Spicular analysis of surficial sediments as a supplementary tool for studies of modern sponge communities
© Łukowiak 2016
Received: 19 October 2015
Accepted: 16 January 2016
Published: 20 April 2016
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.
KeywordsCryptic sponges Excavating sponges Triptolemma endolithicum Alectona wallichii Samus anonymus Cliona mucronata
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 . 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., ). 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 ; 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 ). 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 ).
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) . 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., ).
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 . 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 . 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, ).
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., [5–7, 30, 31, 37, 46]) and fresh-water sponge associations from all over the world [24–26, 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.
Sponge list noted from Bocas del Toro, Panama
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
Ircinia strobilina (Lamarck, 1816)
Ircinia felix (Duchassaing & Michelotti, 1864)
Ircinia campana (Lamarck, 1814)
Dysidea etheria de Laubenfels, 1936
Spongia (Spongia) pertusa Hyatt, 1877
Spongia (Spongia) tubulifera Lamarck, 1814
Hyattella cavernosa (Pallas, 1766)
Hyattella intestinalis (Lamarck, 1814)
Hyrtios proteus Duchassaing & Michelotti, 1864
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 (Petrosia) pellasarca (de Laubenfels, 1934)
Petrosia weinbergi van Soest, 1980
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)
Chalinula molitba (de Laubenfels, 1949)
Chalinula zeae de Weerdt, 2000
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
Amphimedon compressa Duchassaing & Michelotti, 1864
Amphimedon virdis Duchassaing & Michelotti, 1864
Amphimedon erina (de Laubenfels, 1936)
Amphimedon complanata (Duchassaing, 1850)
Niphates caycedoi (Zea & van Soest, 1986)
Niphates erecta Duchassaing & Michelotti, 1864
Niphates amorpha Wiedenmayer, 1977
Cribrochalina vascum (Lamarck, 1814)
Niphates ramosa Gammill, 1997
Callyspongia vaginalis (Duchassaing & Michelotti, 1864)
Callyspongia armigera Duchassaing & Michelotti, 1864
Callyspongia fallax Duchassaing & Michelotti, 1864
Callyspongia pallida (Hechtel, 1965)
Terpios manglaris Rützler & Smith, 1993
Prosuberites laughlini Díaz et al., 1987
Suberites aurantiacus (Duchassaing & Michelotti, 1864)
Spirastrella coccinea Schmidt, 1868
Spirastrella hartmani Boury-Esnault, Klautau, Bézac, Wulff & Solé-Cava, 1999
Spirastrella cf. mollis Verill, 1907
Dipastrella megastelata Hechtel, 1965
Placospongia intermedia/melobdeoides Sollas, 1888
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)
Tethya aff. seychellensis (Wright, 1881)
Tethya actinea de Laubenfels, 1950
Tectitethya crypta (de Laubenfels, 1949)
Tectitethya keyensis Sara & Bavestrello, 1996
Monanchora arbuscula (Duchassaing & Michelotti, 1864)
Monanchora unguifera (Dendy, 1922)
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
Acarnus nicoleae van Soest, Hooper & Hiemstra, 1991
Acarnus souriei (Lévi, 1952)
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)
Lissodendoryx issodictyalis (Carter, 1882)
Lissodendoryx (Lissodendoryx) colombiensis Zea & van Soest, 1986
Forcepia (Forcepia) colonensis Carter, 1874
Tedania (Tedania) ignis (Duchassaing & Michelotti, 1864)
Tedania klausi Wulff, 2006
Desmapsamma anchorata (Carter, 1882)
Iotrochota birotulata (Higgin, 1877)
Merlia normani Kirkpatrick, 1908
Biemna caribea Pulitzer-Finali, 1986
Biemna tubulata (Dendy, 1905)
Neofibularia nolitangere (Duchassaing & Michelotti, 1864)
Chondrilla caribensis f. hermatypica Duran & Piantoni, 2007
Chondrilla caribensis f. caribensis Rützler, Duran & Piantoni, 2007
Chondrosia collectrix Schmidt, 1862
Chondrosia reniformis Nardo, 1847
Halisacra caerulea Vacelet & Donadey, 1987
Ectyoplasia ferox (Duchassaing & Michelotti, 1864)
Dragmacidon reticulatum (Ridley & Dendy, 1886)
Dragmacidon lunaecharta (Ridley & Dendy, 1886)
Ptilocaulis walpersi (Duchassaing & Michelotti, 1864)
Axinella corrugata (George & Wilson, 1919)
Dragmaxia cf. undata Alvarez, van Soest & Rützler, 1998
Myrmekioderma rea (de Laubenfels, 1934)
Myrmekioderma gyroderma (Alcolado, 1984)
Halichondria lutea Alcolado, 1984
Halichondria magniconulosa Hechtel, 1965
Halichondria melanadocia (de Laubenfels, 1936)
Hymeniacidon caerulea Pulitzer-Finali, 1986
Petromica ciocalyptoides van Soest & Zea, 1986
Svenzea zeai (Alvarez, van Soest & Rützler, 1998)
Scopalina ruetzleri (Wiedenmayer, 1977)
Agelas dispar (Duchassaing & Michelotti, 1864)
Agelas clathrodes (Schmidt, 1870)
Agelas conifera (Schmidt, 1870)
Discodermia dissoluta Schmidt, 1870
Samus anonymus Gray, 1867
Cinachyrella alloclada (Uliczka, 1929)
Cinachyrella apion (Uliczka, 1929)
Cinachyrella kuekenthali (Uliczka, 1929)
Geodia papyracea Hechtel, 1965
Geodia giberosa Lamarck, 1815
Erylus formosus Sollas, 1886
Stellettinopsis megastylifera (Wintermann-Kilian & Kilian, 1984)
Penares schulzei (Dendy, 1905)
Stelletta fibrosa Schmidt, 1862
Stryphnus raratriaenus Cárdenas, Menegola, Rapp & Díaz, 2009
Alectona wallichii (Carter, 1874)
Thrombus kittonii Carter, 1874
Triptolemma endolithicum van Soest, 2009
Aplysilla gracilis (Merejkowsky, 1878)
Chellonaplysilla erecta (Row, 1911)
Igernella notabilis (Duchassaing & Michelotti, 1864)
Spongionella (Megalopastas) sp.
Plakortis angulospiculatus (Carter, 1879)
Plakortis halichondrioides (Wilson, 1902)
Plakortis simplex species complex Lehnert & van Soest, 1998
Plakinastrella onkodes Uliczka, 1929
The spicule assemblages are deposited in the Institute of Paleobiology, Polish Academy of Sciences, Warszawa, Poland, under ZPAL Pf.24 and ZPAL Pf.25.
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, 
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° . However, the cladi do not always divide three times and some are only divided dichotomously . 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 . Samus anonymus occupies cavities of the porous concretion and the chambers previously excavated by boring sponges . This tetractinellid was first considered to belong to Hadromerida [20, 56, 71] and Homosclerophorida ; its lithistid affinity was also considered . Currently, it is regarded as the only species within family Samidae (suborder Spirophorina; ).
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 (, WPD). So far, however, it was not reported in Bocas del Toro.
Mucronate tylostyles of Cliona mucronata Sollas, 
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 . 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 .
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 ).
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  but with some doubts (for more details see WPD).
Tuberculate diactines of Alectona wallichii 
The spicules of A. wallichii include robust tuberculate and smooth diactines (or derived polyactines) and microsclere amphiasters. The tuberculate diactines are acerate (; Fig. 4a, b). These fusiform, slightly curved spicules are covered by rows ( describes twelve rows) of tubercles. The tubercles are alternately situated along the longitudinal lines placed along the spicule . The tubercles may be of spine to mushroom shape . The sizes of diactines vary from 22 to 805 µm × 16 to 125 µm (for more details, see Table 2 in [48, 57]).
Short-shafted mesotriaenes of Triptolemma endolithicum van Soest, 
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 . The mesotriaenes have symmetrical, short conical rhabdomes that can be blunt  or sharp pointed . 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 . Mesotriaenes with diversely branched clads may differ according to size within one specimen . The rhabdomes are 62–21 × 20–25 μm each. The cladomes are up to 400 μm  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 , or crevices of the coralligenous concretions . 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 .
Triptolemma endolithicum was so far noted only in the Southern Caribbean (i.e., Colombia) by van Soest .
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 , 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 ), 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 .
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 , 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.
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.
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).
It is suitable only for tracking sponges with very characteristic, highly diagnostic spicule types.
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.
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.
The authors declare that they have no competing interests.
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