Utilizing sponge spicules in taxonomic, ecological and environmental reconstructions: a review

Reconstructing sponge communities

Numerous studies have used assemblages of disassociated spicules for reconstructions of former sponge associations. The first attempts to reconstruct sponge communities based on loose spicules at a larger scale were published at the turn of the 19th and 20th century for example in the works of Carter (1871) and Dunikowski (1882). In turn, the studies of Hinde and Holmes (Hinde & Holmes, 1892; Hinde, 1910) focused on rich spicule assemblages of the Southern Hemisphere and revealed an apparent richness of the Eocene sponge fauna of New Zealand and Western Australia, respectively. Ever since these pivotal attempts to comprehend the complexity of sponge spicule associations, fossil, sub-fossil, and recent spicules have become the subject of numerous locality- or region-specific studies that focused on assessing the sponge community compositions (Schrammen, 1924; Reif, 1967; Moczydłowska & Paruch-Kulczycka, 1978; Mostler, 1976, 1990; Hartman, Wendt & Wiedenmayer, 1980; Gruber & Reitner, 1991; Kaesler, 2004 and the literature cited therein). Wiedenmayer (1994) summarized the knowledge on the post-Paleozoic sponge spicule record from different stratigraphic units and compared the spicules derived from the fossil record with their possible counterparts present in modern sponge taxa. The results of these investigations led him to provide discussion of the origins and history of some sponge groups, including their ecological dependencies and paleobiogeography. The studies of sponge spicules further intensified in subsequent years (Brasier, Green & Shields, 1997; Castellani et al., 2012; Carrera & Maletz, 2014; Łukowiak, Pisera & Stefanska, 2019). For instance, Łukowiak (2015) supplemented the work of Hinde (1910) and revealed the richness of the sponge community of southern coasts of the Australian continent. The reconstructed community was later compared with that of New Zealand (Łukowiak, 2016a) that was initially described by Hinde & Holmes (1892). Beresi (2003) reviewed the studies on Cambrian sponge spicules (and chancelloriid sclerites) from the Argentine Precordillera, while Frisone et al. (2014) described isolated spicules form the Eocene of Italy. Interestingly, despite that there are many complications associated with studies of fossil loose sponge spicules, analyses of the spicular record from modern surficial sediments may be helpful in traditional faunistic studies. They can detect the presence of extant sponges that can be easily overlooked due to their small size, or cryptic or excavating nature. For instance, Łukowiak (2016b) focused on the sponge spicules from the lagoon reef of Bocas del Toro, Panama, and noticed the presence of highly diagnostic spicules belonging to cryptic and excavating sponges that had not been noted from that area before. Similar studies can be performed in freshwater habitats to consider the history the sponge communities (Wilkins et al., 1991) or of individual sponge taxa (Hall & Herrmann, 1980).

Assessing sponge community dynamics in time

The information obtained from loose spicules has been also applied to investigate the changes in the record of spicule assemblages through time. Such studies require spicule-rich sediment portions (Volkmer-Ribeiro, De Ezcurra & Parolin, 2007) and the best results are obtained when an uninterrupted spicule record is available. It seems that absolutely-dated sediment cores are the best way to obtain continuous record of the changes in spicule assemblages (Bertolino et al., 2014, 2017a, 2017b, 2019; Gaino et al., 2012; Łukowiak et al., 2018; Rasbold et al., 2019a).

The spicules obtained from different time intervals can be further processed by means of quantitative (Volkmer-Ribeiro et al., 2006; Bertolino et al., 2014; Łukowiak et al., 2018; Rasbold et al., 2019a), semiquantitative (Karabanov et al., 2000), and qualitative (Yang, Duthie & Delorme, 1993; Bertolino et al., 2014) methods. Such approaches allow to explore the stability (Bertolino et al., 2014) and dynamics (Bertolino et al., 2017b; Łukowiak et al., 2018) of the sponge associations in a given place over the millennial time span. They also allow to compare the recent and ancient sponge communities (Łukowiak, 2016a; Łukowiak et al., 2018; Bertolino et al., 2014, 2017a, 2017b, 2019). Bertolino et al. (2017b) investigated fluctuations in the sponge community structure from the coralligenous biogenic build-ups from the Liguarian Sea (Western Mediterranean). They compared sponge faunas from the last 3,500 years (and from 40 YBP in particular) with the modern sponge community of this place, showing turning points in sponge diversity and abundance. They inferred a considerable reduction of species richness that occurred during a time interval of about 40 years (1973–2014) and that affected mainly the massive/erect sponges; particularly those of the clade Keratosa and, to a lesser degree, encrusting and cavity dwelling sponges (Bertolino et al., 2017b).

In turn, Łukowiak et al. (2018) confronted the modern sponge community of Bocas del Toro, Caribbean Panama, with the spicule record from the same area covering the last 900 years of sponge community dynamics. In their study, Łukowiak et al. (2018) recognized changes in the structure of the sponge community (expressed through the decrease in the number of spherical and ovoid spicules belonging mostly to some chondrillids, Placospongia spp. and Geodia spp., and the increase in the numbers of monaxonic spicules, mostly of haplosclerids and axinellids) and investigated the correlation between their data with records of contemporaneous reef inhabitants. As main sponge predators in this area are turtles and fishes (parrot- and anglerfishes), and the turtles feed mostly on sponges with spherical spicules, they concluded that the increase in the numbers of spherical spicules in the sediment relative to monaxons could be connected with the overfishing of the hawksbill turtle Eretmochelys imbricata that became gradually less abundant at that time.

Ecological and environmental reconstructions

Recognition of the characteristics of former sponge communities can initiate larger-scale reconstructions of the environmental conditions in the studied area. Once the loose spicules are assigned to their respective taxa, the next crucial step is to become familiar with their ecology (Volkmer-Ribeiro & Machado, 2007); that is, habitat requirements and environmental preferences of particular sponge species or larger clades (see Supplemental Information 2). For example, Koltun (1960) already pointed out the existence of sponge taxa of specific environmental requirements which make them potential indicators of water salinity, temperature, or depth. Recognized sponge communities can provide information about the water regime, flow, and velocity (lentic vs. lotic conditions; for example, Parolin, Volkmer-Ribeiro & Stevaux, 2007, 2008; Machado, Volkmer-Ribeiro & Iannuzzi, 2012; Kuerten et al., 2013), pH (Harrison & Warner, 1986; Pisera & Saez, 2003), light intensity (e.g., Harrison, 1974; Supplemental Information 2), temperature (e.g., Gammon, James & Pisera, 2000; Gaino et al., 2012), currents (e.g., Molina-Cruz, 1991), salinity (e.g., Cumming, Wilson & Smol, 1993), and depth (e.g., Hinde & Holmes, 1892; Pisera, Cachao & Da Silva, 2006; Łukowiak, Pisera & Schlögl, 2014; Łukowiak, 2016a; see Fig. 6). Also, less obvious parameters can be reconstructed through the investigations that use sediment spicules, such as dissolved silica concentrations (Kratz et al., 1991). In their work, Kratz et al. (1991) measured the width of megascleres obtained from lake deposits to estimate the silica concentration in the last 12,000 years in the area of Wisconsin (USA). They concluded that the concentrations of dissolved silica were gradually decreasing over that time. However, Kratz et al. (1991) did not provide precise assignment of the spicules to any of the three possible species (Spongilla lacustris, Corvomeyania everetti, and Eunapius fragilis) rising concerns that the size shift may have actually resulted from species replacement. A possible differential dissolution of spicules as a function of depth could also influence their size. It is essential to note, however, that the authors were aware of these problems.

Sponge spicules are also common components of soils (Kaczorek et al., 2018 and the literature cited therein) and can provide information about soil origins (Jones & Beavers, 1963; Wilding & Drees, 1968; Harrison, 1988b; Schwandes & Collins, 1994). In most cases, the spicules found in soils belong to freshwater sponges (Harrison, 1988b) and are indicative of the fluvial origin of the deposits (Chauvel, Walker & Lucas, 1996). The distribution, type and degree of fracturing of spicules in soil can help to reveal whether the sediments are autochthonous or allochthonous, and, if the latter, where they originated (Wilding & Drees, 1968; Schwandes & Collins, 1994). Schwandes & Collins (1994) showed that in well-drained soils the number of spicules is smaller than in those that are poorly-drained and noticed that in the dry pounds the number of spicules increased towards the pond center, thus clarifying the precise location of these ancient waterbodies.

Sponge spicules are also found in other types of wet terrestrial environments; in waterlogged soils, hydric soils (Schwandes & Collins, 1994), and marshland (Volkmer-Ribeiro, 1992). Apart from providing information on the origins of soils, spicules can reveal the occurrence, duration, and intensity of floods (Golyeva, 2008) or the presence of eolian transport (Wilding & Drees, 1968).

Through the use of demosponge spicules and by applying the facies analysis it is possible to reconstruct sedimentary environment of spicule-rich deposits (Mehl & Lehnert, 1997; Frisone et al., 2014). The recognition of sponge taxa with very narrow and specific environmental preferences can facilitate the reconstructions of water depth (Fig. 6), temperature, and climate (Parolin, Volkmer-Ribeiro & Stevaux, 2008; Pisera, Siver & Wolfe, 2016), though it is necessary to bear in mind that some sponges (notably hexactinellids and lithistids) that are generally thought to be deep-water indicators, are also reported form shallow waters (2 m; Leys et al., 2004; Perez et al., 2004). Therefore, bathymetric reconstructions should not be based on a single taxon.

However, such actualistic approach needs to be applied with caution. Under certain favorable conditions (e.g., calm hydrodynamic setting and high water dissolved silica (DSi) concentrations (Alvarez et al., 2017)), modern sponges that are interpreted as indicators of cold deep waters may have inhabited warm and shallow settings in the past (Gammon, James & Pisera, 2000).

Sponge distribution is closely associated with water nutrient level, including water DSi concentrations (for more details see Alvarez et al., 2017). Sponge assemblages were studied to estimate the distributions of sponges along a DSi gradient and to assess the validity of fossil sponges as a paleoecological tool for inferring DSi concentrations in the past oceans (Alvarez et al., 2017). The study showed a correlation between the presence of hexactinellid sponges in an environment and high DSi levels; for the other sponge groups the linkage was not so straightforward and depth could have been another factor that could have some impact on the spatial distribution of sponge assemblages (Alvarez et al., 2017).

The reconstructions of geographical ranges of sponge taxa, in turn, lead to new paleobiogeographical and ecological inferences. A southern Australian shallow water sponge community reconstructed by Łukowiak (2016a) broadened the geographical ranges of some sponge taxa (e.g., Dotona pulchella and Mycale (Rhaphidotheca) loricata) in the late Eocene. Their bathymetrical range changed too as today they occupy deep water niches and are considered to be Tethyan relicts. The broader geographical occurrences in the geological past further explain the disconnected distribution of some sponge groups in modern times and possibly elucidate their migration pathways. When compared the fossil sponge community of southern Australia with the recent one, the taxonomic composition of the sponge fauna in this region appears to be relatively stable since the Eocene (Łukowiak, 2016a).

Of special interest and importance are sponges inhabiting freshwater environments because they represent accurate environmental indicators (Harrison, 1988a, 1988b; Volkmer-Ribeiro & Turcq, 1996; Frost, 2001; Volkmer-Ribeiro, De Ezcurra & Parolin, 2007; Parolin, Volkmer-Ribeiro & Stevaux, 2008). Their spicules, together with gemmuloscleres (the spicules of sponge resting bodies) (Manconi & Pronzato, 2002), are widely used as a proxy for reconstructions of the parameters associated with the water quality (Yang, Duthie & Delorme, 1993).

Some characteristics of sponge spicules can change depending on environmental parameters, such as the silica concentrations of the habitat (Turner, 1985; Matteuzzo et al., 2015), which may provide a paleolimnological measure of long-term silica dynamics or past water-chemistry conditions (Kratz et al., 1991). Such inferences became possible mainly owing to the studies of the environmental preferences of modern freshwater sponges (Harrison, 1974, 1977, 1979; Harrison & Harrison, 1977, 1979; Harrison, Gleason & Stone, 1979; Poirrier, 1969, 1974; Volkmer-Ribeiro, 1981; Evans & Montagnes, 2019). The development in our understanding of the base-line ecological parameters of many extant freshwater sponge species was gathered and summarized by Harrison (1988b) and the literature cited therein who provided a comprehensive and useful key to environmental preferences of North American freshwater sponge species that could be applied in paleolimnological studies (see Supplemental Information 2; for example, Racek, 1966, 1970, 1974; Harrison, 1990).

Importantly, the spicular data can be used for quantitative studies irrespective of the species assignment. The abundance of sponge spicules in combination with the data obtained from other organisms (e.g., diatoms, chrysophyte cysts, plant phytoliths, and scales) is an indicator of suitable habitat conditions and the decrease in the numbers of spicules can be interpreted to be due to the deterioration of water quality (Yang, Duthie & Delorme, 1993) or changes of past salinity conditions (Cumming, Wilson & Smol, 1993). Gaiser et al. (2004) reconstructed a complex 5,500-year-long hydrological history of a temporary pond in the Savannah River Site, South Carolina (USA). They reconstructed a transformation from a vegetated marsh to an open, permanently flooded water body about 3,750–4,630 YBP. The return to a wetland community took place ~3,750 YBP (Gaiser et al., 2004). Even though the authors recognized the presence of three sponge species in their assemblage, they did not explore whether their occurrence is indicative of an important environmental information (water pH, conductivity). The most comprehensive assessment of the use of freshwater sponge spicules for paleoenvironmental reconstructions was conducted in riverine and lentic systems in Caatinga (Santos et al., 2016) and Pantanal wetlands ecosystems (McGlue et al., 2012; Kuerten et al., 2013; Rasbold et al., 2019b) in Brazil. Parolin, Volkmer-Ribeiro & Stevaux (2007, 2008), Guerreiro et al. (2013) and Zviejkovski et al. (2017) focused mostly on reconstructing the history of lake sediments on colluvial-alluvial terraces in the Upper Paraná River, while Rasbold et al. (2019a) investigated the history of island deposits. Rasbold et al. (2019a) reconstructed the evolution and origin of two closely located riverine islands (Bandeirantes and Grande) during the late Pleistocene to Holocene in the northern Brazil (Upper Paraná River). The spicules of freshwater sponges were used to reconstruct the assemblage composition, the relationship between species richness and frequency, and spicule preservation, as well as to complement the facies analysis. Rasbold et al. (2019a) revealed the differences in formation of these two islands. For example, in one of them the lacustrine environments were predominant since the mid-Holocene (the lentic environment is inferred from the presence of spicules of Tubella variabilis and Radiospongilla amazonensis), whereas the second island was cut off from the river floodplain by channel avulsion and influenced by the river flow (as indicated by the presence of spicules of riverine species, including Uruguaya corallioides, Oncosclera schubarti, O. navicela and Corvospongilla seckti). In the coastal area of Rio Grande do Sul (S Brazil), in turn, the numbers and the morphotypes of sponge spicules (and gemmuloscleres) of several freshwater bodies provided evidence for a regular succession of seasonally drier periods (Volkmer-Ribeiro et al., 2006). Further, the study showed that the analysis of sediment spicules could also predict the evolution of this limnic area (Volkmer-Ribeiro et al., 2006). In the northern part of Brazil sponge spicules were used to investigate the origins of deposits of karstic lake (Machado, Volkmer-Ribeiro & Iannuzzi, 2016), while in central-west Brazil the evolution of the limnic system was reconstructed (Machado, Volkmer-Ribeiro & Iannuzzi, 2014). Machado, Volkmer-Ribeiro & Iannuzzi (2014) investigated sediments from about 52,000 to 27,500 YBP and recognized three stages of the development of the lake: the installation, establishment, and development stage. Following the recognition of environmental preferences of the identified sponge species, they estimated the weather patterns. For instance, the presence of spicules belonging to Corvoheteromeyenia australis indicated polar incursions. The presence of spicules of Corvomeyenia thumi, in turn, suggested that drier and hotter weather conditions might have been predominant for short time periods (between ~48,333 and 34,700 YBP). The history of the paleolake ended with complete filling of the basin and disappearance of the sponge spicules and can be correlated with the Last Glacial Maximum, which occurred between 25,000 and 11,000 YBP (Machado, Volkmer-Ribeiro & Iannuzzi, 2014).

Isotopes in sponge spicules as a geochemical proxy

The structural and chemical properties of siliceous shells of seawater diatoms were found to be archives of silicon isotope composition (δ³⁰Si) and a proxy for past silicic acid utilization, thus providing insights into silicon cycling in ancient oceans (De La Rocha, Brzezinski & De Niro, 1997; De La Rocha et al., 1998; Racki & Cordey, 2000; Egan et al., 2012). These studies initiated the investigations of the use of silicon isotope composition in other marine organisms producing siliceous skeleton, including sponges (Douthitt, 1982; De La Rocha, 2003). Sponges, as bottom dwellers, provide information about deep-water dissolved silica (DSi) concentrations. The studies of Hendry & Robinson (2012) were conducted on materials picked from core-top sediments that were obtained from several different ocean basins. The spicules were evaluated with respect to whether the Si isotopic fractionation depends on the geographic distribution, salinity, and water temperature. It was discovered that the relationship between Si(OH)₄ and δ³⁰Si in sponge spicules is the same in different oceans and does not depend on water temperature and salinity. Thus, global ocean silicon cycling can be inferred through quantification of the changes in deep water dissolved silicon concentrations (Fontorbe et al., 2017; Hendry et al., 2019). The silicon isotopic fractionation appears to be biologically controlled due to preferential uptake of the light isotope (Wille et al. 2010) and is a function of silicic acid concentration (Hendry & Robinson, 2012). Also, Hendry et al. (2010a) showed that there are no significant post-depositional effects or early diagenetic overprints on Si fractionation in deep sea sponge spicules. It was further showed that the relationship between δ²⁹Si and δ³⁰Si in sponges is consistent with kinetic fractionation during biomineralization and that fossil spicules preserve the primary δ³⁰Si signal recorded in living sponges (Hendry et al., 2010a). However, Cassarino et al. (2018) revealed the differences in silicification mechanism between the two major clades, demosponges and hexactinellids. The fused dictyonal frameworks of hexactinellids, characterized by secondary silicification, exhibit extremely light δ³⁰Si signatures. This is probably due to the enzymes that mediate silica deposition. The differences in spicule structure, that is, the level of fusion of the skeleton and hence, the presence of the secondary silica deposition as well as the presence of considerable amounts of organic molecules, may also play an important role in silica fractionation (Cassarino et al., 2018). Thus, sponges with the dictyonal framework do not fit the asymptotic relationship with DSi. Also, specific groups of sponges (carnivorous or those with hypersilicified or giant spicules) give anomalous geochemical signatures (Hendry et al., 2019). Hendry et al. (2019) further revealed differences in isotopic fractionation between mixed-species and monospecific sponge assemblages, showing a smaller variability among monospecific aggregations (Hendry et al., 2019). Thus, the reconstructions of past water silica should be made on sponges with certain spicule types; that is, using the spicules of demosponges and hexactinellids, except those whose skeletons show the dictyonal framework and those with abnormal morphologies (Hendry et al., 2019).

Nevertheless, sponge spicules seem to be among the most promising sources for the reconstruction of deep water silicic acid concentration over the geological time. Deep sea sponge spicules and diatoms from sediment cores obtained in the Scotia Sea (Southern Ocean) have shown that water Si(OH)₄ concentrations can be reconstructed for sediments deposited within the last tens of thousands of years (Hendry et al., 2010b); though, the reconstructions of water dissolved silicon level have been also inferred from spicules originating from the Eocene (De La Rocha, 2003; Fontorbe et al., 2016, 2017). Fontorbe et al. (2017) used the silicon isotopic composition of sponge spicules and radiolarian tests in 50–23 Ma timespan (Eocene and Oligocene) in order to reconstruct deep-water silica levels and to examine upper ocean δ³⁰Si. The decrease of δ³⁰Si and hence the higher dissolved Si concentrations in sponge spicules was interpreted as being related to the shift towards a solely Southern Ocean source of deep-water in the Pacific during the Paleogene (Fontorbe et al., 2017). Although the studies aiming to recreate the whole-ocean silica cycling have not been conducted on materials older than Eocene (De La Rocha, 2003; Fontorbe et al., 2017), they do not seem to be limited by time; rather, they depend on the quality of the spicular record.

Other studies applied germanium to silicon ratios (Ge/Si) from the siliceous sponge spicules to trace the Si sources and cycling (indicators, among others, of continental weathering and hydrothermal activity). Sutton (2011) showed that the reconstruction of Si concentrations in ancient water is more accurate when comparing two geochemical proxies for Si utilization, Ge/Si and Si isotope composition of siliceous organisms. She also suggested that the reconstruction of deep-water Si level from sponge spicules is more helpful in investigations of whole ocean changes than from the surface water provided by the Ge/Si or Si isotope composition of diatoms (Sutton, 2011). Ellwood et al. (2006) investigated the reconstructions of paleo-Ge and -Si concentrations using two models that depend on two scenarios of Ge incorporation into sponge silica. They explored which of them works best for reconstructions of paleo-Ge and which for paleo-Si concentrations (Ellwood et al., 2006).

Jochum et al. (2017) used the slowly-growing basal spicule (basalium) of the modern deep-sea sponge Monorhaphis chuni to reconstruct silica and Ge/Si ratios during the last deglacial period. The basalium of M. chuni was also used for the assessment of seawater paleotemperatures of East China Sea throughout the last 11,000 years (±3,000 years) by measuring isotopic composition and Mg/Ca ratios taken according to spicule growth, incrementally from the center of the spicule to its surface (Jochum et al., 2012).