Two sea anemones (Cnidaria: Anthozoa: Actiniaria) from the Southern Ocean with evidence of a deep-sea, polar lineage of burrowing sea anemones Author Gusmão, Luciana C. Author Rodríguez, Estefanía text Zoological Journal of the Linnean Society 2021 2021-02-18 193 1392 1415 https://doi.org/10.1093/zoolinnean/zlaa176 journal article 3130 10.1093/zoolinnean/zlaa176 f0ab84e8-4ff4-46a8-a567-a9acd016305c 0024-4082 5752621 D000BAA9-51C4-46FE-AC9B-BB361B601FA2 SCYTOPHORUS STRIATUS HERTWIG, 1882 ( FIGS 6–8 ; TABLE 2 ) Material: AMNH 5268 ( nine specimens ), Nathaniel B. Palmer R/ V , NBP11-03 Expedition , Sta. 14, off Burdwood / Namuncurá Bank , Drake Passage , Antarctica , 54º42.84’S 62º14.99’W , 732 m , 11 May 2011 , Hein Dredge , collected by M . R . Brugler . AMNH 5275 ( three specimens ), ‘ Nathaniel B. Palmer’ R/V, NBP11-03 Expedition, Deep Site – North Grassy Knoll, Sta. 10, Burdwood / Namuncurá Bank , Drake Passage , Antarctica , 54°43.35’S 62°14.21’W , 720 m , 11 May 2011 , Blake Trawl , collected by M. R . Brugler. AMNH 5254 ( 20 specimens ), Nathaniel B. Palmer R / V , NBP11-03 Expedition, Sta. 16, off Burdwood/Namuncurá Bank, Drake Passage, Antarctica , 54º48.52’S 62º07.20’W , 1423 m , 13 May 2011 , Hein Dredge, collected by M. R . Brugler. AMNH _ IZC 00361338 ( three specimens ), Nathaniel B. Palmer R / V , NBP11-03 Expedition , Sta. 22, off Burdwood / Namuncurá Bank , Drake Passage , Antarctica , 54º50.50’S 62º07.53’W , 1922 m , 14 May 2011 , Hein Dredge , collected by M. R . Brugler . Additional material examined for comparison: Scytophorus antarcticus ZMH C1452 ( one specimen : holotype ); locality: South Georgia. Halcampoides purpureus AMNH 4498 ( one specimen ); locality: Southern Ocean , Antarctica , Kapp Norvegia, Sta. PS 56/105-1, 10°57’S 12°15.05’W , GKG , giant box corer, collected in 2000 by P. López-González bi-layered cuticle on column with foreign material attached to it, p -mastigophores A in actinopharynx . Figure 7. Internal anatomy and microanatomy of Scytophorus striatus . A, micro-CT scan of longitudinal section through flattened pedal disc; note absence of basilar musculature (arrows); B, cross-section through mid-scapus showing area between furrows; note body layers and bilayered cuticle (indicated by arrow); C, histological longitudinal section through distal column showing strong, circular endodermal musculature; D, detail of distal scapus showing high muscle processes of strong, circular endodermal musculature (indicated by arrow); E, histological longitudinal section through tentacle showing ectodermal longitudinal musculature; F, micro-CT longitudinal scan through a whole specimen showing flattened pedal disc, actinopharynx, tentacles and gastrovascular cavity; note foreign material attached to epidermis of column and pedal disc; G, micro-CT scanning through distal column showing actinopharynx and two indistinct siphonoglyph (indicated by asterisks); H, cross-section through mid-scapus showing 14 macrocnemes (indicated by numbers) arranged in seven pairs; I, histological cross-section through mid-scapus showing arrangement of mesenteries in seven pairs (indicated by numbers); J, micro-CT cross-section scan through scapulus showing 14 mesenteries; K, micro-CT cross-section scan through distal scapus showing actinopharynx and weak siphonoglyphs (indicated by asterisks); note weak parietobasilar musculature of extra mesentery (indicated by arrow); L, micro-CT cross-section scan through proximal column; note all 14 mesenteries with gonads (= macrocnemes); M, detail of retractor of macrocneme with pennon distally (indicated by asterisk); N, detail of strong parietobasilar musculature of macrocneme; O, detail of macrocneme with both oocytes and spermatic cysts. Abbreviations: ac, actinopharynx; d, directive pair; ep, epidermis; ga, gastrodermis; gc, gastrovascular cavity; me, mesoglea; pd, pedal disc; t, tentacles. Scale bars: A, E, M, N, 0.2 mm ; O, 0.3 mm ; B, F, 4 mm ; C, D, 1 mm ; G–L, 2 mm . External anatomy ( Fig. 6 ): Body elongate in preserved specimens ( Fig. 6A, B ) but with aboral end flattened without a well-defined physa ( Fig. 6A–C ). Column cylindrical with 14 longitudinal furrows/evaginations ( Fig. 6B ), divided into scapulus and scapus ( Fig. 6D ) and tenaculi throughout scapus ( Fig. 6E ); column with epidermis covered by yellow cuticle distributed on scapus ( Fig. 6B, E ). Column diameter 5–11 mm distally and 7–9 mm proximally; 18–40 mm length in preserved specimens. Oral disc small, circular, contracted in all specimens ( Fig. 6A, B, D ); diameter 2–7 mm in preserved specimens. Margin of column tentaculate; tentacles 14, smooth; putatively arranged in a single cycle. Figure 8. Cnidom of Scytophorus striatus . A, B, D, E, G, H, basitrich; C, spirocyst; F, I, p –mastigophore A. ( 330–331 m ). AMNH 4501 ( one specimen ); locality: Southern Ocean , Antarctica , Bransfield Strait , Sta. PS 56/164-1, 63°04.80’S 59°32.80’W , Agassiz Trawl , collected on 28 April 2000 by P. López-González ( 858–859 m ) . AMNH 4502 ( one specimen ); locality: Southern Ocean , Antarctica , West Deception Island , Sta. PS 56/183-1, 62°07.15’S 60°22.60’W , Bottom Trawl , collected on 3 May 2000 by P. López-González ( 200–204 m ) . Halcampoides abyssorum Danielssen, 1890 USNM 53297 ( seven specimens ); locality: North Pacific Ocean , Bering Sea , Alaska , Punuk Islands , Stranger M /S, collected on 15 July 1937 by W. Williams ( 27 m ) . Diagnosis: Fourteen mesenteries arranged in seven pairs, 14 tentacles, hermaphrodite, strongly attached, Internal anatomy, microanatomy ( Fig. 7 ): Aboral end flat, not physa-like, but without basilar musculature ( Fig. 7A ). Overall body wall thickness varies along column: generally thicker on furrows (epidermis 53–119 µm, mesoglea 33–119 µm, gastrodermis 50–122 µm) than rest of column (epidermis 32–84 µm, mesoglea 19–88 µm, gastrodermis 50–94 µm) ( Fig. 7B ). Bi-layered cuticle on column (19–35 µm) ( Fig. 7B ). Longitudinal endodermal musculature of column strong ( Fig. 7C ); higher muscle processes in distal column, but not forming a differentiated marginal sphincter muscle ( Fig. 7D ). Longitudinal musculature of tentacles ectodermal ( Fig. 7E ). Actinopharynx approximately one-third of the length of the column, longitudinally sulcate, more heavily folded proximally ( Fig. 7F ). Two indistinct siphonoglyphs ( Fig. 7G, K ). Mesenteries with unusual arrangement: 14 perfect mesenteries arranged in seven pairs, including a single pair of directives ( Fig. 7H, I ). Macrocnemes span entire length of body, from proximal ( Fig. 7J ) to distal column ( Fig. 7L ). Retractors of macrocnemes small, strong, circumscript, with clear pennon distally ( Fig. 7M ). Parietal musculature well developed, strong ( Fig. 7N ), equally developed in all mesenteries ( Fig. 7I ), more developed proximally ( Fig. 7L ). Basilar musculature absent ( Fig. 7A ). The four specimens examined hermaphroditic ( Fig. 7O ): one to three oocytes per macrocneme (major axis of oocytes 217– 597 µm) and many spermatic cysts (major axis of spermatic cysts 94–311 µm); all specimens collected in May. Table 2. Size ranges of the cnidae of Scytophorus striatus ; M, mean; SD, standard deviation; S, proportion of specimens in which each cnidae was found; N , total number of capsules measured; F, frequency; +++, very common; ++, common; +, fairly common; -, rare.

Categories	Range of length and width	± SD	S	N	F
of capsules (µm)
COLUMN
Basitrichs (A–B)	14.4–34.2 × 3.2–5.6	21.3 ± 5.5 × 4.1 ± 0.5	98	4/4	+++
TENTACLES
Spirocysts (C)	17.8–41.1 × 2.9–6.1	30.0 ± 4.3 × 4.3 ± 0.7	198	4/4	+++
Basitrichs (D)	24.0–37.6 × 2.5–5.3	29.2 ± 2.1 × 3.5 ± 0.5	114	4/4	+++
PHARYNX
Basitrichs (E)	22.2–51.1 × 3.1–6.5	30.4 ± 5.2 × 4.0 ± 0.6	93	4/4	+++
P- mastigophores A (F)	14.4–25.9 × 4.6–7.0	20.9 ± 2.0 × 5.6 ± 0.5	105	4/4	+++
FILAMENT
Basitrichs I (G)	19.0–27.2 × 3.0–4.5	23.0 ± 1.7 × 3.7 ± 0.3	37	4/4	+
Basitrichs II (H)	48.9–86.6 × 4.0–6.1	63.0 ± 6.7 × 5.1 ± 0.4	130	4/4	+++
P- mastigophores A (I)	19.4–28.2 × 4.1–6.2	23.1 ± 2.2 × 5.3 ± 0.4	29	4/4	+

Cnidom: spirocysts, basitrichs and p-mastigophores A. See Figure 8 and Table 2 for size and distribution. Distribution and natural history: Over a dozen specimens of Scytophorus striatus were collected in the same trawl suggesting they might be locally abundant in the Burdwood Bank (also known as Namuncurá Bank) at 1423 m . Many of these specimens were collected attached to scleractinian corals ( Fig. 6A ) indicating that at least some of them live burrowed in the sand but attached to solid substrates, which were plentiful in the trawl (e.g. coarse sand and coral gravel). The species was collected in an area in which octocorals and stylasterid hydroids were also trawled. Scytophorus striatus was previously known only from its type locality between the Kerguelen Islands and Heard Island and McDonald Islands ( 52°4’S , 71°22’E ) in somewhat shallow waters ( 274 m ). This new record for S. striatus extends the distribution of the species from the Indian Ocean region of Antarctica (Kerguelen) to the Atlantic portion of the sub-Antarctic region (Burdwood/Namuncurá Bank), a region that connects continental South America to the northern region of the Antarctic Peninsula. We also extend significantly the bathymetric range of S. striatus to 720–1922 m depth. Scytophorus is one of only six genera found in both Antarctic and sub- Antarctic regions (~7% of Antarctic fauna: Rodríguez et al ., 2007 ). Remarks: Specimens of S cytophorus striatus examined in this study largely agree with the original description in terms of external anatomy and musculature. We document and provide the cnidom and cnidae size ranges of S. striatus for the first time (see Fig. 8 and Table 2 ) and show that it differs from the one given for S. antarcticus by Carlgren (1927) and our own examination of its holotype (ZMH C1452; see Fig. 9 ). Both species differ in the size of basitrichs in the column and the actinopharynx, which in the column only overlaps in the lower range of those in S. striatus , and the presence of p- mastigophores in the actinopharynx in S. striatus . Although Carlgren (1927) does not specify the types of nematocysts in S. antarcticus , we confirmed their identity ( Table 2 ), including those of the mesenterial filaments not provided by him (i.e. basitrichs, p -mastigophores A). One of the most consistent differences between S. antarcticus and S. striatus is fertility: S. antarcticus is gonochoric, whereas S. striatus is hermaphrodite. Although hermaphrodite and gonochoric specimens may coexist in a population, hermaphrodites tend to be rare (e.g. Jennison, 1981 ; Van Praët, 1990 ; Rodríguez et al. , 2013). The fact that all five specimens of S. striatus examined in this study were hermaphrodite leads us to believe that it is a specific character of S. striatus . Likewise, we confirmed that the holotype of S. antarcticus (ZMH C1452) is female, corroborating the reproductive differences between the two species.