Heterorotula lucasi Manconi & Copeland, 2022

Manconi, Renata, Copeland, John, Kunigelis, Stan & Pronzato, Roberto, 2022, Biodiversity of Nearctic inland water: discovery of the genus Heterorotula (Porifera, Spongillida, Spongillidae) in the Appalachian Mountains, with biogeographical implications and description of new species, ZooKeys 1110, pp. 103-120 : 103

Heterorotula lucasi Manconi & Copeland sp. nov.

Figs 1 , 2 , 3 , 4 , 5 , 6 , 7 , 8 , 9

Type locality.

Pigeon River 35.9396; -83.1786, Cocke County, Tennessee, USA.

Type data.

Holotype. USNM 1662182, entire specimen, 70% ethanol, coll. J. Copeland, 30 July 2013. Paratype. USNM 1662183, fragments, 70% ethanol. Pigeon River, Cocke County, Tennessee, USA, 35.9396; -83.1786, coll. J. Copeland, 30 July 2013.

Other material.

BMNH 1890.1.9.339, holotype, Heterorotula capewelli type species of genus Heterorotula . WAM Z27997 , FW-POR 881, Heterorotula multiformis ( Weltner , 1910) ( Australia), WAM Z98316 , FWPOR 883, Heterorotula cf. multidentata (Weltner, 1895) ( Australia) .

Diagnosis.

Heterorotula lucasi sp. nov. is characterized by (a) gemmuloscleres as spiny birotules with flat rotules (distal and proximal) of significantly different diameters with crenulated/notched to shallowly incised margins, (b) absence of skeletal microscleres, (c) skeletal acanthoxeas spiny, and (d) free (not sessile) gemmules.

Etymology.

The specific epithet lucasi refers to lux meaning light in Latin and is dedicated to Lucas Edward Copeland whose enthusiasm and love for the natural history of the forests and streams of the Appalachian Mountains of Tennessee resulted in many wonderful discoveries.

Description.

Adult sponges with gemmules. No brooded larvae were found. Growth form (Fig. 1C ) encrusting 1-4 mm in thickness and to 16 cm in diameter. Surface with irregular ridges, hispid from emerging spicules, and with a network of subdermal canals covered by a hyaline dermal membrane. Color tawny in vivo (Fig. 1C ), light yellow to light brown in alcohol (Fig. 1D ). Consistency of live sponge soft and fragile. Spongin scanty in skeletal network, arranged as irregular polygonal meshes, to abundant in gemmular Gemmular theca and basal spongin plate. Ectosomal skeleton of slender megascleres in paucispicular fibres, with no special architecture (Fig. 2B ) supports the dermal membrane. Choanosomal skeleton (Fig. 2A ) as a network of multi-spicular fibres, with scanty spongin. Basal spongin plate well developed.

Megascleres (Figs 2 , 3 ) fusiform acanthoxeas 223.1-335.0 μm (276.8 ± 24.7) in length and 7.7-13.7 μm (10.9 ± 1.0) in width, slightly curved, with variably dense spines except towards the variably pointed tips, to less frequently nearly spineless. Acanthoxeas shaft from slender in ectosomal area to stouter in the endosome. Microscleres absent.

Gemmules (Fig. 4 ) scattered in skeletal network, subspherical, 448-613 μm (528 ± 55.9) in diameter. Foramen simple (Fig. 4E, F ) with smooth undulate margins, slightly elevated above gemmule surface. Gemmular cage (Fig. 4C, D ) of acanthoxeas with small spines.

Gemmular theca trilayered ~50 μm in thickness (Fig. 5 ). Outer layer fibrous to compact with distal rotules more or less embedded (Fig. 5A, B, D ). Pneumatic layer well developed and thick, ranging in the same gemmule from mainly fibrous to chambered network of irregularly polygonal meshes of variable size (Fig. 5B, C ). Inner layer (Fig. 5A, D ) multilayered of 3-5 layers of compact spongin. Gemmuloscleres radially embedded (Fig. 5A, B ) as a dense monolayer in pneumatic layers of Gemmular theca , with distal smaller rotules partly covered by outer layer and proximal larger rotules, partly overlapping one to each other, not embedded into inner layer (Fig. 5A, B ).

Gemmuloscleres (Figs 6 - 8 ) slender birotules 19.8-48.6 μm (35.1 ± 5.5) in length, with narrow spiny shaft 2.7-4.4 μm (3.3 ± 0.3) in width. Shaft spines of three types (a) simple, short curved to straight, smooth spines, (b) spines with tips arranged in asterose clusters (microspines in rosettes), and (c) large, acute spines up to 3 μm long bearing secondary microspines (Fig. 7 ). Rotules flat with crenulated/notched to shallowly incised margins and both rotules inner and outer surfaces bearing numerous microspines sometimes in radial tows (Fig. 8A ) of significantly different diameters t (74) = 18.67, p <0.00005) (Fig. 6 ). Large proximal rotules 19.4-24.4 μm (21.6 ± 1.1) in diameter, small distal rotules 16.6-21.7 μm (18.9 ± 1.1) in diameter.

Habitat

(Fig. 1B ). All four specimens of Heterorotula lucasi sp. nov. were found bearing gemmules on the underside of shaded rocky substrate in shallow running water at an altitude of 325 m. Associated aquatic community was composed of diatoms, Spongillidae of three genera/species Heteromeyenia latitenta (Potts, 1881), Radiospongilla cerebellata (Bowerbank, 1863), and Trochospongilla horrida (Weltner, 1893); Mollusca of two families Pleuroceridae and Corbiculidae , Diptera larvae of the families Chironomidae and Simuliidae ; Ephemeroptera larvae of two families Baetidae and Heptageniidae ; Trichoptera larvae of family Hydropsychidae , and Odonata larvae of family Gomphidae . The climate of the study area is temperate having an average annual rainfall of 112 cm. In addition to rain events, flow rates of the Pigeon River are influenced by water releases from a hydroelectric dam in Haywood County, North Carolina. Over its 113 km course the Pigeon River drops from an elevation of 800 m at Canton, North Carolina to 310 m at its confluence with the French Broad River near Newport, Tennessee.

Geographic range.

Heterorotula lucasi sp. nov. is only known from Pigeon River (type locality, 35.9396, -83.1786) in Tennessee. The location of this single population lays far outside the previously known range of the genus.

Figures

Figure 1. Study area A 1 Tennessee in the southeastern region of the United States A 2 location of Cocke County in Tennessee A 3 type locality of Heterorotula lucasi sp. nov. is indicated by a black circle in the Pigeon River (35.9396, - 83.1786) B riparian habitat of the new sponge species at the type locality C macrophotograph in vivo of holotype (USNM 1662182) with tawny color and encrusting growth form on a rocky substrate D macrophotograph of holotype in alcohol.

Figure 2. Heterorotula lucasi sp. nov. from the Pigeon River, Tennessee (type locality). Micrographs of skeletal network with scanty spongin by SEM A multispicular fibres of entosomal area B paucispicular fibers of ectosomal area. Scale bar: 500 μm.

Figure 3. Heterorotula lucasi sp. nov. from the Pigeon River, Tennessee (type locality). Micrographs of skeletal megascleres by SEM A acanthoxeas fusiform from nearly spineless to variably spined excepts towards the tips B detail of an oxea smooth only at the tip C spiny shaft of an acanthoxea; scattered spines and microspines on shaft. Scale bars: 100 μm (A); 20 μm (B); 10 μm (C).

Figure 4. Heterorotula lucasi sp. nov. from the Pigeon River, Tennessee (type locality). Micrographs of gemmules by SEM A gemmule with multilayered Gemmular theca armed by radial gemmuloscleres around the central cavity bearing a mass of totipotent cells B outer layer at Gemmular theca surface with a few emerging rotules of gemmuloscleres, acanthoxeas of the Gemmular cage and sligtly elevated foramen closed by a membrane C Gemmular theca of an aged gemmule covered by diatoms frustules, surrounded by the spicular Gemmular cage of acanthoxeas and outer layer with open foramen after hatching D Gemmular theca with a fragment of spicular Gemmular cage and outer layer armed by dense distal rotules of gemmuloscleres E fibrous structure of outer layer with sligtly elevated foramen closed by a membrane before hatching F fibrous structure of outer layer around foramen and sparse broken shafts of gemmuloscleres. Scale bars: 500 μm (C, D); 300 μm (A, B); 100 μm (E); 20 μm (F).

Figure 5. Heterorotula lucasi sp. nov. from the Pigeon River, Tennessee (type locality). Micrographs of gemmular Gemmular theca cross sections by SEM A Gemmular theca with the radial monolayer of short and long spiny birotules bearing crenulated / notched margins of rotules. proximal, partly overlapping, rotules adherent to the multilayered inner layer (cross section, outer layer, and pneumatic layer not evident) B trilayered Gemmular theca with short and long spiny birotules embedded in the fibrous / chambered pneumatic layer in between the smooth outer layer and the multilayered inner layer, C radial birotules in the fibrous to chambered pneumatic layer D proximal rotule with crenulated / notched margins adherent to the multilayered inner layer surrounding the central gemmular cavity containing totipotent cells. Scale bars: 100 μm (A); 50 μm (B); 30 μm (C); 20 μm (D).

Figure 6. Heterorotula lucasi sp. nov. from the Pigeon River, Tennessee (type locality). Size differences in proximal and distal rotules. Scale bars: 5 μm (A); 5 μm (B); scale bars are slightly different in length.

Figure 7. Heterorotula lucasi sp. nov. from the Pigeon River, Tennessee (type locality). Spine morphology of shafts of gemmuloscleres by SEM.

Figure 8. Heterorotula lucasi sp. nov. from the Pigeon River, Tennessee (type locality) A crenulated margins and miceospines of rotules and gemmulosclers B variation in size and spines of gemmuloscleres. Scale bars: 30 μm (B); 20 μm (A).

Figure 9. Disjunct biogeographic pattern of genus Heterorotula (Porifera, Spongillida, Spongillidae) with enclaves in Nearctic and Neotropical regions. The Nearctic H. lucasi sp. nov. from Tennessee is indicated in red. Heterorotula multidentata is considered an alien species in Japan.