Ann Vanreusel; Annelies De Groote; Sabine Gollner; Monika Bright

“ Three possible reasons for the low nematode densities at vents are put forward: (1) The substrate is unsuitable for supporting high abundances. Vents consist of recently formed hard substrates, such as basalt or sulphide minerals precipitates, with no or little sediment covering the hard substrate. Vent fluid reaches the water column through sulphide chimneys or crack and crevices of basalt, on which large foundation species, such as bivalves and tubeworms, grow. Most hydrothermal vents provide living space for meiofauna only on these hard substrates, or on the associated foundation species. ”

“ Most seeps show taxonomically very different dominant species and genera, even at geographically adjacent sites (Nordic Margin) (Table 2) . Striking is that many of the seep-dominant species (or at least morphologically similar species) are known from shallow water environments. Halomonhystera disjuncta for instance, the dominant species at the Barents sea slope, is a cosmopolitan, bacterivorous species known for its high resistance to environmental stress, especially to heavy metals [66] . ”

“ The similarity in nematode genus composition between vent ecosystems and control sites, stands in clear contrast with the presence of a specialized endemic hydrothermal megafauna. There is no specially adapated nematode fauna observed at vents so far. No symbionts are found, while the dominant vent genera are also present in the regular deep-sea sediments. The ephemeral nature of vents, in combination with their strongly isolated nature, possibly does not allow for the evolution and distribution of specially adapted forms, like in the macro- or megabenthic size class. ”

“ Interestingly, genera richness at vents is significantly lower than at seeps (Table 6) . Possibly the extremely low genera richness at vents is explained by the fact that vents are more disturbed and stressed. Indeed, species present at deep-sea hydrothermal vents have to deal with volcanic eruptions, waxing and waning of vents and associated fluctuations of physico-chemical conditions (temperature, sulphide, oxygen, and pH) in relatively short time scales [3] . ”

“ Vents seem not characterized by elevated densities. Both chemosynthetic driven ecosystems are showing low nematode diversity, and high dominance of single species. Genera richness seems inversely correlated to vent and seep fluid emissions, associated with distinct habitat types. Deep-sea cold seeps and hydrothermal vents are, however, highly dissimilar in terms of community composition and dominant taxa. There is no unique affinity of particular nematode taxa with seeps or vents. ”

“ Nematode diversity at seeps and vents
Local diversity of the benthos is in general relatively high in deep-sea sediments, with low dominance and a high number of species co-existing on the same spot [60] , [61] . For nematodes it is not different: the most abundant or dominant genera, like Acantholiamus, Thalassomonhystera, Microlaimus or Leptolaimus, represent the communities for less than 20% in general, and contain many con-generic species [2] . Local species numbers can reach values higher than 100, whereas species richness often increases with densities [62] – [63] . ”

“ Except for the dominance of a Sabatieria species and a monhysterid in two shallow seep studies, there is no further similarity in nematode fauna from shallow and deep waters.
Shallow vents are, similar to deep-water vents, characterized by low densities (often <100 ind. 10 cm−2) , with values ranging from 1 to 1075 ind. 10 cm−2 [25] – [26] . There is no major nematode genus similarity between shallow and deep-water vents. Also studies on macro- and megafauna showed that the dominating fauna from shallow-water vents are different from those found at deep-sea vents [118] . ”

“ Since several species are present at seeps, it is likely that the higher food input results in a competitive advantage of fast growing species that are blooming, whereas others with slower growth remain at constant low levels.
Vents are also characterized by low diverse and uneven nematode communities (S: 7±3; J′: 0.6±0.2; H′loge: 1.0±0.6) (data from [20] , [54] – [30] ) . Interestingly, vents show a clear pattern of genera richness and diversity inverse correlated to stress (vent fluid emissions) . ”

“ However, also the presence of other benthic taxa may interfer with the nematode success. In addition to nematodes, polychaetes of sulphide tolerant families, such as Capitellidae, Spionidae and Dorvilleidae, may thrive in the same seep conditions [4] , and may compete with them for food, space or oxygen, or act as potential predators. Two studies indicate a significant negative correlation between meio- and macrofauna densities in sulphidic sediments from a whale fall [22] or at the seeps along the Nordic margin [41] .
Increased standing stock is not only explained by increased densities. ”

“ Seep sediments are often dominated by a single species, representing 50 to 90% of the total community. However, the number of other nematode taxa still can be relatively high at seeps, but each of these taxa are represented by only a few individuals per 10 cm2. Only Siboglinid fields are an exception, with the dominant genus being represented by only 12 to 49%. Interestingly, lowest evenness and lowest diversity are detected in bacterial mats (mean J′: 0.02; H′loge: 0.03) . In this habitat the oxygen layer was only 1 mm thin, and total sulphide concentrations were up to 1 mMol. ”

“ Nematode genera from deep-sea hydrothermal vents and cold seeps have not developed any obvious adaptations, but they must have certain tolerance for sulphidic and/or anoxic conditions. For example, the Halomonhystera disjuncta species is thriving up to 5 cm depth in the sulphidic sediments of the Beggiatoa mats, but no evidence of detoxification mechanisms such as sulphur inclusions were found. ”

“ Deep-sea hydrothermal vent or cold seeps communities appear to have no strong or exclusive affinity to other communities from sulphidic environments, such as the “thiobios” of sulphidic sediments, shallow-water vents, or cold seeps, despite the presence of reducing chemicals and hypoxia. Some thiobiotic genera, like Sabatieria and Terschellingia are shared, but not any of the known chemosynthetic nematode species with symbionts was found so far in deep-sea vents or seeps
The knowledge we have to day on deep-water seep and vent meiofauna is only a tip of the iceberg. ”

“ Ovoviviparity is only known for a few marine nematode species. Permanent sulphidic sediments, in combination with anoxia at HMMV, create harsh conditions, which suggests that internal development of juveniles is an adaptation for securing the survival and growth of the vulnerable brood. Since brooding behaviour requires a substantial parental energy investment, it must provide strong benefits. ”

“ This apparently different physical nature of both chemosynthetic ecosystems is therefore likely to explain lower genera richness at vents. Other possible reasons are that the coexistence of nematodes, with various other, highly abundant epifaunal organisms at vents, might result in competitive exclusion, and could explain low eveness of single nematode species, in association with low densities. ”

“ Remarkable exceptions on these general trends of high local diversity and low density and biomass are ecosystems, known as hydrothermal vents [3] , and cold seeps [4] . These systems are largely driven by chemosynthetic derived energy, and not directly dependent on photosynthesis. They appear locally on active or passive margins in the case of cold seeps, or mid-ocean ridges and back-arc basins in the case of hydrothermal vents [3] – [5] . ”

“ At vents, nematode densities and biomass are always low. It is likely that the presence of hard or soft substrates, the latter being more favourable for nematodes, is reponsible for the differential response between seeps and vents. Competition for food- or space with macro- or megafauna, or even the meiofauna such as copepods is possibly an additional factor responsible for the high variation at seeps and the lower numbers at vents, although evidence is lacking so far. ”

“ In addition, members of Chromadorida, Metoncholaimus, and Paracyatholaimus were only found on bare basalt but not at vents. Control sediment samples cluster relatively close to the seep infauna samples (R = 0.23; p = 0.001) , but also have a a high dissimilarity (78%) . Genera causing the dissimilarity, were present in unequal densities in control and seep samples, with Halomonhystera and Microlaimus contributing with 5% each highest to the dissimilarity. This might point to the importance of substrate type (hard substrates at vents versus sediments in seeps) to nematode communities. ”

“ However the exact mechanisms of adaptation of Terschellingia or Sabatieria species to the sulphidic or oxic environment remains unclear. Some authors pointed to the presence of dark, often multilayered intracellular globules in the intestinal cells of nematode species typical for sulphidic muds (i.e. Sabatieria wieseri, Terschellingia longicaudata, Sphaerolaimus papillatus, Siphonolaimus ewensis, Pontonema vulgare) . ”

“ Understanding the high capacity of nematodes to thrive in anoxic and/or sulphidic conditions may open a window to understand life in even more extreme conditions in past and future. The threat of large scale anoxia and ocean acidification through global warming urge the needs for identification of adaptational processes through micro-evolution and speciation on a relatively short time scale, for which vents and seeps can act as natural experiments. ”

“ The vigorous diffuse flow at the Siboglinid habitat (max. 32–54°C; max. 283 μM sulphide; min pH 4.4) shows very low diversity (S: 2±1; H′loge: 0.3±0.2) . Bivalves with moderate diffuse flow (e.g. ∼8°C; ∼150 μM sulphide; ∼pH 6.7) are characterized by higher diversity (S: 9±2; H′loge of 0.6±0.2) (Tables 5 and 6) . Only evenness is similar (both J′: 0.6) in tube worm and bivalve habitats. Similar to seeps, often a single species highly dominates the vent community. On average, the dominance of a single species is 66%, but is ranging from 15 to 100%. ”

“ At seeps, analyses of the fatty acids and stable isotopic signatures of the Halomonhystera species from HMMV [113] indicate that this species thrives on chemosynthetically derived carbon, as provided by the free-living sulphide-oxidizing bacteria. The digestive tract is fully developed in this monhysterid species, and there is no evidence for endo- or ectosymbionts as based on SEM or TEM observations. Also at vents, the large majority of nematodes are deposit feeders [30] , however biomarker analysis are lacking so far. ”

“ However, if further molecular evidence confirms this connection, the exchange between the deep sea and the shallow water seems to have taken place several times since different shallow water taxa colonized geographically separated seeps. Vent communities are often dominated by Thalassomonhystera, a typical deep-sea genus. At vents the taxonomic simmilarity with adjacent regular deep-sea sediments is much higher, supporting rather the importance of local adaptation than that of long distance distribution. ”

“ In contrast to seeps, deep-water hydrothermal vents in general do not show high nematode densities or biomass. The communities are often impoverished or show similar densities compared to their adjacent background habitats [20] – [30] , [21] (Table 1 and 3) . In bacterial mats 1–78 ind. 10 cm−2 [27] occurred, and on bivalves also only 1 to 72 ind.10 cm−2 were found [20] , [52] , [53] , [30] . The tube worm habitat showed a high variation from very low nematode densities (1 ind. 10 cm−2) to higher values of about 900 ind. ”

“ The general observation of low nematode densities at vents so far, is rather striking and at first sight controversial: energy and space are copious and plentious in a harsh, although inhabitable biochemical environment. ”

“ They are considered as important indicators of habitat heterogeneity in marine environments, including the deep sea, since they are common, numerous and speciose, and in close contact with seafloor related processes [2] . Despite their numerical importance, still little is known on their ecology and distribution in the deep sea, especially in association with seeps and vents. ”

“ There is a strong need for more ecological, biogeographical and taxonomical research, using biomarker, molecular, physiological, and (ultra) morphological analysis, in order to understand their trophic position and importance, their origin and distribution and their adaptation. More specific the following aspects should be prioritized for future reseach on vents and seeps: (1) We can only speculate so far on the connectivity between isolated seeps and vents and the dispersal mechanisms for nematodes. ”

“ Nematodes are rather tolerant to anoxia, but they do not survive long-term exposure [49] . As nematodes respire aerobically, they cannot be permanent resident in anoxic sediments and, to avoid damaging conditions associated with long-term exposure to anoxia, they need the capacity to move away [46] , [50] , [51] . ”

“ Like H. disjuncta, T. longicaudata has an extensive geographical range including estuarine sediments off the North Sea [66] , [67] , [71] , mangrove mudflats off northeastern Australia [72] – [73] , the southeast coast of India [74] , off the Atlantic coast of France, in the Black Sea [75] and the Gulf of Mexico, off eastern China (Qingdao province [76] ) as well as New Zealand and the Solomon Islands [77] . In [78] a broad ecological and geographic range is suggested based on molecular evidence. ”