General

From Antiquity, and probably even before, foraminifera have attracted attention by their lenticular tests fossilized in the sediment. Herodote (V century before J. C.), Strabon and Pline the Older (both around J. C.) have reported numerous of those small eerie stones (tests of Nummulites) in the limestone of the Giza pyramids. Actually, they did not recognize their organic origin, which was established much later by Leonardo da Vinci (in the XV century) or by Agricola (in the XVI century). At the beginning of the XIX century, Alcide d’Orbigny proposed the first classification of Foraminifera, literally “hole bearer” (from Latin “foramen”

meaning hole and “ferre” meaning bearing) and included them among mollusks (d 'Orbigny, 1826). Nine years later, Dujardin (1835) showed that foraminifera were in fact single-cell organisms and placed them among amoeboid protozoa (Sarcodina). Several different classifications of foraminifera were established based on morphological characteristics (Cushman, 1928; Loeblich and Tappan, 1988; Neyumayr, 1887; Schubert, 1921; Schultze, 1854). One of the most recent ones distinguished 12 sub-orders and 2446 genera according to the composition and the structure of the test (Loeblich and Tappan, 1988). Several molecular phylogenetic studies demonstrate the inaccuracy of this taxonomy, but no new updated higher-level classification was published yet (Pawlowski 2009). Currently, foraminifera are placed in the supergroup of Rhizaria (Adl et al., 2005) based on phylogenomic data (Burki and Pawlowski 2006), but their relationships with other representatives of this supergroup remains controversial (Pawlowski and Burki 2009).

First fossilizable foraminifera, including multilocular agglutinated species, appeared around 520 Myr ago during Cambrian (Culver, 1991). However, the divergence of the foraminifera from their rhizarian ancestors have been estimated, based on local molecular clocks, to have occurred between 690 and 1’150 Myr (Pawlowski et al., 2003). Early non-fossilizable foraminifera (Monothalimida) were naked or presented organic or agglutinated test. The multilocular calcareous orders (Rotaliida and Miliolida) evolved about 350 Myr ago (Pawlowski et al., 2003).

Modern foraminifera are mainly marine although there are examples of fresh water (Holzmann and Pawlowski, 2002) and terrestrial (from damp rain forest soil) species (Meisterfeld et al., 2001). Around 40 planktonic morphospecies are described, but they may represent a much higher number of molecularly distinct entities (Kucera and Darling, 2002).

Benthic species are morphologically far more diverse (more than 4’900 described) but their richness is also largely underestimated, particularly that of monothalamous organic-walled species (Pawlowski et al., 2005).

Foraminifera are basically single-celled organisms characterized by a network of granuloreticulopodia. Some of the biological functions of the cell, as well as its interactions with the environment, are conducted by those anastomosing pseudopodia. They enable fixation to the substrate or locomotion; they are used for the feeding process allowing resources input and metabolic wastes output; they participate in particles transport for building the test; and finally, they are involved in reproduction, predation or simply interactions with other organisms. A dynamic system of microtubules ensures bidirectional movement of reticulopodia. The granules are moving inside and on the surface of the podia and mostly consist in mitochondria and various vesicles required for aerobic respiration and metabolic transportation (Sen Gupta, 1983). Benthic species living within the photic zone are mainly grazing on diatoms and other algae, while those below the photic zone feed on phytodetritus and bacteria. The food is captured by invagination of the pseudopodial membrane forming large digestive vacuoles. Those vacuoles are then transported through the pseudopodia to the intra test cytoplasm where the digestion occurred. Most foraminifera possess an outer protective layer which can be organic (mainly proteinaceous), agglutinated (with mineral particles embedded into an organic matrix or a calcareous cement), calcareous (composed of secreted calcite or aragonite crystals) or finally siliceous (a minority). Although the foraminiferal test has been extensively studied, its precise chemical composition and its detailed construction process remain poorly known. Depending on species and its environment, foraminiferal test can be extremely diverse. It is basically composed of single or interconnected multiple chambers and possesses generally one or several apertures. Naked foraminifera have simply developed a particularly thick layer of glycoproteins and polysaccharides to protect their cytoplasm. Foraminiferal growth and reproduction are not always well understood, especially for the deep-sea species. Some foraminifera possess a single and large nucleus (up to 100 µm in diameter) while others have hundreds or thousands

of small nuclei (less than 10 µm in diameter) distributed in the whole cytoplasm. The foraminiferal life-cycle is quite complex and consists schematically in an alternation of sexual and asexual generations. During sexual reproduction, uninucleate gamont produce amoeboid or flagellated gametes, which fuse to form zygotes, and become then diploid agamonts.

Nuclei of each mature agamont undergo two meiotic divisions, before its cytoplasm fissures and produces embryonic haploid gamonts. Foraminifera can follow three types of sexual reproduction: gametogamy, which takes place outside the test in the sea water; gamontogamy, which occurs by a direct contact between gamonts; and autogamy, which is a kind of autofertilization inside the test. Finally, this classical cycle can be sometimes modified.

Agamonts can undergo mitotic divisions instead of meiosis, and the asexual cycle can be repeated several times. Such complex life cycle can have consequences on the local gene flow, but nothing is known about this aspect.

Compared to other free-living protists, the phylum of Foraminifera has been extensively studied regarding morphology, ecology and evolution of its representatives.

Regrettably, scientists have not been attracted by foraminifera only because of the poetic shapes of their test or because their amazing diversity was offering multitude of opportunities to describe new species. Actually, foraminifera stir up interest in highly diverse fields of biogeosciences. First of all, the abundance, the diversity, and the continuity of foraminiferal fossils record, which counts about 50’000 species described (Debenay and Pawlowski, 1996), make them the most important proxies for paleoceanographic studies. Isotopic and chemical composition of their tests as well as their species assemblage can reflect the age of sedimentary strata and bring precious information on past environmental parameters such as temperature, oxygen concentration or primary productivity. Those inferences are based on observations of living foraminifera at different spatial scales: from microhabitats to regional patterns (Gooday, 2003). Concerning benthic species, special efforts have been devoted to relate organic carbon fluxes to the composition of foraminiferal assemblages (Wefer et al., 1999; Weinelt et al., 2001). Total foraminiferal standing stocks are considered as good indicators of food availability (Douglas, 1981; Phelger, 1976), while particular species would tend to be associated with certain levels of carbon flux (Altenbach et al., 1999; Fontanier et al., 2002). Then, foraminifera are also recognized for their economic importance in the petroleum industry, which largely rely on microfossils to find potential oil deposits (Broadman et al., 1987).

Benthic foraminiferal assemblages are also of great interest for marine ecology.

Because they are ubiquitous, small and numerous enough to be statistically analysed, they represent excellent bioindicators (Kramer and Botterweg, 1991). For instance, larger symbionts-bearing species can attest of coral reefs health (Hallock, 2000). Shallow water foraminifera have been extensively studied for pollution assessment (Scott et al., 2001; Yanko et al., 1999). Numerous investigations showed they were extremely sensitive to a wide range of pollutants as domestic and agricultural wastes, trace metals or oil spill (Alve, 1995;

Armynot du Châtelet et al., 2004; Buckley et al., 1974; Ellison et al., 1986; Frontalini and Coccioni, 2008). Scientists recommend their general use for environmental monitoring (Debenay et al., 2000).