Towards a better understanding of the genus Sciurella Allman, 1883 (Cnidaria: Hydrozoa: Plumulariidae): evidence from an integrative study Author Galea, Horia R. Hydrozoan Research Laboratory, 405 Chemin Les Gatiers, 83170 Tourves, France. Author Maggioni, Davide 0000-0003-0508-3987 Università degli Studi di Milano-Bicocca, Dipartimento di Scienze dell’Ambiente e della Terra, Piazza della Scienza 1, 20126 Milano, Italy. davide. maggioni @ unimib. it; https: // orcid. org / 0000 - 0003 - 0508 - 3987 & Università degli Studi di Milano-Bicocca, Marine and High Education (MaRHE) Center, 12030 Faafu Magoodhoo, Republic of the Maldives. davide.maggioni@unimib.it Author Di Camillo, Cristina G. 0000-0002-4031-8158 Università Politecnica delle Marche, Dipartimento di Scienze della Vita et dell’Ambiente, Via Brecce Bianche, 60131 Ancona, Italy. c. dicamillo @ univpm. it; https: // orcid. org / 0000 - 0002 - 4031 - 8158 c.dicamillo@univpm.it text Zootaxa 2021 2021-09-20 5040 1 1 32 journal article 10.11646/zootaxa.5040.1.1 1175-5326 5530885 519AA954-9B8F-4903-8379-E30704ABC375 Sciurella indivisa Allman, 1883 Figs 1–7 , 19 , 20 ; Table 2 Sciurella indivisa Allman, 1883: 9 , 15, 23, 26, pl. 5 figs 1–4.— Allman, 1888 : lxv, lxix.— Kirkpatrick, 1890: 609 .— von Lendenfeld, 1885a: 479 .— von Lendenfeld, 1885b: 626 .— von Lendenfeld, 1885c: 644 .— von Lendenfeld, 1887: 28 .— Nutting, 1900: 15, 31.— Billard, 1908: 759 .— Bedot, 1916: 196 .— Bedot, 1917: 17 , 18.— Bedot, 1918: 231 .— Van Praët, 1979: 933.— Di Camillo et al ., 2008: 1592 . Nemertesia indivisa — Billard, 1910: 38 .— Billard, 1913: 60 , fig. 50.— Bedot, 1917: 18 .— Bouillon et al ., 2006: 369 .— Ramil & Vervoort, 2006: 123. Nemertesia sp. 1 — Schuchert, 2015: 348 , fig. 20. non Sciurella indivisa —Kirckpatrick, 1890: 604, 609 [= Sciurella cylindrica ( Kirchenpauer, 1876 ) ]. non Nemertesia indivisa — Schuchert, 2003: 215 , fig. 63 [= Sciurella cylindrica ( Kirchenpauer, 1876 ) ]. Material examined. MNHN H.L. 1373, Australia , QLD, Cape York , Somerset Island: a slide mounted by A. Billard containing a 2.4 cm long, unstained stem fragment bearing distally a gonotheca [this is part of the type material housed in the Natural History Museum, London, UK ; the slide is labelled in Billard’s handwriting « Sciurella indivisa Allm. / type du Challenger / Nemertesia indivisa (Allm.) / 9.X.1908 ].— MNHN H.L. 1374: a slide (with the same label as the preceding one) mounted by A. Billard, containing three unstained cladia, of which one was detached from the stem together with its apophysis and a pair of gonothecae.—MHNG-INVE-0137405, Indonesia , North Sulawesi , North Minahasa Regency, Bunaken Marine Park, Manado Tua I., 1.623017°, 124.714263°, 25 m , 15 Feb. 2005 : several stems and fragments up to 8.5 cm , detached from substrate above insertion on hydrorhiza; a 5 cm high stem bears distally many female gonothecae, the others are sterile.—MHNG-INVE-0137406, Indonesia , North Sulawesi , North Minahasa Regency, Bunaken Marine Park, Siladen I., 1.626414°, 124.802058°, 20 m , 20 Feb. 2005 : several stems and fragments up to 6.4 cm high, all sterile.—MHNG-INVE-0091092, Japan , Okinawa I., 26.713720°, 127.878600°, 29 m , 19 Jun. 2008 : DNA extracted from a portion of colony identified by Schuchert (2015) as Nemertesia sp. 1 , GenBank: MZ 099712 (16S), MZ 348925 (18S), MZ 099659 (28S). Description. Colonies forming clumps of several stems growing on dead corals, with no evident hydrorhizae ( Fig. 1A ); stems up to 8.5 cm high, simple or forked, monosiphonic, with canaliculate coenosarc ( Fig. 5H ), divided into a regular succession of moderately long internodes by means of deep, transverse constrictions of the perisarc ( Figs 2B–D ; 5A–C ); each internode with several apophyses supporting the cladia, and a varied number of nematothecae on surface ( Figs 3A ; 5B, C ); there are generally 4 apophyses, occasionally as few as 2 or 3, or as many as 5, 6 or 8, their number being directly related to the length of the internode; apophyses in younger, slenderer stems given off irregularly ( Fig. 2B ), but showing a distinct tendency to adopt a bipinnate arrangement in older, thicker stems (two opposite, or nearly so, cladia near to the proximal node, and two opposite, or nearly so, cladia near the distal node; Fig. 2D ); apophyses relatively short, pointing upward, bearing a conspicuous, adcauline mamelon with broad, circular aperture, two pairs of axillar nematothecae inserted on each side at the origin from internode, as well as an unpaired, central nematotheca above ( Fig. 3B, C, E ) (the latter only present when the apophysis is not situated just below the distal stem internode, Fig. 3D ); stem internodes with a belt of several nematothecae near the proximal node, as well as a number of nematothecae irregularly scattered on the surface of the internode, each nematotheca in relation to a given coenosarcal tube ( Figs 3A ; 5B, C ). Cladia given off at ca . 45° with the stem, up to 11 mm long, delimited or not from the corresponding stem apophysis by a proximal, oblique node; the presence of a first, short, quadrangular, ahydrothecate internode provided with an adaxial nematotheca (exceptionally two) is nearly constant in one stem ( Fig. 3A, B ), but decidedly absent ( Figs 3C ; 5D ) in others, including the fertile stem; remainder of cladium homomerously-divided, composed of a regular succession of up to 18 hydrothecate internodes separated by slightly oblique, distinct nodes; each internode moderately long, with a hydrotheca in middle, spanning about half its length, and its complement of three nematothecae; two internal perisarcal ridges, one proximally and one distally ( Fig. 4A, B ) (the former absent in proximal most cormidium, Fig. 3A, C ). Hydrotheca long, tubular, fully adnate ( Figs 4B ; 5E ), abaxial wall distinctly thick, straight for most of its length, imperceptibly concave proximally and slightly flared distally; adaxial wall straight, with perisarc thickened laterally at junction with the internode behind ( Figs 3C ; 4B ); base concave, hydropore set next to the origin of abaxial wall; aperture transverse, circular in apical view, rim even, except for two lateral sinuations at fusion site with the internode behind; three nematothecae, of which one mesial, on a conspicuous projection, far below the hydrothecal base ( Figs 4K ; 5E ), and a pair of laterals ( Figs 4A, I, J ; 5E–G ); hydranths contracted, column elongated (filling most part of the hydrothecal lumen), distally provided with a reduced number of filiform tentacles. All nematothecae, including those of the stem, relatively short, movable and bithalamic; rim of upper chamber deeply scooped adaxially ( Fig. 4J, K ). Gonothecae occurring in pairs, given off from each side of the stem apophyses, just below the mamelon ( Figs 6A ; 7B–F ); female in present material; body broadly ovoid in frontal view, provided with a number of prominent, conical spines, generally arranged in three lateral pairs, one unpaired apically, and 1–2 abaxial ones ( Figs 6B ; 7E ); each spine with 1–2 nematothecae, of which one is apical, and the second commonly basal, although it could be borne in the middle of the spine ( Fig. 7G ); each spine is served by an independent coenosarcal tube derived from the central spadix, each branch ending up in a nematophore ( Fig. 6A ); occasionally, some spines could be bifid, and some nematothecae unrelated to a spine, but simply borne on the surface of the gonotheca; in lateral view, the gonotheca appears distinctly flattened dorsoventrally, and is concave on its adaxial side and convex on the abaxial side; it is widest in middle, and thins out toward its margins; a circular aperture is borne on a small projection of the adaxial side ( Fig. 6C , arrowhead); two large, spherical oocytes are contained within each gonotheca, and subsequently released and confined to a «brooding chamber» formed by the adaxial wall of the gonotheca with the corresponding stem internode ( Fig. 7F ). Color in life: cauli pale-brown, cladia white, female gonothecae translucent, oocytes white, spadix brown. FIGURE 1. In situ photographs of Sciurella indivisa Allman, 1883 . A . Colony from Bunaken. B . Fertile stem from Sebayur Kecil Island, Komodo National Park (photo courtesy of Lindsay Warren). C, D . Details of a fertile stem from Bunaken showing many gonothecae with their branched blastostyles and embryos developing in brooding chambers formed by the thecae with the stem. FIGURE 2. Details of four different stems of Sciurella indivisa Allman, 1883 , showing variation in the arrangement of cladia: verticils of three (A), irregular (B), alternate (C), bipinnate (D). From samples: MNHN H.L. 1373 (A – type material) and MHNG-INVE-0137405 (B–D); stems in A and B are fertile (portions with gonothecae not shown). Scale bar: 1 mm. FIGURE 3. Structure of the stem in Sciurella indivisa Allman, 1883 . A . Internode (only the “frontal” cladia are shown). B–D . Three stem apophyses supporting cladia, with (B) or without (C, D) proximal nematothecate internode (N.B.: Only the “frontal” pair of axillar nematothecae is depicted in B–D). E . Detail of the axil of a stem apophysis in apical view, showing mamelon and lateral pairs of nematothecae. From samples: MHNG-INVE-0137405 (A–C, E), MNHN H.L. 1373 (D – type material). Scale bars: B–E = 200 µm; A = 500 µm. 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. Remarks. In one stem from Siladen, nearly all cladia begin with a short, quadrangular, nematothecate internode ( Fig. 3A, B ), while in some others it is either occasionally present or totally absent ( Fig. 3C ). As no signs of damage followed by subsequent regeneration could be noted, it is assumed that its occurrence is variable in this species. Its presence is also illustrated by Allman (1883 : pl. 5, figs 2–3) in his original account, but does not seem to occur in all stems, as demonstrated here through the reinspection of the type ( e.g. MNHN H.L. 1373, Fig. 3D ), nor in the material assigned by Schuchert (2015: 348 , fig. 20B) to Nemertesia sp. 1 (see below a discussion on this material). FIGURE 5. SEM study of Sciurella indivisa Allman, 1883 (part). A . Portion of stem. B, C . Two close-ups showing the pattern of the insertion of cladia. D . Detail of a stem apophysis supporting a cladium, showing its associated nematothecae. E–G . Three cormidia in various views. H . Cross-section through both a stem and a gonotheca, showing the canaliculate coenosarc and ramified blastostyle, respectively. All from sample MHNG-INVE-0137405. FIGURE 6. Gonotheca of S. indivisa Allman, 1883 . A . Portion of fully fertile stem. B–D . Gonothecae seen frontally (B, D) and laterally (C); note aperture in C (arrowhead). From samples: MHNG-INVE-0137405 (A–C), MNHN H.L. 1374 (D – type material). Scale bars: B–D = 300 µm; A = 500 µm. In some stems, the cauline apophyses give rise occasionally to two cladia, one in the normal position, while the other is given off laterally from below one side of the mamelon, through a short athecate apophysis, followed by a quadrangular, nematothecate segment. Stems of this species reportedly reach as much as 25 cm in height ( Allman 1883: 26 , «ten inches»). According to the original account, the cladia are arranged «in four longitudinal alternating series» ( Allman 1883: 26 ), but verticils of three were found in the part of the type material (MNHN H.L. 1373) examined here ( Fig. 2A ). In the quite rich material of the Siboga , the cladia are reportedly said either scattered or verticillate 16 . In some of the youngest stems from Bunaken examined here, the cladia are either alternately-arranged ( Fig. 2C ) or decidedly scattered to spirally-arranged ( Fig. 2B ), while in the oldest ones, they adopt a rather bipinnate arrangement ( Fig. 2D ). The adequate understanding of the morphology of the fully-formed gonotheca was a gradual process. Allman (1883: 26) described it as «urn-shaped in front view, with two symmetrically placed hollow lateral processes near the distal end», and «compressed laterally, and when viewed in profile is seen to have its axis curved backwards nearly in a semicircle». Later on, Billard (1908) , upon the reexamination of the type , described the gonothecae as concave, 16 “They are either scattered or verticillate” ( Billard 1913: 60 ) [translated from French]. FIGURE 7. SEM study of Sciurella indivisa Allman, 1883 (continued). A . Portion of a fully fertile stem. B–F . Detailed views showing the morphology of the gonothecae. G . Close-up of the dorsal side of a gonotheca, showing the distinctive spines and their associated nematothecae. H . Detail of a nematotheca. All from sample MHNG-INVE-0137405. 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. with an irregular outline, their distal part being provided with three lobes 17 . Even later, Billard (1910) , evidently having been in possession of the hydroid collection of the Siboga , stressed again the lobate condition of the gonothecae, while specifying that they were both inaccurately drawn by Allman and imprecisely described earlier by himself 18 . Finally, he reiterated ( Billard 1913 ) the statements from his 1910 work in nearly the same words, and provided an illustration of two gonothecae, one seen frontally and the other almost in profile view ( Billard 1913 : fig. L). Unlike the gonothecae met with in our specimens from Bunaken ( Figs 6B ; 7A–G ), they were provided with much broader, bifid or even trifid marginal lobes, only the proximal most still adopting an elongated, conical shape. The two gonothecae present on slide MNHN H.L. 1374 are certainly not those depicted by Billard, as they only bear simple, conical projections; one of them is illustrated in Fig. 6D herein (the other is even more crushed). Consequently, it is difficult to tell whether Billard’s illustrations are either diagrammatic representations or real gonothecae with much more structurally complex shapes than those examined in the course of the present study. In light of the data provided by Billard (1913) 19 upon the examination of numerous specimens, it seems that the structure of the stem apophyses supporting the cladia is the same as that met with in our material, i.e. two pairs of nematothecae flank an apophysis provided adaxially with a conical mamelon ( Fig. 3E ), while an uneven nematotheca is found a short distance above on the stem internode ( Fig. 3B, C ). The same also results from the examination of specimen MNHN H.L. 1373 belonging to the type series ( Fig. 3D – note in this example the absence of the unpaired, superior nematotheca due to the proximity of a distal node). A similar situation occurs in the Japanese material assigned to Nemertesia sp. 1 by Schuchert (2015 : fig. 20B). In addition, the bipinnate arrangement of their cladia along the stems, and the relatively long cormidia provided both proximally and distally with an internal, annular ridge towards the nodes (compare Fig. 4F and 4B ), suggests that his material is, with little doubt, S. indivisa . Cladial internodes in S. indivisa are highly variable in length: those of the type series (specimens MNHN H.L. 1373 17 “[…] in the preparations of the type species that I have examined, the distal part of the gonothecae is lobed (three lobes), instead of being entire. These gonothecae are thus irregular in shape and, additionally, are concave-convex, instead of being planar” ( Billard 1908: 759 ) [translated from French]. 18 “ The gonothecae are not accurately illustrated by Allman either; their distal part is irregularly lobed, instead of being entire, like in Allman’s drawing, or provided with three lobes, as I stated earlier […]. They are, additionally, concave-convex, instead of being planar; their concavity faces the stem, so as to form a sort of brooding chamber, as I was able to document it in the specimens gathered by the « Siboga » Expedition” ( Billard 1910: 39 ) [translated from French]. 19 “The apophysis supporting the hydrocladium is provided with two pairs of axillar nematothecae and a basal mamelon bearing an aperture; there is a stem nematotheca above the insertion of hydrocladia” ( Billard 1913: 60 ) [translated from French]. and 1374) are quite short ( Figs 4E and 4D , respectively), while those in material from Bunaken are comparatively longer ( Fig. 4B, C ), especially above the hydrotheca. Such size variations were also noted by Billard (1913) in the abundant material of the Siboga . The hydrothecae, too, similarly display varied depths (compare Figs 4B, C, F and 4D, E ; see also Table 2 ). Distribution. Australia : Cape York, QLD ( Allman 1883 ). Indonesia : Sape Strait, between Sumba and Komodo islands ( Siboga Stn. 49); W of Jampea I., Selayar Islands Regency ( Siboga Stn. 65); Borneo bank, off SE Kalimantan ( Siboga Stn. 77); between Misool I. and West Papua , Raja Ampat Regency ( Siboga Stn. 164); off the W coast of Kur I., Moluccas ( Siboga Stn. 250); NE of Aru Islands Regency ( Siboga Stn. 274); Sailus Besar I., Pangkajene Dan Kepulauan Regency ( Siboga Stn. 315) ( Billard 1913 , as Nemertesia indivisa ); Bunaken Marine Park, North Minahasa Regency (present study); Komodo National Park, West Manggarai Regency (present study; N.B.: the specimen illustrated in Fig. 1B was not sampled and therefore not included in the specimens examined in the formal identification). Japan : Okinawa I. ( Schuchert 2015 , as Nemertesia sp. 1 ) ( Fig. 19 ). Depth range: 9–29 m (compiled from the references given in the synonymy and our data).