Patchiness and transience of resources: ephemeral benthic oases

Considering deep-sea ecosystems in an overall view, it is obviously valuable to ask what could be the factors driving the richness and the diversity of the deep-sea benthos. More precisely, the distribution of energy resources over space and time should now be considered.

Ocean floor could be chiefly depicted as a wide place with extremely stable conditions (the abyssal plains) delimited by a remarkably heterogenous and disturbed zone (the continental margins). On the scale of the vast seabed, natural resources and populations of abyssal plains are extremely patchy and appear as minute and heterogeneous points. As it has been described previously, geological activity as well as sedimentation can induce this pattern of patchiness occurring at different scales. At large scale, it is quite clear that hydrothermal vents, cold seeps and whale falls provide occasionally great amount of food resources attracting and nurturing many organisms of wide size ranges. However, those spots remain rare considering the global surface of the oceanic bottoms and the effective patchiness of the deep sea has to be searched within smaller features. At medium scale, an important contribution of the floors heterogeneity consists in living organisms themselves. Biogenic structures have been found to enhance biological activity in their proximity by providing numerous goods and services like resources and advantageous structures. For instance, deep-sea corals have been recognised, in some area, to shelter large benthic communities (Krieger and Wing, 2002; Malakoff, 2003). Nematodes, polychaetes, crustaceans and bryozoans associated with large agglutinated foraminifera also illustrate, at smaller scale, the high epibiotic diversity found on the oceans floor (Gooday, 1984a, b). Habitat partitioning induced by such organisms seems to be of the most relevance in this global context of low biomass (Jumars and Eckman, 1983). Since there are few organisms, these advantageous biotic structures remain rare and thus intensively occupied. Passive deposition of larvae, depending on the sediment microtopography and hydrodynamic conditions, could also explain this patchy distribution (Butman, 1987). Finally, at small scale, fine particles and amorphous aggregates, which have reached the bottom, can attract microorganism communities and provoke patchiness. There are two different contributions to the particulate organic matter (POM): suspended particles and sinking particles (Karl et al., 1988). POM and flocculent material as gelatinous bodies forming the marine snow has been found to be hotspots of diversity for microplanktonic populations (Alldredge and Silver, 1984; Silver et al., 1978;

Simon et al., 2002). In the benthic meio- and microfaunal ecosystems, this organic input should have similar function, whenever particles are big enough to reach the bottom and if they are of nutritional interest compared to the surroundings. In the water column, aggregates of various sizes have been reported not only to concentrate individuals but also to differ in species composition from those of the ambient water (Crump et al., 1999; DeLong et al., 1993). It is sometimes difficult to detect, isolate and study such aggregates on the ocean floor but they should also be likely to present differences in species composition compared to the neighborhood. Spatial distribution of life in deep-sea bottoms consists thus in narrow hotspots of alternative diversity and huge concentration gradients. Gradients of biotic concentrations occurring on the seafloor are, by far, greater than those existing in terrestrial ecosystems. For instance, density of organisms in hydrothermal vent zones can be 10,000 to 100,000 times higher than in the surroundings (Juniper et al., 1998). Transition zones between deep-sea ecosystems seem highly reduced whereas, on land, environment has a quite continuous pattern considering specimens and species occurrence. This might be explained by a lower global food availability inducing a lower global biomass, which concentrates only where amounts of food are maximum (Grassle, 1991; Grassle and Maciolek, 1992). Moreover, there are evidences that geographically close areas could present large differences not only in abundance but also in species number and composition (Jumars, 1976; Jumars and Hessler, 1976). There are thus apparent barriers to genetic flows between ecosystems, which, in the deep sea, almost come down to barriers between resources hotspots. However, it remains unclear to what extent physical features (as topography or currents) and biological restrictions (as oxygen or food deprivation) consist in real enclosures separating populations. In some cases, the reason of a limited gene flow between populations have been clearly identified, as for the vent-endemic mussels of the genus Bathymodiolus separated by deep-sea currents (Won et al., 2003). It is also likely that the species richness of a given hotspot would be determined mainly by the occurrence of specimens (if they are close to the spot or not) and by the specific colonization ability of species. Therefore, it is absolutely necessary to investigate how those patchy ecosystems evolve with time.

Since food resources are major factors shaping the deep-sea ecosystems, the duration has to be taken into account. Large organic pieces settling to the floor and geological special features are typically spontaneous events, which often appear instantaneously where there was nothing just before. After reaching one of those new islands, an organism should still colonize

it, which implies staying and eventually reproducing. The future of a newly arrived population depends directly on the durability of the providential oasis. Typical duration of hydrothermal vents is a couple of years (Grassle, 1985), while that of cold seeps is over million years (Olu et al., 1996). Interesting correlations between organisms life span and their habitat duration time have been reported and could result from colonization strategies. For instance, the tube worm Lamellibrachia luymesi living in cold seeps has the life span record, for a deep-sea non colonial invertebrate, of 250 years during which it will slowly grow up to two meters (Bergquist et al., 2000). At the opposite, Riftia pachyptila is able to colonize a new hydrothermal vent, reach sexual maturity and a size of 1.5 m, in less than two years (Govenar et al., 2004). Deep-sea corals, which are suspension feeders and can maintain their colonies over 4000 years, represent another exception among the short living habitats of the bottoms.

However, they seem to occur only in zones of constant particulate flux or on seamounts (Roark et al., 2009). Those deep reefs (which can cover enormous areas) as well as the cold seeps represent fundamentally atypical ecosystems of the oceans floor. Indeed, they should be the place of positive or negative natural selection, since they are long lasting and supposedly stable enough for competition to occur. Therefore, they may have a crucial function in the global diversification processes of the deep sea. Coral reefs, vents, seeps or carcasses are, by far, less numerous than microhotspots constituted by smallest biogenic structures, organic aggregates or particulate food. A special attention must thus be paid to the food supply of smallest size, which probably rules general patterns of deep-sea diversity. As for the larger inputs, the occurrence of these modest nutrient sources on the sediment floor is largely spontaneous and ephemeral. At regional scale, emergence of benthic microhotspots can nevertheless follow the seasonality of surface waters or land (Ittekkot et al., 1984). For instance, episodic blooms of phytoplankton can provoke regular episodes of faecal pellets and moults fall (Thiel et al., 1989). In the same way, downslope currents, associated with intense cascading events, bring nutritive particles to the bottom, depending on terrestrial climatic conditions, which can be cyclic (O'Connell et al., 1985). Evidences of seasonal response among deep-sea benthic species are also reported. Concerning the meiofauna, it is interesting to notice some clues of seasonal reproduction cycles (Kitazato et al., 2000; Tyler, 1988), as well as short response to the arrival of phytodetritus on the sea bottom (Bahls et al., 2004;

Gooday, 2002a; Gooday and Turley, 1990). The seasonality brings the issue of the predictability for the food pulses with the question whether the deep-sea benthos can predict such events. However, the huge water column, which separates the benthos from the food

production zones and which is often disturbed by currents, scatters hotspots on the deep-sea floor and make their occurrence largely unpredictable over space and time. The duration of those minute but common spots is quite short: for most of them, it takes from weeks to months to be drained out their nutritive substance. It has even been shown that bodies of coccolithophorids and macroaggregates of phytodetritus are completely decomposed at the sediment surface within one year (Cole et al., 1987; Gardner et al., 1983). Most ecosystems of the oceans floor appear and disappear with an erratic cadence and have typically shorter life than organisms themselves. Those need thus to cope with fugitive food resources. During the rare opulent periods, energy input into their metabolism has to be maximized, either to be stocked in prevision of scarcity, or to be used immediately for vital processes as growth and reproduction. It is likely that a great part of the deep-sea benthos alternates vegetative periods and short moment of enhanced metabolism. To be able to use a great amount of resources in a short time, many sessile organisms have turn into opportunist feeding behavior by moving from microphagous suspension feeders to macrophagous predators (Gage and Tyler, 1991).

The fast and episodic growth observed in xenophyophores (Gooday et al., 1993) could also indicate an evolutionary response to the transitory food pulses from the water column.

Bioturbation is another reason why benthic microhabitats briefly evolve and disappear. On its uppermost layer, the deep-sea floor is disturbed by organisms which mix, dig or displace the sediment. Although fauna is sparser in the oceans bottom than in shallow areas, deep-sea bioturbation and its consequences on ecosystems should not be overlooked. Firstly, because deposit feeders must ingest greater quantities of sediment, since the bottom is poor in nutritious organic compounds (Deming and Colwell, 1982; Smith et al., 1986). Secondly, because any slight perturbation of the soil deeply affects the topology of meio- and microfaunal habitats (Meadows and Tufail, 1986). From the smallest organisms’ point of view, environment should be so often disturbed that competition between species should rarely have time to occur. A successful strategy to cope with the transience of resources could thus simply consist in arriving among the firsts at the hotspot and developing as fast as possible. Consequently, benthic communities flourishing on the oceans floor should count many “efficient colonizators”. In the megafauna, echinoderms represent a group particularly fit to rapidly colonize newly available niches or, as in the deep-sea, new hotspot of food resources. Aggregations of sea urchins Echinus affinis have been observed around short-lived patches of phytodetritus (Billett et al., 1983) and spectacular “herds” of holothurians Kolga hyalina have also been reported on phytodetrital hotspots (Billett and Hansen, 1982). In both

examples, many specimens from a single species are found to thrive on the ephemeral “open buffet service”. Most of the food resource will probably disappear before other species succeed to colonize the same hotspot, which induces a local low richness. If one of those providential islands would have sustained echinoderms life longer, other species would have had opportunity to colonize it. In the very next step, competition for colonization would have occurred and the local richness would have increased until being proportional to the richness of immigrants. Main part of the diversity found in deep-sea hotspots should thus result from immigration. Extend the durability of a hotspot should have similar consequences on local diversity as an increase in immigration rate. Depending on organisms and on their dispersal ability, a given hotspot should be considered as a young or an old ecosystem with low or high richness respectively. Microorganisms like viruses, bacteria and protists should also possess great skills for colonization, since they have high potential of dispersal, and since they reproduce faster than bigger organisms. Interestingly, microbes represent the greatest proportion of the deep-sea benthic biomass and process the main part of the carbon cycle (Danovaro et al., 2008a). Could the deep-sea taxonomic structure, where species of high dispersal potential prevail, reflect the instability of its ecosystems?

Following the resources availabilities, most of ecosystems from the ocean floor are patchy and transient. Intuitively, the benthic hotspots could be thought to offer a low local species richness. However, their distribution over space and time could also induce evolutionary responses drastically different between taxa.