New Genus and Species of Lithistid Demosponges from Submarine Caves in Nuku Hiva (Marquesas Islands) and Tahiti Iti (Society Islands), French Polynesia

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New Genus and Species of Lithistid Demosponges from Submarine Caves in Nuku Hiva (Marquesas Islands) and Tahiti Iti (Society Islands), French Polynesia The European Zoological Journal, 2021, 749–770 Vol. 88, No. 1, https://doi.org/10.1080/24750263.2021.1939450 New genus and species of lithistid demosponges from submarine caves in Nuku Hiva (Marquesas Islands) and Tahiti Iti (Society Islands), French Polynesia A. SCHUSTER 1*, A. PISERA 2, M. EKINS 3,4,5, & C. DEBITUS 6,7 1Department of Biology, NordCEE, Southern University of Denmark, Odense M, Denmark, 2Institute of Paleobiology, Polish Academy of Sciences, Warszawa, Poland, 3Biodiversity and Geosciences, Queensland Museum, South Brisbane, Australia, 4Griffith Institute for Drug Discovery, Griffith University, Brisbane, Australia, 5School of Biological Sciences, University of Queensland, St Lucia, Australia, 6IRD, EIO, Université de la Polynésie française, Faaa, and 7IRD, CNRS, Ifremer, LEMAR, Université de Bretagne Occidentale, Plouzané, France (Received 23 November 2020; accepted 1 June 2021; first published 27 June 2021) Abstract Lithistid demosponges are well known from limestone caves of karstic origin in the Mediterranean Sea. However, they have never been reported from submarine caves of volcanic origin in the South Pacific. Here, we describe and provide DNA barcodes for four new lithistid demosponges including one new genus. All species grew on basaltic rocks inside lava tubes on Nuku Hiva Island (Marquesas Islands) and Tahiti Iti peninsula on Tahiti Island (Society Islands) in French Polynesia. Three of the species have rhizoclone desmas as choanosomal skeletons and belong to the family Scleritodermidae (Microscleroderma miritatarata sp. nov. and Microscleroderma lava sp. nov.) and Siphonidiidae (Gastrophanella basaltica sp. nov.). The new genus Levispongia gen. nov. belongs to the family Corallistidae. The new species Levispongia meyeri gen. nov. sp. nov. has dicranoclone desmas, complex dichotrianes with strongly spinose upper surfaces of the cladome and microstyles as the only microscleres. Phylogenetic relationships of these new species are discussed and compared with other material from the Caribbean and Central to the West Pacific Ocean. urn:lsid:zoobank.org:pub:844E385C-9A92-4F1B-B85C-9C1E319CD13F Keywords: Cave sponges, lithistid demosponges, DNA barcoding, relict fauna, French Polynesia Introduction Voultsiadou 2012). Since most of these caves are Submarine caves share several ecological features accessible by SCUBA diving, they provide a unique which often resemble that of deep-sea habitats includ- opportunity to study various aspects of deep-sea ing darkness, hydrodynamic, geochemical and faunal sponge biology and systematics (Vacelet 1996). compositions (Harmelin & Vacelet 1997). Although However, we still know little about the diversity and differences in pressure, temperature and habitat sizes connectivity of sponges from different cave systems exist (Moldovan et al. 2019), these submarine caves around the world, especially how many of these spe- are often colonized by deep-sea invertebrates like gas- cies are cryptic or relict, present as a living fossil. tropods, annelids, crustaceans and sponges (Bussotti Sponge cave biodiversity has been well studied in the et al. 2006; Gerovasileiou et al. 2015; Culver & Pipan Mediterranean Sea (e.g. Gerovasileiou et al. 2016). 2019). In particular, the abundance of demosponges The Mediterranean submarine caves are all of karstic represents an important element of submarine cave origin (limestones) and are a large biodiversity reser- communities (Bibiloni et al. 1989; Gerovasileiou & voir of sponge species that are otherwise only recorded *Correspondence: A. Schuster, Department of Biology, NordCEE, Southern University of Denmark, Campusvej 55, Odense M 5300, Denmark. Email: [email protected] © 2021 The Author(s). Published by Informa UK Limited, trading as Taylor & Francis Group. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. 750 A. Schuster et al. from the deep-sea (Gerovasileiou & Voultsiadou flows and are of volcanic origin. This is an important 2012). In particular, the occurrence of a polyphyletic finding not only because they grow on these basaltic group of demosponges historically called lithistids volcanic rocks inside lava tubes, but also due to the (Pisera & Lévi 2002a; Schuster et al. 2015) seems to fact that the new genus and species described herein be highly abundant and thrive in these cave systems represent the first records of lithistids from this (Pérez et al. 2004; Manconi et al. 2006; Manconi & extreme isolated archipelago in French Polynesia. Serusi 2008; Pisera & Vacelet 2011; Pisera & Thus, our results will be of profound interest for Gerovasileiou 2018). Lithistids are characterized by further biogeographical and systematic studies on an articulated choanosomal skeleton composed of this evolutionary important demosponge group. siliceous desmas. Molecular systematics placed the majority of these desma-bearing sponges into the order Tetractinellida Marshall 1876 (Schuster et al. Material and methods 2015). In oceans today, lithistids are normally found Specimen collection and morphological investigations in deep-waters of the tropics (Carvalho et al. 2015; Schuster et al. 2021), however, some species are also Lithistid sponges from Marquesas were collected by found in shallow waters (Pomponi et al. 2001). It is SCUBA diving in the 80 m long lava tube called postulated that the majority of these sponges were Ekamako, on Nuku Hiva southern shore originally shallow water sponges that moved into dee- (Marquesas Islands) (Figure 1(b,c)): Research per waters as silica concentrations decreased in shal- Vessel (R/V) called Alis, cruise BSMPF-1 (Debitus low water (Pisera 2004). Few records exist of lithistid 2009), site MNH03, 8°56.173’S, 140°05.593ʹW, cave fauna occurring outside the Mediterranean Sea 11 m, 29/08/2009 (Figure 1). They grew from (Gerovasileiou et al. 2016; Gómez et al. 2021). Some 10 meters (m) distance from the entrance of the lithistids were described from shallow crevices in coral cave and continued to appear deeper into the cave reefs of Madagascar (Vacelet & Vasseur 1965), from (Pérez et al. 2012). Other sponges in this cave were the central western Atlantic in Belize and Fernando de the non-lithistid demosponges Xestospongia sp. (6– Noronha (Muricy & Minervino 2000), and a few more 10 m), Dactylospongia elegans (6–10 m distance from were observed in a large submarine cave on Palawan in the entrance), Suberea sp. (6–10 m distance from the the Philippines, which represents the only known entrance), Epipolasis sp. (6–10 m distance from the record of cave lithistids so far in the Pacific Ocean entrance) and Cinachyrella sp. (8 m distance from (Pisera & Vacelet 2006). In all investigated caves, the the entrance), some of them probably represent new dominant lithistid species seem to belong to rhizomor- species too, but await formal description. ine families like Scleritodermidae Sollas, 1888, The sponges from Tahiti Iti peninsula were also Azorizidae Sollas, 1888 Siphonidiidae Von collected by SCUBA diving from a lava tube inside Lendenfeld, 1903 and dicranoclone family the Te Pari Cave (Tahiti Island, Windward Islands, Corallistidae Sollas, 1888. All of which are usually Society Islands) (Figure 1 D,E). For more details on recorded from deep-waters. The observed morpholo- the cruise see Debitus (2013). The entrance of this gical features from all these various cave lithistids show cave is about 10 m wide and its sandy bottom lies at high affinities to those of the Mesozoic of Europe 12 m depth. It forms a right angle 25 m after the (Łukowiak et al. 2014; Frisone et al. 2016; cave mouth and is another 180 m long (measured Świerczewska-Gładysz 2016), which would suggest with a hand depth sounder). It is a regular 6–8 m that most of these species represent a relict fauna wide cylinder, that narrows and rises towards the with probable Tethys origin as already predicted for end. The sides and bottom (after the turn) are other non-cave lithistids (Reid 1967; Manconi 2011) formed of irregular basaltic rocks. The cave ends in and recently tested with molecular clocks for the lithis- a narrow, rocky, chaotic pipe, inaccessible for divers. tid genus Vetulina Schmidt, 1879 (Sphaerocladina The roof at the end of the cave is characterized by an Schrammen 1924) (Schuster et al. 2018). air pocket as it is above sea level. The presence of In this integrative taxonomy study, we describe for a few dead leaves indicated freshwater inflows, prob- the first time four new lithistid demosponges and one ably during heavy rains. The top water column tem- new genus from two shallow submarine caves in perature in the cave was around 26°C, while the French Polynesia: Ekamako Cave at the southern lower bottom was warmer around 28°C, and the coast of Nuku Hiva (Marquesas Islands) and Te open sea temperature was 30°C. This cooler top Pari Cave on Tahiti Iti peninsula (Tahiti island, water temperature would confirm the inflow of Windward Islands, Society Islands) (Figure 1). In freshwater, thus keeping the upper layer of the cave contrast to the above-mentioned limestone caves, water cooler. Further indication for freshwater the Polynesian cave systems are formed by large lava inflow is given by the observation of some cave New rock sponges from caves in French Polynesia 751 Figure 1. Map of sampling sites. (a): Overview of French Polynesia in the South Pacific Ocean. (b,c): Sampling site at Nuku Hiva Island (Marquesas Islands). (d,e): Sampling site at Tahiti Iti peninsula. Red arrows indicate the position of caves where lithistids were collected. openings that are close to trails where locals sp., Haliclona spp., Halichondria sp., Chondrilla sp., observed salty water coming out during rough seas Cinachyrella sp., Luffariella sp., Rhabdastrella sp.). and killing the surrounding plants, however, no light The lithistids were found further inside the cave on could be observed inside the cave. Moreover, the the walls and roof of the cave, with Microscleroderma water at the surface in the back (end) of the cave lava sp.
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