John W. Murray

MORTALITY, PROTOPLASM DECAY RATE, AND RELIABILITY OF STAINING TECHNIQUES TO RECOGNIZE ‘LIVING’ FORAMINIFERA: A REVIEW

Non-vital staining, especially with rose Bengal, has been widely used in ecological studies to differentiate between the tests of dead (unstained) foraminifera from those presumed to be living at the time of collection (stained). Doubts have been expressed about staining methods because of the possibility that dead individuals may retain undecayed protoplasm for weeks or months after death; when stained, such individuals would be recorded as living. To assess the importance of such false positives, it is necessary to examine rates of mortality, and the modes of generation of empty tests, i.e., whether due to reproduction, growth stages (leaving empty tests during growth) or death. It can be argued that reproduction, ontogeny, and death through predation lead to tests devoid of protoplasm. Whereas reproduction may affect only a small proportion of the population of each species (due to high pre-reproductive mortality), predation in oxygenated environments may be responsible for the major part of that pre-reproductive mortality. In oxygenated environments, disease or adverse environmental conditions are most likely to lead to dead individuals having tests containing protoplasm. In dysaerobic/anoxic environments, predation by macrofauna may be excluded, so foraminifera die through other causes and thus more tests with dead protoplasm may be potentially available for staining. Therefore, for most other environments, the problem of staining dead individuals is almost certainly overstated. Furthermore, from comparative studies, it seems that the most commonly used technique (staining with rose Bengal) is as reliable as others. Now that new vital staining techniques, especially the use of fluorescent probes, are being introduced, it is timely for further objective comparative studies of all techniques to be made in order to evaluate data already gathered and to develop the best strategies for future ecological studies according to whether they are field-based or experimental.

The niche of benthic foraminifera, critical thresholds and proxies

Ecological studies of benthic foraminifera are carried out to explain patterns of distribution and the dynamics of communities. They are also used to provide data to establish proxy relationships with selected factors. According to niche theory, the patterns of distribution of benthic foraminifera are controlled by those environmental factors that have reached their critical thresholds. For each species, in variable environments, different factors may be limiting distributions both temporally and spatially. For a species or an assemblage to be useful as a proxy its abundance must show a strong correlation with the chosen factor. Since numerous factors influence each species, it is only in those environments where the majority of factors show little variation but one particular factor shows significant variation that the proxy relationship for that factor can be determined. On theoretical grounds, the reliability of using foraminiferal abundance as a proxy of a selected environmental factor should be restricted to the range close to the upper and lower thresholds. For oxygen, foraminifera are potential proxies for the lower limits but once oxygen levels rise to values of perhaps >1 or 2 ml l-1, there is no longer a relationship between oxygen levels and abundance. By contrast, the flux of organic matter over a large range shows a sufficiently close relationship with foraminiferal assemblages so that transfer functions can be derived for the deep sea. However, the relationship at species level is far less clear cut. Much more accurate estimates of primary productivity and modern organic flux rates are required to improve the determination of past flux rates.

A benthic foraminiferal proxy of pulsed organic matter paleofluxes

In the temperate open ocean of the modern northeast Atlantic, the spring bloom of phytoplankton leads to a seasonal pulse of detrital organic material (phytodetritus) to the ocean floor. Opportunistic benthic foraminifera rapidly colonise this food resource, producing large numbers of individuals whose tests are ultimately added to the sediment. One of these taxa,Epistominella exigua, shows periodic peaks in abundance in the fossil record at many open ocean sites. Previously, such peaks have been commonly interpreted to result from changes in physicochemical properties of bottom water mass and thus deep-sea circulation. The main purpose of this paper is to propose thatE. exigua may be used as a proxy of pulsed organic matter inputs to the deep ocean and therefore as an indicator of relative changes in productivity.

Marginal marine environments of the Skagerrak and Kattegat: a baseline study of living (stained) benthic foraminiferal ecology

This is the first detailed investigation of the distribution and ecology of living (stained) shallow water (0–6 m) foraminifera along the Skagerrak–Kattegat coast, eastern North Sea. A total of 25 species (13 agglutinated; 12 calcareous) are common in the 169 sediment surface samples which were collected from 27 geographic areas. The sediment grain size and total organic carbon (TOC) content are strongly variable and the salinity and temperature ranges were 10–31‰ and 9–30°C, respectively, at the time of sampling (July to October) but temperatures down to freezing occur during the winter. The species are divided into six environmental categories of which the first five comprise euryhaline and the sixth essentially stenohaline taxa: (1) species associated only with marsh plants, (2) species basically, but not entirely, associated with marsh plants, (3) species basically, but not entirely, restricted to non-marsh areas, (4) species solely recorded in non-marsh intertidal to subtidal environments, (5) species restricted to subtidal areas, (6) species basically living in the most open marine areas. In this region, marshes have a patchy distribution and they are small and compressed due to low tidal ranges ( 80% mud. Ammoscalaria runiana is common only in coarse-grained sediments (<20% mud) with low TOC (≤0.7%). There are no marked biogeographic boundaries within the Skagerrak–Kattegat area but 10 of the 25 commonly occurring species have not been reported from the adjacent Baltic Sea, probably partly due to the brackish character of the water there. The southern limits of distribution of the northern species, Elphidium albiumbilicatum, Ammotium cassis, and Ophthalmina kilianensis, are in the Kattegat–Baltic Sea.

Natural dissolution of modern shallow water benthic foraminifera: taphonomic effects on the palaeoecological record

Comparison of the living and dead assemblages of benthic foraminifera from the coastal areas of the Skagerrak‐ Kattegat reveals that, although there are considerable similarities in terms of the presence=absence of species, there are major differences in relative abundance at species level. Furthermore, the relative abundance of calcareous tests in the living assemblages is considerably higher than that of the dead assemblages (average values of 67 and 30%, respectively). Since the environments are microtidal, there is little transport of foraminiferal tests due to tidal currents so there are no introduced exotic species although there is local transport caused by waves and wave-induced currents. However, the major taphonomic process appears to be dissolution, of calcareous tests. This is manifested through etching and breakage of test walls, leading to complete decalcification which leaves a residue of organic linings of certain taxa (e.g., Ammonia beccarii), and a marked increase in abundance of agglutinated tests in the dead assemblages. Although dissolution is normal in marsh settings throughout the world, the Skagerrak‐Kattegat area is unusual in the intensity of dissolution in the subtidal zone. Whereas most of the calcareous species occur throughout the investigated depth range (except marsh), two of the subtidal agglutinate species (Eggerelloides scaberand Ammotium cassis) show upper depth limits. Consequently, the agglutinated foraminifera are better indicators than calcareous foraminifera of upper depth limits in these shallow subtidal environments.

MAJOR ASPECTS OF FORAMINIFERAL VARIABILITY (STANDING CROP AND BIOMASS) ON A MONTHLY SCALE IN AN INTERTIDAL ZONE

Temporal and spatial variability of intertidal benthic foraminiferal assemblages in the surface (0–1 cm) sediments have been determined by a time series survey (27 months) of the Hamble estuary, southern England. One pair of replicates was collected each month from two stations at different elevations in the intertidal zone. The assemblages were dominated by three species, Haynesina germanica, Ammonia beccarii (forma tepida ), and Elphidium excavatum. Patchiness occurred on a scale of a few centimeters and had a major impact on tracking temporal changes in the standing crop. The study clearly shows the need for replicate sampling in order to obtain reliable information especially on absolute abundance data. The absence of juveniles is due to loss through drying the samples prior to picking. The results show that it is not possible to determine the lifespan of continuously reproducing species (i.e., young individuals always present) where it is impossible to follow the growth of cohorts, and for the same reason it is not possible to make production calculations. While there is a cyclicity in standing crop at station 2 (mid intertidal zone), this is not the case at station 1 (lower intertidal zone). Species diversity showed reasonable annual cyclicity at both stations. At neither station is there any correlation between the size of the standing crop and the chlorophyll a content of the surface sediment. There was some cyclicity in the peaks of biomass (only determined for sta. 1) in all three species and considerable variability from one year to the next. Thus this area is extremely variable, there is no obvious annual pattern in standing crop, and the best measures of seasonality seem to be species diversity and biomass.

The enigma of the continued use of total assemblages in ecological studies of benthic foraminifera

Pioneering studies of foraminiferal ecology were carried out by Phleger in the 1950s and summarized in his landmark book (Phleger, 1960). He introduced the idea of taking samples of known area and volume, distinguishing live from dead by staining, and attempting to quantify the input of foraminiferal tests to the sediment. Since then advances in ecological understanding have come from improved sediment sampling techniques, the introduction of a spectrum of methods for differentiating live from dead, new technology for determining a wider range of environmental parameters and with ever greater precision, and the application of statistical techniques for determining relationships between biota and environment. However, in spite of this, progress is inhibited by a misconception. Ecological studies should be based on living assemblages and this is invariably the case where they are carried out by biologists. Foraminiferal dead assemblages represent the addition of material from a succession of previous living assemblages time-averaged over several to many years and modified to a lesser or greater extent by taphonomic processes (e.g., transport loss or gain of tests; loss of calcareous …

TEMPORAL VARIABILITY IN VERTICAL DISTRIBUTIONS OF LIVE (STAINED) INTERTIDAL FORAMINIFERA, SOUTHERN ENGLAND

The temporal variability (over 27 months) in abundance, depth of life in the sediment, and species diversity of hard-shelled, live (stained) foraminifera in an intertidal area has been determined. Throughout the investigation period, the same three species (Haynesina germanica, Ammonia beccarii (tepida), Elphidium excavatum) were dominant at the two investigated stations, the maximum abundance of all species (dominant and subsidiary) was in the surface 0.25 cm, and there was a general lack of seasonal change in the vertical distribution of the foraminifera. Seasonality does not seem to be a controlling factor for the vertical distribution of individuals in this area and none of the foraminifera showed high subsurface abundances. Because of the difference in depth position of the redox boundary within the sediment (often 1 cm) and the maximum abundance of individuals (surface 0.25 cm) the former cannot be the main factor limiting their vertical distribution of abundance. The generally high dominance of individuals in the surface few millimeters is probably related to the presence there of microalgal food and limited burrowing activity of the sparse macrofauna. Subsidiary species colonized the area ephemerally, thus the number of species recorded varied from one season to another. The minimum and maximum number of species found at any single sampling event were 5 and 22, whereas the cumulative number of stained species found throughout the investigation period was 35 (plus at least three soft-shelled forms). Species diversity is one of the principal univariate methods used to assess both natural variability and possible human impacts. The large natural seasonal variability demonstrated here suggests that caution should be taken in assessing the significance of diversity changes when based on occasional sampling only.

Taphonomic experiments on marginal marine foraminiferal assemblages: how much ecological information is preserved?

The most important taphonomic processes affecting the composition of benthic foraminiferal assemblages are transport and destruction of tests. The latter includes dissolution of calcareous tests. We have previously simulated nature experimentally by dissolving mainly shelf to deep sea samples in weak acid to give acid-treated assemblages (ATA). In this study we sampled the marginal marine environments of the Skagerrak/Kattegat and found that the main taphonomic process there is dissolution of calcareous tests. Consequently, the taphonomic processes occurring in this area represents a perfect natural analogue of what we suspect to be the main mechanism for the formation of some fossil agglutinated assemblages. The evidence for this is that some living assemblages dominated by calcareous forms become original dead assemblages (ODA) often consisting entirely of agglutinated species and equivalent to ATAs. The principal ATA is dominated by Miliammina fusca and this ATA can be derived from 10 different types of ODA including those that are strongly dominated by various calcareous taxa. This residual M. fusca assemblage represents a broad range of intertidal to shallow subtidal environments. On the other hand, marsh living assemblages are completely agglutinated and obviously give rise to agglutinated ODA/ATAs but not necessarily dominated by the same taxa. All the ATAs faithfully record the low species diversity characteristic of marginal marine environments. The principal conclusion is that in spite of the severe taphonomic loss, the preserved assemblages record much ecological detail. This is in accordance with similar investigations of deeper water assemblages and has important consequences for palaeoecology. This study demonstrates unequivocally that it is always essential to compare data on living and dead assemblages in order to determine the pathways to fossilisation. The use of total (living plus dead) assemblages in this area would give unrepresentative and misleading results.

Living foraminifers of lagoons and estuaries

Specific composition, numerical abundances, size relationships, biomass and diversity relationships, application to paleoecologic studies