Aracia sinaloae, Tovar-Hernández, María Ana, 2014

Tovar-Hernández, María Ana, 2014, Aracia sinaloae sp. n., a new brooding, simultaneous hermaphroditic fan worm from southern Gulf of California (Polychaeta: Sabellidae), Zootaxa 3784 (4), pp. 389-400 : 390-399

Aracia sinaloae sp. n.

Figures 1–4

Material examined. Type material. Holotype ( MCZ –20145), Paratype ( MCZ –20146): Shrimp farm Don Jorge S. A. de C. V., Urías Estuary, Mazatlán, Sinaloa, México, Sta. 7, 23°09'13.3"N, 106°18'25.4"W, on settling panels for serpulid Ficopomatus miamiensis (Treadwell) in shrimp ponds, 2 April 2009, Rendón and Méndez leg. PARATYPES: SIO – BICA 3617 (1), Shrimp farm Don Jorge S. A. de C. V., Urías Estuary, Mazatlán, Sinaloa, México, 23°09'10.54"N, 106°18'22.84"W, on settling panels for serpulid Ficopomatus miamiensis (Treadwell) in shrimp ponds, 6 November 2009, Tovar leg. Preserved in 95% ethanol. MCZ –20147 (10), EMU– ICML –10034/ 10035 (50); CNP– ICML –POP–72–001 (55); UAA–M142B, M145C, M147A (mounted on SEM stub) (14): Water pump, Urías Estuary, Mazatlán, Sinaloa, México, 23°09'16.1"N, 106°18'19.2"W, associated with Rhizophora mangle roots, 10 August 2010, Villalobos and Ramírez leg. SIO – BICA 3618 (5): Water pump, Urías Estuary, Mazatlán, Sinaloa, México: 23°09' 16.1"N, 106°18'19.2"W, associated with Rhizophora mangle roots, 19 February 2009, Rendón leg. Preserved in 95% ethanol.

Additional material. GEOMARE– POLY –002: Water pump, Urías Estuary, Mazatlán, Sinaloa, México: 23°09'16.1"N, 106°18'19.2"W, 42 specs., associated with Rhizophora mangle roots, 7 August 2009, Salgado and Villalobos leg. GEOMARE– POLY –003: Water pump, Urías Estuary, Mazatlán, Sinaloa, México: 23°09'16.1"N, 106°18'19.2"W, 100+ specs., associated with Rhizophora mangle roots, 10 August 2010, Villalobos and Ramírez leg.

Description. (based on holotype; variation among paratypes in parentheses). Holotype and paratypes fertile, complete. Body 3.2 mm long (3–5.1 mm); 0.4 mm wide (0.4–0.6 mm). Branchial crown length 1.8 mm (1.4–2.8 mm). Branchial lobes joined mid-dorsally. Six pairs of radioles arranged in two semicircles, not involuted midventrally and not joined by palmate membrane. Radioles with two rows of skeletal cells in side view. Outer margins of radioles flat ( Figs. 1 D, F, 2B–C), without eyes, ocelli or flanges. Radiolar tips ¼ length of radioles ( Figs. 1 B, 2A–B) (1/ 2 in some paratypes), except for dorsal-most pair which are 1/2 length of other radioles ( Fig. 2 C). Dorsal-most pair of radioles shorter than others, bearing pinnules only along proximal half, distal pinnules thinner and twice as long as those of other radioles. Dorsal-most pair of radioles hold one cocoon with embryos ( Figs. 1 B, E, 2D). Dorsal lips triangular, separated, twice as long as broad, lacking radiolar and pinnular appendages ( Figs. 4 B, E–G). Ventral lips low, distally rounded, fused. Ventral sacs absent. Dorsal margins of collar diagonal (45°), fused to faecal groove, exposing anterior peristomial ring ( Figs. 1 D, 2A–B, G). Lateral collar margins oblique, not covering anterior peristomial ring on live specimens ( Fig. 1 F), but covering ring once fixed ( Fig. 2 C). Ventral collar lappets triangular, not overlapping, with short incision, not longer than half the ventral length of collar ( Figs. 2 H, 4A). Peristomial eyes present, ellipsoid ( Fig. 1 F). Posterior peristomial ring with a patch of mid-ventral cilia ( Fig. 2 H). Ventral shield of collar rectangular, half as long as shields in posterior thoracic segments, not indented at midline by collar lappets ( Figs. 2 H, 4A). Subsequent ventral shields rectangular, twice as long as collar shield, not indented by tori ( Fig. 4 A).

Thorax with eight chaetigers (5–8). Chaetiger 1 (collar chaetae) with two rows of six narrowly hooded chaetae each, superior row longer ( Fig. 3 A). Other thoracic chaetigers with notopodia and neuropodia. Notopodia with two types of chaetae ( Fig. 3 A–B): superior group with 6–8 narrowly hooded chaetae, arranged in arc ( Figs. 3 D, 4H), inferior group with two oblique rows of paleate chaetae ( Fig. 3 B–C), with 4–5 paleae each, with oval hoods and very long tips (longer than hood length). Thoracic neuropodial tori with 6–7 avicular uncini each ( Fig. 3 E). Uncini with very short handles and well-developed breast ( Fig. 4 I), 6–7 rows of equal-size teeth above main fang, covering ½ of extension of main fang ( Fig. 3 E). Companion chaetae with mucro gradually pointed towards tip ( Fig. 3 E). Abdomen with 22 chaetigers (13–22). Abdominal neuropodia with 6–8 broadly hooded chaetae, similar to superior thoracic notochaetae but slightly bulbous, in two rows ( Fig. 3 F–G). Abdominal notopodial tori with 6–9 uncini, breast and manubrium similar to those in thorax, uncini increasing in size from ventral to dorsal edge of torus, ventral-most uncinus within a torus with 8 rows of teeth covering ¾ of the main fang length, dorsal-most uncinus with 8 rows of teeth covering 1/2 of the main fang length ( Figs. 3 H–I, 4J).

Pydigium rounded, eyespots absent. Tubes leathery, smooth, composed of fine sediments.

Color of living specimens. Radioles with four brown bands alternating with white bands, each band occupying the distance of three pinnules and continuous with pinnules ( Fig. 1 A–B). Pink cocoon ( Fig. 1 B, E). Brooded larvae with a pair of red eyes. Body wall transparent, gut yellow ( Fig. 1 A–C). Mid-dorsal margins of collar white ( Fig. 1 D). All ventral shields white. First five abdominal segments with large orange oocytes floating free in coelom ( Fig. 1 A–C). Last eight abdominal segments whitish with sperm ( Fig. 1 A–B). Peristomial eyes dark red ( Fig. 1 F).

Post-fixation color. Body pale yellow. Radioles retain four brown bands.

Methyl Green glandular pattern. Ventral lappets, ventral shields, and pygidium stain dark blue. Base of ventral lappets stains darker than the rest of the glandular tissue ( Fig. 4 A).

Reproduction. Simultaneous hermaphrodite. Seventy-three asynchronous oocytes floating free in coelom of first five abdominal segments (45–130 oocytes in paratypes), 47–105 µm in diameter ( Figs. 1 A–C, 4K). Sperm in last eight abdominal segments with cap-like acrosome, nucleus short and cylindrical, flattened anteriorly ( Figs. 1 A–B, 4L); spermatids occurring in tetrads. Cocoon with 17 brooded larvae attached to dorsal-most radiolar pair (15– 28 larvae in paratypes) ( Figs. 1 A–B, E, 4C). Brooded larvae oval, 125 µm long, with pair of eyes, proto- and neurotroch ( Figs. 2 D–F, 4C–D). Released larvae were not observed.

All collections assessed during February, April, and August 2009 and August 2010 were represented mostly by reproductive individuals. Amongst these, three patterns were found: (a) sexually mature with sperm, oocytes, and cocoons with embryos; (b) sexually mature (with sperm and oocytes) but without cocoons; and (c) without gametes but cocoons attached to radioles. Juveniles were found bearing four pairs of radioles, dorsal-most pair of radioles unmodified, eight thoracic segments and 10 abdominal segments ( Fig. 2 B).

Amongst paratypes, only one has a thorax ( MCZ –20146) composed of five chaetigers (all others have eight chaetigers). This paratype has oocytes and a double posterior abdominal chaetiger, probably due to a regeneration process.

Habitat. Aracia sinaloae sp. n., was found in temperatures from 25.8 to 30.8°C and salinity 37–41‰, associated with settling panels for the invasive serpulid polychaete F. miamiensis and attached to R. mangle roots. Among mangrove roots, F. miamiensis forms small aggregates where A. sinaloae sp. n., and two other species of sabellid worms coexist: Megalomma coloratum (Chamberlin) and Parasabella sp.

Etymology. The specific epithet sinaloae is in honor of El Colegio de Sinaloa, A. C., for supporting my research to document the biodiversity of aquatic invertebrates in Sinaloa, Mexico.

Remarks. The fixation process employed on Aracia sinaloae sp. n., showed that in live specimens the anterior peristomial ring is exposed laterally ( Fig. 1 F) but in fixed specimens the junction between crown and thorax is covered by the lateral collar margins ( Fig. 2 C). On the other hand, the length of radiolar tips and pinnules of the dorsal-most radiolar pair in the new species varies possibly due to variation in fixation and/or preservation techniques. Thus, the degree of lateral exposure of the anterior peristomial ring and the length of radiolar tips are not considered here for comparative purposes with the other two species as mentioned in the following paragraphs.

Aracia sinaloae sp. n., is unique amongst the two previously described species in the genus by the presence of a rectangular ventral shield on chaetiger 1, shorter by half than those in posterior thoracic segments (as long as following thoracic shields in A. heterobranchiata and A. riwo ); 6–7 rows of teeth in thoracic uncini (4–5 in A. heterobranchiata , 5 in A. riwo ) and eight rows of teeth in abdominal uncini (4–5 in A. heterobranchiata , 5 in A. riwo ), covering from ½ to ¾ of the main fang length (1/ 2 in A. heterobranchiata and A. riwo ).

In A. sinaloae sp. n., and A. riwo the peristomial eyes are ellipsoid (rounded in A. heterobranchiata ); the ventral lappets of the collar are triangular, not overlapping (rounded, overlapping in A. heterobranchiata ); and the mucro of companion chaetae are gradually pointed towards the tip (pointed abruptly in A. heterobranchiata ). In A. sinaloae sp. n., and A. heterobranchiata pygidial eyes are absent (present in A. riwo ); the dorsal collar margin is diagonal, exposing the anterior peristomial ring (low or level in A. riwo ), and the inferior thoracic chaetae are distributed in two rows (single rows in A. riwo ). In A. sinaloae sp. n., and A. riwo the dorsal lips are triangular, longer than broad (roughly squared, distally truncate, broader than long in A. heterobranchiata ) ( Table 1 ).

On the last feature, Nogueira et al. (2004) interpreted the dorsal lips of A. riwo to be the same as A. heterobranchiata (short, broader than long, roughly squared, distally truncate) although Rouse (1996) only described the presence of dorsal lips and the absence of radiolar or pinnular appendages. In their (Nogueira et al. 2004) figure 9, a transversal section of dorsal lips allows a re-interpretation of these structures as triangular, such as in A. sinaloae sp. n., although re-examination of type material of A. riwo is certainly needed to estimate the length of dorsal lips and to confirm its shape.

The transverse colored bands on radioles is a common pattern in all Aracia species: 3–4 bands of orange/ brown in A. riwo , four dark brown bands in A. heterobranchiata and four brown bands in A. sinaloae sp. n. Body color in live material is white for A. riwo , transparent in A. sinaloae sp. n., and unknown in A. heterobranchiata .

As the length of dorsal lips varies among the three species recognized in Aracia (wider than long or longer than wide), as well as the shape of ventral lappets (rounded or triangular) and the degree of overlapping (overlapped, not overlapped), these characters should be avoided in the generic definition.

On the reproductive features. Protandric or simultaneous hermaphroditism has been recorded in only seven of the 39 currently recognized genera within the family Sabellidae . Simultaneous hermaphrodites can have eggs and sperm in the same segments as in Caobangia abbotii Jones , C. brandti Jones , Branchiomma luctuosum (Grube) , Parasabella media Bush , P. microphthalma (Verrill) , Sabellastarte magnifica (Shawn) ( Rouse & Fitzhugh 1994; Licciano et al. 2002) and B. bairdi (McIntosh) ( Tovar-Hernández et al. 2009a), whereas simultaneous hermaphrodites with gametes located in different segments occur in Amphiglena mediterranea (Leydig) , A. marita Chlebovitsch , A. nathae Rouse , A. terebro Rouse , Laonome kroyeri Malmgren , L. salmacidis Claparède , Aracia riwo ( Rouse & Fitzhugh 1994) and A. sinaloae sp. n. Laonome albicingillum Hsieh is also a simultaneous hermaphrodite ( Hsieh 1995) but the distribution of gametes is unknown. Protandric hermaphroditism has been described only in S. spectabilis (Grube) ( Bybee et al. 2006) ; while supposed in S. spallanzanii (Gmelin) ( Giangrande & Petraroli 1994) , further investigations revealed that species to be gonochoric (Giangrande et al. 2000).

Feature A. heterobranchiata A. riwo ( Rouse, 1994) A. sinaloae sp. n. (Nogueira et al. 2004)

Feature A. heterobranchiata A. riwo ( Rouse, 1994) A. sinaloae sp. n. (Nogueira et al. 2004)

Abdominal uncini With 4–5 rows of teeth, With 5 rows of teeth, covering With 8 rows of teeth, dentition covering a half of the main a half of the main fang length of those from ventralmost fang length uncinus within a torus covering ¾ of the main fang length; dorsalmost uncinus covering 1/ 2 of the main fang length

Pygidial eyes Absent Present, several of various Absent sizes, in two groups, rounded,

red (black post-fixation)

Oocytes diameter 30–90 µm 200 µm (maximum) 47–105 µm Protection of larvae in sabellids can be intratubular or extratubular, although the first pattern is most common in the group ( Rouse & Fitzhugh 1994). In extratubular brooding, three states have been documented. The first was observed in Parasabella media and Branchiomma lucullanum (Delle Chiaje) where larvae are brooded in a jelly ring around the mouth of the tube ( McEuen et al. 1983). In the second type, found only in Chone infundibuliformis Krøyer ( Okuda 1946) , larvae are in a jelly mass attached to the mouth of the tube. In the third type, larvae are attached in a mass to a radiole, as seen in Perkinsiana antarctica (Kinberg) ( Knight-Jones & Bowden 1984; Gambi & Patti 1999; Gambi et al. 2000) and in all members of Aracia : A. heterobranchiata and A. sinaloae sp. n., brood embryos within a capsule attached to the modified dorsal-most pair of radioles, while in A. riwo the capsule is attached to an unmodified ventral-most radiolar pair. There are 15– 28 larvae per cocoon in A. sinaloae sp. n., 6–14 in A. riwo , and four in A. heterobranchiata (Nogueira et al. 2004 recorded four embryos for one paratype, but illustrate at least 14 larvae for the holotype).

Spermiogenesis may be in a cluster of more than 100 spermatids attached to a cytophore as occurs in Caobangia Jones , in tetrads as in Aracia riwo , A. sinaloae sp. n., B. luctuosum , and Parasabella media , or in clusters of less than 100 spermatids as in Amphiglena Claparède and Laonome Malmgren ( Rouse & Fitzhugh 1994; Fitzhugh & Rouse 1999; Rouse et al. 2006). Spermatozoa of A. sinaloae sp. n., are similar to that recorded for A. riwo (cap-like acrosome, nucleus short and cylindrical, flattened anteriorly), but unknown for A. heterobranchiata .

Based on the system of classifying sperm by Jamieson & Rouse (1989), ect-aquasperm are found in broadcasting species with external fertilization, where sperm are released into the water and fertilize similarly released eggs; this occurs for instance in B. luctuosum ( Licciano et al. 2002) , and S. spectabilis ( Bybee et al. 2006) . Ent-aquasperm are found in species with in-situ fertilization, where sperm are released freely into the ambient water but are gathered by or in some other way reach the female prior to fertilization; this type is reported in Amphicorina spp. ( Rouse 1992), Amphiglena spp. ( Rouse 1993; Rouse & Gambi 1998a, b), Perkinsiana antarctica ( Gambi & Patti 1999) , T. heterouncinata ( Fitzhugh & Rouse 1999; Simon & Rouse 2005), Aracia riwo ( Rouse 1996) and A. sinaloae sp. n.

Egg size in sabellid genera varies from very small (82 µm in Amphicorina brevicollaris (Rouse) and Jasmineira regularis Hartman ( Giangrande 1997) , to 250 µm as in Parasabella microphthalma (Verrill) , to the largest sizes of 500 µm in Potamilla torelli (Malmgren) ( Rouse & Fitzhugh 1994) and 600 µm in Amphiglena marita ( Chlebovitsch 1959) . The diameter of oocytes in species of Aracia varies from 30–90 µm in A. heterobranchiata (Nogueira et al. 2004) , up to a maximum of 200 µm in A. riwo ( Rouse 1996) , and 47–105 µm in A. sinaloae sp. n.

Finally, further study is needed to document the larval development and settling, as well as ecology in populations of A. sinaloae sp. n., since it shares habitat with the invasive reef-building worm F. miamiensis in the Urías Estuary.

Figures

FIGURE 1. Aracia sinaloae sp. n., live colour. A, Entire body, dorsal view, showing distribution of oocytes and sperm; B, as A, arrow indicates cocoon; C, thorax and anterior abdomen showing oocytes through body wall as indicated by arrow; D, detail of collar and base of branchial crown, dorsal view; E, cocoon attached to dorsal-most radiolar pair; F, collar and base of branchial crown, lateral view, showing peristomial eye as indicated by arrow. A – F, Holotype MCZ – 20145. Scale bars: A – B, 1 mm; C – D, F, 0.5 mm; E, 0.8 mm.

FIGURE 2. Body structures of Aracia sinaloae sp. n. A, Adult, dorsal view; B, juvenile, dorsal view; C, branchial crown of mature specimen, lateral view; D, cocoon; E, detail of embryos; F, larva; G, collar, dorsal view; H, collar, ventral view, midventral patch of cilia as indicated by arrow. A – H, Paratypes UAA – M 142 B, M 145 C mounted for SEM. Abbreviations: apranterior peristomial ring, fg—faecal groove, vsc—ventral shield of collar. White arrow in F: neurotroch, black arrow: prototroch. Scale bars: A, 500 µm; B – D, 200 µm; E, G – H, 100 µm; F, 20 µm.

FIGURE 3. Chaetae and uncini of Aracia sinaloae sp. n. A, Thoracic chaetigers (1: chaetiger 1, 2: chaetiger 2, 3: chaetiger 3); B, thoracic chaetae; C, paleate chaetae; D, thoracic, narrowly hooded chaetae; E, thoracic uncini and companion chaetae; F, abdominal noto- and neurochaetae; G, abdominal neurochaetae; H – I, abdominal uncini. A – I, Paratypes UAA – M 147 A mounted for SEM. Scale bars: A, 50 µm; B, D, 20 µm; C, E – H, 10 µm; I, 5 µm.

FIGURE 4. Aracia sinaloae sp. n. A, Ventral collar lappets and ventral shields stained with methyl green; B, dorsal lips indicated by arrows and embryos attached to right dorsal-most radiole; C, left dorsal-most radiole with two attached early larvae indicated by arrows; D, late larvae; E – F, dorsal lips (indicated by arrows), dorsal view; G. dorsal lips (indicated by arrows), frontal view of peristomium (ventral lips and radioles removed); H, superior group of thoracic notochaetae; I, thoracic uncinus; J, abdominal uncinus; K, oocytes; L, spermatozoa. A – K, Paratypes EMU – ICML – 10034 / 10035. Abbreviations: vlventral lappets, vsc—ventral shield of collar. Scale bars: A, 0.5 mm; B, E – G, 0.25 mm; C – D, 100 µm; H, 20 µm; I – J, 5 µm; K, not scaled, 40 X; L, not scaled, 100 X.

Tables

TABLE 1. Comparison of the three species currently recognized in the genus Aracia.

Radiolar tips (except those of the dorsalmost radioles)	Short, ~2–3 times length of distal pinnules (less than ¼ of the length of radioles)	Long, up to half length of radioles	Medium to long: ¼-1/2 of the length of radioles
Dorsalmost radioles (fertile specimens)	Modified: shorter than remaining ones, bearing pinnules only along proximal half, distal pinnules thinner and longer than those of other radioles. Radiolar tips long (½ of the length of other radioles)	Unmodified	Modified: shorter than remaining ones, bearing pinnules only along proximal half, distal pinnules thinner and longer than those of other radioles. Radiolar tips long (½ of the length of other radioles)
Dorsal lips	Short, broader than long, roughly squared, distally truncate, without radiolar and pinnular appendages	Triangular, not fused (separated), without radiolar and pinnular appendages (see comment in remarks section)	Triangular, longer than broad, not fused (separated), without radiolar and pinnular appendages
Ventral lips	Low, fused to each other	Low, fused basally to each other	Low, fused to each other
Lateral collar margin Dorsal collar margin	Oblique, not covering anterior peristomial ring Diagonal (45°) exposing the anterior peristomial ring	Oblique, not covering anterior peristomial ring Low (level) exposing anterior peristomial ring	Oblique, not covering anterior peristomial ring (live specimens), covering anterior peristomial ring (post-fixed) Diagonal (45°) exposing the anterior peristomial ring
Peristomial eyes	Rounded, black	Ellipsoid, red	Ellipsoid, red
Ventral lappets of collar	Rounded, overlapping, with a short incision (1/4 of the ventral length of the collar)	Triangular, not overlapped with a medium length incision (less than half the ventral length of collar)	Triangular, not overlapped, with a medium length incision (less than half the ventral length of collar)
Ventral shield of collar	Rectangular, as long as following thoracic shields but divided in two parts	Rectangular, as long as following thoracic shields	Rectangular, half as long as posterior thoracic shields
Thoracic notochaetae	Superior chaetae narrowly hooded, in an arc. Inferior chaetae paleate, in two rows	Superior chaetae narrowly hooded, in an arc. Inferior chaetae paleate, in single rows	Superior chaetae narrowly hooded, in an arc. Inferior chaetae paleate, in two rows
Thoracic uncini	With 4–5 rows of teeth, covering half of the main fang length	With 5 rows of teeth, covering half of the main fang length	With 6–7 rows of teeth, covering half of the main fang length
Companion chaetae	Mucro abruptly pointed	Mucro gradually pointed towards tips	Mucro gradually pointed towards tips
Abdominal neurochaetae	Elongate, broadly hooded, in two rows	Elongate, broadly hooded, in two rows	Elongate, broadly hooded, in two rows ......continued on the next page