Heterorotula kakahuensis (Traxlerı 1896)

Pronzato, Roberto & Manconi, Renata, 2019, An overview on the freshwater sponge fauna (Demospongiae: Spongillida) of New Zealand and New Caledonia with new insights into Heterorotula from deep thermal vents of the Lake Taupo, Journal of Natural History 53 (35), pp. 2207-2229 : 2207-2229

publication ID	https://doi.org/ 10.1080/00222933.2019.1694716
DOI	https://doi.org/10.5281/zenodo.3664965
persistent identifier	https://treatment.plazi.org/id/039087DA-E76D-8D08-CCB8-42042E7FF936
treatment provided by	Valdenar
scientific name	Heterorotula kakahuensis (Traxlerı 1896)
status

Treatment

( Figures 1 View Figure 1 (C)ı 5 – 11)

Ephydatia kakahuensis Traxlerı 1896 ; Geeı 1931; Schröderı 1935; Heterorotula kakahuensis Penney and Racekı 1968 ; Manconi and Pronzatoı 2002; Heterorotula sp. de Ronde et al. ı 2002; Rota and Manconiı 2004; Jones et al. ı 2007

Studied material

Two sets of historical material from Lake Taupo have been investigated by LM and SEM. The first set ( Figure 6 View Figure 6 )ı collected in 1923 and labelled BMNH 23.10.7.1 (sampleı slideı and stub FW-POR 429) was a mixed sample composed mainly of Heterorotula kakahuensis ( Figure 7 View Figure 7 ) and fragments of a problematic Spongillida ( Figure 8 View Figure 8 ). These latter fragments preliminarily studied here are characterised by an anisotropicı paucispicular skeleton; scanty spongin; smooth oxeas (195 – 321 × 9 – 14 µm; n = 25) with tapered tips as megascleresı rare stylesı rare centrotylotes and malformed spicules; shortı thinı smooth oxeas also present; sessile gemmules (750 – 950 µm in diameter) adhering to the basal spongin plate; bilayered gemmular theca; pneumatic layer absent; gemmuloscleres as spiny strongyles to oxeas (70 – 135 × 7 – 9 µm; n = 25) tangentially arranged in the theca ( Figure 8 View Figure 8 ).

The second set of sponge fragmentsı BMNH Dry Box n. 9 without label collected in 1924 (sampleı slideı stub FW-POR 428ı FW-POR 429) identified as Heterorotula kakahuensis was characterised by megascleres as oxeas spiny except at tipsı frequently centrotylote (177 – 246 × 9 – 19 µm; n = 25) ( Figure 7 View Figure 7 ).

More recent materials (1998) sampled from the Horomatangi Geothermal System (38° 49 ʹ 39.50 ” Sı 175°59 ʹ 45.88 ” E) of Lake Taupo at 125 – 180 m of depth by the submarine Jago together a video ( New Zealand – Germany Taupo ’98 dive project) were kindly supplied by Karen Hissman ( FW-POR 564ı FW-POR 565ı FW-POR 566ı FW-POR 567) ( Figures 9 – 10 View Figure 9 View Figure 10 ) and a few specimens/fragments have been frozen and registered (Belinda Alvarez de Glasbyı in litteris; see also de Ronde et al. 2002). We compared these latter specimens by LM and SEM ( Figures 9 – 10 View Figure 9 View Figure 10 ) with the previous descriptions and illustrations ( Figure 3 View Figure 3 ) and vs reanalysed BMNH materials ( Figure 7 View Figure 7 ).

Description (emended from original)

Sponges notably largeı up to 15 × 25 cm in vivo. Growth form ranging from encrusting with ripples and burls to massive with flabellate or lobate surfaceı with single lobes reaching up to 3 cm in length. Large oscula at the top of some lobes. Colour whiteı sometimes with pinkish and bluish patchesı suggesting a symbiosis with bacteria. Consistency fragile in vivo ı softı compressible. Skeletal network anisotropic with ascending primary fibres joined by irregular secondaries. Megascleres as spiny oxeas (188 – 288 × 11 – 22 µmı n = 27ı FW-POR 564; 170 – 240 × 8 – 12 µmı n = 27ı FW-POR 566); spines with rosette – like tips (verticillate). Malformed megascleres and gemmuloscleres also present. Microscleres absent. Brooded larvae in the mesohyl. Gemmules rareı subspherical (500 – 600 µm in diameter) sometimes within a cage of spiny oxeas. Foramen open (SEM)ı simple (without collar) and with a conspicuous area of gemmular surface smooth (without spicules). Gemmular theca thickı with a not well-defined structureı pneumatic layer irreguları not well developed with minute chambers only in some areas. Gemmuloscleres birotules radially embedded in the gemmular thecaı with proximal rotules closely adhering to the inner layer of compact spongin and distal rotules emerging at its surface. Inner layer sublayered. Birotules with densely spiny/tubercled/granulated rotules; shaft length variable in the same gemmule (38 – 44 × 4 – 7 µmı rotule diameter 15 – 26 µm; FW-POR 565). Rotules notably polymorphic within the same gemmuleı flat to curved with toothed marginsı with rays or hooks of variable number and morph ( Figure 9 View Figure 9 (G – I)).

Habitat

Sponges were found as flourishingı scattered assemblages at two hydrothermal vent fields with gas streaming (Te Hoata and Te Pupu)ı in Lake Taupo at a depth of 126 – 145 m ( Figure 10 View Figure 10 ). Maximum density was 25 specimens /m 2 in some areas covering 60 – 70% of the available substrata (see also de Ronde et al. 2002)ı which consisted of inactive chimneysı pinnacles and rocky crops ( Figure 10 View Figure 10 ). Elevated concentrations of silicaı salt and hydrocarbonsı together with high temperatures (44 °C) characterised the water column at a depth range of 126 – 173 m (see also de Ronde et al. 2002). In these environmental conditionsı dermal membrane notably detached from the underlying choanosome in vivo (Jago video) suggests active water pumping.

Life cycle

The presence of larvae and gemmules (cryptobiosis) indicates sexual and asexual reproduction.

Associated organisms

Protozoansı oligochaetesı nematodesı ostracodsı copepodsı amphipods and other taxa not identified at present were revealed by the dissection of spongesı together with frustules of at least six genera of diatoms densely incorporated into the mesohyl of sponges ( Figure 11 View Figure 11 ) (see also Rota and Manconi 2004; Jones et al. 2007). Epibenthic macrofauna sharing the same habitat with the sponges includes freshwater crayfish ( Paranephrops planifrons Whiteı 1842 ) and native fishesı viz. the koaro ( Galaxias brevipinnis Güntherı 1866 ) and the common bullyı or toitoi ( Gobiomorphus cotidianus McDowallı 1975 ) ( Forsyth and Howard-Williams 1983; de Ronde et al. 2002).

Geographic range

Endemic to New Zealand and recorded from Kakahu Riverı Canterburyı South Island; creek near Invercargillı South Island; Rotoiti Lakeı South Island; Lake Taupoı North Islandı coastal area and deep thermal vents; Lake Pupukeı Takapunaı Aucklandı North Island.

Historical accounts

Chilton (1883) collected the first freshwater sponge sample of the Kakahu River in New Zealandı which was green with an encrusting growth form and a smooth surfaceı adhering to submerged stones and sticks in shallow running water (six miles from Temuka; Figure 1 View Figure 1 (C)). Traxler (1896) re-examined Chilton ’ s materials andı probablyı new samples from the Kakahu River. His comparative analysis vs Ephydatia ramsayi from Australiaı described by Haswell (1882) ı and vs the European Ephydatia fluviatilis (Linnaeusı 1759) ı as described by Vejdovsky (1883) ı resulted in the description of Ephydatia kakahuensis with details of the spicular complementı gemmules and morphometries ( Figure 5 View Figure 5 (A)). The type material has apparently been lostı however a cotype (slide) is preserved in the Berlin Zoological Museum has ( Gee 1931 ı p. 49).

Kirkpatrick (1921) studied small specimens (~ 2.5 cm in diameter and height) stranded after a gale on the north shore of the Lake Taupo (356 m aslı North Islandı collected by Mr H.H. Hill of Napier; Figure 1 View Figure 1 (C)) and registered in the Natural History Museumı London (BMNH 21.11.15.1 – 2). Growth form ranged from thin flat crusts without visible oscules in some specimensı to conical with a single large osculeı and others again were irregular and meandrine. The texture was fairly firmı and the body permeated by fine sand. Gee (1931) studied the New Zealand collection registered in the Australian Museum of Sydney with two specimens labelled Spongilla and a third one Ephydatia fluviatilis . He identified all three as Ephydatia kakahuensis ı despite the total absence of gemmules in any of themı and summarised previous data in a sort of mini-review. Schröder (1935) reported on four sponges (~ 2 cm in length × 1.5 cm in thickness; Figure 5 View Figure 5 (B)) associated to the bryozoan Fredericella sultana Blumenbachı 1779 at a depth of 40 m in Lake Rotoitiı North Island. No further records had emerged for a long time (33 years) when Penney and Racek (1968 ı p. 103) considered ‘ it advisable to include it provisionally in the genus Heterorotula until evidence as to the contrary can be demonstrated ’. After 22 yearsı Crowell (1990) described the new species of water mite Unionicola (Pentatax) billieaehonore associated to Ephydatia kakahuensis in Lake Rotoiti and Lake Taupo ( Figure 1 View Figure 1 (C)).

Remarks

Erroneous identifications of H. kakahuensis have occasionally been reported ( Chilton 1883; Hutton 1904; Gee 1931; Schröder 1935) as Ephydatia fluviatilisı Spongilla lacustrisı Spongilla fluviatilis and Spongilla fragilis (see details in Historical accounts).

Moreover the BMNH 23.10.7.1 set analysed ( Figure 6 View Figure 6 ) resulted in a mix of two taxaı viz. H. kakahuensis ( Figure 7 View Figure 7 ) and a problematic species of Spongillida (see gemmules Figure 8 View Figure 8 ) sharing some traits with the genus Pottsiela described from Brazil by Volkmer- Ribeiro et al. (2010) and presently known from the Neotropicalı Nearctic and Eastern Palaearctic bioregions (Manconi and Pronzato 2016 ı 2019 a). Unfortunatelyı the poorly preserved material does not allow any unequivocal identification. Further newly sampled materials and integrative studies could help to allocate it in the appropriate taxonomic position.

According to the original description by Traxler (1896) ı H. kakahuensis is characterised by spiny oxeas as megascleres (203 – 244 × 8 – 12 µm); gemmules up to 600 µm in diameter; birotules as gemmuloscleres with spiny shafts (30 – 45 × 2 – 3 µm) with granulated rotules and indented margins (16 – 24 µm in diameter). By contrastı Schröder (1935) described megascleres as spiny oxeası except for the tips (183 – 265 × 9 – 12 µm); gemmules from 380 – 600 µm in diameter; birotules as gemmuloscleres with irregular shafts (30 – 42 × 3 – 4 µm) and rotules (17 – 22 µm in diameter) apparently smooth and with indented margins. Penney and Racek (1968) reported slenderı spinyı short oxeas as megascleres (185 – 260 × 9 – 12 µm); gemmules 380 – 540 µm in diameter; birotules as gemmuloscleres of a single dimensional class (30 – 40 × 5 µm)ı with rotules 17 – 22 µm in diameter. The New Zealand endemic H. kakahuensis was originally assigned by Traxler (1896) to the genus Ephydatia Lamourouxı 1816 on the basis of morphological and morphometric comparison with a European specimen of Ephydatia fluviatilis ( Figure 8 View Figure 8 ). All subsequent reports ( Haswell 1882; Kirkpatrick 1921; Gee 1931; Schröder 1935) indicate the species as an Ephydatia . We agree with Penney and Racek (1968 ı p. 97)ı who designated the new genusı affirming that ‘ Heterorotula is more closely related to Ephydatia than to any other genus (omissis). H. kakahuensis from New Zealand is insufficiently described (omissis). Its generic statusı thereforeı cannot as yet be reliably resolved. Until further material can be studiedı it seems advisable to leave the New Zealand species provisionally within this genus ’. The synapomorphic condition of key traits at the genus level further complicates the problem. As stated by Penney and Racek (1968) ı Ephydatia and Heterorotula are very closeı particularly with regard to the diagnostic morphology of the gemmuloscleres (birotules) and the length of the shaft: short in the former genus (12 – 65 µm) and partly overlapping with the larger length range of Heterorotula (24 – 84 µm). Moreoverı the rotules of Ephydatia are always indented and spiny ( Figure 3 View Figure 3 (A – B))ı while in Heterorotula they are prevalently irregular at the margins and tubercled ( Figure 3 View Figure 3 (C – E)). Our studies revealed a large morphological variability of the gemmuloscleres of H. kakahuensis ı confirming its inclusion in the genus Heterorotula but not excluding an affinity with the Ephydatia group lineage ( Figures 3 View Figure 3 (A – B)ı 5(B)).