Suberites dandelenae, Samaai, Toufiek, Maduray, Seshnee, Janson, Liesl & Ngwakum, Benedicta, 2017

Samaai, Toufiek, Maduray, Seshnee, Janson, Liesl & Ngwakum, Benedicta, 2017, A new species of habitat – forming Suberites (Porifera, Demospongiae, Suberitida) in the Benguela upwelling region (South Africa), Zootaxa 4254 (1), pp. 49-81 : 70-76

Suberites dandelenae sp. nov.

( Figures 3 ; 11a–h; Table 2 ; Table 3; Table S1).

Synonomy. Suberites tylobtusa sensu Uriz, 1988 , pg 38 (Not Suberites tylobtusa Lévi, 1958 ); Suberites ficus sensu Samaai & Gibbons, 2005 , pg. 28, figs. 3A, 21 a–e. Suberites carnosus sensu Samaai & Gibbons, 2005 , pg. 27, figs. 2O, 20 a–d.

Material examined. Holotype. SAMC –A088677 (cross ref. TS 1625), West coast, Station A29477 (30°26'0"S, 16°48'59"E), depth 180 m, collected by FRS Africana, January 2009.

Other Material examined Holotype MNHN DCL 1301, Suberites tylobtusa Lévi, 1958 ; Holotype BMNH 1847.9.7.51, Halichondria fícus Johnston, 1842 .

Paratypes. SAMC –A088678 (cross ref. TS 1815), West coast, Station A30349 (31°47'58"S, 17°54'29"E), depth 114 m, collected by FRS Africana, January 2010 . SAMC –A088679 (cross ref. TS 1592), West coast, Station A29471 (29°12'0"S, 15°59'0"E), depth 166 m, collected by FRS Africana, January 2009 .

TS 1586, West coast, Station A29444 (30°58'0"S, 17°27'0"E), depth 134 m, collected by FRS Africana, January 2009 . TS 1587, West coast, Station A29442 (30°30'59"S, 17°19'0"E), depth 111 m, collected by FRS Africana, January 2009 . TS 1599, West coast, Station A29478 (30°19'0"S, 16°54'59"E), depth 154 m, collected by FRS Africana, January 2009 . TS 1602, West coast, Station A29482 (29°37'59"S, 16°20'0"E), depth 157 m, collected by FRS Africana, January 2009 . TS 1612, West coast, Station A29481 (29°40'59"S, 16°12'59"E), depth 166 m, collected by FRS Africana, January 2009 . TS 1614, West coast, Station A29480 (29°53'0"S, 16°18'0"E), depth 182 m, collected by FRS Africana, January 2009 . TS 1631, West coast, Station A29439 (30°50'0"S, 16°52'0"E), depth 198 m, collected by FRS Africana, January 2009 . TS 1633, West coast, Station A29479 (30°0'0"S, 16°20'59"E), depth 187 m, collected by FRS Africana, January 2009 . TS 1640, West coast, Station A27448 (32°0'24"S, 17°24'59"E), depth 160 m, collected by FRS Africana, January 2009 . TS 1783, West coast, Station A30328 (32°17'52"S, 16°53'53"E), depth 296 m, collected by FRS Africana, January 2010 . TS 1787, West coast, Station A30382 (29°32'13"S, 15°45'14"E), depth 175 m, collected by FRS Africana, January 2010 .

TS 1794, West coast, Station A30389 (29°20'13"S, 16°0'58"E), depth 168 m, collected by FRS Africana, January 2010 . TS 1798, West coast, Station A30340 (31°58'46"S, 16°52'10"E), depth 282 m, collected by FRS Africana, January 2010 . TS 1830, West coast, Station A31415 (31°22'5"S, 17°30'56"E), depth 147 m, collected by FRS Africana, January 2010 . TS 1836, West coast, Station A31460 (29°20'11"S, 16°1'1"E), depth 168 m, collected by FRS Africana, January 2011 . TS 1850, West coast, Station A31406 (32°7'32"S, 17°19'11"E), depth 184 m, collected by FRS Africana, January 2011 . TS 1859, West coast, Station A31417 (31°43'30"S, 17°1'30"E), depth 256 m, collected by FRS Africana, January 2011 . TS 1828, West coast, Station A30350 (31°34'58"S, 17°48'2"E), depth 118 m, collected by FRS Africana, January 2010 . TS 1876, West coast, Station A31405 (32°7'55"S, 17°12'7"E), depth 211 m, collected by FRS Africana, January 2011 . TS 1807, West coast, Station A30351 (31°19'47"S, 17°35'8"E), depth 133 m, collected by FRS Africana, January 2010 . TS 1810, West coast, Station A30357 (30°42'58"S, 16°53'19"E), depth 191 m, collected by FRS Africana, January 2010 . TS 1816, West coast, Station A30403 (31°8'38"S, 17°41'41"E), depth 89 m, collected by FRS Africana, January 2010 .

Other voucher specimens. TS 1584, West coast, Station A29490 (30°16'59"S, 15°43'59"E), depth 235 m, collected by FRS Africana, January 2009 . TS 1585, West coast, Station A29500 (31°29'0"S, 17°40'59"E), depth 125 m, collected by FRS Africana, January 2009 . TS 1589, West coast, Station A29443 (30°54'59"S, 17°20'0"E), depth 147 m, collected by FRS Africana, January 2009 . TS 1594, West coast, Station A29507 (33°22'0"S, 17°44'0"E), depth 183 m, collected by FRS Africana, January 2009 . TS 1601, West coast, Station A29501 (31°38'59"S, 17°47'59"E), depth 120 m, collected by FRS Africana, January 2009 . TS 1604, West coast, Station A29483 (29°29'59"S, 16°16'59"E), depth 155 m, collected by FRS Africana, January 2009 . TS 1611, West coast, Station A29502 (31°30'59"S, 17°58'0"E), depth 95 m, collected by FRS Africana, January 2009 . TS 1623, West coast, Station A29475 (30°22'59"S, 16°34'0"E), depth 208 m, collected by FRS Africana, January 2009 . TS 1628, West coast, Station A29461 (31°16'59"S, 17°12'59"E), depth 206 m, collected by FRS Africana, January 2009 . TS 1644, West coast, Station A29455 (32°18'59"S, 18°0'59"E), depth 103 m, collected by FRS Africana, January 2009 . TS 1784, West coast, Station A30359 (31°0'5"S, 16°0'52"E), depth 320 m, collected by FRS Africana, January 2010 . TS 1786, West coast, Station A30392 (29°8'33"S, 16°19'49"E), depth 138 m, collected by FRS Africana, January 2010 . TS 1789, West coast, Station A30341 (31°52'39"S, 17°7'3"E), depth 211 m, collected by FRS Africana, January 2010 . TS 1795, West coast, Station A30383 (29°36'57"S, 15°55'19"E), depth 178 m, collected by FRS Africana, January 2010 . TS 1797, West coast, Station A30392 (29°8'33"S, 16°19'49"E), depth 138 m, collected by FRS Africana, January 2010 . TS 1809, West coast, Station A30356 (30°49'35"S, 16°39'34"E), depth 239 m, collected by FRS Africana, January 2010 . TS 1813, West coast, Station A30385 (29°18'43"S, 16°33'41"E), depth 126 m, collected by FRS Africana, January 2010 . TS 1817, West coast, Station A30384 (29°46'46"S, 16°0'46"E), depth 185 m, collected by FRS Africana, January 2010 . TS 1819, West coast, Station A30395 (29°44'59"S, 16°29'17"E), depth 156 m, collected by FRS Africana, January 2010 . TS 1823, West coast, Station A30325 (32°48'44"S, 17°42'33"E), depth 142 m, collected by FRS Africana, January 2010 . TS 1826, West coast, Station A30352 (31°10'23"S, 17°20'33"E), depth 178 m, collected by FRS Africana, January 2010 . TS 1877, West coast, Station A31438 (30°38'19"S, 16°53'37"E), depth 186 m, collected by FRS Africana, January 2011 . TS 1621, West coast, Station A29470 (29°7'59"S, 16°5'59"E), depth 163 m, collected by FRS Africana, January 2009 .

TS 1805, West coast, Station A30353 (30°54'52"S, 17°3'18"E), depth 197 m, collected by FRS Africana, January 2010 . TS 1806, West coast, Station A30399 (30°21'1"S, 16°48'2"E), depth 179 m, collected by FRS Africana, January 2010 . TS 1812, West coast, Station A30381 (29°24'13"S, 15°30'20"E), depth 181 m, collected by FRS Africana, January 2010 . TS 1814, West coast, Station A30391 (29°28'59"S, 16°20'25"E), depth 151 m, collected by FRS Africana, January 2010 . TS 1837, West coast, Station A31413 (31°38'59"S, 17°39'16"E), depth 130 m, collected by FRS Africana, January 2011 . TS 1840, West coast, Station A31446 (29°0'26"S, 16°15'34"E), depth 141 m, collected by FRS Africana, January 2011 . TS 1841, West coast, Station A31439 (30°38'23"S, 17°9'20"E), depth 150 m, collected by FRS Africana, January 2011 . TS 1848, West coast, Station A31440 (30°40'43"S, 17°25'5"E), depth 98 m, collected by FRS Africana, January 2011 . TS 1849, West coast, Station A31441 (30°23'34"S, 16°59'47"E), depth 150 m, collected by FRS Africana, January 2011 . TS 1862, West coast, Station A31462 (29°39'28"S, 16°2'58"E), depth 181 m, collected by FRS Africana, January 2011 . TS 1868, West coast, Station A31437 (30°33'26"S, 16°50'0"E), depth 186 m, collected by FRS Africana, January 2011 .

Other South African & Namibian material examined. SAM –H4898 (Ts 330), Elands Bay (32°20’S, 18°20’E), depth 2–5 m, collected by T. Samaai and M. J. Gibbons, 7 April 1997 . Ts 343a, Elands Bay (32°20’S, 18°20’E), depth 2–5 m, collected by T. Samaai and M.J. Gibbons, 7 April 1997 . Ts 344, Ts 346, Ts 348, Ts 355, St Helena Bay (32°40’S, 18°10’E), depth 2–5 m, collected by T. Samaai and M.J. Gibbons, 9 April 1997 . Ts 412, Black Rock, Lüderitz , Namibia (24°50’S, 14°40’E), depth 12 m, collected by NSFRI, 20 March 1998 . SAM – H4897 (Ts 540), Oranjemund (26°31’S, 15°01’E), depth 78 m, collected by A. Goosen, from ‘ Jago’ submersible, April 1999 . Ts 541, Oranjemund (26°31’S, 15°01’E), depth 78 m, collected by A. Goosen, from ‘ Jago’ submersible, April 1999 .

Description of gross morphology. Massive sponge with rounded lobes and apical oscula ( Figure 11 a). Two morphotypes are distinguishable: (a) globulous, widest at the base, with one large apical osculum terminally, and (b) elongate, with compressed base from where a few globular lobes rise, each widest in the middle and terminating in a small osculum. Varied size, up to 40 cm in diameter. Surface smooth, microscopically hirsute, not velvety. Oscules 1–2 cm in diameter on the apical end of the lobe; ostia 0.1 mm in diameter. Consistency spongy, soft, depending on the degree of contraction. Ectosome not discernable. Colour in life straw orange brown with some having tinges of yellow, choanosome orange–yellow internally; in preservative light brown or straw yellow to khaki. Mud encrusted specimens are greyish brown.

Megascleres. Type I Tylostyles. Thin, long, straight or curved, with a sharp gradually tapering end, heads well rounded, distally fusiform, 505 (413–576) × 7 (7) µm, n = 10 ( Figure 11 b–I). Type II Tylostyles. More robust, thickened and somewhat curved, head well defined and rounded, distally fusiform, 351 (307–413) × 19 (14–24) µm, n = 10 ( Figure 11 b–II). Type III Tylostyles. Thick, straight, head well defined and rounded 465 (451–490) ×14 (9.6–19) µm, n = 10 ( Figure 11 b–III). Large tylostrongyles (tylobtuse strongyles). Thick, variable size, head poorly defined, but round, often somewhat wider than opposite rounded end, 271 (240–307) × 24 (19–29) µm, n = 10 ( Figure 11 c). Centrotylostrongyles. Thick, variable size, straight or slightly curved, with bulbous centre, end not fusiform but hastately rounded 307 (259–346) ×14 (9.6–19) µm, n = 10 ( Figure 11 d). Centrotyloxeas. Thick, variable size, sinuous or slightly curved, with bulbous centre, end fusiform, but some forms are centrotylostrongyles, 414 (365–518) ×16 (14–19) µm, n = 10. Small tylostrongyles (tylobtuse strongyles). Thick, variable size, head well defined, and rounded, 163 (115–201) ×24 (19–29) µm, n = 10 ( Figure 11 e). Small mutant tylostrongyles (kidney–shaped) also present with size approximately 86 (76–96) x 19 µm, n = 10 ( Figure 11 f). Some specimens e.g. TS 1815 and TS 1592 lack the tylobtuse strongyles (see Figure 3 ). These megascleres are present in variable proportions in all the specimens examined.

Microscleres. Microrhabds (microacanthostrongyles, usually centrotylote), rare in some specimens or even absent (e.g. Figure 3 —specimen TS 1592), 10–15 µm ( Figure 11 g). The morphology of the microacanthostrongyles is similar to that found in S. ficus . It is present in variable proportions in all the specimens examined.

Skeleton. Choanosomal skeleton consists of a subradiate, composed of a confused irregular reticulation of bundles of tylostyles, which meander vertically through the choanosome. Spicules radially arranged near the surface, and the internal skeleton confused, almost halichondroid ( Figure 11 h). The ectosome consists of a distinct, compact, radially disposed layer of small dermal tylostyles, 200–400 µm wide. Distal ends of tylostyles project slightly beyond the ectosomal surface.

DNA barcodes. Two unique cox1 haplotypes were identified among a total of 20 specimens. GenBank accession nos. KY463455 (haplotype 1) and KY463456 (haplotype 2).

Etymology. Named after Ms Dandelene Reynolds, a technician in DEA, who passed away in 2010.

Phenotypic variation. The species variability is limited to the sponge size with a uniform straw orange brown.

Type locality. The type material was collected from the west coast of South Africa, from unconsolidated sediment in a region with seasonal cold-water upwelling.

Distribution. South African and Namibian west coast (BCLME) ( Figures 7 & 12 )

Ecology. Uriz (1988, 1990) proposed that S. tylobtusus (Red Sea sponge) was translocated by fisheries activities to the continental shelf off southern Africa between 1960 and 1984, as earlier surveys conducted over many decades had failed to detect it. These earlier surveys however, were not comprehensive or thorough, and focused their efforts around Cape Town, Saldanha Bay, Still Bay and Durban, all of which fall outside its distributional range.

Suberites dandelenae sp. nov. is particularly abundant at depths ranging between 80–500 m, on the continental plateau of the west coast of South Africa and Namibia ( Samaai & Gibbons 2005; Uriz 1988, 1990) ( Figure 7 & 12 ) where it may dominate epibenthic communities in terms of biomass, forming “sponge beds or facies” ( Uriz 1988, 1990). During various trawl surveys on the west coast of South Africa (with the Research Vessels Dr Fridjof Nansen and RV Africana), more than 6 tons /km2 of sponge material were obtained during several hauls within depths ranging 120– 275 m. The greatest mass of sponges collected was 18 tons /km2, from a depth near 138 m off Doring Bay (2006–Cruise 402, Station 1250). The three localities off Port Nolloth produced 3–3.5 tons /km2 of sponges collected on average, while 6 tons /km2 of sponges were obtained from one site at a depth of 195 m in the proposed Namaqualand MPA (Nansen Cruise 402, Station 1196, 2006) ( Figure 13 ). The commercial trawler fleet generally fishes in water that is deeper (200–1000 m) than that of the sponge beds, but there is an overlap in the distribution of the sponge and diamond mining and oil and gas operations (Atkinson et al. 2011; Sink et al. 2012). The potential threats of these activities on the filter feeding sponge community have yet to be assessed.

Suberites dandelenae sp. nov. is not a reef builder, but it can be habitat forming and occurs in soft sediment environments. The sponge beds constitute an ecologically important habitat of great complexity for fishes and both motile and sessile invertebrates, and they may play an important role in the ecology and diversity of the west coast region. Indeed, their presence could constitute a Vulnerable Marine Ecosystem (VME) or an Ecologically and Biologically Significant Area (EBSA).

Remarks. The identification of Suberites at the species level based on morphological features is difficult, because species of this genus are highly polymorphic and have a simple skeleton and spicular structures, which are more or less homogeneous (Solé– Cava & Thorpe 1986; Van Soest 2002). Having said that, it has been argued that the use of qualitative characters such as the presence or absence of microscleres (microstrongyles) is helpful in distinguishing species, e.g. S. ficus from S. domuncula ( Hartman 1958; Hiscock et al. 1983). However, it is clear from the present results (Table S1) that although there are taxonomically useful spicule differences between specimens, these qualitative and quantitative differences can be misleading in defining a species. Suberites dandelenae sp. nov. specimens show considerable variation in the relative proportion or presence of different spicule types.

Typically, S. dandelenae sp. nov. has three distinct types of megascleres, but some specimens (see Table 2 ) possess only tylobtuse strongyles and microstrongyles, or they lack tylobtuse strongyles but possess microstrongyles, and some specimens lack both tylobtuse strongyles and microstrongyles (see also Figure 3 ). This exemplifies the importance of studying a range of specimens to find phenotypic and histological characters that are useful in fitting the puzzle to correctly identify or separate species. Differences only become evident when the specimens are studied together ( Tables 2 & Table S1). The new species exhibits a number of affinities with S. ficus (see Uriz 1988, 1990), both in terms of external morphology and in the structure of the centrotylote microscleres. It differs from S. domuncula , S. carnosus and S. tylobtusus in external morphology, having centrotylote microscleres and generally larger megaslere spicules (see Tables 3 & Table S1).

The absence of centrotylote microscleres, tylostrongyle megascleres and the poorly developed tylostyle megascleres in some specimens of S. dandelenae sp. nov. illustrates that secondary loss of spicules can occur readily. Sponge taxonomy is largely based on spicule morphology, but spicules have already been shown to be potentially unreliable for phylogenetics due to their high level of morphological homoplasy ( Fromont & Bergquist 1990; Manuel et al. 2003; Cárdenas et al. 2011), as well as for alpha–taxonomy due to intra–specific variation ( Schönberg & Barthel 1998).

Zea (1987) found that spicules, especially microscleres, can be present or absent in sponge specimens depending on their location, and that variations in megascleres are rare. Maldonando et al. (1999) showed that variation in spicule type and shape can also be explained by silicon limitation. Although there is considerable latitudinal variability in the frequency, intensity and seasonality of upwelling in the Benguela ecosystem, the region is not generally considered to be silicon–poor in deeper water. It is worth noting here that whilst surface waters may become stripped of silica by diatoms in upwelling areas, the same is not true of bottom waters where the sponges are found owing to remineralisation ( Pitcher et al. 1992). Location and seawater chemistry are unlikely to be responsible for the considerable variation in spicule types found in S. dandelenae sp. nov. as samples collected from the same trawl often had different spicule complements ( Figure 8 ).

The magnitude between depth differences in concentration of dissolved silicate (and temperature), have been examined in order to assess their potential relevance in the development and/or maintenance of the sponge aggregations. The mean concentration of silicate, a crucial nutrient used by sponges to build their silica skeleton, ranges from 12.22 to 17.36 µM over the year between 100–400 m depth, being only approximately 20 µM lower on average than values deeper than 400 m. Suberites dandelenae sp. nov. is most abundant between the 100–200 m depth range. Temperature values decrease towards the deeper depths.

It remains unclear what the particular conditions are that have favored the impressive aggregation of S. dandelenae sp. nov. between 100–200 m depth range. As this sponge is characterized by a well–developed organic body by having a massive silica skeleton, it would be expected to require large amounts of dissolved silicon for growth and build its skeletal framework. However, average silicate concentrations where the sponges are found were stable, even in areas where the sponge occurs in far lower abundance. The data suggest that dissolved silicon availability in the southern Benguela may not be particularly responsible for the occurrence of S. dandelanae sp. nov.. Intra–specific variation in spicule complement can often be the result of phenotypic plasticity due to the influence of environmental factors. Our study, like that of Cárdenas & Rapp (2013) presents another case of intra– specific spicule variation, most probably as a consequence due to sponge size (or age), as opposed to reflecting changes due to environmental conditions or latitudinal/bathymetric variations ( Figure 14 ). However, little more than mere speculation can be offered at the current stage of knowledge, because virtually nothing is known both about the reproductive biology and dispersal ability of this new Suberites species. This study reiterates the point by Cárdenas & Rapp (2013) that taxonomist should be careful when delinating species only by the presence or abundance of one type of spicule. A few examples of such inappropriate use of spicules as morphological characters exist in the genera Erylus, Geodia ( Cárdenas & Rapp 2013) and Crambe ( Maldonado et al. 1999).

Based on the above considerations, megasclere type may not be a stable or valid taxonomic character for species discrimination within the genus Suberites . The structure and presence of centrotylote microscleres, as a trait for species identification, should also be considered carefully due to the rarity and possible inconsistent occurrence of this type of microsclere in the new species. Nevertheless, the present species is clearly distinct from other Suberites species (Table S1), and any uncertainties regarding this particular trait are irrelevant in its recognition as a new species.

Further studies are needed to fully document the population dynamics of S. dandelenae sp. nov. in light of our conclusions that the species has a restricted geographical range in the southern Benguela upwelling region, and it is critical to understand the species' ecological role in the region’s coastal and continental shelf marine ecosystems.

Figures

FIGURE 3. Three specimen groups for west coast S. dandelenae sp. nov.

FIGURE 7. Geographical distribution of Suberites dandelenae sp. nov. along the west coast of South Africa (Green dots); Red dots—other sponge species distributions collected during trawl surveys.

FIGURE 8. Geographical distribution of the various groups within S. dandelenae sp. nov. along the west coast of South Africa.

FIGURE 11. Type specimens of S. dandelenae sp. nov.; a. habitus; b. Various sizes of tylostyles; c. Large tylostrongyles; c & d. Small & medium tylostrongyles; e. Microspined microcentrostrongyles; f. Skeletal architecture of Suberites dandelenae sp. nov.

FIGURE 12. Geographical distribution of S. dandelenae sp. nov. in the Benguela Large Marine Ecosystem (BCLME)

FIGURE 13. Heatmap indicating high densities of S. dandelenae sp. nov.

FIGURE 14. Percentage frequency of occurrence for the various groups found in S. dandelenae sp. nov.