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Australian Journal of

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Description of a new species of chromodorid nudibranch, Goniobranchus solitaryensis sp. nov. (Mollusca: Heterobranchia: Nudibranchia: Chromodorididae) from south-eastern Australia
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Matt J. Nimbs [1*], Stephen D. A. Smith [2]
[1] National Marine Science Centre, Southern Cross University, Bay Drive, Coffs Harbour, NSW 2450, Australia.
[2] Aquamarine Australia, Mullaway, NSW 2456, Australia.
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Abstract
A new species of chromodorid nudibranch, Goniobranchus solitaryensis sp. nov., is described from the Solitary Islands, northern New South Wales, Australia. The species is distinguished from all congeners by the combination of deep purple-black gills and rhinophores, a white mantle with scattered red spots including a characteristic pair of larger central spots that may coalesce into a transverse hourglass shape, and a broad golden-yellow mantle margin. Phylogenetic analysis of concatenated COI and 16S rRNA sequences places G. solitaryensis sp. nov. as the sister taxon to G. fidelis (Kelaart, 1858), from which it differs by a minimum uncorrected p-distance of 3.85% at COI (mean 5.42%). All other congeners are >14% divergent. The new species adds to the remarkable assemblage of red-spotted mimetic chromodorids in south-eastern Australia and is currently known from the Solitary Islands in the Mid-North Coast and Julian Rocks, in the Northern Rivers regions of New South Wales.
urn:lsid:zoobank.org:pub:A06847EA-8B9B-4ACE-B4DC-FDA75F62106E
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Introduction
The family Chromodorididae Bergh, 1891 is the most species-rich family of dorid nudibranchs, comprising over 300 described species across 16 genera (Johnson & Gosliner, 2012). Chromodorids are predominantly found in tropical coral reef habitats and subtropical coastal waters and are characterised by their vivid colouration, which may serve as aposematic warning signals to potential predators (Rudman, 1991). The chromodorids sequester defensive chemicals, primarily terpenoid compounds, from sponges upon which they feed, storing these metabolites in specialised mantle glands that act to deter fish predation (Winters et al., 2018a; Cheney et al., 2016). The genus Goniobranchus Pease, 1866 was originally described in the nineteenth century but was subsequently treated as a junior synonym of Chromodorisfor over a century. Molecular phylogenetic analyses by Johnson & Gosliner (2012) revealed that Chromodoris as traditionally circumscribed was non-monophyletic, leading to the re-erection of Goniobranchus as a valid genus for one of the distinct clades recovered. Goniobranchus currently contains approximately 57 described species (Soong et al., 2021) and can be distinguished from other chromodorid genera, in part, by the upright position of their egg ribbons. Within Goniobranchus, several species complexes have been recognised based on shared colour pattern elements, including a 'red-reticulate group' (Yap et al., 2020) and a 'white with marginal bands group' (Soong et al., 2021).
In south-eastern Australia, an assemblage of red-spotted chromodorid nudibranchs has evolved convergent colour patterns, forming a putative mimicry ring (Rudman, 1991). Rudman (1991) first proposed that the similarity among these species, characterised by white mantles bearing red spots and yellow or orange mantle margins, represented collective aposematic colouration that warned predators of chemical defences sequestered from their sponge diets. This hypothesis was subsequently supported by Winters et al. (2018b), who used visual modelling and pattern analysis to demonstrate that the appearance of red-spotted nudibranchs was similar from the perspective of predatory fish, and that the red-spot colour pattern had evolved independently multiple times across distantly related chromodorid lineages. Winters et al. (2018b) further showed that while levels of distastefulness toward palaemonid shrimp remained relatively constant across taxa in the mimicry ring, toxicity levels varied significantly, suggesting a system of Müllerian mimicry with unequal chemical defences.
The south-eastern Australian, red-spotted mimicry ring includes species from multiple genera. Within Goniobranchusitself, the principal members include G. splendidus (Angas, 1864), G. daphne (Angas, 1864), G. hunterae (Rudman, 1983), G. tasmaniensis (Bergh, 1905) and G. loringi (Angas, 1864). Members from other genera comprise Hypselodoris bennetti (Angas, 1864), Mexichromis festiva (Angas, 1864), Mexichromis mariei (Crosse, 1872), Verconia haliclona (Burn, 1957), and Chromodoris thompsoni (Rudman, 1983) (Rudman, 1991; Winters et al., 2018b; Nimbs & Smith, 2017). Although some of these taxa are common and widespread (e.g. G. splendidus andH. bennetti), others are less frequently observed and exhibit restricted geographic ranges (e.g. G. hunterae, G. loringi, and C. thompsoni) (Nimbs & Smith, 2017).
In the wider Indo-Pacific, G. splendidusis the sister taxon to putative species in the G. tinctorius complex (Rüppell & Leuckart, 1828), a widespread group of cryptic red-reticulate taxa (Wilson et al., 2016). Recent molecular analyses have revealed that the red-reticulate Goniobranchus complex contains multiple species-level lineages, and that the non-reticulate, spotted G. splendidusfalls within this complex (Yap et al., 2020). The genus also contains species within a 'G. fidelis colour group' (Rudman, 1985), which are distinguished by orange outer, and red or purple inner, mantle border bands with dark gills and rhinophores.
Observations of animals that appear to be a red-spotted form of Goniobranchus fidelis (Kelaart, 1858) have been recorded from northern New South Wales since the late 1980s (Rudman, 1999) and from Queensland in 2023 (Mullins, 2023). Rudman (1999) considered this variant a strange colour form of G. fidelis, noting that it shared the dark (black) rhinophores and gills typical of that species, but possessed a golden-yellow mantle border and red spots rather than the broad orange-red mantle margin characteristic of typical G. fidelis. Rudman (1999) further suggested that, at the southern extent of its range, this form possessed a large central red spot that may have evolved to mimic the sympatric G. splendidus which, in northern NSW, often displays fewer but larger red spots or a single large central spot rather than the many scattered spots typical of its southern populations (Winters et al, 2017). We hypothesised that this putative colour form of G. fidelis represents a distinct, undescribed species that has converged on elements of the south-eastern Australian, red-spotted mimicry ring. Here, we test this hypothesis using molecular data and describe Goniobranchus solitaryensis sp. nov. from the Solitary Islands, northern New South Wales.
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Materials & Methods
Sample collection and field observations were conducted using SCUBA. Voucher specimens were deposited with the Australian Museum (AUSTMUS) and other material with Southern Cross University, National Marine Science Centre (NMSC). Animals were narcotised in 7% MgCl₂/seawater solution. Three specimens were preserved in 95% ethanol for genetic analysis. Three further specimens were preserved in 10% formalin/seawater solution. Photographs were taken in situ using an Olympus TG-6 camera.
Small tissue samples were taken from the posterior foot of each of the ethanol-preserved animals and were sent to the Australian Genome Research Facility (AGRF), Sydney for DNA extraction, PCR, and Sanger sequencing. We generated partial COI and 16S rRNA gene fragments using the universal COI primers LCO1490 and HCO2198 (Folmer et al. 1994) and the 16S primers 16Sar-L and 16Sbr-H (Palumbi 1996). Sequence data were returned from AGRF as single-direction reads, which were uploaded into Geneious Prime (v.2024.0) for de novo assembly. Chromatograms were inspected manually and low-quality ends were trimmed prior to the generation of consensus sequences. All sequences were aligned using MAFFT algorithm and alignment boundaries were refined manually. Coding sequences were checked using translation with the invertebrate mitochondrial code. Sequences generated in this study were deposited in GenBank (Table 1).
Additional COI and 16S sequences for congeneric species and the outgroup taxon Doris kerguelenensis were downloaded from GenBank. New and downloaded sequences were aligned separately for COI and 16S using MAFFT (Katoh & Standley 2013) with alignment boundaries trimmed manually to regions of unambiguous homology. The two alignments were then concatenated into a single matrix, and phylogenetic reconstruction was performed using the neighbour-joining algorithm with the HKY substitution model. Node support was assessed via bootstrap resampling (1,000 replicates), with values below 0.50 omitted. Mean uncorrected pairwise p-distances were calculated in MEGA (v.X; Kumar et al. 2018) using the number of base differences per site, with gaps and missing data treated using pairwise deletion.
Following the iterative taxonomic approach advocated by Yeates et al. (2011), we consider the concordance of molecular (COI divergence, phylogenetic clustering) and external morphological (colour pattern) evidence sufficient to delimit this species from its congeners. Internal anatomical characters such as radula morphology and reproductive system are highly conserved within Goniobranchus (Johnson & Gosliner, 2012).
Descriptions of variation in colour pattern and morphology were aided by examination of images of additional individuals posted to iNaturalist (n = 24 individuals).
{insert table 1}
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Results
A phylogenetic tree reconstruction using concatenated partial COI and 16S markers for the red-spotted chromodorid nudibranchs recovered 18 species. Goniobranchus solitaryensis sp. nov. clustered as a maximally supported (BS = 1.0) sister taxon to G.fidelis (Fig. 1).
Goniobranchus solitaryensis sp. nov. had a mean intraspecific divergence of 2.15% (range 1.41–2.53%, n = 3). The nearest congener was G. fidelis, from which G. solitaryensis was separated by a minimum distance of 3.85% (mean 5.42%, range 3.85–6.91%), revealing a clear barcode gap between the maximum intraspecific (2.53%) and minimum interspecific (3.85%) distances. All other congeners were >14% divergent (Table 2). Among species represented by multiple specimens, intraspecific distances were consistently lower than this interspecific threshold: G. fidelis 0.98% (n = 6), G. splendidus 1.23% (n = 3), G. daphne 0.46% (n = 2), G. geometricus 0.35% (n = 3), G. hunterae0.15% (n = 2), and G. tasmaniensis 0.00% (n = 2). The slightly elevated intraspecific distance in G. solitaryensis relative to most congeners is comparable to that observed in G. splendidus and remains well below the interspecific threshold with G. fidelis.
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Discussion
The recognition of G. solitaryensis sp. nov. as a distinct taxon adds to the growing body of evidence that south-eastern Australia harbours considerable intrageneric diversity within Goniobranchus. The Solitary Islands, situated at a biogeographic boundary where tropical and temperate marine faunas overlap (Malcolm et al., 2010), are well placed for the evolution of novel species through processes such as range-edge isolation. The distribution of G. solitaryensis in northern NSW and Queensland, where it co-occurs with the large-spotted northern form of G. splendidus, is consistent with Rudman's (1999) suggestion that the red-spotted pattern of this species may have evolved under selective pressure to resemble the local form of G. splendidus. Whether G. solitaryensisparticipates in the same Müllerian mimicry complex as the other red-spotted chromodorids of the region is a matter that may be tested through chemical ecology and predator-learning experiments (i.e. Winters et al., 2018b).
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Fig. x. Photographs of living specimens of Goniobranchus solitaryensis sp. nov. All specimens photographed at Split Solitary Island, NSW, Australia. (A) Specimen NMSC.207(a).SDAS and NMSC.207(b).SDAS feeding on host sponge, photo by MN; (B–D) Photographic series of animals exhibiting variation in coalescence of central dorsal spot. Photos by MN.
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Fig x. Phylogenetic reconstruction of red-spotted chromodorid nudibranchs from eastern Australia using concatenated partial COI and 16S markers. Neighbour-joining tree generated using Geneious Tree builder based on HKY substitution model. Node values are bootstrap support. Support values <0.5 not included. Accession/voucher numbers in square brackets [].
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Table content
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Key title
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Taxonomy
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Otiorhymirus dongara sp.n.
Justicia muelleri (R.M.Barker) A.R.Bean comb. et stat. nov.
Exsuperoteuthis persephone (Berry, 1918)
Megachile (Eutricharaea) kurandensis Cockerell 1910
Austrohorus ineptus sp. nov.
Genus Insigniteuthis gen. nov.
Opisthoteuthis pluto Berry, 1918
Orasemorpha grandilaevis sp. nov.
Megachile (Eutricharaea) macrocephala Leijs sp. nov.
Paraprasophyllum laticallosum
Isoodon macrourus capensis new subsp.
Megachile (Austrochile) auricauda Leijs sp. nov.
Megachile (Austrochile) quinqecincta Leijs sp. nov.
Isoodon macrourus capensis new subsp.
Paralaoma miniscula Hyman, Bell & Bonham sp. nov.
Megachile (Eutricharaea) simplex Smith1953
Hibbertia lanigera K.R.Thiele & Hammer, sp. nov.
Isoodon nauticus insulanus new subsp.
Hibbertia pallida Steud., Pl. Preiss. [J.G.C.Lehmann] 1(2): 272 (1845).
Family Punctidae Morse, 1864
Otiorhymirus dongara sp.n.
Naumannius metallicus sp. nov.
Heterodontonyx fulvidorsalis (Turner, 1910)
Solanum transiens A.R.Bean sp. nov.
Heterodontonyx erythroura (Cameron 1906)
Varanus kuranda Wells & Wellington, 1985
Megachile (Austrochile) wintinnaensis Leijs sp. nov.
Megachile (Austrochile) silaceacincta Leijs sp. nov.
Megachile (Eutricharaea) rhodogastra Cockerell 1910
Megachile (Eutricharaea) obtusa Smith 1853
Castoreum queenslandicum G.Borkowski & Davoodian, sp. nov.
Megachile (Austrochile) batleyi Leijs sp. nov.
Megachile (Austrochile) enoda Leijs sp. nov.
Scorpionoides nugentae sp. nov.
Costopeplum rhytidatum (Darragh, 1997), n. comb.
Hodophilus darwinensis (A.M. Young) L.J. Vaughan & T.W. May, comb. nov.
Justicia rhadinophylla (Lepschi) A.R.Bean comb. et stat. nov.
Megachile (unplaced) hampsoni Cockerell 1906, comb. nov.
Scorpionoides gen. nov.
Coccygidium fulguritum Atkin-Zaldivar sp. nov.
Heterodontonyx solomonis Turner
Kevin's taxon for table test
Megachile (Austrochile) helvicauda Leijs sp. nov.
Megachile (Eutricharaea) gregaldanae King & Leijs sp. nov.
Paralaoma albina Hyman, Bell & Bonham sp. nov.
Isoodon auratus auratus (Ramsay, 1887)
Isoodon obesulus (Shaw, 1797)
Heterodontonyx fulvidorsalis (Turner, 1910)
Justicia betonica L.
Megachile (Eutricharaea) darwiniana Cockerell 1906
Genus Paralaoma Iredale, 1913
Megachile (Austrochile) flamea Leijs sp. nov.
Megachile (Austrochile) calvalineata Leijs sp. nov.
Megachile (Eutricharaea) kuschei Cockerell 1939
Isoodon macrourus macrourus (Gould, 1842)
Opisthoncus sexmaculatus (C.L. Koch)
Isoodon peninsulae Thomas, 1922
Coccygidium fulguritum Atkin-Zaldivar sp. nov.
Megachile (Austrochile) amnicola Leijs & King sp. nov.
Megachile (Austrochile) cafrae Leijs & King sp. nov.
Isoodon obesulus (Shaw, 1797)
Genus Paralaoma Iredale, 1913
Isoodon fusciventer halae new subsp.
Hibbertia aurea Steud., Pl. Preiss. [J.G.C.Lehmann] 1(2): 272 (1845).
Megachile (Eutricharaea) captionis Cockerell 1914
Proshermacha scimitar Sagastume-Espinoza, Wilson & Harvey, sp. nov.
Scorpionoides scintillans sp. nov.
Varanus tristis (Schlegel, 1839)
Justicia brandegeeana Wassh. & L.B.Smith
Heterodontonyx distictus (Smith, 1868)
Isoodon macrourus macrourus (Gould, 1842)
Heterodontonyx tuberculatus (Smith, 1855)
Megachile (Eutricharaea) macularis Dalla Torre 1896
Megachile (Eutricharaea) variegata Leijs sp. nov.
Megachile (Austrochile) glatzi Leijs sp. nov.
Heterodontonyx tuberculatus (Smith, 1855)
Hydrophis donaldi Ukuwela, Sanders and Fry, 2012
Megachile (Eutricharaea) gregaldanae King & Leijs sp. nov.
Megachile (Austrochile) lucidacincta Leijs sp. nov.
Hibbertia sparsa K.R.Thiele & Hammer, sp. nov.
Megachile (Austrochile) falcicula Leijs sp. nov.
Megachile (Austrochile) paula Leijs sp. nov.
Megachile (Eutricharaea) sequior Cockerell 1910
Megachile (Austrochile) bilineata Leijs sp. nov.
Otiorhymirus gen. nov.
Megachile (Eutricharaea) maculariformis Cockerell 1907
Megachile (Austrochile) nigricauda Leijs sp. nov.
Opisthoncus sexmaculatus (C.L. Koch, 1846)
Megachile (Austrochile) yeatesi Leijs & King sp. nov.
Megachile (Austrochile) binotata Leijs sp. nov.
Eumida cf. fuscoculata sp. “smooth pharynx”
Isoodon nauticus Thomas, 1922 new stat.
Isoodon auratus barrowensis (Thomas, 1901)
Megachile (Eutricharaea) haematogastra Cockerell 1921
Isoodon microtis new sp.
Megachile (Austrochile) fulvopilosa Leijs & King sp. nov.
Paralaoma monticunea Hyman, Bell & Bonham sp. nov.
Heterodontonyx wahisi Chavoshi& Rodriguez sp nov
Coccygidium vittatum Atkin-Zaldivar sp. nov.
Hibbertia jayhornii K.R.Thiele sp. nov.
Acknowledgments
The authors are grateful to Richard C. Willan for ideas and discussion associated with the concept of variant taxa within the red-spotted Goniobranchus group in NSW, to Martyn Kennedy and associates at Otago University for his assistance in laboratory work and genetic sequencing, Ian Shaw for permission to use the image in Figure 3 and David Mullins for information on observations in Queensland. All specimens were collected under NSW Department of Primary Industries Scientific Collection Permits (P12/0010-1/OUT12/4394, P14/0014-1.1)
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References
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