Joan Bernhard

Woods Hole Oceanographic Institution | WHOI · Department of Geology and Geophysics

Prior observations suggest that foraminiferan protists use their reticulopodia (anastomosing pseudopodia) to alter sediment fabric by disrupting laminations of subtidal marine stromatolites, erasing the layered structures in an experimental setting. Because microbialites and foraminifera are found in non-marine settings, we hypothesized that forami...

Fjord systems are typically affected by low‐oxygen conditions, which are increasing in extent and severity, forced by ongoing global changes. Fjord sedimentary records can provide high temporal resolution archives to aid our understanding of the underlying mechanisms and impacts of current deoxygenation. However, such archives can only be interpret...

The health of coastal marine environments is severely declining with global changes. Proxies, such as based on microeukaryote communities, can record biodiversity and ecosystem responses. However, conventional studies rely on microscopic observations of limited taxonomic range and size fraction, missing putatively ecologically informative community...

Hydrothermal vents are critical to marine geochemical cycling and ecosystem functioning. Although hydrothermal vent-associated megafauna and chemoautotrophic prokaryotes have received extensive dedicated study, smaller hydrothermal vent-associated eukaryotes such as meiofauna and nanobiota have received much less attention. These communities compri...

Certain benthic foraminifera thrive in marine sediments with low or undetectable oxygen. Potential survival avenues used by these supposedly aerobic protists include fermentation and anaerobic respiration, although details on their adaptive mechanisms remain elusive. To better understand the metabolic versatility of foraminifera, we studied two ben...

Several foraminifera are deposit feeders that consume organic detritus (dead particulate organic material with entrained bacteria). However, the role of such foraminifera in the benthic food web remains understudied. Foraminifera feeding on methanotrophic bacteria, which are 13C-depleted, may cause negative cytoplasmic and/or calcitic δ13C values....

Certain benthic foraminifera are known to thrive in marine sediments with low oxygen or even without detectable oxygen. Potential survival avenues used by these supposedly aerobic protists include fermentation and anaerobic respiration, although details on their adaptive mechanisms remain somewhat elusive. To better understand the metabolic versati...

Nitrogen and sulfur are key elements in the biogeochemical cycles of marine ecosystems to which benthic foraminifera contribute significantly. Yet, cell-specific assimilation of ammonium, nitrate and sulfate by these protists is poorly characterized and understood across their wide range of species-specific trophic strategies. For example, detailed...

An appropriate proxy could help to better understand dissolved oxygen variations in the past, helping to predict potential outcomes of future environmental changes. In the Changjiang Estuary (China), the foraminifer Cribrononion subincertum (C. subincertum) shows a distinct population maximum in the topmost sediment, an indication of an epifaunal s...

Several foraminifera are deposit feeders that consume organic detritus (dead particulate organic material along with entrained bacteria). However, the role of such foraminifera in the benthic food-web remains understudied. As foraminifera may associate with methanotrophic bacteria, which are 13C-depleted, feeding on them has been suggested to cause...

Hypoxia is of increasing concern in marine areas, calling for a better understanding of mechanisms leading to decreasing dissolved oxygen concentrations ([O2]). Much can be learned about the processes and implications of deoxygenation for marine ecosystems using proxy records from low‐oxygen sites, provided proxies, such as the manganese (Mn) to ca...

Oceanic deoxygenation is increasingly affecting marine ecosystems; many taxa will be severely challenged, yet certain nominally aerobic foraminifera (rhizarian protists) thrive in oxygen-depleted to anoxic, sometimes sulfidic, sediments uninhabitable to most eukaryotes. Gene expression analyses of foraminifera common to severely hypoxic or anoxic s...

Ocean chemistry is changing as a result of human activities. Atmospheric carbon dioxide (CO2) concentrations are increasing, causing an increase in oceanic pCO2 that drives a decrease in oceanic pH, a process called ocean acidification (OA). Higher CO2 concentrations are also linked to rising global temperatures that can result in more stratified s...

The adverse effects of engineered nanomaterials (ENM) in marine environments have recently attracted great attention although their effects on marine benthic organisms such as foraminifera are still largely overlooked. Here we document the effects of three negatively charged ENM, different in size and composition, titanium dioxide (TiO2), polystyre...

Microscopy techniques have been widely applied to observe cellular ultrastructure. Most of these techniques, such as transmission electron microscopy, produce high‐resolution images, but they may require extensive preparation, hampering their application for in vivo examination. Other approaches, such as fluorescent and fluorogenic probes, can be a...

Bryozoa is a phylum of about 6000 extant species that are almost exclusively colonial. Few species of the uncalcified Gymnolaemata, the ctenostomes, however, show solitary forms that essentially consist of single zooids. Recently, several specimens of a solitary ctenostome bryozoan were encountered for the first time in the deep Mediterranean Sea,...

The assimilation of inorganic compounds in foraminiferal metabolism compared to predation or organic matter assimilation is unknown. Here we investigate possible inorganic‐compound assimilation in Nonionellina labradorica, a common kleptoplastidic benthic foraminifer from Arctic and North Atlantic sublittoral regions. The objectives were to identif...

Foraminifera in sediments exposed to gas-hydrate dissociation are not expected to have cellular adaptations that facilitate inhabitation of chemosynthesis-based ecosystems because, to date, there are no known endemic seep foraminifera. To establish if foraminifera inhabit sediments impacted by gas-hydrate dissociation, we examined the cellular ultr...

Haynesina germanica, an ubiquitous benthic foraminifer in intertidal mudflats, has the remarkable ability to isolate, sequester, and use chloroplasts from microalgae. The photosynthetic functionality of these kleptoplasts has been demonstrated by measuring photosystem II quantum efficiency and O 2 production rates, but the precise role of the klept...

Microscopy techniques have been widely applied to observe foraminiferal ultrastructures. Most of these techniques such as transmission electronic microscopy allow obtaining high-resolution images, though they require an extensive preparation of samples potentially hampering their application and limit “in vivo” examination. Fluorescent and fluoroge...

Research of the past few decades has revealed a great variability of metabolisms (e.g. adaptation to different microhabitats, feeding strategies, symbiosis, survival to stressful conditions) among benthic foraminiferal species. This metabolic variety is reflected in the cell by a great diversity of organelles, cellular organization and organelle as...

Symbioses between anaerobic or microaerophilic protists and prokaryotes are common in anoxic and oxygen-depleted habitats ranging from marine sediments to gastrointestinal tracts. Nevertheless, little is known about the mechanisms of metabolic interaction between partners. In these putatively syntrophic associations, consumption of fermentative end...

Because prokaryotes (Eubacteria, Archaea) are ubiquitous in the marine realm, it may not be surprising that they are important to the diet of at least some foraminifera. Over recent decades, Transmission Electron Microscopy (TEM) has revealed that, at the ultrastructural level, additional intimate relationships exist between prokaryotes and foramin...

Transmission electron microscope (TEM) observation has revealed much about the basic cell biology of foraminifera. Yet, there remains much we do not know about foraminiferal cytology and physiology, especially for smaller benthic foraminifera, which inhabit a wide range of habitats. Recently, some TEM-coupled approaches have been developed to study...

We report systematic transmission electron microscope (TEM) observations of the cellular ultrastructure of selected, small rotalid benthic foraminifera. Nine species from different environments (intertidal mudflat, fjord, and basin) were investigated: Ammonia sp., Elphidium oceanense, Haynesina germanica, Bulimina marginata, Globobulimina sp., Noni...

Assimilation, sequestration and maintenance of foreign chloroplasts inside an organism is termed “chloroplast sequestration” or “kleptoplasty”. This phenomenon is known in certain benthic foraminifera, in which such kleptoplasts can be found both intact and functional, but with different retention times depending on foraminiferal species. In the pr...

Heavy metals are known to cause deleterious effects on biota because of their toxicity, persistence and bioaccumulation. Here, we briefly document the ultrastructural changes observed in the miliolid foraminifer Pseudotriloculina rotunda (d'Orbigny in Schlumberger, 1893) and in the perforate calcareous species Ammonia parkinsoniana (d'Orbigny, 1839...

Agglutinated foraminifera create a shell by assembling particles from the sediment and comprise a significant part of the foraminiferal fauna. Despite their high abundance and diversity, their response to environmental perturbations and climate change is relatively poorly studied. Here we present results from a culture experiment with four differen...

Hiroshi Kitazato was awarded the 2016 Joseph A. Cushman Award for Excellence in Foraminiferal Research at the Annual Cushman Reception on 27 September 2016, in Denver, Colorado. The award was conferred to him due to his pioneering and highly original biological and ecological studies of benthic foraminifera, especially his culturing studies and inn...

We documented the annual cycle of the carbon isotopic composition of dissolved inorganic carbon (δ¹³CDIC) in the water columns of the Skagerrak and Baltic Sea to obtain an increased understanding of the processes involved controlling the carbon isotopic distribution in shelf seas. The lowest δ¹³CDIC values (− 4.9‰) were found in the low-oxygen, bra...

Homotrema rubrum is a (sub)rropical, sessile foraminiferan that reinforces the coral-reef framework by calcifying in cracks, crevices and on the cryptic undersides of coral colonies and other reef substrata. It secretes a pigmented carbonate skeleton that can be well preserved in the fossil record and, thus, has the potential to influence paleoecol...

Heavy metals such as mercury (Hg) pose a significant health hazard through bioaccumulation and biomagnification. By penetrating cell membranes, heavy metal ions may lead to pathological conditions. Here we examined the responses of Ammonia parkinsoniana, a benthic foraminiferan, to different concentrations of Hg in the artificial sea water. Confoca...

Mann-Whitney U Test for differences lipid dimension. Significant differences are marked in bold. (XLS)

Typical paired NR confocal images. (A) Bright Field image. (B) Neutral lipids (triglycerides, esters of cholesterol and free fatty acids) in yellow. (C) Polar lipids (phospholipids, sphingolipids and non-esterified cholesterol) in red. (D) Merged Bright Field, yellow and red channels. (TIF)

Lipid dimension counting. (XLSX)

Deep-sea hypersaline anoxic basins (DHABs) in the Eastern Mediterranean Sea are considered some of the most polyextreme habitats on Earth. In comparison to microbial activities occurring within the haloclines and brines of these unusual water column habitats near the Mediterranean seafloor, relatively little is known about microbial metabolic activ...

A new benthic foraminifer, Helenina davescottensis nov. sp., is described from an oligohaline carbonate marsh (palustrine environment) located in a sinkhole on Grand Bahama Island, The Bahamas. The uppermost stratigraphy in the sinkhole is characterized by up to 260 cm of peat, which is overlain by 5-10 cm of carbonate sediment that contain H. dave...

Some benthic foraminiferal species are reportedly capable of nitrate storage and denitrification, however, little is known about nitrate incorporation and subsequent utilization of nitrate within their cell. In this study, we investigated where and how much 15N or 34S were assimilated into foraminiferal cells or possible endobionts after incubation...

The oceans are absorbing increasing amounts of carbon dioxide (CO2) as a result of rising anthropogenic atmospheric CO2 emissions. This increase in oceanic CO2 leads to the lowering of seawater pH, which is known as ocean acidification (OA). Simultaneously, rising global temperatures, also linked to higher atmospheric CO2 concentrations, result in...

Greenhouse gas venting into the oceans and atmosphere is important to understand and predict in the context of climate change. A puzzle exists regarding the carbonate of foraminiferal tests (shells) from methane seeps: Are the tests obtained from seep sediments actually grown during methane emissions? If so, this is a physiological conundrum becaus...

Since the beginning of industrialization, carbon dioxide (CO 2) concentrations have increased in the atmosphere, causing an increase in oceanic pCO 2 that drives a decrease in oceanic pH, a process called ocean acidification (OA). Higher CO 2 concentrations have been linked to rising global temperatures, which can result in more stratified surface...

The deep-sea hypersaline anoxic basins (DHABs) of the Mediterranean (water depth ~3500 m) are some of the most extreme oceanic habitats known. Brines of DHABs are nearly saturated with salt, leading many to suspect they are uninhabitable for eukaryotes. While diverse bacterial and protistan communities are reported from some DHAB haloclines and bri...

The sediment microbiota of the Mediterranean deep-sea anoxic hypersaline basins (DHABs) are understudied relative to communities in the brines and halocline waters. In this study, the active fraction of the prokaryotic community in the halocline sediments of L' Atalante, Urania, and Discovery DHABs was investigated based on extracted total RNA and...

Insights into oceanographic environmental conditions such as paleoproductivity, sea-surface temperatures, deep-water temperatures, salinity, ice volumes, circulation patterns, and nutrient cycling have all been obtained from geochemical analyses of biomineralized carbonate of marine organisms. However, we cannot fully understand geochemical proxy i...

Oceanic and coastal waters are acidifying due to processes dominated in the open ocean by increasing atmospheric CO2 and dominated in estuaries and some coastal waters by nutrient-fueled respiration. The patterns and severity of acidification, as well as its effects, are modified by the host of stressors related to human activities that also influe...

Agglutinated foraminifera comprise a significant part of the foraminiferal fauna. These foraminifera create a shell (i.e., test) by assembling sediment particles together with an organic or calcareous cement. Despite their abundance and diversity, their response to environmental change is relatively poorly studied. Recent studies have shown the res...

The responses of Ammonia parkinsoniana (Foraminifera) exposed to different concentrations of lead (Pb) were evaluated at the cytological level. Foraminifera-bearing sediments were placed in mesocosms that were housed in aquaria each with seawater of a different lead concentration. On the basis of transmission electron microscopy and environmental s...

To allow observation of cellular ultrastructure in foraminifers (or other meiofauna) preserved in their life position within sediments, modifications of the Fluorescently Labeled Embedded Core (FLEC) method are described. Such an approach will allow determinations of both fine-scale (sub-millimeter scale) distributional data and cell biological dat...

Some of the most extreme marine habitats known are the Mediterranean deep hypersaline anoxic basins (DHABs; water depth ∼3500 m). Brines of DHABs are nearly saturated with salt, leading many to suspect they are uninhabitable for eukaryotes. While diverse bacterial and protistan communities are reported from some DHAB water-column haloclines and bri...

Specimens of Bolivina argentea and Bulimina marginata, two widely distributed temperate benthic foraminiferal species, were cultured at constant temperature and controlled pCO2 (ambient, 1000 ppmv, and 2000 ppmv) for six weeks to assess the effect of elevated atmospheric CO2 concentrations on survival and fitness using Adenosine Triphosphate (ATP)...

Specimens of Bolivina argentea and Bulimina marginata, two widely distributed temperate benthic foraminiferal species, were cultured at constant temperature and controlled pCO2 (ambient, 1000 ppmv, and 2000 ppmv) for six weeks to assess the effect of elevated atmospheric CO2 concentrations on survival and fitness using Adenosine Triphosphate (ATP)...

Geochemical proxies recorded in biomineralized carbonate have provided a sound foundation for paleoceanography and paleoclimate studies, yet significant uncertainties exist about where and when certain key taxa calcify. Insights into environmental conditions such as sea surface temperatures, deep-water temperatures, salinity, ice volumes, oceanic c...

We report a study of the sterols produced by the thecate allogromid foraminiferan, Allogromia laticollaris, grown in culture. Gas chromatographic retention time, together with mass spectrometric fragmentation patterns of trimethysilyl and acetate derivatives enabled us to assign a suite of C-27-C-30 sterols. Two C-30 sterols were identified as (24E...

Microbialites are organosedimentary structures that are formed through the interaction of benthic microbial communities and sediments and include mineral precipitation. These lithifying microbial mat structures include stromatolites and thrombolites. Exuma Sound in the Bahamas, and Hamelin Pool in Shark Bay, Western Australia, are two locations whe...

Although hypersaline environments pose challenges to life because of the low water content (water activity), many such habitats appear to support eukaryotic microbes. This contribution presents brief reviews of our current knowledge on eukaryotes of water-column haloclines and brines from Deep Hypersaline Anoxic Basins (DHABs) of the Eastern Medite...

Microbialites, which are organosedimentary structures formed by microbial communities through binding and trapping and/or in situ precipitation, have a wide array of distinctive morphologies and long geologic record. The origin of morphological variability is hotly debated; elucidating the cause or causes of microfabric differences could provide in...

Microbialites (stromatolites and thrombolites) are mineralized mat structures formed via the complex interactions of diverse microbial-mat communities. At Highborne Cay, in the Bahamas, the carbonate component of these features is mostly comprised of ooids. These are small, spherical to ellipsoidal grains characterized by concentric layers of calci...

Species-range expansions are a predicted and realized consequence of global climate change. Climate warming and the poleward widening of the tropical belt have induced range shifts in a variety of marine and terrestrial species. Range expansions may have broad implications on native biota and ecosystem functioning as shifting species may perturb re...

The responses of marine taxa to ocean acidification are varied, with, for example, some exhibiting decreased and some increased calcification rates. Experiments were conducted to assess the effect of elevated atmospheric carbon dioxide concentrations on the survival, fitness, shell microfabric and growth of Amphistegina gibbosa, a symbiont-bearing,...

Manipulative culture experiments are one means to assess the impact of a changing environment on foraminiferal species composition and abundance. We performed an 11- month long experiment to assess the impact of different feeding rates on foraminiferal reproduction, growth, and species composition. The experiment was run at 7 C and atmospheric p...

Symbioses between Bacteria, Archaea, and Eukarya in deep-sea marine environments represent a means for eukaryotes to exploit otherwise inhospitable habitats. Such symbioses are abundant in many low-oxygen benthic marine environments, where the majority of microbial eukaryotes contain prokaryotic symbionts. Here, we present evidence suggesting that...

Until recently, the process of denitrification (conversion of nitrate or nitrite to gaseous products) was thought to be performed exclusively by prokaryotes and fungi. The finding that foraminifera perform complete denitrification could impact our understanding of nitrate removal in sediments as well as our understanding of eukaryotic respiration,...

In the paper “A culture-based calibration of benthic foraminiferal paleotemperature proxies: 18O and Mg/Ca results” by H. L. Filipsson et al. (Biogeosciences 7, 1335– 1347, doi:10.5194/bg-7-1335-2010, 2010) Fig. 4 was printed twice as Figs. 4 and 5. Please find here the corrected figure.

“Dead zones” are man-made hypoxic zones (oxygen concentrations of less than 2 mg l−1) that include the seafloor and the water column immediately above it. Such low oxygen concentrations result from the aerobic decay of organic debris from locally elevated primary production that is fueled by anthropogenic nutrient inputs to the coastal ocean (e.g.,...

Oxygen-depleted to anoxic regions of marine environments similar to those found in the Cariaco Trench and the deep Black Sea occur globally and have likely persisted throughout the Earth’s history. Such anaerobic environments have no doubt played an important role in the early formation and evolution of the known biosphere. It is likely that eukary...

ANOXIA defines the lack of free molecular oxygen in an environment. In the presence of organic matter, the metabolism of anaerobic prokaryotes soon produces compounds such as free radicals, hydrogen sulfide, or methane that are typically toxic to aerobes. The concomitance of suppressed respiration and the presence of toxic substances suggests that...

Nitrogen can be a limiting macronutrient for carbon uptake by the marine biosphere. The process of denitrification (conversion of nitrate to gaseous compounds, including N(2) (nitrogen gas)) removes bioavailable nitrogen, particularly in marine sediments, making it a key factor in the marine nitrogen budget. Benthic foraminifera reportedly perform...

We measured ingestion and digestion rates of the pathogenic bacterium Campylobacter jejuni by a freshwater ciliate Colpoda sp. to determine whether Campylobacter is able to resist protist digestion. Campylobacter and the nonpathogenic bacterium Pseudomonas putida LH1 were labeled with a 5-chloromethylfluorescein diacetate, which fluoresces in intac...

Benthic foraminifera were cultured for five months at four temperatures (4, 7, 14 and 21 °C) to establish the temperature dependence of foraminiferal calcite δ18O and Mg/Ca. Two Bulimina species (B. aculeata and B. marginata) were most successful in terms of calcification, adding chambers at all four temperatures and reproducing at 7 and 14 °C. For...