First Record of the Mesopelagic Narcomedusan Genus Solmissus Ingesting a ﬁsh, with Notes on Morphotype Diversity in S

Home , Aeginidae, Narcomedusae, Solmissus

Plankton Benthos Res 13(2): 41–45, 2018 Plankton & Benthos Research © The Plankton Society of Japan

First record of the mesopelagic narcomedusan genus Solmissus ingesting a ﬁsh, with notes on morphotype diversity in S. incisa (Fewkes, 1886)

1,2, 1,2 Mitsuko Hidaka-Umetsu * & Dhugal J. Lindsay

1 School of Marine Bioscience, Kitasato University, Sagamihara, Kanagawa, Japan 2 Japan Agency for Marine-Earth Science and Technology (JAMSTEC), Yokosuka, Kanagawa, Japan Received 8 November 2017; Accepted 25 January 2018 Responsible Editor: Jun Nishikawa

Abstract: An individual narcomedusa assignable to Solmissus incisa sensu lato was observed having ingested a ﬁsh at 573 m depth near the southeast slope of the Kaikata seamount, Japan. Solmissus is a very common deep-sea narcomedusan genus that is widely considered to be a predator specializing on gelatinous plankton. Several cryptic species, with differences in the number of tentacles and form of manubrial pouches, are thought to be included in the nominal species Solmissus incisa. Therefore, the present study gives a short description of the morphotype of Solmissus incisa s.l. observed with a ﬁsh in its stomach, as well as several individuals of the same morphotype that had ingested gelatinous prey.

Key words: Izu-Ogasawara Islands, mesopelagic, piscivorous, Solmissus incisa, stomach contents

Introduction Materials and Methods The common midwater narcomedusan genus Solmissus ROV Hyper-Dolphin video footage from a Super-HARP is widely regarded to be a predator specializing on ge- high-definition video camera (Lindsay 2003) were ana- latinous zooplankton prey (e.g. Raskoff 2002). The feed- lyzed for Dive 81 (Southeast slope of Kaikata Seamount, ing behaviour and stomach contents of 82 individuals of launched at 26°42.168′N, 141°06.425′E on 7 March 2002) Solmissus were reported by Raskoff (2002), based on ROV and Dive 83 (Northeast slope of Sumisu Caldera, launched observations in the Monterey Bay, California, and that at 31°29.070′N, 140°09.198′E on 9 March 2002). Physico- study found that 88.6% of prey items were gelatinous zoo- chemical data were collected using a SeaBird SBE19 CTD plankton, with not a single fish ingested and with the small (Conductivity, Temperature and Depth profiling system) number of non-gelatinous prey presumed to be bycatch and an SBE13 oxygen sensor attached to the vehicle on from the stomach contents of ingested gelatinous preda- all dives. Depth, temperature, salinity and dissolved oxy- tors. gen were correlated to the presence of a given animal by During cruise KY02-03 of the R/V Kaiyo to the Izu- matching the time on the CTD series to the timecode on Ogasawara Island chain from 18 February–13 March 2002, video. The original BCT-124HDL HDCAM tapes (1080i, the Remotely Operated Vehicle (ROV) Hyper-Dolphin re- 29.97 fps) were digitized using an AJA Ki Pro (Apple corded several Solmissus ingesting gelatinous prey such ProRes 4:2:2 codec, QuickTime .mov container). Still im- as salps and a narcomedusa, but also an individual that ages of 1920×1080 pixels were captured using Quicktime had ingested a fish. Herein we report, for the first time, an Pro 7.6.6 by copying the frame at native resolution and observation of piscivory by the mesopelagic narcomedusan pasting into an Adobe Photoshop CC (Ver. 2015) docu- genus Solmissus, along with observations of feeding on ge- ment, before applying auto tone, auto contrast, and auto latinous zooplankton by two other individuals of Solmissus color on the default values and saving as TIFF format. incisa s.l., with notes on their morphology. Information on the individuals treated in the present study and their file names is presented in Table 1.

* Corresponding author: Dhugal Lindsay; E-mail, [email protected] 42 M. Hidaka-Umetsu & D. J. Lindsay

Table 1. Solmissus incisa s.l. “white socks” individuals observed with material in their guts during the present study. Solmissus incisa morphotype “White Socks” Individual 1 Individual 2 Individual 3 Bell shape Disk-like, concave Disk-like, concave Disk-like, concave Height of bell/bell diameter 0.15 0.17 0.13 Number of tentacles 24 22 24 Tentacle length/bell diameter 1.26 1.45 1.10 Colour of tentacles tipped with white tipped with white tipped with white White portion/tentacle length 31–35% 24–39% 28–41% Shape of stomach pouches Pentagonal Pentagonal Pentagonal length of stomach pouch/bell diameter 0.20 0.23 0.14 stomach pouch length /width at widest point 1.25 1.30 ̶ stomach pouch length /width at base 1.66 2.16 ̶ width at base/space between 7.0 3.5 ̶ adjacent stomach pouches Bell height: lappet length: velum length 10 : 7.5 : 7.5 10 : 10 : 7.5 11.3 : 10 : 7.5 Gonads globular, opposed pairs globular, opposed pairs globular, opposed pairs Depth 573 m 614 m 619 m Dive Locality Kaikata Seamount Outside the Sumisu Caldera Outside the Sumisu Caldera Date March 7, 2002 March 9, 2002 March 9, 2002 Latitude, Longitude 26.70 N, 141.11 E 31.48 N, 140.15 E 31.48 N, 140.15 E Temperature 9.71°C 9.64°C 9.54°C Salinity 34.27 34.32 34.33 Oxygen 3.3 mL/L 2.7 mL/L 2.7 mL/L Filename HPD0081-20020307-115539- HPD0083-20020309-151503- HPD0083-20020309-151122- SHHD-Front-1920x1080_ SHHD-Front-1920x1080_ SHHD-Front-1920x1080_ HDCAM-1of3-TC115553916 HDCAM-1of2-TC15150316 HDCAM-1of2-TC15112201 to120221320DF-NoImpose- to15184114DF-Noimpose- to15144910DF-Noimpose- Solmissus_incisa_s.l.-Mitsuko_ Solmissus_incisa_s.l.-Mitsuko_ Solmissus_incisa_s.l.-Mitsuko_ Hidaka-KAPPAKURAGE- Hidaka-KAPPAKURAGE- Hidaka-KAPPAKURAGE- eating_ﬁsh_573m_24T.mov eating_salp_614m_22T_SS1. eating_Narco_619m_24T_ mov SS1.mov

four marginal tentacles with distal quarter to two fifths of Results much stronger whitish colour than proximal length, presumably caused by very high concentrations of nemato- Solmissus Haeckel, 1879 cysts. Gonads with a single egg, thereby being spherical Diagnosis or oval in shape when mature, in 2–4 oppositional pairs, Narcomedusae with perradial and undivided stomach placed opposite each other on the margins of each perra- pouches; with tentacles leaving umbrella opposite centre of dial manubrial pouch. each stomach pouch, equal in number to that of pouches; pouches not extending beyond points of origin of tentacles; Comments without peripheral canal system; without otoporpae. The stomach contents of these individuals were a fish belonging to the Order Stomiiformes [Maurolicinae or Description of present material (n=3) Phosichthyidae] (Fig. 1A, B), salps (Fig. 1C–E) and a nar- Solmissus incisa s.l. of 22–24 tentacles type (S. incisa comedusa (Fig. 1F), which were completely ingested. The T22–24) with flattened, disc-like exumbrella, concave at salps were not identifiable to a lower taxa, but it is highly apex. Mesoglea fairly thick but transparent and relatively possible that they were the blastozooids of Salpa sp. (J. soft. No visible nematocyst patches on surface of exum- Nishikawa, personal communication). The ingested narco- brella. Velum well-developed. Manubrium large, circular. medusa was one-third of the diameter of the Solmissus Twenty-two to twenty-four perradial manubrial pouches of individual that had ingested it, and had a rigid, biconvex rectangular to pentagonal shape. Twenty-two to twenty- umbrella of a width 3.3 times as wide as high. It had thick Solmissus also ingests fish 43

Fig. 1. Solmissus incisa T22–24 individuals with their stomach contents. Individual 1 with 24 tentacles observed at 573 m with an ingested fish (A) with a close-up of the stomach contents (B). Individual 2 with 22 tentacles observed at 614 m with ingested salps (C) with a close-up of the stomach contents and manubrial pouches (D) and in lateral view (E). Individual 3 with 24 tentacles observed at 619 m with an ingested narcomedusa (F). gelatinous swellings where the stomach pouches must have Discussion been situated before they were digested, and had 10 tentacles. Apart from the lower tentacle number it resembled Currently the genus Solmissus comprises six species, Solmissus marshalli Agassiz & Mayer, 1902 very closely. with three species [S. albescens (Gegenbaur, 1857), S. in- 44 M. Hidaka-Umetsu & D. J. Lindsay cisa (Fewkes, 1886) and S. marshalli] being widely accept- have small clusters of nematocysts on their exumbrellar ed and a further two [S. faberi Haeckel, 1879, S. bleekii surface” though Kramp (1957) explicitly states that the ex- Haeckel, 1879] generally considered doubtful. Solmissus umbrella of the former is smooth. The medusa in Raskoff's atlantica Zamponi, 1983 has been determined not to be a (2002) Fig. 2A has obvious nematocyst patches on the sur- valid species by Genzano et al. (2008), rather being pro- face of the exumbrella but the morphology of the stomach visionally assignable to the Aeginidae sensu lato and the pouches and bell shape are not reminiscent of S. marshalli, present authors concur. The description of S. albescens presumably indicating he considered it a small specimen has been emended by Gili et al. (1998), but the taxonomy of S. incisa s.l. The medusa in Raskoff's (2002) Fig. 3A–E of the remaining species is a quagmire of confusion. The seems to have both 16 tentacles and a thick and rigid ex- species S. marshalli was described based on a single indi- umbrella, suggesting that it is indeed S. marshalli, and vidual with a thick and rigid bell of 60 mm diameter and although the resolution is sub-optimal it does appear that a tentacle/stomach pouch number of 14 (Agassiz & Mayer there may be nematocyst patches scattered over the bell 1902). The widths of the distal portions of the stomach margin. In any case, until a thorough revision of the ge- pouches were figured to be 2–3 times as wide as the wid- nus is undertaken it seems prudent that photographs and/or est spaces between the pouches and the length of each descriptions of the material in question be provided when stomach pouch to be 1.3–1.6 times as long as its width at reporting on the ecology of Solmissus species, as has been its widest (Plate 5, Fig. 24 in Agassiz & Mayer 1902). The attempted in the present paper. maximum number of tentacles for this species has usu- Morphologically, S. incisa T22–24 could possibly be at- ally been recorded as 16 (e.g. Bigelow 1909, Toyokawa tributable to S. faberi, based on the number of tentacles/ et al. 1998, DJL personal observations). However, several manubrial pouches and the rectangular to pentagonal per- records in the literature refer to medusae with more than radial manubrial pouches, although these pouches were not 16 tentacles (e.g. Kramp 1957, Mills & Goy 1988). Sol- split at their distal ends. The whitish colour of the distal missus incisa has been suggested to be a species complex portion of the tentacles and, when mature, the form and of several cryptic species (Toyokawa et al. 1998, Lindsay placement of the gonadal tissue, seem to be stable and et al. 2015, Licandro et al. 2017) and indeed the original recurring morphological traits for this morphotype of S. description was based on an amalgamation of several bro- incisa s.l., referred to in the JAMSTEC HQ video database ken medusae from more than one station (all around 39°N, as “Solmissus white socks”. Recent reports on in situ ROV 79°W) and with tentacle numbers ranging between 24–32 observations of Solmissus species have introduced at least (Fewkes 1886) and bell diameters from 50–100 mm, sug- two morphotypes of Solmissus incisa, as shown in Lindsay gesting more than one species may well have been con- et al. (2015) in Fig.51.27 where a.b. has 23 tentacles and tained in the original material. Haeckel (1879) had already rectangular manubrial pouches, while c.d. has 32 tentacles described, seven years previously, three Solmissus species and oval manubrial pouches. The former morphotype, al- with 12 (S. ephesius), 24 (S. faberi) and 32 (S. bleekii) ten- though still lacking mature gonads, seems to be the mor- tacles, respectively. Solmissus bleekii, from the Atlantic photype we refer to as “S. incisa T22–24 (white socks)” in coast of South Africa, with 32 tentacles and long, narrow the present report. stomach pouches that are twice as long as they are wide Three kinds of stomach contents were observed: fish, (Haeckel 1879), could very well be one of the cryptic spe- salps, and a narcomedusa (Fig. 1A–F). Feeding behavior cies contained within the S. incisa species complex. Based and stomach contents of Solmissus spp. have been report- on tentacle number, one could also assume the same might ed in detail by Mills & Goy (1988) and Raskoff (2002). apply to S. faberi, a species described from the south-west- These previous studies suggested that Solmissus spp. are ern Atlantic (32°S, 26°W), but the heart-shaped form of primarily, if not exclusively, predators on other gelatinous the stomach pouches, which are split into two sub-pockets zooplankton, and suggested that Solmissus spp. are able at the tentacle insertion point (Haeckel 1879), bring this to capture relatively fast-moving, large prey due to their assertion into doubt. Solmissus ephesius (Mediterranean) having long, spined tubules in their nematocysts (apotri- was synonymized with S. albescens by Kramp (1957). Re- chous isorhizas). The present study indicates either that at cent taxonomic work on another group of narcomedusae least one type of Solmissus can capture and ingest fish as has shown that one should not be too hasty to synonymize well as gelatinous prey or that fish may be ingested as by- poorly-known taxa and collections from the type localities catch through predation on piscivorous pelagic cnidarians. of all the above species is recommended (Lindsay et al. Apotrichous isorhizas are a nematocyst type unique to nar- 2017). comedusae, and these were described as being distributed Mills & Goy (1988) gave a valuable report on the in situ mostly on the upper side of the tentacles in Solmissus spp. behaviour of S. marshalli but the medusa in their Fig. 3d (Mills & Goy 1988). However, the present morphotype appears to be S. incisa s.l., based on the higher number of of S. incisa s.l. appears to have nematocysts on all faces tentacles and general morphology. Raskoff (2002) in his of the distal ends of the tentacles, suggesting its foraging study of behaviour and diet in Solmissus stated that “all strategy may differ from the “stealth” strategy described sizes of S. marshalli and small specimens of S. incisa also by Raskoff (2002). Solmissus spp. are very common and Solmissus also ingests fish 45 ubiquitous in the deep sea, presumably playing an impor- daria: Hydrozoa) from the temperate southwestern Atlantic tant role in the midwater ecosystem. In order to correctly Ocean: a review. Zootaxa 1750: 1–18. assess the ecological role of the various Solmissus mor- Gili J-M, Bouillon J, Pagès F, Palanques A, Puig P, Heussner S photypes it is imperative that the taxonomy of the genus be (1998) Origin and biogeography of deep-water Mediterranean addressed to allow the correct names to be assigned to the hydromedusae including the description of two new species species observed with in situ survey tools such as ROVs. collected in submarine canyons of Northwestern Mediterra- nean. Scientia Marina 62: 113–134. Haeckel E (1879) Das System der Medusen. Erster Theil einer Acknowledgements Monographie der Medusen. Denkschriften der Medicinisch- Naturwissenschaftlichen Gesellschaft zu Jena 1: 1–360. (in We are grateful to Dr. Kevin Raskoff and an anonymous German) reviewer for their critical and constructive comments on Kramp PL (1957) Hydromedusae of the Discovery Collections. the manuscript. We sincerely thank the captain and crew of ‘Discovery’ Rep, Vol. 29, pp. 1–128, text-figs. 1–19, Pl. i–vii. the R/V Kaiyo as well as the operations team of the ROV Licandro P, Fischer A, Lindsay DJ (2017) Cnidaria: Scyphozoa Hyper-Dolphin for their dedicated efforts. We also thank and non-colonial Hydrozoa. In: Marine Plankton: A Practical Dr. Hiroyuki Yamamoto of the Environmental Impact As- Guide to Ecology, Methodology, and Taxonomy (eds Castel- sessment Research Group, within the Research and De- lani C, Edwards M). ISBN 978-0-19-923326-7, Oxford Uni- velopment Center for Submarine Resources, JAMSTEC, versity Press, New York, pp. 198–231. DOI: 10.1093/acpro for his support. This study is a contribution to the Deep f:oso/9780199233267.001.0001 Ocean Stewardship Initiative (DOSI). This study was par- Lindsay DJ (2003) Bioluminescence in the mesopelagic realm. tially supported by grants-in-aid by KAKENHI from the Kaiyo Monthly, Spec Ed 35(9): 606–612. Japan Society of the Promotion of Science (Nos. 24248032, Lindsay D, Umetsu M, Grossmann M, Miyake H, Yamamoto H 26304030, 23405031) and the Cross-ministerial Strategic (2015) Chapter 51, The Gelatinous Macroplankton Community Innovation Promotion Program (SIP) for the Development at the Hatoma Knoll Hydrothermal Vent. In: Subseafloor Bio- of New-generation Research Protocols for Submarine Re- sphere Linked to Hydrothermal systems: TAIGA Concept (eds sources; Core Research for Evolutional Science and Tech- Ishibashi J, Okino K, Sunamura M). ISBN 978-4-431-54864-5, nology. Springer, Tokyo, pp. 639–666. DOI: 10.1007/978-4-431-54865- 2_51 Lindsay DJ, Grossmann MM, Bentlage B, Collins AG, Min- References emizu R, Hopcroft RR, Miyake H, Hidaka-Umetsu M, Ni- Agassiz A, Mayer AG (1902) Reports on the scientific results of shikawa J. 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