The deep-sea elpidiid holothuroid, Penilpidia ludwigi, was recorded using a Remotely Operated Vehicle in the Western, Central, and Eastern Mediterranean Sea. This species, endemic to the basin, was previously captured above the seabed in sediment traps and based on these records its swimming ability was assumed. The present study reports the first in situ observations of swimming P. ludwigi and provides an update on the geographic and bathymetric distribution of this species. A large aggregation of thousands of specimens was observed in the Levantine Sea with a maximum local density 300 ind. m−2. The ROV surveys allowed observation of the behavior of the species and description of its mode of swimming. Active swimming using strokes of the tentacle crown is combined with drifting benefiting of the current, the former used for fast escape the latter mainly for energy-saving displacement. Swimming behavior allows P. ludwigi to exploit various deep-sea habitats including seamounts, canyons, and ridges inaccessible to non-swimming deposit feeders.
The deep-sea holothuroid fauna remains poorly known worldwide owing to limited accessibility of the deep seafloor, despite it being the largest habitat on the planet (Haedrich and Maunder 1985; Gebruk et al. 2013; Mecho et al. 2014). Holothuroids of the family Elpidiidae are one of the most common and ecologically important epibenthic taxa in the deep sea from the lower continental slope to the hadal zone (Hansen 1975; Gebruk 1990, 2008; Billett 1991; Tyler et al. 1996). Representatives of the elpidiid genus Penilpidia Gebruk, 1988 are usually small, generally 15–20 mm long, with a gelatinous consistency (Gebruk 1988). The genus was established to accommodate the species Penilpidia ludwigi (von Marenzeller, 1893) and Penilpidia pacifica Gebruk, 1988. In the Mediterranean Sea, the deep-sea family Elpidiidae is only represented by P. ludwigi, originally assigned to the genus Kolga Danielssen & Koren, 1879 and only recently re-described by Gebruk et al. (2013). This species, endemic to the Mediterranean Sea (Hansen 1975), was firstly found during the Pola expedition in 1891 north and northwest off Crete, at depths from 755 to 1292 m (von Marenzeller 1893). It was only recorded again a hundred years later by the Meteor 25 expedition, close to the type locality and off Egyptian coasts, with 37 specimens sampled at depths from 1006 to 4766 m (Fiege and Liao 1996). The same authors suggested that the apparent absence of this species in the western basin could be a result of inadequate sampling. In 2001, 150 specimens of P. ludwigi were reported between 1200 and 1700 m depth in the La Fonera Canyon (north-western Mediterranean) owing to accidental sampling in sediment traps (Pagès et al. 2007). Based on the occurrence of several specimens in traps deployed 22 m above the seabed, the authors hypothesized re-suspension of specimens as a result of near-bottom turbulence or a swimming behavior of these holothuroids, though never observed before. In the same area, in the Blanes Canyon, at depths between 900 and 1500 m, Mecho et al. (2014) sampled 200 specimens of P. ludwigi in sediment traps and 19 more specimens using an epibenthic sledge. Massive occurrence and aggregative behavior of this species were linked to trophic and oceanographic features. Indeed, Pagès et al. (2007) suggested that P. ludwigi was particularly abundant in traps during spring, because of the food availability linked to seasonal increase in the downward flux of organic particles. The occurrence of peaks in abundance related to seasonal influx and phytodetritus accumulation on the seafloor is a well-known phenomenon in other deep-sea holothuroid species (Billett and Hansen 1982; Billett et al. 1983; Billett 1991; Roberts et al. 2000; Bett et al. 2001; Wigham et al. 2003; Gebruk et al. 2013; Hamel et al. 2019).
Based on a somatic water content of 85.3–93.9% in species of Elpidiidae (Billett 1991), Pagès et al. (2007) argued that specimens of P. ludwigi were likely to be neutrally buoyant, supporting the idea of turbulence as a lifting mechanism within the water column followed by re-suspension. Once lifted, specimens apparently drifted with currents. This mechanism could explain their wide dispersal and the occurrence of aggregations. Swimming behavior of P. ludwigi was also contemplated, albeit not being considered as likely as re-suspension because of the small size of specimens (5–20 mm in length), more similar to small non-swimming Elasipodida than to swimming Elpidiidae (Pagès et al. 2007). Moreover, it was thought that P. ludwigi did not swim due to the lack of adaptations for swimming, such as brims (formed by fused tube feet), a frontal lobe, enlarged oral tentacles, and/or an antero-dorsal velum (Rogacheva et al. 2012; Gebruk et al. 2013). The lobe, formed by enlarged tentacles, allows other Elpidiidae to swim, as for example in species of the genus Peniagone Théel, 1882 (Rogacheva et al. 2012). Similarly, Pelagothuriidae such as Enypniastes eximia Théel, 1882 use the frontal lobe to actively swim (Ohta 1985; Pawson and Foell 1986; Pagès et al. 2007). Shirayama et al. (1985) and Miller and Pawson (1990) suggested that some species without a velum can swim by flexing the posterior portion of the body with a rhythmic pulsation of the anterior brim, for example Pannychia moseleyi Théel, 1882. However, P. ludwigi was not considered to be among the swimming benthopelagic holothuroids to date. Possible swimming behavior of P. ludwigi was even recently in discussion (Gebruk et al. 2013). In the present study, the occurrence of P. ludwigi in different areas of the Mediterranean Sea is reported, and the first high-definition observations of specimens in their natural environment is provided, definitely proving the active swimming ability of this species. New observations include a record of a large population of P. ludwigi of a magnitude never previously reported, recorded using a Remotely Operated Vehicle (ROV). The geographic and bathymetric distribution of P. ludwigi across the Mediterranean Sea are also reviewed and discussed.
Material and methods
Three main areas of the Mediterranean Sea were surveyed. The first one was located in the Balearic Sea, between the two main islands of Ibiza and Mallorca (Balearic Archipelago; Fig. 1), where ROV surveys were carried out on a pockmarks field close to the Oliva Bank Seamount and on the upper portion of the Emile Baudot Escarpment (Acosta et al. 2001a, 2001b; Mastrototaro et al. 2017). The former site is characterized by large pockmarks from 400 to 750 m in depth (Acosta et al. 2004), identified as a gas seepage zone by the Spanish Institute of Oceanography (IEO 2005), while the second site lies on the top of a large escarpment on the southeast side of the Balearic Promontory (Acosta et al. 2001a). Both sites are characterized by compact mud colonized by dense populations of the bamboo coral Isidella elongata (Esper 1788) (Mastrototaro et al. 2017).
The second study area stretched around the volcanic Archipelago of the Aeolian Islands, in the Tyrrhenian Sea (Fig. 1). This area includes the seven main islands of the archipelago, all steep-sided volcanoes either active or dormant, with six offshore islets. The seafloor is characterized by several volcanic outcrops, seamounts, gullies, submarine channels, and canyons down to more than 2000 m in depth (Romagnoli et al. 2013). The seabed in this area is characterized by muddy facies with I. elongata and sea pens together with scattered rocky substrates colonized by cold-water corals.
The third study area was located off Lebanon, in the Levantine Sea (Fig. 1). This last area is characterized by a narrow continental shelf, perpendicularly crossed by various canyon systems that connect coastal zones to deep-sea habitats, from approximately 50 to 1600 m deep. The seafloor in the bathyal zone is mostly covered by mud, dominated by echinoderms, large foraminifera, brachiopods, tube worms, tube-dwelling anemones, and some sea pens.
Data acquisition and analysis
Video footage and photos were obtained using a Saab Seaeye Falcon DR ROV equipped with an HDV (high-definition video) camera with Minimum Scene Illumination of 2.0 lx (F1.4), a 0.5-in. CCD (Charge-Coupled Device) pick-up device, an image sensor, and 3.8-mm spherical and wide angle lenses. The ROV also hosted a depth sensor, a compass, and two laser beams providing a 10-cm scale for measurements of frame areas and sizes of organisms. ROV transects were carried out at an average speed of 0.2–0.3 kn, and the ROV position was continuously recorded using a LinkQuest Tracklink USBL Transponder with up to 0.25° accuracy.
A total of 160 ROV dives were performed, 58 in the Balearic Archipelago, between 69 and 1004 m in depth; 51 in the Aeolian Archipelago, between 28 and 989 m in depth; and 48 off Lebanon, between depths of 36 and 1050 m. There were two transects with P. ludwigi present in the Balearic Sea, eight in the Tyrrhenian Sea, and six in the Levantine Sea (Table 1).
All observed specimens of P. ludwigi were counted and their behavior was analyzed and described (e.g., swimming, walking, drifting, feeding, etc.). Population density (specimens/m2) was estimated based on the number of specimens observed and the total area surveyed for each ROV transect (Table 1). The area surveyed was calculated considering the length of each transect, based on the ROV positioning system, and the camera objective width obtained thanks to the two laser beams. In particular, the view width was kept almost constant during the transects, around 1 m2, in order to allow the observation of the small specimens of P. ludwigi.
A total of 3676 specimens of P. ludwigi were observed, 31 in the Balearic Sea, 99 in the Tyrrhenian Sea, and 3546 in the Levantine Sea. The specimens were unpigmented and transparent with the exception of the greyish-brown digestive tract, whose color was due to the sediment contained in it. The body shape was elongated, ovoid, 3–4 times as long as wide, and dorso-ventrally flattened. The mouth was surrounded by 10 large tentacles forming a mouth tube. The posterior half of the body was seen to be bearing six pairs of free tube feet. The dorsal velum was present, consisting of two parts, each formed by two papillae fused at the base. One pair of conspicuous free dorsal papillae was developed in the posterior one third of the body (Fig. 2a–c).
Swimming behavior was observed in specimens of P. ludwigi in all study areas. Swimming was performed with consecutive phases of the tentacle crown sweeps (Fig. 2d).
Three specimens of P. ludwigi in the Levantine Sea were seen to be carrying an unidentified ectoparasite (Fig. 2e).
Distribution and aggregations
Table 2 reports a summary of all Mediterranean records of P. ludwigi, including data reported in the present study. P. ludwigi, even though recently considered a rare species in the Mediterranean Sea (Mecho et al. 2014), appears to be distributed throughout the basin (Fig. 3), at depths from 485 to 4766 m. Great bathymetric range was observed in the Aegean Sea, from 755 to 4353 m depth, and in the Balearic Sea, from 485 to 1700 m depth. In other sectors of the Mediterranean Sea, the species was found within narrower bathymetric ranges, 700 m deep in the Alboran Sea, depths from 813 to 947 m in the Tyrrhenian Sea, 3848–4766 m deep in the Ionian Sea (the deepest record so far), and 792–1006 m in depth in the Levantine Sea (Table 2).
In the Balearic Sea, 13 specimens were observed on the Emile Baudot Escarpment, at depths from 520 to 550 m, and 18 specimens in the pockmarks field close to the Oliva Bank Seamount, at 485–518 m in depth (Fig. 1). These records of P. ludwigi were the shallowest in the Mediterranean Sea, as well as the first high-definition observation of the species in its natural environment. A further 99 specimens were observed around the Aeolian Archipelago, and this was the first record of the species in the Tyrrhenian Sea. A high abundance of specimens on a large area was observed in the Levantine Sea, off Beirut (346 specimens at B1, 2 at B2, and 29 at B3) and off Sidon (757 specimens at S1 and 2403 at S2), while only a few specimens were observed off Tripoli (9 specimens at T1) (Table 1; Table 2). At S1 and S2, P. ludwigi was present with an average density throughout the transect of 1.10 and 1.85 ind. m−2, respectively. Despite being widespread along the transects, the population observed in the Levantine Sea showed a patchy distribution, with a local maximum estimated density of 300 ind. m−2 at S2 (Fig. 4). Aggregations of specimens were particularly evident between 800 and 1050 m in depth, with two peaks of density at the depth ranges of 851–900 and 1001–1050 m (Fig. 5).
Most of the observed specimens of P. ludwigi were on the seabed, slowly moving or feeding on the sediment (Fig. 2b), while only a few specimens were actively swimming when first encountered with the ROV. Swimming behavior was observed in 25.8% of specimens in the Balearic Sea, 8.1% in the Tyrrhenian Sea, and only in 1.7% in the Levantine Sea, thus with highly variable proportions across the different observations. It can be suggested that swimming is used by P. ludwigi for certain needs, such as changing feeding grounds, fast displacement, or escape. Active swimming can be coupled with drifting. In this way, this benthopelagic holothuroid benefits from currents by preserving the energy required for locomotion. Some of the swimming specimens were observed maintaining active swimming for about 1 min; then, they remained stretched horizontally and slowly drifted, sometimes moving with few strokes to maintain their altitude above the seabed or just remaining still and sinking down. Active swimming in specimens was facilitated by the tentacle crown performing regular strokes, giving the body an S-like shape in certain swimming phases (Fig. 2c–d). Most of the swimming specimens occurred within 2–3 m above the seabed, and occasionally up to 10 m.
Swimming behavior as a potential escape strategy was clearly observed in the Balearic Sea in one specimen of P. ludwigi feeding on the seabed. After the mechanical disturbance owing to a gentle touch by the tail of a small blackmouth catshark Galeus melastomus Rafinesque, 1810. The specimen of P. ludwigi defecated rapidly and propelled itself upward with rapid flexing of the lobe formed by the tentacle crown (Fig. 6a–h). The rapid expulsion of the feces, in 1.4 s from the moment of disturbance, and the concomitant contraction of the anterior part of the body brought the specimen into a vertical position, suitable to lift off (Fig. 6c). Vertical lift until about 40 cm above the seabed was then achieved through powerful strokes of the tentacle crown (Fig. 6e–f). During the downward motion of the anterior end of the body, the oral tentacles were expanded to provide a greater surface area for upward lift, while they were relaxed and passively folded together when the anterior body end moved upwards. The specimen was able to move about 2 m away from the disturbance point in just 25 s of powerful strokes; then, active swimming ceased and the specimen acquired a horizontal position (Fig. 6g). Thereafter, it started passively and slowly drifting and descending towards the seabed. After touching the seabed, the specimen started walking and feeding again (Fig. 6h). A similar reaction was observed in the Levantine Sea, where two specimens of P. ludwigi were feeding on the seabed when two hermit crabs, Pagurus alatus Fabricius, 1775, met and start fighting (Fig. 6i–n). The two specimens of P. ludwigi soon swam away, while the epibiont Actiniaria Hormathia alba Andrès, 1880 settled on the hermit crab shells and closed their polyps. The fighting of the two P. alatus raised a sediment cloud that prevented to see any contact or direct disturbance, and consequently to estimate the time of reaction of P. ludwigi.
On the seabed, all the specimens of P. ludwigi held the same position, with body parallel to the seafloor, the tentacle tube more or less vertical, and the oral tentacles held in contact with the substratum. No specimens were observed feeding in the water column, confirming that P. ludwigi only feeds on the seabed, using oral tentacles to collect detrital material from the sediment.
Deep-sea holothuroids have received considerable attention in the Pacific and in the Atlantic Oceans. Many species records have been made in the northeast Atlantic (e.g., Hansen 1975; Gebruk 1990; Billett 1991; Madsen and Hansen 1994) and on the Mid-Atlantic Ridge (Gebruk 2008; Rogacheva et al. 2012, 2013), while in the Mediterranean Sea very few records have occurred to date. However, the use of ROVs significantly increases the amount of data on deep-sea species occurrences and behavior, allowing observations in the natural environment even for rare or uncommon species (e.g., Aguilar et al. 2011; Angeletti et al. 2014; Mastrototaro et al. 2016; Chimienti et al. 2018a, 2018b; Knittweis et al. 2019). Given the soft-body, gelatinous consistence of elasipodids, visual methods of study of these important representatives of deep-sea communities are much more effective, as well as being less invasive compared to traditional sampling by grabs and dredges (Rogacheva et al. 2013).
Our in situ observations of P. ludwigi revealed an important morphological character in this species—the anterior dorsal velum. This feature is common in many other elpidiids, and it was also shown for the congeneric species, Penilpidia desbarresi Gebruk, Rogacheva & Pawson, 2013. However, in P. ludwigi, this feature was not known: it was lacking in the original description (von Marenzeller 1893) and was not developed in specimens used for re-description of this species, because they were juveniles (Gebruk et al. 2013). Thus, the morphology of Penilpidia appears not to be as “primitive” as considered before: the dorsal velum is a feature of morphologically advanced elpidiid holothuroids (Gebruk 1994). As suggested by Rogacheva et al. (2013), the function of this organ is that of balancing the body near the seafloor using near-bottom currents.
Distribution and aggregations
The present study demonstrates the wide geographic and bathymetric distribution of P. ludwigi throughout the Mediterranean Sea and reports for the first time the occurrence of this species in the Central Mediterranean Sea. Despite being considered a rare species, the high number of observations in the present study suggests that new records may occur in the future in other areas of the basin. Our shallow records of P. ludwigi in the Balearic Sea have expanded the known bathymetric range of this species, shifting the upper depth limit from 700 to 485 m, with the deepest occurrence at 4766 m in depth.
Despite being present from the westernmost Alboran Sea to the easternmost Levantine Sea (Fig. 3), forming occasional massive aggregations, records of P. ludwigi are still occasional. For example, this species has been observed only once in areas subject to several deep-sea visual explorations in the last 20 years, such as the Alboran cold-water coral province and the Balearic canyons and seamounts (Lastras et al. 2016; Mastrototaro et al. 2017; Chimienti et al. 2019). Furthermore, this deep-sea elpidiid has never been documented in other highly explored areas of the basin, such as the cold-water coral provinces of the Gulf of Lion, Santa Maria di Leuca, and Bari Canyon (Chimienti et al. 2018c).
The observation of large aggregations of P. ludwigi off Lebanon adds new information to the question about the ecological importance of this species. Large aggregations were previously recorded by Pagès et al. (2007) and Mecho et al. (2014), both using sediment traps deployed in a wide area off Catalonia (Fig. 3; Table 2). These authors reported 150 and 200 specimens, respectively, but these accidental samplings did not allow density estimations. Our in situ observation of a high number of specimens in the Levantine Sea over a known area allowed the first quantitative estimation of high abundance of P. ludwigi.
Information about the causes of massive aggregations of deep-sea species is still fragmentary and incomplete. The seafloor topography is considered as one of the factors driving aggregations, because canyons, trenches, and other depressions trap organic matter attracting deposit-feeding holothuroids (Gebruk et al. 2013). In fact, high densities of elpidiid holothuroids are characteristic of canyon systems worldwide (Rowe 1971; Pagès et al. 2007; Mecho et al. 2014). However, they are not exclusive to seafloor depressions; thus, the large aggregation of P. ludwigi was recorded off Lebanon on a more or less gentle slope at depths between 800 and 950 m (Fig. 4). Similarly, a high density of the related species, P. desbarresi, with 50 ind. m−2 was recorded at 525 m on the slope of southwestern Newfoundland (Gebruk et al. 2013).
Pagès et al. (2007) hypothesized coupling between aggregations of P. ludwigi and increased fluxes of organic matter related to seasonal high primary production. This general relationship between massive aggregations and food availability has also been suggested for other deep-sea holothuroids in the north-eastern Atlantic Ocean, such as Kolga hyalina Danielssen & Koren, 1879, Benthogone rosea Koehler, 1895, and Amperima rosea E. Perrier, 1886 (Danielssen and Koren 1879; Billett and Hansen 1982; Billett et al. 1983; Wigham et al. 2003). The dense aggregation reported in the present study in the Levantine Sea occurred in autumn and was related to the peak of chlorophyll-a and colored dissolved organic matter (CDOM) in the area (El Hourany et al. 2017). Our records are in agreement with aggregative behavior of small elpidiid holothuroids in areas of accumulation of organic matter on the seafloor (Gebruk 1990; Billett 1991; Roberts et al. 2000; Gebruk et al. 2013).
P. ludwigi appears to be a powerful and active swimmer; thus, the question of swimming ability in this species (Gebruk et al. 2013) is now clarified. In the present study, this elpidiid was commonly observed swimming when first encountered; therefore, it can be considered as a “frequent swimmer” (i.e., species which often swims, but spends most of its time on the seafloor) according to categories in Rogacheva et al. (2012).
Deep-sea swimming holothuroids have been reported many times since the first observation of swimming behavior in Bathyplotes natans M. Sars, 1868 by Sars (1867). Different phases of swimming have been described in many species (Barnes et al. 1976; Pawson and Foell 1986; Gebruk 1990; Miller and Pawson 1990; Rogacheva et al. 2012). As for P. ludwigi, usually, it is a combination of body flexing movements, using the velum, swimming lobes, and/or other morphological structures. According to our new observations, P. ludwigi swims actively using expanded oral tentacles forming a swimming lobe. Often this is the most powerful and effective locomotory organ in swimming holothuroids (Rogacheva et al. 2013). On the contrary, some non-swimming holothuroids can perform different strategies to modify their buoyancy, such as inflating water, changing their body shape, and being able to tumble or float at speeds significantly faster than through benthic crawling, being carried away passively (Hamel et al. 2019).
The orientation of P. ludwigi in the water column can change rapidly depending on the phase of swimming, as shown by Rogacheva et al. (2012) for other benthopelagic holothuroids. As in other swimming holothuroids, P. ludwigi empties the intestine before taking off from the seafloor, as a mechanism to “drop off the weight” (Rogacheva et al. 2013). However, a powerful active movement is required to take off since specimens possess little negative buoyancy even with empty guts.
Drifting occurred only for a few seconds between two swimming strokes, or before landing on the seafloor. Landing was slow by means of parachuting with stretched body, tentacles, and tube feet, or fast due to body contraction that decreased buoyancy. According to our observations, active swimming in P. ludwigi is more common than drifting, or it is coupled with it for energy-saving displacements using currents. As in other deep-sea swimming holothuroids, this behavior increases the area that can be exploited for feeding especially in an environment characterized by low supply of organic matter, patchily distributed and intermittently arriving on the seafloor (Rogacheva et al. 2012). P. ludwigi likely takes advantage of swimming to reach habitats inaccessible to non-swimming deposit feeders in topographically diverse deep-sea environments, such as ridges, slopes, canyon flanks, and seamounts. Our observations also demonstrate that the swimming behavior can help holothuroids in responding to physical disturbances, such as mechanical contact with potentially dangerous organisms, while they feed on the seabed.
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This study was funded by the MAVA Fondation pour la Nature, IF International Foundation, Smile-Wave Fund, Pictet Charitable Foundation, Adessium Foundation, Robertson Foundation, the Foundation for the Third Millennium, Fundación Biodiversidad, Spanish Ministerio de Agricultura, Alimentación y Medio Ambiente, and National Geographic (Grant EC-176R-18).
Conflict of interests
The authors declare that they have no conflict of interest.
No animal testing was performed during this study.
Sampling and field studies
All necessary permits for sampling and observational field studies have been obtained by the authors from the competent authorities. The study is compliant with CBD and Nagoya protocols.
The datasets generated during and/or analyzed for the current study are available from the corresponding author upon request.
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Communicated by S. Stöhr
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Chimienti, G., Aguilar, R., Gebruk, A.V. et al. Distribution and swimming ability of the deep-sea holothuroid Penilpidia ludwigi (Holothuroidea: Elasipodida: Elpidiidae). Mar Biodiv 49, 2369–2380 (2019). https://doi.org/10.1007/s12526-019-00973-9
- Sea cucumber
- Mediterranean Sea