P u b l i s h i n g
Invertebrate Systematics C o n t i n u i n g I n v e r t e b r a t e Ta x o n o m y
Volume 16, 2002 © CSIRO 2002
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Invertebrate Systematics, 2002, 16, 813–835
IT0 36 SR.uEn.iLngsth-Aeardmsi:tPaegtroanmdicJa. Nin. tAh.eHPoacpiefrc
Discovery of Petromica Topsent in the Pacific Ocean: a revision of the genus with a new subgenus (Chaladesma, subgen. nov.) and a new species (P.(C.) pacifica, sp. nov.) (Porifera:Demospongiae:Halichondrida:Halichondriidae) S. E. List-Armitage and J. N. A. HooperA Queensland Museum, PO Box 3300, South Brisbane, Qld 4101, Australia. To whom correspondence should be addressed. Email:
[email protected]
A
Abstract. Petromica Topsent, a sublithistid demosponge with affinities to Halichondriidae (Demospongiae: Halichondrida), is revised from type material to explore the phylogenetic and biogeographic relationships of a new species, P. pacifica, sp. nov., from the southern Great Barrier Reef and south-eastern Queensland, being the first record of the genus for Australian waters and for the Pacific Ocean. The present work brings the total number of species known worldwide to eight. Phylogenetic analysis confirms the monophyly of the genus and its synonymy with the nominal genus Monanthus. These analyses indicate that the new species is most closely related to two western Atlantic species (southern Brazilian to the central Caribbean), for which a new subgenus Chaladesma, subgen. nov. is proposed. Chaladesma differs from the nominotypical subgenus in its soft consistency confined to the basal portion of the choanosome (v. firm to rigid), reflecting the poorly developed desma skeleton, and lack of desma zygoses; possession of multiple papillae supported internally by sinuous tracts of oxeas (v. either no papillae or papillae supported by spiral plumose tracts); a single size class of oxeas (v. two size classes); and a moderately high proportion of monocrepidial desmas (with visible axial canal) (40–45%) (v. 0–5%, except in P. plumosa, which has 90% monocrepidial desmas).
Introduction Petromica Topsent, 1898 is a sublithistid demosponge (a ‘soft’ sponge with desmata megascleres included in its spicule complement). A comprehensive revision of the genus was published recently by Muricy et al. (2001), based on re-examination of all type material and new collections from Brazil. This revision brought the number of known species worldwide to seven (including elevation of several subspecies to full species rank). Species are known from the north-eastern Atlantic (Azores and Mediterranean), the Caribbean–south-east Atlantic (central Caribbean to southern Brazil), south-eastern Africa (Natal and East London coasts), and western (Amirante), central (Sri Lanka) and eastern (Andaman Islands) Indian Ocean. Prior to the present study, however, the genus was unknown in the Pacific Ocean. Muricy et al. (2001) proposed that Petromica was both monophyletic and had affinities with the order Halichondrida, family Halichondriidae (following the earlier proposal of Van Soest and Zea (1986), with apparent close © CSIRO 2002
relationships to the genera Topsentia and Ciocalypta in particular) – as opposed to an alternate scheme in which ‘lithistids’, or desma-bearing sponges, are assigned to an order Lithistida (e.g. Topsent 1890). Although there are no plausible arguments to dispute the allocation of this genus to Halichondriidae (with affinities based on the morphometric data concerning the free (non-lithistid) skeleton), or alternatively, to provide a more plausible allocation of the genus to another established higher taxon – especially now that the order Lithistida is formally abandoned (Pisera and Lévi 2002a) – there remain several unresolved questions concerning the phylogenetic and biogeographic relationships among species of Petromica and the importance of various characters used to determine their relationships. Opinion that Petromica belongs to the Halichondriidae is now substantial based on morphological data (Van Soest and Zea 1986; Van Soest et al. 1990; Diaz et al. 1993) and there is some molecular support for this hypothesis (Kelly-Borges and Pomponi 1994), but like many other sublithistid demosponges there is still some dispute about its higher 10.1071/IT00036
1445-5226/02/050813
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systematic relationships that cannot be fully resolved using morphometric datasets alone. At the time of the Muricy et al. (2001) revision, we had also independently completed a detailed review of all nominal Petromica species based on all nominal type material in an attempt to place a new species discovered from the southern Great Barrier Reef and south-eastern Queensland. We arrived at a similar conclusion to Muricy et al. (2001), supporting the monophyly of the genus, the synonymy of Monanthus and the elevation of several subspecific taxa to full species rank. We differed, however, in our conclusions regarding phylogenetic and biogeographic affinities among species. Muricy et al. (2001) provided a comprehensive discussion of the history of the genus, including its various taxonomic assignments (at family and ordinal levels), which do not need to be repeated here. Similarly, these authors provide detailed redescriptions of all nominal species that also do not require repetition here (although some of our observations differ from those of Muricy et al. (2001), which we summarise here in species’ diagnoses). In contrast, the present work focuses on re-evaluating all morphometric characters previously used to assess taxonomic affinities between species (based on re-assessment of these characters from the relevant type material) and proposes several new characters to evaluate species-level relationships. We describe a new species from north-eastern Australia, being the first record of the genus for the Pacific. We also propose a new subgenus classification for Petromica based on the close affinities between the new Pacific species and two other species from South America (extending into the Caribbean). This subgeneric classification contrasts markedly from classical biogeographic models based on Tethyan and Gondwanan affinities.
Materials and methods Specimens of P. pacifica were collected using SCUBA and photographed in situ using Nikonos V camera systems. Specimens were deposited in the Queensland Museum, Brisbane, Australia (QM). Methods of sponge tissue preparation and identification follow Hooper (1996). Spicule sizes were measured using light microscopy and camera lucida using a calibrated stage micrometer. Measurements of 30 random samples of all spicules are indicated as minimum– (mean)–maximum dimensions. A taxon × character matrix was constructed (Table 1) based on data from Muricy et al. (2001: characters 1–29, fig. 16, appendices 1–2), including two outgroup taxa (Desmanthus and Gastrophanella) and new characters discovered in the present analysis (characters 30–37). Additional data used to construct Table 1 were also taken from Muricy and Minervino (2000), Van Soest and Hajdu (2000) and Pisera and Lévi (2002b). Parsimony analysis and tree building was conducted using PAUP* 4.0b8 (Swofford 2001) and MacClade 4.0 (Maddison and Maddison 2000) respectively. Searches were performed with the following options set: algorithm = branch and bound; addition sequence = furthest; collapse zero length branches; multistate taxa = polymorphisms; optimisations = ACCTRAN; rooting by outgroup; all
S. E. List-Armitage and J. N. A. Hooper
characters unordered and with equal weight; consensus trees calculated using strict consensus and 50% majority rule; and bootstrapping with 1000 replicates.
Definitions The following definitions refer to desma morphology as it applies to Petromica (following Kelly-Borges and Pomponi (1994), Kelly (2000) and Pisera and Lévi (2002b); and at the advice of these authors, personal communication). These terms are defined here to clarify some of the confusion among sponge taxonomists regarding desma morphology, differing in part from those used by contemporary workers (e.g. Van Soest and Hajdu 2000; Muricy et al. 2001), and including some erroneous definitions in the ‘Thesaurus of Sponge Morphology’ (Boury-Esnault and Rützler 1997). Desma. Megasclere spicule that defines the polyphyletic group ‘Lithistida’; of various geometry and usually complex morphology, often secondarily modified and very irregular; may be articulated with adjacent desmas to form an interlocking ‘lithistid’ choanosomal skeleton, or only partially or incompletely articulated, or non-articulated, to form a ‘sublithistid skeleton’ (as in the case of Petromica). Epirhabd. Part of the desma formed by the deposition of concentric layers of silica around the crepis. (We have also used the term epirhabd to refer to the central body of the desma from which the rays (or clones) arise; the term rhabdome has sometimes been used for this structure) (see Fig. 1). Clone. Ray or arm of the desma that branches from the central epirhabd; the number of clones is dependent on the crepis geometry. In Petromica, clones are partly or entirely anaxial given that the crepis is absent (acrepidial desmas) or only very short and confined entirely to the small epirhabd (monocrepidial desmas). The term cladome (or cladii) has been used in this context by authors (e.g. Muricy et al. 2001), but this is improper usage because it refers to the tangential rays found in tetracrepidial ectosomal desmas (phyllotriaenes) and is not homologous to the rays on monocrepidial desmas (see Fig. 1). Crepis. Inceptional body of a desma (the axial filament) that is visible as central canal (monocrepid desma) or canals (tetracrepid desma), or absent entirely (acrepid desma) (see Fig. 7). Recently, Kelly (2003) found that putative acrepidial megaclone desmas of Pleroma (a lithistid sponge in the family Pleromidae), actually contained thin short crepi, and suggests (M. Kelly, personal communication) that acrepidial desmas are all monocrepidial with the crepis obscured by the granular nature of the silica deposition. If this is true, then the use of the terms acrepidial and monocrepidial here refers to the absence or presence of a visible axial filament and not necessarily an inference on the potential differences in derivation of these two desma spicules. Zygome. The terminal ray of a desma; may be articulated with that of an adjacent desma to form an interlocking (‘lithistid’) or partially articulated (‘sublithistid’) skeleton, or not articulated at all (in which case bearing small tubercles or digits). Zygoses. Junctions between zygomes of adjacent interlocking desmas; may be entirely or loosely fused.
Abbreviations BMNH IM MNHN MNRJ MOM QM ZMA
The Natural History Museum, London. Zoological Survey of India, Calcutta. Muséum National d’Histoire Naturelle, Paris. Museu Nacional, Rio de Janeiro, Brazil. Musée Océanographique de Monaco, Monaco. Queensland Museum, Brisbane, Australia. Zoölogisch Museum, Universiteit van Amsterdam, The Netherlands.
Desma ramification (0, low–moderate no. clones; 1, large number of clones)
Desma zygomes (branch tips) (0, smooth; 1, microspined) Desma articulation (0, no zygoses; 1, poorly or moderately formed zygoses; 2, well formed zygoses) Desma distribution (0, throughout choanosome and ectosome; 1, basal skeleton only) Raphide microscleres (0, absent; 1, present) Desma crepis (1, only acrepid; 2, mostly acrepid but also some monocrepid, 80%) Subectosomal spaces (1, absent; 2, present) Oxea size classes (1, single; 2, two) Average no. of desma zygomes (0, 0–3; 1, 4–6) Max. no. of desma zygomes (0, 0–3; 1, 4–6) Mean epirhabd length (1, 1–400 µm; 2, 400–500 µm; 3, >500 µm ) Mean epirhabd width (1, 1–35 µm; 2, 35–50 µm; 3, >50 µm) Mean clone length (1, 1–170 µm; 2, >170 µm)
25
26 27
31 32 33 34 35 36 37
29 30
28
21 22 23 24
19 20
18
17
11 12 13 14 15 16
10
09
Shape (0, massive-burrowing; 1, encrusting; 2, cup-shaped) Body margins (0, unspecialised; 1, rounded) Maximum size (0, >10 cm; 2, 5–10 cm; 3, 5) Papillae shape (0, cylindrical digitate; 1, conical–truncate) Papillae termination (0, open; 1, blind) Papillae height (0, 5 cm) Colour alive (0, yellow; 1, orange; 2, red; 3, blue; 4, white; 5, grey; 6, purple) Colour in EtOH (0, whitish–drab-cream; 1, yellowish; 2, beige–tan–light brown; 3, grey; 4, blue) Body surface (0, smooth; 1, hispid; 2, conulose; 3, rough–even–lumpy; 4, surface projections) Superficial canals (0, absent; 1, thin, vein-like) Oscule diameter (0, 500 µm)
01 02 03 04 05 06 07 08
Character
2 1 0 0 1 2 2
1 3
1
0 0
0
0 0 0 1
? 2
1
1
1 0 0 0 1 1–2
1
0
0 0 1 2 0 1 1 0–4
Petromica (C.) ciocalyptoides
2 1 0 0 1 1 1
0 3
1
0 0
0
0 0 1 1
0 2
1
1
0 1 1 1 1–2 1
2
0–1
0 1 1 2 1 0–1 0 0–1
Petromica (C.) citrina
2 1 1 1 1 1 1
0 3
1
0 0
0
0 0 0 0
0 2
1
1
1 0 1 0 1 1
2
0
0 0 1 2 1 0–1 0 0–1
Petromica (C.) pacifica
2 2 0 0 2 2 1
0 2
0
1 1
1
0 1 0 1
0 2
1
0–1
1 0 1 1 0 NA
2
0–2
0 0 2 0 NA NA NA ?
2 2 0 1 1 2 1
0 4
0
0 1
0
0 0 0 1
1 2
2
0
0 0 0 0 0 NA
1
0
1 1 2 0 NA NA NA ?
2 2 0 1 2 3 2
0 2
0
0 1
0
0 0 0 1
0 2
1
1
0 0 0 0 0 0
1
0
0 0 2 1 0 1 0 ?
2 2 1 1 2 3 2
0 2
0
0 2
1
0 1 0 1
1 2
2
1
0 ? 0 1 2 ?
2
1–2
1 0 2 2 0 0 0 ?
1 2 0 0 3 3 2
0 1
0
0 1
0
0 1 1 1
1 2
2
1
1 0 0 1 0 0
1
0
1 0 1 1 0 0–1 0 ?
Petromica (P.) Petromica (P.) Petromica (P.) Petromica (P.) Petromica (P.) grimaldii plumosa tubulata massalis digitata
2 1–2 NA NA NA NA NA
0 NA
NA
NA NA
NA
1 0 0 NA
1 1
0
1
0 0 1 0 1 1
1
0–4
0–1 0 0–1 0–2 NA–1 NA–0–1 NA–0 1–2–3
Hymeniacido n spp
2 2 NA NA NA NA NA
0 NA
NA
NA NA
NA
0 1 0–1 NA
NA 1
0
2
0 0 0 0 0 1
1
0–2
0 0 0–1 0–1 NA–0–1 NA–0–1 NA–1 2–4
Topsentia spp
1 1 NA 1 1 1 2
0 1
0
0 2
1
1 1 0 0
NA 0
0
0–1
0–1 0 0–1 0 2 NA
1
3
1 0 0–1 0 NA NA NA 0–1–3–5
1 NA 1 1 1 1 1
0 3
0
0 2
1
2 0 0 0
0 3
0–1
3
0–1 1 0–1 0 2 NA
1
0–2–3
0–2 0–1 0–1–2 0 NA NA NA 0–4–6
Desmanthus Gastrophanella spp spp
Table 1. Taxon × character matrix for Petromica Characters 1–29 from Muricy et al. (2001); new characters 30–37. Additional data from Muricy and Minervino (2000), Van Soest and Hajdu (2000), Pisera and Lévi (2002b). NA, not applicable character; ?, unknown state
Petromica in the Pacific 815
816
S. E. List-Armitage and J. N. A. Hooper
Fig. 1. Petromica (Chaladesma) pacifica, sp. nov. A–H, Variation in tips of oxeas; I–J, oxeas demonstrating variable curvature; K–N, desmas, ranging from a young form (K) to more ornate forms of multibranching zygomes (L–N). Annotations: e, epirhabd; c, clone; z, desma zygosis.
Definition
Systematics Order HALICHONDRIDA Gray Halichondriadae Gray, 1867: 518. Halichondrina Vosmaer, 1887: 335. Halichondrides Lévi, 1953: 3. Halichondriida Wiedenmayer, 1977: 148.
Ceractinomorpha Demospongiae with styles, oxeas, strongyles or intermediate spicules of widely diverging sizes, not functionally localised; skeleton plumoreticulate, dendritic or confused; microscleres if present microxeas and/or trichodragmas (from Hooper and Van Soest 2002).
Petromica in the Pacific
Family HALICHONDRIIDAE Gray Halichondriadae Gray, 1867: 518. Halichondridae Vosmaer, 1887: 335. Stylotellinae Lendenfeld, 1888: 185. Ciocalyptidae Hentschel, 1923: 408. Spongosoritidae Topsent, 1928: 35. Petromicidae Topsent, 1928: 24. Halichondriidae de Laubenfels, 1936: 133. Hymeniacidonidae de Laubenfels, 1936: 136. Monanthidae de Laubenfels, 1936: 139.
Diagnosis Halichondrida with confused arrangement of smooth oxeas and/or styles in the choanosome and usually an organised special ectosomal skeleton consisting of tangentially arranged or densely confusedly arranged crust of oxeas and/or styles of sizes similar to or smaller than those of the choanosome (from Erpenbeck and Van Soest 2002).
Genus Petromica Topsent Petromica Topsent, 1898: 226–229, fig. 1a. – Topsent, 1904: 64–66, pl. v, figs 2–4, pl. viii, fig. 6; Dendy, 1905: 104–105, pl. 4 fig.5; Topsent, 1928: 105–106; Pulitzer-Finali, 1970: 334; Van Soest et al. 1990: 41, 43, figs 57, 66; Diaz et al. 1991: 143–144, fig. 8; Diaz et al. 1993: 288–289, figs 1c,d, 9; Boury-Esnault et al. 1994: 57; Muricy et al. 2001: 105. Monanthus Kirkpatrick, 1903: 176–177, figs 6–7. – Burton, 1929: 9, plate 1, fig. 8a; Van Soest & Zea, 1986: 201–205, figs 1–6; Van Soest et al. 1990: 41, 43, figs 58–59. Type species: Petromica grimaldii Topsent, 1898 (by monotypy).
Definition Halichondriidae with monaxial desmas branching in various planes, forming loosely articulated or non-articulated (‘sublithistid’) choanosomal skeletal structure. Diagnosis (Expanded from Muricy et al. (2001) and Erpenbeck and Van Soest (2002).) Massive, globular or encrusting sponges, often with blind or open fistule-like papillae. Colour usually yellow, drab or light brown. Surface smooth, hispid or sometimes with sharp conulose surface projections. Consistency firm but compressible to rigid, friable to soft in one group of species. A detachable dermal membrane may be present, often with confused tangential reticulation of oxeas. Choanosomal skeleton with oxeas forming variable ascending tracts and dispersed in confusion. Desmas always present, varying from isolated, non-articulated, and concentrated in the basal layer of the sponge to articulated, fused, dispersed throughout the choanosome and ectosome. Oxeas smooth, fusiform, 380–1570 µm long (in species with only one size class of oxea), and including second class of smaller oxeas in some species (35–275 µm long). Oxea terminations range from sharply-pointed fusiform, to blunt, hastate, strongylote or mucronate, often with telescoped
817
points. Desmas monaxial (acrepid or monocrepid rhizoclone), with complex branching in several planes. Acrepid desmas (with the axial filament either absent or not visible) universal among species, but several have varying proportions of monocrepid desmas (with visible axial filament). Desmas 150–970 µm long, varying from simple, smooth and poorly ramified with no zygomes, to complex, highly ramified forms with microspined tips or multiple finger-like digitate zygomes, or occasionally with ‘ball-and-socket’ zygoses (but rarely are these fully articulated within the skeleton).
Key to species of Petromica 1. Generally soft consistency; multiple papillae supported internally by sinuous tracts of oxeas in a single size class; desmas predominantly monocrepidial, confined to the base of the skeleton and lacking zygoses between them (subgenus Chaladesma)............................................................................... 2 Generally firm to rigid consistency; few or no papillae; oxeas in two size classes; sublithistid skeleton extends into subectosomal or ectosomal regions; desmas mainly acrepidial; desma zygoses range from poorly articulated to nearly fused (subgenus Petromica) .................................................................................. 4 2. Desma zygomes usually number more than four (desma clone length 100–(159.3)–270 µm).................................................. P. pacifica Desma zygomes (branch tips) usually number two to three............ 3 3. Surface smooth and hispid; papillae long, cylindrical digitate; desmas relatively large (clone length 70–(355)–726 µm); dermal membrane easily detachable; raphide microscleres present ........................................................................... P. ciocalyptoides Surface conulose; papillae relatively short, conical-truncate; desmas relatively short (clone length 50–(126)–300 µm); dermal membrane barely detachable ......................................... P. citrina 4. Massive, burrowing growth form, with or without papillae; choanosomal ascending tracts of oxeas vague, sinuous ............. 5 Encrusting growth form; choanosomal ascending tracts of oxeas coalescent ................................................................................... 6 5. Papillae absent; desmas with few zygomes but microspined .............................................................................. P. grimaldii Papillae present; desma zygomes smooth and number more than four ..............................................................................P. tubulata 6. Desma skeleton with well-formed zygoses; many desma zygomes (up to six, average of four) ......................................... P. massalis Desma skeleton with poorly or moderately formed zygoses........... 7 7. Desma crepis length >500 µm long; oxeas >1000 µm long; subectosomal spaces present ........................................P. digitata Desma crepis length
