Tsitsikamma (Tsitsikamma) favus Samaai & Kelly, 2002

Samaai, Toufiek, Kelly, Michelle, Ngwakum, Benedicta, Payne, Robyn, Teske, Peter R., Janson, Liesl, Kerwath, Sven, Parker, Denham & Gibbons, Mark J., 2020, New Latrunculiidae (Demospongiae, Poecilosclerida) from the Agulhas ecoregion of temperate southern Africa, Zootaxa 4896 (3), pp. 409-442 : 417-423

Tsitsikamma (Tsitsikamma) favus Samaai & Kelly, 2002

( Figs 8 , 9 , Table 1, 2)

Tsitsikamma favus Samaai and Kelly, 2002: 718 ; fig. 6 A–G.

Tsitsikamma favus, Samaai et al. 2003: 11 ; fig. 3f; 17; fig. 6A; Parker-Nance et al. 2019: 105; fig. 1a–p; table 1.

Type & locality (not examined). Holotype — NHMUK 1997.7 .3.2, Rheeders Reef, Tsitsikamma National Park, 34.166° S, 23.900° E, 22 m, collected by P. Coetzee, 1995.

Material examined. NIWA 110724 , Table Top Reef, Algoa Bay, Port Elizabeth , 33.980° S, 25.693° E, 18 m, collected by Patrick L. Colin , CRRF, 4 Oct 1998, identified by Michelle Kelly , NIWA, Auckland; NIWA 110826 , White sands Reef, Algoa Bay , Port Elizabeth , 33.995° S, 25.707° E, 14 m, collected by Patrick L. Colin , CRRF, 17 Feb 1999, identified by Michelle Kelly , NIWA; NIWA 111059 , Grootbank, Plettenberg Bay , 34.007° S, 23.496° E, 10–14 m, collected by Patrick L. Colin , CRRF, 22 Mar 2000, identified by Michelle Kelly , NIWA, Auckland; SAMC-A091443, Grootbank, Plettenberg Bay , 34.007° S, 23.496° E, 10–14 m, collected by Patrick L. Colin , CRRF, 22 Mar 2000, identified by Michelle Kelly , NIWA, Auckland. SAMC-A090900, SAMC-A090902, Flat Rock, Jeffreys Bay , 34.102° S, 24.958° E, 13 m, collected by M. Pfaff, S. Kirkman, I. Malick and L. Snyders , 8 Aug 2016; SAMC-A090901, Grootbank, Plettenberg Bay , 34.006° S, 23.495° E, 40 m, collected by T. Samaai , 25 Feb 1999; SAMC-A090903, Seal Point, Cape St Francis , 34.223° S, 25.852° E, 15 m, collected by T. Haupt & I. Malick , 9 Aug 2016; SAMC-A090904, SAMC-A091416, SAMC-A091417, SAMC-A091418, Evans Peak, Algoa Bay, Port Elizabeth , 33.842° S, 25.816° E, 30 m, collected by Rhodes University , May 2010; SAMC-A090905, Bell Buoy, Sardinia Bay, 33.980° S, 25.698° E, Algoa Bay , Port Elizabeth , 16 m, collected by C. Evans , 25 May 2009; SAMC-A090906, Tsitsikamma National Park , 34.091° S, 23.895° E, 14 m, collected by T. Samaai , May 2009; SAMC-A091414, Rheeders Reef, Tsitsikamma National Park , 34.166° S, 23.900° E, 18 m, collected by M. Davies-Coleman , 1 Oct 1998; SAMC-A091415, Rheeders Reef, Tsitsikamma National Park , 34.166° S, 23.900° E, 22 m, collected by M. Davies-Coleman , 25 Feb 1994; SAMC-A091419, SAMC-A091420, SAMC-A091421, Evans Peak, Algoa Bay, Port Elizabeth , 33.842° S, 25.816° E, 30 m, collected by Rhodes University , May 2009; SAMC-A091422, SAMC-A091423, SAMC-A091424, Phillips Reef, (33.974° S, 25.681° E), Algoa Bay, Port Elizabeth , 30 m, collected by Rhodes University , 10 Aug 2010; SAMC-A091425, Suicide Reef, Sardinia Bay, 34.005° S, 25.636° E, Algoa Bay , Port Elizabeth , 16 m, collected by C. Evans , 25 May 2009; SAMC-A091426, off Christian Centre, Sardinia Bay, 34.053° S, 25.648° E, Algoa Bay , Port Elizabeth , 16 m, collected by C. Evans , 25 May 2009; SAMC-A091427, Swim Thru, Sardinia Bay, 34.049° S, 25.648° E, Algoa Bay , Port Elizabeth , 16 m, collected by C. Evans , 25 May 2009; SAMC-A091428, Seal Point, Cape St Francis , 34.223° S, 25.852° E, 15 m, collected by T. Haupt & I. Malick , 8 Aug 2016; SAMC-A091429, Table Top Reef, Algoa Bay, Port Elizabeth , 33.980° S, 25.693° E, 16 m, collected by Patrick L. Colin , CRRF, 4 Oct 1998, identified by Michelle Kelly , NIWA. SAMC-A091442, Grootbank, Plettenberg Bay , 34.006° S, 23.384° E, 16 m, collected by T. Samaai , 25 February 1999.

Additional material (not examined). CASIZ 300535, Table Top Reef, Algoa Bay, Port Elizabeth , 33.980° S, 25.693° E, 16 m, collected by Patrick L. Colin, CRRF, 4 Oct 1998 , identified by Michelle Kelly, NIWA; CASIZ 300636 , White sands Reef, Algoa Bay , Port Elizabeth , 33.995° S, 25.707° E, 14 m, collected by Patrick L. Colin, CRRF, 17 Feb 1999 , field identification by L. J. Bell, CRRF, listed in Parker-Nance et al. (2019); CASIZ 301054, Grootbank, Plettenberg Bay , 34.007° S, 23.496° E, 10–14 m, collected by Patrick L. Colin, CRRF, 22 Mar 2000 , identified by Michelle Kelly, NIWA, Auckland; SAIAB 141112 , Knoll Reef, Tsitsikamma National Park , 34.166° S, 23.900° E, 18 m, collected by C. Buxton & M. Davies-Coleman, 2 May 1993 ; SAIAB 141356 , Rheeders Reef, Tsitsikamma National Park , 34.166° S, 23.900° E, collected by P. Coetzee, R. Palmer & B. Carté, 18 Mar 1995 .

Type location. Rheeders Reef, Tsitsikamma National Park, 22 m.

Distribution. Plettenberg Bay, Tsitsikamma Marine Protected Area, St. Francis Bay, St. Jeffreys Bay, Sardinia Bay and Algoa Bay.

Diagnosis. Varying morphology being either massive, lobate sometimes hemispherical to thickly encrusting, 5–10 cm thick and 10–20 cm diameter, surface very rugose and crowded with large single to multichambered cylindrical lance-shaped (button shaped) oscules, 1–4 mm wide, 6 mm high and with cauliform areolate porefields, 3 mm wide, 3–5 mm high, with no membrane ( Fig. 8 ). Sponge is hard and slightly compressible or soft and fleshy; colour in life vary being either dark brown, liver brown, turquoise or dark green ( Fig. 8 ; Table 1), internally olive or dark green/brown; in alcohol, ectosome black or dark brown, choanosome black. The choanosome is divided into honeycomb-like chambers and convoluted layers by very thick reinforced tracts of anisostyles, forming meshes that are elliptical in shape and 5800 μm wide ( Fig. 9 ). The ectosome is composed of a thick, dense feltwork of tangential and paratangential anisostyles. A single layer of erect isochiadiscorhabds lines the surface of the ectosome ( Fig. 9 ). Megascleres ( Table 1, 2) are anisostyles in two size categories: (1) slightly curved and thickened centrally, 621 (537–700) × 14 (14) μm); (2) thinner slightly curved centrally: type species: 530 (480–566) × 9.6 (9.6) μm) ( Table 2). Microscleres ( Fig. 9 ; Table 1, 2) are isochiadiscorhabds with three whorls of cylindrical, conical tubercles, the apex of each tubercular projection is acanthoses; some isochiadiscorhabds (10%) malformed or having a rudimentary forth whorl ( Fig. 9 ): 48 (41–60) × 9 (7.2–9.6). Sponge occurs in exposed coastal bays from Plettenberg Bay to Algoa Bay at depths of 9–40 m; abundant between 15–20 m in areas of strong surge where coastal upwelling occurs. Attached to hard rocky substrata associated with other invertebrates. Specimens are often abundant and occur within a metre distance from one another. The species contains biologically active pyrroloiminoquinone alkaloids, tsitsikammamines A and B and discorhabdin derivatives +14-Bromo-3-dihydrodiscorhabdin C and 14-Bromodiscorhabdin C that may have pharmacological potential [Cytotoxicity against Human Colon Tumour cell line (HCT 116)] ( Antunes et al. 2004, 2005).

DNA sequence data. We sequenced partial COI of collected material from different localities; GenBank accession numbers: COI MK153285 – MK153287 , MK153289 , MK153292 – MK153293 , MK153288 , MK153290 – MK153291 .

Remarks. When T. (T.) favus was first described, it was considered to be rare ( Samaai and Kelly 2002; Samaai et al. 2006) as it was only known from reefs shallower than 20 m at Tsitsikamma MPA and Algoa Bay. We have made spicule measurements and compared the isochiadiscorhabd morphology for a variety of Tsitsikamma specimens collected from St. Francis Bay (FB), Jeffreys Bay (JB), and the deeper reefs (30–40 m) off Grootbank, Plettenberg Bay (PB) (see also Parker-Nance et al. 2019) and found them to be similar in morphology and spiculation to T. (T.) favus described by Samaai et al. (2004) from Tsitsikamma MPA (T) and Algoa Bay (AB). These locations are within a 100 nautical mile (nmi) radius (T – PB = approx. 20 nmi; PB – JB = approx. 50 nmi; JB – AB = approx. 40 nmi) and form part of an extensive subsurface cold-water ridge area on the south coast (Agulhas ecoregion) (see Hutchings et al. 2002). Extensive surveys conducted along the South African coast in the last couple of years, failed to spot any T. favus south of 30◦ S or north of 33◦ S, thus suggesting this species has a geographic range that is influenced by coastal upwelling (see Fig. 2 , 3 ). This is in marked contrast to the southeast coast environment were the three new Tsitsikamma spp. were retrieved.

While we have expanded both the geographical and depth range of this species, its range is nonetheless small, and restricted to coastal upwelling zones on the south coast of South Africa. The morphology, spicule complement, and spicule sizes of the new material all fall within the size range of the type specimen ( Table 2) .

Examination of the numerous T. (T.) favus specimens across its geographical ranged allowed us to assess the intra-specific morphological variation of the external morphology, colour, shape of oscula and areolate porefields and the shape of the isochiadiscorhabds and structure of the conical tubercles. We found that the majority of isochiadiscorhabds possess three whorls, with a small percentage being malformed or having a rudimentary forth whorl ( Fig. 9 ). The variation in isochiadiscorhabd morphology of T. (T.) favus was also observed by Samaai and Kelly (2002), Kalinski et al. (2019) and Parker-Nance et al. (2019). Tsitsikamma (T.) favus have a characteristic base pigmentation of deep brownish black or liver brown that is often and variously tinged with deep green to dark turquoise; the ethanol preservative is always oily-looking and deeply pigmented; while the preserved specimens are dark brown. Some species are a lighter oak brown throughout. It is interesting to note that specimens of T. (T.) favus without discorhabdins are a lighter brown than their discorhabdin-containing siblings ( Samaai and Kelly 2002).

Tsitsikamma (T.) favus occurs with T. (T.) scurra in areas of local coastal upwelling or high wave surge. Tsitsikamma (T.) scurra differs from T. (T.) favus in the following characteristics: 1) Tsitsikamma (T.) scurra is lime green with a brownish surface in situ, and has long, hollow, strappy oscular fistules ( Fig. 10 ), while T. (T.) favus is turquoise to dark brown or olive brown, semispherical and with short surface extensions ( Fig. 8 ); 2) Tsitsikamma (T.) scurra has a folded globular thick encrusting growth structure with thin sandpaper-like ectosome ( Fig. 10 ) ( Samaai et al. 2006; Parker-Nance et al. 2019) while T. (T.) favus has a globular to semi-spherical morphology with a dense, thick ectosome; 3) Tsitsikamma (T.) scurra has larger, thicker anisostyles [thick 829 (774–882) × 24 μm; thin 669 (585–738) × 17 μm] than T. (T.) favus [thick 621 (537–700) × 14 (14) μm; thin 530 (480–566) × 9.6 (9.6 μm], but the isochiadiscorhabds are smaller than those found in the type species [ T. (T.) scurra : 41 (38–45) × 8 μm; T. (T.) favus : 48 (41–60) × 9 (7.2–9.6) μm] (see Table 1); 4) Isochiadiscorhabds of Tsitsikamma (T.) scurra ( Fig. 10 ) have three whorls of conico-cylindrical tubercules project at 45° to the shaft in pairs whereas up to five complete whorls as well as many intermediate forms are found in T. (T.) favus . The tubercles projections are either arranged in pairs or in groups of three in T. (T.) favus ; 5) The distribution of the two species is disparate; Tsitsikamma (T.) scurra is recorded from Hout Bay in the southern Benguela ecoregion while T. (T.) favus is recorded from the Agulhas ecoregion; 6) Tsitsikamma (T.) scurra only contains the biologically active pyrroloiminoquinone alkaloid derivative 14-Bromodiscorhabdin C ( Antunes et al. 2004), while in T. (T.) favus the biologically active pyrroloiminoquinone alkaloid tsitsikammamines A and B and discorhabdin derivatives +14-Bromo-3-dihydrodiscorhabdin C and 14-Bromodiscorhabdin C are found ( Samaai and Kelly, 2002; Antunes et al. 2004, 2005).

Tsitsikamma (T.) favus can also be compared to T. (T.) nguni : (1) Tsitsikamma (T.) nguni is dark slate to black coloured in situ, thickly encrusting or hemispherical, and has small short, blunt rounded knob-shape or button like oscula and small round porefields; (2) Tsitsikamma (T.) nguni are also firm and ridged, with a thick ectosome visible, like in T. (T.) favus (Parker-Nance et al. 2019) ; (3) Tsitsikamma (T.) nguni have on average smaller anisostyles [thick 555 (428–672) × 14 (10–19) μm; thin 561 (449–832) × 10 (3–14) μm] (see also Tables 1, 2) (Parker-Nance et al. 2019) than T. (T.) favus [thick 621 (537–700) × 14 (14) μm; thin 530 (480–566) × 9.6 (9.6) μm]; (4) the isochiadiscorhabds are similar in average size (51 (40–60) μm) to that found in type species [ T. (T.) favus : 48 (41–60)] ( Table 1, 2). Tsitsikamma (T.) favus and T. (T.) nguni differ in the number of the cylindrical-conical tubercles found on the isochiadiscorhabds; three per group in T. (T.) favus and four to six in T. (T.) nguni (Parker-Nance et al. 2019) (see also Fig. 5 ). The other apparent difference between T. (T.) favus and T. (T.) nguni is in the surface morphology, where T. (T.) favus have short, thick cauliform areolate porefields and lance-shaped oscula, oppose to blotchedshaped porefields and small button-shaped oscula in T. (T.) nguni .

No intraspecific genetic diversity was found for the COI gene sequence of specimens of T. (T.) favus in this study. The same results were also found by Parker-Nance et al. (2019) for specimens of T. (T.) favus using the 28S rRNA gene sequences.

Figures

FIGURE 2. Distribution of the two major ocean currents that sweep the coastal regions of South Africa; the warm Agulhas current on the south and east coasts, and the cold Benguela current on the west coast. Green circles indicate areas of coastal upwelling.

FIGURE 3. Map of South Africa showing sampling localities for sponges over the period 2010–2017: A. Shallow-water sampling localities (1–40 m), including the mesophotic reefs on the Agulhas Bank; B. Deep-water sampling localities (50–500 m) by trawl surveys and dredging (black dots) and locations were sponges were collected (red dots); C & D. Locations on the southeast coast, between Tsitsikamma and Amathole region, where Tsitsikamma and Cyclacanthia species co-occur, Tsitsikamma being endemic to the southeast coast (shown in C), Cyclacanthia also occurring further north in the Natal ecoregion (not shown here).

FIGURE 5. Microsclere morphology in Tsitsikamma (Tsitsikamma) and T. (Clavicaulis subgen. nov.) species (not to scale): A. T. (T.) favus Samaai & Kelly, 2002; B. T. (T.) scurra Samaai & Kelly 2003; C. T. (T.) amatholensis sp. nov.; D. T. (T.) nguni Parker-Nance, 2019; E. T. (Clavicaulis) pedunculata Samaai & Kelly, 2003; F. T. (C.) madiba subgen. et sp. nov.; G. T. (C.) michaeli Parker-Nance, 2019; H. T. (C.) beukesi subgen. et sp. nov.

FIGURE 8. Variation in in situ morphology and colouration of Tsitsikamma favus Samaai & Kelly, 2002. Specimens collected from (A) Tsitsikamma National Park, (B) St. Francis Bay, (C) Tsitsikamma National Park, (D) Grootbank, Plettenberg Bay, (E) Algoa Bay, (F) St. Francis Bay, (G) Algoa Bay, (H) Jeffreys Bay, (I) Jeffreys Bay.

FIGURE 9. Variation in the isochiadiscorhabd of Tsitsikamma (T.) favus Samaai & Kelly, 2002: A, B. Isochiadiscorhabd, holotype NHMUK 1997.7.3.2; C. Skeletal architecture, holotype NHMUK 1997.7.3.2, showing thick ectosome (dark band) and honeycomb-like chambers and convoluted layers of very thick reinforced tracts of anisostyles, forming meshes that are elliptical in shape; D, E. Isochiadiscorhabd, specimen SAMC-A090903; F, G. Isochiadiscorhabd, specimen SAMC-A091421; H–J. Isochiadiscorhabd, specimen SAMC-A091442.

FIGURE 10. Tsitsikamma (T.) scurra Samaai & Kelly, 2003, holotype NHMUK2003.1.10.3: A. Preserved holotype; B, C. Isospinodiscorhabds from holotype; D. Skeletal architecture from holotype showing the ectosome (dark band) and choanosome of Tsitsikamma (T.) scurra. Tsitsikamma (T.) amatholensis sp. nov.: E. Preserved paratype SAMC-A090877; F–H. Isochiadiscorhabds from paratype; I. Preserved holotype SAMC-A090878; J–L. Isochiadiscorhabds from holotype; M. Skeletal architecture of holotype showing ill-formed, irregular reticulation of anisostyles and a single layer of erect isochiadiscorhabds lines the surface of the ectosome.