• Web Resources on Foraminifera
• References
• Practical: looking at Foraminifera

• Classification, ecology and biogeography of modern forams
  • What are foraminifera?
  • Morphology/taxonomy
  • Phylogeny
  • Environmental indicators
• Limits of actualism?
  • faunal turnovers, extinctions
  • K/T boundary non event
  • Palaeocene/Eocene Thermal Maximum extinction
  • Eocene-Oligocene and middle Miocene: gradual turnovers
  • Pleistocene ‘Stilostomellaextinction’

Charles Darwin, letter to W.B. Carpenter, 1872

• Habitat covers a huge part of the world (largest habitat on Earth)
• Habitat resistant to change -> IF faunas reflect environmental changes (e.g., temperature) -> global change
• Faunas highly diverse, ecological theories may be tested (stability-diversity hypothesis, species-energy hypothesis, patchiness hypothesis)
• Global extinctions in the deep sea: very unusual events, during last 90 million years only one (55 Ma ago)
• Need to understand how they make test if you want to dissolved/analyze it

• neritic = 0-200 m
  • upper bathyal = 200-600 m
  • middle bathyal = 600-1000 m
  • lower bathyal = 1000-2000 m
    • upper abyssal = 2000-3000 m
    • lower abyssal > 3000 m

Note that ‘bathyal’ covers sites on continental margins as well as in open ocean (sea mounts)

• Protist, network of ‘granuloreticulate pseudopodia’
• Complex life cycles (sexual and asexual generations)
• Naked forms exist, commonly a ‘test’ (shell) is present

Genetic information indicates that unicellular eukaryotes, which were until recently classified into the Kingdom Protista (Other Kingdoms: Kingdom Prokaryotes, Kingdom Plantae, Kingom Animalia, Kingdom Fungi). Nowadays we recognize the Superkingdoms Archaea and Eubacteria (formerly Prokaryotes), and the Superkingdom Eukaryotes (Protists, mushrooms, plants, animals). The Superkingdom Eukarya is being reinterpreted, with many group formerly placed together in “protists’ now being elevated to the level of ‘Kingdom’. This means that we now think that, for instance, foraminifera are as different from other protists (e.g., dinoflagellates, radiolarians, diatoms) as cows are from oak trees. Genetic information also strongly indicates that Foraminifera together with test-less, freshwater forms form a monophyletic group, which split off from other life forms early on, maybe in the late Proterozoic.

• Chamber: cavity containing cytoplasm
• Chambers separated by septa; connected by foramina (holes) in septa
• Foramen in last chamber is called aperture
• External lines of junction of chamber walls and septa: sutures
• Chambers enveloping earlier ones: involute
• Chambers leaving earlier ones visible: evolute
• Disk-shaped spiral where two sides look the same: planispiral
• Disk-shaped spiral with one evolute, one involute side: trochospiral

• 1: single chamber (unilocular, monothalamous)
• 2: uniserial
• 3: biserial
• 4: triserial
• 5: planispiral to biserial
• 6: milioline
• 7: planispiral evolute
• 8: planispiral involute
• 9: streptospiral
• 10-12: trochospiral

• 1. Open end of tube
• 2. Terminal radiate
• 3. Terminal slit
• 4. Umbilical
• 5. Loop shaped
• 6. Interiomarginal
• 7. Interiomarginal multiple
• 8. Areal cribrate
• 9. Phialine lip
• 10. Bifid tooth
• 11. Umbilical teeth
• 12. Umbilical bulla

Presently most abundant groups in the deep sea are underlined

• ALLOGROMIDA: organic wall, usually 1 chamber; Cambrian-Recent
• ASTRORHIZIDA:agglutinated, organic cement, usually 1 chamber or branching tube; Cambrian-Recent
• LITUOLIDA: agglutinated, organic cement, many chambers, usually planispiral spiral; Cambrian-Recent
• TROCHAMMINIDA: agglutinated; organic cement, many chambers, usually trochospiral; Cambrian-RecentTEXTULARIIDA: agglutinated, low Mg-calcite cement; Cambrian-Recent
• FUSULINIDA: microgranular calcite; many complex chambers; Silurian-Permian
• MILIOLIDA: high Mg calcite, imperforate, many chambers (porcellaneous, no pores); miliolid chamber arrangment; Carboniferous-Recent
• CARTERINIDA: low Mg calcite, hyaline, pores or no pores; spicules, plani- or trochospiral; Tertiary-Recent (?)
• SPIRILLINIDA: low Mg calcite; hyaline; single crystal; spiral; Jurassic-Recent
• LAGENIDA: low Mg calcite, hyaline; pores, 1 or many chambers, uniserial or planispiral; monolamellar; Carboniferous-Recent
• BULIMINIDA: low Mg calcite; hyaline; pores; many chambers; bilamellar; toothplate; Triassic?-Recent
• ROTALIIDA: low Mg calcite; hyaline;  pores; many chambers; bilamellar; trocho- or planispiral, annular, irregular; Triassic-Recent
• GLOBIGERINIDA: low Mg calcite (aragonite in few extinct forms); pores; many chambers; bilamellar; radial crystals (PLANKTON); Jurassic-Recent
• INVOLUTINIDA: aragonite; 2 chambers - 2nd tube
• ROBERTINIDA: aragonite; pores; many chambers; trochospiral; Triassic-Recent
• SILICOLOCULINIDA:opaline silica, no pores; chamber arrangements as in miliolids; Miocene-Recent

Genetic evidence suggests strongly that Allogromida (‘naked’) and Astrorhizida (agglutinated) are one order.

• All common deep-sea groups today (rotaliids, buliminids, lagenids, textulariids) and many of the more common families and morphotypes within these groups have existed in the deep sea (~>1000 m) since the Late Cretaceous (~ Campanian)
• Miliolids are dominantly warm, shallow water forms, with few genera in the deep sea, since middle Miocene

• Probably not support (small organisms in water - no support needed)
• Probably not protection (many are swallowed whole by predators, although some predators drill holes in tests)
• Metabolism - get rid of salts? (but some forms precipitate calcite from undersaturated water)
• Varying functions: keep nucleus/nuclei protected, keep symbionts together, light for symbionts
• Structures direct pseudopods - feeding importance

• Cytoplasm different from main mass within test (endoplasm - ectoplasm)
• Granules are various organelles (e.g., mitochondria, microtubules, phagosomes)
• Main mass exits from aperture; also protoplasm around test
• Anastomizing; bidirectional flow; streaming process not understood
• Membrane, surrounding microtubules

• Form complex ‘spiderweb’, continually remodeling as while transporting material towards and away from main body
• Motility, attachment, collecting material, extruding material, feeding, exchange gases, chamber formation, protection
• Digestion (partially)

• Herbivores: graze algae
• Passive suspension feeding (pseudopods), e.g., C. wuellerstorfi
• Deposit feeding (very common in deep sea)
• Ingest sediment, algal cells, bacteria, organic detritus
• Carnivory (also multicellular organisms); sticky pseudopods
• Parasitism (other forams, molluscs)
• Uptake of dissolved organic matter
• Endosymbiosis: algae, possibly bacteria; kleptochloroplasts
• Many are selective feeders, e.g., fresh phytoplankton, more degraded matter

• In general: detritivores (non-selective: take up mud with foraminifera and other food particles)
• Mollusca, including various snails (gastropods, e.g., Natica), juveniles of which drill holes in tests
• Specialized foram eater: scaphopods (Dentalium), elephant’s tooth shell

• no males and females differentiated
• variable how common sexual reproduction is: many species have many asexual generations per sexual generation

Note that the gametes may exist in free form for at least several days, and function as ‘propagules’, i.e., help in spreading benthic forms worldwide (hence many cosmopolitan taxa).

(calcite, hyaline)

• Endoplasm combines with pseudopods, assumes shape of next chamber ‘anlage’ (logarithmic size increase), sometimes whole test surrounded by cyst (collected grains, including sediment, algae, etc.)
• Organic lining forms around ‘anlage’; pseudopods active
• Precipitation of calcite on one (monolamellar) or both sides of lining (bilamellar) and over earlier formed chambers

Foraminifera cover calcite wall of earlier chambers, and walls between chambers are (in bilamellar forms) existing of 4 layers (one from each adjoining chamber), so that one should be careful in using spot-analysis (laser-zapping) of foraminiferal subsequent chambers and septa in foraminifera with the aim of using these analysis for very high resolution records.

As an additional complexity: some (porcellaneous) foraminifera have been shown to take up a droplet of water within the cytoplasm, then use ions in the ‘internal pool’ to form thin craysallites within that droplet, thus causing chemical/isotopic heterogeneity. Other use ions from droplet, but appear to keep that droplet open to exchange with sea water.

Some species (e.g., hyaline Amphistegina) use ‘pooled ions’, others (e.g., porcellaneous Amphisorus) do not. We do not know whether these are typical for the larger groups or not; at least another few small hyaline species also used ‘pooled ions’.

Much early data on deep-sea benthic foraminifera (and on other deep-sea groups) were collected on the 1872-1876 Challenger Expedition (benthic foraminifera described by Brady, 1881, 1884). For updated taxonomy and re-publication of plates see Jones, 1994.

• Widely varying estimates of total oceanic foraminiferal biomass; up to 50% of eukaryotic biomass (0.02 to 10 g/m²)
• More than 10⁶/m²
• Opportunistic feeders: species are not usually proxies for a simple environmental parameter (depth, salinity, food supply, oxygen)

Fundamental niche: species could theoretically exist under these condition

Realized niche: species really exists under these conditions (smaller space than fundamental niche)

In the 1970s, Lohmann first recognized that the water masses in the North Atlantic (e.g., AntArctic Bottom Water, AABW, and North Atlantic Deep Water, NADW) were characterized by typical foraminiferal assemblages recognized in multivariate analysis (Lohmann, 1978). It turned out, however, that it was not possible to typify global water masses by faunal assemblages consistently, leading to disappointment in the 1980s. In the 1990s, however, many new studies of recent faunas were directly or indirectly linked to the JGOFS (Joint Global Ocean Flux Studies), and led to recognition of the importance of food in the life of foraminifera: they depend upon food delivered from primary productivity in the surface waters, 1000s of meters away.

Marine snow: particles mm-cm sized, consisting of dead and dying phytoplankton, zooplankton exoskeletons, fecal matter). These fall at a speed of 10²-10³ m/day; a single unicellular alga would probably not even sink to the sea floor, being re-suspended many times.

Seasonality of productivity at pelagic mid latitudes: pulse of phytodetritus, followed by rapid growth-reproduction of some benthic foraminifera

Relatively high, continuous supply along continental margins; there freshly produced organic matter is augmented with more refractory organic material derived from lateral transport

Very little (~1% or less) primary produced material reaches sea floor; follows seasonal productivity (‘fresh phytodetritus)

Ballasted by silica (diatoms), carbonate (foraminifera), dust; in fecal pellets; in glutinous material (diatoms, cyanobacteria); in ‘giant balls of mucus’, larvacean (tunicate) houses; carrion falls (‘dead whales’); lateral transport (refractory organic matter)

Discrepancy between food requirements of faunas and supply in sediment traps: faunas need more than what is delivered

In the present world we thus see bentho-pelagic coupling, in which the benthic faunas reflect what happens at the ocean surface where their food is produced.

Jorissen et al., 1995: TROX model (TR - trophic, food; OX - oxygen). Food is main limiting/determining factor in low food regions, where all organic matter is used up at the sediment/water interface. In such regions there is no food for infaunal ) within sediment) species. In very high food regions, the foraminifera and other organism do not eat everything raining down, and the sediment pore waters become anoxic (oxidation of some organic matter); here also foraminifera can not live within the sediment. In mesotrophic regions foraminifera may live down until 10-15 cm, with epifaunal, shallow infaunal, middle infaunal and deep infaunal taxa.

Can we use present benthic foraminifera as source for proxy information on such environmental parameters as temperature, salinity, depth, primary productivity, oxygenation? If  we can, is that information valid for reconstruction of past environments?

• Generally, not useful for age determination (Late Cretaceous-Paleogene; early-middle Eocene; Oligocene-early Miocene; middle Miocene-Recent
• Shelf - upper slope faunas are used in biostratigraphy, as are larger benthic foraminifera (reefal environments)

1. Planktic/Benthic ratio: paleodepth, dissolution, surface productivity
2. Benthic Foraminiferal Accumulation Rate: surface productivity
3. Species % abundance, Species Diversity: paleodepth, oxygenation of bottom waters, productivity, seasonality of productivity, labile/refractory organic matter, water masses, current activity, CaCO₃ corrosivity
4. ‘Morphotypes’: microhabitats (infaunal/epifaunal) oxygenation, productivity

1. Planktic/Benthic

• Paleodepth: planktic forams not in coastal zones (neritic), P/B >>100 in open ocean
• Dissolution: planktic forams fragment, dissolve before benthics; deep-sea floor low P/B values indicate depth below lysocline
• Surface productivity: more difficult, but at higher food supply productivity (or: in shallower waters) more benthic foraminifera

How to distinguish planktic and benthic foraminifera:

• If there are zillions of them (in absence of dissolution), they’re plankton
• There are MANY fewer planktic species, so know your planktics (size fraction). In plankton, the chamber form is inflated, the wall structure may be cancellate, aperture is interiomarginal (but aperture may be covered, there may be multiple apertures).
  • Difficulties:
    • Trochospiral forms : look at aperture
    • Biserial forms: look at aperture (but there are forms, e.g., biserial genus Streptochilu, looks very much like the benthic genus Bolivina

2. Benthic Foraminiferal Accumulation Rate (BFAR): how does ‘food reaching bottom’ relate to ‘primary productivity’?

• Linkage between surface productivity and quantity of bottom life (Herguera & Berger; number of forams/m²/kyr; >150 mm)
• How much food reaches the sea floor: not ONLY dependent upon productivity (water depth), not a linear relation
• Lateral transport of organic matter (focusing)
• Labile/refractory organic matter
• Discrepancy between observations of sediment community oxygen consumption and particulate organic carbon (SCOC:POC)

3.a Species % abundance

• Paleodepth: observation (photosymbionts)
• Oxygenation of bottom waters, productivity: very difficult to separate effects
• Seasonality of productivity: ‘phytodetritus species’, i.e., observation
• Labile/refractory organic matter: observations, feeding experiments
• Water masses: observations
• Current activity: observations, shape of foraminifera (‘tree-shaped’)
• CaCO₃ corrosivity: observations (Nuttallides umbonifera)

3b. Species Richness, Diversity

• Deep-sea faunas: highly diverse, MANY species rare, few species common (many benthic specimens needed for analysis)
• Species richness: number of species (number of specimens counted) - rarefaction techniques
• Various mathematical expressions of a combination of number of species present and evenness of distribution of specimens over species (e.g., Shannon-Weaver)
• Low diversity, high dominance (low evenness): disturbed/not favorable environment

4. ‘Morphotypes’: Infaunal/Epifaunal

• Can we determine mode of living from shape of test ? E.g., infaunal epifaunal? Thus know the ‘microhabitat’ in which the foram lives? Example: biserial = infaunal; trochospiral = epifaunal
• Partially, yes. Many exceptions, even with present-day forams (Buzas et al., ‘93: assignments ~ 75% correct)
• Foraminifera move through sediment (follow food and/or oxygen gradients)
• Effects low oxygen (oxygen important ONLY if <0.5 to 1.0 mg/L); Kaiho Benthic Foram Oxygenation Index BFOI doubted (Kaiho, 1994, 1999)

How to define infaunal and epifaunal:

Average Living Depth (ALD₁₀), Jorissen et al., 1995:

• Epifaunal/epiphytic: living above sediment - water interface (rocks, plants)
• Epi/shallow infaunal: 0-1.5 cm
• Intermediate infaunal: 1.5-5.0 cm
• Deep infaunal: 5-10 cm

• Low oxygen (difficult to separate high food and low oxygen effects)
• Opportunistic growing (high food -> early reproduction, rapidly varying circumstances)
• CaCO₃ corrosive

Just on faunas, not possible to decide which is most important factor in specific case

• Non-event at K/T boundary
• Extinction at P/E boundary
• Gradual turnover across oxygen isotopic events Eocene-Oligocene and middle Miocene
• ‘Stilostomella’ extinction (1.2-0.6 Ma; Mid Pleistocene revolution)

Note: diversity high globally in greenhouse world, drops, and diversity gradient may have been established at formation on Antarctic ice sheets (Thomas and Gooday, 1996; Thomas et al., 2000).  Various groups of common deep-sea benthic foraminifera (Epistominella exigua, indicator of fresh phytodetritus deposition; Nuttallides umbonifera, indicator of AABW) only became common at Eocene-Oligocene transition (establishment Antarctic ice cap.

• No ‘phytodetritus’ species (opportunistic, seasonal growth blooms)
• Unserial lagenids, stilostomellids, pleurostomellids (all long, then forms) buliminids-bolivinids common in open-ocean settings; ‘high food’ taxa in present oceans.
• Counterintuitive: at high temperatures, metabolic rates faster, equal food supply would mean more oligotrophic faunas
• Less common in open ocean species with complex apertures (linked to pseudopod shape and streaming behavior; feeding habits)

• Benthic faunas suggest high food supply
• Data from planktonic organisms suggest lower productivity
• More efficient transfer of food to sea floor? Different pattern of ocean  circulation - Hay’s eddies, rather than water masses?
• Different primary producers (e.g., more diatoms? More sticky mucus, thus faster transport?
• Lower oxygen, thus less organic matter degraded? (not very promising in few of data on present Mediterranean, Red Sea)
• Primary productivity on sea floor?

• Symbiontic chemosynthetic bacteria
• Present day cold seeps: benthic foraminiferal species that also occur elsewhere, bolivinids/buliminids (high food)
• Forams living as cold-seep clams do; at higher temperatures, bacteria higher metabolic rates thus higher productivity

WHY no serious consequences of collapse productivity’ on food-starved deep-sea biota, in presence of bentho-pelagic coupling?

• Less bentho-pelagic coupling:
• Different ocean circulation, different food transfer from surface to bottom
• More chemosynthetic productivity on sea floorSurface productivity did NOT collapse: blooms of different taxa

• ~ 30-50% species extinction; net deep-sea extinction similar globally
• Drop in diversity (but in many places affected by dissolution)
• Many cosmopolitan, large, heavily calcified species extinct.
• Post extinction species dominance patterns NOT the same globally: some places apparently more food, some places apparently less food
• Post extinction faunas dominated by small, thin-walled species

• Asphyxiation? (low oxygen). No independent evidence for global anoxia-hypoxia (e.g., high organic carbon, lamination), although in some places low oxygen conditions did prevail (e.g., middle East).
• Starvation? Eutrophication? It seems to be variable regionally; possibly more differences between highest and lowest productivity values.
• Dissolution? Organic-cemented, agglutinated foraminifera also show unusual faunal patterns (Glomospira-peak), and extinction also occurs at the few localities were dissolution is minor.
• Possibility: high global temperatures caused metabolic problems &endash; productivity problems; needs further investigation.

• Paleogene-Late Cretaceous community structure of benthic forams may reflect different structure of food supply to forams
• Possibility that transfer of food from surface to bottom was different (ocean circulation?); or different primary producers (diatoms?); or different seasonality (less)?
• Possibility of greater importance of chemosynthesis for food to forams
• Reorganization of faunas at cooling of deep oceans reflects establishment of present-day food supply structure -> more fresh phytodetritus to sea floor
• More reorganization in middle Miocene (more cooling, expansion polar ice sheets)
• Last, by then rare, taxa typical for earlier times extinct at Mid Pleistocene Revolution (Hayward, 2001)

• Size fraction studied (prefer > 63 mm)
• Water masses in the present oceans (temperature, salinity, oxygenation) are NOT determinants of faunas (some properties of water masses, e.g., current speed, may be)
• Foraminiferal paleobathymetry below shelf depth and without information on specific region is NOT accurate or precise
• Oxygen important ONLY if below values ~0.5-1.0 ml/L
• In most cases, interpretation of faunas not easy (unless one feature of environment dominates)
• Present not necessarily key to past