RESEARCH REPOSITORY This is the author’s final version of the work, as accepted for publication following peer review but without the publisher’s layout or pagination. The definitive version is available at: http://dx.doi.org/10.1111/jfb.13315 Nyegaard, M., Loneragan, N.R. and Santos, M.B. (2017) Squid predation by slender sunfish Ranzania laevis (Molidae). Journal of Fish Biology, 90 (6). pp. 2480-2487. http://researchrepository.murdoch.edu.au/id/eprint/36727/ Copyright: © 2017 The Fisheries Society of the British Isles. It is posted here for your personal use. No further distribution is permitted. RevisedManuscript 1 First report of squid predation by slender sunfish Ranzania laevis (Molidae: 2 Actinopterygii) 3 4 M. NYEGAARD1*, N. LONERAGAN1, M.B. SANTOS2 5 6 1School of Veterinary and Life Sciences, Murdoch University, South Street, Murdoch 7 6150, Western Australia, Australia; 2Instituto Español de Oceanografía, Centro 8 Oceanográfico de Vigo, Subida a Radio Faro, 50, 36390 Vigo, Pontevedra, Spain. 9 10 11 Ranzania laevis diet *Author to whom correspondence should be addressed. Tel: +61 893606453, email: [email protected] 12 Abstract 13 In addition to crustaceans, remains from 17 individual squid were found in the stomach 14 of a 58 cm slender sunfish Ranzania laevis from Australia, adding a new prey item to 15 their little studied diet. Taken together with existing data from the literature, 16 crustaceans appear to be a common prey item, with larger R. laevis (26-65 cm) also 17 taking small fish and squid. Along with new documentation on breaching, the 18 unexpected finding of squid in the stomach confirms that these fish are fast and agile 19 predators. 20 21 22 Key words: diet, crustacean, beak, Ommastrephidae, Octopoteuthis, breaching 23 The curious and little studied Slender Sunfish Ranzania laevis (Pennant 1776), 24 sometimes mistaken for a “mutant fish", is a small and agile member of the family of 25 Ocean Sunfishes (Molidae). It is cosmopolitan, found in tropical and temperate oceans 26 across the world (Fraser-Brunner, 1951; Hutchings, 2001), and is reported as both 27 solitary (Scott, 1995) and schooling (e.g. Castro & Ramos, 2002; Horn et al., 2016). 28 Despite a wealth of literature on R. laevis and its many synonyms, spanning several 29 centuries (Fraser-Brunner, 1951), many studies have focused on anatomy, systematics 30 and/or the unusual occurrence of single individuals (e.g. Aldrovandi, 1613; Plancus, 31 1746; Jenkins 1895; Raven, 1939, Hale, 1944; Purushottama et al., 2014, etc.), with few 32 studies investigating their biology (Smith et al., 2010; Horn et al., 2016). Despite their 33 perceived rarity and tendency to be encountered as singular specimens, large schools, 34 by-catches and strandings in the hundreds of individuals are occasionally reported 35 (Schmidt, 1921; Butler et al., 1997; Quéro et al., 2001; Castro & Ramos, 2002; Smith et. 36 al., 2010; Horn et al., 2016). They have been unjustly described as “exceedingly poor 37 swimmers” (Gudger, 1935), while they are in fact agile and fast (Jenkins, 1895; Raven, 38 1939) and sufficiently powerful to breach out of the water (Figure 1); a behavior 39 apparently not described in the literature previously. The mouth is small, oval, relatively 40 inflexible and probably permanently open (Fitch, 1969, Robison, 1975), although it has 41 been suggested it closes along the vertical axis (Fraser-Brunner, 1951; Tyler, 1980). 42 Observations of live fish during stranding events indicate they are unable to close their 43 mouths (M. Nyegaard, pers. obs.; Figure 2). 44 45 The diet of R. laevis is not well documented, and is usually described in the literature in 46 general terms, such as “shell-fish” (Pennant, 1776; Buckland, 1891), “crustacean 47 animals” (Couch, 1862), “(probably) jelly-fishes and ctenophores” (Wheeler et al., 1975), 48 “planktonic crustaceans” (Heemstra, 1986), and “(probably) small pelagic fish” (Speechi 49 & Bussani in Dulčić et al., 2007), or with references to the diet of the much bigger ocean 50 sunfish (Mola mola) or Molidae in general (e.g. Scott, 1995; Dulčić et al., 2007; 51 Purushottama et al., 2014). Only eight previous accounts of R. laevis stomach contents 52 were found in an extensive literature search, comprising information from 36 sunfish of 53 various sizes, obtained from both fishing and stranding events (Table 1). The reported 54 stomach contents comprised seaweed (Plancus, 1746), “worms of the testaceous”, small 55 crabs (Donovan, 1808), crushed shells, decomposed matter (Francis in Steenstrup & 56 Lütken, 1898), littoral seaweeds (Barnard, 1927), megalopa stage of shore-crab 57 (Barnard, 1935), small fish and fish larvae, pteropod mollusks, various crustaceans 58 including megalopa and zoea stages of crabs (Fitch, 1969), calanoid and cyclopoid 59 copepods, ostracods, amphipods (Robison, 1975), unidentified digested material, 60 seagrass, invertebrates, sand/rock and a feather (Smith et al., 2010). Overall, diet 61 information from non-stranded R. laevis is extremely limited for fish with lengths > 30 62 cm (Table 1); only one account was found, whereby a 65 cm sunfish was “taken on the 63 sands, near the infirmary” (Francis in Steenstrup & Lütken, 1898), seemingly away from 64 its normal habitat in deeper waters. 65 66 In November 2013, a 58 cm total length, 6.51 kg female R. laevis was caught on squid 67 bait by a commercial tuna and billfish longline fishing vessel off Queensland, Australia 68 (25°10’S 155°20’E), in a deep water area (> 4000 m) just east of the Recorder Seamount 69 in the northern Tasman Sea Basin. The unusual by-catch was frozen immediately after 70 capture, handed in to the Australian Fisheries Management Authority and kept frozen 71 during transport to the laboratory in Perth, Western Australia. The dilated stomach was 72 removed after thawing, and the contents emptied into a 300 µm sieve, gently rinsed 73 under running water, fixed in 95% ethanol, then examined under a binocular 74 microscope. 75 76 The stomach contents consisted predominantly of a dark, slimy substance with 77 fragmented crustacean remains, in advanced stages of digestion. Once this substance 78 was sieved, hard remains from at least 17 individual squid were found, consisting of 13 79 upper and 9 lower mandibles (beaks), and a small number of pen fragments. The squid 80 beaks were identified to the lowest possible taxon using a published guide (Clarke, 81 1986) and a reference collection of cephalopod beaks provided by the late Malcolm 82 Clarke from his extensive collection identified from the stomach of predators. A 83 standard measurement, the lower rostral length (LRL) (Clarke, 1986), was taken of the 84 lower beaks (LB) with a binocular microscope fitted with an eyepiece graticule. Dorsal 85 mantle length (DML) and body weight of the squid were estimated using standard 86 regressions for lower beaks (Clarke, 1986). Complete pairs of cephalopod beaks were 87 not present, and in all cases, DML and weight was estimated from the lower beak. The 88 remains were identified as belonging to 11 individuals of the family Ommastrephidae, 1 89 individual of Octopoteuthis sp., and 5 individuals from 3 different, unidentified species 90 (Table 2). Squid DML and weight were estimated for all the identified lower beaks, and 91 ranged from 4.7 to 38.1 mm (mean ± 1 SD = 20.6 ± 11.9 mm), and 0.2 to 3.9 g (1.4 ± 1.4 92 g), respectively, for the Ommastrephids, and 23.1 mm, and 2.4 g for Octopoteuthis sp. 93 (Table 2). The largest identified squid, an Ommastrephid with a DML of 38.1 mm, 94 constituted approximately 7% of the sunfish length. Taking into account the additional 95 head and tentacles of the whole squid, this was not an insubstantial prey item for the 96 sunfish to ingest through its small mouth (35 mm vertical diameter). Relatively large 97 prey items were also reported by Fitch (1969), who found that two of his R. laevis, 98 measuring 28 and 30 cm respectively, contained otoliths of ribbonfish (T. altivelis), with 99 estimated fish lengths of about 7.5 cm, or 25-27% of the predator’s length. 100 101 The presence of remains from 17 individual squid in this large, freshly caught sunfish 102 suggests it had been hunting actively for this type of prey. This is the first time squid 103 have been documented in the diet of R. laevis, and, together with previous findings of 104 fish remains, suggests they are active hunters, with at least some measure of stealth 105 and/or speed associated with their feeding behavior. Their ability to launch themselves 106 out of the water provides further evidence of their speed and agility. 107 108 Squid predation in the Molidae is not unique to R. laevis. Anecdotally, M. mola is known 109 to feed on squid, at least occasionally, as mentioned by some authors (e.g. Houghton et 110 al., 2006; Bray, 2017). Captive sunfish will also keenly feed on squid (M. Hansen, 111 Øresundsakvariet and K. Ydesen, Nordsøen Oceanarium, pers. comm. 2017). However, 112 cephalopods are not typically listed among prey items found in the stomachs of M. mola 113 (e.g. Pope et al., 2010; Syväranta et al., 2012; Harod et al., 2013; Nakamura & Sato, 114 2014), and actual reports in the literature are scarce (Bennett, 1840; Sousa et al., 2016). 115 While recent studies have greatly improved the understanding of the M. mola diet, 116 pointing to a broad diet in smaller M. mola, with an ontogenetic shift towards a 117 gelatinous diet with growth (e.g. Syväranta et al., 2012; Harrod et al., 2013; Nakamura & 118 Sato, 2014; Nakamura et al., 2015; Sousa et al., 2016), the importance of cephalopods is 119 currently not known.