The typical deep-sea citizens

As we have seen before, foraminifera form a large phylum and can be found in all marine habitats that have been studied, no matter the depth (Todo et al., 2005) or the latitude (Bergsten, 1994; Brandt et al., 2007). Benthic species seem to be especially successful in the deep-sea where they can reach, in some areas, more than 50% of biomass (Gooday et al., 1992; Snider et al., 1984). Abundance of calcareous taxa appears to decrease with depth beyond the shelf break (Hughes et al., 2000; Kurbjeweit et al., 2000). Below the carbonate compensation depth (CCD), organic walled and agglutinated species dominate the benthic foraminiferal assemblage. They play a main role in the carbon cycle (Kitazato et al., 2000;

Moodley et al., 2000) and occupy a central position in the deep-sea bottom ecosystems (Sen Gupta, 1999). Finally, with their wide variety of ecological niches, benthic foraminifera encompass all the different “deep-sea ways of life” and appear to be particularly suitable for studying the dispersal ability and subsistence under food restrictions.

Feeding strategies of deep-sea foraminifera can be considered as different ways to cope with patchy and ephemeral resources. There are two general and basically opposite trends in their feeding behaviour: specialization and opportunism. Particular species tend to be associated with either higher or lower levels of organic fluxes (Altenbach et al., 1999;

Fontanier et al., 2002; Gooday, 2003). This could suggest that, under strong food limitation or stable conditions, competition occur and specialized species dominate. Some cases of such highly specialized foraminifera; as those shaped to perform suspension feeding or osmotrophy; have already been evocated in the previous section. Many of those specialized species are monothalamous agglutinated forms that present fragile tests of sometimes unusual shapes. They have been preferentially observed in places of constant and limited organic fluxes where environmental conditions were stable (Gooday, 2003). On the contrary, other foraminiferal species seem to dominate when food become suddenly abundant, possibly because they are extremely fast to exploit the resources and develop rapidly on the eutrophic spots. This hypothesis would be congruent with the observations of species dominance shift during seasonal nutrient inputs (Bahls et al., 2004; Gooday, 2002a; Gooday and Lambshead, 1989), sometimes coupled with reproduction events (Kitazato et al., 2000; Ohga and Kitazato, 2003). Generally, occurrence of hyaline calcareous rotaliid foraminifera can be more strongly correlated with the organic matter than that of agglutinated taxa (Gooday et al., 2008;

Gooday, 2003). Moreover, Betram and Cowen reported, during artificial substrates colonization experiments, that the settlement rate of agglutinated species was uniform over time, whereas calcareous ones presented higher rates during periods of enhanced particles flux (Bertram and Cowen, 1999). Since some opportunist species show a greater response to food input, it could be thought that their selection would have occurred mainly through food type rather than through habitats. Some authors emphasized the important issue of different food preferences for deep-sea benthic foraminifera (Kitazato et al., 2003; Nomaki et al., 2005a;

Nomaki et al., 2005b). It would actually concern the decomposition state of nutrients that have sunk to the sea floor rather than their precise nature or composition. Indeed, among calcareous taxa, some species seem to prefer degraded and labile phytodetritus, while others appear associated with more refractory material (Caralp, 1989; Fontanier et al., 2002). If these observations would reflect a general trend of opportunist species, it would have radical consequences on their dispersion. According to some studies in Eastern Pacific Ocean, calcareous species distribution patterns are dominated by a response to surface ocean productivity (Loubere, 1996; Loubere and Fariduddin, 1999). Since degradation level of nutrients depends largely on the depth rather than on the geographic position, those opportunist species could be rightfully expected to have bathymetrically restricted broad geographic ranges.

Still in order to hunt for possible clues of benthic foraminiferal adaptation to the deep-sea environment, their dispersal ability should be considered. Using once more the simplistic distinction between opportunist and specialized species, it could be proposed that the two kinds have different trends in dispersal ability. Since opportunist species have greater skills for colonization of newly formed food sources, they should also be particularly efficient to reach those spots and thus, should tend to be highly dispersed. One active and three passive ways of dispersal have been recognized in foraminifera (Alve, 1999; Murray, 2006). The active dispersal, occurring via self-locomotion, is unlikely to have much impact at largest scales. By contrast, benthic foraminifera can be passively dispersed by getting into suspension in the water column and being transported, potentially over long distances. This dispersal mode can apply to the first stages of development (gametes, zygotes, propagules or juveniles), to species having temporary planktonic phase, or even to the small-size adult forms. Passive dispersal of benthic foraminifera can occur by water masses displacement (with currents for instance), by sediment displacement (with canyons avalanches), or with biotic activities (as

for parasitic or epibotic species). Because reproduction and development cycles of deep-sea foraminifera are still largely unknown, their respective contribution to dispersal potential remain purely speculative. Nevertheless, even if gametes and zygotes may not survive over a long periods of transport (Murray, 2006), propagules could tolerate greater distances (Alve and Goldstein, 2002, 2003). Those hypotheses are extremely difficult to test in the deep sea by in situ experiences. It is thus essential to seek an accurate way to assess somehow the general trends of foraminiferal dispersal ability. The most obvious way to enquire this feature could consist in observing their distribution at large scale.

A significant part of the research on foraminiferal biogeography was done by John W.

Murray, who recognized four main factors, which could be correlated with the distribution of modern benthic foraminifera: food availability, oxygen concentration, depths and currents (Murray, 1991). After a large revue of species occurrences in the different oceans of the world, it appeared that more than a half of the 938 common morphospecies studied was restricted to one of ten biogeographic regions. Seven species were found in eight regions or more, and three of them (Epistominella exigua, Cibicides wuellerstorfi and Globocassidulina subglobosa) occurred in nine of the ten investigated areas. According to Murray’s data, most of the benthic foraminifera would thus have restricted biogeography, which would conflict with the idea of great dispersal ability. However, the three species having the wider distribution are characteristic of bathyal and abyssal environment. This might reflect a stronger trend to ubiquity in the deep sea.

Moreover, sampling efforts, especially in the deep sea, probably do not reflect accurately the presence/absence of species. At regional scale, the surface of the collected sediment represents such a small proportion of regional total surface that numerous rare species could easily be missed by erratic sampling. Additionally, the foraminiferal diversity is highly variable at micro and mesoscale (Semeniuk, 2000) and could create considerable bias in a poor sampling (Soetaert and Heip, 1990). Even in the ideal case, where a sampling would perfectly reflect the distribution at the particular time of collecting, it would not mean that the lacking species do not have the ability to occur there. Indeed, ecologists conceptually separate the “fundamental” niche, where a species could potentially exist, from the “realized” niche, where the species really does exist (Hutchinson, 1957). It can be, for instance, that a particular species temporally disappears from a location which however suites it, because it is excluded

by other species through competition for food. During days, months or years, no representatives of this species would physically occupy the region until competitive pressure would disappear. For that reason, species occurrence remains poorly informative considering their dispersal potential. It has been suggested that ubiquitous morphospecies may not consist in a single entity but would rather represent a cluster of distinct species sharing the same morphology (Haynes, 1992). Molecular studies confirm this suggestion, identifying large number of cryptic species in shallow water foraminifera (Pawlowski and Holzmann, 2008), but nothing was known about the genetics of deep-sea species before this work started.

Searching for dispersal clues among benthic foraminifera appears finally as a quite risky investigation based mainly or only on distribution studies. Unfortunately, distribution assessment depends highly on sampling, which is obviously too poor to be relevant for deep- sea foraminifera. It is virtually impossible to demonstrate that a particular species does not occur in a particular region. However, if widely dispersed or ubiquitous species actually exist, it should not be a task out of reach to find one of them. Therefore, searching for cosmopolite species rather than for biogeography pattern could be a more relevant strategy to begin with.

Benthic foraminifera offer not only an amazing species richness to explore but also taxa of fundamentally different evolutionary paths. If there are some specific patterns of speciation in the oceans floor, they should be found among foraminiferal species. For that reason, biologists should pay a very special attention to those typical deep-sea citizens.

Indeed, identify the foraminiferal evolutionary response to the patchiness and transience of food could highly contribute to understand general biodiversification processes in the deep sea.