Anthony E. Rathburn

Benthic foraminifera associated with cold methane seeps on the northern California margin: Ecology and stable isotopic composition

Release of methane from large marine reservoirs has been linked to climate change, as a causal mechanism and a consequence of temperature changes, during the Quaternary and the Paleocene. These inferred linkages are based primarily on variations in benthic foraminiferal stable isotope signatures. Few modern analog data exist, however, to assess the influence of methane flux on the geochemistry or faunal characteristics of benthic foraminiferal assemblages. Here we present analyses of the ecology and stable isotopic compositions of living (Rose Bengal stained) and dead (fossil) foraminifera (>150 mm) from cold methane seeps on the slope off of the Eel River, northern California (500‐525 m), and discuss potential applications for reconstructions of methane release in the past and present. Calcareous foraminiferal assemblages associated with Calyptogena clam bed seeps were comprised of species that are also found in organic-rich environments. Cosmopolitan, paleoceanographically important taxa were abundant; these included Uvigerina, Bolivina, Chilostomella, Globobulimina ,a ndNonionella. We speculate that seep foraminifera are attracted to the availability of food at cold seeps, and require no adaptations beyond those needed for life in organic-rich, reducing environments. Oxygen isotopic values of the tests of living foraminiferal assemblages from seeps had a high range (up to 0.69‰) as did carbon isotopic values (up to 1.02‰). Many living foraminiferal isotope values were within the range exhibited by the same or similar species in non-seep environments. Carbon isotopic values of fossil foraminifera found deeper in the sediments (18‐20 cm), however, were 4.10‰ ( U. peregrina) and 3.60‰ ( B. subargentea) more negative than living d 13 C values. These results suggest that d 13 C values of foraminiferal tests reflect methane seepage and species-specific differences in isotopic composition, and can indicate temporal variations in seep activity. A better understanding of foraminiferal ecology and stable isotopic composition will enhance paleo-seep recognition, and improve interpretations of climatic and paleoceanographic change.

Temporal variability in living deep-sea benthic foraminifera: a review

The deep ocean environment is disturbed by various processes, many of which involve episodic inputs of organic matter. Some inputs (e.g., phytodetritus at mid-high latitudes in the North Atlantic and Northeast Pacific) are seasonally pulsed, others (e.g., falls of whale carcasses) are irregular and unpredictable, but together, they evoke a variety of responses from the benthic biota. In the case of deep-sea foraminifera, only those responses arising from seasonal food pulses have been fairly well-documented. The population dynamics of deep-sea benthic foraminifera (total live populations and individual species) appear to be controlled largely by two inversely-related parameters, the flux of organic matter to the seafloor and concentrations of oxygen in the sediment porewater. Organic matter (food) inputs are most intense along bathyal continental margins, and their oxidation often leads to the depletion of oxygen in surface sediments. Under these conditions, foraminiferal faunas are dominated by low-oxygen tolerant, infaunal species, the abundance of which fluctuate in response to seasonally varying amounts of food and oxygen. At some sites (e.g., Sagami Bay, off Japan), species migrate up and down in the sediments, tracking critical oxygen concentrations. Where oxygen concentrations are consistently low (less than about 0.5 ml l−1), as in parts of the California Borderland, foraminifera may undergo population increases solely in response to food pulses. In the abyssal North Atlantic, and in some continental margin areas of this ocean, organic matter inputs are weaker and do not lead to oxygen depletion within surface sediments. These systems are food limited and seasonal population fluctuations reflect the availability of food (phytodetritus) rather than oxygen. Here, the species which respond to phytodetritus are mainly epifaunal or shallow infaunal opportunists which represent a small proportion of highly diverse communities (2 or 3 out of >120 species per core of 25.5 cm2 surface area). Seasonal phytodetrital pulses to the deep-seafloor, and hence, foraminiferal population dynamics, are not entirely predictable. Being dependent on climatic and upper-ocean processes, they vary in intensity from year to year and occasionally (e.g., at the Porcupine Abyssal Plain (PAP) in 1997) fail to materialise. Foraminiferal responses to irregular (non-seasonal) organic matter inputs are poorly-known. However, there is some evidence that whale falls, turbidite deposits, hydrothermal vents and seeps are exploited by species typical of organically-enriched, low-oxygen environments rather than by a specialised fauna. Fossil foraminiferal assemblages from bathyal and abyssal environments may provide evidence for an increase or decrease in the seasonality of surface production as well as for longer-term changes in palaeoproductivity. However, the accurate interpretation of this record depends on filling the many gaps which remain in our understanding of relations between benthic foraminiferal ecology and seasonal phenomena in the deep ocean.

Benthic processes on the Peru margin: a transect across the oxygen minimum zone during the 1997-98 El Nino

Oxygen minimum zones (OMZs) are widespread features in the most productive regions of the world ocean. A holistic view of benthic responses to OMZ conditions will improve our ability to predict ecosystem-level consequences of climatic trends that influence oxygen availability, such as global warming or ENSO-related events. Four stations off Callao, Peru (~12°S, Station A, 305 m; Station B, 562 m; Station C, 830 m and Station D, 1210 m) were sampled to examine the influence of the low bottom-water oxygen concentration and high organic-matter availability within the OMZ (O2 < 0.5 ml L−1) on sediments, benthic communities, and bioturbation. Sampling took place during early January 1998, an intense El Nino period associated with higher-than-normal levels of O2 on the shelf and upper slope. Peru slope sediments were highly heterogeneous. Sediment total organic carbon content exceeded 16%, lamination was present below 6 cm depth, and filamentous sulfur bacteria (Thioploca spp.) were present at Station A, (305 m, O2 < 0.02 ml L–1). Deeper sites contained phosphorite crusts or pellets and exhibited greater bottom-water oxygenation and lower content and quality of organic matter. X-radiographs and 210Pb and 234Th profiles suggested the dominance of lateral transport and bioturbation over pelagic sedimentation at the mid- and lower slope sites. Macrofauna, metazoan meiofauna and foraminifera exhibited coherence of density patterns across stations, with maximal densities (and for macrofauna, reduced diversity) at Station A, where bottom-water oxygen concentration was lowest and sediment labile organic matter content (LOC: sum of protein, carbohydrate and lipid carbon) was greatest. Metazoan and protozoan meiofaunal densities were positively correlated with sediment LOC. The taxa most tolerant of nearly anoxic, organic-rich conditions within the Peru OMZ were calcareous foraminifera, nematodes and gutless phallodrilinid (symbiont-bearing) oligochaetes. Agglutinated foraminifera, harpacticoid copepods, polychaetes and many other macrofaunal taxa increased in relative abundance below the OMZ. During the study (midpoint of the 1997–98 El Nino), the upper OMZ boundary exhibited a significant deepening (to 190 m) relative to ‘normal’, non-El Nino conditions (< 100 m), possibly causing a mild, transient oxygenation over the upper slope (200–300 m) and reduction of the organic particle flux to the seabed. Future sampling may determine whether the Peru margin system exhibits dynamic responses to changing ENSO-related conditions.

Magnesium and strontium compositions of Recent benthic foraminifera from the Coral Sea, Australia and Prydz Bay, Antarctica

Analyses of the Mg/Ca and Sr/Ca ratios of the modern benthic foraminifera, Cibicides wuellerstorfi (epifaunal) and Uvigerina species (infaunal) from the Coral Sea, and Cibicides refulgens (epifaunal) and Trifarina angulosa (infaunal) from Prydz Bay, Antarctica revealed relationships with temperature that have possible applications for reconstructions of bottom-water paleotemperatures. A positive relationship exists between the Mg/Ca and Sr/Ca ratios of Cibicides wuellerstorfi and Cibicides refulgens and ambient temperatures, at least within the range of -2 and 6°C. For the correlation between Mg/Ca compositions and temperature the r2 values range from 0.78 (C. wuellerstorfi alone) to 0.88 (C. wuellerstorfi and C. refulgens together). At present, the Mg/Ca-temperature relationship must be regarded as tentative because of significant overlap of standard error values. The relationship between the Sr/Ca compositions of C. wuellerstorfi and bottom-water temperature yields an r2 value of 0.95. These results indicate that Sr/Ca and possibly Mg/Ca ratios of Cibicides wuellerstorfi may provide useful information for the assessment of paleotemperature. Single-species data are presently insufficient to assess the influence of ambient temperature on trace-element compositions of Uvigerina species. Trifarina angulosa may have Mg/Ca compositions which are positively related to temperature, but Sr/Ca values seem unaffected by temperature. This may be due to pore-water influences on infaunal tests or to vital effects. Although more modern data are needed, our present results suggest that Sr/Ca ratios and possibly Mg/Ca ratios of some benthic foraminifera have the potential to be useful paleothermometers, at least within a temperature range of −2 to 6°C.

Microfossil and stable-isotope evidence for changes in Late Holocene palaeoproductivity and palaeoceanographic conditions in the Prydz Bay region of Antarctica

Microfaunal and microfloral data from two gravity cores, and stable-isotope results from one of these cores taken on Fram Bank near Prydz Bay, Antarctica indicate changes in sea-ice patterns and oceanographic conditions which may have been linked to regional and global climate changes that occurred over the past 8000 yr. Modern diatom assemblages indicative of ice free conditions 1–2 months of the year, and dominated by Nitzschia species became prevalent some time around 2000–2700 yr B.P. The occurrence of Chaetoceros spp. diatom spore-dominated assemblages, and increased abundances of benthic and planktonic foraminifera, ostracods, and diatoms, coupled with carbon- and oxygen-isotope changes around 2700–3400 yr B.P. strongly suggests that this area of the shelf experienced conditions conducive to increased productivity during this time period. Based on diatom assemblage associations recognized in modern environments, the upper water column of Fram Bank shelf waters was probably stratified during that time due to the presence of low-salinity melt water and a very shallow mixed layer, protected from storms, with sea-ice cover for less than 10 months per year. The close correspondence of δ13C and δ18O values from N. pachyderma (r2 = 0.74) throughout one core suggests that whatever oceanographic conditions influenced δ18O also influenced δ13C. Changes in Prydz Bay microfossil abundances and isotopes may result from alterations in circulation patterns, upwelling conditions, or sea-ice patterns which significantly affected benthic and planktonic productivity in the area. The environmental conditions indicated by older sediments in the cores are less clear, but an ice tongue may have been in place 3200–3800 yr B.P., and minor fluctuations in productivity are indicated around 6000 and 7000–7500 yr B.P. The lower 100 cm of both cores may not represent in situ deposition, but if the corrected AMS dates reflect the actual age of the sediments analyzed, microfossil and isotope data indicate that productivity, and oceanographic conditions were very variable around 8500-8600 yr B.P. The chronology adopted herein must be regarded as tentative until further study of the area has been undertaken.

A hydrothermal seep on the Costa Rica margin: middle ground in a continuum of reducing ecosystems

Upon their initial discovery, hydrothermal vents and methane seeps were considered to be related but distinct ecosystems, with different distributions, geomorphology, temperatures, geochemical properties and mostly different species. However, subsequently discovered vents and seep systems have blurred this distinction. Here, we report on a composite, hydrothermal seep ecosystem at a subducting seamount on the convergent Costa Rica margin that represents an intermediate between vent and seep ecosystems. Diffuse flow of shimmering, warm fluids with high methane concentrations supports a mixture of microbes, animal species, assemblages and trophic pathways with vent and seep affinities. Their coexistence reinforces the continuity of reducing environments and exemplifies a setting conducive to interactive evolution of vent and seep biota.

Relationships between the stable isotopic signatures of living and fossil foraminifera in Monterey Bay, California

[1] Fossil foraminifera are critical to paleoceanographic reconstructions including estimates of past episodes of methane venting. These reconstructions rely on benthic foraminifera incorporating and retaining unaltered the ambient isotopic compositions of pore fluids and bottom waters. Comparisons are made here of isotopic compositions of abundant live and fossil foraminifera (Uvigerina peregrina, Epistominella pacifica, Bulimina mexicana, and Globobulimina pacifica) collected in Monterey Bay, CA from two cold seeps (Clam Flats and Extrovert Cliffs) and from sediments � 5 m outside of the Clam Flats seep. Clam Flats has steep d 13 CDIC gradients (to <� 45%), but DIC at Extrovert Cliffs is less enriched in 12 C (to approximately � 22%). Oxygen isotope values of fossil foraminifera at Clam Flats are � 1.5% enriched in 18 O over the living foraminifera, as well as those of both live and fossil foraminifera at Extrovert Cliffs, suggesting they may have lived during the last glacial maximum. Statistical comparisons (Student’s t and Kolmogorov-Smirnov tests) of d 13 C and d 18 O values indicate that live and fossil foraminifera come from different populations at both Clam Flats and Extrovert Cliffs. At Clam Flats, the difference appears to result from alteration enriching some fossil foraminifera in 12 C over live foraminifera. At Extrovert Cliffs, the fossil foraminifera are enriched in 13 C over the live foraminifera, suggesting they lived prior to the onset of venting and thus that venting began recently. The short time of venting at Extrovert Cliffs may be responsible for the less alteration there compared with Clam Flats. These results indicate that preservation of foraminifera is likely to be poor within long-lived cold seeps, but that foraminifera living in the surrounding sediment may incorporate and preserve broad basin-wide changes in isotopic compositions of the ambient water.

Bioturbation by symbiont-bearing annelids in near-anoxic sediments: Implications for biofacies models and paleo-oxygen assessments

Anoxic or nearly anoxic conditions (<4 μM O2) have long been associated with the absence of bioturbation and animal traces. This premise has guided interpretation of paleoceanographic conditions from rocks and sediments. We recently observed a high-density, living assemblage of highly mobile, symbiont-bearing, burrowing, phallodrilinid oligochaetes within a nearly anoxic basin (<1 μM O2 [0.02–0.03 ml l−1]) on the Peru margin (305 m). These observations were made during the most intense part of the 1997–98 El Nino when there may have been slight oxygenation of an otherwise anoxic basin, but oligochaete presence prior to this event is likely. The occurrence of symbiont-bearing gutless oligochaetes mainly within the upper 5 cm of the sediment column coincided with a bioturbated zone overlying distinctly laminated sediments. Our observations redefine the lower oxygen limit of macrofaunal bioturbation to ≪2 μM, and indicate a need to modify currently accepted ideas about the relationship between bioturbation and paleo-oxygen concentration. These results also address an ongoing debate about the lifestyles of bioturbating organisms in oxygen-poor settings.

Phylogenetic placement of Cibicidoides wuellerstorfi (Schwager, 1866) from methane seeps and non‐seep habitats on the Pacific margin

Benthic foraminifera are among the most abundant groups found in deep-sea habitats, including methane seep environments. Unlike many groups, no endemic foraminiferal species have been reported from methane seeps, and to our knowledge, genetic data are currently sparse for Pacific deep-sea foraminifera. In an effort to understand the relationships between seep and non-seep populations of the deep-sea foraminifera Cibicidoides wuellerstorfi, a common paleo-indicator species, specimens from methane seeps in the Pacific were analyzed and compared to one another for genetic similarities of small subunit rDNA (SSU rDNA) sequences. Pacific Ocean C. wuellerstorfi were also compared to those collected from other localities around the world (based on 18S gene available on Genbank, e.g., Schweizer et al., 2009). Results from this study revealed that C. wuellerstorfi living in seeps near Costa Rica and Hydrate Ridge are genetically similar to one another at the species level. Individuals collected from the same location that display opposite coiling directions (dextral and sinstral) had no species level genetic differences. Comparisons of specimens with genetic information available from Genbank (SSU rDNA) showed that Pacific individuals, collected for this study, are genetically similar to those previously analyzed from the North Atlantic and Antarctic. These observations provide strong evidence for the true cosmopolitan nature of C. wuellerstorfi and highlight the importance of understanding how these microscopic organisms are able to maintain sufficient genetic exchange to remain within the same species between seep and non-seep habitats and over global distances.

A New biological proxy for deep-sea paleo-oxygen: Pores of epifaunal benthic foraminifera.

The negative consequences of fossil fuel burning for the oceans will likely include warming, acidification and deoxygenation, yet predicting future deoxygenation is difficult. Sensitive proxies for oxygen concentrations in ancient deep-ocean bottom-waters are needed to learn from patterns of marine deoxygenation during global warming conditions in the geological past. Understanding of past oxygenation effects related to climate change will better inform us about future patterns of deoxygenation. Here we describe a new, quantitative biological proxy for determining ocean paleo-oxygen concentrations: the surface area of pores (used for gas exchange) in the tests of deep-sea benthic foraminifera collected alive from 22 locations (water depths: 400 to 4100 m) at oxygen levels ranging from ~ 2 to ~ 277 μmol/l. This new proxy is based on species that are widely distributed geographically, bathymetrically and chronologically, and therefore should have broad applications. Our calibration demonstrates a strong, negative logarithmic correlation between bottom-water oxygen concentrations and pore surface area, indicating that pore surface area of fossil epifaunal benthic foraminifera can be used to reconstruct past changes in deep ocean oxygen and redox levels.