Several species of monoplacophorans have been observed and photographed alive, usually when they were collected attached to a polymetallic nodule or other object (Urgorri et al. 2005; Wilson et al. 2009; Wiklund et al. 2017). The Neopilina sp. in American Samoa were found attached to continuous bedrock, so would never have been collected by conventional grab sampling, and confounded the effort in this study to collect one via the ROV. The present new record expands the diversity of living monoplacophorans, but fits within the known geographical range, bathymetry, and body size for the group. This contribution adds a record of the animals in situ, and observations of the soft parts without the effects of pressure and temperature changes associated with collecting the specimens to the sea surface. The trackways indicate a potentially much larger local population.
Comparisons with other living monoplacophorans
Living monoplacophoran species are mostly small, at most 3 mm in shell length. Prior to this record, there were only six species that exceeded 10 mm. Across global monoplacophoran diversity, small species (up to about 5 mm), include a broad bathymetric range, from 180 m to over 6300 m deep; the Antarctic species Laevipilina antarctica has a broad eurybathic distribution from 210 to 3136 m (Schrödl et al. 2006). The largest species (over 10 mm) are restricted to abyssal depths, and all are from depths of 3000–6489 m (Haszprunar 2008). This new record for Neopilina (3760 to 3837 m) thus falls within the expected depth range for a large-bodied monoplacophoran.
The larger species of monoplacophorans are in three genera: Adenopilina (a single species from the Gulf of Aden, Arabian Sea), Vema, and Neopilina. The present record differs from Vema spp., which are from even deeper waters and have six pairs of gills rather than five. New gills are added anteriorly during ontogeny (Warén and Hain 1992), and the individual gills add new lamellae (Moskalev et al. 1983). Adult gill count appears to be fixed and has been used to differentiate these two genera (Warén and Gofas 1996).
Features of the body as well as the shell have been described for most living monoplacophorans (Ivanov and Moskalev 2007). It is not entirely clear what level of distortion is caused by processes of collection and preservation. Comparison is limited from the present video footage because of the restricted viewing angles and magnification. For example, the postoral tentacles were mostly obscured by the velum here, and similarly, Laevipilina cachuchensis had flexible velar lobes and gills that were more extended when alive than after preservation (Urgorri et al. 2005). The comprehensive descriptions of N. galathaea mentioned concern about preservational distortion of the gills, and those authors restricted their gill observations to a specimen where shell breakage protected the gill lamellae from compaction by sediment (Lemche and Wingstrand 1957). The unusually long and gracile gills on this new Neopilina sp. are strikingly different even from other species that have been figured from live photographs (e.g. Urgorri et al. 2005), but all previous observations of soft parts were at the surface after collection. Although long and clearly visible, the gills of this Neopilina sp. did not move during the available video. This is in contrast to a vibrating motion reported from aquarium observations of Laevipilina hyalina (Lowenstam 1978). Those historical experiments likely caused unusual stress to the animals, including overheating by incandescent lighting, and the same movement was not reported in later aquarium observations of the same species (Wilson et al. 2009). At cold temperatures of the deep seafloor (monoplacophorans observed in American Samoa living in 1.5 °C water), ectothermic animals are expected to move slowly.
The first underwater photograph of a living monoplacophoran, and still the deepest live observation, was an image of a trail and associated shell (Menzies et al. 1959). Those authors described deep, straight, furrow-like tracks attributed to monoplacophorans, photographed at 5821-m depth. When the animal is attached to the substratum, a monoplacophoran is very difficult to distinguish from a gastropod limpet. Interestingly, there is one substantial behavioural difference that evidentially separates monoplacophorans from at least patellacean limpets. Patellogastropod limpets will not traverse even a fine layer of soft sediment or sand and will only move across a bare hard bottom (Lindberg and Pearse 1990; D.R. Lindberg, pers. comm.; the authors, unpub. obs.). This may or may not extend to other limpet-like gastropods, but the Neopilina sp. were traversing a silt layer overlying a hard bottom, where a patellacean limpet would not crawl, and other monoplacophoran species move freely in soft sediment. This point may be helpful in differentiating monoplacophorans in video data.
It is not clear whether all trackways observed in our study site (‘Utu’ seamount), including at a second nearby seamount (‘Leoso’), can be attributed solely to monoplacophorans. The track dimensions are comparable to the shell width of the two adult individuals we observed, and no other animals were seen that could also have contributed such trails. Additionally, two monoplacophorans were observed in association with the trails on ‘Utu’ seamount, strengthening the proposed link between the trackways and the animals. The only previous trackway attributed to a living monoplacophoran, Vema ewingi, was comparatively very straight and did not meander as in the trackways observed here, but the observation of Vema ewingi was on soft substratum and the still image was constrained to a very small range of view (Menzies et al. 1959). Here, a large area was covered in criss-crossing tracks and it was not possible to attribute a single animal to a single trackway. There may have been more monoplacophorans present, as the topology was complex and included many depressions that would obscure an animal of this size (Supplementary Video).
The putative scratch marks we observed within the cleared area of a trackway very close to one specimen have the appearance of radular scraping (Fig. 2). Monoplacophoran radulae are similar to those of chitons (Haszprunar and Ruthensteiner 2013). A previous record of potential monoplacophoran radular scratches had a different appearance, but a direct comparison may be inappropriate, as those marks were on the tissue of a xenophyophore (Tendal 1985). Several descriptions have documented the gut contents of monoplacophorans, and some species may target particular food items (Tendal 1985; Warén and Hain 1992); however, as a group, they are apparently mainly detritivores that ingest sediment (Lemche and Wingstrand 1957). At least one other species, Vema ewingi was observed with a faecal pellet that matched the surrounding sediment (Menzies et al. 1959), as we observed apparent faecal material of Neopilina sp. here with the same texture and colour as the surrounding detritus.
Monoplacophoran habitats under threat
Other species of monoplacophorans retrieved from similar abyssal depths were all associated with soft sediment or where there was no sediment description the habitat was assumed to be similar to that photographed for Vema ewingi (Menzies et al. 1959; McLean 1979). One other species was reported from ferromanganese crust at 2000 m, similar conditions to the new record here (Moskalev et al. 1983). Yet habitat is variable even at genus level; Neopilina spp. are found on clay (N. galathaea), on silt on hard bottom or boulder (N. rebainsi, and herein), and on gorgonian coral (N. starabogatovi). Monoplacophorans as a whole are found on soft sediment, hard bottoms, nodules, and biotic substrata (Ivanov and Moskalev 2007). Six species in four genera have been found living on polymetallic nodules, including the most accessible living monoplacophoran Laevipilina hyalina (Urgorri et al. 2005; Ivanov and Moskalev 2007; Wilson et al. 2009). These new records of Neopilina sp. were found on a ferromanganese-encrusted seamount. Although monoplacophorans are perceived as rare, there are hundreds of seamounts spanning similar depths (Staudigel and Koppers 2015) in the South Pacific region, which may represent suitable habitat for these molluscs.
Polymetallic crusts and nodules are of increasing interest as a target of the rapidly developing field of deep-sea mining. Monoplacophorans, a rare and enigmatic group of organisms that live at low densities and still hold the answers to some of the great evolutionary mysteries, may be at risk from future commercial exploitation of seabed mineral resources. We still know very little about the biology of many deep-sea animals. Key biological questions can only be answered with access to physical specimens; however, in situ video observations are a proven tool to rapidly gain additional data and the environmental context for many elusive species.