. Such species include: Nonionella stella , which dominates the laminated sediments of the silled Santa Barbara Basin and comprises up to 82% of the living assemblage when [O 2 ] is below 2 μM (∼0.04 ml/l); the closely related species Nonionellina labradorica , which occurs in oxygen-depleted, silled fjords of Sweden; Stainforthia fusiformis , which dominates dysoxic sediments of Norwegian fjords; and Bulimina elegantissima , which is abundant in a shallow-water oil seep site supporting the filamentous, sulfide-oxidizing bacteria Beggiatoa . The literature contains examples of at least eight Elphidium species and one species from each of three other foraminiferal genera (i.e., Haynesina , Nonion , Reophax ) that are known to sequester chloroplasts. These foraminifera are typically infaunal and/or may live under dysoxic conditions. Photosynthetic activity of the sequestered chloroplasts might provide oxygen to the host foraminifera, thereby enabling them to inhabit anoxic pore waters. However, given that most of the surveyed sites occur in the aphotic zone where light levels are too low to fuel photosynthesis, it is more likely that the host employs an as yet unidentified biochemical pathway associated with the sequestered chloroplasts. Additionally, these foraminifera have external test ornamentations that may facilitate separation of the chloroplasts from their algal prey. We discuss potential uses for these morphological features in interpreting the fossil record.

Survival, ATP pool, and ultrastructural characterization of benthic foraminifera from Drammensfjord (Norway): response to anoxia

While much evidence indicates that certain benthic foraminifera are facultative anaerobes, little is known regarding the physiologic response of foraminifera to anoxia. In order to assess their response, specimens of four foraminiferal species, collected from a typically dysoxic area of Drammensfjord, Norway (45 m water depth), were incubated in seawater purged with nitrogen. Over a time course of > 3 weeks, the specimens were extracted for adenosine triphosphate (ATP) in a nitrogen-flushed glove bag to assess their survival and ATP reserve under such conditions. For comparative purposes, similar extractions were done on conspecifics one week after their collection from the seafloor, as well as on other conspecifics, obtained from the same site, incubated in aerated conditions. The survival rates of nitrogen-treatedAdercotryma glomeratum, Psammosphaera bowmanni, and Stainforthia fusiformis were not significantly lower than those of the control specimens. However, the ATP concentrations of nitrogen-incubated A. glomeratum and S. fusiformis were significantly lower than those of their aerated conspecifics, while there was no significant difference between the [ATP] of P. bowmanni from the two treatments. Both the survival rate and the ATP concentrations of nitrogen-incubated Bulimina marginata were significantly lower than those of control specimens. The ultrastructure of B. marginata and S. fusiformis incubated in N2 for 18 days were compared with those of specimens fixed within 15 minutes of collection. For both species, the specimens that survived the experimental treatment had ultrastructures indistinguishable from those fixed just after field collection. However, the ultrastructure of B. marginata differed from that of S. fusiformis in that it lacked the numerous peroxisome-endoplasmic reticulum (ER) complexes and what appeared to be algal chloroplasts observed in S. fusiformis. Copious arrays of paracrystals were observed in both species from the experimental treatment as well as the shipboard-fixed specimens, suggesting that neither population had extensive pseudopodial networks. When considered in combination, our results indicate that the four species respond to and survive anoxia differently, with responses including dormancy and, as yet unidentified, anaerobic metabolic pathways.

Experimental and field evidence of Antarctic foraminiferal tolerance to anoxia and hydrogen sulfide.

Abstract The common occurrence of foraminifera in strata deposited under anoxic environmental conditions throughout the geologic record raises the question of whether foraminifera actually survive anoxic or reducing conditions. To test this, benthic foraminifera from McMurdo Sound, Antarctica were exposed to anoxic or reducing conditions for 30 days. These Antarctic forms are known to be exposed to anoxic events in their natural environment. An adenosine triphosphate (ATP) assay was used to determine foraminiferal survival, and their ultrastructure was examined using transmission electron microscopy (TEM) to evaluate any possible effect that might have resulted from exposure to anoxic or reducing conditions. The experimental treatments did not have any statistically significant effects upon the foraminifers with regards to survival or average ATP content per individual including the four most common living species. Some ultrastructural evidence for encystment (fibrillar membrane-bound bodies in the cytoplasm of many specimens) was observed. Field data include the observation thatGlobocassidulina cf.G. biora resides in sediments to depths of 7 cm, as evidenced by ultrastructural investigations. A specimen ofGlobocassidulina cf.G. biora collected from sediments containing anoxic pore waters showed numerous bacteria within the confines of the organic lining. The occurrence of cytoplasmic inclusions similar in appearance to car☐ysomes within these bacteria suggest possible affinities to the chemolithotrophicThiobacillus. Bacteria of this type were not observed in specimens collected from oxygenated pore waters. These field and laboratory findings suggest that certain foraminifera may be facultative anaerobes able to withstand reducing conditions.

Benthic foraminiferal assemblages in Explorers Cove, Antarctica : A shallow-water site with deep-sea characteristics

Abstract During November and December 1993, we sampled foraminiferal populations living at a 25–28m deep site in Explorers Cove, McMurdo Sound, Antarctica, by means of an airlift suction apparatus and sediment coring. Mean standing stocks (stained specimens per 10cm2) were 8.55±2.60 (all specimens >1mm, 0–10cm layer), 62.1±27.5 (all specimens >500μm, 0–10cm layer), 483 (all specimens >63μm, 0–1cm layer) and 632 (all specimens >28μm, 0–1cm layer). The fauna comprises diverse taxa including both hard-shelled and soft-shelled forms. The coarser fractions (>1mm) are dominated by large agglutinated foraminifera, mainly “spheres” and domes (psammosphaerids, saccamminids, notodendrodiids), but also contain some large calcareous taxa (Cibicides, Pyrgo). The finer fractions (>500, >63, >28μm) yield numerous soft-bodied monothalamous foraminifera in addition to the more commonly studied calcareous and multilocular agglutinated forms. Many species adopt epifaunal or shallow infaunal (0–1cm layer) microhabitats but a few smaller ones are more deeply infaunal (>1cm). A variety of trophic strategies can be inferred from the limited available evidence. Some abundant large species (Crithionina spp., Gromia oviformis) may be shallow infaunal or epifaunal deposit feeders, but the most striking feature of the fauna is the conspicuous occurrence of large epifaunal species which appear to be suspension feeders (e.g. Astrammina, Astrorhiza, Notodendrodes, Cibicides). Some of these foraminifera can probably switch trophic mode, for example, from suspension feeding to osmotrophy in response to a fluctuating food supply. The Explorers Cove fauna includes a mix of wide-ranging and endemic species. The main features of the fauna are consistent with environmental similarities (uniformly low temperatures, physical tranquillity, episodic food inputs) between Explorers Cove and deeper water settings. In the Northern Hemisphaere, comparable faunas (i.e. those in which large agglutinated taxa are a conspicuous element) are found in deep sublittoral and fjordic areas (100–1000m), as well as at some bathyal and abyssal localities (down to several thousands of metres) which receive a substantial organic matter input from processes such as upwelling. Foraminifera probably play a major ecological role in these systems, particularly in trophic interactions and organic carbon cycling. Their success may depend on two main attributes. First, they possess extremely efficient food gathering organelles (reticulopodia) and second, they become quiescent when starved but can rapidly increase their metabolic rate when presented with food. Our SCUBA-accessible study site in Explorers Cove provides a unique opportunity to clarify the role that these important protists play in shallow Antarctic waters as well as in more remote deep-water environments.

USE OF THE FLUORESCENT CALCITE MARKER CALCEIN TO LABEL FORAMINIFERAL TESTS

We describe a novel application of the fluorescent compound calcein (Bis[N,N-bis(carboxymethyl)aminomethyl]-fluorescein), which was used to fluorescently label foraminiferal calcite. Foraminifers that were incubated in a 10 mg L−1 solution of calcein and seawater precipitated normal-looking chambers during and after calcein incubation, which lasted up to three weeks. The survival rate of specimens incubated in calcein was similar to that of control specimens; some specimens reproduced during or after calcein exposure. Thus, this calcein-tagging method is non-lethal. Chambers precipitated during calcein incubation fluoresced a yellow-green when viewed with epifluorescence or laser scanning confocal microscopy (470 nm excitation, 500 nm emission). When viewed alternatively with reflected light, chambers formed after calcein incubation were easily distinguished from calcein-marked chambers, because calcite precipitated after calcein exposure does not fluoresce. Fluorescence is retained through fixation and air drying, thus the signal can be viewed in archived specimens. The method was executed on specimens from 15 species collected from three habitats with diferent environmental conditions. Results indicate that calcein is incorporated by all 15 species. The method has a number of potential applications, including experiments aimed at identifying benthic foraminifers that are faithful recorders of paleoceanographic proxies, as well as field studies to assess locations and chronology of foraminiferal calcification.