Squid Predation by Slender Sunfish Ranzania Laevis (Molidae)

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/

RevisedManuscript

1 First report of squid predation by slender sunfish Ranzania laevis (Molidae:

2 Actinopterygii)

4 M. NYEGAARD1, N. LONERAGAN1, M.B. SANTOS2

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.

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.

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).

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.

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.

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.

120

121 Crustaceans was a common stomach content component for nearly all R. laevis reviewed

122 in this study, consumed by fish of all sizes from 10-60 cm. Although sparse, the data 123 furthermore suggests that the R. laevis diet changes with fish growth, as also reported for

124 M. mola (op.cit.), but probably not towards a gelatinous diet. The 7 smaller, non-

125 stranded R. laevis (10-11 cm) had consumed small pelagic crustaceans (calanoid and

126 cyclopoid copepods), as well as ostracods and amphipods (Robison, 1975). The larger

127 R. laevis (26-60 cm) had also eaten crustaceans (such as free swimming megalopa and

128 zoea stages of crabs), pteropods and fish larvae, as well as taking more substantial prey

129 such as small fish and squid (Fitch, 1969; this study). Notwithstanding the low number

130 of stomachs examined, and the inherent difficulties of detecting gelatinous prey items

131 through traditional stomach content analysis (Sousa et al., 2016), there is at present no

132 indications that R. laevis take ‘classic’ M. mola gelatinous prey such as siphonophores,

133 scyphozoans etc. The reports of R. laevis stomach contents of seaweed, seagrass,

134 sand/rocks and feather (Table 1) may well represent accidental ingestion during

135 capture/stranding processes, as suggested by Fitch (1969) and Smith et al. (2010). Their

136 apparent inability to close their mouths, even during protracted stranding events

137 (Figure 2), supports this notion.

138

139

140 The authors are grateful to J. Keatley, for handing in his unusual bycatch, S. Hall from the

141 Australian Fisheries Management Authority, who forwarded the specimen, D. Howlett,

142 who shared his footage of breaching slender sunfish, and two anonymous reviewers

143 who provided helpful comments to improve this manuscript.

144

145

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Table 1 Stomach contents reported in the literature for Ranzania laevis and some of its synonyms.

Reference No:size Area Collection Stomach contents (cm) method, time Plancus, 17461 1?:- - - “Ex folis muscis, fucisque aliis marinis vivere hunc piscem credibile est, nam practer has res nihil aliud reperi in ejus stomacho, & intestinis.” [Nothing but seaweed (‘Musci fucique alii marini’) is found in its stomach and intestines.” Donovan, 1:25- Bristol “Caught” “This fish subsists on worms of the testaceou and other tribes, small crabs, &c. 18082 30?5 Channel, UK fragments of these being found on dissection in the stomach.” Francis in 1:65 Swansea, UK “Taken on the “Et Exemplar af ‘den lange klumpfisk’ (Ranzania) (det fra Swansea Bay, 1813) Steenstrup & sands”, 1843 havde I Maven ‘nogle faa knuste skaller’ ‘and some decomposed matter’” [a Lütken, 18983 specimen of the oblong sunfish (Ranzania) (from Swansea Bay, 1813) had in its stomach ‘a few crushed shells’ ‘and some decomposed matter’]. Barnard, 19274 1: - South Africa Trawler, “Its stomach contained several pieces (in various stages of digestion) of littoral May 1926 seaweeds, some of which had evidently been torn off the rocks.” Barnard, 19354 1: - South Africa Stranded, “The stomach … contained a large number of Megalopa stage of the common Aug 1934 shore-crab Playusia chabrus.” Fitch, 1969 3:26-30 California Purse seiner, “… the stomachs…[contained]...an assortment of crustaceans, fish and mollusk Sep 1968 remains… Numerically, crustaceans were the most important food items, but fish, in the two stomachs containing their remains, had contributed the greatest bulk.” Table 1: “Fish (Trachipterus altivelis, myctophid larva, unidentified larva), Crustaceans (natantian shrimp, hyperiid amphipods, crab megalops, crab zoea, unidentified crustaceans), Mollusks (pteropod).” Robison, 1975 7:10-11 Btw Hawaii Mid-water “…in addition to a quantity of partially digested material, [the stomachs & mainland trawl, contained] the exoskeletons of calanoid copepods (Pleuromamma gracilis, USA Jul 1971 Candacia sp.), cyclopoid copepods (Oncacea sp., Corina sp.), ostracods, and fragments of amphipods.” Smith et al., 21:50-62 Western Stranding, “Most stomachs were relatively empty. Four stomachs were relatively full and 2010 Australia May 2008 these contained predominantly seagrass… unidentified digested material comprised 77 % by volume and seagrass (Posidonia sinuosa and P. australis)

comprised 19 % ... Invertebrates [including crustacean remains, Dr. Kim Smith, pers. com. December 2016] comprised about 1% … Sand/rock and a feather were also present.” 1“Mola piscis”, an early name not assessed by Fraser-Brunner (1951). The species was verified from Figure 1, page 304 in Plancus (1746), which clearly features R. laevis. 2Tetrodon truncatus (Donovan, 1808); 3Orthagoriscus oblongus (Jenyns, 1835); 4 R. truncata (Barnard, 1927; 1935); synonyms of R. laevis (Fraser-Brunner, 1951). 5Gauging from the illustration on plate XLL in Donovan (1808), the fish was likely 25-30 cm total length.

Table II Identification to the lowest possble taxon of squid upper beaks (UB) and lower beaks (LB), from the stomach of a 58 cm slender sunfish (Ranzania laevis), caught by a commercial longliner off Queensland in November 2013. The estimates for total number of individuals (N) are based on the number of upper or lower beaks, whichever is greater. Measurement of the lower beaks were used to derive estimates of individual dorsal mantle lengths (DML) and individual squid weights (W). The second estimate of weight (AW) is adjusted to take account of all the cephalopods in the taxon, including those identified from the upper beaks. Taxon Remains N LRL DML W (g) AW (g) (mm) (mm) Ommastrephidae 11 UB + 5 LB 11 1.19 38.1 3.9 15.6 0.77 20.7 1.1 0.74 19.1 1.0 0.71 18.1 0.9 0.39 4.7 0.2 Octopoteuthis sp. 1 LB 1 1.35 23.1 2.4 2.4 Species 1 2 LB 2 Species 2 1 LB 1 Species 3 2 LB 2 Not identified 3 UB -

Figure Captions 1 and 2

Figure 1 A slender sunfish Ranzania laevis squirting water (B,C,D: black

arrows) while breaching in a shallow bay near Albany, Western Australia (35°

5.68’ S 117° 57.73’ E) during a stranding event in April 2016. Stills from footage by

Darren Howlett, local resident, Albany.

Figure 2 A) Open mouth of a live slender sunfish Ranzania laevis during a

stranding events on Cheynes Beach, Western Australia (34° 52.69’ S 118° 23.91’ E)

in May 2016. B) Even when ‘gasping’ after stranding, the mouth does not move or

close. Images by Marianne Nyegaard.

Figure 1 Click here to download Figure Fig I.tiff Figure 2 Click here to download Figure Fig II.tiff