Pisionidens ixazaluohae, Petersen, H. Cecilie B., Gonzalez, Brett C., Martínez, Alejandro & Worsaae, Katrine, 2016

Petersen, H. Cecilie B., Gonzalez, Brett C., Martínez, Alejandro & Worsaae, Katrine, 2016, New species of Pisionidens (Sigalionidae, Annelida) from Akumal, México, Zootaxa 4136 (1), pp. 165-173 : 167-171

Pisionidens ixazaluohae n. sp.

( Tables 1–2, Figs 1–2 )

Material examined. Half Moon Bay, Akumal, Quintana Roo, México, 15 specimens. Holotype: complete adult male (ZMUC-POL-2435, stub-mounted for SEM), 13.3 mm long, 65 segments. Coarse sand, swash zone, 0.2 m depth, 20°24.22'N, 87°18.28'W. Collectors: B. C. Gonzalez & A. Martínez 19.06.2014. Paratypes: 1 male (ZMUC-POL-2436, stub-mounted for SEM), 4 females (1 stub-mounted for ZMUC-POL-2437, 3 preserved and stored in ethanol ZMUC-POL-2439, ZMUC-POL-2440), 4 incomplete specimens (ZMUC-POL-2441), sex unknown (4.25–8.72 mm, 24–41 segments, stored in ethanol) and 4 specimens in bad condition (ZMUC-POL- 2442), sex unknown (7.88–17.75 mm, fixed in PFA, stored in PBS), same locality and sampling date as holotype. Diagnosis. Muscular and slender body, anteriorly and posteriorly tapering. One pair of anterior, basally fused antennae, two smooth lateral prostomial palps; one pair of ventral elongated cirri on segment 2, one pair of dorsal elongated cirri on segment 3. Pharynx eversible, with a terminal crown of 18 papillae and two pairs of hook-shaped jaws. Achaetous parapodia with distal glandular disc present from segment 8 onward. Males with one row of midventral pores from segment 11 to posterior end. One pair of club-shaped copulatory organs on segment 45.

Description. All measurements from the holotype, parenthetical numbers from paratypes. Body slender, muscular, white to pale yellow (fixed specimens) ( Fig. 1 A), with thick cuticle and smooth body surface. Length 13.3 mm (7.33–17.75 mm, n=10), width including parapodia 0.45 mm (0.47–0.69 mm, n=5), width excluding parapodia 0.34 mm (0.24–0.52 mm, n=15), 65 segments (45–62, n=5).

Fused conical prostomium with segment 1, one pair of antennae fused at base ( Fig. 2 A). One pair of palps, smooth, 0.28 mm long (0.22–0.34 mm, n=7), emerging laterally from prostomium ( Fig. 2 A). One pair of dorsal eyes in segment 2 ( Fig. 1 B). Cerebral ganglion large, bilobed, extending from middle of segment 1 to segment 4. Mouth ventral with eversible pharynx, equipped with two pairs of hooked jaws ( Fig. 1 C). Pharynx with a terminal crown of 18 digitiform papillae ( Fig. 2 B), central papilla largest, decreasing in size laterally.

Segments 1–3 lacking parapodia, segments 4-7 with rudimentary parapodia. Ventral cirri on segment 2 (buccal segment), long and tapering, similar in length to palps; dorsal cirri on segment 2 small, bottle-shaped ( Fig. 2 A, C). Dorsal cirri on segment 3 (see Rouse and Pleijel 2001) longest among anterior appendages, approximately twice the length of palps ( Fig. 2 A); ventral cirri on segment 3 small and bottle-shaped ( Fig. 2 C). All anterior appendages smooth. From segment 4 posteriorly, dorsal and ventral cirri small with subdistal and distal cilia ( Fig. 2 D). Rudimentary parapodia and cirri may be lacking in some specimens from segment 4 to segment 7 ( Fig. 2 C). Parapodia initiating on segment 8, achaetous in mature specimens (unknown in juveniles). All parapodia cylindrical and slender, with subdistal tufts of compound cilia; distal disc with adhesive glands ( Fig. 2 D). Notoacicula absent, neuroacicula straight ( Fig. 1 D). Adult males with midventral line of segmentally repeated pores ca. 35 µm wide (n=2) from segment 11 to last segment prior to pygidium, pore diameter smaller on copulatory segment (ca. 10–15 µm, n=2) ( Fig. 2 E); midventral pores lacking in females and juveniles. Paired lateral fields of ca. 35 epidermal pores (2-5 µm) present between parapodia. Pygidium with one pair of cirri, short and cylindrical ( Fig. 2 F). Anus dorsal.

One pair of male copulatory organs, on segment 45 in holotype (42, n=1), with short dorsal cirri, parapodia and ventral cirri absent. Copulatory organ approximately same length as body width (0.40 mm, n=1), club-shaped, curved latero-ventrally, with subdistal node-shaped process ( Fig. 2 G) and small papillae distally; tip slightly curled, with small terminal process ( Fig. 2 H), but lacking cuticular hooks. Females appear to differ from males externally only in the absence of copulatory organs and mid-ventral pores.

Molecular information. Newly generated sequences for Pisionidens ixazaluohae n. sp. included 1800 bp of 18S rDNA (Gb accession number KX282503 ), 1039 bp of 28S rDNA (Gb accession number KX282504 ), 510 bp of 16S rDNA (Gb accession number KX282502 ), and 582 bp of COI (Gb accession number KX282505 ). In previous molecular analyses (Gonzalez et al. 2015), Pisionidens ixazaluohae n. sp. was recovered next to Pisionidens sp. ( Norlinder et al. 2012), forming the well-supported sister clade of all the species of Pisione included in the analyses.

The COI gene fragment of Pisionidens ixazaluohae n. sp. presents 83.4% similarity to the COI of Pisionidens sp. (Acc. Num JN852943 ), being the only Pisionidens sequence available in GenBank. This similarity accounts for 94 mutations, three of them non-synonymous.

Remarks. Pisionidens ixazaluohae n. sp. is characterized by having only one pair of copulatory organs, while the previously described species possess two to four pairs. P. ixazaluohae n. sp. differs from P. indica ( Aiyar & Alikuhni 1940) and Pisionidens tchesunovi, Tzetlin 1987 by lacking true parapodia on segments with copulatory organs. This feature is similarly found in Pisionidens maturata, Yamanishi 1976 . However, P. ixazaluohae n. sp. is distinguished from P. m at ur a t a and P. indica by having one continuous series of midventral pores (versus two separate series of ventral pores). A comprehensive comparison of taxonomic characters and distribution of all described species of the genus Pisionidens is given in Table 2 .

Holotype ZMUC-POL-2435 Ađult Male 1 13.3 mm 64 45 0.28 mm 0.35/ 0.43 mm 0.45/ 0.34 mm Paratype 1 ZMUC-POL-2436 Ađult Female 1 11.0 mm 54 0.26 mm 0.34/ 0.44 mm 0.51/ 0.37 mm Paratype 2 ZMUC-POL-2437 Ađult Male 1 10.6 mm 61 42 0.22 mm 0.22/ 0.35 mm 0.49/ 0.30 mm Paratype 3 ZMUC-POL-2438 Ađult Female 1 4.2 mm 24* 0.31 mm 0.30/ 0.36 mm 0.47/ 0.29 mm Paratype 4 ZMUC-POL-2439 Ađult Female 1 13.4 mm 62 0.32 mm 0.33/ 0.38 mm */ 0.34 mm

Paratype 5 ZMUC-POL-2440?? 2 8.2 mm 45 0.25 mm 0.19/ 0.35 mm */ 0.30 mm

Ađult? 17.7 mm 52 * * 0.69/ 0.52 mm Paratype 6 ZMUC-POL-2441 Ađult? 4 14.1 mm * * * */ 0.45 mm

Ađult? 16.5 mm * 0.30 mm 0.31/ 0.45 mm */ 0.45 mm

?? 7.9 mm * * * */ 0.28 mm

Ađult? 8.7 mm 41 *?/ 0.39 mm */ 0.35 mm

Paratype 7 ZMUC-POL-2442 Ađult? 4 6.2 mm * * * */ 0.38 mm

Ađult? 13.1 mm * * * */ 0.26 mm

?? 7.3 mm * * * */ 0.24 mm

Ađult? 6.2 mm * * * */ 0.44 mm Type locality. Half Moon Bay, Akumal, Quintana Roo, México.

Habitat. Coarse sand in the swash zone of an exposed beach: 0–0.25 m depth. Several other annelids were found in the samples including Claudrilus cf. ovarium ( Di Domenico et al. 2013) , Saccocirrus sp., Polygordius sp., Microphthalmus sp., Macrochaeta sp., Pholoe sp., as well as high numbers of Ingolfiella sp. and otoplanid flatworms.

Distribution. Caribbean Sea, Akumal, México.

Etymology. Named after the Mayan goddess of water, Ixazaluoh.

Figures

FIGURE 1. Light microscopy images of Pisionidens ixazaluohae n. sp. (A) Whole specimen. (B) Anterior end, details of eyes. (C) Details of jaws. (D) Details of a midbody parapodia. Abbreviations: an, anterior; dc, dorsal cirri; ey, eye; gl, glands; jw, jaws; nac, neuroacicula; po, posterior; vc, ventral cirrus. Segments indicated by roman numerals.

FIGURE 2. SEM images of Pisionidens ixazaluohae n. sp. (A) Anterior end with pharynx, appendages, and first segments; dorsal view. (B) Anterior end with details of pharynx; anterior view. (C) Anterior body-segments; lateral view. (D) Details of parapodia and cirri; lateral view. (E) Midbody segments of male with ventral pores and copulatory organ. (F) Posterior segments and pygidium with pygidial cirri; ventral view. (G) Midbody segments with copulatory organs; ventral view. (H) Details of male copulatory organ; ventro-lateral view. Abbreviations: ant, antennae; ci, cilia; co, copulatory organ; dc, dorsal cirrus; dp, distal process; gl, glands; lpf, lateral pore fields; mvp, midventral pore; pa, palps; pap, papillae; pc, pygidial cirrus; pha, pharynx; pp, parapodia; sdp, subdistal process; vc, ventral cirrus. Segments indicated by roman numerals.

Tables

TABLE 2. Comparative table of taxonomic characters of all described species of the genus Pisionidens with information on distribution. * Trunk segments have been counted from segment 1, with segment 2 considered the buccal segment as in other sigalionids. Abbreviations: seg, segment.

Character	P. indica	P. ixazaluohae n. sp.	P. maturata	P. tchesunovi
Length	up to 18 mm	up to 17.7 mm	up to 30 mm	up to 16 mm
Number of segments	up to 82	up to 64	up to 60	up to 60
Start of true parapodia	seg. 8	seg. 8	seg. 7*	seg. 4*
Ventral pores in males	anterior and posterior series	one continuous series	anterior and posterior series	anterior and posterior series
Number of male copulatory organs	one to three pairs	one pair	four to five pairs	three pairs
True parapodia on male copulatory organs	present	absent	absent	present
Dorsal cirrus on male copulatory organs	present	present	absent	present
Distribution	cosmopolitan	México	Japan	Red Sea