Southern range extensions for twelve heterobranch sea slugs (Gastropoda: Heterobranchia) on the eastern coast of Australia

Abstract

Port Stephens, on the central New South Wales coast, provides ideal oceanographic and benthic conditions for the settlement and growth of larvae of tropical species delivered from the north by the East Australian Current. The popularity of the bay for recreational and scientific diving has facilitated extensive documentation of the biota over several decades, confirming its high biodiversity. Of the 313 species of heterobranch sea slugs recorded from Port Stephens to date, 30 are not known to occur further south. Our observations increase the number of taxa with a southern distribution limit at Port Stephens by 12 species and add to a growing list of marine taxa that are progressively extending their southern range, potentially as a result of climate change.

Introduction

Heterobranch sea slugs (hereafter simply sea slugs) are predominantly tropical marine animals that, on the eastern Australian coast, exhibit a latitudinal gradient with rapid attenuation of species diversity from more than 1,000 species in the northern Great Barrier Reef (GBR) to approximately 500 in central New South Wales (NSW) (Rudman & Willan, 1998). The southward flow of the East Australian Current (EAC) brings warm water from tropical latitudes to the Tasman Sea (Booth et al., 2007; Malcolm et al., 2010) and with it planktonic larvae (Booth et al., 2007; Malcolm et al., 2010). With increasing latitude, the current moves offshore and generates eddies (mostly in summer) that deliver an intermittent supply of these tropical larvae to the central and southern NSW coast (Burn, 2006).

South-eastern Australia is a recognised climate change ‘hot-spot’ (Hobday & Lough, 2011) where strengthening of the EAC and increasing water temperature may facilitate the arrival and establishment of novel species that may alter species interactions (Underwood & Chapman, 2007). In this area, southward shifts in distribution are anticipated for many marine organisms (Przeslawski et al., 2008), with range extensions already documented for some species of fishes (Figueira & Booth, 2010; Harasti, 2015), scleractinian corals (Baird et al., 2012), sea slugs (Nimbs et al., 2015), and host anemones and their complement of commensal crustaceans (Scott et al., 2015). New species records will come about through greater intensity of observations (sea slugs are inherently rare in time and space - Marshall & Willan, 1999) and as a result of range shifts due to warming conditions. Those changes resulting from warming seas have important implications for marine conservation management particularly for species with a very restricted range (O’Hara 1995).

Comprehensive data on the occurrence of a range of marine organisms tend to be confined to locations near major population centres due primarily to the proximity of research facilities (Smith 2005, 2008a, b; Burn, 2006). For this reason, species lists for the central NSW coast, especially adjacent to Sydney, are comprehensive, particularly for fishes (Gladstone, 2007; Morton & Gladstone, 2011; Harasti et al., 2015). The occurrence and distribution of sea slugs is also well known, however to record range extensions reliably, it is imperative that observations of any taxa not previously recorded in an area are thoroughly documented.

The Port Stephens–Great Lakes Marine Park encompasses 98,000 ha of coastal and shelf waters between Cape Hawke and Birubi Beach, incorporating the extensive Port Stephens embayment (Fig. 1). Within the marine park, varying oceanographic conditions, sea bed topography and sessile assemblages contribute to a high species diversity that is a mixture of tropical, subtropical and temperate flora and fauna (DECCW, 2010, Smith et al., 2010). Being close to Newcastle, the second largest city in NSW, and with easy access for SCUBA divers and watercraft, the biotic and abiotic aspects of Port Stephens have been well studied (e.g. Harasti et al., 2014; Poulos et al., 2015; Davis et al., 2015).

Fig. 1

Map of Port Stephens eastern basin with dive sites indicated. Shading represents land

Many sea slug species of tropical origin are regularly observed in Port Stephens where conditions are conducive for the settlement of veliger larvae that may have travelled considerable distance on the EAC. In this paper, observations of 12 sea slug species are recorded at significant distances (at least 300 km) south of their previously reported southern limit. Coastal lagoons and estuaries provide sheltered locations for successful settlement and growth of more tropically adapted marine organisms (Willan et al., 1979) and accessible, safe diving conditions. These factors, combined with the increasing popularity of diving-based citizen science activities in the region (e.g. Smith & Edgar, 2014 and the current Sea Slug Census program) increase the likelihood that additional species will not only occur in the region, but also that they have a reasonable probability of being found.

Materials and methods

Port Stephens is a large, drowned river valley fed by two major, eastward-flowing rivers, the Karuah and the Myall, and comprises two basins that exhibit differences in substrate and hydrodynamics. The marine-influenced eastern basin is characterised by a complex of channels and shoals formed by the influence of strong tidal flows (Vila-Concejo et al., 2007) with a diverse range of marine habitats (Davis et al., 2015). A narrow entrance and elevated shoreline to the south-east provide considerable protection from the effects of strong southerly winds and large ocean swells. The tidal range in the sheltered port is approximately 1.4 m (Creese & Wales, 2009) and the average depth is 14 m (Poulos et al., 2015).

Organic input from rivers and tidal flow contribute considerable volumes of food to support suspension-feeding organisms such as sponges, ascidians, octocorals and hydroids (Smith 2008a, b; Smith et al., 2010). These organisms, in turn, provide food and habitat for a diverse assemblage of sea slugs. Several popular shore-dive sites, noted for their diverse invertebrate life and opportunities for macro-photography, are located on the southern shoreline of the eastern basin, centered around Nelson Bay (32°42′54″S 152°9′01″E) (Fig. 1).

The ‘Pipeline’ supports a mixed habitat comprising rocky reef with large macrophytes and sandy sediments with seagrasses, sponges and octocorals (Harasti & Gladstone, 2013). ‘Seahorse Gardens’ is 900 m east of the ‘Pipeline’ and supports octocoral colonies situated in sandy substrate with sponges located in deeper areas (Harasti et al., 2014). ‘Fly Point’ lies to the east of ‘Seahorse Gardens’ within a sanctuary (no take) zone that has been protected since 1983. Situated on a prominent point, this site has complex topography including a series of substantial ledges at various depths. While many habitats are similar to those at ‘Pipeline’, there are extensive areas of large sponges in the deeper sections (to 24 m) (Coleman and Marsh 1997). ‘Little Beach’ is 450 m east of ‘Fly Point’ and comprises sandy substrate interspersed with seagrasses, sponges and gorgonians (Harasti et al., 2014).

Observations of sea slugs were made between 2009 and 2015 using SCUBA at the four dive sites. Many observations were made during recreational diving activities, as incidental sightings whilst undertaking other research or as part of broader research projects carried out by TRD and ML. Other observations were made as part of a Southern Cross University (SCU)/Combined Hunter Underwater Research Group (CHUG) citizen-science project to document the diversity of sea slugs at three-monthly intervals over a two-year period (the Sea Slug Census).

Records of all species of sea slugs were collated from the authors’ databases as well as from extensive photographic material from key underwater photographers. Species observations that had been reported online (in Nudi Pixel or the Sea Slug Forum) were considered as published observations.

Results

Systematics

• Order CEPHALASPIDEA Fischer, 1887

• Family AGLAJIDAE Pilsbry, 1895 (1847)

• Genus Philinopsis Pease, 1860

• Philinopsis orientalis (Baba, 1949)

• Synonym: Aglaja orientalis Baba, 1949

This distinctive aglajid was originally named Aglaja orientalis by Baba (1949) from specimens found off Kurosaki and Hayama in Sagami Bay, Japan. Baba expressed doubts about that generic location in correspondence with RCW. It was recently transferred into the genus Philinopsis (Camacho-García et al. 2013). Since then, it has been found at several locations throughout the Indo-Pacific including La Reunion and New Caledonia (Rudman, 2003f). It is distinguished by the presence of numerous scattered white spots and areas of opaque white marks containing smaller yellow lines and spots that form a line across the head and transversely across the mid-notum, and a patch on the tail (Gosliner et al., 2008, p. 42). In Australian waters, there are published records of P. orientalis from Rottnest Island, WA (Wells & Bryce, 2000, p. 31–32) and from the (northern) GBR (Marshall & Willan, 1999, p. 171) (Table 1). An observation of a 15 mm specimen at 8 m depth on 14 February, 2015 at ‘Fly Point’ (Fig. 2a) extends the east coast range for this species by 2,246 km to central NSW.

Table 1 Selected records of Philinopsis orientalis from Australian waters

Fig. 2

a. Philinopsis orientalis. Fly Point, 14 February, 2015. b. Jorunna ramicola. Pipeline, 30 November, 2013. c. Thordisa tahala. Little Beach, 15 January, 2015. d. Marionia pustulosa. Seahorse Gardens, 7 March, 2015. Photos: a, Matt Doyle; b, c, Tom Davis; d, Kristine O’Keefe

• Order NUDIBRANCHIA Cuvier, 1817

• Family DISCODORIDIDAE Bergh, 1891

• Genus Jorunna Bergh, 1876

• Jorunna ramicola M. C. Miller, 1996

Jorunna ramicola was described first from New Zealand (Miller, 1996); however, it has subsequently been found widely in the Indo-Pacific Ocean with a distribution that includes Madagascar, Japan, Philippines and Papua New Guinea (Camacho-García & Gosliner, 2008; Gosliner et al. 2008) (Note that this assumption of a single species has not been tested genetically and species of Jorunna are notoriously difficult to identify morphologically). As with many discodorids, this species exhibits protective resemblance (Behrens et al., 2005) by mimicking the surface pattern and colour of its host sponge (Callyspongia) and is thus well camouflaged. In Australia, this species has been recorded several times from subtropical QLD and northern NSW (Table 2). Prior to our observation of a 12 mm individual at 6 m depth from the ‘Pipeline’ on 30 November, 2013 (Fig. 2b), the southernmost record of J. ramicola was at Hastings Point, NSW, on 27 April, 2010 (Riek, 2013a). The Nelson Bay record extends the range south by 500 km.

Table 2 Records of Jorunna ramicola from Australian waters

• Genus Thordisa Bergh, 1877

• Thordisa tahala Chan & Gosliner, 2007

The original description of Thordisa tahala was based on descriptions from preserved specimens from Madagascar, Indonesia and the Marshall Islands (Chan & Gosliner, 2007), indicating a wide Indo-Pacific distribution (Gosliner et al., 2008). The specific name was derived from Malagasy (tahala = ridge) for the network of raised ridges on the dorsum and, in conjunction with its colour, the network pattern distinguishes T. tahala from any other species within the genus (Chan & Gosliner, 2007). The previously known range of T. tahala in Australian waters was a 210 km section of coast from the Gneering Shoals in southern QLD to the Brunswick River, NSW (Table 3). This observation on 22 January, 2015 of a 60 mm specimen (Fig. 2c) at 8 m depth, at night, from ‘Little Beach’ extends the east coast range for this species by 480 km.

Table 3 Records of Thordisa tahala from Australian waters

• Family TRITONIIDAE Lamarck, 1809

• Genus Marionia Vayssière, 1877

• Marionia pustulosa Odhner, 1936

Marionia pustulosa is a moderately large sea slug which, when amongst its host octocoral, is camouflaged using a complex pattern of reticulated lines, various muted colours and many elevated papillae on its dorsum, oral veil and rhinophoral sheaths. This dendronotid nudibranch appears endemic to Australia and was first described by Odhner from a specimen sourced from Port Curtis, QLD, in 1929 and later redescribed by Thompson (1972) using a live specimen found in Moreton Bay, QLD, in 1972. It has been recorded from Dampier, WA, Noosa, QLD (Coleman, 2008), and North Solitary Island, NSW (Australian Museum, 1989), amongst other locations (Table 4). This species was photographed by Carol Buchanan in Nelson Bay in March 1988 and again in March 1996; however, these observations remained unpublished. Those earlier observations, and another of a 35 mm specimen (Fig. 2d) in 6 m of water at ‘Seahorse Gardens’ on 7 March, 2015 increase the southern range of M. pustulosa by 332 km.

Table 4 Records of Marionia pustulosa from Australian waters

• Family TERGEPEDIDAE Bergh, 1889

• Genus Trinchesia Ihering, 1879

• Trinchesia ornata (Baba, 1937)

• Synonyms: Catriona ornata (Baba, 1937), Cuthona ornata Baba, 1937

Trinchesia ornata is recognised by its orange body with blue and yellow cerata (Gosliner et al., 2008) and by its obligate predation of thecate hydroids (Gosliner, 1987; Marshall & Willan, 1999). Although originally described from Tomioka in Japan (Baba, 1937), its range extends from South Africa (Gosliner, 1987, pp. 20, 116), La Réunion (Nudi Pixel, 2011d) to Japan, Hong Kong (Gosliner et al., 2008), Indonesia, Thailand, Philippines, Palau (Nudi Pixel, 2011e) and Australia (Marshall & Willan, 1999; Coleman, 2008). In Australia, T. ornata has previously been recorded from various locations from Heron Island in the southern GBR to Byron Bay, NSW (Table 5). It is rather difficult to see underwater, but is assumed to be quite common. On 8 December, 2013 a 5 mm specimen was observed at ‘Little Beach’ on rocky reef at 8 m deep (Fig. 3a), 475 km south of its previously reported southernmost distributional limit.

Table 5 Records of Trinchesia ornata from Australian waters

Fig. 3

a. Trinchesia ornata. Little Beach, 8 December, 2013. b. Trinchesia puellula. Little Beach, 11 September, 2013. c. Facelina rhodopos. Little Beach, 15 December, 2014. d. Sakuraeolis nungunoides. Fly Point, 23 August, 2013. Photos: a, b, c, Tom Davis; d, Nicola Davis

• Trinchesia puellula Baba, 1955

• Synonyms: Cratena puellula Baba, 1955, Catriona puellula (Baba, 1955), Cuthona puellula (Baba, 1955)

Baba (1955) described this species from a single 10 mm animal from Hayama, Sagami Bay, Japan. It is characterised by the presence of orange markings on both the rhinophores and oral tentacles, vertical white lines on the cerata, and the black speckled appearance of the digestive gland within the cerata (Rudman, 2002d). It was later reported from California (Marcus, Er. 1961) and then from Australia in 2008 at Gneering Shoals, QLD (Table 6), implying a broad distribution across the Pacific Ocean, most likely facilitated by shipping. Little is known of the biology and ecology of this species with few observations recorded outside Japanese waters. Our recent observation of a 5 mm specimen on sand at ‘Little Beach’ on 11 September, 2013 at 7 m depth constitutes a southward range extension of 680 km (Fig. 3b).

Table 6 Records of Trinchesia puellula from Australian waters

• Family FACELINIDAE Alder & Hancock, 1855

• Genus Facelina Alder & Hancock, 1855

• Facelina rhodopos Yonow, 2000

• Synonym: Pruvotfolia rhodopos (Yonow, 2000)

This aeolid has an Indo-Pacific distribution from the Red Sea (Yonow, 2000), through La Réunion (Bidgrain, 2006), Kenya, Philippines, Indonesia (Nudi Pixel, 2011a) and Malaysia (Rudman, 2002a) to Australia. Facelina rhodopos bears clusters of cerata tipped with pink/peach rings and an opaque longitudinal metapodial line which are diagnostic of the species (Yonow, 2000). In Australian waters, it has been found in the northern GBR at Lizard Island, QLD, and in northern NSW from Hastings Point and Sandy Beach (Table 7). On 15 December, 2014 at ‘Little Beach’, we observed a 15 mm specimen at 7 m depth on a rocky reef (Fig. 3c) at night. This record extends the east coast range southward by 300 km.

Table 7 Records of Facelina rhodopos from Australian waters

• Genus Sakuraeolis Baba, 1965

• Sakuraeolis nungunoides Rudman, 1980

Sakuraeolis nungunoides was originally described from Tanzania in tropical eastern Africa. Its range has subsequently been found to extend into the Indo-Pacific reaching Malaysia, the Philippines, New Caledonia and Australia (Rudman, 2003d). This species bears long, transparent cerata which are frequently held erect; each has a subapical orange band. A median orange band extends between the base of the rhinophores and the oral tentacles. The rhinophores are long, tapering, translucent and tipped in orange (Rudman, 2003d). When irritated, S. nungunoides straightens and ‘bristles’ each ceras which, according to Rudman, is similar to the behaviour of a porcupine (Swahili = Nungunungu), for which this species is named. In Australia, S. nungunoides has been recorded from the Sunshine Coast (Mudjimba Island), QLD, to the Brunswick River, NSW (Table 8). The observation of a 35 mm specimen at ‘Fly Point’ on 23 August, 2013 at 14 m, and two additional individuals ‘Little Beach’ at 11 m deep on 2 February, 2015 (Fig. 3d) extend its southern range by 475 km.

Table 8 Records of Sakuraeolis nungunoides from Australian waters

• Family POLYCERIDAE Alder & Hancock, 1845

• Genus Kaloplocamus Bergh, 1880

• Kaloplocamus peludo Vallès & Gosliner, 2006

This polycerid feeds on arborescent bryozoans and possesses numerous dorsal papillae (Gosliner & Vallès, 2006) that afford it a strong resemblance to its prey (Gosliner et al., 2008, p. 105). Kaloplocamus peludo has a wide Indo-Pacific distribution and, in Australia, has been recorded at Heron Island, QLD, in 2007, and more recently at Currimundi Reef, QLD in 2014 (Table 9). This observation of a 10 mm specimen at ‘Fly Point’ on 11 September 2014 at 7 m depth represents a 640 km southward range extension (Fig. 4a).

Table 9 Records of Kaloplocamus peludo from Australian waters

Fig. 4

a. Kaloplocamus peludo. Fly Point, 11 September, 2014. b. Tambja victoriae. Fly Point, 20 February, 2010. c. Polycera risbeci. Pipeline, 23 November, 2014. d. Thecacera pacifica. Fly Point, 6 December, 2014. Photos: a, Tom Davis; b, Roxanne Streatfeild; c, David Harasti; d, Meryl Larkin

• Genus Tambja Burn, 1962

• Tambja victoriae Pola, Cervera & Gosliner, 2005

This species is distinguished from other Tambja species by the presence of dark blue rhinophores surrounded by dark blue rhinophoral sheaths edged in yellow (Gosliner et al., 2008, p. 118) and is known to feed on arborescent bryozoans. Its distribution is thought to be restricted to the western Pacific Ocean, extending from the Philippines to Papua New Guinea and eastern Australia (Rudman, 2005; Gosliner et al., 2008). However, this has not been tested genetically. Australian records indicate a distribution spanning the northern GBR to the Gold Coast in southeastern QLD (Table 10). The observation of a 30 mm individual at ‘Fly Point’, on 20 February, 2010 at 7 m depth constitutes a southward range extension of 700 km (Fig. 4b).

Table 10 Records of Tambja victoriae from Australian waters

• Genus Polycera Cuvier, 1816

• Polycera risbeci Odhner, 1941

This small polycerid is distinguished by the presence of several transverse, broken, brown lines across the body (Marshall & Willan 1999, p. 53; Gosliner et al., 2008, p. 102). The gills are pale yellow and the rhinophores are large. Polycera risbeci occurs in the tropical Indian and western Pacific Oceans (Gosliner et al., 2008, p. 102) with an Australian distribution extending from Heron Island, QLD, to northern NSW (Table 11). On 23 November, 2014 an individual measuring approximately 4 mm was observed at the ‘Pipeline’ at 5 m (Fig. 4c) extending its southern range by 665 km.

Table 11 Records of Polycera risbeci from Australian waters

• Genus Thecacera Fleming, 1828

• Thecacera pacifica (Bergh, 1884)

• Synonyms: Ohola pacifica Bergh, 1884, Thecacera inhacae MacNae, 1958

Thecacera pacifica has an orange body with black, blue and white tips to the tail and both the extra-rhinophoral and extra-branchial appendages (Gosliner et al., 2008, p. 109). This well-known species has become colloquially known as the Pikachu sea slug in Japan and on social media after its similarity to a popular Pokémon toy (Rudman, 2003c; Simonitch, 2012). It has a wide distribution from southern Africa, the Red Sea, Japan, Australia, Hawai’i and the Gulf of Mexico (Gosliner et al., 2008, p. 109), though this has not been tested genetically. The extension of this species into the Gulf of Mexico may be the result of dispersal via shipping as is the case for its congener T. pennigera (Willan, 1976). Although T. pacifica has been found several times in WA, including observations as far south as Esperance in 1985 and Albany in 2010, it has been recorded only once on the east coast at the Tweed River, NSW, in 2013 (Table 12). An observation of a 30 mm individual at ‘Fly Point’ at 7 m depth on 6 December, 2014 extends its southern range by 685 km (Fig. 4d).

Table 12 Records of Thecacera pacifica from Australian waters

Discussion

Preliminary results from a biogeographic study of sea slug distribution on the NSW coast (by MN) record 313 species for Port Stephens. Of those, 30 species have not been found further south on the east coast (Table 13).

Table 13 Sea slug species with a southern distribution limit on the eastern Australian coast at Port Stephens, NSW

As a well-studied sea slug ‘hot spot’, there are extensive records for Port Stephens that clearly indicate a sustained high species richness. These observations of 12 heterobranch sea slugs substantially (i.e., by distances greater than 300 km) south of their previously reported range provide support for other observations of range extensions of other taxa during the last decade. For example, the tropical stichodactylid actinian Stichodactyla haddoni (Saville-Kent, 1893), host for three species of tropical commensal shrimps, was recently reported from Port Stephens and Sydney Harbour (Scott et al., 2015). Other documented range extensions on Australia’s eastern coast include four heterobranch sea slugs on the mid-north coast of NSW (Nimbs et al. 2015) and a number of intertidal mollusc species in eastern Tasmania (Pitt et al., 2010).

There are two important additional points to make about the range extensions to Port Stephens that have been documented here. Firstly, almost half of the species were found only as juveniles suggesting that, whilst they may recruit to the Port, they may not survive to adulthood or to form breeding populations there. Indeed, the fate of juveniles found at the limit of their geographic range is a topic requiring further study. Secondly, whilst our primary hypothesis is that the range extensions result from climate change related processes, the alternate hypothesis of greater sampling effort needs to be considered. Port Stephens is progressively attracting greater attention from scientists and also from citizen scientists who are becoming more experienced in differentiating between similar heterobranch taxa, particularly the smaller species. Citizen science participation has expanded substantially over the past few years through programs such as the Sea Slug Census and the Nelson Bay Nudi Festival. Therefore, it is likely that at least some of the range extensions reported here may be of species that were overlooked in the past.