22 Jan 2014: Gollner S, Ivanenko VN, Arbizu PM, Bright M (2014) Correction: Advances in Taxonomy, Ecology, and Biogeography of Dirivultidae (Copepoda) Associated with Chemosynthetic Environments in the Deep Sea. PLOS ONE 9(1): 10.1371/annotation/d2c17821-286d-4a63-a6ae-348a456d9d0c. https://doi.org/10.1371/annotation/d2c17821-286d-4a63-a6ae-348a456d9d0c View correction
Copepoda is one of the most prominent higher taxa with almost 80 described species at deep-sea hydrothermal vents. The unique copepod family Dirivultidae with currently 50 described species is the most species rich invertebrate family at hydrothermal vents.
We reviewed the literature of Dirivultidae and provide a complete key to species, and map geographical and habitat specific distribution. In addition we discuss the ecology and origin of this family.
Dirivultidae are only present at deep-sea hydrothermal vents and along the axial summit trough of midocean ridges, with the exception of Dirivultus dentaneus found associated with Lamellibrachia species at 1125 m depth off southern California. To our current knowledge Dirivultidae are unknown from shallow-water vents, seeps, whale falls, and wood falls. They are a prominent part of all communities at vents and in certain habitat types (like sulfide chimneys colonized by pompei worms) they are the most abundant animals. They are free-living on hard substrate, mostly found in aggregations of various foundation species (e.g. alvinellids, vestimentiferans, and bivalves). Most dirivultid species colonize more than one habitat type. Dirivultids have a world-wide distribution, but most genera and species are endemic to a single biogeographic region. Their origin is unclear yet, but immigration from other deep-sea chemosynthetic habitats (stepping stone hypothesis) or from the deep-sea sediments seems unlikely, since Dirivultidae are unknown from these environments. Dirivultidae is the most species rich family and thus can be considered the most successful taxon at deep-sea vents.
Citation: Gollner S, Ivanenko VN, Arbizu PM, Bright M (2010) Advances in Taxonomy, Ecology, and Biogeography of Dirivultidae (Copepoda) Associated with Chemosynthetic Environments in the Deep Sea. PLoS ONE5(8): e9801. https://doi.org/10.1371/journal.pone.0009801
Editor: Anna Stepanova, Paleontological Institute, Russian Federation
Received: October 23, 2009; Accepted: February 1, 2010; Published: August 31, 2010
Copyright: © 2010 Gollner et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This work was supported by the Austrian Science Foundation grant FWF (P20190-B17 to MB), by ChEss (mini-grant to SG), and Census of Diversity of Abyssal Marine Life grant and the Russian Foundation for Basic Research Grant (09-04-01523-а) to VNI. ChEss was covering the publishing costs. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Copepoda are estimated to contribute more than 15% to the total number of animal species known from deep-sea hydrothermal vents worldwide . Almost 80 species are currently described from the orders Harpacticoida, Calanoida, Cyclopoida, Poecilostomatoida and Siphonostomatoida, but many more species await identification and description . The Dirivultidae, a family belonging to the Siphonostomatoida, is the most diverse one of all animal families at vents with 13 genera including 50 described species. The most diverse genus is Stygiopontius with 21 species. Similar diverse faunal groups at deep-sea hydrothermal vents are Gastropoda with about 100 described species, including the prominent family Lepetodrilidae with 20 species and within this family the large genus Lepetodrilus (13 known species). Polychaeta are also represented with currently 111 species and the Polynoidae including 24 species .
In hard substrate ecosystems like many hydrothermal vents, copepods can be the most abundant and diverse meiofaunal taxon , . Copepods in general play an important role in various ecosystems, being usually the second dominant higher meiofauna taxon following the nematodes . They are known from marine and freshwater plankton, marine sediments, cryptic habitats (soil, forest litter, terrestrial mosses, tree holes), subterranean habitats (springs, pools in caves), anchialine caves, deep-sea vents, and as animal and plant associates . Their ecological importance is high and in some ecosystems as e.g. in the plankton, copepods are the main primary consumers. Copepods are essential for nutrient recycling and their fecal pellets are a central source for detritus feeders, but also the animals themselves are an abundant feeding source for macrofauna .
Dirivultidae are found in frequent and diverse numbers at hydrothermal vents around the globe. For this review we developed a simple identification table which should help scientists to identify these copepods easy in future. Ecological aspects such as abundance and diversity patterns are evaluated. We also provide an update on current distribution patterns of this unique family and discuss the origin of Dirivultidae.
We reviewed the literature of Dirivultidae, including all species descriptions and ecological studies. Original species descriptions were used to develop a key to genera and species. We investigated the occurrence of dirivultids in chemosynthetic habitats such as hydrothermal vents, cold seeps, wood falls and whale falls in the deep sea to provide a complete overview of the distribution of this unique family. In addition, we also considered trophic interactions and compared abundance and diversity patterns of Dirivultidae in various ecosystems and habitat types to gain insight into the ecology of these copepods. Biogeographical patterns were analyzed by separation into four large regions: the Atlantic, North East Pacific, East Pacific, and West Pacific, following the definition of Desbruyères et al. . We use the thus obtained information to discuss the origin of the Dirivultidae.
Results and Discussion
Dirivultidae belong to the siphonostomatoid copepods and their morphological characteristics include: The body is cyclopiform with length ranging from 0.5 to 1.8 mm (Figure 1A, Figure 2). The prosome is 4 segmented, the urosome 4–5 segmented in females and 5–6 segmented in males. The first urosomite bears the leg 5. The oral cone is short and robust formed by labrum and labium (Figure 1D). In addition to the oral cone in the genera Ceuthoecetes, Dirivultus and Nilva a cutting borer is formed by the labium (Figure 1E). Mandible, maxillule, maxilla, and maxilliped are present (Figure 1A, 1D, 1E). Rami of legs 1 to 3 and exopod of leg 4 are 3-segmented (Figure 1G). Endopod of leg 4 is 2-segmented (Figure 1 H). The development is as follows: females carry two egg-sacks each containing one, frequently two (rarely more) large, yolky eggs; nauplii hatch as non-feeding lecithotrophic larvae, lacking mouth and labrum, and lacking a naupliar arthrite on the coxa of the antenna . The exact number of naupliar stages is unknown; the lecithotrophic nauplius may moult directly into the first copepodid stage. Five copepodid stages with well developed mouth parts and gut follow, the sixth stage being the adult.
The figure was created by selecting drawings of previous publications and adding additional information to illustrate the key to genera (Table 1) and to species (Tables 2, 3, 4). A: lateral view of a dirivultid (length ∼1 mm) . B–H ventral view of: B: antenna of Stygiopontius lauensis . C: antenna of Ceuthoecetes introversus . D: oral cone of Benthoxynus spiculifer . E: oral cone of C. introversus . F: maxilliped of S. lauensis . G: leg 1 of S. lauensis . H: leg 4 of S. lauensis . I: dorsal view of urosome of Aphotopontius acanthinus . Scale bars: B–H: 100 µm; I: 200 µm.
A: habitus, ventral view. B: habitus, dorsal view. C: oral cone and anterior appendages. Scale bars 100 µm. (A, B: ; C: by VNI).
The presumably derived characters distinguishing Dirivultidae from Ecbathyriontidae and other siphonostomatoids are the 2-segmented endopod of leg 4 (is 3-segmented in Ecbathyriontidae and many other siphonostomatoids) and the fusion of ancestral segments 3–8 in the proximal part of the antennule into one compound segment which is armed with 6 pairs of setae. Morphological observations suggest that Ecbathyriontidae, a family consisting of a single species (a new species and genus is in preparation, pers. com. VNI) (Ecbathyrion prolixicauda, Humes 1987) and found at hydrothermal vents, can be considered the only sister-group of Dirivultidae . The synapomorphy of the taxon Ecbathyriontidae – Dirivultidae is the presence of a double segment in the female antennule. This double segment is armed with 2 pairs of setae and formed by fusion of two segments which correspond to the ancestral segments 15 and 16 .
The type genus of the Dirivultidae is Dirivultus Humes & Dojiri, 1980, and the other 12 genera are Aphotopontius Humes, 1987; Benthoxynus Humes, 1984; Ceuthoecetes Humes & Dojiri, 1980; Chasmatopontius Humes, 1990; Exrima Humes, 1987; Fissuricola Humes, 1987; Humesipontius Ivanenko & Ferrari, 2003; Nilva Humes, 1987; Rhogobius Humes, 1987; Rimipontius Humes, 1996; Scotoecetes Humes, 1987; and Stygiopontius Humes, 1987 (Table 1). The genera can be mainly distinguished by the setation of the endopod of leg 4 (Figure 1H). The genera Chasmatopontius and Fissuricola are considered as basal due to the existence of 3 inner setae on the distal (second) endopodal segment of leg 4. These 3 setae indicate that the ancestor had three endopodal segments on leg 4. The distal (third) and middle (second) segments of a 3-segmented condition are fused into a distal double-segment in the 2-segmented condition. The presence of this former middle segment on the endopod of leg 4 is evidenced by the retention of 1 inner proximal seta of this segment (2 setae are indicated for the ancestor of siphonostomatoid). Ten other genera of dirivultids are characterized by a remarkably uniform 2-segmented endopod of leg 4. The distal endopodal segment of the 2-segmented endopod is armed with 2 setae at most, 1 terminal and 1 inner. The inner seta is lost in several genera of dirivultids. The proximal endopodal segment of leg 4 in dirivultids is armed with 1 inner seta at most as in the ancestral state of siphonostomatoids (this seta is lost in several genera of dirivultids). The endopod of leg 4 is lost completely in the monotypic genus Humesipontius. Table 1 is a key to genera featuring setation and some additional characters allowing genus identification. Schematic drawings of dirivultid morphology and important characters for identification are given in Figure 1.
Fifty species belong to the 13 dirivultid genera (Table 2, Table 3, and Table 4) –. Six genera (Chasmatopontius, Fissuricola, Humesipontius, Rimipontius, Nilva, and Scotoecetes) are monotypic; 3 genera (Benthoxynus, Dirivultus, Exrima) contain 2 species; Rhogobius holds 3 species and Ceuthoecetes 4 species. Most diverse genera are Aphotopontius and Stygiopontius with 10 and 21 species, respectively. In addition, our collection contains 2 species of Stygiopontius and 1 species of Chasmatopontius which are new to science but undescribed yet (SG, VNI pers. obs.). Tables 2 to 4 provide keys of genus specific characters allowing species identification within genera. Synonyms are as followed: Aphotopontius rapunculus (Humes and Segonzac, 1998) was transferred to Rhogobius rapunculus (Humes, 1987) [2; IVN in prep.]; A. temperatus (Humes, 1997) was synonymized with A. atlanteus . Stygiopontius lumiger (Humes, 1989) and S. bulbisetiger (Humes, 1996) were synonymized with S. sentifer and S. pectinatus, respectively .
Interestingly, only females or males are known in certain species despite the collection of sometimes thousands of specimens in a sample (see Table 5). For example, only females of Stygiopontius pectinatus, a species associated with the shrimp Rimicaris exoculata were found after inspection of more than 7400 individuals . Whether the lack of finding both sexes has a biological background (e.g. parthenogenesis) or is simply due to wrong classification because of an acute sexual dimorphism remains to be studied, for example by life mating observations or by using genetic tools. Indeed, COI analyses of Stygiopontius hispidulus helped to find the male of that species (SG in prep.).
Dirivultidae occur at deep-sea vents but have not been found in other chemosynthetic habitats such as shallow vents, seeps, whale falls (see Table 6) or wood falls nor in deep-sea or shallow-water sediments (PMA pers. obs.). At vents, however, they are not restricted to areas with vent flow, but can also survive away from vents on the bare basalt along the axial summit trough. Several species were encountered about 10 meters away from vents in the axial summit trough at the 9°50′N East Pacific Rise (EPR) region . Also Aphotopontius acanthinus and Stygiopontius hispidulus were recently detected in samples taken about 1 km off-axis in the 9°50′N EPR region (SG pers. obs.).
Apparently, dirivultids are specialized to colonize hard substrate. Their relatively large body with powerful swimming/crawling legs suggests that they are well adapted to an epibenthic life style , but they might not be able to live within vent and seep sediments. However, while surfaces of tubeworms, mussels and other foundation species are colonized by dirivultids at vents, they are not inhabited by dirivultids at seeps. Further, whale bones and wood providing large surfaces for colonization are also devoid of dirivultids. We think that the large, continuous area of suitable substrate might play an important role for dirivultids to flourish at midocean ridges, but prevents them from colonizing relatively small patches of hard substrate of biotic origin (e.g. tubes, shells, bones, wood), which are surrounded by soft deep-sea sediments.
The occurrence of dirivultids is restricted to vents and the surrounding axial summit trough, which is in contrast to other meiofauna taxa. Harpacticoid copepod genera found at seeps and vents are usually unknown from deep-sea sediments, but their genera and sometimes even the species are known from shallow water sites (for more details see Martínez Arbizu et al. in prep.). Nematode genera detected at vents and seeps have been reported from deep-sea sediments but also from shallow regions (for more details see Vanreusel et al. in prep).
Dirivultidae were found mostly on hard substrates (basalt and sulfide precipitates) in aggregations of invertebrates, such as bivalves (Bathymodiolus thermophilus, B. puteoserpentis, Calyptogena magnifica), vestimentiferan tubeworms (Riftia pachytila, Ridgeia piscesae), alvinellids (Alvinella pompeiana, A. caudata, Paralvinella sulfincola, P. pandorae, P. grasslei, P. hessleri), and shrimps (Rimicaris exoculata) (Table 5; , , , –, –). A total of 24 species each was found within bivalve beds and vestimentiferan bushes. Ten species each were located in alvinellid and shrimp aggregations. Two species were found in bacterial mats growing on basalt, and 3 species were detected in the plankton above vents. Unfortunately, the specific habitat of 8 species (Aphotopontius baculigerus, Fissuricola caritus, Rhogobius pressulus, Stygiopontius appositus, S. brevispina, S. lauensis, S. verruculatus) is unknown.
Most dirivultids are habitat generalists as they are able to live at different hydrothermal flux regimes and in different aggregates of megafauna. The majority of species was found in more than 2 different habitats, and only 38% of species were found in a single habitat (6 spp. at bivalves, 5 spp. at shrimps, 4 spp. at vestimentiferans, 1 sp. at alvinellids). 45% of species were detected in 2 habitats, most of them (11 from 19 spp.) in bivalve and in vestimentiferan habitats. 17% (7 spp.) were observed in three habitat types. Since it is known that those megafauna organisms are found at distinct flux regimes (alvinellids and shrimp at high flow with temperatures >50°C, tubeworms at vigorous flow with moderate temperatures (<30°C), bivalves at low flow (<15°C) , ), most dirivultids must be able to tolerate a wide range of hydrothermal fluid flux regimes.
Information on where exactly and how dirivultids live is rare, since this often requires direct observations. Up to 10 copepods were counted per shrimp (Rimicaris exoculata) on the Mid-Atlantic Ridge. They were located on the mouthparts among dense bacteria growth, in the gill chambers, and/or probably were also swimming freely among shrimp swarms . The close-up of a video camera from the submersible showed that dirivultids are crawling on alvinellid tubes colonizing sulfide chimneys at the East Pacific Rise (SG, MB pers. obs.). In this habitat type, temperatures among worms are ranging from 40°C to 100°C, sulfide concentrations can be above 1000 µM and oxygen is depleted , . Two of those dirivultid species, Benthoxynus spiculifer and Scotoecetes introrsus (both found in association with Paralvinella spp.), were investigated more in detail and exhibited high hemoglobin concentrations, with a very high and temperature sensitive oxygen affinity. This could be one of the crucial adaptations to live in low-oxygen environments , .
Abundance and diversity.
Quantitative data on copepod (and dirivultid) abundances are only available thusfar for the East Pacific Rise (EPR), Juan de Fuca Ridge (JFR), and Mid-Atlantic Ridge (MAR). Copepod abundance at deep-sea hydrothermal vents is on average below 80 ind. 10 cm−2, and ranging from 36 to 474 ind. 10 cm−2 at alvinellids , , 1 to 50 ind. 10 cm−2 at tubeworms , , and 13 to 41 ind. 10 cm−2 at mussels , . They make up 37±23% of total meiofauna communities associated with megafauna aggregations on hard substrates. Dirivultidae are the main copepod family with usually a dominance of 80% (Table 6) , , , –.
Interestingly, there are often less males than females in dirivultid populations. For example, the female to male ratio at JFR was 7.6∶1 for Stygiopontius quadrispinosus, 10.6∶1 for Aphotopontius forcipatus, and 1.5∶1 for Benthoxynus spiculifer . Also, many species from tubeworm and mussel associated communities from the Northern EPR showed a female bias or even completely lacked males (Aphotopontius hydronauticus, A. probolus, A. acanthinus). But also, certain species such as Ceuthocetes acanthothrix, C. introversus, and Scotoecetes introrsus were male dominated .
In other chemosynthetic habitats no dirivultids have been found and instead harpacticoids were dominant. Similar to vent epifauna, seep epifaunal communities showed a relatively high dominance (34±27%) of copepods within the meiofauna communities. Copepods comprised 10–43% of the meiofauna in tubeworm associated communities, and 17–99% in mussel associated communities . Relative abundance of copepods is lower in sediments from seeps and vents compared to epizooic communities from these habitats. In seep sediments, the relative abundance of copepods was usually <15% within the meiofauna community (Table 6; –). Only 4 samples showed a higher relative abundance , . In one sample, in the center of a mud volcano, copepods highly dominated , and in another study on bacterial mats the relative abundance of copepods was 33±21% . Vent infauna (most studies are from shallow-water vents) composition is highly variable with relative abundances of copepods ranging from 0 to 68% , –.
Dirivultid copepod communities are less species rich at high flow alvinellid habitats than at low flow mussel and tubeworm habitats. Copepod communities associated with the alvinellid Paralvinella sulfincola at high temperature vents (communities sampled 4 cm away from 255°C peaks) at JFR were highly dominated by Stygiopontius quadrispinosus (80%), followed by Benthoxynus spiculifer (almost 20%) . A similar dominance pattern was also found at high temperature vents of the EPR, where S. hispidulus was the most successful species in alvinellids Alvinella pompejana and A. caudata habitats . In total 10 species are known from the alvinellid habitat (Table 5).
In contrast, diversity of dirivultids was relatively high at sites with lower temperatures (∼10–20°C). At JFR B. spiculifer reached a relative abundance of 60%, and S. quadrispinosus of 10%. Aphotopontius forcipitatus and various Harpacticoida were additionally present at these lower temperature vents . At the East Pacific Rise, copepod communities associated with the tubeworm Riftia pachyptila (max. temp. 18–23°C) and with the mussel Bathymodiolus thermophilus (max. temp. 2–10°C) were equally diverse with 6 to 14 copepod species each. Dirivultids dominated the community with 75 to 97%. Most abundant species were Scotoecetes introrsus (25±20%), Benthoxynus tumidiseta (19±20%), Ceuthoecetes introversus (16±13%), Ceuthoecetes aliger (13±11%), and Aphotopontius mammillatus (12±10%) . A similar copepod diversity pattern was observed in a mussel (Bathymodiolus puteoserpentis) associated community at the Mid-Atlantic ridge, where dominant copepods were the dirivultids with Aphotopontius atlanteus (57±23%) and Aphotopontius forcipitatus (26±8%). Other copepods included Halectinosoma sp. 2 (8±5%), Aphotopontius temperatus (4±2%), Rimipontius mediospinifer (3±2%) and Bathylaophonte azorica (1±1%) . Total number of dirivultid species found at tubeworm and bivalve habitats is 25 and 24, respectively (Table 5).
A conspicuous successional pattern in diversity was found by studying new, mature, and senescent vents at JFR. New vents were mainly colonized by the dirivultid Aphotopontius forcipitatus (80%), and mature vents were characterized by a more even distribution of several copepods but with a dominance of dirivultid species. At senescent vents, with no vent flux, dirivultids were low in abundance. These communities were dominated by a cyclopoid species (Barathricola rimensis) and various harpacticoid and calanoid copepods . It should be mentioned that there is no information on hydrothermal vent flux temperature from new and mature vents.
Most dirivultid species can be considered primary consumers and are grazing on bacterial mats and detritus , . This could be inferred by analyses of mouthparts and by the finding of partly dissolved bacteria and mucus in the foregut of specimens , . Copepods associated with shrimps were feeding on bacteria located on the shrimp mouthparts or on bacteria in the water column . Detailed stable carbon and nitrogen isotopes in combination with fatty acid composition and morphological examination proved that Stygiopontius quadrispinosus and Benthoxynus spiculifer are mainly bacterivorous and, interestingly, food partitioning at the same trophic level occurred between these two species. S. quadrispinosus had a small mouth opening (∼5 µm) and its diet was based on specific bacterial strains, composed of autotrophic bacteria. In contrast, B. spiculifer had a larger mouth opening (∼20 µm) and was feeding on various autotrophic and heterotrophic bacteria, .
Only members of the genera Ceuthoecetes, Dirivultus, and Nilva have a different form of feeding, and are thought to feed on vestimentiferans . The oral cone of these parasites is cylindrical and the labium is transformed into a cutting borer (Figure 1E). Photographs of vestimentiferans showed round wounds in the tentacular crown which were thought to be inflicted by Dirivultus dentaneus. However, it is also stated that indentations could be an artifact caused by the fixation . Dirivultus spinigulatus was observed feeding on vestimentiferan plume filaments .
Dirivultids are a food source for macrofauna. Stable isotope studies on Paralvinella showed that copepods were part of its diet. It was hypothesized that copepods were consumed along with debris while the animal was grazing on the chimney surface . It is unknown yet, but highly probable, that also many other macrofauna species feed on dirivultids.
Dirivultids are highly successful in their distribution since they are known from 4 main biogeographic regions, the Atlantic (A), North East Pacific (NEP), East Pacific (EP), and West Pacific (WP) (Figure 3; Table 5; , , , –, –). A total of 13 genera with 50 species are currently known and most are endemic to a single region. Only five species occur in 2 regions and those belong to the two most diverse dirivultid genera Stygiopontius and Aphotopontius. We are not aware of any other region studied, in which dirivultids did occur. It has be taken into account that the majority of studies was historically carried out in the East Pacific. Therefore we expect that future collections will improve our knowledge of the distribution patterns in this family.
Current findings of dirivultid genera on mid-ocean ridges and back-arc basins in the Atlantic (red color code), North East Pacific (green color code), East Pacific (blue color code), and West Pacific (purple color code). The number of species is given between brackets. Map modified after Van Dover et al. .
The diversity hotspot is the East Pacific with 33 species from 10 genera. Four genera with 4 species are known from the North East Pacific and 3 genera with 6 species from the West Pacific. In the Atlantic, a total of 3 genera with 12 species are currently recognized.
Nine of the 13 genera are endemic. Six genera are restricted to the East Pacific (Ceuthoecetes (4 spp.), Exrima (2 sp.), Fissuricola (1 sp.), Nilva (1 sp.), Rhogobius (3 spp.), and Scotoecetes (1 sp.)). The genus Chasmatopontius is only known from the West Pacific (1 sp.), Humesipontius only from the North East Pacific (1 sp.), and Rimipontius only from the Atlantic (1 spp.) (Figure 3). 45 of the 50 described dirivultid species are endemic to a single a biogeographic region (EP: 30 spp.; A: 8 spp.; WP: 4 spp.; NEP: 3 spp.) (Table 5).
The genus Stygiopontius has representatives in all four regions (EP: 11 spp.; A: 9 spp.; WP: 4 spp.; NEP: 1 sp.). Aphotopontius was found in the Atlantic (2 spp.), North East Pacific (1 sp.) and East Pacific (8 spp.). Benthoxynus is known with a single species each from the North East Pacific and the East Pacific, and Dirivultus from the West Pacific (1 sp.) and from off California (Dirivultus dentaneus; not at vents) (Figure 3). However, only five species are known from 2 regions. The Atlantic and East Pacific share the species Stygiopontius mirus and S. rimivagus, the Atlantic and the West Pacific have S. pectinatus in common, the Atlantic and North East Pacific Aphotopontius forcipatus, and the East Pacific and the West Pacific S. stabilitus.
Dispersal of copepods in the pelagial is often but not exclusively during their copepodid stage . Adults and copepodid stages of Rimipontius mediospinifer, Stygiopontius cladarus, S. pectinatus were found in plankton at 80–300 m above vents in the Mid-Atlantic Ridge . Other dirivultids from 9°50′N at the EPR were caught in sediment traps positioned around and above vents (Lauren Mullineaux pers. com., SG pers. obs.). However, copepodids have also been sampled from tubeworm and mussel associations suggesting that at least part of the copepodid development is also possible within the benthos . Although detailed studies on dispersal abilities (such as duration of nauplii and copepodids stages, their buoyancy and feeding strategies) lack, the first observations of copepods and their copepodids in the plankton give a hint that the global distribution of Dirivultidae may have been possible due to long-distance dispersal via ocean currents.
Origin and phylogenetic relationship
The distribution of extant dirivultids points to a pathway of immigration from shallow waters, and not from the deep-sea sediments, nor from other deep-sea chemosynthetic habitats as it has been suggested for many other vent animals , . Dirivultidae are only known from deep-sea hydrothermal vents and from the axial summit trough, but are unknown from deep-sea sediments. We conclude that other deep-sea chemosynthetic habitats did not facilitate immigration as stepping stones towards vents  or that dirivultids belong to the wide-spread sulphophilic fauna, because this family is unknown from seeps, whale falls, or any other reducing ecosystems. The only exception is the species Dirvultus dentaneus, which was once collected from the siboglinid tubeworm Lamellibrachia barhami at 1125 m depth off southern California . L. barhami is known from the subduction zone cold seeps on the North America continental margin and from a sedimented hydrothermal region at Middle Valley on the Juan de Fuca Ridge . Due to its limited distribution, it is also unlikely that dirivultids recently originated from a widespread fauna of generalists. Whether dirivultids have a long term in situ evolution remains to be tested. For small animals, immigration via their foundation species could be another option to invade the vent habitat. However, we suggest that alvinocarid shrimp, vestimentiferan tubeworms or bivalves did not act as ancestral carrier species. These megafauna species invaded the vent ecosystem via seeps, but dirivultids are not found there . Alvinellid polychaetes are only found at vents, and the order Terebellida (to which alvinellids belong to) is found in shallow waters . We propose that it is most likely that the dirivultid ancestor immigrated from the shallow water, the habitat where nowadays most Siphonostomatoida are found in association with various invertebrates and vertebrates . Maybe, invasion was possible via the hard substrate ecosystem of mid-ocean ridges from shallow waters towards greater depths.
Dirivultidae are considered to have a basal position within the large order Siphonostomatoida due to the presence of an simple oral cone with a loosely associated labrum and labium, instead of a complex oral structure called siphon (with a fused labrum and labium) as found in many other siphonostomatoids . The Siphonostomatoida includes more than 40 families with clear morphological distinction from other copepods (by the formation of an oral cone) but with unresolved phylogenetic relationships . Siphonostomatoids live in association with other animals and most of them are animal parasites exhibiting a siphon for cutting and/or sucking. Two thirds of the species (with a total of >1550) are described as parasites of fishes and mammals, the other third are parasites or associates of invertebrates such as ascidians, polychaetes, bryozoans, cnidarians, crustaceans, echinoderms, or sponges . In contrast, most dirivultids are not parasitic, but are free-living and bacterivorous and often live in aggregations of invertebrates at hydrothermal vents , . The bacterivorous feeding type (as seen from the simple mouth structure) of dirivultids suggests that they are basal to the other siphonostomatoids.
The phylogenetic relationships within Dirivultidae are unsolved yet, as detailed morphological comparisons and genetic analyses are by far not complete. The evolution of the formation of the oral cone (a key character of siphonostomatoids) has led to controversial ideas. The first idea, which in our opinion is the most probable one, is that the dirivultid ancestor had a simple oral cone (bacterivorous feeding). This is supported by the bacterivorous species Chasmatopontius and Fissuricola which are considered basal also due to the existence of 3 inner setae on the distal (second) endopodal segment of leg 4 (see Taxonomy). Over time, Dirivultidae adapted successfully to vents and developed there a more complex oral cone (evolution to a parasitic mode of life). In consequence, the “cutting borer”, a modified distal disk of the oral cone formed by the labium of the parasitic genera Ceuthoecetes, Dirivultus, and Nilva would have evolved secondarily and independent from other parasitic Siphonostomatoida. The second idea is that the feeding apparatus in dirivultids could have evolved from a complex oral cone of secondary consumers (fused labrum and labium) back to a simple oral cone of primary consumers (with a loosely associated labrum and labium). The background of this hypothesis is that other families of the Siphonostomatoida are known to be mostly parasites, and in dirivultids, the antennae, maxillipeds and mandibles have the characteristic form known from those other parasitic Siphonostomatoida . This would imply that Ceuthoecetes, Dirivultus, and Nilva are on the basis of Dirivultidae. However, it should be mentioned here that it remains to be clarified if these morphological features are related to adaptations of the feeding mode (parasitism) or to adaptations of the life style mode of dirivultids (which are free living on foundation species, so antennae could also be used to hold themselves on the foundation species and not to fall off). Interestingly, the Monstrilloida, a former copepod order that was recently placed within the Siphonostomatoida according to molecular analyses, are primary consumers. For this taxon, it has been suggested that they secondarily returned from an ectoparasitic to a free-living mode of life . Only detailed morphological analyses in combination with gene analyses can help unravel the unsolved origin and phylogenetic relationships of Dirivultidae.
Dirivultidae is the most diverse taxon at deep-sea hydrothermal vents. With the discovery of new vent sites and with the study of sites where macrofauna species are already known but not the meiofauna, species number is expected to increase further. Although they can be highly abundant in some vent habitats, only a few studies include this family in a broader ecological context. One goal is to take this family into account and the here provided key should help scientists to do so. Biogeographic patterns are expected to change with future collections; especially knowledge from the West Pacific region and the Indian Ocean is very scarce at the moment, and the polar regions remain completely unstudied. Origin and evolutionary processes are unclear yet, and in the future, genetic analyses will help to understand species distributions and speciation processes.
This review would not have been possible, if a single taxonomist, Arthur G. Humes, had not put such an effort into describing the majority of dirivultid species. We would like to thank all scientists who shared their samples, making this study of dirivultids possible.
Analyzed the data: SG VNI PMA. Wrote the paper: SG MB. Conception: SG MB. Revised article for intellectual content: VNI PMA.
- 1. Tunnicliffe V, McArthur AG, McHugh D (1998) A biogeographical perspective of the deep-sea hydrothermal vent fauna. Adv Mar Biol 34: 353–442.V. TunnicliffeAG McArthurD. McHugh1998A biogeographical perspective of the deep-sea hydrothermal vent fauna.Adv Mar Biol34353442
- 2. Ivanenko VN, Defaye D (2006) Arthropoda, Crustacea, Copepoda. In: Desbruyères D, Segonzac M, Bright M, editors. Handbook of deep-sea hydrothermal vent fauna. Linz: Densia. 316 p.VN IvanenkoD. Defaye2006Arthropoda, Crustacea, Copepoda.D. DesbruyèresM. SegonzacM. BrightHandbook of deep-sea hydrothermal vent faunaLinzDensia316
- 3. Desbruyères D, Segonzac M, Bright M (2006) Handbook of hydrothermal vent fauna. Linz: Denisia. 544 p.D. DesbruyèresM. SegonzacM. Bright2006Handbook of hydrothermal vent faunaLinzDenisia544
- 4. Gollner S, Zekely J, Govenar B, Nemeschkal HL, Le Bris N, et al. (2007) Tubeworm-associated permanent meiobenthic communities from two chemically different hydrothermal vent sites at the East Pacific Rise. Mar Ecol Prog Ser 337: 39–49.S. GollnerJ. ZekelyB. GovenarHL NemeschkalN. Le Bris2007Tubeworm-associated permanent meiobenthic communities from two chemically different hydrothermal vent sites at the East Pacific Rise.Mar Ecol Prog Ser3373949
- 5. Tsurumi M, de Graaf RC, Tunnicliffe V (2003) Distributional and biological aspects of copepods at hydrothermal vents on the Juan de Fuca Ridge, north-east Pacific Ocean. J Mar Biol Assoc UK 83: 469–477.M. TsurumiRC de GraafV. Tunnicliffe2003Distributional and biological aspects of copepods at hydrothermal vents on the Juan de Fuca Ridge, north-east Pacific Ocean.J Mar Biol Assoc UK83469477
- 6. Giere O (2009) Meiobenthology, the microscopic fauna in aquatic sediments. Berlin Heidelberg: Springer Verlag. 527 p.O. Giere2009Meiobenthology, the microscopic fauna in aquatic sedimentsBerlin HeidelbergSpringer Verlag527
- 7. Huys R, Boxshall GA (1991) Copepod Evolution. London: The Ray Society. 468 p.R. HuysGA Boxshall1991Copepod EvolutionLondonThe Ray Society468
- 8. Ivanenko VN, Martínez Arbizu P, Stecher J (2007) Lecithotrophic nauplius of the family Dirivultidae (Copepoda; Siphonostomatoida) hatched on board over the Mid-Atlantic Ridge (5°S). Mar Ecol 28: 49–53.VN IvanenkoP. Martínez ArbizuJ. Stecher2007Lecithotrophic nauplius of the family Dirivultidae (Copepoda; Siphonostomatoida) hatched on board over the Mid-Atlantic Ridge (5°S).Mar Ecol284953
- 9. Humes AG (1987) Copepoda from deep-sea hydrothermal vents. B Mar Sci 41(3): 645–788.AG Humes1987Copepoda from deep-sea hydrothermal vents.B Mar Sci41(3)645788
- 10. Ivanenko VN (1999) Comparative analysis of the antennules of the asterocherid females (Copepoda, Siphonostomatoida) - symbionts of marine invertebrates. In: Schram FR, von Voupel Lein JC, editors. Crustaceans and the Biodiversity Crisis. pp. 207–216.VN Ivanenko1999Comparative analysis of the antennules of the asterocherid females (Copepoda, Siphonostomatoida) - symbionts of marine invertebrates.FR SchramJC von Voupel LeinCrustaceans and the Biodiversity Crisis207216
- 11. Humes AG, Dojiri M (1980) A siphonostome copepod associated with a vestimentiferan from the Galapagos Rift and the East Pacific Rise. Proc Biol Soc Was 93(3): 697–707.AG HumesM. Dojiri1980A siphonostome copepod associated with a vestimentiferan from the Galapagos Rift and the East Pacific Rise.Proc Biol Soc Was93(3)697707
- 12. Humes AG, Dojiri M (1980) A new siphonostome family (Copepoda) associated with a Vestimentiferan in deep water off California. Pac Sci 34(2): 143–151.AG HumesM. Dojiri1980A new siphonostome family (Copepoda) associated with a Vestimentiferan in deep water off California.Pac Sci34(2)143151
- 13. Humes AG (1984) Benthoxynus spiculifer n. gen., n. sp. (Copepoda: Siphonostomatoida) associated with Vestimentifera (Pogonophora) at a deep-water geothermal vent off the coast of Washington. Can J Zool 62: 2594–2599.AG Humes1984Benthoxynus spiculifer n. gen., n. sp. (Copepoda: Siphonostomatoida) associated with Vestimentifera (Pogonophora) at a deep-water geothermal vent off the coast of Washington.Can J Zool6225942599
- 14. Humes AG (1989) New species of Stygiopontius (Copepoda, Siphonostomatoida) from a deep-sea hydrothermal vent at the East Pacific Rise. Zool Scr 18: 103–113.AG Humes1989New species of Stygiopontius (Copepoda, Siphonostomatoida) from a deep-sea hydrothermal vent at the East Pacific Rise.Zool Scr18103113
- 15. Humes AG (1989) Rhogobius pressulus n. sp. (Copepoda: Siphonostomatoida) from a deep-sea hydrothermal vent at the Galapagos Rift. Pac Sci 43(1): 27–31.AG Humes1989Rhogobius pressulus n. sp. (Copepoda: Siphonostomatoida) from a deep-sea hydrothermal vent at the Galapagos Rift.Pac Sci43(1)2731
- 16. Humes AG (1990) Aphotopontius probolus, sp. nov., and records of other siphonostomatoid copepods from deep-sea vents in the eastern Pacific. Scient Mar 54(2): 145–154.AG Humes1990Aphotopontius probolus, sp. nov., and records of other siphonostomatoid copepods from deep-sea vents in the eastern Pacific.Scient Mar54(2)145154
- 17. Humes AG (1990) Copepods (Siphonostomatoida) from a deep-sea hydrothermal vent at the Mariana Back-Arc Basin in the Pacific, including a new genus and species. J Nat Hist 24: 289–304.AG Humes1990Copepods (Siphonostomatoida) from a deep-sea hydrothermal vent at the Mariana Back-Arc Basin in the Pacific, including a new genus and species.J Nat Hist24289304
- 18. Humes AG (1991) Siphonostomatoid copepods from a deep-water hydrothermal zone in the Lau Basin, South Pacific. Bull Mus natn Hist nat, Paris 13(4): 121–134.AG Humes1991Siphonostomatoid copepods from a deep-water hydrothermal zone in the Lau Basin, South Pacific.Bull Mus natn Hist nat, Paris13(4)121134
- 19. Humes AG, Lutz RA (1994) Aphotopontius acanthinus, new species (Copepoda: Siphonostomatoida), from deep-sea hydrothermal vents on the East Pacific Rise. J Crustacean Biol 14(2): 337–345.AG HumesRA Lutz1994Aphotopontius acanthinus, new species (Copepoda: Siphonostomatoida), from deep-sea hydrothermal vents on the East Pacific Rise.J Crustacean Biol14(2)337345
- 20. Humes AG (1996) Deep-sea Copepoda (Siphonostomatoida) from hydrothermal sites on the Mid-Atlantic Ridge at 23° and 37°N. B Mar Sci 58(3): 609–653.AG Humes1996Deep-sea Copepoda (Siphonostomatoida) from hydrothermal sites on the Mid-Atlantic Ridge at 23° and 37°N.B Mar Sci58(3)609653
- 21. Humes AG (1999) Copepoda (Siphonostomatoida) from Pacific hydrothermal vents and cold seeps, including Dirivultus spinigulatus sp. nov. in Papua New Guinea. J Mar Biol Assoc UK 79: 1053–1060.AG Humes1999Copepoda (Siphonostomatoida) from Pacific hydrothermal vents and cold seeps, including Dirivultus spinigulatus sp. nov. in Papua New Guinea.J Mar Biol Assoc UK7910531060
- 22. Humes AG, Segonzac M (1998) Copepoda from deep-sea hydrothermal sites and cold seeps: description of a new species of Aphotopontius from the East Pacific Rise and general distribution. Cah Biol Mar 39: 51–62.AG HumesM. Segonzac1998Copepoda from deep-sea hydrothermal sites and cold seeps: description of a new species of Aphotopontius from the East Pacific Rise and general distribution.Cah Biol Mar395162
- 23. Ivanenko VN, Ferrari FD (2002) A new genus and species of the family Dirivultidae (Copepoda: Siphonostomatoida) from a deep-sea hydrothermal vent at the Juan de Fuca Ridge (the northeastern Pacific) with comments of dirivultid distribution. Arthropoda Selecta 11(3): 177–185.VN IvanenkoFD Ferrari2002A new genus and species of the family Dirivultidae (Copepoda: Siphonostomatoida) from a deep-sea hydrothermal vent at the Juan de Fuca Ridge (the northeastern Pacific) with comments of dirivultid distribution.Arthropoda Selecta11(3)177185
- 24. Ivanenko VN, Martínez Arbizu P, Stecher J (2006) Copepods of the family Dirivultidae (Siphonostomatoida) from deep-sea hydrothermal vent fields on the Mid-Atlantic Ridge at 14°N and 5°S. Zootaxa 1277: 1–21.VN IvanenkoP. Martínez ArbizuJ. Stecher2006Copepods of the family Dirivultidae (Siphonostomatoida) from deep-sea hydrothermal vent fields on the Mid-Atlantic Ridge at 14°N and 5°S.Zootaxa1277121
- 25. Gollner S, Riemer B, Martínez Arbizu P, Le Bris N, Bright M (2010) Diversity of meiofauna from the 9°50′N East Pacific Rise across a gradient of hydrothermal fluid emissions. PLoS ONE 5(8): e12321.S. GollnerB. RiemerP. Martínez ArbizuN. Le BrisM. Bright2010Diversity of meiofauna from the 9°50′N East Pacific Rise across a gradient of hydrothermal fluid emissions.PLoS ONE5(8)e12321
- 26. Heptner MV, Ivanenko VN (2002) Copepoda (Crustacea) of hydrothermal ecosystems of the World Ocean. Arthropoda Selecta 11(2): 117–134.MV HeptnerVN Ivanenko2002Copepoda (Crustacea) of hydrothermal ecosystems of the World Ocean.Arthropoda Selecta11(2)117134
- 27. Ivanenko VN, Heptner MV (1998) New data on morphology and redescription of Aphotopontius mammillatus Humes 1987 (Copepoda, Siphonostomatoida, Dirivultidae) from deep-sea hydrothermal vents in the eastern Pacific (Guaymas Basin). J Marine Syst 15: 243–254.VN IvanenkoMV Heptner1998New data on morphology and redescription of Aphotopontius mammillatus Humes 1987 (Copepoda, Siphonostomatoida, Dirivultidae) from deep-sea hydrothermal vents in the eastern Pacific (Guaymas Basin).J Marine Syst15243254
- 28. Ivanenko VN (1998) Deep-sea hydrothermal vent copepoda (Siphonostomatoida, Dirivultidae) in plankton over the Mid-Atlantic Ridge (29°N), morphology of their first copepodid stage. Zool Zh 77(1): 1249–1256.VN Ivanenko1998Deep-sea hydrothermal vent copepoda (Siphonostomatoida, Dirivultidae) in plankton over the Mid-Atlantic Ridge (29°N), morphology of their first copepodid stage.Zool Zh77(1)12491256
- 29. Zekely J, Van Dover CL, Nemeschkal HL, Bright M (2006) Hydrothermal vent meiobenthos associated with Bathymodiolus aggregations from Mid-Atlantic Ridge and East Pacific Rise. Deep-Sea Res Pt I 53: 1163–1378.J. ZekelyCL Van DoverHL NemeschkalM. Bright2006Hydrothermal vent meiobenthos associated with Bathymodiolus aggregations from Mid-Atlantic Ridge and East Pacific Rise.Deep-Sea Res Pt I5311631378
- 30. Humes AG (1989) Copepoda from deep-sea hydrothermal vents at the East Pacific Rise. Bull Mus natl Hist nat, Paris 11: 829–849.AG Humes1989Copepoda from deep-sea hydrothermal vents at the East Pacific Rise.Bull Mus natl Hist nat, Paris11829849
- 31. Etter RJ, Mullineaux LS (2001) Deep-Sea Communities. In: Bertness MD, Gaines SD, Hay ME, editors. Marine Community Ecology. Sunderland, Massachusetts: Sinauer Associates Inc. pp. 367–394.RJ EtterLS Mullineaux2001Deep-Sea Communities.MD BertnessSD GainesME HayMarine Community EcologySunderland, MassachusettsSinauer Associates Inc367394
- 32. Le Bris N, Govenar B, Le Gall C, Fisher CR (2006) Variability of physico-chemical conditions in 9°50′N EPR diffuse flow vent habitats. Mar Chem 98: 167–182.N. Le BrisB. GovenarC. Le GallCR Fisher2006Variability of physico-chemical conditions in 9°50′N EPR diffuse flow vent habitats.Mar Chem98167182
- 33. Le Bris N, Zbinden M, Gaill F (2005) Processes controlling the physico-chemical micro-environments associated with Pompeii worms. Deep-Sea Res Pt I 1071–1083.N. Le BrisM. ZbindenF. Gaill2005Processes controlling the physico-chemical micro-environments associated with Pompeii worms.Deep-Sea Res Pt I10711083
- 34. Le Bris N, Gaill F (2007) How does the annelid Alvinella pompejana deal with an extreme hydrothermal environment? Rev Environ Sci Biotechnol 6: 167–221.N. Le BrisF. Gaill2007How does the annelid Alvinella pompejana deal with an extreme hydrothermal environment?Rev Environ Sci Biotechnol6167221
- 35. Hourdez S, Lamontagne J, Peterson P, Weber RE, Fisher CR (2000) Hemoglobin from a deep-sea hydrothermal-vent copepod. Biol Bull 199: 95–99.S. HourdezJ. LamontagneP. PetersonRE WeberCR Fisher2000Hemoglobin from a deep-sea hydrothermal-vent copepod.Biol Bull1999599
- 36. Sell AF (2000) Life in the extreme environment at a hydrothermal vent: hemoglobin in a deep-sea copepod. P Roy Soc Lond 267: 2323–2336.AF Sell2000Life in the extreme environment at a hydrothermal vent: hemoglobin in a deep-sea copepod.P Roy Soc Lond26723232336
- 37. Copley JTP, Flint HC, Ferrero TJ, Van Dover CL (2007) Diversity of meiofauna and free-living nematodes in hydrothermal vent mussel beds on the northern and southern East Pacific Rise. J Mar Biol Assoc UK 87(5): 1141–1152.JTP CopleyHC FlintTJ FerreroCL Van Dover2007Diversity of meiofauna and free-living nematodes in hydrothermal vent mussel beds on the northern and southern East Pacific Rise.J Mar Biol Assoc UK87(5)11411152
- 38. Dinet A, Grassle F, Tunnicliffe V (1988) Premières observations sur la meiofauna des sites hydrothermaux de la dorsale East-Pacifique (Guaymas, 21°N) et de l'Explorer Ridge. Oceanol Acta 85: 7–14.A. DinetF. GrassleV. Tunnicliffe1988Premières observations sur la meiofauna des sites hydrothermaux de la dorsale East-Pacifique (Guaymas, 21°N) et de l'Explorer Ridge.Oceanol Acta85714
- 39. Gollner S, Zekely J, VanDover CL, Govenar B, Le Bris N, et al. (2006) Benthic copepod communities associated with tubeworm and mussel aggregations on the East Pacific Rise. Cah Biol Mar 47: 397–402.S. GollnerJ. ZekelyCL VanDoverB. GovenarN. Le Bris2006Benthic copepod communities associated with tubeworm and mussel aggregations on the East Pacific Rise.Cah Biol Mar47397402
- 40. Bright M, Plum C, Riavitz LA, Nikolov N, Martínez Arbizu P, et al. (in press) Epizooic metazoan meiobenthos associated with tubeworm and mussel aggregations from cold seeps of the Northern Gulf of Mexico. Deep-Sea Res Pt I. M. BrightC. PlumLA RiavitzN. NikolovP. Martínez Arbizuin pressEpizooic metazoan meiobenthos associated with tubeworm and mussel aggregations from cold seeps of the Northern Gulf of Mexico.Deep-Sea Res Pt I
- 41. Jensen P, Aagaard I, Burke RA Jr, Dando PR, Jorgensen NO, et al. (1992) “Bubbling reefs” in the Kattegat: submarine landscapes of carbonate-cemented rocks support a diverse ecosystem at methane seep. Mar Ecol Prog Ser 83: 103–112.P. JensenI. AagaardRA Burke JrPR DandoNO Jorgensen1992“Bubbling reefs” in the Kattegat: submarine landscapes of carbonate-cemented rocks support a diverse ecosystem at methane seep.Mar Ecol Prog Ser83103112
- 42. Montagna PA, Spies RB (1985) Meiofauna and Chlorophyll associated with Beggiatoa mats of a natural submarine petroleum seep. Mar Environ Res 16: 231–242.PA MontagnaRB Spies1985Meiofauna and Chlorophyll associated with Beggiatoa mats of a natural submarine petroleum seep.Mar Environ Res16231242
- 43. Montagna PA, Bauer JE, Toal J, Hardin D, Spies RB (1987) Temporal variability and the relationship between benthic and meiofaunal and microbial populations of a natural coastal petroleum seep. J Mar Res 45: 761–789.PA MontagnaJE BauerJ. ToalD. HardinRB Spies1987Temporal variability and the relationship between benthic and meiofaunal and microbial populations of a natural coastal petroleum seep.J Mar Res45761789
- 44. Montagna PA, Bauer JE, Hardin D, Spies RB (1989) Vertical distribution of microbial and meiofaunal populations in sediments of a natural coastal hydrocarbon seep. J Mar Res 47: 657–680.PA MontagnaJE BauerD. HardinRB Spies1989Vertical distribution of microbial and meiofaunal populations in sediments of a natural coastal hydrocarbon seep.J Mar Res47657680
- 45. Olu K, Lance S, Sibuet M, Henry P, Fiala-Medioni A, et al. (1997) Cold seep communities as indicators of fluid expulsion patterns through mud volcanoes seaward of the Barbados accretionary prism. Deep-Sea Res Pt I 44(5): 811–841.K. OluS. LanceM. SibuetP. HenryA. Fiala-Medioni1997Cold seep communities as indicators of fluid expulsion patterns through mud volcanoes seaward of the Barbados accretionary prism.Deep-Sea Res Pt I44(5)811841
- 46. Palmer MA (1988) Meiofauna dispersal near natural petroleum seeps in the Santa Barbara Channel: a recolonization experiment. Oil Chem Pollut 4: 179–189.MA Palmer1988Meiofauna dispersal near natural petroleum seeps in the Santa Barbara Channel: a recolonization experiment.Oil Chem Pollut4179189
- 47. Powell EN, Bright TJ (1981) A thiobios does exist - Gnathostomulid domination of the canyon community at the East Flower Garden Brine Seep. Int Revue ges Hydrobiol 66: 675–683.EN PowellTJ Bright1981A thiobios does exist - Gnathostomulid domination of the canyon community at the East Flower Garden Brine Seep.Int Revue ges Hydrobiol66675683
- 48. Powell EN, Bright TJ, Woods A, Gittings S (1983) Meiofauna and the thiobios in the East Flower Garden Brine Seep. Mar Biol 73: 269–283.EN PowellTJ BrightA. WoodsS. Gittings1983Meiofauna and the thiobios in the East Flower Garden Brine Seep.Mar Biol73269283
- 49. Sergeeva NG, Gulin MB (2007) Meiobenthos from an active methane seepage area in the NW Black Sea. Mar Ecol 28: 152–159.NG SergeevaMB Gulin2007Meiobenthos from an active methane seepage area in the NW Black Sea.Mar Ecol28152159
- 50. Shirayama Y, Ohta S (1990) Meiofauna in a cold-seep community off Hatsushima, Central Japan. Journal of the Oceanographical Society of Japan 46: 118–124.Y. ShirayamaS. Ohta1990Meiofauna in a cold-seep community off Hatsushima, Central Japan.Journal of the Oceanographical Society of Japan46118124
- 51. Soltwedel T, Portnova D, Kolar I, Mokievsky V, Schewe I (2005) The small-sized benthic biota of the Hakon Mosby Mud Volcano (SW Barents Sea slope). J Marine Syst 55: 271–290.T. SoltwedelD. PortnovaI. KolarV. MokievskyI. Schewe2005The small-sized benthic biota of the Hakon Mosby Mud Volcano (SW Barents Sea slope).J Marine Syst55271290
- 52. Sommer S, Gutzmann E, Pfannkuche O (2007) Sediments hosting gas hydrates: oasis for metazoan meiofauna. Mar Ecol Prog Ser 337: 27–37.S. SommerE. GutzmannO. Pfannkuche2007Sediments hosting gas hydrates: oasis for metazoan meiofauna.Mar Ecol Prog Ser3372737
- 53. Van Gaever S, Moodley L, de Beer D, Vanreusel A (2006) Meiobenthos at the Arctic Hakon Mosby Mud Volcano, with a parental-caring nematode thriving in sulphide-rich sediments. Mar Ecol Prog Ser 321: 143–155.S. Van GaeverL. MoodleyD. de BeerA. Vanreusel2006Meiobenthos at the Arctic Hakon Mosby Mud Volcano, with a parental-caring nematode thriving in sulphide-rich sediments.Mar Ecol Prog Ser321143155
- 54. Van Gaever S, Olu K, Deryke S, Vanreusel A (2009) Metazoan meiofaunal communities at cold seeps along the Norwegian margin: Influence of habitat heterogeneity and evidence for connection with shallow-water habitats. Deep-Sea Res Pt I 56: 772–785.S. Van GaeverK. OluS. DerykeA. Vanreusel2009Metazoan meiofaunal communities at cold seeps along the Norwegian margin: Influence of habitat heterogeneity and evidence for connection with shallow-water habitats.Deep-Sea Res Pt I56772785
- 55. Robinson CA, Bernhard JM, Levin LA, Mendoza GF, Blanks JK (2004) Surficial hydrocarbon seep infauna from the Blake Ridge (Atlantic Ocean, 2150m) and the Gulf of Mexico (690–2240m). Mar Ecol 25(4): 313–336.CA RobinsonJM BernhardLA LevinGF MendozaJK Blanks2004Surficial hydrocarbon seep infauna from the Blake Ridge (Atlantic Ocean, 2150m) and the Gulf of Mexico (690–2240m).Mar Ecol25(4)313336
- 56. Kamenev GM, Fedeev VI, Selin NI, Tarasov VG (1993) Composition and distribution of macro- and meiobenthos around sublittoral hydrothermal vents in the Bay of Plenty, New Zealand. New Zeal J Mar Fresh 27: 407–418.GM KamenevVI FedeevNI SelinVG Tarasov1993Composition and distribution of macro- and meiobenthos around sublittoral hydrothermal vents in the Bay of Plenty, New Zealand.New Zeal J Mar Fresh27407418
- 57. Tarasov VG, Gebruk AV, Shulkin VM, Kamenev GM, Fadeev VI, et al. (1999) Effect of shallow-water hydrothermal venting on the biota of Matupi Harbour (Rabaul Caldera, New Britain Island, Papua New Guinea). Cont Shelf Res 19: 79–116.VG TarasovAV GebrukVM ShulkinGM KamenevVI Fadeev1999Effect of shallow-water hydrothermal venting on the biota of Matupi Harbour (Rabaul Caldera, New Britain Island, Papua New Guinea).Cont Shelf Res1979116
- 58. Thiermann F, Windoffer R, Giere O (1994) Selected meiofauna around shallow water hydrothermal vents off Milos (Greece): ecological and ultrastructural aspects. Vie Milieu 44(3): 215–226.F. ThiermannR. WindofferO. Giere1994Selected meiofauna around shallow water hydrothermal vents off Milos (Greece): ecological and ultrastructural aspects.Vie Milieu44(3)215226
- 59. Vanreusel A, Van den Bossche I, Thiermann F (1997) Free-living marine nematodes from hydrothermal sediments: similarities with communities from diverse reduced habitats. Mar Ecol Prog Ser 157: 207–219.A. VanreuselI. Van den BosscheF. Thiermann1997Free-living marine nematodes from hydrothermal sediments: similarities with communities from diverse reduced habitats.Mar Ecol Prog Ser157207219
- 60. Zeppilli D, Danovaro R (2009) Meiofaunal diversity and assemblage structure in a shallow-water hydrothermal vent in the Pacific Ocean. Aquat Biol 5: 75–84.D. ZeppilliR. Danovaro2009Meiofaunal diversity and assemblage structure in a shallow-water hydrothermal vent in the Pacific Ocean.Aquat Biol57584
- 61. Limén H, Stevens C J, Bourass Z, Juniper SK (2008) Trophic ecology of siphonostomatoid copepods at deep-sea hydrothermal vents in the northeast Pacific. Mar Ecol Prog Ser 359: 161–170.H. LiménJ. Stevens CZ. BourassSK Juniper2008Trophic ecology of siphonostomatoid copepods at deep-sea hydrothermal vents in the northeast Pacific.Mar Ecol Prog Ser359161170
- 62. Tunnicliffe V (1992) The nature and origin of the modern hydrothermal vent fauna. Plaios 7: 338–350.V. Tunnicliffe1992The nature and origin of the modern hydrothermal vent fauna.Plaios7338350
- 63. Van Dover CL (2000) The ecology of hydrothermal vents. Princeton New Jersey: Princeton University Press. 424 p.CL Van Dover2000The ecology of hydrothermal ventsPrinceton New JerseyPrinceton University Press424
- 64. Smith CR, Baco AR (2003) Ecology of whale falls at the deep-sea floor. Oceanogr Mar Biol: An Annual Review 43: 311–354.CR SmithAR Baco2003Ecology of whale falls at the deep-sea floor.Oceanogr Mar Biol: An Annual Review43311354
- 65. Boxshall GA, Halsey SH (2004) An introduction to copepod diversity. Dorchester: The Ray Society. 970 p.GA BoxshallSH Halsey2004An introduction to copepod diversityDorchesterThe Ray Society970
- 66. Boxshall GA (1990) The skeletomusculature of siphonostomatoid copepods, with an analysis of adaptive radiation in structure of the oral cone. Phil T Roy Soc B 328: 167–212.GA Boxshall1990The skeletomusculature of siphonostomatoid copepods, with an analysis of adaptive radiation in structure of the oral cone.Phil T Roy Soc B328167212
- 67. Martin JW, Davis GE (2001) An updated classification of the recent Crustacea. Science Series Los Angeles County Natural History Museum 39: 1–124.JW MartinGE Davis2001An updated classification of the recent Crustacea.Science Series Los Angeles County Natural History Museum391124
- 68. Huys R, Llewellyn-Hughes J, Conroy-Dalton S, Olson PD, Spinks JN, et al. (2007) Extraordinary host switching in siphonostomatoid copepods and the demise of the Monstrilloida: Integrating molecular data, ontogeny and antennulary morphology. Mol Phylogenet Evol 43(2): 368–378.R. HuysJ. Llewellyn-HughesS. Conroy-DaltonPD OlsonJN Spinks2007Extraordinary host switching in siphonostomatoid copepods and the demise of the Monstrilloida: Integrating molecular data, ontogeny and antennulary morphology.Mol Phylogenet Evol43(2)368378
- 69. Van Dover CL, German CR, Speer KG, Parson LM, Vrijenhoek RC (2002) Evolution and Biogeography of Deep-Sea Vent and Seep Invertebrates. Science 295: 1253–1257.CL Van DoverCR GermanKG SpeerLM ParsonRC Vrijenhoek2002Evolution and Biogeography of Deep-Sea Vent and Seep Invertebrates.Science29512531257