Iphione Kinberg, 1856

Salazar-Vallejo, Sergio I., Piotrowski, Christina N. & Paulay, Gustav, 2024, Revision of Iphione Kinberg, 1856 (Annelida, Aphroditiformia, Iphionidae), Zootaxa 5548 (1), pp. 1-84 : 13-16

Iphione Kinberg, 1856

Iphione Kinberg, 1856: 383 , 1858: 8; Baird 1865: 181; de Quatrefages 1865: 266; Grube 1876: 50; Grube 1878: 21; Darboux 1900: 108 (syn.); Gravier 1901: 226; Izuka 1912: 63; Horst 1917b: 65; Fauvel 1932: 12; Fauvel 1953b: 32; Day 1967: 43; Fauchald 1977: 63; Pettibone 1986: 6; Hanley & Burke 1991: 38 (diagn., key); Wehe 2006: 61 (diagn., key).

Norepea Baird, 1865: 200 (type species: Polynoe peronea Schmarda, 1861 by monotypy); synonymy after Chamberlin 1919: 40, Fauchald 1977: 65, and Pettibone 1986:6.

Type species. Iphione ovata Kinberg, 1856 , by subsequent designation (Hartman 1959: 82).

Diagnosis. Iphionids with prostomium with long lateral antennae, median antenna rarely present; two pairs of eyes; palps with longitudinal rows of papillae; 13 pairs of elytra on segments 2, 4, 5, 7, alternating segments to 23, and then on 27; elytral surface with macrotubercles usually projected, spinous or smooth, elytral margins smooth or with fimbriae; most neurochaetae thick, rarely acicular, tips unidentate or bidentate, rarely hooded, with subdistal transverse rows of spinules.

Remarks. Baird (1865) was first to designate a type species for Iphione , stating: “The typical species is the Polynoë muricata of Savigny, so beautifully represented by that author in his great work on Egypt.” Further, Farber (1976: 95, footnotes 5, 6) noted that this type of phrasing was common in the 1840s, and while the Code has not been established, there were recommendations for using types and type species ( Gray 1840, Strickland 1845), although the first draft of the Rules for Nomenclature was published in 1843, and adopted in 1865 ( Strickland 1843, Sclater 1878). This subsequent designation was accepted by Pettibone (1986: 2). Regretfully, Article 67.5 of the Code ( ICZN 1999) explicitly rules out type species designations based on the word ‘typical’, making Baird’s designation not valid. Hartman (1959) was first to validly designate a type with Iphione ovata Kinberg, 1856 .

While the type species of Norepea Baird, 1865 is clearly an Iphione , what species it represents has been contentious. Michaelsen (1892: 95) regarded Polynoe peronea Schmarda, 1861 described from Sri-Lanka, as a junior synonym of I. spinosa Kinberg, 1858 , probably because both have elytra with smooth margins, without fimbriae. However, he noted differences: “The present specimen deviates from Kinberg’s description markedly, as the antennae are not quite smooth, but with sparse (ca. 15), cylindrical papillae.” In contrast, Willey (1905: 246–247) regarded P. peronea as a junior synonym of I. muricata (Savigny in Lamarck, 1818), even though I. spinosa was described with smooth elytral margins and that he noted that Grube (1878: 22) “states that the outer and posterior margin of the scale is fimbriated which is not so in I. peronea .” Pettibone (1986: 4) regarded P. peronea as an unidentifiable Iphione species and the lack of type material implies that it will remain a nomen dubium.

Distribution. Iphione appears to be restricted to, but ranges across, the entire tropical Indo-Pacific, from the Red Sea to South Africa and east to the Hawaiian and Tuamotu Islands and Americas, mostly in shallow rocky or mixed bottoms. No specimens are known from the tropical Atlantic, except one Red Sea species has recently invaded the Mediterranean Sea ( Goren et al. 2017). The record by Gibson (1886: 150) of I. muricata from the Liverpool area was shown to be erroneous ( Hornell 1891: 224).

Diagnostic characters for Iphione species

Elytra

Variation in some morphological features of the elytra have been explored by Piotrowski et al. (2024). Because the elytra in Iphione are overlapped, portions are exposed, others are covered by adjacent elytra. Elytra are usually wider than long, the first pair oval, the second and third U-shaped, and the last roughly triangular. Elytral surface is mostly areolated, and areolation varies with size, less well-developed, but covering larger areas in small than large specimens ( Piotrowski et al. 2024). Elytra have distinct anterior and posterior regions, and outer and inner areas. There is often a hyaline marginal band, usually along the outer elytral margins.

Elytra are ornamented by diverse projecting structures that are categorized as macrotubercles, microtubercles, and fimbriae. These can all be broken, eroded or overgrown by epibionts. Finer details are best seen in smaller specimens because their elytra are thinner and are less obscured by foreign particles.

Macrotubercles are distributed over much of the elytral surface, are fragile and often eroded, conical to digitate, ornamented by short stem spines and larger, stiff distal filaments ( Fig. 1E, F ), and retain a small amount of sediment. Microtubercles are similar to macrotubercles, but small and arranged in several densely packed rows, especially along the posterior elytral margin ( Fig. 1D, G ). Fimbriae typically occur in a marginal or submarginal band (rarely in inner elytral areas except in regenerating elytra), are flexible and easily bent, globular to cylindrical, ornamented with long, thin spines of similar size along their length and with long, flexible distal filaments, and usually covered by a thick layer of sediment particles that are difficult to remove.

Hanley & Burke (1991: 41) indicated that fimbriae might become macrotubercles depending on “the degree of chitinization of the outer edge of the elytron.” This is hardly the case; first, fimbriae and macrotubercles can be present side by side, but no intermediate forms have been documented, and their basement lies along different elytral areas (opaque versus hyaline), especially in larger specimens, and second, along posterior elytral margins, some small macrotubercles might proceed from a low conical stiff structure into a larger, stiff one as elytra continues growing peripherally, whereas adjacent fimbriae are shape-conservative, and do not seem to re-shape themselves into small macrotubercles.

Elytral morphology varies with growth in some species and not in others. Additional rows of macrotubercles are added with growth in Iphione ovata ( Piotrowski et al. 2024) , but not in I. readi sp. nov. as shown in Fig. 1 A–C based on three specimens from one lot collected in the Sudanese Red Sea (NMH 1941.4.4.168–172) that were 9–25 mm long, 7.0– 12.5 mm wide.

Neurochaetal rows of denticles

The number of rows of denticles on neurochaetae appears not to be a reliable diagnostic feature, because it varies substantially within species with size.

One median cirrigerous parapodium was removed from seven specimens from New Caledonia, two in I. hyndmani sp. nov. (UF 5689, 15 mm long, 8 mm wide; UF 5695, 28 mm long, 13 mm wide), and five others of I. fimbriata de Quatrefages, 1866 (UF 5020, 5025, 5620, 5656, 5677; 20–27 mm long, 10–13 mm wide), and four specimens of I. ankeri sp. nov. from the Mariana Islands (UF 134, 217, 1691, 1704; 12–15 mm long, 6–9 mm wide). The New Caledonia smaller specimen had 17–25 transverse rows of denticles in neurochaetae, whereas the larger specimen had 14–38 rows. Other New Caledonia specimens had 19–29 rows in the smallest specimen (UF 5656), and 28–44 in the largest one (UF 5677). Thus, some smaller specimens had 10–18 rows (UF 134, 1704), whereas the largest one (UF 217; 15x 9 mm) had 20–26 rows. Consequently, the number of transverse rows of denticles is size-dependent and is discarded as diagnostic. On the other hand, even though they can be finer along first two chaetigers, most Iphione species have neurochaetae subdistally swollen with falcate tips, and only one species ( I. hourdezi sp. nov., see below) has barely swollen neurochaetae, such that they can be regarded as acicular, with tips mostly straight.

Anatomy

The ventral surface is almost completely flat ( Fig. 2A ), with very shallow intersegmental borders, and a midventral longitudinal whitish band posteriorly. The digestive system is a straight tube, narrowing posteriorly ( Fig. 2B ); the pharynx extends 2/5 body length, connects to a long, funnel-shaped stomach, the connection lies within a rather homogeneous sheath, the stomach connects to the intestine and progressively narrow towards the posterior end. The pharynx and stomach walls do not stain with Methyl Green. The pharynx wall is very thick, about 4–5 times thicker than the stomach wall ( Fig. 2C ), and its connection includes an elastic collar that must be fully expanded when the pharynx is exposed. Two blunt enteric caeca project near the junction of the stomach and intestine. There are additional large, globular, lateral caeca entering parapodial coelom in chaetiger 8. Histological analysis in other aphroditoideans have indicated a very narrow enteric connection, and carmine injection has shown that gut contents do not enter the metameric lateral caeca ( Darboux 1900: 222); further, despite the presence of glandular epithelia, the role of lateral caeca in digestion is not completely understood.

Dissection of the pharynx revealed upper and lower jaws. Middorsal and midventral papillae at the apex of the everted pharynx are larger than the others; jaws have a roughly triangular shape, with an apical fang and two accessory denticles, the latter larger in upper ( Fig. 2D ) than lower jaws ( Fig. 2E ).

The pharynx is cylindrical with 11 pairs of marginal papillae in all specimens having pharynx exposed. In dorsal view ( Fig. 3A ), the marginal papillae are lobate, almost of the same size, and arranged in a row except for with two middorsal papillae that are stacked one above the other; behind the papillae there is a smooth area, followed by a rugose surface. The same smooth area is also present ventrally behind the papillae ( Fig. 3B ). Upper and lower jaws are both paired and very close to each other. In both frontal and lateral views ( Fig. 3C, D ), the main fang and accessory denticles are conspicuous because they are darker than surrounding tissues. In lateral view the pharynx aperture is semicircular with upper and lower regions projecting further anteriorly than mid-lateral areas; a semicircular ridge (also seen in dorsal view) may function as the attachment site of the lateral retractor muscles, (motor muscles of Dales, 1962: 402, Fig. 7B ). Two specimens from the same locality and of different size (UF 411) had their pharynx exposed; in both cases, there are 11 pairs of marginal papillae ( Fig. 3E, F ) and the lateral ones are the smallest, and often difficult to be seen. Further, the smaller specimen has two accessory denticles, whereas the larger one has three, and in the larger specimen, behind the last exposed accessory denticle, there is another one still covered by integument, and it is noted because of its paler pigmentation. The number of accessory denticles may not be a diagnostic feature because it is size-dependent.

Iphione species can be separated by features of elytra, notopodia and neurochaetae (see also Piotrowski et al. 2024). Elytra can have fimbriae or lack them; if present, fimbriae filaments can be minute, small or elongate. Elytral macrotubercles vary in shape, number of rows and size relationships among them: macrotubercles can be low, cushion-shaped, conical to digitate or cylindrical, and arranged in one to more than two rows in adult specimens, and although most have macrotubercles decreasing in size posteriorly, sometimes this trend is reversed, or the difference between the first and second row can be very marked. Microtubercles are usually present along posterior elytral margin; most species have them with long filaments, and only one species has short filaments. The basal tubercle of dorsal cirri of notopodia is usually projected, but in a few species it can be indistinct. Neurochaetae of most species are subdistally swollen, in one species, they are rather acicular with usually unidentate tips, a few species have bidentate tips, and one species has hooded tips. The combinations of these features were used to prepare the key to species below.

Key to species of Iphione Kinberg, 1856

1 Elytra with macrotubercles arranged in 2 or more rows, never cushion-shaped, rarely marginal........................ 2

- Elytra with macrotubercles arranged in a single row, cushion-shaped (falcate in juveniles), along posterior elytral half; fimbriae minute............................................................................................. 14

2(1) Elytra with margins fimbriate............................................................................ 3

- Elytra with margins smooth, non-fimbriate................................................................ 11

3(2) Fimbriae well-developed, as long or longer than macrotubercles................................................ 4

- Fimbriae minute, smaller than macrotubercles............................................................. 10

4(3) Macrotubercles distinct, arranged in up to 5 rows............................................................ 5

- Macrotubercles small, arranged in up to 10 rows; fimbriae along lateral and posterior margins................................................................................................. I. henshawi Pettibone, 1986 Hawaii

5(4) First row of macrotubercles slightly larger than those present in other rows........................................ 6

- First row of macrotubercles markedly larger than those present in other rows; macrotubercles in 2—three rows............................................................................................ I. readi sp. nov. Red Sea

6(5) Fimbriae length less than 1/10 minimal elytral width......................................................... 7

- Fimbriae length about 1/5 as long as minimal elytral width; macrotubercles in 1—two rows along posterior elytral margin............................................................................ I. richeri sp. nov. New Caledonia

7(6) Dorsal cirrophores with distinct basal tubercle.............................................................. 8

- Dorsal cirrophores with basal tubercle indistinct; elytra with 3–4(5) rows of macrotubercles..................................................................................................... I. hyndmani sp. nov. Hong Kong

8(7) Posterior elytral margins with microtubercles with long filaments............................................... 9

- Posterior elytral margins almost smooth (microtubercles with short filaments); median elytra with 2—three rows of macrotubercles............................................... I. muricata (Savigny in Lamarck, 1818), Mauritius

9(8) Median elytra with two rows of macrotubercles........................................... I. ankeri sp. nov. Guam

- Median elytra with 4–5 rows of macrotubercles...... I. fimbriata de Quatrefages, 1866 , Northeastern Australia, Torres Strait

10(3) Neurochaetae subdistally swollen, tips falcate; median elytra with macrotubercles in 2—three rows......................................................................................... I. malifera Piotrowski, 2014 Philippines

- Neurochaetae barely swollen subdistally, acicular, tips mostly straight; median elytra with macrotubercles in two rows.............................................................................. I. hourdezi sp. nov. New Caledonia

11(2) Neurochaetae unidentate.............................................................................. 12

- Neurochaetae bidentate............................................................................... 13

12(11) Elytra with macrotubercles conical................................................ I. ovata Kinberg, 1856 Hawaii

- Elytra with macrotubercles subcylindrical, tapered, with distal spines, arranged in 5–6 rows.... I. wilsoni sp. nov. Coral Sea

13(11) Elytral macrotubercles progressively smaller towards postero-lateral margin................................................................................................ I. coriolis Hanley & Burke, 1991 Chesterfield Islands

- Elytral macrotubercles progressively larger towards postero-lateral margin........... I. harrisae sp. nov. French Polynesia

14(1) Neurochaetae unidentate; cirrigerous parapodia with basal tubercle of dorsal cirrophore blackish distally, pale basally; ventral cirrostyles bases pale...................................................... I. treadwelli Pettibone, 1986 Hawaii

- Neurochaetae bidentate; cirrigerous parapodia with basal tubercle of dorsal cirrophore blackish basally, pale distally; ventral cirrostyles bases blackish............................................... I. corbariae sp. nov. Saya de Malha Bank

Figures

FIGURE 1. Iphione readi sp. nov. (incl. I. muricata sensu Savigny (1822)), non-type specimens, left elytra 7 of non-type specimens (NHM 1941.4.4.168–172), arranged vertically. A. 9 mm long specimen. B. 16 mm long specimen. C. 23 mm long specimen. D. Iphione muricata (Savigny in Lamarck, 1818) non-type small specimen (11.5 mm long, MAGNT W2894), elytron 6 (E, F indicate areas enlarged in E and F, and asterisk indicates the enlarged area in G). E. Close-up of macrotubercle (Mt) and fimbriae. F. Same. G. Close-up of microtubercles along posterior margin. Scale bars: A, 0.4 mm; B, D, 0.5 mm; C, 0.8 mm; E, F, 100 µm; G, 70 µm.

FIGURE 2. Iphione ovata Kinberg, 1856, non-type specimens (2 ECOSUR 0000, Sta. 30, 13 mm long). A) Ventral view. B. Ventral body wall and most muscle bundles removed, oval masses are ovaries. C. Pharynx and gut ventral wall removed (*: enteric caeca). D. Pharynx, upper jaws separated medially. E. Pharynx, lower jaws separated medially (Pa: papilla, Ph: pharynx, St: stomach). Scale bars: A, 1.38 mm; B, 1.43 mm; C, 1.48 mm; D, 0.32 mm; E, 0.27 mm.

FIGURE 3. Pharynx features. A. Iphione henshawi Pettibone, 1986, non-type specimen (BPBM R481), anterior end, pharynx exposed, dorsal view. B. Same, ventral view. C. Same, frontal view of pharynx (numbers indicate papillae). D. Same, left lateral view. E. Iphione muricata (Savigny in Lamarck, 1818), restricted, non-type specimens (UF 411), smaller specimen (9 mm wide), pharynx, frontal view (numbers indicate upper papillae). F. Another, larger specimen (16 mm wide), pharynx, frontal view (numbers indicate upper papillae). Scale bars: A, B, 1.3 mm; C, 0.9 mm; D, 0.7 mm; E, 0.3 mm; F, 0.6 mm.

FIGURE 7. Iphione fimbriata de Quatrefages, 1866, reinstated, holotype (MNHN POLY TYPE 325). A.Anterior region, dorsal view. B. Left elytron 7, after brushing off sediment, dorsal view (inset: close up of dirty to clean fimbriae). C. Chaetiger 16, left parapodium, posterior view. D. Chaetiger 12, left parapodium, after removal of notochaetae and Methyl green stain. E. Same, upper notochaetae. F. Same, lower neurochaetae. Scale bars: A, 1.7 mm; B, 1 mm; C, 0.6 mm; D, 0.5 mm; E, 170 µm; F, 200 µm.