Sciurella cylindrica ( Kirchenpauer, 1876 ) Galea & Maggioni & Di Camillo, 2021

Galea, Horia R., Maggioni, Davide & Di Camillo, Cristina G., 2021, Towards a better understanding of the genus Sciurella Allman, 1883 (Cnidaria: Hydrozoa: Plumulariidae): evidence from an integrative study, Zootaxa 5040 (1), pp. 1-32 : 14-24

Sciurella cylindrica ( Kirchenpauer, 1876) , comb. nov.

Figs 8–16 , 19 , 20 ; Table 2

Plumularia cylindrica Kirchenpauer, 1876: 26 , 34, 45, pl. 1 fig. 1.— Allman, 1883: 20.— Bale, 1884: 146.— Kirkpatrick, 1890:

609.— Bedot, 1912: 339.— Bedot, 1916: 180.— Bedot, 1917: 18.— Bedot, 1918: 216.— Bedot, 1921: 36. Plumularia cylindria Kirchenpauer, 1876 : pl. 4 fig. 1 (incorrect original spelling). Plumularia (Isocola) cylindrica (K.)— Calder & Brinckmann-Voss, 2011: 53. Nemertesia cylindrica (K.)— Bale, 1919: 350.— Pennycuik, 1959: 178.— Watson, 2000: 49, fig. 38.— Ramil & Vervoort, 2006:

121. Sciurella cylindrica (K.)— Bedot, 1921: 36.— Van Praët, 1979: 933. Antennularia cylindrica Bale, 1884: 146 , pl. 10 fig. 7.— von Lendenfeld, 1885a: 478.— von Lendenfeld, 1885b: 626.— von

Lendenfeld, 1885c: 642.— von Lendenfeld, 1887: 26.— Kirkpatrick, 1890: 609.— Bedot, 1917: 17.— Bedot, 1921: 36. non Nemertesia cylindrica (B.)— Nutting, 1927: 227 [= Sciurella dolichotheca ( Allman, 1883) ]. Sciurella indivisa — Kirkpatrick, 1890: 604, 609 (non Sciurella indivisa Allman, 1883 ). Nemertesia indivisa — Schuchert, 2003: 215, fig. 63 (non Sciurella indivisa Allman, 1883 ).

Material examined. MHNG-INVE-0137407, Indonesia, Bali, near Tulamben, -8.291824°, 115.609316°, 20 m, 29 Jan. 2020: a profuse colony composed of sterile stems up to 15 cm high, GenBank : MZ 099711 (16S), MZ 099675 (18S), MZ 099658 (28S).— AMS Y.617, Australia, Darwin, off Rail Pier, -12.46667°, 130.83333°, depth unknown, Jul. 1929: two stem fragments, one sterile, the other bearing female gonothecae, both as parts of a profuse colony, identified by J.E. Watson (unpublished) as Nemertesia cylindrica ( Kirchenpauer, 1876) .

Description. Colonies erect, up to 15 cm high, composed of clumps of basally adjacent stems arising from large masses of fibrous hydrorhizae anchored in sandy bottom; stolonal fibers slender, tortuous, irregularly branched, forming anastomoses, with straw colored perisarc enmeshing the proximal parts of the stems. Stems thick, slightly flattened laterally, with a bamboo-like appearance due to the presence of regular, very distinct nodes; occasionally forked, monosiphonic throughout, with shiny, copper-colored perisarc ( Fig. 8A ). Coenosarc appressed to the inner wall of stem perisarc, leaving an empty, broad, central lumen; coenosarc canaliculate, composed of numerous hollow tubes running parallel to the stem ( Fig. 10 , lower diagram), occasionally forming anastomoses, number gradually decreasing towards distal end; coenosarcal tubes joined laterally by common epidermis, the endoderm being restricted to the individual hollow tubes. Stems divided into internodes by means of broad, transverse to irregular to oblique nodes, with comparatively thinner, discolored perisarc ( Fig. 9 ); internodes rather short ( Figs 9 ; 11A ), slightly flattened laterally (left-right) ( Fig. 10 , lower diagram), with bulges at both ends; each internode bearing generally four cladial apophyses, a whorl of nematothecae just above the proximal bulge, as well as a number of irregularly scattered nematothecae on surface ( Figs 11A ; 12A, B ; 13A–D ), all nematothecae in relationship with the paths of the coenosarcal tubes; cladial apophyses short, given off at about 45° with the longitudinal axis of the stem, ending distally in slightly oblique node; each apophysis with a prominent, conical, mamelon (with rounded aperture) on adcauline side, and a number of nematothecae flanking it laterally, as well as in the axil formed with the stem internode (there were as few as 2 nematothecae on each side in the pinnate stems, and as much as 6 per side in the bipinnate stems) ( Figs 11B–D ; 12C–F ; 13E, F ). Each internode with one pair of cladia given off close to the proximal node and a second pair situated next to the distal node, plane of the first pair forming an acute angle with that of the second pair with respect to the antero-posterior aspect of the colony; cladia in each pair given off at the same level and diametrically opposed; lower and upper cladium on each side of the stem inserted on its lateral, flattened sides, and pointing out- and upwardly in the same direction, so that the cladia form two parallel, longitudinal rows on each side of the stem (bipinnate) ( Fig. 10 , upper diagram). This arrangement is generally constant throughout the stems, regardless the fact that some internodes (or even entire portions or stems) may bear as few as two hydrocladia or as much as six. Occasionally, wholly or partly simple-pinnate stems ( Fig. 9C ), or stems pinnate on one side and bipinnate on the opposite side ( Fig. 9B ), occur within the same colony. Cladia more or less distinctly delimited from their corresponding stem apophyses by slightly oblique nodes ( Fig. 11A–C ); up to 8 mm long, divided homomerously into up to 22 cormidia by means of slightly oblique nodes ( Fig. 15C ); each internode with a centrally-placed hydrotheca occupying more than half of its length, and its three associated nematothecae: one mesial and a couple of laterals ( Fig. 14A, B ); hydrotheca long, tubular, slightly tapering below, fully adnate adaxially, abaxial wall almost straight ( Fig. 14B ), aperture distal, circular ( Fig. 14C ), perpendicular to the long axis of theca, rim entire, lowered adaxially at junction with the internode behind ( Fig. 15D ). Mesial nematotheca borne on a small, proximal, abaxial protuberance of the internode ( Figs 14B, J ; 15D, E ); similar in shape to those of the stem; bithalamic, movable, with tall basal chamber and rather shallow upper chamber whose wall is distinctly scooped adaxially; lateral nematothecae borne on inconspicuous apophyses, movable; comparatively shorter and more globular than their mesial counterparts, wall of upper chamber similarly scooped adaxially ( Figs 14I ; 15E, F ). Hydranths contracted; the number of their filiform tentacles could not be ascertained. Gonothecae borne in pairs on the cladial apophyses of the stem, one confined to each side ( Fig. 16A–D ). Female gonothecae, the only ones examined here, pod-shaped ( Fig. 16B, D ), without pedicels ( Fig. 14L ), laterally flattened, curved adaxially ( Fig. 16A–C ), broadest in their lower third when seen frontally ( Fig. 16B, D ), distally provided with a slit-like, rounded aperture ( Fig. 16E ); perimeter bearing 6–8 nematothecae ( Fig. 16B–D ) similar in shape ( Fig. 16F ) to those of the trophosome; lumen of gonotheca filled with three large, spherical oocytes ( Fig. 8B ). Aberrant, conjoined twin gonothecae ( Fig. 16B ), occasionally occur. Color in life: cauli copper-colored, cladia orange. No live gonothecae were observed.

Remarks. The description of the trophosome given above is based on the profuse, though sterile, material from Bali (MHNG-INVE-0317407). The two stems, including one fertile, from Australia (AMS Y.617) are similar in structure, and the morphology of the gonotheca described above is based on one of them.

As noted in the description, the stems are generally unbranched; in a few instances, a stem internode gives rise (perpendicularly to a given, generally distally-placed, internode) to a secondary stem that rapidly curves upwards at an acute angle with the original stem, the secondary stem adopting a vertical posture, as well. Branched stems were also reported by Watson (2000: 49).

The number of cladia per stem internodes and their arrangement are variable, and the following situations were documented in the Balinese material: 1) the generally bipinnate structure can be locally altered, either within the same stem or among stems belonging to the same colony, with the occurrence of either entirely pinnate stems or pinnate portions ( Fig. 9C ), in the latter situation situated proximally and/or distally along a given stem; 2) an intermediate arrangement, with stems pinnate on one side and bipinnate on the opposite side ( Fig. 9B ); 3) while in the majority of stems the two proximal and the two distal cladia of an internode are diametrically opposed, there are cases in which the two proximal cladia are given off from one side of the stem, while the two distal cladia arise from its opposite side; 4) as noted above, the stems with a bipinnate arrangement of cladia generally have internodes bearing four cladia, but internodes with as few as two or as much as six cladia occur; 5) in the stems with simplepinnate cladia, each internode generally bears two alternate cladia, although internodes with one or three cladia are not uncommon ( Fig. 9B, C ).

As noted in the introduction, the synonymy of this species was, for a long time, a matter of debate. Plumularia cylindrica Kirchenpauer, 1876 was based on a syntype ( Table 1) and, although the general morphology of the cormidia in those specimens proves identical (compare Fig. 14F and 14G ), their cladia are reportedly said to have been inserted slightly differently in each of these materials 20. Unfortunately, this statement could not be checked, as the syntype material was destroyed by fire in 1943 (Helma Roggenbuck, pers. comm.) 21. Given some differences in the arrangement of cladia noted by some authors (see below) and the high similarities of their cladial internodes, it can be reasonably assumed that both materials were conspecific.

Antennularia cylindrica Bale, 1884 , whose holotype was not reexamined, is reportedly very similar to P. cylindrica (see footnote 5), and their respective cormidia are proportionally the same (compare Fig. 14E and 14F, G ), suggesting that both nominal species are undoubtedly conspecific, with Kirchenpauer’s hydroid having priority, under the combination Sciurella cylindrica ( Kirchenpauer, 1876) , comb. nov. (see below, under «Genetic results and discussion», our arguments in favor of maintaining the genus Sciurella as valid).

20 “The position of the hydrocladia is somewhat different in the specimens from the two localities, in that, in the Javanese one, it is not as decidedly opposite as it is in the others” ( Kirchenpauer 1876: 45) [translated from German].

21 The specimen from Zamboanga bore the catalogue number 3691, and that from Zamboanga the number 3692; both were housed in the Zoological Museum, Hamburg, Germany prior to their destruction during World War II.

Since no notable differences are exhibited by the cormidia of S. cylindrica compared to those of S. indivisa , some authors [e.g. Kirkpatrick (1890), followed by Billard (1908, 1910, 1913), Bedot (1917), Bale (1919), Pennycuik (1959), Schuchert (2003)] regarded them as conspecific. However, although sometimes discrete, size differences appear nevertheless constant among the materials examined in the course of this study: S. indivisa has always longer internodes compared to S. cylindrica and, occasionally, their distal end is provided with an internal, annular ridge of perisarc (compare Fig. 4A–F and 14B, D–H , respectively).

Short cormidia, similar to those present in our material, are met with in the sterile specimens identified by Schuchert (2003) as N. indivisa ( Fig. 14H ), suggesting that the correct specific assignation of his hydroid should be S. cylindrica . Its «laterally held hydrocladia […] directed towards sides, in opposite pairs» ( Schuchert 2003: 216, fig. 63B) further supports this assumption.

Watson (2000) discovered, for the first time, fertile specimens of a Nemertesia -like hydroid with deep hydrothecae and urn-shaped gonothecae provided with nematothecae, thus demonstrating that her material «cannot be N. indivisa » ( Watson 2000: 51) . The gonothecae in her specimens seem to have been even more ripe than those observed by us in sample AMS Y.617, as their apertures were wide open, and flanked by two blunt, lateral lobes of perisarc ( Fig. 14M ). In contrast, the most mature gonothecae we observed had slit-like, rounded apertures ( Fig. 16E ), while some others, decidedly immature, were closed ( Fig. 14L ).

Cormidia in Watson’s material (see her fig. 38B) are indistinguishable not only from those of the types of both Bale’s ( Fig. 14E ) and Kirchenpauer’s ( Fig. 14F, G ) nominal species, but also from those met with in the Balinese ( Fig. 14B ) and Australian ( Fig. 14D ) materials examined here, suggesting that all are conspecific.

As noted above, the insertion of cladia along the stem seems variable in this species. Kirchenpauer (1876: 45) described them as opposite, the four cladia of an internode actually adopting a bipinnate arrangement, a situation also met with in both Schuchert’s material (2003: fig. 63B) and ours from Bali. Bale (1884: 146), however, observed in his unique specimen of A. cylindrica that each stem internode bore «from one to three whorls of ramuli, each whorl consisting of three, which alternate in position with those above and below», a condition met with in the fertile Australian fragment studied herein (sample AMS Y.617). Watson (2000: 49) observed verticils «of up to eight around each internode, reducing to four or five in distal stem region». In our opinion, these differences are probably related to the age of each stem, similarly to the situation met with in S. indivisa (see remarks under that species).

The number of nematothecae associated to the cladial apophyses of the stem seems equally variable: «about five in and around each axil» ( Bale 1884), «up to four […] and 1–2 or more close to apophysis» ( Schuchert 2003), «two or three flanking mamelon at base of apophysis» ( Watson 2000), commonly 2–3 (but occasionally up to 4) in sample AMS Y.617, and from as few as 2 to as much as 6 in our pinnate and bipinnate stems, respectively, from Bali.

Distribution. Indonesia: Java [ Kirchenpauer (1876), as Plumularia cylindrica n. sp.]; Kei Islands [ Schuchert (2003), as Nemertesia indivisa ( Allman, 1883) ]; Bali (present study). Philippines: Zamboanga, ( Kirchenpauer 1876, as Plumularia cylindrica n. sp.). Australia: Port Curtis, QLD [ Bale (1884), as Antennularia cylindrica n. sp.; doubtful record, without description and figures, by Pennycuik [(1959), as N. cylindrica ( Kirchenpauer, 1876) ]; Murray and Warrior (= Tudu) islands, QLD [ Kirkpatrick (1890), as Sciurella indivisa Allman, 1883 ] ( Fig. 19 ). Depth range: 6–39 m (compiled from the references given in the synonymy and our data).

Figures

FIGURE 4. Cormidia of Sciurella indivisa Allman, 1883. A–F. Various cormidia in frontal (A) and lateral (B–F) aspects. G–K. Lateral (G, I, J) and mesial (H, K) nematothecae. From samples: MHNG-INVE-0137405 (A–C, I–K), MNHN H.L. 1374 (D, G, H – type material), MNHN H.L. 1373 (E – type material). Specimen in F is redrawn from Schuchert (2015, as Nemertesia sp. 1). Scale bars: G–K = 50 µm; A–F = 200 µm.

FIGURE 8. Sciurella cylindrica (Kirchenpauer, 1876). A. In situ photograph of a small, infertile stem from Tulamben, Bali (photo courtesy of Lindsay Warren), sympatric with the material dealt with herein. B. Detail of a preserved fertile stem bearing female gonothecae with visible oocytes, from sample AMS Y.617.

FIGURE 9. Details of three different stems of Sciurella cylindrica (Kirchenpauer, 1876) from the same colony, showing variation in the arrangement of cladia: bipinnate (A), transition from bipinnate to pinnate (B), pinnate (C). All from sample MHNG- INVE-0137407. Scale bar: 1 mm.

FIGURE 10. Diagrammatic illustration of the arrangement of hydrocladia along mature stems of Sciurella cylindrica (Kirchenpauer, 1876) from Bali, in lateral (above) and apical (below) views.

FIGURE 11. Structure of the stem in Sciurella cylindrica (Kirchenpauer, 1876). A. Internode showing the distribution pattern of the nematothecae. B, C. Cladial apophyses from two different stems, in lateral view. D. Detail of the axil of a cladial apophysis in frontal view, showing mamelon above and associated lateral nematothecae. From samples: MHNG-INVE-0137407 (A, B, D), AMS Y.617 (C). Scale bars: B–D = 200 µm; A = 500 µm.

FIGURE 12. Distribution of the stem nematothecae in Sciurella cylindrica (Kirchenpauer, 1876). A, B. Two portions of a stem, each showing a few successive internodes and their nematothecae. C–F. Close-ups of four cladial apophyses seen laterally, showing variation in the number of their associated nematothecae.All from sample MHNG-INVE-0137407. Scale bars: C–F = 200 µm; A, B = 500 µm.

FIGURE 13. SEM study of Sciurella cylindrica (Kirchenpauer, 1876) (part). A, B. Portions of stems with either bipinnate (A) and pinnate (B) arrangements of cladia. C, D. Details of internodes belonging to two different stems with bipinnate cladia. E, F. Details of stem apophyses supporting cladia from two different stems. From sample:s MHNG-INVE-0137407 (A, B, D, E) and AMS Y.617 (C, F). Scale bars: E, F = 100 µm; D = 200 µm; A–C = 500 µm.

FIGURE 14. Cormidia, nematothecae and gonothecae of Sciurella cylindrica (Kirchenpauer, 1876). A–H. Various cormidia in frontal (A), lateral (B, D–H) and apical (C) aspects. I–K. Lateral (I) and mesial nematothecae, the latter seen both laterally (J) and adaxially (K). L, M. Immature (L) and ripe (M) female gonothecae. From samples MHNG-INVE-0137407 (A–C, I–K), AMS Y.617 (D, L). Figure E is redrawn after Bale (1884, as Antennularia cylindrica), F and G after Kirchenpauer (1876, as Plumularia cylindrica; F from Java, G presumably from Zamboanga), H after Schuchert (2003, as Nemertesia indivisa), and M after Watson (2000, as Nemertesia cylindrica). Scale bars: I–K = 50 µm; A–H = 200 µm; L, M = 300 µm.

FIGURE 15. SEM study of Sciurella cylindrica (Kirchenpauer, 1876) (continued). A, B. Nematothecae associated to the stem apophyses supporting the cladia. C. Portions of cladia. D. Two cormidia from neighboring cladia seen laterally. E. Fronto-apical view of a cormidium. F. Latero-frontal view of a hydrotheca. From samples: MHNG-INVE-0137407 (A–D) and AMS Y.617 (E, F). Scale bars: B, F = 50 µm; A, D, E = 100 µm; C = 200 µm.

FIGURE 16. SEM study of Sciurella cylindrica (Kirchenpauer, 1876) (continued). A. Portion of fully-fertile stem. B–D. Female gonothecae (note aberrant twin gonotheca in B). E. Distal part of a gonotheca showing slit-like aperture. F. Nematothecae, note the adaxial emargination of the wall of their upper chamber. All from sample AMS Y.617. Scale bars: F = 25 µm; E = 50 µm; D = 200 µm; C = 300 µm; B = 500 µm; A = 2 mm.

FIGURE 19. Geographical distribution of Sciurella spp.

FIGURE 20. Plumulariidae phylogenetic hypothesis showing the position of Sciurella species (highlighted) in the family. Numbers at nodes show Bayesian posterior probabilities, maximum likelihood bootstrap values, and maximum parsimony bootstrap values, respectively.