Lissodendoryx (Waldoschmittia) hawaiiana ( de Laubenfels, 1950 )

Cruz-Barraza, José Antonio, Carballo, José Luis & Aguilar-Camacho, José María, 2023, Taxonomy and molecular phylogenetic position of new species and new records of Coelosphaeridae (Demospongiae: Poecilosclerida) from the Mexican Pacific, Zoological Journal of the Linnean Society 199 (2), pp. 511-532 : 522-528

Lissodendoryx (Waldoschmittia) hawaiiana ( de Laubenfels, 1950)

( Figs 8 , 9 )

Synonymy

Damiriana hawaiiana de Laubenfels, 1950: 50 .

Damiriana hawaiiana Green & Gómez, 1986: 292 , figs 54–56.

Lissodendoryx (Waldoschmittia) hawaiiana Núñez, Calcinai & Gates 2017: 21 .

Material examined

MBC #11506, West Coast of the Coconut Island, Oahu (Hawaii, USA) 15/X/1958, 3 m depth . LACM #1954- 9, Bahia Santa Lucia (Acapulco, Guerrero), 16°50.59”N, 99°55.46”W, 01/I/1954, 2–7 m depth, R/V VELERO IV. AHF 1596-54. LEB-ICML-UNAM-147, Bahia Chacala (Chacala, Nayarit), 21°9’57’’N, 105°13’38’’W, 20/II/2000, 2 m depth . LEB-ICML-UNAM-396, Punta Santiago (Manzanillo, Colima), 19°5’41’’N 104°25’22’’W, 16/XI/2001, 2 m depth . LEB-ICML-UNAM-1618, Parque de la Reina (Acapulco, Guerrero), 16°50’55.56’’N, 99°54’2.6’’W, 04/V/2008, 5 m depth . LEB-ICML-UNAM-1631, Isla Papagayo (Acapulco, Guerrero), 16°51’16’’N, 99°53’05’’W, 06/IV/2008, 6 m depth . LEB-ICML-UNAM-1784, Farallón del Obispo (Acapulco, Guerrero), 16°51’20.21’’N, 99°52’25.92’’W, 16/III/2007, 5 m depth . LEB-ICML-UNAM-1793, Isla Papagayo (Acapulco, Guerrero), 16°51’18.10’’N, 99°55’04.75’’W, 23/III/2007, 6 m depth . LEB-ICML-UNAM-1806, Playa Tlacopanocha (Acapulco, Guerrero), 16°50’49.71’’N, 99°54’28.11’’W, 22/IX/2007, 7 m depth . LEB-ICML-UNAM-1809, Playa Tlacopanocha (Acapulco, Guerrero), 16°50’49.71’’N, 99°54’28.11’’W, 22/IX/2007, 7 m depth . LEB-ICMLUNAM-1810, Playa Tlacopanocha (Acapulco, Guerrero), 16°50’40.72’’N, 99°54’29.28’’W, 22/IX/2007, 2 m depth . LEB-ICML-UNAM-1845, Playa Tlacopanocha (Acapulco, Guerrero), 16°50’39. 41’’N, 99°54’25.00’’W, 14/IX/2008, 2.5 m depth . LEB-ICML-UNAM-1884, Playa La Bruja (La Paz, Baja California Sur), 24°13’23’’N, 110°18’44’’W, 25/I/2010, 3 m depth . LEB-ICML-UNAM-1938, Playa la Concha (La Paz, Baja California Sur), 24°12’9.91’’N, 110°18’2.41’’W, 07/VI/2010, 8 m depth . LEB-ICML-UNAM-2441, Playa la Concha (La Paz, Baja California Sur), 24°12’9.91’’N, 110°18’2.41’’W, 17/ IX/2012, 4 m depth . LEB-ICML-UNAM-2447 Playa la Concha (La Paz, Baja California Sur), 24°12’9.91’’N, 110°18’2.41’’W, 17/IX/2012, 2 m depth . LEB-ICML-UNAM-3055, La Entrega (Oaxaca), 15°42’50’’N, 96°05’20’’W, 22/X/2014, 4 m depth .

Description: Encrusting, cushion-shaped, or massive sponge (from 1 to 4 cm thick), covering areas from 2 to 17 cm in maximum diameter ( Fig. 8A, B ). The surface is uneven, with small raised ridges (1 to 1.5 mm) running homogeneously over the body. Small ostial-pores (from 1–2 mm in diameter) are regularly distributed on the surface. Oscules are circular to oval in shape from 2 to 7 mm in diameter and slightly elevated from the surface (from 1.5 to 2.1 cm high). Ectosomal membrane is flexible and resistant in live specimens. Consistency is briưle. Mucous in live specimens. It is compressible and elastic asser fixation. Colour in life orange and pale in preserved specimens.

Skeletal characteristics

Skeleton: Ectosomal skeleton is a layer (20 µm thick) of tylotes arranged tangentially including dispersed microscleres ( Fig. 8C ). Choanosomal skeleton is an isotropic reticulation formed by oxeas in multispicular primary tracts (40–90 µm thick) interconnected by secondary pauci-multispicular tracts (20–60 µm thick). ºuadrangular meshes are from 80 to 250 µm wide ( Fig. 8D ). Microscleres are sigmas and isochelae, dispersed in the body without any special organization.

Spicules: Ectosomal tylotes are straight or slightly curved, with smooth heads ( Fig. 9A ), sometimes with an incipient head (anisotylote). Tylotes length: 165–(190.2)–235 µm; shass diameter: 1.3–7.5 µm; head diameter: 3.8–8 µm. Choanosomal oxeas are fusiform with hastate tips or slightly curved with acerate tips, both with tapered ends ( Fig. 9B ). Oxeas with blunt tips and style forms are also present. In addition, slender and slightly smaller oxeas also appear; probably immature spicules. General oxeas length: 128–250 µm; shass diameter: 1.3–10 µm. Microscleres are sigmas and isochelae. Sigmas are in two categories: Sigmas I; small ‘C-S’-shaped with small denticle at the ends, from 10 to 25 µm ( Fig. 9C ). Sigmas II; very scarce and only were found in a few specimens, they are larger than Sigma I, with regular C-shaped and robust chord, from 35–40 µm. Arcuate tridentate isochelae from 10–37 µm ( Fig. 9D ; Table 5 ).

Distribution and habitat

Lissodendoryx (Waldoschmittia) hawaiiana is distributed in the Pacific Region, from Hawaii to Mazatlán Bay ( Mexico) ( Laubenfels 1950, Green and Gomez 1986, Núñez et al. 2017). In Mexico, this species is growing over rocky substrates, mainly on coral reef areas, from La Paz (BCS) to La Entrega (Oaxaca), and from 2 to 8 m in depth ( Fig. 1 ). Except for the sample collected in Bahia Chacala (Nayarit), which was found on a small harbour.

Remarks: Lissodendoryx (Waldoschmittia) hawaiiana was initially described from Hawaii (as Damiriana hawaiiana ) by de Laubenfels, 1950. Later, it was recorded in Mexican Pacific waters by Green and Gomez (1986). Asserwards, Van Soest (2002) re-examined the holotype of D. hawaiiana and proposed its synonymy with Lissodendoryx schmidti (Ridley, 1884) , which was described in Australia and later considered of wide distribution. Recently, Núñez et al. (2017) reviewed new Hawaiian specimens of this species and resurrected L. (W.) hawaiiana based on two differences in the spicule morphologies compared to L. schmidti : (1) the presence of small sigmas characterized by small denticles at the extremities, which were also detected by de Laubenfels (1950) and Van Soest (2002); (2) the shape of the isochelae, which is slightly straighter in L. (W.) hawaiiana . The Mexican specimens matched the original and recent description of L. (W.) hawaiiana , in addition to the high similarity of the 28S sequences.

Molecular phylogenetic relationships

Here, we provide DNA sequences of 28S rDNA for Celtodoryx chichiltik sp. nov. domains C1–C2 (paratype LEB-ICML-UNAM-850; GenBank accession: OP715763) and for two Lissodendoryx species domains, C1–D2: two specimens of L. (L.) albemarlensis (LEB-ICML-UNAM-2374, 2379; GenBank accessions: OP740709, OP740710, respectively), and three specimens of L. (W.) hawaiiana (LEB-ICMLUNAM-2441, 2447, and 3055; GenBank accessions:OP704020, OP704019, OP704021, respectively). A COI sequence of L. (L.) albemarlensis (specimen LEB-ICML-UNAM-2374; GenBank accession: OP715763) is also included (see Table 1 ). We aimed to establish their molecular taxonomy and their phylogenetic relationships within the order Poecilosclerida . The multiple 28S sequence alignments resulted in 848 bp in length, 449 were variable sites, with 353 parsimony-informative. Meanwhile, COI alignments consisted of 559 bp, with 272 variable sites 202 were parsimony-informative. The phylogenetic trees for each locus were mainly congruent between BI and ML, respectively, although there were some low-supported branches retrieved in the ML trees. The Posterior Probability (PP) obtained from BI, followed by the Bootstrap Proportion (BP) from the ML analysis, are shown at each node of the phylogenetic trees presented (BP/PP; Figs 10 , 11 ).

Our molecular results for both loci were according to previous molecular studies, which showed that most of the families of the order Poecilosclerida were not retrieved as monophyletic ( Morrow et al. 2012, Redmond et al. 2013, Taker et al. 2013). Similarly, members of the family Coelosphaeridae were clustered separately or in small groups throughout the topologies. In the 28S tree ( Fig. 10 ), neither Lissodendoryx nor Celtodoryx were retrieved as monophyletic, and the species of both genera were clustered together with other Poecilosclerida species, forming at least two well-supported Coelosphaeridae main clades. One of these main clades (98% PP/74% BP) is subdivided in one subclade (94% PP/69% BP) that contains Hymedesmia pansa Bowerbank, 1882 (Hymedesmiidae) and an unresolved polytomy containing sequences of Celtodoryx chichiltik sp. nov., Acanthancora sp. (Hymedesmiidae) , and a small group formed by Lissodendoryx (Acanthodoryx) fibrosa (Lévi, 1961) and an unidentified specimen belonging to the genus Lissodendoryx . The other subclade (98% PP/89% BP) contains sequences of Lissodendoryx (Ectyodoryx) arenaria Burton, 1936 , Crella incrustans (Carter, 1885) (Crellidae) and Plocamiancora arndti Alander, 1942 (Myxillidae) . The second main clade (100% PP/89% BP) contains sequences of Celtodoryx ciocalyptoides , Tedania sp. , two species of the genus Myxilla Schmidt, 1862 , and a subclade (robust in PP 91%, but low-supported in BP 52%) mainly containing Coelosphaeridae sequences, where Forcepia sp. was grouped as a sister clade of a well-supported group (100% PP/99% BP) formed by Lissodendoryx spp. (including our sequences), and a sequence of Mycale fibrexilis Wilson, 1894 (Mycalidae) that perhaps could be a misidentified specimen (see Discussion). Specifically, our L. (L.) albemarlensis sequence was clustered with M. fibrexilis and L. (A.) sigmata , while our sequences of L. (W.) hawaiiana were grouped with its Hawaiian conspecific sequence ( Fig. 10 ). The nucleotide variation between Mexican and Hawaiian specimens is in three polymorphic sites of the D2 domain ( Table 6 ). Other Coelosphaeridae sequences such as Lissodendoryx (Lissodendoryx) complicata (Hansen, 1885) and Inflatella sp. were clustered in different molecular clades.

For the COI topology, the genus Lissodendoryx was also shown as non-monophyletic. Albeit most species of this genus were grouped in a well-supported (100% PP/100% BP) clade, at least one sequence of Lissodendoryx flabellata Burton, 1929 was clustered separately in a different molecular clade ( Fig. 11 ). In this molecular tree, a sequence of M. fibrexilis (from the same specimen as the 28S sequence) was clustered with L. (L.) isodictyalis . They formed a sister group of a large and low-supported clade (53% PP/<50% BP) that included several Lissodendoryx sequences: L. (A.) sigmata , Lissodendoryx (Lissodendoryx) colombiensis Zea & van Soest, 1986 , L. (W.) hawaiiana , our L. (L.) albemarlensis , and four unidentified Lissodendoryx spp. In addition, some unidentified sequences (named Demospongiae species) showed high nucleotide similarities with our sequences. So, we include them in the molecular analysis, suggesting that these unidentified sequences could be species belonging to the genus Lissodendoryx .

Figures

Figure 1. Location of the sampling stations along the coast of Mexico.The numbers show the distribution of the species:(1) Celtodoryx chichiltik sp. nov.; (2) Lissodendoryx (Anomodoryx) incrustans sp. nov.; (3) Lissodendoryx (Lissodendoryx) albemarlensis; (4) L. (W.) hawaiiana.

Figure 8. Lissodendoryx (Waldoschmittia) hawaiiana. A, B, External morphology of alive and preserved specimens, respectively; C, tangential view of ectosomal skeletal structure; D, cross-section view of choanosomal skeletal structure.

Figure 9. SEM images of spicules of Lissodendoryx (Waldoschmittia) hawaiiana. A, Tylote and detail of its head; B, variety of oxeas morphology and detail of its ends: C, sigmas I; D, arcuate isochelae.

Figure 10. Phylogenetic reconstruction of 28S rRNA nuclear-ribosomal region (C1, C2–D2). The tree presented was obtained by BI and includes ML values. The number at each node represents the PP in % from BI, followed by the BP from ML; a (–) indicates that a particular analysis supported the node at less than 50%.The GenBank accession numbers are given asser each taxon name.

Figure 11. Phylogenetic reconstruction of the COI mtDNA fragment. The tree presented was obtained by BI and includes ML values. The number at each node represents the PP in % from BI, followed by the BP from ML; a (–) indicates that a particular analysis supported the node at less than 50%.The GenBank accession numbers are given asser each taxon name.