Revision of Rhabdastrella distincta (Thiele, 1900)
A re-description of the holotype and description of two recently re-collected specimens
Anne Twaalfhoven (10149996) Biology BSc Thesis, July 2016
University of Amsterdam: dr. P. (Peter) Roessingh, p.roessingh@uva.nl
Naturalis Biodiversity Center, Leiden: dr. N.J. (Nicole) de Voogd, nicole.devoogd@naturalis.nl
Abstract
Sponge taxonomy is largely founded upon outdated descriptions originating from pre-modern times. Luckily, the material that these descriptions are based upon is often still available in Natural History Collections. In this article two sponge samples collected in 2009 from Ternate, Indonesia are compared to the type material of Rhabdastrella distincta. The holotype was described in 1896 by Thiele (1900). This article reviews the material for the first time ever since. The two recently collected samples are the first records of the species since its description. Descriptions of all three samples are based upon external morphology, skeletal structure, spicule measurements and spicule analysis by electron microscopy. It is revealed that, contrary to previous descriptions, the spherasters of R.
distincta are stubbed with spines. Consequently, it is argued that the relation of R. distincta to its
Introduction
When researching environmental change and biodiversity, Natural History Collections (NHC’s) can be of high value. Former taxonomists collected and described large collections of specimens that now serve as the foundation of our current knowledge on marine biodiversity (Jackson, 2001; Hooper & van Soest, 2002; Hoeksema et al, 2011). For reef systems, systematic ecological observations and methodological sampling started no earlier than the 1930’s (Jackson, 2001), and most recent surveys only encompass relatively short timespans (Jackson, 2001; van der Meij et al., 2010; Lister, 2011; Hoeksema et al., 2011). Especially for reef systems, NHC’s can serve as historical baselines in monitoring long term biodiversity changes and designating indicator species. NHC’s are thus useful tools in justifying signals of environmental change (Suarez & Tsutsui, 2004; Hoeksema et al., 2011; de Voogd, 2012).
One such NHC was obtained by the German professor W.G. Kükenthal in 1896. Amongst other organisms, he collected about 100 specimens of sponges near the island of Ternate in the Moluccan Sea. Kükenthal’s collection was described by Kieschnick (1896), but his findings were later revised by Thiele (1900 & 1903). These works still serve as the most important sponge records for the area. Their papers contained 51 new species, some of which have never been recorded since and most likely are endemic or even singletons (de Voogd, 2012). It wasn’t until 2009 that the same area was sampled again, this time by the combined efforts of Naturalis (The Netherlands) and E-Win, LIPI (Indonesia) (Hoeksema & van der Meij, 2010). In this expedition over 300 sponge specimens were obtained. Of the species found by Kükenthal, a mere 30 were re-collected. These recent samples offer the opportunity to evaluate the descriptions of the German authors.
Rhabdastrella distincta is one of these re-collected species. R. distincta was originally described as Coppatias distinctus by Thiele (1900). In 1903 Thiele merged the genera Coppatias and Jaspis.
Consequently, all species that lacked small oxeas were placed into the new genus Rhabdastrella, R.
distincta becoming the type species for this particular genus and species. R. distincta is now classified
within the family Anacorinidae Schmidt 1870 and defined as ‘- an Ancorinidae with euasters, among
which large spherasters or sterrospherasters are abundant. Triaenes may be reduced or absent’ (Uriz,
2002). Thiele describes C. distinctus to be overgrown with a Gellius sponge (now Haliclona (Gellius) Gray 1867). Due to this cryptic growth form, the species is extremely hard to find and to our
knowledge, there are no records of R. distincta growing without a sponge epibiont. In fact, after its description, the species has never been collected again.
Since Thieles short description, the species has never been properly reviewed. During the Ternate expedition in 2009, two specimens were obtained that show strong resemblance to R. distincta. This article compares the newly collected specimens to the type material. Additionally, a re-description of the type material is given, substantiated with electron microscope (SEM) images.
Materials & Methods
Specimen collectionIn November 2009, 300 specimens were collected using SCUBA from the reefs of Ternate, in the Northern Mollucan sea. The specimens were preserved in 70% ethanol and deposited in the sponge collection of the Naturalis Biodiversity Centre (RMNH), in the Netherlands.
The NHC collected by Küktenthal in 1896 is located in the Natural History Museum of Berlin. Sub samples of the specimens were taken and are kept in Naturalis.
Specimen Analysis
Specimen descriptions are based on external morphology, skeletal architecture and spicule morphology.
For skeletal analysis, tangential sections of the ectosome and perpendicular sections of the
choanosome were cut by hand. The sections were air-dried and mounted in Ultrabed on a microscope slide. The slides were studied under a Leitz high power light microscope.
Spicule preparations were made by dissolving a small piece of the specimen in 60% Nitric Acid (HNO3) after which the residue was rinsed three times with water and three times with 96% ethanol. The spicules were air-dried on microscopic slides and mounted in Ultrabed. Additionally, spicules
Scanning Electron Microscope (SEM). Spicules were measured using the Leitz high power light microscope in combination with Leica Application Suite V4.8. Oxea dimensions are given as a range of length measurements x range of width measurements. For oxyasters and oxyspherasters only the range in diameter is given. For spherasters, ray length was measured as well. Spicule-size ranges are taken from 20-30 measurements.
Abbreviations used in this article are RMNH (Naturalis Centre for Biodiversity, Leiden) and ZMB (Museum für Naturkunde und der Universität Humbolt zu Berlin, Berlin, Germany). Classification is done in accordance to Systema Porifera (Hooper & van Soest, 2002).
Results
Class Desmospongiae Order Astrophorida
Family Ancorinidae Schmidt 1870 Genus Rhabdastrella Thiele 1903
Rhabdastrella distincta, Thiele 1903
Material examined: Holotype ZMB. 3190, Indonesia, Ternate, Kükenthal leg., Kütkenthal ded.,3.XII.1902
External morphology: To Thiele, only a 2 x 1 cm piece of the holotype was at hand. To me, only a photograph of the specimen was available (fig.1). The specimen’s colour is black. According to Thiele it was overgrown with Gellius couchi (now accepted as Haliclona (Gellius) fibulata (Schmidt, 1862)). Skeletal analysis: Ectosomal and choanosomal slides are unclear. Arrangement in spicules is hard to find. Oxeas appear to be dispersed confusedly in choanosome. High abundancy of spherasters and oxyasters in ectosome (fig.3d).
Spicules: Megascleres: large oxeas, fusiform, 646 -1012 um x 17- 27um (905 x 21, n= 20). Short, pointy ends.
Microscleres: eurasters: Oxyasters having 6 rays of equal length. Diameter 62 um – 101 um (82, n=20). Spherasters having 12-16 rays, ray length 6 um – 17 um (11, n=29), diameter 22 um – 59 um (41, n= 29). Centrum takes up about 3/4th of diameter. Rays have spines perpendicular to ray axis getting more abundant near the ends. Oxyspherasters having about 13 rays emerging from small centrum. Diameter 16 um – 26 um (22, n=20).
Material examined: RMNH POR. 5341, Indonesia, Halmahera, Maitara Maitara NW, stat TER.010, N 0*44’32”, E 127*21’50.9”,29-10-2009, depth unknown, Fieldnr #TER10/291009/092, coll. N.deVoogd
External morphology: Piece is largely overgrown with two other species (fig.2a,b). Color after preservation in alcohol is dark green to black. Some pinkish and white growth/sediment attached. Shape is bulky (fig.2a,b). Structure is very firm and resilient. Leather-like ectosome. Rest of the body crumbles apart when cut into thin slices. Dimensions: 11 x 4 x 1 cm.
Skeletal analysis: Ectosomal and choanosomal slides are quite unclear. Confusedly dispersed oxeas in choanosome, spherasters densely concentrated in ectosome.
Spicules: Megascleres: large oxeas, fusiform, 684 – 991 um x 12 – 20 um (867 x 16, n=20). Ends are short and pointy.
Microscleres: Oxyasters having 6-7 rays of mostly equal lengths. No centrum. Diameter 43 um – 92 um (63, n=21). Spherasters having 8-13 rays. Ray length 5 um – 18 um (11, n=22). Diameter 20 um-52 um (39, n=22). Rays are smooth with an occasional spine at the tip. Oxyspherasters having about 13 -15 rays, no centrum. Diameter 16 um- 25 um (20, n=21) (fig. 6).
Material examined: RMNH POR. 5554, Indonesia, Halmahera, off Tidore Pulau Pilongga S, N 0*42’44.1”, E 127*28’47.3”, 12-11-2009, depth 20m, Fieldnr #TER35/121109/?, coll. ?
External morphology: Rather thin layer overgrowing another sponge species, layer gets thicker and more like a cushion towards the end. Ectosome feels leather-like, however rough at some spots. Color is dark green to black after preservation in alcohol. Several pinkish and white spots of sediment or colonial growth (fig.2c,d). Dimensions: 8 x 2 x 1 cm (Haliclona included. Over most of the specimen,
R. distincta forms a 2 mm thick crust).
Skeletal analysis: Dense concentration of spherasters in cortex is clearly visible (fig.3b). Bundles of oxeas in endosome. Oxyasters are scattered between oxeas.
Spicules: Megascleres: Large oxeas, fusiform, 842 um – 967 um x 7 um – 23 um (776 x 13, n=24). Tips are pointy but slightly rounded. Oxyasters having 5-6 rays emerging from small centrum. Diameter 76 um - 98 um (84, n= 8). Spherasters having 11-15 rays. Ray length 10 um- 13um. Diameter 19 um – 43 um (35, n=26). Sometimes no centrum. Rays are smooth with an occasional spine at the tip. Oxyspherasters having about 11 rays. Diameter 13 um – 24 um (17, n= 21).
Table 1. Overview of spicule measurements (um) of studied specimens. Ranges and the mean are given from
20-30 measurements. * ZMB 3190 = Holotype.
Figure 1. Holotype Coppatias distinctus (Rhabdastrella distincta) Thiele 1900. Species description by Thiele (1900) was
based on this small specimen.
Specimen Oxeas Oxyasters Spherasters Oxyspherasters
ZMB 3190 * Range 646 -1012 x 17- 27 62 – 101 22 - 59 16 - 26 Mean 905 x 21 82 41 22 Thiele 1900 850 x 25 40 15 RMNH POR 5341 Range 684 - 991 x 12 - 20 43 – 92 20 - 52 16 - 25 Mean 867 x 16 63 39 20 RMNH POR 5554 Range 842 - 967 x 7 - 23 76 - 98 19 - 43 13 - 24 Mean 776 x 13 84 35 17
Figure 2. External morphologies R. distincta samples. A; POR 5341 R. distincta overgrown with two sponge epibionts. B.
POR 5341 other side. C. POR 5554 R. distincta. D. POR 5554 Haliclona epibiont.
Figure 3. Skeletal images R. distincta. A. Endosome POR 5554. Oxeas confusedly dispersed though slightly in bundles.
Spherasteres and oxyspherasters scattered in between oxeas. B. Cortex POR 5554. Densely packed spherasters. C. Haliclona
– R. distincta intergrowth. Greyish structure on top is Haliclona, exclusively consisting of medium sized oxea. Brownish
Figure 4. Original drawing of R. distincta spicules by Figure 5. Reconstruction of Thiele (1900) Thiele (1900). 12a. Oxea. 12b. Spheraster, without spines. by Uriz (2002). A. Oxea. B. Oxyaster,
Figure 6. SEM images of R. distincta spicules. A. oxeas. B. Oxea tip. C. Oxyaster. D. Oxyspheraster. E. Spherasters ZMB 3190 E. Spheraster rays are stubbed with spines. Spines are present though less
Discussion
Three samples of the sponge R. distincta were described here, among which the type material that was collected over a century ago. The other two samples (POR 5341 and POR 5554) were collected in 2009 and were suspected to be of that same species. POR 5341 and POR 5554 show strong resemblances to the holotype in appearance as well as in skeleton and spicule arrangement. Both recent samples are of exactly the same color. The touch and structure of the cortex of both sponges is identical.
The growth-form of the latter two samples slightly differs. POR 5341 is a thicker, firmer cushion whereas POR 5554 is more of a thin layer overgrowing another sponge. POR 5554 seems more interwoven with its epibiont than POR 5341 (fig.2, fig 3c). In fact, one may state that POR 5554 grows over its host, while POR 5341 is overgrown by another sponge. Moreover, the different appearances of the sponge epibionts suggest that both samples are associated with different sponges. Presumably species of Gelliodes and Haliclona. Evidently, more research is needed in order to understand the relations of R. distincta with its epibiont species.
No significant differences were found in spicule measurements amongst the samples, though the holotype’s spicules are generally slightly larger than POR 5341 and 5554 (table 1). SEM images show no abnormalities between the samples that suggest one of the samples to be of a different species. However, some differences can be observed in the forms of the spherasters amongst the different samples. The distinct spines characterizing the rays of the holotype occur less frequently on the spherasters of POR 5341 and 5554 (fig. 6). In some cases, they are completely absent. Spherasters of POR 5554 have a smaller centrum (in some cases even no centrum at all) than the other two samples. These deviations may be the result of varying silica levels in the water.
Based on the SEM images and spicule measurements, I conclude that POR 5341 and POR 5554 are indeed R. distincta. Nevertheless, molecular analysis is necessary to provide full certainty.
The SEM images of the holotype have shown that the original description by Thiele (1900) misses the characteristic spines on the spherasters (fig. 4). Thiele’s original description was rewritten and
redrawn by Uriz in 2002 (fig. 5). However, Uriz (2002) did not have access to the holotype, so no material was examined for the publication. Hence, the spines remain unnoticed in this latest description as well.
Thiele’s (1900) and Uriz’ (2002) drawings show another rather rounded, bulky spheraster (fig. 4.12c, fig.5d). Thiele mentions that he specifically drew the shape because he thought it was an odd, peculiar item and worth to notify; ‘In fig. 12c habe ich eine eigentümliche Abnormität dieser Sternform
abgebildet.’ Uriz copies this drawing, but does not clarify its abnormality in her description, making
the odd spheraster appear like a regular component of R. distincta. Nor our light microscope nor our electron microscope revealed a spheraster resembling Thieles drawing. However, spherasters appear blurry underneath a light microscope that is not properly adjusted. What Thiele drew might just have been a normal spheraster, or an intermediate growth form of a spheraster.
Besides the odd spheraster, the re-description by Uriz (2002) misses out on yet another crucial factor. Uriz (2002) does not mention that R. distincta was found overgrown by Gellius (Haliclona). In 2005, Longakit et al. collected a Rhabdastrella sp. from the reefs around the Island of Cebu, Philippines. Their description highly resembles R. distincta as the specimen is found in contact with Haliclona
amboinensis. However, they do not feel confident to make the species allocation as they state that (in
systema Porifera) for R. distincta (Thiele, 1900) ‘there was no mention of any close association with
another sponge’. However, Thiele did indeed mention such an association in his original description.
There may thus be a fair chance that the sponge found by Longakit et al (2005) is indeed R. distincta. Currently, the genus Rhabdastrella is allocated within the family Ancorinidae Schmidt 1870 (Hooper & van Soest; Uriz, 2002). Within the Systema Porifera (2002) it is officially defined as ‘Ancorinidae
with euasters, among which, large spherasters or sterrospherasters are abundant and mainly
concentrated in the cortex. Triaenes may be reduced or absent in some species’. At present, the genus
contains 21 valid species (World Porifera Database, 2012). Since its foundation in 1903 by Thiele several synonyms have been introduced. Earlier, in 1888, Sollas founded Aurora, for Stelletidae
without a 2 layered cortex and large spherasters, Aurora globostellata being the type species. In 1911 Row initiated Diastra for Epipolasidae with two kinds of spherasters (of which one simulates a sterraster) and a skeleton consisting almost fully of a cortical layer of tangentially placed oxea. Dendy then argued in 1916 that the genera Diastra and Rhabdastrella ought to be merged within Aurora. Based on the typical sterrospherasters of Aurora species he emphasizes the significance of Aurora as a genus linking the Geoiidae and Stellettidae. He notifies that Aurora globostellata and Rhabdastrella
distincta are closely related, as well as Diastra sterrastraea and Aurora Rowi. Instead of proposing a
new genus for his newly discovered species Aurora cribriporosa, which has large rough spherasters and no triaenes, he thus proposes to place all species within Aurora. De Laubenfels recognizes in 1957 that Aurora is preoccupied and proposes Aurorella as a new name. Nevertheless, Hechtel (1983) uses Aurorella as a subgenus of Rhabdastrella for his species Rhabdastrella (Aurorella) fibrosa, which has similar microscleres to other Rhabdastrellae, but lacks triaenes.
Remarkably, Dendy (1916) states that R. distincta and R. globostellata are closely related because both have large ‘smooth’ spherasters. Additionally, he mentions that R. cribriporosa (collected from the Solomon Islands) too is closely related to R. distincta, their main difference being R.
cribriporosa’s spherasters, which are described as having ‘a large centrum and conical rays beset with short spines’. Yet, the SEM images in this article have shown that this description strikingly matches
the spherasters of R. distincta (fig. 6, ZMB 3190). Spherasters of the holotype of R. distincta do have spines as well. Actually, Dendy’s description of R. cribriporosa sounds very similar to R. distincta. Both having a darkish color and a cortex of leathery texture. The skeleton being an ‘irregular feltwork
of moderate sized oxea’. Dendy differentiates between the different sizes of spherasters, describing
large, normal and minute ones. In the present description of R. distincta the spherasters were not classified according to size, however different sizes were observed and this would certainly be a valid point of focus for future reviews. In conclusion, considering the results of this review, R. distincta and
R. cribriporosa may be more similar than previously thought. Additionally, it is elucidated here that R. globostellata and R. distincta do not share the characteristic of totally smooth spherasters. Another
difference between the latter two is the absence of triaenes in R. distincta, which are characteristic for
R. globostellata. R. distincta and R. globostellata might thus be less related than assumed by Dendy
(1916).
Apart from R. globostellata, not many Rhabdastrellae have been collected from the waters around Indonesia. However other Rhabdastrellae collected within the Indo-Pacific region include; R. aurora (Hentschel, 1909), R. membranacea (Hentschel, 1909) and R. reticulata (Carter, 1883) from around Australia. All of the above are characterized by triaenes. The loss of triaenes in R. distincta (and also in R. cribriporosa) is believed to be secondary, and occurred in several Ancorinid lineages (Cardenás et al., 2011; Haiju & van Soest, 1992). Seeing that R. distincta does not possess triaenes nor
sterrasters, characters that are coined typical for the genus by several authors, one may wonder whether R. distincta is a logical representative type species to the genus. It might be more straightforward to restore the genus Aurora – by the name of Aurorella de Laubenfels 1957- with
Aurorella (Rhabdastrella) globostellata as type species.
Conclusion
This article compared three sponge samples that all appeared to be Rhabdastrella distincta. Amongst these samples was the holotype that was collected in 1896 and was not reviewed ever since. The present analysis has shown that, contrary to previous assumptions, the rays of the spherasters of the holotype are rough instead of smooth, and lined with spines. This puts the relation of R. distincta to other Rhabdastrella species (a.o R. cribriporosa and R. globostellata) under discussion.
Considering the lack of triaenes and sterrasters in R. distincta, its position as type species is deferred. Thorough molecular analysis will be necessary in order to truly elucidate the validity of the
Aknowledgements
First and foremost, I would like to thank Nicole de Voogd for introducing me to the world of sponges and guiding me through the complicated chaos of sponge taxonomy. Secondly I owe thanks to Esther van der Ent, Niels van der Windt, Gydo Geyer and Thomas Swierts for their daily support and pleasant lunch breaks. Furthermore, thanks to Peter Roessingh for his steady supervision. Lastly, it should be noted that this bachelor project was facilitated by Naturalis Biodiversity Centre Leiden and the University of Amsterdam. Type preparations were provided by Museum für Naturkunde und der Universität Humbolt zu Berlin, Germany. Other sponge samples were collected by Nicole de Voogd as a result of the Ternate-Halmahera expedition (2009), co-organized by the Research Centre for
Oceanography, PPO-LIPI, Jakarta, Indonesia, and Naturalis.
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