INTRODUCTION
Mangroves are salt-tolerant trees that build complex coastal habitats, restricted to subtropical and tropical areas. These habitats are defined by the presence of marine organisms able to cope with fluctuating salinity, low oxygen concentration, presence of natural sulphide, high temperatures and periodic exposure to air (Puce et al., Reference Puce, Arillo, Cerrano, Romagnoli, Bavestrello, Futin, Westfall, Cartwright, Daly and Wyttenbach2004). They show extraordinary high rates of productivity, providing through the mangrove litter the basis of a complex food web; moreover they play a paramount economical and social role for the local communities (Tomascik et al., Reference Tomascik, Mah, Nontji and Moosa1997), significantly reduce coastal erosion and provide protection from tropical cyclones and tidal waves (UNESCO, 1979; Danielsen et al., Reference Danielsen, Sørensen, Olwig, Selvam, Parish, Burgess, Hiraishi, Karunagaran, Rasmussen, Hansen, Quarto and Suryadiputra2005). Moreover, their key role as one of the most important sink areas for CO2 has recently been highlighted (Donato et al., Reference Donato, Kauffman, Murdiyarso, Kurnianto, Stidham and Kanninen2011). Unfortunately, mangroves are among the most imperilled marine ecosystems since they are subjected to extreme anthropogenic pressures, such as organic run-off from land, disturbances from suspended sediment and damage from clear-cutting (Alongi, Reference Alongi2002).
The mangrove forests of South-east Asia are among the most species-rich, since the Indo-Malayan region is considered a hotspot of biodiversity (Chapman, Reference Chapman1977). In particular in Indonesia, mangroves are dispersed throughout the Archipelago (Tomascik et al., Reference Tomascik, Mah, Nontji and Moosa1997). Mangroves create habitats for numerous species; the stilt roots and pneumatophores play the role of hard substrata in an otherwise soft sediment environment (Ellison & Farnsworth, Reference Ellison and Farnsworth1992).
Most of the knowledge about mangrove ecosystems derives from studies about ecology, distribution and taxonomy in the Caribbean (Díaz & Rützler, Reference Díaz and Rützler2009; Guerra-Castro et al., Reference Guerra-Castro, Young, Pérez-Vázquez, Carteron and Alvizu2011; Díaz, Reference Díaz2012). The Caribbean mangroves sponge communities are distinct from those in reefs, and contain species that appear to be specifically adapted to survive extremes in salinity, temperature and sedimentation (Rützler, Reference Rützler1995; Wulff, Reference Wulff2000, Reference Wulff2005; Engel & Pawlik, Reference Engel and Pawlik2005; Pawlik et al., Reference Pawlik, McMurray and Henkel2007; Nagelkerken et al., Reference Nagelkerken, Blaber, Bouillon, Green, Haywood, Kirton, Meynecke, Pawlik, Penrose, Sasekumar and Somerfield2008).
Competition for space in the mangroves is considered intense and hard substrate required by sponges is limited; as a consequence, species with high growth rates and good competence for spatial competition are considered favoured (Engel & Pawlik, Reference Engel and Pawlik2005; Wulff, Reference Wulff2005, Reference Wulff2010; Nagelkerken et al., Reference Nagelkerken, Blaber, Bouillon, Green, Haywood, Kirton, Meynecke, Pawlik, Penrose, Sasekumar and Somerfield2008).
Taxonomic knowledge on sponges associated with mangroves, from the Indo-Pacific and, in particular, from the Indonesian Archipelago is very poor, and new data have only very recently become available from that area (Calcinai et al., Reference Calcinai, Bastari, Curin, Bavestrello, Theodorus, Lalamentik, Segre-Reinach and Cerrano2012; Becking et al., Reference Becking, Cleary and de Voogd2013).
This paper aims to provide initial data on sponge composition in two small mangrove forests at Bangka Island (North Sulawesi, Indonesia) and to describe a new species associated with the mangrove habitat.
MATERIALS AND METHODS
The studied material comes from two different mangrove forests located at the western coast of Bangka Island (North Sulawesi, Indonesia) (Figure 1). The first sampling station (ST1) is an artificial, narrow channel about 500 m long, cutting a Rhizophora sp. forest (from 1.758256°N125.136779°E to 1.755319°N 125.133107°E). Rhizophora is the dominant mangrove, while Sonneratia alba and Bruguiera spp. are rarely present.
Fig. 1. Indonesian archipelago with Bangka Island. The arrows point to the two sampled stations.
The second station (ST2) (from 1.815533°N 125.120133°E to 1.817000°N 125.120500°E) is a wide inlet, about 120 m long, characterized by Rhizophora and Bruguiera trees. These two forests are about 6.5 km apart and in the area the maximum tide excursion can be higher than 3 m, playing a key role in the mixing of seawater.
Specimens were collected by snorkelling during high tide period by visually oriented transect, on September 2011. The collection was intended to be qualitative and all the specimens detected were collected from the inner to the outer side of the mangrove forest.
The spicule complement was studied according to Rützler (Reference Rützler, Stoddart and Johannes1978). From 30 measurements for each spicule type, size range, mean and standard deviation (in parentheses) were calculated. Dissociated spicules were transferred onto stubs and sputtered with gold for SEM analyses and observed with a scanning electron microscope (Philips XL 20).
RESULTS
SYSTEMATICS
Order TETRACTINELLIDA Marshall, 1876
Family ANCORINIDAE Schmidt, 1870
Dercitus (Stoeba) bangkae sp. nov.
(Figure 2)
Fig. 2. Dercitus bangkae sp. nov.: (A) the holotype covering coral pieces; (B) Skeleton made of a crust of calthrops with dispersed microscleres; (C, N) regular calthrops; (D, E) irregular dichocalthrops; (F) regular dichocalthrop; (G, H) modified calthrops; (I, M, N) amphiaster-like sanidasters; (J–L) modified sanidasters.
TYPE MATERIAL
Holotype: Indonesia, North Sulawesi, Bangka Island (1.756333°N 125.134666°E), water depth: 1 m, MSNG-58345, specimen MA16, 9 November 2011.
DIAGNOSIS
Encrusting Dercitus (Stoeba) with calthrops, dichocalthrops and sanidasters. Irregular dichocalthrops with bifid, bent or rounded extremities. Regular dichocalthrops are very rare. Sanidasters are very variable in shape from amphiaster-like to irregular forms with spines at the extremities.
DESCRIPTION
Encrusting sponge, 0.5–1 mm in thickness. The holotype covers and consolidates a coral piece about 8 cm long and two other small portions of coral (Figure 2A). Two other sponges were found in the same coral substrate (Table 1). The colour in the preserved state is light brownish; the surface is microhispid and full of sediment. Oscules are not visible.
Table 1. Species recorded in the two sampled stations with habitat, depth and distribution.
Skeleton: A crust of calthrops with dispersed microscleres (Figure 2B).
Spicules: The spicule complement consists of calthrops, dichocalthrops and sanidasters. Calthrops regular in shape, but variable in size, with cladi 20–162.8 (±62.7) – 270 µm × 7.5–21.2 (±8.4) – 35 µm and cladomes 105–257 (±93.3) – 420 µm (Figure 2C, N); other calthrops have cladi terminally bent, rounded and often of different length (Figure 2G, H). Numerous irregular dichocalthrops with one, two or all the bifid cladi (Figure 2D–F). Dichocalthrops often have deuterocladi variable in length of 30–77.2 (±23.0) – 115 µm, protocladi 95–132.5 (±19.1) – 155 µm and rhabdomes 140 × 2 µm (only three spicules measured). Regular calthrops and modified dichocalthrops are the dominating spicules (64% and 35% respectively) with regular dichocalthrops occurring only for 1%.
Sanidasters are very variable in shape, but constant in size (7.5 – 14.0 (±3.4) – 17.5 µm); they may be amphiaster-like with groups of spines concentrated in two central clusters and with spined extremities (Figure 2I, M, N) and sanidasters with groups of spines concentrated at one extremity and in the centre of the spicule (Figure 2J–L). These sanidasters have often only one pointed, curved tip, covered with spines (Figure 2K). Numerous intermediated forms occur with a single, or both rounded tips (Figure 2L–N); microspines may occur along the axis (Figure 2M).
ETYMOLOGY
Named for its type locality, Bangka Island.
DISTRIBUTION
Known only from the type locality.
REMARKS
This species, characterized by calthrops and dichocalthrops as megascleres and by sanidasters clearly belongs to the genus Dercitus subgenus Stoeba (van Soest et al., Reference van Soest, Beglinger and De Voogd2010).
Dercitus (S.) bangkae sp. nov. is characterized by megascleres with numerous modifications and by sanidasters very variable in shape. In particular, the sanidasters with only one pointed tip are peculiar of this species and are not present in any other species of this genus.
There are five species of this subgenus described from the Indo-Pacific area (van Soest et al., Reference van Soest, Boury-Esnault, Hooper, Rützler, de Voogd, Alvarez de Glasby, Hajdu, Pisera, Manconi, Schönberg, Janussen, Tabachnick, Klautau, Picton, Kelly, Vacelet, Dohrmann, Díaz and Cárdenas2015). None of them fits with D. (S.) bangkae sp. nov. here described especially for the spicule shape.
Dercitus (S.) extensus (Dendy, Reference Dendy and Herdman1905) has very thin, oxea-like sanidasters; D. (S.) fijiensis van Soest et al. (Reference van Soest, Beglinger and De Voogd2010) has spicules different in shape: pointed sanidasters and deutherochlads have very short protocladi (19–26.5–30 × 13–25.2–42 µm). D. (S.) occultus Hentschel, 1909 is an endolithic species characterized only by dichocalthrops as megascleres; D. (S.) pauper Sollas, Reference Sollas1902 is pink in colour, has thin sanidasters (1 µm in thickness) and small megascleres (calthrops cladi 60–70 µm, van Soest et al., Reference van Soest, Beglinger and De Voogd2010). D. (S.) simplex (Carter, 1880) has only dichocalthrops and sanidasters are rod-like without modification.
The survey has shown the presence of 19 species belonging to 11 families and 15 genera (Table 1). All the samples were collected on mangrove trunks or roots, or in the surrounding substratum (e.g. Dercitus (Stoeba) bangkae sp. nov. on coral fragments). The majority of collected species is typical of coral reef (e.g. Biemna fortis, Amorphinospis excavans). Only two species, Spongia (Spongia) cf. matamata and Hyrtios communis have been found in lagoon or in mangrove habitat respectively (de Laubenfelds, Reference de Laubenfels1954). Also Becking et al. (Reference Becking, Cleary and de Voogd2013) reported sponges living both on coral reef and inside mangrove habitat in Berau (Indonesia).
DISCUSSION
The present survey highlights strong differences between the sponge fauna of the studied mangroves and that of the mangroves of the Caribbean area. Considering the high heterogeneity and biodiversity of the Indonesian Archipelago and the wide distribution of mangroves, it is evidently important to develop a general assessment of the sponge fauna associated with Indonesian mangroves. At the moment, even if at a very small spatial scale, it is clear that the two sampled mangrove forests have different species assemblages. In ST2, only four species were collected (Table 1), while 17 species were collected from ST1 (Table 1). Out of a total of 19 species only two species (Cladocroce burapha and Amorphinopsis excavans) were found in both of the mangrove forests, while two species were exclusively present in ST2 (Topsentia halichondrioides and Tedania (Tedania) brevispiculata) and 15 exclusively in ST1 (Table 1).
While in the Caribbean, mangrove sponges often are large in size, with massive growth forms, and brilliant colours (Rützler & Feller, Reference Rützler and Feller1996; Díaz et al., Reference Díaz, Smith and Rützler2004) in Bangka Island mangrove sponges are all of small dimensions (up to 12 × 10 cm) and dull coloured. Also Barnes & Bell (Reference Barnes and Bell2002), from the West Indian Ocean, found that almost the majority of sponges were encrusting, and Becking et al. (Reference Becking, Cleary and de Voogd2013) showed that mangrove habitat in Berau is characterized by small sponges.
In Caribbean mangroves, Chalinidae is generally the most diversified family (de Weerdt, Reference de Weerdt2000; Díaz et al., Reference Díaz, Smith and Rützler2004; Wulff, Reference Wulff2004; Guerra-Castro et al., Reference Guerra-Castro, Young, Pérez-Vázquez, Carteron and Alvizu2011; Díaz, Reference Díaz2012). Tedania (Tedania) ignis, Lissodendoryx (Lissodendoryx) isodictyalis, Geodia gibberosa, Halichondria (Halichondria) melanadocia, Haliclona (Reniera) manglaris, Dysidea etheria, Hyrtios proteus, Mycale (Carmia) microsigmatosa and Spongia (Spongia) tubulifera are considered the most common sponge species of Caribbean mangrove (Sutherland, Reference Sutherland1980; Díaz et al., Reference Díaz, Smith and Rützler2004; Engel & Pawlik, Reference Engel and Pawlik2005). In a survey of the Quirimba Archipelago of Mozambique a few species belonging to the family Chalinidae and Biemnidae (genera Haliclona sp. and Biemna sp.) were recorded (Nagelkerken et al., Reference Nagelkerken, Blaber, Bouillon, Green, Haywood, Kirton, Meynecke, Pawlik, Penrose, Sasekumar and Somerfield2008). In Berau (Indonesia) mangroves, species of the families Chalinidae, Halichondriidae, Tethyidae are reported as the most common (Becking et al., Reference Becking, Cleary and de Voogd2013). This aspect is here confirmed, since species of the family Chalinidae and Halichondriidae were the most common. Species belonging to genera Haliclona (four out of 19) together with the genera Tedania and Biemna have been recorded in Bangka mangroves. The species Cladocroce burapha and Biemna fortis were found both in Berau and Bangka regions.
Considering the key role mangrove habitats play in the functioning of tropical ecosystems, and the pivotal role of sponges in reef dynamics (Wulff, Reference Wulff2006) and as a refuge for several species (Cerrano et al., Reference Cerrano, Calcinai, Pinca, Bavestrello, Suzuki, Nakamori, Hidaka and Kayanne2006), it is important to fill the lack of knowledge on the Porifera adapted to survive in these unique and endangered habitats.
ACKNOWLEDGEMENTS
This research has been granted by the Polytechnic University of Marche in the framework of a scientific collaboration with the University of Sam Ratulangi (Manado). Authors are indebted with the staff of the research outpost Coral Eye (http://coraleye.net/contact-us.html) for logistic support.
