A wide benthic taxa for a wide range of niches

"The case of the three species of protozoan (I forget the names) which apparently select differently sized grains of sand, etc., is almost the most wonderful fact I ever heard of. One cannot believe that they have mental power enough to do so, and how any structure or kind of viscidity can lead to this result passes all understanding." Charles Darwin, letter to W.B.

Carpenter, 1872 (Darwin and Seward, 1903).

The first and the most obvious characteristic of benthic foraminifera is their high species richness. Estimations of modern species number range from 1’000 to 10’000 (Boltovskoy and Wright, 1976; Jones, 1994; Minelli, 1993; Murray, 2007; Vickerman, 1992).

Benthic foraminifera are not only rich in term of species number, but also amazingly diverse considering their morphology and ecology. Foraminifera are one of a few groups of protists with a size ranging from micrometers to centimeters and species scattered between microfauna and macrofauna. Micro- and nanoforaminifera have been reported in the smallest fraction of the sediment with some mature specimens smaller than 30 µm (Gooday, 1995;

Pawlowski et al., 1993). In contrast, some giant agglutinated species, like xenophyophores, can reach 25 cm in diameter (Tendal, 1990). The shape, the structure and the composition of the test also present huge variations. The acquisition of granuloreticulopodia in the early history of foraminifera must have largely participated in their diversification. Indeed, this new type of pseudopodia is likely to have enhanced their ability to manipulate particles and thus, to construct various types of tests (Travis and Bowser, 1991), providing efficient protection against predators and environmental conditions, as well as a compartment to store food and to protect juveniles (Lipps, 1983). The large radiation of early unilocular foraminifera revealed

by molecular study (Pawlowski et al., 2003), could directly result from the successful evolutionary pathway of the tested species. Each morphology has therefore to be regarded as an evolutionary response to an ecological niche and thus as a clue for biotic and abiotic pressures. In this perspective, some authors showed obvious relationships between foraminiferal morphologies and their way of life, their microhabitats or the nature of substrate they were living on (Corliss and Chen, 1988; Kitazato, 1988a, b). Since trophic pressures are obvious diversification driving forces, morphological richness could be overviewed through the different food resources exploited by each morphospecies. The wide variety of feeding behaviors well reflects the amazing richness of the phylum (Goldstein, 1999). Some of the large species occurring in the shallow reefs shelter photosynthetic symbionts within their hyaline test, which lets the light through. In some cases, symbionts only provide a small fraction of the energy input, as for Archaias angulatus and Sorites marginalis, which still get their main resource by feeding on unicellular algae (Lee and Bock, 1976). In other cases, symbionts provide their hosts with most of the organic carbon they require, as for Heterostegina genus (Röttger et al., 1980).

A clear relationship between the trophic behavior and the morphology of agglutinated foraminifera has been established by Jones and Charnock (1985), who distinguished four morphological groups corresponding to different feeding strategies: 1) the suspension feeders, fixed and standing up on the soil with branched or tubular shape; 2) the surface feeders, which can be grazers, detritivorous or omnivorous and which have globular or coiling shape; 3) the diggers, which are infaunal detritivorous or herbivorous, typically elongated or ribbed; 4) the herbivorous epiphytes, with biserial and trochospirally coiled shapes. Osmotrophy (assimilation of dissolved organic matter through cell surface) is a quite common feeding strategy among deep-sea foraminifera (DeLaca et al., 1981) and could reflect one of their ways to cope with oligotrophic environment (Lipps, 1982). Parasitism should also be mentioned as a possible trophic adaptation of benthic foraminifera. For instance, Hyrrokkin sarcophaga is a well known ectoparasite of bivalve and sponges (Cedhagen, 1994), while Fissurina marginata has been described as an ectoparasite of Discorbis vilardeboanus (Le Calvez, 1947) and Planorbulinopsis parasita was observed to live as an endoparasite inside the test of Alveolinella quoyi (Banner, 1971). Development of morphological features driven by trophic reasons is thus perfectly illustrated by the wide morphospecies richness of benthic

foraminifera, especially for the deep-sea species exposed to low or transient concentrations of nutrients.

In the same way, oxygen concentration in the water and in the sediment, which is closely linked to organic matter availability, may have impact on evolution of foraminifera.

The correlations between foraminiferal morphology and different oxygen supply, as well as species occurrence in particular oxycity, have been studied (Kaiho, 1994; Schönfeld, 2001).

Some calcareous species, notably within genus Bolivina, present thinner and less ornamented walls, enhancing oxygen penetration where the bottom-water oxygen is low (Douglas, 1979, 1981). In general, an increasing proportion of hyaline calcareous species compared to agglutinated taxa are observed at poorly oxygenated bottoms (Gooday et al., 2000; Levin et al., 2002).

Finally, this short and incomplete overview of relations between benthic foraminiferal morphologies and environmental conditions should also include investigations on hydrographic parameters. Correlation has been shown between composition and shape of agglutinated foraminiferal tests on the one hand and bottom currents and physical disturbances on the other hand. Tranquil environments would be dominated by finely agglutinated forms with delicate and branching tests, while disturbed areas with strong currents are inhabited by robust, coarse-grained and often infaunal species (Kaminski and Schröder, 1987). However, it is not clear if some of those morphological features result from the hydrographic conditions or rather from nutrients distribution patterns induced by hydrography.

The plasticity of benthic foraminiferal tests is a good reason to be extremely careful with species identification based only on morphology. It is not always possible to find a trait, which can be relevant regarding the origin of a species, and which does not result from homoplasy. Moreover, the ecophenotypic variations are so important in some taxa that it is difficult to define species boundaries. For that reason, alternative methods are required to complete the morphological approach of the diversity. Molecular tools can bring another piece of information likely to enhance the accuracy of an evolutionary scenario. The application of molecular analysis to assess the foraminiferal diversity is quite recent (Pawlowski et al., 1994) and based, until now, exclusively on nuclear ribosomal RNA genes (Pawlowski, 2000). Mitochondrial genes are not yet available for foraminifera (Pawlowski,

2009) and the only other coding genes so far investigated (actin, tubulin and ubiquitin) are too conserved for the species richness assessment (Flakowski et al., 2005). The rDNA has been chosen as a molecular marker of forams, as well as many other organisms for two main reasons. The first one is the high number of copies of rRNA genes, which facilitates amplifications by polymerase chain reaction (PCR) from a single cell. The second one is the different levels of variability offered by various regions of ribosomal genes. For instance, SSU alternates conserved and variable regions, while ITS is usually more variable. Most of molecular foraminiferal studies focus on the 3’ fragment of the SSU rDNA (Pawlowski, 2009). Indeed, this fragment provides on the one hand some regions, which are stable enough to design foraminifera-specific primers; and on the other hand variable regions, which enable distinction between species or even between populations. Since foraminiferal SSU provides both regions of high stability and variability, it offers a relevant set of molecular clues to investigate species history and their identification. In this respect, benthic foraminifera differ from many other eukaryotes with much slowly evolving SSU. However, it has to be noticed that foraminifera present sometimes high intraindividual polymorphism within their ribosomal genes copies. One single specimen can display a sequence divergence higher than 1% (Pawlowski, 2009), which complicates the determination of species-specific sequences (Holzmann and Pawlowski, 1996), and which seriously compromises population genetics studies applied to foraminifera. Nevertheless, rDNA-based phylogenetic analyses have shown, on several occasions, their efficiency to resolve cryptic species issue or, on the contrary, cases of overestimated diversity (Hayward et al., 2004; Holzmann and Pawlowski, 1997; Pawlowski et al., 1995; Tsuchiya et al., 2003). So far, molecular investigations converge to show that the species richness of benthic foraminifera, partially reflected by an already amazing wide set of morphologies, is still underestimated.