Southern range extensions for twelve heterobranch sea slugs (Gastropoda: Heterobranchia) on the eastern coast of Australia
© Nimbs et al. 2016
Received: 7 September 2015
Accepted: 2 December 2015
Published: 1 July 2016
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.
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.
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.
Selected records of Philinopsis orientalis from Australian waters
Lizard Island, QLD
Pers. obs. (R. C. Willan)
Coates Reef, QLD
Pers. obs. (R. C. Willan)
Rottnest Island, WA
(Wells & Bryce 2000, p. 31–32)
Nelson Bay, NSW
Order NUDIBRANCHIA Cuvier, 1817
Family DISCODORIDIDAE Bergh, 1891
Genus Jorunna Bergh, 1876
Jorunna ramicola M. C. Miller, 1996
Records of Jorunna ramicola from Australian waters
Genus Thordisa Bergh, 1877
Thordisa tahala Chan & Gosliner, 2007
Records of Thordisa tahala from Australian waters
Family TRITONIIDAE Lamarck, 1809
Genus Marionia Vayssière, 1877
Marionia pustulosa Odhner, 1936
Records of Marionia pustulosa from Australian waters
(Coleman 2008, p. 399)
Port Curtis, QLD
(Coleman 2008, p. 399)
(Coleman 2008, p. 399)
Flinders Reef, QLD
Cobb & Mullins (2009b)
Mud Island, QLD
North Solitary Island, NSW
Australian Museum (1989)
Nelson Bay, NSW
1988, 1996, 2015
Carol Buchanan, this paper.
Records of Trinchesia ornata from Australian waters
Heron Island, QLD
(Marshall & Willan 1999, p. 141)
Heron Island, QLD
Museum Victoria (1980)
Gneering Shoals, QLD
Alexandra Headland, QLD
(Coleman 2008, p. 379)
Byron Bay, NSW
(Coleman 2008, p. 379)
Nelson Bay, NSW
Records of Trinchesia puellula from Australian waters
Gneering Shoals, QLD
Cobb & Mullins (2008)
Nelson Bay, NSW
Records of Facelina rhodopos from Australian waters
Genus Sakuraeolis Baba, 1965
Sakuraeolis nungunoides Rudman, 1980
Records of Sakuraeolis nungunoides from Australian waters
Family POLYCERIDAE Alder & Hancock, 1845
Genus Kaloplocamus Bergh, 1880
Kaloplocamus peludo Vallès & Gosliner, 2006
Records of Kaloplocamus peludo from Australian waters
Genus Tambja Burn, 1962
Tambja victoriae Pola, Cervera & Gosliner, 2005
Records of Tambja victoriae from Australian waters
Hibernia Passage, QLD
Australian Museum (1981)
Swain Reefs, QLD
Australian Museum (1985)
North West Reef, QLD
Australian Museum (1983)
Heron Island, QLD
Cobb & Mullins (2003)
Gold Coast Seaway, QLD
Nelson Bay, NSW
Genus Polycera Cuvier, 1816
Polycera risbeci Odhner, 1941
Records of Polycera risbeci from Australian waters
Genus Thecacera Fleming, 1828
Thecacera pacifica (Bergh, 1884)
Synonyms: Ohola pacifica Bergh, 1884, Thecacera inhacae MacNae, 1958
Records of Thecacera pacifica from Australian waters
Bynoe Harbour, NT
Kendrew Island, WA
Museum Victoria (1975a)
Tweed River, NSW
Rottnest Island, WA
Nudi Pixel (2011c)
Nelson Bay, NSW
Clay Bryce, this paper
Nudi Pixel (2010d)
Sea slug species with a southern distribution limit on the eastern Australian coast at Port Stephens, NSW
Australian Museum (1980)
Nudi Pixel (2012)
Australian Museum (1986)
Pola et al., 2014
Nudi Pixel (2009a)
Nudi Pixel (2008a)
Nudi Pixel (2010c)
Nudi Pixel (2008c)
Nudi Pixel (2010b)
Nudi Pixel (2010a)
Nudi Pixel (2009b)
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.
The authors extend their gratitude to: Denis Riek for detailed information regarding the large number of species he has observed on the Tweed-Byron coast; Deb Aston for her generosity in time and information regarding sea slugs found in the Gold Coast region over many years; and Carol Buchanan for generously allowing the first author full access to her vast collection of heterobranch photographs and personal knowledge gathered over several decades. Thanks are also due to the following photographers for permission to use their images: Matt Doyle for his photograph of Philinopsis orientalis; Roxanne Streatfeild for her photograph of Tambja victoriae; Nicola Davis for her photograph of Sakuraeolis nungunoides; and Kristine O’Keefe for her photograph of Marionia pustulosa. We also acknowledge all of the participants in the Sea Slug Census program for their eager participation in the series of events from 2013 to the present. Kathryn James provided professional design for the photographic figures. Robert Burn kindly checked his copies of Bergh’s publications. This paper was prepared from data collected as part of a BSc (Hons) research project by MN, a PhD project by TRD, and a MSc project by ML. Funding and in-kind support was provided by Southern Cross University and NSW DPI (Fisheries). The authors also thank three anonymous reviewers for their constructive comments that helped improve the manuscript.
MN collated occurrence records and with RCW and SDAS wrote the manuscript. ML, TD, DH and SDAS carried out fieldwork and documented species occurrence. RCW identified the animals from photographs. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
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