Three Antarctic ascidians from Four Ladies Bank: Cnemidocarpa pfefferi (Michaelsen, 1898), Pyura discoveryi (Herdman, 1910) and Bathypera splendens Michaelsen, 1904.
While Antarctic ascidians (sea squirts) have been studied since the early 19th century, few investigations have been made of ascidians on the east coast of Antarctica in Australian Territory (Fig. 1) (Primo and Vasquez 2009; Schories et al. 2015). The specimens under discussion, Cnemidocarpa pfefferi (Michaelsen, 1898), Pyura discoveryi (Herdman, 1910) and Bathypera splendens Michaelsen, 1904, were identified among holothurians (sea cucumbers) curated at Museums Victoria (NMV) (P Mark O'Loughlin, pers. comm., 21 August 2017). The sample was collected during Voyage 5 (BRAD) 1996/97 by Research Survey Vessel Aurora Australis, in the Marine Benthos Program investigating the Antarctic continental shelf in Prydz Bay (Bardsley 1997; Bathie and Pett 2019a).
Prydz Bay is a deep embayment where the giant drainage system of Lambert Glacier ends at the Amery Ice Shelf (Fig. 2). From its deepest at 700 m in the Amery Depression, the sea floor rises gently to Four Ladies Bank, a shelf bank at a depth of 100-200 m (Mackintosh et al. 2014). Much of this sea floor consists of fine mud and biosiliceous ooze (O'Brien et al. 2014). Most areas of Prydz Bay shallower than 690 m show iceberg ploughmarks (O'Brien et al. 1997), some of which are probably relict features from previous glaciation (Harris et al. 1998), but others may have been freshly made by large modern icebergs (O'Brien et al. 2016). The ascidians described below were collected from the western slope of Four Ladies Bank (Quilty 1997), where sediment of gravelly sandy mud is thickly deposited (Harris et al. 1998). For a note on the naming of Four Ladies Bank see Bathie and Pett (2019b).
Materials and Methods
Specimens were collected by T Bardsley, R Ickeringill and C Hayward on 7 March 1997, from Station number AA97-26, 67[degrees]26.58'S, 76[degrees]38.74'E to 67[degrees]77'S, 76[degrees]38.89'E at a depth of 320 m, using beam trawling from Aurora Australis, Research Survey Vessel for Australian National Antarctic Research Expedition.
Specimens were preserved in 70% ethanol. The accession number is 1997/10.
Two oval specimens, greyish white, pleated test, cross-shaped siphons terminal (Figs 3A, 3C).
Fourteen specimens of various sizes, extended divergent siphons, lumpy tunics with a few adherents and threadlike extensions on the base (Figs 3A, 3B).
Three specimens, siphons widely spaced with flat, slit-like apertures. Tunics free of adherents but apparently covered with very small bumps. Rounded shapes (Fig. 3C).
Internal features were examined using a WILD M5 Heerbrugg dissecting microscope and a Zeiss Axiolab light microscope. Images were captured with a Nikon Coolpix AW110 or an Olympus TG4. Drawings were made from images, notes or reference material. Taxonomic authority: World Register of Marine Species (WoRMS).
The specimens identified belong to the suborder Stolidobranchia, one species from the family Styelidae (simple tentacles, more than one gonad on each side of the body), and two from the family Pyuridae (branched tentacles, only one gonad on each side) (Kott 1985).
The Stolidobranch ascidian
The following description is derived largely from Rocha's Glossary of Tunicate Terminology (2011). Fig. 4A incorporates the features below into a generic ascidian drawn by Kott (1969).
Ascidians (Class Ascidiacea), also known as tunicates or sea squirts, are marine invertebrates that are sessile suspension feeders and usually attached to a substrate. A protective fibrous tunic encases the body and provides the attachment point. Ascidians have two apertures: the branchial siphon draws large quantities of water into the body to filter food, and the atrial siphon is the exit point for waste and for larval dispersal. Siphons, usually divergent, may be close, or distant from each other. Branchial tentacles at the base of the branchial siphon prevent large particles from entering the body, and can be simple or compound (branched) (Fig. 4C). Surrounding the base of the siphons are circular muscle bands, from which longitudinal muscle bands radiate around the body. Water entering the siphon passes through the perforated branchial sac, where food filtration occurs. The order Stolidobranchia is defined by folds in the branchial sac which increase the filtering surface. In Stolidobranchs, the dorsal tubercle is a ciliated funnel opening into a duct connected to the neural gland. It appears in the peritubercular area as a small slit or coiled opening protruding above the branchial sac. Having passed through the branchial tentacles--simple (family Styelidae) or compound (family Pyuridae)--food particles are filtered by ciliated stigmata (perforations) (Fig. 4B) of the branchial sac, gathered by a mucus lining of the grooved endostyle and carried toward the midline of the body. The ciliated gutter of the dorsal lamina then delivers this food to the oesophagus and into the digestive tract. A liver or hepatic gland is present only in families Pyuridae and Molgulidae. Waste is eliminated through the anus (which has either a smooth or lobed margin) into the atrial cavity and then expelled via the atrial siphon. Most ascidians have both male and female gonads, which usually mature at different times to avoid self fertilisation (Kott 1997). Ova or sperm are released through gonoducts into the atrial cavity and released into the water column by the atrial siphon.
Cnemidocarpa pfefferi (Michaelsen, 1898) (Ascidiacea, Stolidobranchia, Styelidae)
The upright oval tunic (grey-white in preservative) is 18 mm high and 10 mm wide, and was attached to a siphon of a different ascidian (Pyura discoveryi). Longitudinal pleats end at cross-shaped apertures (Fig. 5) on short terminal siphons, directed away from each other. The test or outer covering is thin and paper-like, but strong, and almost transparent. The delicate body wall adheres to the test. Simple tentacles arise from a muscular ring around the branchial aperture. A muscular ring is also present around the atrial aperture. The peritubercular margin forms a sharp V. Inrolled horns of the dorsal tubercle form the heart shape described by Michaelsen (1898). There are four branchial folds on each side. Longitudinal vessels, dense on the folds but sparse between them, are folded and convoluted as per Kott (1969). Stigmata of the delicate branchial sac observed were long and narrow. The dorsal lamina is smooth and plain edged (Michaelsen 1898), and notably wider at one end. The oesophagus is long and narrow (Monniot et al. (2011). The stomach has 28 long folds. The wide and simple gut loop, not embedded in the body wall but attached only by ligaments (Monniot et al. 2011), is in this specimen distended, and occupies a large part of the body. Such an apparently swollen gut is visible through the test of the only other specimen. The rim of the conspicuous anus is smooth on one side, with eight paddle-shaped lobes on the other (Fig. 6). There are numerous small (1-2 mm) translucent endocarps on the body wall. There are two gonads on each side.
Unique to this species is a sinuous ovary with short paired lateral branches, the limbs curving towards each other as described by Millar (1960), and showing multiple terminal indentations (Fig. 7).
Pyura discoveryi (Herdman, 1910) (Ascidiacea, Stolidobranchia, Pyuridae)
Smallest 13 x 35 mm, largest 35 x 35 mm. As noted by Herdman (1923), length of the siphon is not necessarily proportional to length of the body. The anterior half of the test is notably free of adherents. Corrugations on the tough yellow-brown tunic form horizontal bands extending up long siphons with terminal four-lobed apertures. In common with other observers, we found no siphonal spines (Millar 1960). Short branchial tentacles have narrow primary and rudimentary secondary branches as per Kott (1969). A convoluted dorsal tubercle is readily visible (Fig. 8). An elongated, or 'serpentine' dorsal tubercle was considered by Herdman to be a remarkable and unmistakable characteristic of the species (1923); argument over the form of the dorsal tubercle was resolved by allowing that it becomes more complex with size or age (Van Name 1945). The dorsal lamina has long languets (tongues). The branchial sac has 13 folds in total, consistent with modern descriptions of Pyura discoveryi (Monniot et al. 2011). Although Herdman (1923) observed only six distinct folds on each side, in small or young specimens a seventh fold may be present but represented by only a few longitudinal vessels (Van Name 1945), and easily overlooked (Kott 1969). We noted mesh with six regular oval stigmata but did not see spiral stigmata at the top of a fold as did Monniot et al. (2011). The gut loop is open with well-developed gonads on both sides of the body, each consisting of rounded masses along both sides of a central duct. The anus is lobed (Monniot et al. 2011) (Fig. 9).
Bathypera splendens Michaelsen, 1904 (Ascidiacea, Stolidobranchia, Pyuridae)
The largest specimen is 65 mm wide and 65 mm high. The test is thin with no adherents and appears to be covered with tiny pimples. Siphons are short, with slit-like apertures distant from and perpendicular to each other (Fig. 10). Inside each slit, on each side, is a row of minute plates projecting into the aperture. Each specimen was attached to the substrate by a small area on the posterior end (Herdman 1923). The body was easy to remove from the test without damage (Monniot et al. 2011). There are six high branchial folds on each side. Stigmata are irregular crescent-shapes of various sizes (Kott 1969), said by Monniot et al. (2011) to form spirals (not observed in this specimen). The small dorsal tubercle, which to us resembled the number 9, accords more closely with the original description--a simple comma shape with a lengthways slit on the right side (Michaelsen 1904) (Fig. 11)--than those of later observers. Muscular fibres forming a crisscross pattern across the body do not reach the ventral line (Monniot et al. 2011), rendering visible the elongated right gonad (Fig. 12). The gut loop occupies the ventral half of the left side (Monniot et al. 2011) (Fig. 13). The left gonad lying within the gut loop consists of a narrow tubular ovary overlaid by two rows of testis lobes (Kott 1969). Rows of endocarps are dorsal to the gut loop and the right gonad but limited to the ventral half of the body (Monniot et al. 2011). The stomach is folded. The inside of each siphon is lined with papillae arranged in curved lines converging at the aperture (Fig. 14). At 400 x magnification, we observed each papilla as a hemisphere of triangular spicules on a short pedestal (Fig. 15). The pimples noted on the outside are the same papillae arranged in horizontal rows of astonishing regularity. The presence of such spicules is diagnostic of Bathypera (Michaelsen, 1904). Monniot et al. (2011) concur that such 'stub-like' spicules, 'with a rounded base, upper side divided into spines of equal size' are characteristic of Bathypera splendens, and distinguish that species from the almost identical Antarctic Bathypera hastaefera Vinogradova, 1962, in which the spines are asymmetrical and few (Fig. 16).
The solitary ascidian test may vary morphologically within as well as between species, and it is frequently necessary to dissect to identify definitively (Kott 1997), even when specimens have been observed in situ, in characteristic habitat. Preserved specimens are often pallid and grotesque versions of living animals. Nevertheless ascidians can usually be distinguished from other invertebrates by the presence and form of incurrent and excurrent siphons. The current specimens, however, had been shelved by external morphology with the Class Holothuroidea (sea cucumbers) and were excluded after dissection (P Mark O'Loughlin, pers. comm, 21 August 2017). The siphons of all three species were misleading--those of Pyura discoveryi in length, shape and orientation, and those of Bathypera splendens with barely visible slits instead of multilobed apertures. The larger Cnemidocarpa pfefferi, with barely discernible siphons, had been taken for another Bathypera splendens, and the smaller was a nondescript epibiont of Pyura discoveryi.
Cnemidocarpa pfefferi (Michaelsen, 1898)
These specimens look more like dim sims than animals (Fig. 5). If, after the identification of terminal anterior siphons, Cnemidocarpa had been anticipated, the most likely upright candidate for NMV243197 would have been Cnemidocarpa verrucosa (Lesson, 1830). Observed on a wide range of substrates at shallow or bathyal depths and in a variety of shapes and colours (Brueggeman 1998), C. verrucosa is the most abundant and conspicuous of the genus, found in all Antarctic and sub-Antarctic waters, and the best-studied (Sahade et al. 2004). However, once the tunic was breached, the distinctive gonads of Cnemidocarpa pfefferi were visible through the body wall and conspicuous at incision.
Indentations in the ovarian branches hold the testis ducts, which instead of lengthening as the ovary extends, are pulled tighter across the extension, causing grooves and eventually forming the double branches through which the testis ducts reach the vas deferens on the mesial surface of the ovary (Kott 1969) (Fig. 7). The testis and ovary lie within a common membrane, characteristic of Cnemidocarpa (Millar 1960). The largest reported specimens of Cnemidocarpa pfefferi, at 55 mm high and 22 mm wide, are still those examined by Kott (1969) and found at depths up to 383 m. Slightly smaller specimens have been taken at 770 m (Monniot et al. 2011). This species is widely distributed in Antarctic waters. The genus was originally Styela Fleming, 1822, and S. pfefferi Michaelsen, 1898, one of several species characterised by 'immense' development of ovarian tubes (Kott 1969), distinguished from S. wandeli (Sluiter 1911), which has unusually large testis lobes (Kott 1969).
Pyura discoveryi (Herdman, 1910)
Pyura discoveryi was originally assigned to the genus Halocynthia, and named for the ship Discovery, of the British National Antarctic Expedition 1901-1904 (Herdman 1910). Pyura discoveryi is widely distributed around Antarctica. In various habitats, from rocks at a depth of 200 m to aggregations in ooze at 700 m, individuals attach to the substrate and to each other by irregular surfaces (Millar 1960) and the thread-like processes we observed on the sides of the tunic (Monniot et al. 2011) (Fig. 3 A). Aggregation increases stability on soft sediments, desirable where currents are strong, and increases substrate available to other sessile invertebrates, including other ascidians. Pyura discoveryi has often been observed as an epibiont on Pyura setosa (Sluiter, 1905) (Tatian et al. 1998), and one of our specimens supported a tiny Cnemidocarpa pfefferi.
Although aggregated solitary ascidians do not interact with each other, proximity is advantageous, increasing the likelihood for fertilisation in fast currents that carry gametes away (Kott 1997). The non-feeding larvae, which develop rapidly, have been found to metamorphose faster in response to chemical signals in the water column from the same species, and to settle quickly around adults (Segelken-Voigt et al. 2016). This early life history of ascidians may account in part for the surprisingly patchy and sparse distribution of Antarctic ascidians, noted by Kott (1969) in the few images then available of ascidians in situ, and confirmed recently by studies employing photographic transects of the sea floor rather than the beam trawl (Segelken-Voigt et al. 2016). The latter is known to drag together individuals or small aggregations that may have been widely separated, on substrates that differ considerably, or to represent as unusual a species that was abundant nearby (Monniot et al. 2011). Photo transect methods, on the other hand, which depend on counting specimens in images, are known to underestimate abundances of invertebrates (Sahade et al. 1998). It would be less likely that the small Cnemidocarpa pfefferi attached to Pyura discoveryi would be identified.
Density of benthic filter-feeding invertebrate communities is indicative of abundant plankton in the water layer close to the bottom (Monniot et al. 2011). Melting of sea ice in summer causes high phytoplankton blooms that descend through the water column, forming a major food source (Segelken-Voigt et al. 2016). For sessile animals unable to collect food once it has fallen to sediment surfaces, another major resource is resuspended benthic material (Kowalke et al. 2001). Containing organic detritus, including benthic diatoms such as Fragilariopsis kerguelensis (O'Meara) Hustedt, 1952, abundant at Four Ladies Bank (Quilty 1997), sediment is disturbed by meltwater from the iceshelf, and in the shallow water, by drifting and grinding icebergs. However, loose sediment is also a threat to filter feeders; clogging of branchial apertures and the stigmata of the branchial sac can be fatal (Segelken-Voigt et al. 2016). Ascidians have few defences, the ability to squirt being the most obvious one. Circular muscles regulate the size of the siphonal apertures; contractions of the body muscles compress the body, forcing jets of water out from the siphons (Ruppert et al. 2003). Studies in western Antarctica have found that Cnemidocarpa verrucosa (and possibly C. pfefferi) can increase their rate of squirting. Ascidians whose habit is to lie flat on a side (e.g. phlebobranch Ascidia challengeri Herdman, 1882) survive periods of turbulent sediment by reducing filtering efficiency (Torre et al. 2014). In some species, individuals benefit from a flexible stalk raising them above the turbulence (Segelken-Voigt et al. 2016). In Pyura discoveryi, a lengthened or heightened branchial siphon may be above or turned away by onrushing sediment (see Fig. 45 in Millar 1960), while the atrial siphon projects effluent above the sediment, minimising its own contribution to disturbance (Kott 1969). Some P. discoveryi individuals have siphons quadrangular in section, with deep grooves running along them, a feature apparently unique to this species (Herdman 1923). Other siphons narrow towards the apertures. In either case, compared with those of most solitary ascidians, the siphons are longer in proportion to the bodies even when retracted, and neither the lengths of the siphons relative to the bodies nor their orientations are consistent. Siphonal growth and orientation is a response to the environment (Kott 1997); usually the terminal branchial siphon faces the oncoming current and the dorsal atrial siphon points the other way. This is achieved by differential growth in the siphons in the optimal direction for the individual, some compensation for the inability to move towards potential food (Kott 1997), and we noted siphons pointing horizontally or downwards as well as straight upwards.
An individual P. discoveryi can look much like the holothurian Ypsilothuria bitentaculata (Ludwig, 1893), found at Ningaloo Reef off Western Australia (Byrne and O'Hara 2017). An even more convincing image, of a Mediterranean specimen of this echinoderm with oral and anal siphons, can be seen in Mecho et al. (2014). Somewhat paradoxically, fixed positions in preserved specimens of P. discoveryi can obscure the small range of movement crucial to sessile ascidians, which rapidly and vigorously contract in response to unwanted stimuli. The water of Prydz Bay constantly carries large inorganic particles of glacial origin, which must be filtered out before reaching the branchial sac (Kowalke et al. 2001). In addition to the feathery branched pyurid branchial tentacles, at the base of each siphon is a projecting membrane with a strong ring of muscle, considered by Kott to be a sphincter to close the aperture, and perhaps a safety mechanism in view of the length of the siphon (Kott 1969).
The most similar species to Pyura discoveryi is Pyura haustor (Stimpson 1864), once known only from the Arctic and proposed by Kott (1969) as an example of bipolarity More recently, this species has been found from Alaska to California. Pyura haustor differs in having siphonal spines (Sanamyan and Sanamyan 2006).
Bathypera splendens Michaelsen, 1904
A most remarkable and ornamental genus, according to Herdman (1923), living Bathypera are said to resemble antique beaded purses (Young and Vasquez 1995). Few have been observed in situ. From a manned submersible in Saanich Inlet, British Columbia, these animals appeared brilliantly white and delicate (Fig. 17). Bathypera feminalba Young and Vasquez, 1995 (named for the dive site locally called White Lady Rock), like Bathypera hastaefera Vinogradova, 1962, is separated from Bathypera splendens only by the shape of the spicules on the papillae (Young and Vasquez 1995).
Although the Bathypera test is thin, the magnesium calcite spicules (Lowenstam 1989) are rough to the touch (Millar 1960), and when siphons are retracted, form the barrier across the aperture. Lowenstam (1989) speculated that this may deter invertebrates known to live commensally with other ascidians; it was ineffective against the amphipod and polychaete inside our specimens. Young and Vasquez (1995) demonstrated in their study of juveniles that each spicule begins as a tiny round crystal on the margin of the tunic as the animal grows. They observed no Bathypera with epibionts of any kind, and noted that juveniles were found only around the base of adults, never on them. We investigated one of 16 circular (3 mm in diameter) white patches on the test of B. splendens. A raised thick border of spicules formed the circle, and within were sparse rows of broken spicules surrounded by detritus. Many spicules were missing, leaving behind circular depressions in the regular rows. This may represent unsuccessful predation--tunics of Antarctic Bathypera hold repellent chemical substances (Moles et al. 2015)--or senescence. The lifespan of solitary ascidians is not well documented; one to three years is frequently suggested, and some Antarctic species with slower growth rates may exceed this. Flat species are said to live longer than erect ones such as Bathypera (Kowalke et al. 2001).
Bathyspera splendens, the first of the genus to be described, is eurybathic and found throughout Antarctica. It was initially assigned to the Molgulidae; curved stigmata of the branchial sac are not oriented longitudinally as in most pyurids. However, there is no renal sac characteristic of molgulids. Early observers may have taken endocarps for renal organs (Van Name 1945); the function of endocarps, however, is still not understood, although they may have some role in excretion (Kott 1985) or reproduction (Sahade et al. 2004; Kott 2005).
The other two Bathypera species are B. ovoida (Ritter, 1907), collected from the Pacific Ocean (at a depth of 184 m off Japan, and 3680 m off California) (Young and Vasquez 1995), and Bathypera goreaui Millar and Goodbody, 1974, known only from a reef near Discovery Bay, Jamaica (Millar and Goodbody 1974). These differ obviously from B. splendens and B. feminalba in that the siphonal apertures point the same way. Again the shape of the spicules on the papillae is characteristic; as is the number of branchial folds (Van Name 1945). Some past controversy can be attributed to deterioration of spicules when specimens had been preserved in unbuffered formalin (Lowenstam 1989). New, Bathypera species, or the expansion of known geographical distributions, may result from sampling of abyssal depths around the globe, and as scuba divers report from shallower water than has previously been sampled in the Antarctic (Schories et al. 2015).
Unlike P. discoveryi with its hair-like projections enabling it to anchor in silt, B. splendens attaches to the substrate by a smooth posterior surface patch. In Saanich Inlet, B. feminalba was dredged from shell rubble or stony bottoms, but never from soft sediments; likewise B. goreaui. B. feminalba was observed to be most abundant on vertical cliffs. Young and Vasquez (1995) concluded that B. feminalba thrives on hard surfaces where currents are gentle.
Trawls of Four Ladies Bank were likely to encounter thick sediment and strong currents (Harris et al. 1998). We note, however, that much of the sandy or muddy bottom investigated off Terre Adelie (eastern Antarctica) contained large angular pebbles, on which ascidians had settled (as they had on other sessile animals like sponges or tubeworms) (Monniot et al. 2011). Among unregistered ascidians from Prydz Bay (1991, 1993) awaiting investigation at Museums Victoria are several specimens we now judge to be B. splendens, along with numerous P. discoveryi--conditions suitable for both these species had persisted over several years.
Our task was to examine some marine invertebrates from Prydz Bay noted 'not holothurian'. We identified three species of solitary Stolido-branch ascidians, not previously recorded as present in Museums Victoria's survey collection: Cnemidocarpa pfefferi, Pyura discoveryi and Bathypera splendens. These species are poorly represented in Australian zoological online catalogues, and the records largely represent collections made in the 1930s; the few recent additions are from the 2008 CEAMARC survey. This may be attributed to the scale of the task of digitising records, but the absence of relevant literature indicates otherwise. Our investigation suggests that there are ascidians collected from Australian Antarctic Territory waiting to be examined.
Thank you to Museums Victoria's Collection Manager Melanie Mackenzie for making these specimens available to us and facilitating the investigation. Thank you to Barbara Hall (FNCV Marine Research Group) who had found for us records of Antarctic ascidians long before we knew we needed them. We are grateful to staff of the Marine Invertebrate Laboratory for use of work space, computer and microscopes, and to Leon Altorr and Platon Vafiadis (both MRG) for assistance with map reproduction and advice on images, respectively. Thanks also to Katie Shoemaker for expediting permissions for the Bathypera feminalba image, courtesy of Ocean Networks Canada. We are grateful to the editors of The Victorian Naturalist for their helpful comments on the manuscript.
Bardsley TM (1997) Marine Benthos Program--Preliminary Report. In Voyage Leader's Report. Voyage 5 1996/97. 28 January - 29 March, 1997. Aurora Australis. Attachment 3. Voyage Leader P Quilty (Australian Antarctic Data Centre: Data management and spatial data service) <https://data.aad.gov.au/aadc/voyages/display_voyage.cfm?set_code=199697050> [Accessed 27 September 2017]
Bathie C and Pett J (2019a) Notes on the ascidian component of a marine benthos survey in Australian Antarctic Territory. The Victorian Naturalist 136, 16-20.
Bathie C and Pett J (2019b) The four ladies of Prydz Bay: Notes on the naming of a submarine formation featuring in surveys of marine benthos in Australian Antarctic Territory. The Victorian Naturalist 136, 45-47.
Brueggeman P (1998) Chordata:Tunicata. Ascidians/tunicates. Underwater Field Guide to Ross Island and Mc-Murdo Sound, Antarctica. (National Science Foundation Office of Polar Programs. United States Antarctic Program), <http://www.peterbrueggeman.com/nsf/fguide/> [Accessed 04 December 2017]
Byrne M and O'Hara T (Eds) (2017) Australian Echinoderms. Biology, Ecology and Evolution (CSIRO Publishing: Clayton, Victoria)
Harris PT, Taylor F, Pushina Z, Leitchenkov PE, O'Brien PE and Smirnov V (1998) Lithofacies distribution in relation to the geomorphic provinces of Prydz Bay, East Antarctica. Antarctic Science 10, 227-235.
Herdman WA (1910) Tunicata. In National Antarctic expedition (ship 'Discovery'), 1901-1904, Natural History 5, 1-26. cited in WoRMS Editorial Board (2018) World Register of Marine Species. doi:10.14284/170
Herdman WA (1923) Ascidiae Simplices. Australasian Antarctic Expedition 1911-14. Scientific Reports. Series C: Zoology and Botany. Vol. 3, Part III. (Government Printer: Sydney)
Kott P (1969) Antarctic Ascidiacea. Monographic account of the known species based on specimens collected under U.S. government auspices, 1947-1965. Antarctic Research Series Volume 13. (American Geophysical Union: Washington)
Kott P (1985) The Australian Ascidiacea Part 1. Phlebo-branchia and Stolidobranchia. Memoirs of the Queensland Museum 21, 1-440.
Kott P (1997) Tunicates (Sub-Phylum Tunicata). In Marine Invertebrates of Southern Australia Part III, pp. 1092-1255. Eds S Shepherd and M Davies (South Australian Research and Development Institute [Aquatic Sciences]: Richmond, SA)
Kott P (2005) Catalogue of Tunicata in Australian Waters. (Australian Government Department of Environment and Heritage: Canberra)
Kowalke J, Tatian M, Sahade R and Arntz W (2001) Production and respiration of Antarctic ascidians. Polar Biology 24, 663-669. doi 10.1007/s003000100266.
Lowenstam HA (1989) Spicular morphology and mineralogy in some Pyuridae (Ascidiacea). Bulletin of Marine Science 45, 243-252.
Mackintosh AN, Verleyen E, O'Brien PE, White DA, Jones RS, McKay R, Dunbar R, Gore DB, Fink D, Post AL, Miura H, Leventer A, Goodwin I, Hodgeson DA, Lilly K, Crosta X, Golledge NR, Wagner B, Berg S, van Ommen T, Zwartz D, Roberts SJ, Vywerman W and Masse G (2014) Retreat history of the East Antarctic Ice Sheet since the Last Glacial Maximum. Quaternary Science Reviews 100, 10-30. http://dx.doi.org/10.1016/j.quascirev.2013.07.024
Mecho A, Billett D, Ramirez-Llodra E, Aguzzi J, Tyler P and Company J (2014) First records, rediscovery and compilation of deep-sea echinoderms in the middle and lower continental slope of the Mediterranean Sea. Scientia Marina 78, 281-302. doi: <http://dx.doi.org/10.3989/scimar.03983.30C>
Michaelsen W (1898) Vorlaufige Mittheilung uber einige Tunicaten aus dem Magalhaensischen Gebiet, sowie von Sud-Georgien. Zoologischer Anzeiger 21, 363-371 <http://www.biodiversitylibrary.org/item/37581> [Accessed 07 December 2017]
Michaelsen W (1904) Die stolidobranchiaten Ascidien der deutschen Tiefsee Expedition 1898-1899. In Wissenschaftliche Ergebnisse der Deutschen Tiefsee Expedition auf dem dampfer 'Valdivia' 1898 - 1899. Volume 7, Part 2. pp. 181-260. Ed. C Chun (Fischer: Jena, Germany) <http://www.biodiversitylibrary.org/page/6308044#page/311/mode/1up> [Accessed 08 September 2017]
Millar RH (1960) Ascidiacea. Discovery Reports. Vol. 30, 1-160. (Cambridge University Press: Cambridge)
Millar RH and Goodbody I (1974) New species of Ascidians from the West Indies. Studies on the Fauna of Curacao and other Caribbean Islands 148, 142-161. <http://www.repository.naturalis.nl/document/549830> [Accessed 03 September 2017]
Moles J, Nunez-Pons L, Taboada S, Figuerola B, Cristobo J and Avila C (2015) Anti-predatory chemical defences in Antarctic benthic fauna. Marine Biology 162, 1813-1821. doi 10.1007/s0027-015-2714-9.
Monniot F, Dettai A, Eleaume M and Cruaud C (2011) Antarctic Ascidians (Tunicata) of the French Australian survey CEAMARC in Terre Adelie. Zootaxa 2817, 1-54.
O'Brien PE, Beaman R, De Santis L, Domack EW, Escutia C, Harris PT, Leventer A, McMullen K, Post A, Quilty PG, Shevenell AE and Batchelor CL (2016) Submarine glacial landforms on the cold East Antarctic margin. Geological Society, London, Memoirs 46, 501-508. https://doi.org/10.1144/M46.172
O'Brien PE, Harris PT, Post AL and Young N (2014) East Antarctic continental shelf: Prydz Bay and the Mac. Robertson Land Shelf. Geological Society, London, Memoirs 41, 241-254. doi: 10.1144/M41.18
O'Brien PE, Leitchenov G and Harris PT (1997) Iceberg Plough Marks, Subglacial Bedforms and Grounding Zone Moraines in Prydz Bay Antarctica. In Glaciated Continental Margins: An Atlas of Acoustic Images, pp. 228-231. Eds TA Davies, T Bell, A Cooper, H Josenhans, L Polyak, A Solheim, MS Stoker and JA Stravers (Springer: Netherlands). (eBook) doi: 10.1007/978-94-011-5820-6.
Ocean Networks Canada. 2012. New species revealed in our backyard. <https://www.oceannetworks.ca/new-species-revealed-our-backyard.> [Accessed 5 December 2017]
Primo C and Vazquez E (2009) Antarctic ascidians: an isolated and homogeneous fauna. Polar Research 28, 403-414.
Quilty P (1997) Voyage Leader Report-Voyage 5 1996/97 1996/97. 28 January - 29 March, 1997 Aurora Australis. Australian Antarctic Data Centre, <https://data.aad.gov.au/aadc/voyages/display_voyage.cfm? set code=199697050> [Accessed 27 September 2017]
Rocha R (2011) Glossary of Tunicate Terminology. Smithsonian Tropical Research Institute <www.stri.si.edu/sites/taxonomy_training/future_courses/Biological_glossary_Tunicates.html> [Accessed 2 December 2017]
Ruppert E, Fox R and Barnes R (2003) Invertebrate Zoology. A Functional Evolutionary Approach. 7 edn. (Cengage Learning: Boston, US)
Sahade R, Tatian M, Kowalke J, Kuhne S and Esnal GB (1998) Benthic faunal associations on soft substrates at Potter Cove, King George Island, Antarctica. Polar Biology 19, 85-91.
Sahade R, Tatian M and Esnal GB (2004) Reproductive ecology of the ascidian Cnemidocarpa verrucosa at Potter Cove, South Shetland Islands, Antarctica. Marine Ecology Progress Series 272, 131-140.
Sanamyan K and Sanamyan N (2006) Deep-water ascidians (Tunicata: Ascidiacea) from the northern and western Pacific. Journal of Natural History 40, 307-344. doi: 10.1080/00222930600628416.
Schories D, Sanamyan K, Sanamyan N, Diaz MJ, Garrido I, Heran T, Holzhauer J and Kohlberg G (2015) Geographic ranges of ascidians from Antarctica and the southeastern Pacific. Advances in Polar Science 26, 8-23. doi: 10.13679/j. advps.2015.1.00008
Segelken-Voigt A, Bracher A, Dorschel B, Gutt J, Huneke W, Link H and Piepenburg D (2016) Spatial distribution patterns of ascidians (Ascidiacea: Tunicata) on the continental shelves off the northern Antarctic Peninsula. Polar Biology 39, 863-879. doi 10. 1007/s00300-016-1909-y
Tatian M, Sahade R, Doucet M and Esnal G (1998) Ascidians (Tunicata, Ascidiacea) of Potter Cove, South Shetland Islands, Antarctica. Antarctic Science 10, 147-152.
Torre L, Abele D, Lagger C, Momo F, and Sahade, R (2014) When shape matters: Strategies of different Antarctic ascidians morphotypes to deal with sedimentation. Marine Environmental Research 99, 179-187.
Van Name WG (1945) The North and South American Ascidians. Bulletin of the American Museum of Natural History. 84, 1-476.
WoRMS Editorial Board (2018) World Register of Marine Species. doi:10.14284/170.
Young CM and Vasquez E (1995) Morphology, larval development, and distribution of Bathypera feminalba n. sp. (Ascidiacea: Pyuridae), a deep-water ascidian from the fjords and sounds of British Columbia. Invertebrate Biology 114, 89-106.
Carol Bathie and Janet Pett
Marine Research Group, Field Naturalists Club of Victoria Volunteers, Marine Invertebrates, Museums Victoria Email: firstname.lastname@example.org; email@example.com
Received 2 February 2018; accepted 15 November 2018
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|Author:||Bathie, Carol; Pett, Janet|
|Publication:||The Victorian Naturalist|
|Date:||Feb 1, 2019|
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