Open Access

Spicular analysis of surficial sediments as a supplementary tool for studies of modern sponge communities

Helgoland Marine Research201670:5

DOI: 10.1186/s10152-016-0459-6

Received: 19 October 2015

Accepted: 16 January 2016

Published: 20 April 2016

Abstract

The method of spicular analysis that examines surficial sediments has been used to study the sponge spicule assemblage in the lagoon reef of Bocas del Toro, Panama. The method allowed to recognize some highly diagnostic spicule morphotypes that may belong to four sponge species as yet unnoticed in this area. The presence of these sponges must have been overlooked while studying faunistic compositions within an ecosystem due to their cryptic and/or excavating nature. Despite some limitations, the method of spicular analysis may be used as a supplementary tool for the studies of modern shallow-water sponge communities.

Keywords

Cryptic sponges Excavating sponges Triptolemma endolithicum Alectona wallichii Samus anonymus Cliona mucronata

Background

Sponges are sessile filter feeders that inhabit marine and fresh-water ecosystems all over the world. They are the main component of marine fauna and, next to corals, are one of the most important organisms inhabiting reefs and shallow-water habitats [16]. Sponges can also be the key components of deep-sea environments (e.g., [27, 54]). In the past, they usually received considerably less attention than other marine organisms. However, there has been an increase of interest in sponges over the last decades [16, 28, 66].

In spite of the fact that marine sponge fauna is now under intensive studies, in some, even well-studied regions, sponges are still poorly known. The most investigated areas with the best known sponge fauna include Mediterranean, Caribbean, and Australia (e.g., [63]). Still, there are new sponge species described from these sponge-rich regions every year (e.g., [18, 51, 64, 67, 68]), and it is presumed that there is still about twice as many species unknown to scientists [66]; particularly small, cryptic, or excavating species are difficult to observe and sometimes are overlooked. Thus, sponge inventory lists are incomplete.

The main characters used in sponge identification for ecological/general field studies include: shape, color, and consistency of a specimen (e.g., see [13]). However, it is especially the type and the arrangement of the internal mineral skeleton consisting of spicules that is crucial for sponge taxonomical assignment (e.g., see [29]).

Hexactinosan hexactinellid sponges may have a fused skeleton derived from secondary deposition of silica over spicules originally secreted loosely, while lithistid demosponges may have articulated spicules. Spicules can also appear free in the sponge body (as in the case of some hexactinellids) [35]. In the class Demospongiae, the spicules are frequently joined by spongin. The diversity of spicule morphotypes in demosponges is great as there are several hundred spicule morphotypes distinguished in this group (e.g., [8]).

Moreover, the spicule combination within a sponge skeleton is an important feature for sponge classification. Some sponges possess spicules of only one type, while others are characterized by a set of several morphotypes. The spicule set of each species is genetically controlled. However, under unfavorable conditions such as low silica levels in the seawater, not all morphotypes proper to the sponge are produced [39]. Some morphologies are widespread across the classification, while others are much more restricted in occurrence and thus play an important diagnostic role.

The spicular analysis method

Sponge spicules may be incorporated in the sediment in several ways. For example, they may become part of the sediment after the sponge’s death when the body disintegrates and the mineral spicules remain. They are then the only proof of the sponge’s former existence. Heavy storms usually cause detachment of sponge body parts, which may disintegrate and contribute isolated spicules to the sediment. They can also be torn off by various sponge-feeding animals [72]. Thus, under favorable preservation conditions, spicules may give information about the sponges that live or had lived recently in the studied area (see, for example, [6]).

The method of spicular analysis investigates isolated sponge spicules from the sediment and identifies them by comparing them with the spicules of living sponges. This method is usually used to reconstruct fossil and sub-fossil sponge communities. It has become popular in the middle of the twentieth century when it has been applied to reconstruct ancient marine sponge communities (e.g., [32, 33]). Later, it was used for reconstructing both fossil marine (e.g., [57, 30, 31, 37, 46]) and fresh-water sponge associations from all over the world [2426, 44, 45, 69, 70]. However, the spicular analysis technique can also be used to supplement studies of modern sponge communities by indicating the presence of some difficult-to-track sponge species.

Methods

The surficial sediment samples were collected in June 2011 and July 2014 by SCUBA surveys in patch reef environments of the Bocas del Toro archipelago, on the northwestern coast of Panama (Fig. 1). The studied area lies within the Almirante Bay and represents a diverse, well-developed patch reef with a well-studied coral–sponge community (e.g., [13, 15, 17, 19, 21, 22]). Two surface sediment samples, down to a depth of ~1 cm, were recovered in plain patches of shallow-water (~8 m) reef sand (9°21′38.6″N/82°16′40.9″W and 9°21′42.98″N/82°16′47.6″W).
Fig. 1

Map of the sampling area after Łukowiak et al. [36] (modified)

The obtained sediments were processed in the Bocas del Toro Research Station laboratory. The samples were subsequently dried and then treated with hydrogen peroxide (30 %) in order to remove small particles of organic matter. Additionally, a small amount of sediment was treated by acetic acid (60 %) to remove carbonates and thus concentrating siliceous spicules in order to make the rare spicule morphotypes easier to find. The sponge spicules were then transported to the Institute of Paleobiology, Polish Academy of Sciences, Poland, for the further analysis. The spicules were then handpicked from the residue under a binocular microscope NIKON SMZ1270. All representatives of morphological spicule types found in the sediment were mounted on SEM stubs and identified using the SEM. The photographed spicule morphotypes were compared to spicules that belong to sponges listed from the Bocas del Toro region (Table 1). The sponge list was compiled from published data, e.g., [10, 13, 15, 17, 19, 21, 22] and the STRI webpage database. Next, the studied spicules were compared with the spicules of sponges noted from the wider Caribbean area [e.g., [1, 23, 61, 62, 64, 73, 74]; World Porifera Database (WPD)]. For details of the terminology used in this paper, see the Thesaurus of Sponge Morphology [8] and Systema Porifera [29].
Table 1

Sponge list noted from Bocas del Toro, Panama

Order

Family

Species

Verongiida

Aplysinidae

Aiolocroia crassa (Hyatt, 1875)

  

Aplysina lacunosa (Lamarck, 1814)

  

Aplysina archeri (Higgin, 1875)

  

Aplysina fulva (Pallas, 1776)

  

Aplysina cauliformis (Carter, 1882)

  

Aplysina insulares Duchassaing & Michelotti, 1864

  

Aplysina fistularis (Pallas, 1766)

  

Verongula rigida Esper, 1794

  

Verongula reiswigi Alcolado, 1984

Dictyoceratida

Irciniidae

Ircinia sp.

  

Ircinia strobilina (Lamarck, 1816)

  

Ircinia felix (Duchassaing & Michelotti, 1864)

  

Ircinia campana (Lamarck, 1814)

  

Dysidea etheria de Laubenfels, 1936

 

Spongiidae

Spongia sp.

  

Spongia (Spongia) pertusa Hyatt, 1877

  

Spongia (Spongia) tubulifera Lamarck, 1814

  

Hyattella cavernosa (Pallas, 1766)

  

Hyattella intestinalis (Lamarck, 1814)

 

Thorectidae

Hyrtios sp.

  

Hyrtios proteus Duchassaing & Michelotti, 1864

Haplosclerida

Petrosiidae

Xestospongia sp.

  

Xestospongia muta (Schmidt, 1870)

  

Xestospongia bocatorensis Díaz, Thacker, Rützler & Piantoni, 2007

  

Neopetrosia rosariensis (Zea & Rützler, 1983)

  

Neopetrosia proxima (Duchassaing & Michelotti, 1864)

  

Neopetrosia subtriangularis (Duchassaing, 1850)

  

Neopetrosia carbonaria (Lamarck, 1814)

  

Petrosia sp.

  

Petrosia (Petrosia) pellasarca (de Laubenfels, 1934)

  

Petrosia weinbergi van Soest, 1980

 

Phloeodictyidae

Oceanapia peltata (Schmidt, 1870)

  

Oceanapia nodosa (George & Wilson, 1919)

  

Oceanapia oleracea (Schmidt, 1870)

  

Oceanapia bartschi (de Laubenfels, 1934)

  

Aka coralliphaga (Rützler, 1971)

  

Siphonodictyon brevitubulatum Pang, 1973

  

Calyx podatypa (de Laubenfels, 1934)

 

Chalinidae

Chalinula molitba (de Laubenfels, 1949)

  

Chalinula zeae de Weerdt, 2000

  

Haliclona sp.

  

Haliclona (Rhizoniera) curacaoensis (van Soest, 1980)

  

Haliclona (Reniera) implexiformis (Hechtel, 1965)

  

Haliclona (Reniera) manglaris Alcolado, 1984

  

Haliclona (Reniera) mucifibrosa de Weerdt et al., 1991

  

Haliclona (Reniera) tubifera (George & Wilson, 1919)

  

Haliclona (Haliclona) vansoesti de Weerdt, de Kluijver & Gomez, 1999 

  

Haliclona (Haliclona) hogarthi (Hechtel, 1965)

  

Haliclona (Halichoclona) albifragilis (Hechtel, 1965)

  

Haliclona (Soestella) twincayensis de Weerdt et al., 1991

  

Haliclona (S.) vermeuleni de Weerdt, 2000

  

Haliclona (S.) caerulea (Hechtel, 1965)

  

Haliclona (S.) piscaderaensis van Soest, 1980

  

Haliclona (Soestella) walentinae Díaz, Thacker, Rützler & Piantoni, 2007

  

Haliclona (Halichoclona) magnifica de Weerdt, Rützler & Smith, 1991 

  

Haliclona (Gellius) megasclera Lehnert & van Soest, 1996

  

Haliclona (Soestella) melana Muricy & Ribeiro, 1999

 

Niphatidae

Amphimedon compressa Duchassaing & Michelotti, 1864

  

Amphimedon virdis Duchassaing & Michelotti, 1864

  

Amphimedon erina (de Laubenfels, 1936)

  

Amphimedon complanata (Duchassaing, 1850)

  

Niphates sp.

  

Niphates caycedoi (Zea & van Soest, 1986) 

  

Niphates erecta Duchassaing & Michelotti, 1864

  

Niphates amorpha Wiedenmayer, 1977

  

Cribrochalina vascum (Lamarck, 1814) 

  

Niphates ramosa Gammill, 1997

 

Callyspongiidae

Callyspongia vaginalis (Duchassaing & Michelotti, 1864) 

  

Callyspongia armigera Duchassaing & Michelotti, 1864

  

Callyspongia fallax Duchassaing & Michelotti, 1864

  

Callyspongia pallida (Hechtel, 1965)

Suberitida

Suberitidae

Terpios sp.

  

Terpios manglaris Rützler & Smith, 1993

  

Prosuberites sp.

  

Prosuberites laughlini Díaz et al., 1987

  

Suberites aurantiacus (Duchassaing & Michelotti, 1864) 

Clionaida

Spirastrelliadae

Spirastrella sp.

  

Spirastrella coccinea Schmidt, 1868

  

Spirastrella hartmani Boury-Esnault, Klautau, Bézac, Wulff & Solé-Cava, 1999

  

Spirastrella cf. mollis Verill, 1907

  

Dipastrella megastelata Hechtel, 1965

 

Placospongiidae

Placospongia intermedia/melobdeoides Sollas, 1888

 

Clionaidae

Cliona sp.

  

Cliona delitrix Pang, 1973

  

Cliona varians (Duchassaing & Michelotti, 1864) 

  

Cliona caribbaea Carter, 1882

  

Cliona tenuis Carter, 1882

  

Cliona aprica Pang, 1973

  

Cliona mucronata Sollas, 1878

  

Spheciospongia vesparium (Lamarck, 1815)

  

Cervicornia cuspidifera (Lamarck, 1815)

Tethyida

Tethyidae

Tethya sp.1

  

Tethya sp.2

  

Tethya aff. seychellensis (Wright, 1881)

  

Tethya actinea de Laubenfels, 1950

  

Tectitethya crypta (de Laubenfels, 1949)

  

Tectitethya keyensis Sara & Bavestrello, 1996

Polymastida

Polymastiidae

Polymastia sp.

Poecilosclerida

Crambeidae

Monanchora arbuscula (Duchassaing & Michelotti, 1864)

  

Monanchora unguifera (Dendy, 1922)

 

Microcionidae

Clathria sp.

  

Clathria (Thalysias) venosa (Alcolado, 1984)

  

Clathria (Thalysias) microchela (Stephens, 1916)

  

Clathria (Thalysias) schoenus (de Laubenfels, 1936)

  

Clathria (Thalysias) echinata (Alcolado, 1984)

  

Clathria ferrea (de Laubenfels, 1936)

  

Clathria aspera Gammill, 1998

  

Artemisina melana van Soest, 1984

  

Holopsama helwigi (de Laubenfels, 1936)

  

Pandaros acanthifolium Duchassaing & Michelotti, 1864

 

Acarnidae

Acarnus nicoleae van Soest, Hooper & Hiemstra, 1991

  

Acarnus souriei (Lévi, 1952)

 

Mycalidae

Mycale sp.

  

Mycale (Paresperella) sp. nov.

  

Mycale (Mycale) laevis (Carter, 1882)

  

Mycale (Arenochalina) laxissima (Duchassaing & Michelotti, 1864)

  

Mycale (Carmia) microsigmatosa Arndt, 1927

  

Mycale magnidarapihidiphera van Soest, 1984

  

Mycale carmigropila Hajdu & Rützler, 1998

  

Mycale citrina Hajdu & Rützler, 1998

  

Mycale arndti van Soest, 1984

  

Mycale cf. americana van Soest, 1984

  

Mycale angulosa (Duchassaing & Michelotti, 1864)

  

Mycale (Mycale) arenaria Hajdu & Desqueyroux-Faúndez, 1994

  

Mycale cf. diversisigmata (van Soest, 1984)

 

Coelosphaeridae

Lyssodendoryx sp.

  

Lissodendoryx issodictyalis (Carter, 1882)

  

Lissodendoryx (Lissodendoryx) colombiensis Zea & van Soest, 1986

  

Forcepia (Forcepia) colonensis Carter, 1874

 

Tedaniidae

Tedania (Tedania) ignis (Duchassaing & Michelotti, 1864) 

  

Tedania klausi Wulff, 2006

 

Desmacididae

Desmapsamma anchorata (Carter, 1882)

 

Iotrochotidae

Iotrochota sp.

  

Iotrochota birotulata (Higgin, 1877)

Merliida

Merliidae

Merlia normani Kirkpatrick, 1908

Desmacellida

Desmacellidae

Biemna sp.

  

Biemna caribea Pulitzer-Finali, 1986

  

Biemna tubulata (Dendy, 1905)

  

Neofibularia nolitangere (Duchassaing & Michelotti, 1864)

Chondrillida

Chondrillidae

Chondrilla caribensis f. hermatypica Duran & Piantoni, 2007

  

Chondrilla caribensis f. caribensis Rützler, Duran & Piantoni, 2007

  

Chondrosia sp.

  

Chondrosia collectrix Schmidt, 1862

  

Chondrosia reniformis Nardo, 1847

 

Halisacridae

Halisacra sp.

  

Halisacra caerulea Vacelet & Donadey, 1987 

Axinellida

Raspaillidae

Ectyoplasia ferox (Duchassaing & Michelotti, 1864)

 

Axinelliade

Dragmacidon reticulatum (Ridley & Dendy, 1886)

  

Dragmacidon lunaecharta (Ridley & Dendy, 1886)

  

Ptilocaulis walpersi (Duchassaing & Michelotti, 1864)

  

Axinellidae sp.

  

Axinella corrugata (George & Wilson, 1919)

  

Dragmaxia cf. undata Alvarez, van Soest & Rützler, 1998

 

Heteroxyidae

Myrmekioderma sp.

  

Myrmekioderma rea (de Laubenfels, 1934)

  

Myrmekioderma gyroderma (Alcolado, 1984)

Suberitida

Halichondriidae

Halichondria sp.

  

Halichondria lutea Alcolado, 1984 

  

Halichondria magniconulosa Hechtel, 1965

  

Halichondria melanadocia (de Laubenfels, 1936)

  

Hymeniacidon caerulea Pulitzer-Finali, 1986

Bubarida

Desmanthidae

Petromica ciocalyptoides van Soest & Zea, 1986

 

Dictyonellidae

Svenzea zeai (Alvarez, van Soest & Rützler, 1998)

Scopalinida

Scopalinidae

Scopalina ruetzleri (Wiedenmayer, 1977)

Agelasida

Agelasidae

Agelas sp.

  

Agelas dispar (Duchassaing & Michelotti, 1864)

  

Agelas clathrodes (Schmidt, 1870)

  

Agelas conifera (Schmidt, 1870)

Tetractinellida

Theonellidae

Discodermia dissoluta Schmidt, 1870

 

Samidae

Cinachyra sp.

  

Samus anonymus Gray, 1867

 

Tetillidae

Cinachyrella alloclada (Uliczka, 1929)

  

Cinachyrella apion (Uliczka, 1929)

  

Cinachyrella kuekenthali (Uliczka, 1929)

 

Geodiidae

Geodia sp.

  

Geodia papyracea Hechtel, 1965

  

Geodia giberosa Lamarck, 1815

  

Erylus formosus Sollas, 1886

 

Ancorinidae

Stellettinopsis megastylifera (Wintermann-Kilian & Kilian, 1984)

  

Asteropus sp.

  

Penares sp.

  

Penares schulzei (Dendy, 1905)

  

Stelletta sp.1

  

Stelletta sp.2

  

Stelletta fibrosa Schmidt, 1862

  

Stryphnus raratriaenus Cárdenas, Menegola, Rapp & Díaz, 2009

 

Thoosidae

Alectona wallichii (Carter, 1874)

 

Thrombidae

Thrombus kittonii Carter, 1874

 

Pachastrellidae

Triptolemma endolithicum van Soest, 2009

Dendroceratida

Darwinellidae

Aplysilla gracilis (Merejkowsky, 1878)

  

Chellonaplysilla erecta (Row, 1911)

 

Dictyodendrillidae

Igernella notabilis (Duchassaing & Michelotti, 1864) 

  

Spongionella (Megalopastas) sp.

Homosclerophorida

Plakinidae

Plakortis angulospiculatus (Carter, 1879)

  

Plakortis halichondrioides (Wilson, 1902)

  

Plakortis simplex species complex Lehnert & van Soest, 1998

  

Plakinastrella onkodes Uliczka, 1929

  

Oscarella sp.

After Guzmán and Guevara [21, 22], Collin et al. [13], Díaz [15], Díaz et al. [17], Gochfeld et al. [19] and Cárdenas et al. [10]; http://biogeodb.stri.si.edu/bocas_database/search/class/1/?page=2; compiled; with sponge species described in this study in bold

The spicule assemblages are deposited in the Institute of Paleobiology, Polish Academy of Sciences, Warszawa, Poland, under ZPAL Pf.24 and ZPAL Pf.25.

Results

Among numerous spicules that are present in the sediment, some can be assigned to sponges already known from the investigated area (for the full list of sponges of Bocas del Toro, see Table 1), and some are noted from the study area for the first time. The spicule morphotypes belonging to species as yet unnoted from Bocas del Toro are described, and their taxonomical position is discussed below.

Amphitriaenes of Samus anonymus Gray, [20]

The spicules found in the surface sediments of the Bocas del Toro lagoon are short-shafted amphiprotriaenes with clads directed forward, away from the rhabd. The cladi are always divided three times. The amphitriaenes vary from slender with well-developed rhabd and thin cladi (Fig. 2c, e) to stout ones with short rhabd and cladi (Fig. 2d, f). The rhabds vary from 30 to 50 µm in length and 20–75 µm in thickness. The total length of the spicule may exceed 400 µm. They are identical with spicules of Samus anonymus.
Fig. 2

Samus anonymus Gray, [20] spicules; a, b amphitriaenes of S. anonymus; from van Soest and Hooper [65], cf sediment spicules

Remarks

Samus anonymus is characterized by small amphitriaenes (Fig. 2a, b) and sigmaspire microscleres. The megascleres may be short-shafted amphiprotriaenes with clads directed forward, away from the rhabd, or amphiplagiotriaenes with the forward-directed clads forming with the rhabd an angle of about 45° [8]. However, the cladi do not always divide three times and some are only divided dichotomously [65]. The rhabds vary from 20 to 80 µm in length and by up to 38 µm in thickness. The cladome may be up to 160 µm, and the total length of an amphitriaene including cladi may exceed 150 µm [65]. Samus anonymus occupies cavities of the porous concretion and the chambers previously excavated by boring sponges [6]. This tetractinellid was first considered to belong to Hadromerida [20, 56, 71] and Homosclerophorida [14]; its lithistid affinity was also considered [65]. Currently, it is regarded as the only species within family Samidae (suborder Spirophorina; [42]).

This cosmopolitan species inhabits shallow-water habitats of the Pacific and Atlantic Oceans, Brazil, Indian Ocean, Mediterranean, and Australia. It was also reported from Cuba, Colombia, Gulf of Mexico, and the Caribbean Sea ([51], WPD). So far, however, it was not reported in Bocas del Toro.

Mucronate tylostyles of Cliona mucronata Sollas, [52]

The spicules found in the surface sediments of Bocas del Toro are short, stout tylostyles with spherical heads and with a well-defined mucronate tip (Fig. 3c–f). The length of the spicules varies from 120–150 µm × 18–22 µm. The head is 16–19 μm × 17–21 μm. Even though the straight, thin tylostyles of Cliona mucronata are similar to tylostyles of some other clionaid spicules (e.g., Cliona ampliclavata, C. aprica, C. tenuis; for more details, see [74], the mucronate tylostyles do not resemble spicules of any other clionaid including species inhabiting this and adjacent areas (e.g., Cliona aprica, C. caribbea, C. delitrix, C. langae; compare also with [43, 74]).
Fig. 3

Cliona mucronata Sollas, [52] spicules; a C. mucronata subtylostyle; redrawn from Vacelet and Vasseur [58], b C. mucronata subtylostyle; redrawn from Calcinai et al. [9], cf sediment spicules

Remarks

Cliona mucronata is characterized by 2 kinds of tylostyles: straight, short, stout tylostyles with spherical heads (sometimes trilobed) and mucronate tips (Fig. 3a, b); and straight, thin tylostyles with oval or spherical heads and hastate tips. In addition to macroscleres, C. mucronata also possess spiraster microscleres that are sometimes transformed into branched amphiasters [9]. The mucronate tylostyles are of about 64–89 µm × 11.5–12.5 μm [9, 59] and with a head of 6.6–14 × 8–11.5 μm [59].

These clionaids (order Clionaida) are excavating, mostly cryptic sponges. They occupy small holes and chambers excavated in a solid calcareous base [49, 52]. They often live, overgrow, and bore in other sponges or corals (see [9]).

Cliona mucronata inhabits the Indian Ocean (including Indo-Pacific Ocean), Indonesia, Madagascar, and Australia (WPD; [9, 58]). This species is not listed for Bocas del Toro in any available source. The nearest locality to Bocas del Toro from which it was noted is the Mexican Tropical Pacific [2] but with some doubts (for more details see WPD).

Tuberculate diactines of Alectona wallichii [11]

The spicules found in the sediment of Bocas del Toro lagoon are very rare and are always broken. However, despite the fragmentation, the mushroom-shaped knobs that cover (most likely) the diactinal spicule forming the longitudinal rows of tubercles are well defined (Fig. 4c). The thickness of the spicule exceeds 50 µm in the thickest place and 30 µm in the thinnest place, and the knobs are about 12 µm in diameter. The tuberculate diactines of Alectona wallichii are very characteristic and do not resemble spicules of any other sponge, including thoosid species inhabiting this and adjacent areas (e.g., Alectona jamaicensis; [43]). In fact, the only other species of Alectona possessing morphologically similar acanthoxeas (but only those with spine-like tubercles, not the mushroom-like ones) is A. millari [12]. Alectona wallichii was synonymized by De Laubenfels [14] with Alectona millari [11]. However, Bavestrello et al. [3] demonstrated that these two species are distinct [48].
Fig. 4

Alectona wallichii [11] spicules; a mucronate diactine—fragment [57], b mucronate diactine; from Vacelet [57], c sediment spicule (fragment)

Remarks

The spicules of A. wallichii include robust tuberculate and smooth diactines (or derived polyactines) and microsclere amphiasters. The tuberculate diactines are acerate ([48]; Fig. 4a, b). These fusiform, slightly curved spicules are covered by rows ([11] describes twelve rows) of tubercles. The tubercles are alternately situated along the longitudinal lines placed along the spicule [11]. The tubercles may be of spine to mushroom shape [48]. The sizes of diactines vary from 22 to 805 µm × 16 to 125 µm (for more details, see Table 2 in [48, 57]).

Alectona wallichii is an excavating thoosid that occupies chambers of coral skeletons [48] and molluscan shells [55].

Alectona wallichii is recorded from North Atlantic Ocean, Indian Ocean [55], Japan Sea, South Africa (Tulėar; WPD; [11], and Hawaii [57]).

Short-shafted mesotriaenes of Triptolemma endolithicum van Soest, [64]

The spicules described here extracted from the bottom sediments of the studied area are various types of mesodichotriaenes. Some of them possess short to moderately long, conically ended rhabds (Fig. 5c–e, g, h), and some others have blunt rhabds (Fig. 5f). The cladomes may be branched only on the very end of the cladi, or the cladi may divide very near the rhabd. The clads are irregularly trifurcated or tetrafurcated (Fig. 5d–g), with desmoid appearance in several different planes. The length of the rhabd varies from 40 to 65 μm. The cladomes are up to 300 μm. The protoclads are 30–180 µm, deuteroclads are 25–100 µm long, trichoclads are 20–55 µm long, and tetraclads are up to 10 µm long. The mesodichotriaene megascleres of T. endholithicum resemble those of T. cladosum [53], but T. cladosum is known only in Indonesia [53].
Fig. 5

Triptolemma endolithicum van Soest, [64] spicules; a, b triaene and mesodichotriaenes of T. endolithicum; from van Soest [64], ch sediment spicules

Remarks

The skeleton of Triptolemma consists of short-shafted mesotriaenes (predominantly mesodichotriaenes) (Fig. 5a, b), frequently complemented by monaxonic megascleres (oxeas or strongyles), amphiasters, metasters transitional to spirasters, and spiny microrhabds which may be partially absent [4]. The mesotriaenes have symmetrical, short conical rhabdomes that can be blunt [38] or sharp pointed [64]. The clads may be irregularly trifurcated or tetrafurcated, with desmoid appearance. The cladome branches out in several different planes. Also the level of division varies within a spicule with dichotomous and tetrafurcated clads co-occurring [38]. Mesotriaenes with diversely branched clads may differ according to size within one specimen [64]. The rhabdomes are 62–21 × 20–25 μm each. The cladomes are up to 400 μm [64] and include protoclads 21–302 × 12–48 μm, deuteroclads 12–72 × 6–20 μm, trichoclads 6–60 × 5–7 μm, and tetraclads up to 27.6 µm long.

Sponges of the genus Triptolemma are cryptic and penetrate other sponges or coral tissue [38], or crevices of the coralligenous concretions [4]. Triptolemma endolithicum is an encrusting species, growing on and in corals. It is usually not visible on the outer surface of the coral, but there are some cavities and corridors filled with Triptolemma in the coral inner part [64].

Triptolemma endolithicum was so far noted only in the Southern Caribbean (i.e., Colombia) by van Soest [64].

Discussion

The surficial sediment deposited in the areas inhabited by sponges is usually loaded with their spicules. Usually, when the sponge skeleton becomes incorporated into the sediment, it disintegrates rapidly to isolated spicules. However, under favorable conditions, the spicules may stay connected together with the collagenous fibrils forming small skeletal clusters. Nevertheless, the latter situation is rather rare and after some time, due to early diagenesis and bioturbation, the spicules become separated, broken, and sometimes selectively segregated (for more details see [36, 50]).

The spicules may be delivered to the bottom sediments in various ways. Some could have belonged to sponge specimens that were mechanically damaged (e.g., during the storms) but not killed. The pieces of the torn sponge tissue settle on the sea bottom and then become incorporated to the sediment either as clusters of sponge spicules or as loose spicules. Also, sponge-eating carnivores, such as some opisthobranches, sea stars, fishes, and turtles, can deliver sponge spicules to the sediment. As the predators consume only small parts rather than whole individuals [72], the sponges may remain alive as well, and only their fragments are detached. In both cases mentioned above, the sponge species might still be present in this area.

By contrast, when a sponge dies, its spicule complement becomes incorporated to the sediment. The spicules are thus the proof of the former presence of the sponge individual and do not necessarily indicate that the species occurs in that area.

It was already suggested that some spicule morphotypes have a greater chance of being preserved in the sediment than others (see [50]), e.g., those of spherical morphology (e.g., spherasters and selenasters) are quite resistant to mechanical destruction. Thus, they might be a dominant component of sponge spicule assemblages (for more details, see [36, 50]) only for taphonomic reasons.

The additional factor is spicule transport. The sediment containing spicules might be carried from other, more or less distant areas e.g., by currents or hurricanes [40].

Finally, the activity of bioturbating organisms has to be considered. Organisms responsible for bioturbation are mostly oligochaetes, polychaetes, bivalves, echinoids, and holothurians [34, 41]. The disturbance and homogenization of the deposits can reach down to about 3–4 cm [34], but in extreme cases, it can exceed even 20–40 cm [47, 60]. Such activity causes reworking and mixing of the sediment that could have been deposited during the last few weeks to tens of years (depending on sedimentation rate).

One has to be aware that spicules in the sediment are a mixture possibly resulting from these processes. Thus, finding spicules that belong to certain sponge species in the surficial sediment is a proof of one or more of the three following processes: (1) the presence of living individuals bearing this type of spicule in this, or nearby areas, (2) the former presence of the sponge bearing this spicule type, or (3) the transport of this spicule morphotype from other (more or less distant) areas.

In the case of the studied sponge spicules, the transport seems not to have played a significant role as most of the species recognized on the basis of the spicules are characteristic for this environment being shallow-water inhabitants. Moreover, this area is not influenced by hurricanes (Aaron O’Dea personal communication). The transport from deeper water is less likely, too. Moreover, some of these spicule morphotypes were quite numerous in the studied sediment (amphitriaenes) which also suggests the autochthonous character of the studied spicule assemblage. Their absence from the sponge list from this area is caused probably by the fact that all of them are cryptic or excavating. It is thus highly plausible that they represent species that still live in the investigated area, but were just overlooked.

Conclusions

The spicular analysis method may be used as an additional tool for tracing sponge species in marine and fresh-water environments all over the world.

Nevertheless, usage of this method is burdened by some limitations:
  1. 1.

    The method only suggests, does not prove, the presence of species in the studied area (conventional taxonomic studies are necessary to confirm the presence of the species).

     
  2. 2.

    It is suitable only for tracking sponges with very characteristic, highly diagnostic spicule types.

     
  3. 3.

    It is best applied in areas with no significant sediment transport and mixing.

     

In Bocas del Toro lagoon, the method of spicular analysis has suggested the presence of four cryptic and/or excavating sponge species unknown in this area before. Those were Samus anonymus, Alectona wallichii, Triptolemma endolithicum, and Cliona mucronata.

Declarations

Acknowledgements

This study was financed by a research Grant from the National Science Centre (NCN) Poland No. 2013/09/D/ST10/04050. The studies made in 2011 were supported by Short Term Fellowship from the Smithsonian Tropical Research Institute and PalSIRP Sepkoski Grant. This paper was also possible thanks to support of the Institute of Paleobiology, Polish Academy of Sciences. I would like to thank all the people who helped me with collecting and processing the material: M. Hynes (STRI Research Intern), B. de Gracia (STRI), and A. O’Dea (STRI). D. Madzia (Institute of Paleobiology), M. Hynes (STRI Research Intern), and A. Jagtap (Northeastern University) are thanked for linguistic improvements of the manuscript. I would like to thank G. Jacome, P. Gondola, F. Rodriguez, and all the team at the Bocas Research Station for their support. Special thanks are to J. Vacelet (Aix-Marseille Université) for providing me photographs of A. wallichii and A. Pisera (Institute of Paleobiology) for critical reading of the manuscript and discussion. I am also indebted to the reviewers which suggestions helped to considerably improve this manuscript.

Competing interests

The authors declare that they have no competing interests.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Institute of Paleobiology PAN

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