Cymonomus curvirostris Sakai 1965

© 2017 Academia Sinica, Taiwan Open Access A Historical Summary of the Distribution and Diet of Australian Sea Hares (Gastropoda: Heterobranchia: Aplysiidae) Matt J. Nimbs1,2,*, Richard C. Willan3, and Stephen D. A. Smith1,2 1National Marine Science Centre, Southern Cross University, P.O. Box 4321, Coffs Harbour, NSW 2450, Australia 2Marine Ecology Research Centre, Southern Cross University, Lismore, NSW 2456, Australia. E-mail: [email protected] 3Museum and Art Gallery of the Northern Territory, G.P.O. Box 4646, Darwin, NT 0801, Australia. E-mail: [email protected].au (Received 12 September 2017; Accepted 9 November 2017; Published 15 December 2017; Communicated by Yoko Nozawa) Matt J. Nimbs, Richard C. Willan, and Stephen D. A. Smith (2017) Recent studies have highlighted the great diversity of sea hares (Aplysiidae) in central New South Wales, but their distribution elsewhere in Australian waters has not previously been analysed. Despite the fact that they are often very abundant and occur in readily accessible coastal habitats, much of the published literature on Australian sea hares concentrates on their taxonomy. As a result, there is a paucity of information about their biology and ecology. This study, therefore, had the objective of compiling the available information on distribution and diet of aplysiids in continental Australia and its offshore island territories to identify important knowledge gaps and provide focus for future research efforts. Aplysiid diversity is highest in the subtropics on both sides of the Australian continent. Whilst animals in the genus Aplysia have the broadest diets, drawing from the three major algal groups, other aplysiids can be highly specialised, with a diet that is restricted to only one or a few species. Although the diets of some widespread, frequently-observed taxa have been investigated, those for lesser-known, endemic taxa remain unclear and require specific investigation. Key words: Aplysia, Dolabrifera, Dolabella, Algae, Biogeography, Anaspidea, Herbivores. *Correspondence: E-mail: matthew[email protected] BACKGROUND The heterobranch family Aplysiidae Lamarck, 1809, encompassing the sea slugs collectively known as ‘sea hares’, currently comprises 64 species distributed among 11 genera (WoRMS 2017). All genera are found in Australian waters except for Barnardaclesia Eales & Engel, 1935 and Paraplysia Pilsbry, 1895. The Australian fauna is numerically uncertain, where, of the 25 species recorded, at least 12 are taxonomically insecure (Nimbs et al. 2017). For the Australian fauna, little is known of their specific diets, however, as with all sea hares, they are almost exclusively epifaunal herbivores (Thompson 1976: 102; Yonow 2008: 96; Gosliner et al. 2015: 100) consuming algae, angiosperms (seagrasses) and filamentous cyanobacteria. As with other shallowwater herbivorous molluscs, polyphagy can occur with accidental ingestion of animal material during grazing (Camus et al. 2008). Some species of sea hares can be highly selective and may specifically target non-plant foods (e.g. Phyllaplysia taylori Dall, 1900 is believed to consume diatoms (Beeman 1970)). Carefoot (1987) also noted that, when starved, captive animals of Aplysia californica J.G. Cooper, 1863 engaged in cannibalism and oophagy. Although the diets of some taxa have been well studied, most studies comprised feeding assays carried out in a laboratory as part of broader analyses of chemical ecology, physiology, or to explore the production of secondary metabolites (Carefoot 1970; Pennings and Paul 1992; Rogers Zoological Studies 56: 35 (2017) doi:10.6620/ZS.2017.56-35 1 © 2017 Academia Sinica, Taiwan et al. 2000; Ginsburg and Paul 2001; Capper et al. 2006). For those in vitro studies, the foods offered were based on observations of algae that were found to co-occur with the sea hare in its natural environment under the assumption that these were the most likely food sources. Whilst aplysiids are predominantly creatures of the tropics and subtropics (Rudman and Willan 1998), their greatest diversity occurs where oceanographic and benthic conditions support suitable macroalgal habitats (Nimbs et al. 2017). Carefoot (1987) noted that the Australian region was the most biodiverse for animals in the genus Aplysia Linnaeus, 1767, and recent work indicates that this can be broadened to include the family Aplysiidae more generally, with the highest diversity occurring in the warm temperate waters of the central New South Wales (NSW) coast (Nimbs et al. 2017). Documentation of Australian sea hare distribution at a regional scale has not previously been undertaken because of taxonomic uncertainties. Nevertheless, with tropical affinity (Rudman and Willan 1998), protracted larval duration (Kempf 1981), and high fecundity (Willan 1979; Wells and Bryce 2003), it is likely that settlement and metamorphosis may occur in novel temperate locations as oceanographic conditions (temperature, currents) change (Malcolm et al. 2011). Indeed, the compilation of a regionalised species inventory for the state of New South Wales by Nimbs and Smith (2017a) enabled the recognition of the southward range extension of the sea hare Syphonota geographica recorded for the first time south of Sydney, an observation that also represents the most southern global record (Nimbs and Smith 2017b). Despite their high regional diversity, seasonal abundance, and occurrence in readily accessible habitats, much of the literature published on Australian sea hares concentrates on taxonomy. As a result, there is a paucity of information regarding their biology and ecology. Thus, in an effort to identify gaps in knowledge, a search of the literature on the distribution and diet of Australian Aplysiidae was undertaken. Notwithstanding the taxonomic insecurity of the Australian fauna, those species listed in Nimbs et al. (2017) were used as a foundation for this work. The aims of this paper are twofold: (1) to explore the present Australian distribution of the Aplysiidae using historic and contemporary observation records and (2) to consolidate the information on diet by reviewing published literature relevant to the Australian fauna and, where available, to supplement this with observations. MATERIALS AND METHODS Distribution of Aplysiidae in Australian waters Australian distribution records were sourced from the literature, books, websites and personal records. The geographic extent includes the waters of continental Australia plus its oceanic islands and reefs (e.g. Lord Howe Island, Middleton and Elizabeth Reefs, Cartier and Ashmore Reefs) as well as external territories of Norfolk, Christmas and the Cocos (Keeling) islands. Whilst many distribution records for the mainland can be pinpointed to individual locations, some give only broad regional descriptors. To accommodate this wide spatial range, presence/ absence data for each taxon were consolidated into currently recognised marine bioregions - the IMCRA 4.0 shelf provinces (COA 2006) (Tables 1 and 2). A comparison of species richness among IMCRA provinces and between the east and west coasts, for the purposes of identifying latitudinal change, was facilitated by calculating the mid-point for each province as the summary independent variable. Review of the diets of Australian Aplysiidae The published literature was searched for information on the diets of the Australian aplysiid species. As some taxa exhibit ontogenic dietary plasticity (Carefoot 1987), the diets of veligers and juveniles were not considered. RESULTS Distribution of Aplysiidae in Australian waters The western South Pacific Ocean has long been known to support the greatest diversity of aplysiids in the world (Eales 1960; Medina et al. 2004). In Australian waters there are the 25 described and undescribed species (23 listed in Nimbs et al. (2017)). Of these 25 taxa, 10 are in the genus Aplysia but, as these may include several synonymous taxa, the actual number is currently uncertain. In a revision of the world species of Aplysia, Eales (1960: 380) listed 12 species from Australia page 2 of 15Zoological Studies 56: 35 (2017) © 2017 Academia Sinica, Taiwan Table 1. List of the Australian IMCRA coastal shelf provinces (with the land based geographic limits of each geographic region), offshore islands and external territories (IMCRA Technical Group - Environment Australia for the Australian and New Zealand Environment and Conservation Council 1998) IMCRA Province (IMCRA 4.0) Extent (listed in IMCRA 3.3) Northern Province Cape Hotham, NT to Cape York, QLD Northeast Transition Cape York, QLD to Cooktown, QLD Northeast Province Cooktown, QLD to Port of Battle Creek, QLD Central Eastern Transition Port of Battle Creek, QLD to south of Coffs Harbour, NSW Central Eastern Province South of Coffs Harbour, NSW to south of Wollongong, NSW Southeast Transition South of Wollongong, NSW to Waratah Bay, Vic Tasmanian Province Cape Naturaliste, Tas to Cape Grim, Tas Bass Strait Province Cape Otway, Vic to Waratah Bay, Vic; Kangaroo Island, Tas to Little Musselroe Bay, Tas Western Bass Strait Transition Cape Otway, Vic to Cape Jervis, SA Spencer Gulf Province Cape Jervis, SA to Point Brown, SA Great Australian Bight Transition Point Brown, SA to Israelite Bay, WA Southwest Province Israelite Bay, WA to Perth, WA Southwest Transition Perth, WA to Geraldton, WA Central Western Province Gnaraloo, WA to North West Cape, WA Central Western Transition Geraldton, WA to Gnaraloo, WA Northwest Province North West Cape, WA to Cape Leveque, WA Northwest Transition Cape Leveque, WA to Cape Hotham, NT Offshore Islands and territories Extent Lord Howe Island Balls Pyramid, Lord Howe Island, Middleton and Elizabeth Reef, NSW (Tasman Sea) Norfolk Island Norfolk Island (Tasman Sea) Cartier, Hibernia and Ashmore Reefs Sahul Shelf, Timor Sea Christmas Island Christmas Island (Indian Ocean) Cocos (Keeling) Island Cocos (Keeling) Islands (Indian Ocean) Table 2. List of data sources for distribution of Aplysiidae in Australian shelf waters Published literature Baker et al. (2015) Benkendorff (2005) Burn (2006; 2015) Chalmer et al. (1976) Cobb and Willan (2006) Coleman (2008) Eales (1960) Gowlett-Holmes (2008) Grove (2006) Hedley (1916) Nimbs and Smith (2017a b); Nimbs et al. (2017) Shepherd and Thomas (1982); Shepherd (2013) Wagele et al. (2006) Wells and Bryce (1993) Online databases Atlas of Living Australia (ALA 2015) Grove (2015) OBIS (2016) Rudman (2010) Reports and personal communications Baker et al. (2015) Janine Baker, pers. comm. (SA) Scoresby Shepherd, pers. comm. (SA) Mark Scott, pers. comm. (Norfolk Island) page 3 of 15Zoological Studies 56: 35 (2017) © 2017 Academia Sinica, Taiwan (A. cronullae Eales, 1960, A. dactylomela Rang, 1828 (syn. A. argus Rüppell & Leuckart, 1830), A. denisoni E. A. Smith, 1884, A. extraordinaria (Allan, 1932), A. gigantea G. B. Sowerby I, 1869, A. juliana Quoy & Gaimard, 1832, A. nigra d’Orbigny, 1837, A. oculifera A. Adams & Reeve, 1850, A. parvula Mӧrch, 1863, A. reticulata Eales, 1960, A. sowerbyi Pilsbry, 1895, A. sydneyensis G. B. Sowerby I, 1869). Later, Carefoot (1987: 170) listed 14 species, adding A. keraudreni Rang, 1828 on the east coast and A. pulmonica Gould, 1852 on the west. However, the latter was recently synonymised with A. argus (Alexander and Valdés 2013). Eales (1960: 322) described a preserved individual of the east coast species A. keraudreni as “A small specimen, much contracted, but probably belonging to this species, [which] came from Sydney, Australia.” However, later in the work, as part of a global analysis of distribution (p. 380), it was omitted from a discussion of Australian animals and mentioned as occurring only in New Zealand. Furthermore, in a tabulated summary of species found in the South West Pacific (encompassing all Australian coastal waters), A. oculifera was omitted from the regional list (p. 381) despite being mentioned in the text (p. 380) as occurring in Western Australia (WA). Whilst Carefoot (1987) and Eales (1960) both report A. nigra as an eastern Australian species, these records are most likely to be for A. juliana. Indeed, Eales discussed the numerous similarities between them. Later, Rudman also highlighted the probability that A. nigra brunnea Hutton, 1875 from NZ was most likely to be A. juliana (Rudman 2003a). Another Aplysia, A. reticulata, has not been mentioned in the literature or observed in Australian waters since Wells and Bryce (1993) recorded it and is also likely to be synonymous with another taxon. In his treatise on the sea slugs from the Abrolhos Islands, WA, O’Donoghue (1924) described a new species, Dolabrifera pelsaertensis, using two specimens collected from Pelsaert Island. As “They do not appear to be referable to any described forms...” (1924: 535), he considered them to be a new taxon. Nevertheless, species of Dolabrifera can be highly variable in both colour and morphology (Rudman 2003b; pers. obs.), depending on diet and habitat. As with many of the Australian taxa described using preserved specimens, D. pelsaertensis is likely to be synonymous with another Dolabrifera. Few data are available regarding this species and a thorough search of the literature failed to find any contemporary reference to, or observations of, D. pelsaertensis. Aplysia argus and A. parvula are the most widespread aplysiids in Australian coastal waters, being found in 16 and 15 shelf bioregions respectively (Figs. 1A and 2A), and they are the only taxa recorded from the Great Australian Bight. Dolabella auricularia (Fig. 2G) and Bursatella leachii (Fig. 2E) also have wide distributions around much of Australia (Rudman 1998b) with both occurring in 12 bioregions. Aplysia sowerbyi (Fig. 2C), currently the only Aplysia recorded from the Northern Shelf Province, is probably circum-continental, however, some gaps remain, particularly in northern Western Australia. With just the single record, Aplysia keraudreni (Fig. 1G) has a highly restricted distribution and A. cronullae (Fig. 1B), A. denisoni (Fig. 1C) and A. reticulata (Fig. 2B), also found in only a few bioregions, are all likely to be synonymous with more widely observed species (Nimbs et al. 2017). Petalifera petalifera (Fig. 3D), Phyllaplysia sp. (Fig. 3F) and the undescribed Bursatella sp. (Fig. 2F) from WA have comparatively short ranges, whereas Dolabrifera brazieri (Fig. 2H), Petalifera ramosa (Fig. 3E), A. sydneyensis (Fig. 2D), A. juliana (Fig. 1F) and A. extraordinaria (Fig. 1D) are more widespread, but restricted to the east coast. Dolabrifera dolabrifera (Fig. 3A), A. oculifera (Fig. 1H) and Syphonota geographica (Fig. 3I) are found on both the east and west coasts, but not in between, and Notarchus indicus (Fig. 3B) exhibits an apparently disjunct distribution: Central Eastern Province in NSW, Spencer Gulf Province in SA and three bioregions in WA. Both Stylocheilus striatus (Fig. 3H) and S. longicauda (Fig. 3G) have been found in several bioregions; however, records are patchy and there are broad spatial gaps. Patchy distribution is also evident for the undescribed Petalifera sp. (Fig. 3C). The only Aplysia found exclusively on the west coast is A. gigantea (Fig. 1E), which occurs in both the Southwest Province and Southeast Transition bioregions. All taxa mentioned above have been illustrated in Nimbs et al. (2017), except Aplysia gigantea, Bursatella sp. and Phyllaplysia sp. (presented here in Fig. 4). No images of Aplysia cronullae, A. reticulata or A. keraudreni were available. page 4 of 15Zoological Studies 56: 35 (2017) © 2017 Academia Sinica, Taiwan Fig. 1. Distribution of the Australian Aplysiidae. (A) Aplysia argus; (B) Aplysia cronullae; (C) Aplysia denisoni; (D) Aplysia extraordinaria; (E) Aplysia gigantea; (F) Aplysia juliana; (G) Aplysia keraudreni; and (H) Aplysia oculifera. (A) (C) (E) (G) (B) (D) (F) (H) page 5 of 15Zoological Studies 56: 35 (2017) © 2017 Academia Sinica, Taiwan Fig. 2. Distribution of the Australian Aplysiidae. (A) Aplysia parvula; (B) Aplysia reticulata; (C) Aplysia sowerbyi; (D) Aplysia sydneyensis; (E) Bursatella leachii; (F) Bursatella sp.; (G) Dolabella auricularia; and (H) Dolabrifera brazieri. (A) (C) (E) (G) (B) (D) (F) (H) page 6 of 15Zoological Studies 56: 35 (2017) © 2017 Academia Sinica, Taiwan Fig. 3. Distribution of the Australian Aplysiidae. (A) Dolabrifera dolabrifera; (B) Notarchus indicus; (C) Petalifera petalifera; (D) Petalifera ramosa; (E) Petalifera sp.; (F) Phyllaplysia sp.; (G) Stylocheilus longicauda; (H) Stylocheilus striatus; and (I) Syphonota geographica. (A) (C) (E) (G) (I) (B) (D) (F) (H) page 7 of 15Zoological Studies 56: 35 (2017) © 2017 Academia Sinica, Taiwan Diet of Australian Aplysiidae The diets of the Australian aplysiids are summarised in table 3. DISCUSSION Distribution of Aplysiidae in Australian waters Aggregating data into IMCRA 4.0 shelf provinces revealed latitudinal patterns of distribution on both the east and west coasts that are consistent with those mentioned for NSW alone (Nimbs et al. 2017), where aplysiid diversity increases with latitude, peaks in subtropical waters at 31-32°S and decreases in temperate waters. This pattern is stronger on the east coast (Fig. 5). Species of Aplysia are more diverse on the east coast, whilst other genera are more evenly distributed on both the east and west coasts. In keeping with the our hypothesis that the central NSW coast is possibly the most speciose region for aplysiids globally, Lord Howe Island and the nearby Middleton and Elizabeth Reefs, both with 8 recorded species, support the highest diversity among the offshore Australian islands and territories. This is followed by Norfolk Island, Fig. 4. Top left: Bursatella sp., Woodman Point, WA, 21 March 2017, photo: Matt Nimbs; top right: Phyllaplysia sp. Sydney Harbour, NSW, 4 February 2002, photo: Andrew Trevor-Jones (identified by W. B. Rudman (Rudman 2002), photo used with permission); bottom: Aplysia gigantea, Woodman Point, WA, 23 March 2017, photo: Matt Nimbs. page 8 of 15Zoological Studies 56: 35 (2017) © 2017 Academia Sinica, Taiwan Table 3. Summary of dietary information for Australian Aplysiidae from field and laboratory observations (excluding larval stages). Algal species that were listed as ‘host’ were not necessarily deemed to be a food source Aplysia Aplysia argus Rüppell & Leuckart, 1830 Chlorophyta: Cladophora Kützing, 1843; Ulva Linnaeus, 1753 [Morton and Miller 1973; Switzer-Dunlap and Hadfield 1979; Carefoot 1987]. Rhodophyta: Corallina Linnaeus, 1758; Laurencia J. V. Lamouroux, 1813; Centroceras Kützing, 1842 '1841'; Gracilaria Grenville, 1830; Acanthophora J. V. Lamouroux, 1813; Spyridia Harvey, 1833 [Carefoot 1987, 1985, 1970; Morton and Miller 1973; Willan 1979; Switzer-Dunlap and Hadfield 1979; Rudman 1998a; Rogers et al. 2000]; red algae as adults [Switzer-Dunlap and Hadfield 1979; Carefoot 1987]; red and green turfing algae [Marshall and Willan 1999: 27]. Aplysia cronullae Eales, 1960 No data. Aplysia denisoni E. A. Smith, 1884 No data. Aplysia extraordinaria (Allan, 1932) Chlorophyta: Ulva [personal observation, Sandy Beach, January 2017.] Aplysia gigantea G. B. Sowerby I, 1869 No data. Aplysia juliana Quoy & Gaimard, 1832 Ochrophyta: Undaria Suringar, 1873 [According to Saito and Nakamura (1961) in laboratory trials A. juliana preferred Undaria pinnatifida over green algae]. Chlorophyta: Ulva [Carefoot 1970; Usuki 1970; Sarver 1979; Rogers et al. 1995; pers obs. Monostroma [Usuki 1981]. Rhodophyta: Red algae [Willan 1979]. Aplysia oculifera A. Adams & Reeve, 1850 Chlorophyta: Ulva [Hurwitz and Susswein 1992; Yonow 2008: p. 97]; Cladophora [Plaut 1993]. Fig. 5. Latitudinal diversity of the Aplysiidae on the eastern and western Australian coasts. Data represent aplysiid species richness for the middle latitude of each IMCRA 4.0 provincial shelf bioregion. page 9 of 15Zoological Studies 56: 35 (2017)