Leucandra cavernicola, Lopes & Pérez & Klautau, 2024

Lopes, Matheus Vieira, Pérez, Thierry & Klautau, Michelle, 2024, Cave-dwelling calcareous sponges (Porifera: Calcarea) from the Marquesas Islands, French Polynesia, Zoological Journal of the Linnean Society 202 (3) : -

Leucandra cavernicola sp. nov.

( Figs 13–15; Table 6)

Zoobank registration: urn:lsid:zoobank.org:act:B17430CD-B013-469E-93F6-0B8377DB2331 .

Type species: Sycinula egedii Schmidt, 1870 .

Diagnosis: White Leucandra with tubular body. Cortical skeleton composed of diactines, microdiactines, triactines, and trichoxeas. Choanosomal skeleton disorganized, with triactines and tetractines. Exhalant openings surrounded with aliactinal triactines and tetractines. Atrial skeleton composed of tetractines.

Etymology: For the cavernous habitat where the species was found.

Type locality: The Four Caves , Nuku Hiva, Marquises Islands, French Polynesia .

Type material: Holotype: French Polynesia: Marquesas Islands: Nuku Hiva Island: UFRJPOR 7517, The Four Caves (8°56.2 ʹ S, 140°07.2 ʹ W), 20 m depth, 11.i.2012, coll. T. Pérez, field number MQ2-GR3-TP07 . Paratypes: UFRJPOR 7521, field number MQ2-GR3-TP02. UFRJPOR 7522, field number MQ2- GR3-TP03. Other data the same as the holotype.

Colour: White to light yellow alive and white in ethanol ( Fig. 13).

Description: Sponge tubular, cylindrical, sometimes wider at the top ( Fig. 13A–C). One single apical osculum with a well-developed neck with a crown of trichoxeas ( Fig. 13D). Consistency firm to the touch. Holotype with an appendix-like structure at the side of the body ( Fig. 13D). In vivo, the external surface shows filaments that disappear after fixation ( Fig. 13). Atrium central and wide. Aquiferous system leuconoid. Skeleton disorganized but with distinct cortical, choanosomal, and atrial regions ( Fig. 14A). Oscular membrane supported by T-shaped triactines and tetractines. Diactines longitudinally disposed near the osculum and at the base of the sponge. Cortical skeleton composed of longitudinal microdiactines, tangential triactines and trichoxeas ( Fig. 14B). Large triactines in the choanosome, and tetractines surrounding the canals ( Fig. 14A). Exhalant openings with aliactines of two types, triactines and tetractines ( Fig. 14C). Atrial skeleton with tangential tetractines that point their apical actine into the atrial cavity ( Fig. 14D). One single triactine with the same shape of the atrial tetractine was seen on the atrial surface of UFRJPOR 7517.

Spicules ( Fig.15; Table 6)

Diactines: Large and fusiform, with both tips sharp, one thicker than the other ( Fig. 15A). Size (UFRJPOR 7517): 670.6 (±123.9)/20.3 (±6.7) µm.

Microdiactines: Lanceolated, undulated, with sharp tips ( Fig. 15B). Size (UFRJPOR 7517): 88.2 (±11.2)/4.5 (±1.2) µm.

Cortical triactines: Sagittal. Actines slightly conical and straight, with sharp tips. Paired actines shorter than the unpaired one, always straight ( Fig. 15C). Size (UFRJPOR 7517): 154.9 (±41.4)/15.4 (±4.2) µm (paired); 183.0 (±56.5)/16.8 (±4.4) µm (unpaired).

Choanosomal triactines: Sagittal to subregular. Actines conical, undulated, with sharp tips. Paired actines usually curved ( Fig. 15D). Size (UFRJPOR 7517): 142.5 (±27.6)/12.8 (±2.5) µm (paired); 176.8 (±25.2)/14.2 (±2.5) µm (unpaired).

Tetractines of the canals: Sagittal. Actines slightly conical to conical and straight, with sharp tips. Paired actines usually curved, due to the position around the canals ( Fig. 15E). Apical actine very short, conical, straight and smooth, with sharp tips. Size (UFRJPOR 7517): 97.2 (±18.8)/8.4 (±1.3) µm (paired); 104.2 (±24.4)/9.8 (±0.5) µm (unpaired); 55.0 (±15.2)/9.2 (±2.6) µm (apical).

Triactines aliactines: Paired actines v-shaped. Actines cylindrical, slender and slightly undulated, with blunt to sharp tips. Paired actines longer than the unpaired one, slightly curved near the tip ( Fig. 15F). Size (UFRJPOR 7517): 53.2 (±5.7)/2.7 µm (paired); 6.8 (±1.4)/2.7 µm (±0.5) (unpaired).

Tetractines aliactines: Paired actines v-shaped. Actines cylindrical, slender, and slightly undulated, with sharp tips. Paired actines longer than the unpaired one and slightly curved near the tip ( Fig. 15G). Apical actine conical, straight, and smooth, with sharp tips. Size (UFRJPOR 7517): 52.0 (±2.9)/2.5 µm (paired); 6.5 (±1.3)/2.7 µm (±0.5) (unpaired); 24.4 (±2.5)/2.6 (±0.4) µm (apical).

Atrial tetractines: Sagittal. Actines slightly conical to conical and slightly undulated, with sharp tips. Usually, one paired actine is shorter than the other. The unpaired actine is shorter than the paired ones ( Fig. 15H, I). Apical actine long, slightly conical to conical, undulated and smooth, with sharp tips ( Fig. 15I). Size (UFRJPOR 7517): 140.1 (±29.6)/11.1 (±2.5) µm (paired); 107.1 (±25.6)/12.3 (±1.6) µm (unpaired); 130.4 (±45.2)/10.6 (±2.5) µm (apical).

Ecology: The specimens were hanging on the ceiling of the cave. Although they looked like a hispid sponge in vivo, they became completely smooth after preservation. Therefore, we suspect that the ‘hispidation’ could be associated filamentous cyanobacteria or sponge mucus.

Geographical distribution: Currently endemic to the type locality. Ecoregion : Marquesas .

Remarks: Considering that the genus Leucandra lacks strong diagnosable characters (Borojević et al. 2002), our new species fits it due to the presence of a leuconoid aquiferous system and disorganized choanosomal skeleton. Moreover, it is important to note that Leucandra is a non-monophyletic genus in molecular phylogenies (e.g. Alvizu et al. 2018). It is even possible that Leucandra cavernicola sp. nov. belongs to a new genus. Nevertheless, the only morphological character that we recognize at the moment to support this potential new genus is the presence of aliactines and, although aliactines have not been described for other leuconoid genera and species before, we do not know if they were just overlooked. For that reason, we decided to currently allocate the new species in Leucandra and not to propose a new genus.

The term aliactine was first given by Van Soest et al. (2015) as ‘butterfly-shaped apopylar tetractines’, due to the shape of the alate paired actines. Later, it was defined as ‘ a specialized butterfly‐shaped tetractine lining apopylar chambers’ ( Łukowiak et al. 2022). In both definitions, the aliactines were wrongly referred to as lining apopyles. In fact, apopylae are the exit openings of choanocyte chambers and aliactines are present in the exit openings of exhalant canals, as also observed for Leucandra cavernicola sp. nov.. On the other hand, for the new species we also found aliactines that are triactines besides tetractines and the apical actines of the tetractines of Leucandra cavernicola sp. nov. were smooth, not ‘swollen and ornamented with irregular spines, curved slightly inwards, likened to “torches” by Hôzawa (1940: 42) ’ as in Paragrantia waguensis (Van Soest et al. 2015) . Nonetheless, triactines and tetractines had the paired actines following the same alate (butterfly-shaped) pattern observed in P. waguensis . For that, we propose an emendation to the definition of aliactines to: A specialized triactine and/or tetractine lining exhalant openings, in which the paired actines have an alate shape, the unpaired actine is reduced and the apical actine of tetractines is either smooth or ornamented with lateral projections. The apical actine of tetractines aliactines does not grow from the centre of the spicule, but from between the paired actines, becoming almost opposite to the unpaired actine.

Interestingly, our molecular reconstruction indicated a clade composed of Leucandra cavernicola sp. nov., Leucandra sp. from Voigt et al. (2012), P. waguensis , and Teichonopsis labyrinthica ( Fig. 4). Because Leucandra sp. does not have a formal description available, we can only make morphological comparisons among the other three species and all of them have aliactines.

The apical actine of the aliactines in P. waguensis is flat at the base and ornamented with irregular projections (‘torchlike’; Hôzawa 1940, Van Soest et al. 2015). The apical actine of T. labyrinthica can be both flat with projections or conical and sharp ( Carter 1878, Dendy 1891). Finally, Leucandra cavernicola sp. nov. has conical and sharp apical actines. It is also interesting to mention that this is the first time that triactines aliactines were observed. Paragrantia waguensis and T. labyrinthica share some features such as a foliose growth form, syconoid aquiferous system, and articulated choanosomal skeleton, while Leucandra cavernicola sp. nov. is tubular, leuconoid, with disorganized choanosomal skeleton and traces of radial orientation. Moreover, T. labyrinthica has microdiactines on the cortical and atrial surfaces, which are present only in the cortex of Leucandra cavernicola sp. nov. and are absent in P. waguensis . Therefore, the aliactines could represent the only synapomorphy of this clade, which must be confirmed with proper reanalyses of the holotype of T. labyrinthica and additional specimens with this type of spicule in Calcaronea.

The two sequences of Leucandra cavernicola sp. nov. were recovered in a polytomic branch at the base of the aliactine-bearing sponge clade ( Fig. 4), despite sharing a single nucleotide of difference over the alignment. Because of the conserved nature of the C-LSU marker in species’ delimitation in both Calcinea and Calcaronea (e.g. Alvizu et al. 2018, Lopes and Klautau 2023), and the matching of morphological diagnostic characters, we consider them as belonging to the same species.

The only species of Leucandra known so far for the French Polynesia is Leucandra tahuatae Klautau et al., 2020 , a species also from Marquesas Island. Nonetheless, it is very different from Leucandra cavernicola sp. nov.. For example, Leucandra tahuatae does not have diactines and has a subatrial skeleton, among other morphological differences. They are also molecularly very different, being present in two distant clades in our tree ( Fig. 4).

Considering other Leucandra species with cortical triactines, diactines, and microdiactines, and with only tetractines in the atrial skeleton, we have eight species: Leucandra conica Lendenfeld, 1885 from Australia (Port Jackson), Leucandra crosslandi (Thacker, 1908) from Cape Verde, Leucandra globosa Tanita, 1943 from Japan, Leucandra riojai Ferrer-Hernández, 1918 from Spain (Mediterranean Sea), Leucandra rudifera (Poléjaeff, 1883) from Bermuda, Leucandra serrata Azevedo and Klautau, 2007 from Brazil, Leucandra spissa (Urban, 1909) from South Africa, and Leucandra sphaeracella Wörheide and Hooper, 2003 from Australia. All of them, however, differ from the new species. Among several features, we can distinguish them by the body shape: Leucandra crosslandi is pear-shaped; Leucandra globosa , Leucandra riojai , and Leucandra serrata are globular; Leucandra spissa is subspherical; and Leucandra sphaeracella is massive bulbous. For Leucandra conica and Leucandra rudifera we cannot consider the body shape to distinguish them from our new species, as the former was described as ‘more or less cylindrical’ and the latter was fragmented. However, we can highlight the shape of the microdiactines, which are rounded at the proximal tip and sharp at the distal one in Leucandra conica , while in the new species it is lanceolated. As for Leucandra rudifera , it has, for example, grapnel spicules in the atrial wall, a characteristic not present in Leucandra cavernicola sp. nov..