Haliclystus californiensis, Kahn, Amanda S., Matsumoto, George I., Hirano, Yayoi M. & Collins, Allen G., 2010

Kahn, Amanda S., Matsumoto, George I., Hirano, Yayoi M. & Collins, Allen G., 2010, Haliclystus californiensis, a “ new ” species of stauromedusa (Cnidaria: Staurozoa) from the northeast Pacific, with a key to the species of Haliclystus, Zootaxa 2518, pp. 49-59 : 50-55

Haliclystus californiensis , new species

Haliclystus californiensis: Gwilliam, 1956 , p. 57; Hirano, 1997, p. 251; Mills & Larson, 2007, p. 173; Miranda et al., 2009, p. 1515 [nomen nudum].

Holotype. Smithsonian Institution, National Museum of Natural History ( USNM) 1106657, northeast Pacific, off Pacific Grove, CA (Otter Point), 36º38’4”N, 121º55’13”W, 12 m depth, on a blade of red alga attached to rock, July 2006, coll. A. Kahn.

Other material examined. Paratypes: USNM 1106654, Monterey, CA, near Monterey Bay Aquarium, depth unknown, July 2006, coll. J. Mariottini and C. Widmer. California Academy of Sciences ( CAS 98108), off Christy Cove, Santa Cruz Island, Channel Islands, CA, 29 m depth, 7 March, 1950, coll. P. Silva. USNM 1139484 Point Piños, Pacific Grove, Monterey Bay, CA, ca. 15 m depth, July 1987, coll. during a marine biology field course (Hopkins Marine Station). USNM 1139485 six specimens—one adult and five juveniles— Horseshoe Cove, Bodega Bay, CA, September 1990, coll. on settling brushes by Laura Rogers- Bennett.

Diagnosis. Haliclystus with conical calyx, slightly longer than wide. Calyx tapering towards stalk, becoming nearly tubular; overall shape resembling a martini glass. Gonads extending from base of calyx to tips of each of eight arms ( Fig. 1 ); 40 to 50 gonadal sacs comprising each gonad, with three or four abreast at the widest. Each arm tipped with a cluster of 60 to 80 capitate secondary tentacles ( Fig. 2 B); with up to five basal tentacles on exumbrellar side possessing a prominent swollen glandular pad ( Fig. 2 B and 2D). Eight primary tentacles lining coronal margin on interradial and perradial axes, alternating with the eight adradial arms ( Fig. 2 A and 2C). Large, horseshoe-shaped anchors, roughly as wide as tall, wrapping around each primary tentacle with open side up ( Fig. 2 A and 2C). Perradial marginal notches between arms about twice as wide and deep as interradial notches ( Fig. 1 ). White nematocyst clusters lining subumbrellar margin ( Fig. 1 ). Exumbrellar surface grainy with nematocysts ( Fig. 2 A and 2E); subumbrellar surface smooth. Pigment stripes along calyx absent. Stalk 1/4 length of calyx in adults.

Description of holotype. Height 21 mm; calyx 17 mm tall, 15.5 mm wide; stalk 4 mm tall, 2.0 mm diameter. Arms united in interradial pairs, with perradial marginal notches twice as wide and deep as interradial ones ( Fig. 1 ). Stalk narrow and short—about 1/4 length of calyx—but well-developed with four chambers and four longitudinal muscle bands extending from base through mesoglea ( Fig. 2 F, 2G, Gwilliam 1956). Four muscle bands continuing through calyx along interradii, then bifurcating in upper third of calyx and extending to base of secondary tentacles ( Fig. 1 ). Before splitting, each muscle band lying exterior to gonads; in upper 1/3 of calyx, bifurcated muscle bands lining interradial margins of gonads and extending up to bases of clusters of secondary tentacles.

species as H. auricula .

Gonads comprising gonadal sacs, beginning at base of calyx and extending to base of secondary tentacles ( Fig. 2 A). Gonads paired in lower 2/3 of calyx, but pairing ends at same point that muscle bands bifurcate ( Fig. 1 ). Each gonad with 40 to 50 reddish-brown gonadal sacs ( Fig. 2 E). Gonadal sacs ovoid, relatively large (up to 1 mm along longest axis) compared to many other members of the genus ( H. auricula , H. octoradiatus , H. sanjuanensis ; Hirano 1997, personal observation). At the widest, just above bifurcation of muscle bands, three to four gonadal sacs lie abreast.

Exumbrella finely granulated with small nematocyst clusters ( Fig. 2 A and 2E); subumbrellar surface smooth. Five to 10 white nematocyst clusters, each with a diameter of about 0.5 mm, lining subumbrellar margin between each arm ( Fig. 1 ). Cnidae examined from gastric filaments and secondary tentacles composed of two size classes of microbasic euryteles and one size class of isorhizas (holotrichous or atrichous; Table 1 ). Tentacles with ovoid euryteles and isorhizas; gastric filaments with smaller, rounder euryteles.

Tip of each arm with 60 to 80 tightly clustered secondary tentacles ( Fig. 2 A and 2B). All tentacles short, capitate. In each cluster, up to five of outermost tentacles with swollen glandular pads at base of tentacular stalk ( Fig. 2 B and 2D).

Eight primary tentacles and anchors lining subumbrellar margin, one between each arm in the interradii and perradii ( Fig. 1 ). Part of primary tentacle retained and well-developed in adult; the anchor surrounding it comprising a large yellow pad with a cleft on upper radius, forming a horseshoe around the tentacle ( Fig. 2 C). Anchors approximately same diameter as largest gonadal sacs of this species.

Color in life red, cryptically matching color of its algal substrate. The alga, presumably a rhodophyte, was not identified. Gonads reddish-brown; nematocyst clusters along subumbrellar margin vivid white; tentacles red. Muscles in stalk and along subumbrellar margin red, but colorless in calyx.

Description of additional material. Adult specimen ( USNM 1139484) from Pt. Piños 15 mm in height; calyx 12 mm tall; stalk 3 mm tall, 2.3 mm diameter (alive). Arms, stalk, muscle bands, and nematocyst clusters as in holotype. Secondary tentacles 40 to 50, clustered; in each cluster, up to three of outermost tentacles with swollen glandular cushions at base of tentacular stalk. Tentacular stalk varying in length, and may be rather long near subumbrellar side of arm. Anchors similar to those of holotype, although one anchor of this specimen was smaller than the others and without the primary tentacle. This may be due to a developmental defect, since all other anchors were similar to each other and to the holotype. Gonads as in holotype, but differing in number of gonadal sacs or follicles. Each gonad with 20 to 30 gonadal sacs. Largest sac about 0.5 mm along longest axis. At the widest, two gonadal sacs lie abreast. Color similar to holotype although ground color of both calyx and stalk almost transparent with slight red tint. Pad of anchor whitishyellow.

The original adult specimen described by Gwilliam (1956), found off of Christy Cove on Santa Cruz Island, is stored at the California Academy of Sciences ( CAS #98108). Half of the specimen was prepared into thin sections, and the remaining tissue has degraded. Still, two intact anchors and the swollen glandular pads of the outermost secondary tentacles were visible on portions of the specimen, allowing us to verify its identity.

The young adult specimen ( USNM 1106654) from Monterey Bay, 8 mm in height, is similar in body shape to the adults. Gonads are partially developed, with distinct gonadal sacs occurring only in the upper 1/3 of the calyx. Anchors are of a similar shape as those in the adult, but the primary tentacle appears a bit larger in proportion as compared to the surrounding anchor.

Six additional specimens ( USNM 1139485), including five juveniles, were collected from Bodega Bay. The juvenile specimens cannot be definitively identified as H. californiensis . We infer them to be the same species because of the co-occurrence of a young adult specimen that can be diagnosed as H. californiensis , but some caution is warranted. In juveniles, approximately 1.8-2.5 mm in height (preserved), the stalk is almost 1/ 2 the length of the calyx height. Outermost tentacles of these specimens were without obvious pads. The anchors were only poorly developed so that the primary tentacles were proportionately longer than in adults. The number of tentacles for each cluster was 4 to 5 (1.8 mm specimen in total height), 5 (1.9 mm specimen), 5 to 6 (2.5 mm specimen), 7 to 8 (2.0 mm specimen). A larger juvenile specimen (4.9 mm in total height) appeared to have more than 10 tentacles for each cluster, however, this specimen was too heavily damaged for more detailed observation. This large juvenile may have glandular pads on outermost tentacles, but that part was also too damaged to see this character. A single specimen ( USNM 1139485) from Bodega Bay was mature, measuring 8.5 mm in total height; calyx 5.9 mm tall; stalk 2.6 mm tall in preserved condition. This mature specimen was with about 30 tentacles for each cluster, of which the outermost three were with glandular pads. It was difficult to locate white nematocyst spots for sure in small preserved specimens, but one small specimen in good condition appeared to have them.

Comparisons. Haliclystus californiensis , sp. nov., joins 10 other species in the genus Haliclystus : H. antarcticus Pfeffer, 1889 , H. auricula (Rathke, 1806) , H. borealis Uchida, 1933 , H. kerguelensis Vanhöffen, 1908 , H. monstrosus ( Naumov, 1961) , H. octoradiatus ( Lamarck, 1816) , H. salpinx Clark, 1863 , H. sinensis Ling, 1937 , H. stejnegeri Kishinouye, 1899 , and H. tenuis Kishinouye, 1910 ( Table 2 ). Original species descriptions were used for the following comparisons unless specifically noted otherwise.

One distinctive feature of H. californiensis is the presence of prominent glandular pads on up to five of its outermost secondary tentacles. Glandular pad swellings are encountered in other Haliclystus species, including H. auricula and H. “ sanjuanensis ”, but they are much slighter than those observed in H. californiensis and are variable in occurrence ( Gwilliam 1956; Hirano pers. obs.). Outside Haliclystus , glandular pads associated with secondary tentacles are fairly widespread, occurring for example in species of Depastromorpha ( Carlgren, 1935) , Kyopoda ( Larson, 1988) , Manania ( Hirano, 1986) .

The most distinctive character of Haliclystus californiensis is the unique shape of the marginal anchors. The anchor forms a large, yellow horseshoe around the primary tentacle, with the cleft pointing up ( Fig. 2 C). Morphologically, the anchors of this species most closely resemble those of H. auricula , H. borealis , and H. tenuis ( Clark 1878; Hirano 1997). As in H. californiensis , many specimens of H. auricula have anchors that surround a rudimentary primary tentacle ( Clark 1878; Hirano pers. obs.). Although the anchors of both H. auricula and H. californiensis curve and are open at the top, the anchors of H. californiensis nearly complete a circuit around the primary tentacle and are approximately as wide as long. The coffee bean-shaped anchors of H. auricula curve gently, wrapping only about halfway into a circle, and are distinctly longer than wide. Unlike H. californiensis , the marginal anchors of H. borealis and H. tenuis are round and without a cleft. In addition, the remnant of the primary tentacle is not retained in adults of either of these two species. The geographic range differs as well; H. borealis and H. tenuis are found in the northwest Pacific, whereas H. californiensis is thus far known only from the coast of California. The gonadal sacs of H. californiensis are ovoid and relatively large (up to 1 mm along the longest axis) compared to many other members of the genus ( H. auricula , H. octoradiatus , H. “ sanjuanensis ”; Hirano 1997, personal observation). The number of secondary tentacles, gonads, and other differences are summarized in Table 2 .

Other species within the genus differ in both morphology and geographic distribution (see Miranda et al. 2009 for further discussion of ranges of the species of Haliclystus ). Two species are found only in the southern hemisphere: H. antarcticus from Antarctica, and probably southern Chile and Argentina ( Miranda et al. 2009), and H. kerguelensis from the southern Indian Ocean. Haliclystus sinensis has been found only off the coast of China, and H. monstrosus is only known near Russia. Haliclystus octoradiatus has been reported from the northeastern Atlantic, near Iceland and Europe. Haliclystus stejnegeri , restricted to the boreal Pacific ( Miranda et al. 2009), differs from H. californiensis in the number of gonadal sacs, with 90 to 240 versus 40 to 50 ( Hirano 1986). The anchors of H. stejnegeri are egg-shaped rather than round, and have a cleft only when there is still a remnant of the primary tentacle. Halclystus auricula is found in the north Pacific and north Atlantic Ocean. Haliclystus salpinx has a somewhat surprising distribution, with specimens reported from the north Pacific [in bays near the San Juan Islands and southern Vancouver Island ( Mills & Larson 2007), and in Alaska and the Russian coast of the Japan Sea ( Mills 2001)] and north Atlantic ( Mills & Larson 2007, Miranda et al. 2009). It differs from H. californiensis by having a long stalk—longer than the height of the calyx—and trumpet-shaped anchors ( Kramp 1961).

Etymology. The specific name refers to the state of California, the first and thus far only region where the species has been found.

Distribution. Specimens have been found in shallow (10-30 m), wave-exposed kelp forests along the California coast from the Channel Islands in the south to Bodega Bay in the north.

Gene sequences. Mitochondrial 16S rDNA and COI were amplified and sequenced from the holotype and young adult specimen (USNM 1106654; GenBank accession numbers GU201828 - GU201831 ).

Figures

FIGURE 1. Haliclystus californiensis, a new species of stauromedusa from the northeast Pacific, photographed alive. Visible features include large, horseshoe-shaped anchors, white nematocyst clusters lining the subumbrellar margin, large reddish-brown gonadal sacs, interradial notches about one half as deep and wide as perradial notches, and the nearly transparent ground color of the calyx and stalk. The stalk is contracted to about half its relaxed length in this photo of the holotype – see Fig. 2 G for relaxed stalk. Scale bar: 5 mm.

FIGURE 2. All images of the live holotype unless noted otherwise. A. Interradial margin. B. Clump of secondary tentacles on one arm, with enlarged glandular pad visible on aboral side of the outermost tentacle. C. Large, horseshoeshaped anchor surrounding a well-developed primary tentacle. D. Close-up of outermost tentacle of a tentacle cluster, showing an enlarged glandular pad at the base. Photo from preserved holotype. E. Gastric filaments visible through outer calyx wall in live specimen. F. Transverse-section through the stalk of CAS # 98108. m – mesoglea, mb – muscle band, ch – chamber, from a collection of permanent slides prepared by Gwilliam (1956). G. Close up of stalk. Scale bars: 0.5 mm, except for that shown on D, which represents 0.2 mm.

Tables

TABLE 1. Dimensions of cnidae found in the gastric filaments and secondary tentacles of Haliclystus californiensis. Measurements provide the minimum, mean (in bold), and maximum length of each type of cnida sampled. The number of cnidae measured corresponds with the number found in prepared squash slides; some were more abundant than others.

Cnidae	Length	Width	n
Euryteles (ovoid)	26.86- 30.58 -34.74 µm	15.00- 16.85 -19.35 µm	11
Euryteles (round)	8.30- 13.22 -19.68	8.80- 10.32 -13.11	40
Isorhizas	15.21- 23.71 -29.13	4.98- 6.61 -9.26	50

TABLE 2. Comparison of Haliclystus species. References for H. tenuis followed by * indicate those that discuss the

	G e o g r a p hi c range	G on a d a l sacs	2o Tentacles	St a l k: ca l y x length	Anchor shape	Reference
H. antarcticus	Southern Ocean: A n t a r c t i c a, S A r ge n t i na, S Chile	50–150	6–224	1/2 to 2/3 length	Biscuit-shaped	Pfeffer (1889), Kramp (1961), Miranda et al. (2009)
H. auricula	N A tl a n t i c, N Pacific	30–200	Usually 100 or more, but as few as 30	Equal length	Coffee bean-shaped	Rathke (1806), Mayer (1910), Hirano (1997)
H. borealis	N Pacific	50, ranging from 30 to 100	20–30	<1/3 length	Large, round, with longitudinal furrow	Uchida (1933), Ling (1937), Kramp (1961), Hirano (1986)
H. californiensis	NE Pacific	40–50	60–80	1/4 length	Horseshoe-shaped	This paper
H. kerguelensis	S Indian	?	50	Twice as long	S m a l l, o va l, w i t h tentacular knob	Vanhöffen (1908), Kramp (1961)