Freshwater sponges ( Porifera , Demospongiae ) indicators of some coastal habitats in South America : redescriptions and key to identification

Surveys for freshwater sponges were performed at several water bodies at sandy environments along a north-south direction of particularly the Brazilian coastal line. The results allowed for the distinction of four different species-specific environments along this coastal border. The main fact considered was the dominant or the sole recurrent occurrence of a single sponge species at one particular habitat. The first one is that of the lagoonal mesohaline habitats at the tropical and subtropical realms, indicated by Spongilla alba Carter, 1849. The second one refers to shallow ponds among dunes at the tropical area indicated by Corvoheteromeyenia heterosclera (Ezcurra de Drago, 1974). The third one is that of also shallow ponds close to the dune belt at the temperate region indicated by Racekiela sheilae (Volkmer-Ribeiro, De Rosa-Barbosa & Tavares, 1988). The fourth one is that of organically enriched environments, at the marginal areas of lagoons and mouth of small rivers, evolving towards freshwater muddy ponds and coastal swamps, not far from the ocean border: Ephydatia facunda Weltner, 1895 is the species to occupy this habitat with almost exclusiveness. The above species are thus proposed as indicators of such habitats and have their descriptions improved and that of their environments summarized. A taxonomic key based on the spicules of the four species is proposed. The results presented aim to contribute to the identification of spicules of these sponges in sediment columns recovered at the Brazilian and South American coastal area. Determination of paleo ocean borders are a present issue of upmost importance in what respects projections of timing and fluctuations of ascending/regressing sea levels.

The wide ranging inventory of Brazilian, in particular, and South American, in general, freshwater sponges is demonstrating that species or assemblages of this fauna present a recurrent occurrence in some specific continental habitats or even biomes.This fact has enhanced the proposition of such species as indicators of several South American freshwater environments as, for instance: Cerrado ponds (VOLKMER- RIBEIRO & MOTTA, 1995, VOLKMER-RIBEIRO et al., 1988b), floating meadwos (TAVARES et al., 2003), Amazonian clear water flood plain lakes and rocky river beds (BATISTA et al., 2003), Amazonian "igapós": black water flood plain lakes (VOLKMER-RIBEIRO & ALMEIDA, 2005), Uruguay and Paraná rivers rocky beds (BONETTO & EZCURRA DE DRAGO, 1970;BATISTA & VOLKMER-RIBEIRO, 2002).These propositions fulfill two main purposes: the first is that of using such species in projects of biodiversity monitoring or its recovering processes in the above mentioned environments.The second one has to do with the growing use the silicous spicules of freshwater sponges are having in paleo-reconstructions, once they are detected in recovered Quaternary sediments (HARRISON, 1988;TURCQ et al., 1998;CANDIDO et al., 2000;GAISER et al., 2004;VOLKMER-RIBEIRO et al., 2006).Recent studies are showing that some fresh water sponges also exhibit recurrent occurrences in certain Atlantic coastal environments of South America.These refer to typical aquatic (TERMIER & TERMIER, 1963) environments resulting at the continental borders upon the sea level regression and sand depositional processes which gave place to lagoons, freshwater ponds and wetlands or yet freshwater ponds formed amidst the dune belt.Several such environments were surveyed for their sponge fauna along this extensive coastal line.The species which exhibited recurrent/dominant occurrences at the same kind of habitat are now proposed as indicators of such environments, bearing in mind the identification of their spicules in sediment columns recovered at the Atlantic edge of the continent and their use in paleoreconstructions and studies of timing of the ocean ingression/regression processes at this edge.For this purpose, a taxonomic key based on the spicules of these species is presented.At the same time their descriptions are given and their respective habitats identified.

MATERIAL AND METHODS
Surveys for freshwater sponges were performed at several water bodies at the sandy belt along a northsouth direction, mostly at the Brazilian costal line.The surveys were manually performed or gemmules were detected in sediments caught with an Ekman dredge.Preparations of dissociated spicules of the specimens and gemmules were done according to VOLKMER-RIBEIRO (1985) for studies with light optical microscopy and for scanning electron microscopy (SEM) (VOLKMER-RIBEIRO & TURCQ, 1996).Also, camera-lucida drawings were made of the spicular components in order to obtain illustrations for the taxonomic key.The minimum, maximum and mean length and width of the spicules as well as the standard deviation were calculated based on the measurements obtained from 50 megascleres, gemoscleres and microscleres of several studied specimens of each species.The SEM photographs were obtained at the Electron Microscopy Laboratory of Pontifícia Universidade Católica do Rio Grande do Sul, Porto Alegre and later treated and mounted with the use of computer graphics.Digital images of representative specimens of each of the four species were also produced.The definitions of the spicule categories follow VOLKMER- RIBEIRO & PAULS (2000).

RESULTS AND DISCUSSION
The results allowed for the distinction of four different species-specific environments along this coastal border.Most interesting is that this listing agrees with the evolving sediment accumulation processes which take place along regressive ocean lines (TERMIER & TERMIER, 1963) starting with lagoons and evolving into closed freshwater lakes and ponds and into muddy, organic rich freshwater wetlands.The four later environments / sponge species associations are: 1. tropical and subtropical lagoonal mesohaline habitats, indicated by Spongilla alba Carter, 1849; 2. shallow ponds among dunes at the tropical area indicated by Corvoheteromeyenia heterosclera (Ezcurra de Drago, 1974); 3. shallow ponds boundaring the continental side of the dune belt at the temperate region, indicated by Racekiela sheilae (Volkmer-Ribeiro, De Rosa-Barbosa & Tavares, 1988); 4. organically enriched environments, at the marginal areas of lagoons and mouth of small rivers, evolving towards freshwater muddy-acid ponds and coastal swamps, not far from the ocean border, where Ephydatia facunda Description.Sponge forming fragile crusts on submerged portions of the aquatic vegetation.Live specimens may be green, due to association with algae.Specimens from minute to large, brittle when dry, yellowish, displaying flabelliform shapes due to the coalescence of the skeletal fibres attached to the fan-like leaves of small macrophytes (Fig. 21).Surface irregular with oscular sieves.The skeleton is a reticulum of very open and irregular meshes of monospicular fibres,   encompassing sand grains of various sizes.Megascleres, two categories of microscleres and occasionally also gemoscleres may be found in the skeletal fibers.Megascleres are anfioxea with gradually tapering extremities, from straight to slightly curved, slightly centrotylote, from smooth to microspined.Microscleres of two classes: smaller umbonated birotules with smooth shafts capped by minute rotules with the border cut in a few irregular hooks curved towards the shaft; longer, slender birotules with straight, spiny shafts and small rotules regularly cut in a number of minute teeth, the rotules may however be so reduced that the spicule turns into a strongyle with straight or curved, irregularly spined shaft.Gemoscleres are anfidiscs of uniform size and shape, with almost flat rotules finely cut into small teeth, shafts with abundant spines with crosshead endings (Fig. 5).Gemmules abundant, distributed throughout the reticulum of the sponge, reflecting the temporary nature of the environment; they are hemispherical (Fig. 6), whitish, and provided with a single foraminal tube (Fig. 7).Gemoscleres radially arranged in the thick pneumatic layer.Fully formed gemmules with a thick outer layer (Fig. 8).Spicule measurements in Table I.This is the only sponge species in the seasonal ponds formed on the inner face of the dune belt closer to the sea, in the geomorphological landscape named Lençóis Maranhenses (northeastern of Brazil), part of which is preserved in the Parque Nacional dos Lençóis Maranhenses (VOLKMER-RIBEIRO et al., 1999), and in other lakes/ponds of the same kind along the northeastern coast of Brazil (Fig. 22).It must be stressed that the species original description (EZCURRA DE DRAGO, 1974) was carried upon material collected at this same region.VOLKMER-RIBEIRO & PAULS (2000) registered C. heterosclera for the seasonal pools in the vicinity of the river Unare (Clarines), on the coastal area of Venezuela.
Typical environment.Seasonal, shallow freshwater ponds, at the tropical range, with crystalline waters and little macrophyte vegetation (Fig. 22) enclosed among the moving dunes that lay closer to the beach line (VOLKMER-RIBEIRO et al., 1999) Description.Sponge forming delicate crusts, of variable size, thickness and shape, on stones or mollusc valves/shells.Dry specimens grey, white or yellow (Fig. 23), when living may be dark green.Skeleton with an isodictial reticulum, oscules conspicuous and numerous; the reticulum however, undergoes modifications, and may show main fibers in thicker crusts.Skeleton fibers composed of straight to slightly curved, gradually very sharp pointed smooth anfioxea, microscleres are profusely spined oxeas with larger spines at the middle portion.Microscleres profusely encrust the surface of the sponge and the reticulum fibres and may surpass the size of the gemoscleres.Gemoscleres are spined birotulates with minute rotules cut in an irregular number of small curved spines (Fig. 9).Gemmules abundant, whitish, large, spherical (Fig. 10) or concave, distributed throughout the reticulum.The fully developed gemmules have a thick outer layer which may conceive the foraminal tube.Foraminal tube long and straight (Fig. 11), pneumatic layer thick with gemoscleres embedded in a disorderly manner (Fig. 12).Spicule measurements in Table II.
VOLKMER-RIBEIRO & TAVARES (1990) registered Spongilla alba throughout the Sistema Lagunar Mundaú-Manguaba, State of Alagoas, including the mesohaline portion, up to the sea border.The record was based on the identification of gemmules found in sediments dredged in order to study the benthic communities of these lagoons.Following the synonymization of Spongilla wagneri Potts, 1889 in S. alba (POIRRIER, 1976), the distribution of S. alba was extended to the states of Rio de Janeiro (WELTNER, 1895) and Amazonas (PENNEY & RACEK,1968), presumably at coastal areas.Specimen MCN-POR 1120 now confirms the record of the species for a coastal area at the State of Rio de Janeiro.The present study also confirms the preference of S. alba for circum-tropical mesohaline environments as previously indicated by HARRISON (1974) and sums up to the illustration and data on the species offered by VOLKMER-RIBEIRO & TRAVESET (1987) and VOLKMER- RIBEIRO & REITNER (1991).
Typical environment.Mesohaline environments (HARRISON, 1974), at the tropical and subtropical realms, with particular emphasis on lagoons, are the ones where S. alba appears as the dominant species.The Sistema Lagunar Mundaú-Manguaba (9º34'-9º45'S, 35º44'-35º58'W), State of Alagoas, Brazil (Fig. 24) (VOLKMER-RIBEIRO & TAVARES, 1990), as well as Lagoa Feia at Rio de Janeiro are typical examples of this environment.The occurrence of the sponge in the Ipanema River, in the Caatinga region, is explained by the fact that this river dries completely (L.C. F. Alvarenga, pers.comm.), as the crusts of the sponge were detached from large stones on the completely dry river bed.On such occasions, the natural percentage of salts is concentrated in the river water becoming as the drought progresses, brackish or mixohaline., 1974).Spicules and gemmules: 5, gemoscleres, large microscleres and small microscleres; 6, gemmule; 7, longitudinal section of the gemmule; 8, detail of the pneumatic layer of the gemmule (gm, gemoscleres; mi-a, large microscleres; mi-b, small microscleres).Racekiela sheilae (Volkmer-Ribeiro, De Rosa-Barbosa & Tavares, 1988) (Figs. 3,(13)(14)(15)(16)25,26,(29)(30)(31)(32) Type locality.Seasonal pond with sandy/peebbled bed, on the side of the road (Figueira trail) going from the State Road RS/101, municipality of Tavares, to the Parque Nacional da Lagoa do Peixe, RS (31º18'57,26"S;51º05'42,.The type locality was georeferenced following indications offered to the senior author by Sheila M. Pauls, in personal communication.Confirmation was at the same time obtained by the sampling of new materials and abundant gemmules at the site.Description.Sponge forming extremely small, slender crusts around the stems of small macrophytes, or on stony or sandy conglomerates in, generally, very shallow waters.Living sponge creamy or greenish when associated with green algae.Dry sponge brownish-yellow (Fig. 25).Spicules of the skeleton in a confused arrangement; skeleton delicate, with conspicuous pinacoderm, riddled with megascleres.Megascleres straight or slightly curved oxeas, smooth or with scanty spines and with gradually tapering extremities.Microscleres absent.Gemoscleres, two categories of birotules, the larger, rare, even in the fully formed gemmules, with a stout shaft provided with short, strong, conical spines, concentrated at the middle portion, rotules small, umbonate, deeply cut in an irregular number of hooks turned towards the shaft; the smaller birrotules, predominant in the gemmular wall, have a slender, smooth to spiny shaft with spines also gathered at the middle portion, rotules expanded and flattened, with the border slightly to heavily indented (Fig. 13).Gemmules spherical or hemispherical (Fig. 14), provided with a short foraminal tube (Fig. 15).Gemoscleres radially embedded in the thick pneumatic layer (Fig. 16), the longest gemoscleres projecting beyond the outer gemmular coat.Spicule measurements in Table III.VOLKMER-RIBEIRO et al. (1988a) described Anheteromeyenia sheilae from scanty material collected at a seasonal pond close to the Parque Nacional da Lagoa do Peixe, State of Rio Grande do Sul.The gemmular deposit found around the marginal area of this seasonal pond (Fig. 30) enhanced the present SEM illustration of the gemmular thick pneumatic coat as well as the confirmation of the original gemmular description.This remarkable gemmular deposit discovered at the pond dry margin (Figs. 31,32) and the absence of remaining specimens point out to the species as a r-strategist at this shallow seasonal pond.Upon restricting the genus Anheteromeyenia to species without pronounced rotules, VOLKMER-RIBEIRO (1996) defined genus Acanthodiscus to contain the excluded species, one of them being A. sheilae in the new combination, Acanthodiscus sheilae.BASS & VOLKMER-RIBEIRO (1998) detected the preocupation of the generic name Acanthodiscus and proposed the new genus Racekiela, resulting in the combination Racekiela sheilae.The genus Racekiela now includes only two species, R. ryderi, in the Palearctic and Nearctic Regions, and R. sheilae, in the Neotropical Region, to date endemic to the coastal area of Rio Grande do Sul.

Ephydatia facunda
The species is dominant in the lakes and swamps of the Estação Ecológica do Taim (Fig. 28), with occurrence proven by the collection of numerous specimens of various sizes and shapes, in all habitats present in this coastal freshwater system, with gemmules formed mainly in November, when the largest specimens were also found.At this system the submerged roots of the floating macrophytes are the available substrate for the sponges and were seen to be used in the following order of frequency: Eichhornia azurea, E. crassipes, Pistia stratiotes and Ceratophylum demersum (VOLKMER-RIBEIRO et al., 1988a).These authors concluded that E. facunda was a species occuring in lagoonal or swampy coastal areas at Rio Grande do Sul.
Subsequently, VOLKMER-RIBEIRO & TAVARES (1990) registered E. facunda for the Sistema Lagunar Mundaú-Manguaba, State of Alagoas.More recently, PINHEIRO et al. (2004) extended this last record to the Rio Niquin, in the municipality of Barra de São Miguel, Alagoas, though in conditions similar to those found in the aforementioned complex.In spite of its abundance in freshwater habitats E. facunda stands mesohaline environments as those of the Sistema Lagunar Mundaú-Manguaba, however with a remarkable preference for the organically enriched habitats at all the registered environments.VOLKMER-RIBEIRO et al. (2006) used gemoscleres of E. facunda contained in the recent sediments of distinct aquatic habitats at the Taim wetland system and demonstrated the validity of using freshwater sponge spicules in paleointerpretation and the study of evolution of coastal waters in South America.
Typical environment.The species is thus characterized as occupying environments with extensive macrophyte coverage (Fig. 28).Due to their association with abundant aquatic vegetation, the waters occupied are generally acid and brownish to black in colour, as a result of the abundance of humic substances and organic material in the sediments.This last association is well characterized in the study of the content of the spicules of E. facunda in recent sediments of the Estação Ecológica do Taim (VOLKMER-RIBEIRO et al., 2006).Freshwater sponges (Porifera, Demospongiae) indicators of some...

Acknowledgements.
The authors thank CNPq and FAPERGS for the CV-R researcher fellowship and VSM IC fellowship, respectively.The authors are grateful to M. Sc.Maria Tereza Queiroz Melo, Director of the Parque Nacional da Lagoa do Peixe, Mostardas, RS, for logistic support at field work.They are indebted to Mariano Cordeiro Pairet Jr. for photographs nºs 31 and 32, to Marcelo P. Barros for photograph nº 26, to Rosana Moreno Senna for photograph nº 28 taken by her deceased husband Prof. Bruno Irgang.To Carolina Coimbra Mostardeiro (IC fellow of CNPq), Rejane Rosa (art assistant) and the staff of the Laboratório de Geoprocessamento, all at Museu de Ciências Naturais, Fundação Zoobotânica do Rio Grande do Sul, for respectively, the measurements of the spicules, the final artwork of the drawings in figures 1-4, the map and the processing of the image in figure 24.They also acknowledge Edilson Morais Brito for photograph nº22.Last, but not least, the authors thank Dr. Eduardo Hajdu, Museu Nacional, UFRJ and an anonymous referee for the valuable suggestions offered.

Fig. 29 .
Fig. 29.Map with the type locality of Racekiela sheilae (Volkmer-Ribeiro et al., 1988): seasonal pond with sandy/peebbled bed, municipality of Tavares, close to the Parque Nacional da Lagoa do Peixe, State of Rio Grande do Sul.

Figs
Figs. 30-32.30, Seasonal pond and type locality of Racekiela sheilae: alongside the road (Figueira trail) linking Tavares to the Parque Nacional da Lagoa do Peixe, State of Rio Grande do Sul.Photo V. S. Machado; 31, Remarkable gemmular deposit discovered at the pond dry margin; 32, Detail of the amount of R. sheilae gemmules recently produced and deposited at the pond dry edge.