Mycale (Mycale) loveni ( Fristedt, 1887 )

Dinn, Curtis, Ott, Bruce, Bouchard Marmen, Mariève, Steeves, Royce, Côté, Geneviève, Hayes, Vonda, Nozères, Claude, Everett, Meredith V., Powell, Abigail & Chu, Jackson W. F., 2023, Two large structure-forming sponges from opposite North American coasts: a taxonomic review of Arctic-Pacific Mycale (Mycale) loveni and the description of a new Arctic-Atlantic Mycale, Canadian Journal of Zoology 101 (9), pp. 807-823 : 809-812

Mycale (Mycale) loveni ( Fristedt, 1887)

( Figs. 2 and 3 and Table 1 )

SYNONYMS: Clathria loveni Fristedt, 1887 , Esperella bellabellensis Lambe, 1905 , Esperella fisheri de Laubenfels, 1926 , Esperia loveni ( Fristedt, 1887) , Myclae (Carmia) bellabellensis ( Lambe, 1905) , Mycale bellabellensis ( Lambe, 1905) , Mycale fisheri ( de Laubenfels, 1926) , and Mycale loveni ( Fristedt, 1887) .

DIAGNOSIS: Stalked sponge with a cavernous funnel- or tubeshaped body, though specimens may be highly polymorphic and attain massive forms. Sponge body varies in size from a few centimetres in length to over one metre in funnel-shaped specimens. Generally found in deep water (> 200 m), though the holotype (22 m) and other specimens have been collected in shallow water ( Fristedt 1887). The sponge body varies in size from a few centimetres in length to over one metre in funnel-shaped specimens.

MATERIALS EXAMINED:

Mycale cf. bellabellensis ( Lambe, 1905) , RBCM 978-00084 - 002 , Edge of Clayoquot Canyon , British Columbia, Canada, 48.955 ◦ N, 126.415 ◦ W, 201 m depth, collected by PBS/JAT, 26 May 1962.

Mycale (Mycale) loveni ( Fristedt, 1887) , RBCM 003-00036 - 002 , off southern Alaska, USA, 55.883 ◦ N, 153.75 ◦ W, 228 m depth, collected by PBS, 1963.

Mycale (Mycale) loveni ( Fristedt, 1887) , RBCM 009-00134 - 005 , Dixon Entrance , British Columbia, Canada, 54.45 ◦ N, 131.7 ◦ W, collected by Pacific Biological Station ( PBS), 12 August 1965.

Mycale (Mycale) loveni ( Fristedt, 1887) , NA086-086-03, West of Olympic Peninsula , Washington, USA, 48.2503 ◦ N, 125.0129 ◦ W, 257 m depth, collected by NOAA, 26 August 2017.

Mycale (Mycale) loveni ( Fristedt, 1887) , NA086-102, West of Olympic Peninsula , Washington, USA, 48.129 ◦ N, 125.084 ◦ W, 276 m depth, collected by NOAA, 28 August 2017.

Mycale (Mycale) loveni ( Fristedt, 1887) , NA086-103-01, West of Olympic Peninsula , Washington, USA, 48.129 ◦ N, 125.084 ◦ W, 276 m depth, collected by NOAA, 28 August 2017.

Mycale (Mycale) loveni ( Fristedt, 1887) , SH1812-039, Daisy Bank , off Salem Oregon USA, 44.665 ◦ N, 124.809 ◦ W, 342 m depth, collected by NOAA, 15 October 2018.

Mycale (Mycale) loveni ( Fristedt, 1887) , SH1812-091, Mendocino Ridge , northern California, USA, 40.2873 ◦ N, 124.6901 ◦ W, 364 m depth, collected by NOAA, 20 October 2018.

Mycale (Mycale) loveni ( Fristedt, 1887) , SH1812-190, Santa Lucia Bank , central California, USA, 34.679 ◦ N, 121.172 ◦ W, 549 m depth, collected by NOAA, 1 November 2018.

Mycale (Mycale) loveni ( Fristedt, 1887) , SH1812-245, Sverdrup Bank , southern California, USA, 33.140 ◦ N, 120.356 ◦ W, 263 m depth, collected by NOAA, 6 November 2018.

Mycale (Mycale) loveni ( Fristedt, 1887) , RL1905-069B, Wind Farm West , central California, USA, 35.062 ◦ N, 121.532 ◦ W, 706 m depth, collected by NOAA, 30 October 2019.

Mycale (Mycale) loveni ( Fristedt, 1887) , NA121-057B, Quinault Canyon, WA, USA, 47.2179 ◦ N, 124.9047 ◦ W, 325 m depth, collected by NOAA, 27 September 2020.

Mycale (Mycale) loveni ( Fristedt, 1887) , NA121-145B, Grays Canyon , Washington, USA, 46.9137 ◦ N, 124.8914 ◦ W, 294 m depth, collected by NOAA, 1 October 2020.

COMPARATIVE MATERIAL EXAMINED: Syntype: Esperella bellabellensis Lambe, 1905 , CMNI 1994-0038 / CMNI 1994-0039 , off Bella Bella , Campbell Island, British Columbia, Canada, 52.17 ◦ N, 128.17 ◦ W, 549 m, collected by F. Landsberg, 1904.

EXTERNAL APPEARANCE ( Figs. 2A, 2B, 2D , 3A, 3B, and 3C ): The external morphology of Mycale (Mycale) loveni is variable. Most authors report M. (M.) loveni as being stalked, though some Gulf of Alaska specimens were reported as massive ( Stone et al. 2011). Fristedt’s (1887) original description from the Chukchi Sea depicts branching, thickly stalked specimens where lateral branches form subquadrangular cells filled with softer macerated tissue. Koltun (1959) reported Russian specimens (Chukchi, Bering, and Okhotsk Seas) with broad funnel-shaped stalks, though some specimens lack the large funnel. The surface is rough and may be grooved or microhispid. The colour while alive is greenish yellow to light yellow to brown. Consistency is somewhat compressible; it is not easily torn across spicule tracts, but smaller spicule tracts can be teased apart. Sponge tissue is easily removed from between the thick skeletal fibres and may be absent upon collection. Table 1 lists the outer morphologies that were examined and those from literature sources.

SKELETON ( Fig. 2C ): The choanosome is composed of branching and anastomosing thick, multispicular tracts composed of styles echinated at varying intervals by loose styles. Between these thick tracts, secondary tracts form polygonal reticulations 1200–1600 µm across, often partly infilled with style brushes. Anisochelae are concentrated on the surface of spicule tracts and scattered throughout. Spicule tracts expand into plumes at the surface, and spicules protrude 100– 200 µm beyond the surface singly or in groups. At the surface, tangential tracts of styles cross-connect these plumes, forming a polygonal reticulation with meshes highly variable in shape and dimension, from 300 to 1200 µm in diameter. Large anisochelae form rosettes that occur sparingly in the ectosome and choanosome. Single large and small anisochelae are scattered throughout the sponge and are concentrated in the outer tissue layer that covers living specimens.

SPICULES ( Figs. 2E–2L and 3D–3K and Table 1 ): From examined specimens, the spicule complement consists of styles as megascleres and anisochelae microscleres, usually clearly divisible into three size classes, each with somewhat different morphologies.

Measurements from CMNI 1994-0038:

Styles: 425– 456 –496 × 11– 13 –15.5 µm. Straight, sharp points may be lanceolate or mucronate. Styles either lack the constriction in the shaft just below the head found in most Mycale species (mycalostyles) or the constriction is slight.

Large anisochelae: 83– 88 –94 µm. Frontal alae are narrow, and slightly rounded. The free portion of the shaft is approximately 1/4 of the total spicule length. Rosettes are variably present and scattered throughout the sponge.

Medium anisochelae: 43– 54 –67 µm. Slight variations in shape are noted between a likely fan-shaped fragment (RBCM 003-00036-002, Figs. 2I and 2J ) and a club-shaped specimen (RBCM 978-00084-002; Figs. 3H and 3I ), where the alae are stouter in the club-shaped specimen. However, this variation is only visible at high magnification and may not be consistent between the two morphotypes.

Small anisochelae: 19– 22 –25 µm. Elongated. In some spicules, there is a miniscule median tooth-like extension arising from the lower alae along the upper rim, but most often this upper rim is flat.

GENETIC DATA: D13–E13 domains of 28S and ITS gene fragments were obtained from Pacific Mycale (Mycale) loveni specimens. Only about 40 bp overlapped in M. (M.) loveni ITS sequences due to low sequence quality from stutter artifacts following three successive homopolymer repeats greater than 9 bp in length ( Fazekas et al. 2010). Maximum likelihood trees comparing available Mycale ITS and D13–E 13 28S sequences resulted in a monophyletic clade for M. (M.) loveni ( Figs. 4 and 5 ). COI sequences for M. (M.) loveni were only obtained in one direction, so consensus sequences were not created; however, most of the top nucleotide BLAST search results for the single direction reads were members of the genus Mycale .

DISTRIBUTION AND ECOLOGY: Mycale (Mycale) loveni has a very wide distribution range that spans the Arctic and North Pacific oceans. The holotype originates from the Chukchi Sea ( Fig. 1A ), with records also identified from the Bering Sea, Aleutian Islands, Gulf of Alaska, and British Columbia, between 22 and 800 m depth. Records from NOAA’s national database for deep-sea corals and sponges ( Hourigan et al. 2015) show M. (M.) loveni to be particularly common around the Aleutian Islands and the Gulf of Alaska, which reflects the historical sampling intensity in this region. There are also sparse records as far south as California, within the Monterey Bay National Marine Sanctuary ( Hourigan et al. 2015). From ROV observations off British Columbia, Canada, in situ sponges were commonly attached to hard substratum ranging in size from small cobbles to exposed bedrock. The usual stalked morphology of M. (M.) loveni may allow this species to inhabit areas inimical to sponge growth once the larvae successfully settle. Mycale (Mycale) loveni was observed to be a common, large, habitat-forming demosponge at Learmonth Bank, Dixon Entrance in sites that were dominated by the abundance of several large glass sponge species, notably Farrea sp. , Aphrocallistes vastus ( Schulze, 1886) and Heterochone calyx ( Schulze, 1886) ( Chu 2010) . Other fauna co-occurring with M. (M.) loveni include Sebastes spp. rockfish, alcyonacean corals such as Primnoa pacifica Kinoshita, 1907 , cup corals, other small corals, crinoids, anemones, holothurians, brachiopods, and sponges ( Chu 2010).

REMARKS: The specimens analyzed here are consistent with Fristedt’s (1887) original description of C. loveni . Fristedt described an erect and irregularly ramous specimen with several slender branches issuing from a firm stalk, and the branches form a mesh that is filled with softer tissue. The styles of this species were described to be thickest near the pointed end, and this holds true for most of the examined specimens; however, the more hastate spicules as described by Koltun (1959) are not present in all specimens. Here we also suggest that the species has three size categories of anisochelae rather than two. This is contrary to Fristedt’s original description, which does not mention a small size category, while de Laubenfels (1932) reported four size categories for large specimens that he considered as Mycale bellabellensis . In most specimens, the separation of anisochelae size categories by length alone is possible using a light microscope, but the spicule shape between the medium- and smallsize categories is noticeably different when viewing spicules using SEM. The syntype of Esperella bellabellensis was initially described by Lambe (1905) as having only large anisochelae with many immature anisochelae, and small sigmas. After examination of the syntype, it is clear that there are three size categories of anisochelae ( Table 1 ), and the sigmas drawn by Lambe were seen in the prepared slides, though they are unlikely to be spicules but rather contamination of the slide.

Stone et al. (2011) synonymized M. (M.) loveni and M. bellabellensis and suggested that different morphotypes of the species are geographically isolated, with club-shaped specimens occurring in the Gulf of Alaska and vase/funnel-shaped specimens occurring in the Aleutians. However, the various morphotypes examined herein are present throughout the range of the species ( Table 1 ). Several morphotypes were observed during an ROV dive at Learmonth Bank ( Figs. 2B–2D and 3C ) ( Chu 2010). Despite some variation in spicule shape between specimens seen using SEM, we maintain that the species is simply highly polymorphic.

Figures

Fig. 2. Mycale (Mycale) loveni fan- and vase-shaped specimens. (A) RBCM 003-00036-002, (B) specimen from Learmonth Bank BC, (C) skeleton from CMNI 1994-0038, and (D) specimen growing among Heterochone calyx sponges from Learmonth Bank, BC. (E– L) Spicules from RBCM 003-0036: (E, F) styles; (G, H) large anisochelae; (I, J) medium anisochelae; and (K, L) small anisochelae (underwater photos: Leys, Tunnicliffe, CSSF).

Fig. 3. Mycale (Mycale) loveni tube- and club-shaped specimens. (A) RBCM 978-00084-002. (B) Detail of dense fibres throughout the sponge. (C) Specimen from Learmonth Bank, BC. (D–K) Spicules from RBCM 978-00084-002: (D, E) styles; (F, G) large anisochelae; (H, I) medium anisochelae; and (J, K) small anisochelae (underwater photo: Leys, Tunnicliffe, CSSF).

Fig. 4. Maximum likelihood phylogenetic tree of ITS1, 5.8S, and ITS2 rDNA constructed with the Jukes–Cantor model in MEGA X. This gene tree shows a monophyletic Atlantic Mycale (Mycale) lorea sp. nov. as a sister species of the Pacific Mycale (Mycale) loveni. Values at each node indicate bootstrap support generated from 1000 replicates.

Fig. 5. Maximum likelihood phylogenetic tree D13–E13 28S rDNA constructed with the Jukes–Cantor model in MEGA X. This gene tree shows a monophyletic Atlantic Mycale (Mycale) lorea sp. nov. as a sister species of the Pacific Mycale (Mycale) loveni. Values at each node indicate bootstrap support generated from 1000 replicates.

Fig. 1. Map of collection locations. (A) Pacific (Mycale (Mycale) loveni, holotype = star). (B, C) Atlantic (Mycale (Mycale) lorea sp. nov., holotype = star), museum specimens = squares, spicule measured specimens = circles, additional specimens identified visually = triangles. Other effective area-based conservation measures (OECMs) where sponges were collected or observed are outlined in pink. The figure was created using ArcMap version 10.8 (Esri, Inc., Redlands, CA, USA) and assembled from the following data sources: collection data sourced from Fisheries and Oceans Canada and NOAA; base map from GSHHG (Wessel and Smith 1996); contour lines from ETOPO1 (NOAA 2009).