Foraminifers (planktonic)

CORREA, NANCY; BOLTOVSKOY, DEMETRIO

Encyclopedia of Marine Geosciences

Springer Verlag

Lugar: Amsterdam; Año: 2016; p. 1 - 15

FORAMS (PLANKTIC) Synonyms Planktonic Foraminifera, Planktonic Foraminifers Definition Planktonic foraminifers (from the Latin ?foramen?: hole or orifice, and ?ferre?: to bear) are exlusively marine, open-ocean, single-celled, eukariotic protists that secrete a multi-chambered calcitic shell. The group comprises 40-50 living morphospecies, but the actual number of genetically different forms is probably much higher. They inhabit all latitudes, chiefly above 100 m depth. Planktonic foraminifers are very important in the biogeochemistry of calcite in the oceans. Their rich fossil record is widely used for stratigraphic and paleoenvironmental studies. Shell and Cell All planktonic foraminifers build shells (around 0.3 mm in size) composed of globular chambers arranged in a streptospiral (where each chamber is half a whorl), planispiral (coiled in a single horizontal plane), trochospiral (helical), or, very rarely, triserial coil. An exception is the genus Orbulina, where the trochospiral test may be resorbed and replaced by a single sphere (Figure 1). Biserial arrangement of chambers is present in some fossil species. The shell is made of calcium carbonate (CO3Ca) with hexagonal crystals (calcite), usually formed by the addition of lamellae separated by organic material. The outer lamella of successive chambers may also cover previous chambers, in which case the wall of earlier parts of the test becomes considerably thicker. In most species prior to gametogenesis the test is covered with an additional calcite layer or crust with coarse crystalline structure. Calcite comprises around 80-90% of the shell material, the remained being represented by MgCO3, FeCO3, SiO2, Sr, and several aminoacids (Boltovskoy and Wright, 1976; Hemleben et al., 1989). The shell wall comprises poreless areas (such as the keel), but most of it is perforated by pores, which are usually obliterated by organic plugs or sieve plates in living specimens. In some species the shell surface may bear pustules or a cancellate, honeycomb-like, ornamentation. Spinose species have long calcitic spines, circular or three-bladed in cross-section, which are shed during gametogenesis. Figure 1. Examples of representative foraminiferal morphospecies. Notice that Globigerina falconensis, Orbulina universa, Globigerinoides ruber, Globigerinoides conglobatus and Sphaeroidinella dehiscens are spinose species (like Globigerinoides sacculifer), but spines are usually absent in speciments retrieved from bottom sediments (like most of those figured here). Scale bar equals 50 µm. G. sacculifer from Bé (1968); all others from Kemle-von Mücke and Hemleben (1999). The cytoplasm typically fills all shell chambers (occasionally the last chamber may be only partly filled), and also extends as a thin layer covering the shell surface, where it forms a dense array of very thin filopodia or reticulopodia. This outer layer may be foamy (?bubble capsule?), or finely reticulate, or smooth and sheath-like. Organelles present in the cytoplasm comprise a single nucleus (usually in one of the inner chambers, with granuar nucleoplasm and strands of chromatin and heterochromatin), small mitochondria, peroxisomes (involved in the synthesis of carbohydrates and metabolism of waste products), endoplasmic reticulum, Golgi complex, vacuoles (digestive, waste, etc.), fibrillar bodies (which probably aid in flotation) (Hemleben et al., 1989). In addition to these, the cytoplasm contains varios inclusions, such as lipid droplets and pigment granules. Reproduction and growth As opposed to benthic species, which show a range of reproductive modes, in planktonic foraminifers the only process that has been observed is the release of thousands of very small (3-5 µm), free-swimming, biflagellated ?swarmers?, which fuse producing a zygote. Subsequently, this zygote grows into an adult individual. Most of the spinose, symbiont-bearing species, as well as some non-spinose ones, have a life span of 2-4 weeks and a lunar or semi-lunar cycle, reproducing at either full moon or new moon; while other non-spinose forms, in particular the deeper-living ones, seem to follow a yearly cycle (Kemle-von Mücke and Hemleben, 1999). All planktonic Foraminifera perform ontogenetic vertical migrations. The deep-living species reproduce in surface waters and then migrate to layers as deep as 1000 m or more (Hemleben et al., 1989). Surface-dwelling species reproduce in the pycnocline or chlorophyll maximum layer and the offspring migrate to the surface. Growth of the shell starts with a small spherical chamber (?proloculus?), and the subsequent addition of progressively larger chambers around it (roughly at the rate of one chamber every 48 hours; Hemleben et al., 1989). Successive stages (five, according to Brummer et al., 1987) are characterized by marked morphological changes, including inflation of chambers, development of pores, development of spine collars, ridges, secondary apertures, etc. Prior to reproduction, the shell wall thickens, spines are shed, and internal septa may disappear. Trophic relationships Most species are fairly omnivorous, feeding on a large spectrum of organisms including diatoms, dinoflagellates, coccolithophorids, radiolarians, ciliates, pteropods, various invertebrate larvae, copepods, etc. Cannibalism has been observed in non-spinose species, but not in spinose forms. Food items can be several times larger than the foraminifer itself. Spinose species tend to prefer animal prey, whereas non-spinose ones feed chiefly on phytoplankton. The prey is surrounded by the protist´s rhizopodia which eventually engulf the organism and transfer ruptured pieces of its body to digestive vacuoles in the extra- or intrashell cytoplasm by protoplasmic streaming (Hembleben et al., 1989). In addition to heterotrophic feeding, many planktonic foraminifers posess algal symbionts (dinoflagellates and chrysophytes) in their cytopasm (Figure 2). Symbiotic algae are common in most (but not all) spinose species (where their presence often seems obligatory), and almost always absent in the non-spinose ones. These algae are normally located in the outer cell layer (where lighting is best), but have also been observed to perform diel migrations within the cell, withdrawing to the inner cytoplasm at night and dispersing around the periphery during the day (Bé et al., 1977). A single foraminifer may host as many as 10,000 symbiotic algae (Spero and Parker, 1985), which are either digested or released into the environment when the host reproduces (thus, newborns acquire their symbionts from the medium, rather than from their parents). For the foraminifer, the advantages of this symbiotic relationship are the energy supply (either as free extracellular organic matter or when symbionts are digested by the host), enhancement of calcification, and intracellular elimination of host waste metabolites (Goldstein, 2003). Figure 2. Zooxanthellae (symbiotic algae) dispersed along the spines and rhizopodia of a specimen of Globigerinoides ruber. From Bé et al. (1977). Taxonomy During recent years the taxonomy of most protists has undergone profound changes in association with the widespread use of molecular and biochemical data (e.g., rRNA gene sequences). A subject of particular interest has been the elucidation of phylogenetic relationships between higher rank taxa, for which reason familiar and suprafamiliar assignements have changed repeatedly. According to Lee et al. (2000) planktonic foraminifers are distributed in 2 superfamilies and 9 families included in the Order Globigerinida of the Class Foraminifera, Phylum Granuloreticulosa. A few years later, Adl et al. (2005) placed the Foraminifera in the ?Super Group? Rhizaria, but refrained from further subdividing them because existing morphology-based schemes are not fully consistent with molecular phylogenetic data. At the genus and species level, the classification of Foraminifera has traditionally been based on features of the test, such as spines, coiling, size and arrangement of chambers, ornamentation, etc. (see Hottinger, 2006, for a complete glossary of terms used in foraminiferal research). As opposed to other protozooplanktonic groups, like the radiolarians, the low diversity of planktonic Foraminifera and their comparatively large size has contributed towards developing a reasonably stable classification system. Most researchers recognize between 40 and 50 living morphospecies (Hemleben et al., 1989), although some stretch this number to 64 (Saito et al., 1981). Molecular data, which are presently available for a number of species, never suggest the need to lump existing morphospecies, but often indicate that traditional taxonomy has included several genetically different organisms under a single name. De Vargas et al. (2004) noticed that the eight morphological species that have been genetically analyzed (DNA sequence coding for the Small SubUnit and Internal Transcribed Spacer of the nuclear ribosomal RNA) until that year contain between three and six distinct genetic entities (?sister species?) each. Interstingly, upon closer examination most of the new, genetically identified species within traditional morphological species, turn out to show minor but recognizable morphological differences (De Vargas et al., 2004). It seems plausible that niche partitioning (driven by regional differences in food availability, salinity, temperature), rather than allopatric speciation through vicariance, is responsible for this diversification (Darling and Wade, 2008; Seears et al., 2012). Geographic patterns of abundance and species composition Data on the distribution patterns of living planktonic Foraminifera come from three sources: plankton tows, sediment traps, and surface sediment samples. Each have advantages and drawbacks. Plankton samples retrieve whole assemblages (unless the mesh size used is too large) unbiased by post-mortem processes (see below), but the sample-size is normally limited and the sample is but a snapshot representative of a very restricted time offset. Sediment traps are particularly suitable for investigating temporal cycles and sedimentation processes, but their yields are subject to several distorting mechanisms, such as lateral advection, selective dissolution and fragmentation due to grazing. Surface sediment samples are by far the most widely available and used for biogeographic purposes, but as proxies of the distribution of the living assemblages they are also the most biased. The sedimentary remains of planktonic foraminifers can differ strongly from the corresponding planktonic assemblages due to a number of mechanisms, including selective dissolution of the less resistant shells (both on the way to the sea floor and after settling), reworking by bottom fauna, winnowing by bottom currents, lateral advection by subsurface and deep currents, submersion and extended survival of colder water forms under warmer water areas (?equatorward shadows?), fragmentation due to grazing, vertical integration of shallow and deep-living species, different reproduction modes, and integration of seasonally dissimilar abundance patters (Vincent and Berger, 1981; Boltovskoy, 1994). Many of these modifications tend to enhance the proportions of cold water species, resulting in assemblages indicative of colder waters than those overlying the corresponding sediments. Despite these shortcomings, the world-wide biogeographic pattern originally proposed by Bé (1977), based chiefly on sedimentary samples, is the most widely accepted today and probably realistic in general terms (Figure 3). Figure 3. Major foraminiferal biogeographic provinces (slighly modified from Bé, 1977); notice resemblance with pattern of mean annual temperature at 10 m (based on data from Locarnini et al., 2006); temperature intervals are: 26 °C. Bar graph at bottom right shows numbers of foram species recorded in each biogeographic province in the South Artlantic (highlighted on main map), as a proportion of the overall total (39) for this area (based on data from Kemle Von-Mucke and Hemleben, 1999). As with most other zooplanktonic organisms, the two major attributes of foraminiferal distribution patterns respond to different constraints: species compositions depend mainly on temperature, whereas abundance depends on primary production. Within normal open-ocean values, other variables have little influence on foraminiferal biogeography. For example, planktonic Foraminifera are scarce or absent altogether in low salinity waters (i.e., below 30?, Boltovskoy and Wright, 1976), but above these values the influence of salinity is very limited (Bijma et al. 1990). The world-wide biogeography of planktonic foraminifers is characterized by a system of latitudinally oriented belt-like provinces, punctuated by conspicuous north-south drifts where ocean currents distort the east-west orientation of isotherms (like, for example, the Gulf Stream in the North Atlantic, or the Humboldt Current in the South Pacific; Figure 3). The limits of these provinces are strikingly similar to near-surface isotherms (Figure 3), which reinforces the notion of the overwhelming importance of temperature for determining specific makeups. Each province is characterized by a particular combination of co-occurring species, but individual species ranges seldom coincide with province boundaries, so that specific ranges overlap extensively and species restricted to any one province are very few (normally below 10% of those present anywhere in the province). Diversity drops conspicuously from the equator to the poles, but highest numbers of species are often found in the subtropics (Figure 3). With a few exceptions, known morphospecies inhabit all three major oceans. Most species dwell in the surface waters, either during their entire life (all species of Globigerinoides, several Globigerina), or as juveniles, while the adults migrate below 100 m (Globigerinella adamsi, Sphaeroidinella dehiscens, Neogloboquadrina pachyderma, etc.), but a number of forms are usually found at 50-100 m (Globigerina bulloides, Hastigerina pelagica, Orbulina universa, Globigerinella aequilateralis, Globigerina calida, Pulleniatina obliquiloculata, Neogloboquadrina dutertrei, Candeina nitida, Globigerinita glutinata). The only deep-water (below 1000 m) form is Hastigerinella digitata (Bé, 1977). Foraminiferal abundances normally range around 0.001 to >1 individuals per L of water, with oligotrophic central oceanic gyres hosting the lowest densities, and high-productivity upwelling regions the highest. Peak densities, however, have been recorded in sea-ice communities (ca. 500 individuals per L; Arnold and Parker, 2003). Although vertical abundance profiles depend on the vertical migrations (chiefly ontogenetic) which most species perform, normally they are characterized by peak abundances in the euphotic layer, around 10-50 m, and steeply decreasing values below this depth (Figure 4). Figure 4. Vertical distribution of planktonic Foraminifera at 3 stations in the Sea of Japan in Fall (from Kuroyanagi and Kawahata, 2004). The annual flux of calcitic tests at 100 m water depth is around 1.3-3.2 Gt, which represents 23-56% of the global, open marine CaCO3 flux. Although much of the calcium carbonate dissolves before reaching the seafloor, the numbers of tests that do settle on the bottom are so high that the resulting carbonate oozes cover almost 50% of the sea floor (Lisitzyn, 1974; Kennett, 1982) (see Deep-Sea Sediments), with remains of planktonic foraminifers largely dominating these deposits, especially in the open ocean. The distribution of this so called ?Globigerina ooze?, however, is uneven. Because the dissolution of calcite increases with depth (see Carbonate Dissolution), down to about 3500 m (depending on ocean basin and area) preservation of foraminiferal tests is excellent or good; between this depth (known as the lysocline) and ca. 4500 m, dissolution is considerably faster and preservation deteriorates rapidly. Below 4500, which is known as the calcite compensation depth (see CCD), the rate of supply of calcium carbonate is balanced by the rate of dissolution, so there is no net accumulation (Seibold and Berger, 1996). Stratigraphic and paleoecologic applications The geologic record of planktonic foraminifers dates back to the late Triassic or Jurassic (BouDagher-Fadel, 2012), becoming particularly abundant since the mid-Cretaceous. They have been used extensively for defining zonal stratigraphies from the upper Valanginian to the Recent (Bolli et al., eds, 1985), proving of great value for oil exploration purposes (see Biostratigraphy). Recent assemblages from the water-column have been used in biogeographic surveys and as tracers of currents and water masses (e.g., Boltovskoy and Wright, 1976). Paleoceanographic studies with Foraminifera are based on several approaches (see Paleoceanography, Paleoceanographic proxies). Past changes in the proportions of species as compared with present-day specific makeups (usually aided by more or less complex mathematical manipulations of the data, like the transfer function techniques proposed by Imbrie and Kipp, 1971), allow reconstructing past ecological and oceanographic settings (temperature, fronts, primary productivity; e.g., CLIMAP, 1976). Downcore changes in the relationship between right-coiling vs. left-coiling specimens of some species (e.g., Neogloboquadrina pachyderma, whose proportions of right-coiling individuals increase with increasing temperature) have been used to reconstruct the water temperature at which these foraminifers lived. Right- vs left-coiling ratios, however, may also depend on other conditions (e.g., Thiede, 1971; Bolli et al., eds, 1985). Stable isotopes of oxygen and carbon in foraminiferal tests are also used to determine shifts in the temperature, salinity, oxygen content, and fertility of the ocean over past hundreds to millions of years (see Rohling and Cooke, 2003, for a review) (see Carbon Isotopes, Oxygen Isotopes). Bibliography Adl, S. M., Simpson, A. G. B., Farmer, M. A., Andersen, R. A., Anderson, O. R., Barta, J. R., Bowser, S. S., Brugerolle, G., Fensome, R. A., Fredericq, S., James, T. Y., Karpov, S., Kugrens, P., Krug, J., Lane, C. E., Lewis, L. A., Lodge, J., Lynn, D. H., Mann, D. G., Mccourt, R. M., Mendoza, L., Moestrup, Ø., Mozley-Standridge, S. E., Nerad, T. A., Shearer, C. A., Smirnov, A. V., Spiegel, F. W., and Taylor, M. F. J. R., 2005. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. The Journal of Eukaryotic Microbiology, 52: 399-451. Arnold, A. J., Parker, W.C., 2003. Biogeography of planktonic Foraminifera. In Sen Gupta, B. K. (ed.), Modern Foraminifera, New York: Kluwer, pp. 103-122. Bé, A. W. H., 1968. Shell porosity of Recent planktonic Foraminifera as a climatic index. Science, 161: 881-884.. Bé, A. W. H., 1977. An ecological, zoogeographic and taxonomic review of Recent planktonic Foraminifera. In Ramsay, A. T. S. (ed.), Oceanic Micropaleontology, London: Academic Press, pp. 1-101. Bé, A. W. H., Hemleben, Ch., Anderson, O. R., Spindler, M., Hacunda, J., Tuntivate-Choy, S. 1977. Laboratory and field observations of living planktonic Foraminifera. Micropaleontology, 23: 155-179. Bijma, J., Faber Jr, W. W., Hemleben, C., 1990. Temperature and salinity limits for growth and survival of some planktonic foraminifers in laboratory cultures. Journal of Foraminiferal Research, 20: 95-116. Bolli. H. M., Saunders, J. B., Perch-Nielsen, K. (eds.), 1985. Plankton Stratigraphy. London: Cambridge University Press, pp. 1-1032. Boltovskoy, D., 1994. The sedimentary record of pelagic biogeography. Progress in Oceanography, 34: 135-160. Boltovskoy, E., Wright, R., 1976. Recent Foraminifera. The Hague: W. Junk, pp. 1-515. BouDagher-Fadel, M. K., 2012 Biostratigraphy and geological significance of planktonic Foraminifera. In Wignall, P. B. (ed.), Developments in paleontology and stratigraphy, 22, New York: Elsevier, pp. 1-301. Brummer, G. J. A., Hemleben, Ch., Spindler, M., 1987. Ontogeny of extant spinose planktonic Foraminifera (Globigerinidae), a concept exemplified by Globigerinoides sacculifer (Brady) and G. ruber (d´Orbigny). Marine Micropaleontology, 12: 357-381. CLIMAP Project Members, 1976. The surface of the ice age earth. Science, 191: 1131?1137. Darling, K. F., Wade, C. M., 2008. The genetic diversity of planktic foraminifera and the global distribution of ribosomal RNA genotypes. Marine Micropaleontology, 67: 216?238. de Vargas, C., Saez, A. G., Medlin L., Thierstein, H. R., 2004. Super-species in the calcareous plankton. In Thierstein, H. R., Young, J. R., (eds.), Coccolithophores: from molecular proccesses to global impact. Berlin/Heidelberg: Springer-Verlag, pp. 251?298. Goldstein, S. T., 2003 Foraminifera: A biological overview. In Sen Gupta, B. K. (ed.), Modern Foraminifera, New York: Kluwer, pp. 37-55. Hemleben, Ch., Spindler, M., Anderson, O. R. 1989. Modern Planktonic Foraminifera. New York: Springer Verlag, pp. 1-363. Hottinger, L. 2006. Illustrated glossary of terms used in foraminiferal research. http://paleopolis.rediris.es/cg/CG2006_M02/index.html. Imbrie, J., Kipp, N.G., 1971. A new micropaleontological method for quantitative paleoclimatology: application to a late Pleistocene Caribbean core. In Turekian, K. K. (ed.), The Late Cenozoic Glacial Ages, New Haven: Yale University Press, pp. 71?181. Kemle-Von Mücke, S., Hemleben, C., 1999. Foraminifera. In Boltovskoy, D. (ed.), South Atlantic Zooplankton. Leiden: Backhuys Publishers, p. 43-73. Kennett, J. P. 1982. Marine Geology. Englewood Cliffs: Prentice Hall, pp. 1-813. Kuroyanagi, A., Kawahata, H., 2004. Vertical distribution of living planktonic foraminifera in the seas around Japan. Marine Micropaleontology, 53: 173?196. Lee, J. J., Pawlowski, J., Debenay, J.-P., Whittaker, J., Banner, F., Gooday, A. J., Tendal, O., Haynes, J., Faber, W. W., 2000. Class Foraminifera. In Lee, J. J. (ed.), The Illlustrated Guide to the Protozoa, 2nd ed., Lawrence, Kansas: Society of Protozoologists, pp. 872-951. Lisitzyn, A. P.,1974. Osadkoobrazovanie v okeanakh. Moskva: Nauka, pp. 1-438. Locarnini, R. A., Mishonov, A. V., Antonov, J. I., Boyer, T. P., Garcia, H. E., 2006. World Ocean Atlas 2005, Volume 1: Temperature. In Levitus, S. (ed.), NOAA Atlas NESDIS 61, U.S. Government Printing Office, Washington, D.C., pp. 1-182. Rohling, E. J., Cooke, S., 2003. Stable oxygen and carbon isotopes in foraminiferal carbonate shells. In Sen Gupta, B. K. (ed.), Modern Foraminifera, New York: Kluwer, pp. 239-258. Saito, T., Thompson, P. R., Breger, D., 1981. Systematic Index of Recent and Pleistocene Planktonic Foraminifera. University of Tokyo Press: Tokyo, pp. 1-190. Seears, H. A., Darling, K. F., Wade, C. M., 2012 Ecological partitioning and diversity in tropical planktonic foraminifera. BMC Evolutionary Biology, 12:54. Seibold, E., Berger, W. H., 1996. The Sea floor. Berlin: Springer-Verlag, pp. 1-356. Sen Gupta, B. K. (ed.), 2002. Modern Foraminifera. New York: Kluwer, pp. 1-371. Spero, H.J., Parker, S.L., 1985. Photosynthesis in the symbiotic planktonic foraminifer Orbulina universa and its potential contribution to oceanic primary productivity. Journal of Foraminiferal Research, 15: 273?281. Thiede, J., 1971. Variations in coiling ratios of Holocene planktonic foraminifera. Deep-Sea Research, 18: 823?831. Vincent, E., Berger, W.H. 1981. Planktonic foraminifera and their use in paleoceanography. In Emiliani, C. (ed.), The Oceanic Lithosphere, The Sea, Vol. 7, New York: Wiley, pp. 1025-1119. Cross-references Biostratigraphy Carbon isotopes/-stratigraphy Carbonate dissolution CCD Deep-sea sediments Foraminifers (benthic) Marine microfossils Oxygen isotopes and ?stratigraphy Paleoceanographic proxies Paleoceanography Demetrio Boltovskoy