INTRODUCTION

Deepstaria enigmatica was first described as a “remarkable new scyphomedusan” and its species name “enigmatica” was based on its puzzling systematic position between Semaeostomeae and Rhizostomeae (Russell, 1967). The genus Deepstaria currently comprises two species, D. enigmatica (Russell, 1967) and D. reticulum (Larson et al., 1988). Members of Deepstaria are characterized by a lack of tentacles, an extensive, thin membranelike umbrella, and long oral arms. Deepstaria enigmatica was described by Russell (1967) from a 50 cm diameter male specimen (gonads located at the proximal ends of fan-shaped mesenteries, which continue distally into the oral arms) collected at 723 m in the San Diego Trough. This partial specimen, of what first appeared as “a large collapsed and puckered, gelatinous bag with a few tentacles streaming from it,” was collected by Eric C. Barham, George Pickwell, and Ronald Church on October 21, 1966 using the U.S. Navy deep submersible DEEPSTAR 4000 (Barham, 1969). DEEPSTAR 4000 was a three-person submarine in service from 1965–1972 with an operational depth of 4000 feet and designed by the Westinghouse Corporation in collaboration with Jacques Cousteau and based on the DIVING SAUCER (Merrifield, 1969). A suction sampler was used to obtain the incomplete specimen, as the individual D. enigmatica was so large it needed to be taken to the surface with part of it still extending from the suction funnel. Much of the existing information about D. enigmatica is from this specimen (now in the British Museum of Natural History, BMNH 1967.5.24.1).

Members of Deepstaria display unique behaviors compared to other scyphozoan species, such as peristaltic locomotion and pursing of the bell margin. Larson et al. (1988) hypothesized that the peristaltic locomotion was necessary because the umbrella is too thin and the subumbrella musculature too diffuse to support more rapid pulsation (Larson et al., 1988). Lacking tentacles, D. enigmatica feeds in a novel fashion by encapsulating its prey within its entire gelatinous umbrella. D. enigmatica's bell is remarkably thin, broad, and delicate, and is easily deformed by the flow of water created by the thrusters of submersibles and ROVs. This trait has contributed to the rarity of observations and collections, as midwater trawls easily shred them.

Gelatinous macroplankton including cnidarian medusae, ctenophores, and pelagic tunicates are becoming increasing recognized as key ecosystem consumers of energy and nutrients (Doyle et al., 2014; Graham et al., 2014). For many years this field was neglected with gelatinous zooplankton often referred to as “forgotten fauna” (Pugh, 1989). Globally, gelatinous zooplankton are now estimated to constitute a carbon biomass of 38.3 Tg C (Lucas et al., 2014) and are receiving increasing attention. Nevertheless, species of Deepstaria and other large deep-sea semaeostome scyphomedusae (30–70 cm) are still rarely observed.

MATERIALS AND METHODS

The observations we report on took place aboard the exploration vessel (E/V) Nautilus (leg NA092) and the Deepstaria enigmatica specimen was encountered on November 15, 2017, off San Benedicto Island, Mexico (19.2′ N, 110.77′ W) via the remotely operated vehicle (ROV) Hercules.

FIGURE 1.

Canon ME20F-SH configuration showing A, backside, B, frontside, and C, mounted to the front of ROV Hercules.

For deep-sea imaging, we configured a polished VITRO VEX 13″ Deep Sea Sphere (Nautilus Marine Service) to house a high-definition/low-light camera with an ISO of 4,560,000 (Canon ME20F-SH) (fig. 1). The camera was equipped with a Canon EF 24 mm f/1.4L II USM lens. The camera and lens settings were controlled live from the ship via a remote controller (Canon RC-V100). All video and control signals were transmitted using a fiber optic multiplexer (Moog Focal 914 HDE).

The midwater Deepstaria enigmatica was filmed on dive no. H1666 at 974 m for 9 min 49 sec using the Canon ME20F-SH camera system described above. Scaling lasers (DeepSea Power & Light) placed 10 cm apart were used to obtain information on the size of the individual (fig. 2). The Deepstaria (jelly fall, either D. enigmatica or D. reticulum) was filmed on dive H1664 at 899 m among a dense assemblage of sponges and corals on a pillow basalt outcrop just below the oxygen minimum zone east of Socorro Island. Videos from Dive H1664 were obtained using an Insite Pacific Zeus Plus HD video camera outfitted with an Ikegami HDL-45A head and Fujinon HA 10 × 5.2 lens.

RESULTS

The encounter with D. enigmatica lasted 9 minutes and 49 seconds (see Video 1, available at  https://doi.org/10.5531/sd.sp.32). The specimen was observed while testing a new color low-light camera system (Canon ME20F-SH) with dimmable LED lighting (SeaLite 2000, DeepSea Power & Light) mounted on the ROV Hercules. The lights were set at their lowest setting (∼274 lumens), a lighting regime <0.04% of the high-power setting (∼76,000 lumens) often used on ROV Hercules. The combined sensitivity of the camera sensor (ISO 4,560,000) and the minimized light disturbance enabled the visualization of bioluminescence from Tomopteris sp. swimming alongside D. enigmatica (fig. 3; see also Video 2, available at  https://doi.org/10.5531/sd.sp.32). While bioluminescence is a common feature in the deep sea, this feature is not captured using standard ROV lighting and HD cameras.

FIGURE 2.

Screenshot taken from video of Deepstaria enigmatica recorded at 974 m, showing the 10 cm spacing of lasers.

In D. enigmatica, we observed that the peristaltic wave is related to the closing of the mouth of the bell, which takes place in <3 sec. The wave begins at the bottom of the organism at a rate of approximately 1.5 cm/sec and then forms a bulge in the center (fig. 4). This bulge persists for the duration of the time that the bell margin is closed (fig. 5A). As D. enigmatica lacks tentacles, this process could be used as a mode of upward propulsion, as well as the mechanism by which it entraps prey. However, it was necessary to move the ROV only ∼1 m upward in the water column directly following the closing sequence. Once the umbrella is closed, there remains only a small circular opening (∼10 cm) that does not open upon disturbance (fig. 6). The specimen of D. enigmatica filmed bumped into the dome of our camera and afforded the opportunity of a close-up of its anastomosing canals (fig. 5B).

FIGURE 3.

Deepstaria enigmatica (below) with a blue-emitting bioluminescent Tomopteris sp. (above).

In a nearby benthic area at a depth of 899 m, we came across a Deepstaria sp. (D. enigmatica or D. reticulum, specific ID not possible from video) carcass (fig. 7). This was among a dense assemblage of sponges and corals on a pillow basalt outcrop just below the oxygen minimum zone east of Socorro Island. The carcass (“jelly fall”) was being consumed by several larger lithodid crabs (Paralomis sp.) (fig. 7) and caridean shrimp (density of >80 individuals/m²).

DISCUSSION

Whereas Deepstaria enigmatica has been known for almost half a century and is one of the larger deep-sea predators, it remains largely unstudied. Its biology, behavior, distribution, and abundance remain relatively unknown. There are partial specimens in museum collections, and DNA sequences for three ribosomal RNA genes are deposited in the National Center for Biotechnology Information ( https://www.ncbi.nlm.nih.gov/nuccore/?term=deepstaria). Scyphomedusae diversity is currently at ∼400 described species and it is estimated that at least 400 additional species await description (Gómez Daglio and Dawson, 2017).

Larson (1986) placed D. enigmatica in the semaeostome family Ulmaridae (Haeckel, 1879) because of the presence of semaeostome-like oral arms and a gastrovascular system consisting of canals. Members of Deepstaria are unusual among jellyfish in possessing a distinct, highly branched network of anastomosing canal systems distributed uniformly over the bell and resembling wire netting. This network is the animals digestive tract and is characteristic of several Ulmaridae. Our observations provide unprecedented detail of their anastomosing canal structure and color in situ prior to any damage resulting from physical collection. Deepstaria enigmatica and D. reticulum (described by Larson, 1986) comprise the subfamily Deepstariinae. Only three Semaeostomeae genera are known to be meso-bathypelagic, Deepstaria, Poralia, and Stygiomedusa. Of these, Deepstaria is the rarest (Larson et al., 1988). Two recent phyloganic analyses both confirm Deepstaria's position in the family Ulmaridae. Somewhat surprisingly, both analyses recover the genus Aurelia, the moon jellyfish, as closely related to Deepstaria (Bayba et al., 2010; Gómez Daglio and Dawson, 2017). Aurelia, a widely studied shallow-water jellyfish, has recently been shown to exhibit life cycle reversal (He et al., 2015). It is interesting to hypothesize whether Deepstaria might exhibit a similar trait, but the rarity of encounters, compounded by the difficulty in conducting such biological studies in the deep sea, makes testing this hypothesis highly challenging.

FIGURE 4.

Time-lapse series of Deepstaria enigmatica closing, illustrating peristaltic motion.

FIGURE 5.

A, Deepstaria enigmatica in a closed/pursed position. B, Close-up image of anastomosing canals in of D. enigmatica.

FIGURE 6.

Various ventral views of Deepstaria enigmatica.

Observed Jelly Fall

The sinking of detritus from surface waters is the primary food source in the deep ocean and supports many heterotrophic benthic ecosystems. While this is mainly composed of millimeter-sized particles of “marine snow” (particles of dead plankton and fecal pellets), there are instances where large food falls such as wood (Turner, 1973), fish (Higgs et al., 2014; Soltwedel et al., 2003), and whale carcasses (Smith and Baco, 2003) occur in the deep ocean and create an intense area of organic enrichment.

A dead jelly or “jelly fall” can also be defined as a carcass that sinks through the water column, eventually causing a point-source of organic enrichment on the seafloor. Observations of gelatinous-bodied falls, including both tunicates (families Salpidae and Pyrosomatidae) and cnidarians (class Scyphozoa), are known from a global review of observations (Lebrato et al., 2012). However, owing to remineralization in the water column (Titelman et al., 2006) and rapid scavenging of a gelatinous body on the seafloor, (Sweetman et al., 2014), it is likely that the contribution of gelatinous material to organic fluxes are underestimated (Dunlop et al., 2017; Sweetman and Chapman, 2011, 2015). For example, it has been shown that dense aggregations of deep-sea scavengers (more than 1000 animals at peak densities) can rapidly assemble at jellyfish baits and consume entire jellyfish carcasses in 2.5 h (Sweetman et al., 2014).

TABLE 1.

Reports of Deepstaria encounters (updated from Larson et al., 1988).

To our knowledge, this is the first known observation of a Deepstaria jelly fall (see Video 3, available at  https://doi.org/10.5531/sd.sp.32). It was located at the lower boundary of the oxygen minimum zone (OMZ) at 899 m (O₂ = 2.98 µmoles/liter; temperature = 5.05° C). ROV observations show a number of species of caridean shrimp and several individual lithodid crabs (Paralomis sp.), actively scavenging the recently deposited carcass. We suspect this to be a recent jelly fall as the meshwork of the gastrovascular system (Russell, 1967) was still visible within the thin, translucent bell structure of the individual. Where these OMZs intercept the seafloor, strong gradients in oxygen availability and organic matter flux are observed (Devol and Hartnett, 2001; Wishner et al., 1995). Sudden pulses of organic matter can therefore be important in supporting benthic ecosystems on the seafloor regions of the OMZ. Given that members of Deepstaria are physically large animals, their relatively sparse distribution in the deep sea may represent a significant flux of detrital material to benthic scavengers. Studies from ROV videography have recently shown the significance of gelatinous predators to deep pelagic food webs (Choy et al., 2017). These in situ ROV images of a deep-sea jelly fall further highlight the importance of utilizing ROVs to make such observations and the overall role that jellies may play in the export of carbon to the deep ocean.

FIGURE 7.

Two lithodid crabs (Paralomis sp.) crabs and several caridean shrimp species surrounding carcass of Deepstaria sp. (at left and below).

Mode of Peristaltic Motion and Prey Capture

By approaching a specimen of D. enigmatica with a relatively low light intensity (274 lumens) and utilizing a low-light camera, we were able to film the organism with its umbrella open. It is not clear whether the light or ROV noise/vibrations caused the umbrella margin to purse closed. Deepstaria is hypothesized to be an ambush predator that catches upward-swimming prey (Larson et al., 1988). While there are are no direct observations of this feeding strategy, subumbrella nematocyst clusters support the hypothesis. Once the prey is enclosed within the umbrella, we show that D. enigmatica can close rapidly (<10 sec) and then open again in ∼1 min (see Video 1, available at  https://doi.org/10.5531/sd.sp.32). “Bagging” prey is not known to occur in other medusae, but has been reported in ctenophores (Harbison et al., 1978). Via analysis of videos (from Larson et al., 1988) we estimated that the peristaltic wave contraction moved at 2 cm/sec. Our observations show a similar rate, but we also note that the wave ultimately stops halfway up the organisms and stays in that pursed position until reopening (figs. 4, 5A).

At right (opposite page) a close-up of one crab feeding on the carcass shows the meshwork of the jelly's gastrovascular system.