A new species of Agelas from the Zanzibar Archipelago, western Indian Ocean (Porifera, Demospongiae).

A new sponge species (Demospongiae: Agelasida: Agelasidae) is described from the eastern coast of Unguja Island in the Zanzibar Archipelago. Agelas sansibarica sp. n. is compared to all other Agelas species described so far. The new species differs from its congeners mainly in its three categories of verticillate spicules (acanthostyles, acanthostrongyles, and acanthoxeas) and their sizes. Acanthostrongyles, well represented in the spicular complement, are an exclusive trait of the new species widening the morphological range of the genus. Summarizing on spicular complement and spicular morphotraits of 36 species belonging to the genus Agelas: i) 32 species show only acanthostyles from Indo-Pacific (n = 14), Atlantic (n = 17), and Mediterranean (n = 1); ii) three Indo-Pacific species show acanthostyles and acanthoxeas; iii) one species Agelas sansibarica sp. n. from the western Indian Ocean is characterised by the unique trait of three categories of verticillate spicules (acanthostyles, acanthostrongyles and acanthoxeas). A key for the Indo-Pacific species is supplied together with short descriptions, illustrations, and geographic range; literature on chemical bioprospecting of the genus Agelas is also provided.

Introduction

The sponge fauna of the Zanzibar Archipelago is poorly studied and data are reported almost exclusively in very old papers (Lendenfeld 1897, Baer 1906, Jenkin 1908, Sollas 1908, Thomas 1976). In none of these papers species belonging to the genus Duchassaing & Michelotti, 1864 (: : : ) are reported. The presence of (Carter, 1883) along the Zanzibar coasts was recently recorded (Said et al. 2010) as producer of bioactive compounds.

The widespread genus , including until now 35 valid species, was established by Duchassaing and Michelotti (1864: 76) describing the type species from the Caribbean Sea. is the only Mediterranean species, and is endemic. The western Atlantic (Gulf of Mexico, Caribbean, and Brazil) hosts 17 species. The majority of the latter (13) were recently revised while the remaining four species were considered dubious or suggested as synonyms (Van Soest 2002, Muricy et al. 2011, Parra-Velandia et al. 2014).

The Indo-Pacific species of number 18, including the new species here described. The most widespread species is (including its variety) recorded in the Australian western Pacific, and the Indian Ocean from the Mascarenes Archipelago (type locality), Seychelles Archipelago, Madagascar, and Mozambique Channel to the southern Red Sea and east to Sri Lanka.

Several species (14) are reported only once from the type locality i.e. Hentschel, 1911; Vacelet, Vasseur & Lévi, 1976; Thomas, 1998 (1997); (Gray, 1867); Thiele, 1903; Gotera & Alcolado, 1987; Lévi, 1993; Pulitzer-Finali, 1986; de Voogd, Parra-Velandia & Van Soest, 2008; Hoshino, 1985; Hoshino, 1985; Lévi & Lévi, 1983; , Pulitzer-Finali 1982; Pulitzer-Finali, 1996.

In the framework of sponges, applied research on bioactive compounds at a global level (e.g. Murray et al. 2013) focuses on species as producers of interesting molecules e.g. , , , , , and (Walker et al. 1981, Fathi-Afshar et al. 1989, Keifer et al. 1991, Braekman et al. 1992, Bernan et al. 1993, König and Wright 1993, Chanas et al. 1996, König et al. 1998, Eder et al. 1999, Assmann et al. 2000, 2001, 2004, Fattorusso and Taglialatela-Scafati 2000, Assmann and Köck 2002, Fujita et al. 2003, Bickmeyer et al. 2004, 2005, 2008, Bickmeyer 2005, Costantino et al. 2006, Meketa and Weinreb 2006, Ferretti 2006, Vik et al. 2006, Ding et al. 2007, Ferretti et al. 2007, 2009, Vergne et al. 2008, Hertiani et al. 2010, Said et al. 2010, Regalado et al. 2011, Mordhorst et al. 2015). In this scenario of intensive bioprospecting, research knowledge of systematics and taxonomy in depth is a key tool to identify and define the status of specimens/biomaterial to be processed.

The present paper aims to report the discovery of a new species of from the Zanzibar Archipelago comparing it to all species belonging to the genus. To support global sharing of information on faunistics and taxonomy of from not widely accessible data sources an updated overview on the morphology and geographic distribution of PageBreak species from the Indo-Pacific area is also provided together with a brief description and exhaustive iconography, as well as a dichotomous key to Indo-Pacific species.

Materials and methods

Representative fragments of six sponge specimens from the Unguja Island were studied. Growth form, surface traits, skeletal architecture, shape and size of the spicules are considered diagnostic morphotraits. Spicule dimensions are given as maximum, minimum, and medium lengths and widths of ca. 400 spicules.

The skeletal architecture was investigated by hand-cut sections of the ectosome and choanosome. To study the three-dimensional arrangements of fibres and spicules in the skeleton, fragments ca. 10 × 10 × 2 mm were cut, cleaned with 5% for 24 h in a warm temperature (35–40 °C), then washed and stirred five times in abundant double distilled water, washed and stirred twice in ethanol 95%, and finally allowed to air dry and gold-sputtered or mounted in Eukitt. The skeletal samples were than studied by and . Spicule preparations were made by dissolving a small fragment of the specimen in 65% boiling nitric acid (HNO3)and cleaned spicules were rinsed four times with water, once with 95% ethanol. The spicules were air-dried on slides, mounted in Eukitt, and observed by a Leitz Dialux 20 EB (LM), as well as on aluminium stubs and coated with gold for the observation with a Vega3 TESCAN type LMU (SEM).

sodium hypochlorite

light microscope

scanning electron microscope

Specimens were deposited at the Museo civico di Storia Naturale “Giacomo Doria” of Genoa, Italy (acronym MSNG). For the taxonomy of genus and species level the Systema (Hooper and Van Soest 2002) and the World Database (Van Soest et al. 2015) are considered as reference.

Systematic account

Phylum

Class

Order

Family

Genus

(junior synonym)

(junior synonym)

(junior synonym)

(nomen nudum)

(nomen nudum)

Diagnosis (emended from Van Soest 2002, p. 820). Massive-lobate, encrusting, tubular, branching or flabellate sponges, often of considerable size, with smooth to finely PageBreakconulose surfaces provided with small rounded and/or key-hole shaped apertures. Colour usually orange or brownish-orange. Consistency toughly compressible, firm. No ectosomal specialization. Choanosomal skeleton isotropic or anisotropic, occasionally irregular, network of primary ascending spongin fibres and secondaries. Main fibres mostly cored by megascleres. Main and interconnecting fibres echinated by megascleres in most cases. Spicules as verticillate styles, or styles and oxeas, or styles, oxeas and strongyles. Biogeographic pattern of 36 nominal species mostly matches tropical waters, a single species occurs in the Mediterranean. The genus has not been recorded from the eastern Pacific, West Africa, and the northern Atlantic European coasts.

Perino & Pronzato sp. n.

http://zoobank.org/7F8E3929-DD8D-4991-A8E0-C391C89AC1D0

Figs 1 , 2 , 3 , 4 , 5

Figure 1.

Genus . Biogeographic pattern (grey areas). The red dot indicates the type locality of the new species sp. n. at Jambiani (06°18'44.8"S, 39°33'32"E), eastern coast of Unguja Island, Zanzibar Archipelago, United Republic of Tanzania.

Figure 2.

sp. n. Type specimen (alcohol preserved, colour different from in vivo) from the Zanzibar Archipelago.

Figure 3.

sp. n. Spicular complement of verticillate acanthostyles, acanthoxeas and acanthostrongyles (SEM).

Figure 4.

sp. n. Spicular complement of verticillate acanthostyles, acanthoxeas and acanthostrongyles (LM).

Figure 5.

sp. n. a skeletal network of spongin fibres echinated by spicules (SEM) b detail of fibres surface echinated by verticillate spicules (SEM) c section of a primary fibre cored by a verticillate acanthostrongyle d–e skeletal network (LM).

Material examined.

Holotype: MSNG 57991 (A30), 70% ethanol, Jambiani (06°18'44.8"S, 39°33'32"E), eastern coast of Unguja Island, Zanzibar Archipelago, United Republic of Tanzania, SCUBA diving, 4.vii.2010, leg. Mr. Okala. Paratypes: MSNG 57992, MSNG 57993, MSNG 57994, MSNG 57995, MSNG 57996 (A12, A26, A27, A28, A29, respectively) ibid.

Diagnosis.

with unique spicular complement composed of three spicular categories, oxeas, styles and strongyles with spines arranged in a variable number of verticilles.

Etymology.

The speciphic epithet refers to the Zanzibar Archipelago.

Habitat.

Coral reef, quite common at 7–12 m of depth. Water temperature 28–31 °C. Salinity 20–36‰ (Fryday 2011). As reported by the Swiss Marine NGO manager of the local sponge farming facility (Jambiani Lagoon) the new species is massively farmed (Christian Vaterlaus, pers. comm., 2010).

Geographic distribution.

Western Indian Ocean, but only recorded from the type locality to date.

Description.

Growth form massive, thick, rounded, 6–10 cm in diameter. Colour in life purple to orange and light brown. Consistency firm and elastic. Surface rough to the touch, finely hispid, finely conulose for tips of ascending fibres supporting the dermal membrane, with regularly scattered circular and convoluted depressions (0.5 cm in diameter) very similar to those of . Oscules few, small, irregularly scattered. Choanosomal skeleton as an irregularly reticulate network of spongin fibres. Primary fibres 50–110 (71.67 ±17.63) μm in diameter, strongly echinate by single, scattered spicules to groups of diverging spicules; ascending primary fibres cored by spicules also present. Secondary fibres 20–50 (35 ± 9) μm in diameter notably echinate and cored by spicules. Tertiary network not observed.

Megascleres as three categories of monaxons mostly with acute spines. Acanthostyles 90–250 (180.72 ± 28.66) × 7.5–20 (13.46 ± 2.59) μm ornate by verticillate spines arranged as 11–27 (17.8 ± 2.86) whorls. Acanthoxeas 130–295 (195 ± 43.09) PageBreakPageBreak× 7.5–15 (12.17 ± 1.89) μm ornate by verticillate spines arranged as 14–26 (19.24 ± 3.47) whorls. Acanthostrongyles 80–245 (148.18 ± 36.82) × 4–17 (11.09 ± 4.24) μm ornate by verticillate spines arranged as 9–26 (15.76 ± 3.85) whorls. Annulate spicules apparently young.

Remarks.

The new species is characterized by the co-presence of three categories of spicules never recorded in other species. Acanthostrongyles are abundant, ca. 20–30 % of the total number of spicules.

Discussion

Geographic range of Indo-Pacific species

Madagascar, Mozambique Channel, Seychelles and Mascarene archipelagos (Western Indian Ocean province) harbour four species, whereas Japan (Ryukyu Archipelago) and New Caledonia enumerates two species each. Only one species each is recorded PageBreakfrom Philippines, Papua New Guinea, and Funafuti. Only one species each is harboured in the Red Sea/Gulf of Aden, Sri Lanka, Moluccas, Sunda Shelf/Java Sea (Indonesia), Hong Kong, Funafuti, and Australia (Fig. 1).

Diagnostic morphotraits comparative analysis of Indo-Pacific species

To discriminate between all 36 species by diverging diagnostic morphotraits is notably difficult, as highlighted in the previous section. Morphotraits of the genus are extremely conservative and different species appear very similar. Focusing on the Indo-Pacific species our attempt was not as completely successful as is also the case for the Atlantic species by Parra-Velandia et al. (2014).

Atlanto-Mediterranean species (18) seems to possess only acanthostrongyles, including the uncertain , , , and not redescribed by Parra-Velandia et al. (2014).

Among the 17 previously known Indo-Pacific species, the spicular complement of 14 species is composed of acanthostyles in a single or two-dimensional classes (see Appendix 1, Figs 6–21 for details).

Figure 6.

. a living specimen b skeleton fragment with two spicular types, axially embedded in a fibre and arming the surface c acanthostyles d acanthoxea (a modified from an original underwater shot by J. Hooper b–d modified from Hentschel 1911).

Figure 21.

. Spicular complement with two dimensional categories of acanthostyles; long acanthostyles spiny only at the tips (modified from Pulitzer-Finali 1996).

. Spicular complement of acanthostyles of two size categories (modified from Vacelet et al. 1976).

. a schematic drawings of two specimens b spicular complement of verticillate acanthostyles c skeleton architecture with echinate fibres, sponge surface on the right (modified from Thomas 1998).

. Drawing of the reticulate network with spongin fibres echinated by verticillate spicules perpendicularly arranged (modified from Carpenter 1856).

. The original illustration of verticillate acanthostyles ornate by spiny whorls by Thiele (1903).

. a very low quality image of the specimen studied by Dendy 1921 b schematic drawing of a branched specimen by Van Soest 1989 c skeleton architecture with echinate fibres d–e spicular complement of verticillate acanthostyles (c modified from Thomas 1981 d modified from Dendy 1921 e modified from Lévi 1961).

. a the sponge specimens of the type series b spicular complement of two spicular types, acanthostyles and acanthoxeas; small oxea-like spicules (bottom, right) are not reported in the original description (modified from Lévi 1993).

. a ramose slim dry specimen b–c spicular complement of verticillate acanthostyles of different dimensional categories (a–b modified from Lévi and Lévi 1983 c modified from Whitelegge 1897).

. a type series specimens (liquid preserved) b a living shallow water specimen c spongin skeleton with spicules d verticillate acanthostyles (modified from de Voogd et al. 2008).

. a–b spicular complement (a modified from Vacelet and Vasseur 1965 b modified from Lévi 1958).

. a drawing of a massive specimen b skeleton fragment c–g spicular complement b–d a modified from Van Soest 1989; b–d modified from Thomas 1979 c modified from Carter 1883 e modified from Vacelet and Vasseur 1965 f modified from Lévi 1964 g modified from Lévi 1961).

. a skeleton architecture b close up of spicules insertion in the spongin fibres c acanthostyles (modified from Hoshino 1985).

. a skeleton architecture b spicular complement (modified from Hoshino 1985).

. a type specimen b spicular complement with two spicular types (modified from Lévi and Lévi 1983).

. a type specimen (dry) b spicular complement of acanthostyles very stout, verticillate by blunt spines (modified from Pulitzer-Finali 1982).

The most common and studied Indo-Pacific species, i.e. , are characterized by a single spicular type acanthostyles, which are extremely variable in morphology, abundance of spines, and dimensional range (sometime more than three times in length) (see Table 1). The Atlantic and the Mediterranean show a similar size variability of acanthostyles. Only the Indo-Pacific , , and show two different categories of spicules, i.e. acanthostyles and acanthoxeas.

Table 1.

. Morphometries and morphotraits by different authors.

References	Acanthostyles μm	Whorls nº	Colour	Habitus size (cm)	Consistency
Carter 1883	132	15–18	-	-	-
Thiele 1903	200 × 14–15	16	-	-	-
Dendy 1905	176 × 16	–	dark brown	tubular 3.1 × 1.6 length × diameter	firm resilient
Laubenfels 1954	170–180 × 10–14	12–18	-	-	-
Lévi 1961	150–160 × 8–12	16–20	brown	massive 6–10 × 4	firm resilient soft
Lévi 1964	275 × 12–13	15–17	-	-	-
Lévi 1967	140–230 × 8–10	10–15	-	-	-
Vacelet and Vasseur 1965	135–250	13–20	-	-	-
Vacelet and Vasseur 1971	80–180 × 7.5–12.5	18–23	brown	encrusting 1.6–1.5 thickness	firm resilient coriaceus
Thomas 1979	112–212 × 6–8	6–8	pale yellow	encrusting cavernous	firm resilient compressible

The new species is characterized by the unique morphotrait of three categories of megascleres, i.e. acanthostyles, acanthoxeas, and acanthostrongyles with spines arranged in verticilles regularly scattered along the entire spicule. No other species exhibit this spicular combination. Acanthostrongyles, well identifiable and abundant, represent an exclusive diagnostic trait of the new species. The functional PageBreakrole of acanthostrongyles is doubled since echinanting spicules arm both the fibres surface and the core of the axial part of fibres.

Summarizing spicular complements and spicular morphotraits of 36 species: i) 32 species show only acanthostyles from Atlantic (17), Mediterranean (1), and the majority (14) of the Indo-Pacific areas; ii) three Indo-Pacific species show acanthostyles and acanthoxeas; iii) only one species sp. n. from the western Indian Ocean show a spicular component composed of acanthostyles, acanthoxeas, and acanthostrongyles.

Key to the Indo-Pacific species

The present key is an attempt to discriminate between the Indo-Pacific species, but the scenario appears very intricate mainly because morphotraits from many descriptions and illustrations are overlapping (see Table 1). A similar attempt, on the Atlantic species, was performed by Parra-Velandia et al. (2014) emphasizing that: “Caribbean taxonomy rests heavily on the external morphology”; as a consequence their key is essentially based on growth form and colour. Since this is the situation, our key is not simply dichotomous and allows the disctintion of only 13 of the 17 Indo-Pacific species (see Appendix 1). The remaining four species have acanthostyles with length ranges which are widely overlapping (from less than 150 to more than 250 μm). Three PageBreakof these (, , and ) are known only from the original descriptions; on the contrary, is reported by several authors but with discordant descriptions (Table 1).

1	Spicular complement composed by 1 or 2 spicular types (acanthoxeas, acanthostyles)	2
–	Spicular complement composed by 3 spicular types (acanthoxeas, acanthostyles, acanthostrongyles)	Agelas sansibarica sp. n.
2	Spicular complement composed by 2 spicular types (acanthoxeas and acanthostyles)	3
–	Spicular complement composed by 1 spicular type (acanthostyles)	4
3	Sponge body cup-shaped	Agelas axifera
–	Sponge body blade-shaped	Agelas novaecaledoniae
–	Sponge body lobed	Agelas mauritiana oxeata
–	Sponge body digitate	Agelas dendromorpha
–	Sponge body as slim cylindrical erected axis (branched or unbranched)	Agelas gracilis
4	Acanthostyles of 2-dimensional categories	5
–	Acanthostyles of 1-dimensional category	7
5	Long acanthostyles spiny only at the tips	Agelas semiglabra
–	Long and short acanthostyles almost entirely spiny	Agelas bispiculata
7	Primary and secondary fibres uncored	8
–	Primary and/or secondary fibres cored	9
8	Acanthostyles longer than 300 μm	Agelas ceylonica
–	Acanthostyles length no more than 200 μm	Agelas cavernosa
9	Primary and secondary fibres cored	Agelas nemoechinata
–	Primary fibres cored and secondary uncored	10
10	Acanthostyles (185–265 × 8–15 μm) with 15–23 whorls	Agelas nakamurai
–	Acanthostyles (130–220 × 4–21 μm) with 8–18 whorls	Agelas braekmani
–	Acanthostyles (80–370 × 5–24 μm) with 11–33 whorls	Agelas linnaei