Adhesive Demersal Eggs Spawned by Two Southern Australianporcupine

Home , Chilomycterus, Chilomycterus antennatus, Cyclichthys, Cyclichthys orbicularis, Diodon, Porcupinefish

Aquacult. Sci. 63（3），357－359（2015）

Short Paper

dealer and maintained in a closed circulating-filtering Adhesive demersal eggs spawned by exhibition aquarium with a coral sand or pebble two southern Australian bottom. porcupine puffers In all cases, spawning was preceded by the abdomen of the female becoming swollen several days prior, whereupon the male commenced chasing the female or 1 2 Hiroyuki DOI , Takayuki SONOYAMA , nestling close to the latter on the bottom until spawn- 2 2 3,＊ Yuko YAMANOUCHI , Kenta TAMAI , Harumi SAKAI ing. Following spawning, even if spawning behavior had 2 and Toshiaki ISHIBASHI not been observed, the abdomen of the female became shrunken. There was no case in which more than one species spawned at the same time. Among the eight Abstract: Eggs spawned in the Shimonoseki Marine species, the eggs of Ch. antennatus and Ch. reticulatus Science Museum Aquarium by eight species of Diodon- were unfertilized. Fertilized eggs of the other species tidae (Allomycterus pilatus, Chilomycterus antennatus, were reared and their specific identity re-established. Ch. reticulatus, Ch. schoepfii, Cyclichthys orbicularis, Spawning and development of Cy. orbicularis and Diodon hystrix, D. holocanthus and D. nicthemerus), spawning of Ch. schoepfii Ch. antillarum (hybridiza- representing four genera, were mostly pelagic, only A. × pilatus and D. nicthemerus spawning adhesive demersal tion) have already been documented (Doi et al. 2015a, eggs. The adaptive implications of such demersal eggs 2015b), and rearing of Cy. orbicularis, A. pilatus and D. require comparative studies on diodontid spawning nicthemerus briefly noted in Japanese (Shimonoseki ecology. Marine Science Museum 2006a, 2006b, 2010). All of the spawned eggs were spherical, the hatched Key words: Porcupine puffer; Spawning; Adhesive larvae from fertilized eggs all being covered by a demersal egg; Pelagic egg “vesicular dermal sac” or “pliable shell” on their head and trunk (Fig. 1). However, eggs from six species, including those which were unfertilized, were pelagic, only A. pilatus and D. nicthemerus spawning adhesive demersal eggs (Fig. 1A, 1C). In the case of D. hystrix, Porcupine puffers of the family Diodontidae include although Wolfsheimer (1957) attributed unfertilized seven genera, 17 species and two subspecies (Leis demersal eggs to that species, the present study clearly 2006; Froese and Pauly 2014). Reports to date on dio- demonstrated that it spawns pelagic eggs, thereby dontid life history have indicated that isolated spherical upholding doubts raised by Leis (1978) and Sakamoto pelagic eggs are spawned, the head and trunk of larvae and Suzuki (1978). The two latter reports also provided being covered by a “vesicular dermal sac” or “pliable evidence against the spawning of demersal eggs by D. shell” (Leis 1978; Sakamoto and Suzuki 1978; Fujita and holocanthus, contrary to the expectations of Nishimura Matsuura 2014). (1960) and Fujita (1962). Accordingly, the present In recent years, eight species of Diodontidae, study recognizes only A. pilatus and D. nicthemerus, representing four genera, have spawned in the amongst the diodontid species for which the eggs are Shimonoseki Marine Science Museum Aquarium: known, as spawning adhesive demersal eggs. Allomycterus pilatus, Chilomycterus antennatus, Ch. Among eight tetraodontiform families, Diodontidae, reticulatus, Ch. schoepfii, Cyclichthys orbicularis, Balistidae, Monacanthidae and Tetraodontidae spawn Diodon holocanthus, D. hystrix and D. nicthemerus, adhesive demersal eggs, and Molidae, Ostraciidae under presence of zero to two other diodontids in the and Triacanthidae spawn pelagic eggs (Fujita and same aquarium including Ch. antillarum and D. lituro- Matsuura 2014). Egg conditions are unknown for sus (Table 1). In each case, wild-caught individuals from Triacanthodidae and Triodontidae. Moreover, Molidae an unknown locality had been purchased from a fish and Ostraciidae share “vesicular dermal sac” or “pliable

Received 18 February 2015; Accepted 7 July 2015. 1 Osaka Aquarium Kaiyukan, 1-1-10 Kaigandori, Minato-ku, Osaka 552-0022, Japan. 2 Shimonoseki Marine Science Museum “Kaikyoukan”, Shimonoseki Academy of Marine Science, Shimonoseki, Yamaguchi 750-0036, Japan. 3 Department of Applied Aquabiology, National Fisheries University, Shimonoseki, Yamaguchi 759-6595, Japan. ＊ Corresponding author: Tel, (+81) 286-5111; Fax, (+81) 286-7435; Email, [email protected] (H. Sakai). 358 H. Doi, T. Sonoyama, Y. Yamanouchi, K. Tamai, H. Sakai and T. Ishibashi shell” characteristics of the head and trunk of larvae eggs, are therefore rare among the three families in with Diodontidae (Leis 1978; Sakamoto and Suzuki sharing the same larval characteristics. 1978; Fujita and Matsuura 2014). Allomycterus pilatus Among pleuronectiform flatfishes, most species and D. nicthemerus, which spawn adhesive demersal of which spawn epipelagic eggs, six species from

Table 1. Spawning data for eight porcupine puffers of the genera Allomycterus, Chilomycterus, Cyclichthys and Diodon, spawned in the Shimonoseki Marine Science Museum Aquarium A. pilatus Ch. antennatus Ch. reticulatus Ch. schoepfii Cy. orbicularis D. holocanthus D. hystrix D. nicthemerus

Establishment date Jun. 2002 Mar. 2004 Dec. 2012 Apr. 2006 Aug. 2001 Feb. 2003 Dec. 2003 May 2006 Spawning date Dec. 2003, Jan. 2004 Apr. 2008 May 2013 May 2008 Jun. 2004 May 2004 Jul. 2005 Oct. 2007 Aquarium size (m3) 3.4 1.1 4.2 1.1 1.1 9.8 16.2 3.4 Salinity (‰)34-35 34-35 34-35 34-35 34-35 34-35 34-35 34-35 Water temperature (℃)1823252325232618 Light/dark (hours) 12/12 11/13 11/13 11/13 12/12 12/12 10/14 12/12 fluorescent lamp fluorescent lamp fluorescent lamp fluorescent lamp fluorescent lamp mercury lamp mercury lamp fluorescent lamp Lightning equipment 40 W×2 40 W×2 40 W×2 40 W×2 40 W×2 250 W×1 250 W×2 40 W×2 Water surface illuminance (lx) 1000 900 540 900 900 1000 5000 1000 Round no. spawned eggs 3000 3000 100000 5000 1000 2000 100000 1500 Egg type adhesive demersal isolated epipelagic isolated epipelagic isolated epipelagic isolated epipelagic isolated epipelagic isolated epipelagic adhesive demersal Fertilized or not fertilized unfertilized unfertilized fertilized＊ fertilized fertilized fertilized fertilized Egg diameter (mm)＊＊ 1.76±0.16 (n=23) not measured 2.18 (n=1) not measured 2.24±0.08 (n=181) 2.12±0.11 (n=21) 1.90±0.05 (n=20) 1.99±0.04 (n=12) Larval total length (mm)＊＊ 3.47±0.13 (n=23) －－－3.53±0.09 (n=48) 2.51±0.39 (n=16) 3.00±0.07 (n=20) 3.98±0.27 (n=3) Other porcupines kept Ch. antillarum D. holocanthus Ch. antennatus Ch. antennatus Ch. reticulates D. nicthemerus absent absent in the same aquarium Ch. schoepfii D. hystrix Ch. antillarum Ch. antillarum D. liturosus

southern Australia western North Distribution＊＊＊ Tasman Sea central West Atlantic circumtropical Indo-West Pacific circumtropical circumtropical southern Australia Atlantic New Zealand＊＊＊＊＊: Fertilized by a male Ch. antillarum (Doi et al. 2015b) ＊＊: Measured by a micrometer attached to a microscope ＊＊＊: According to Leis (2006) and Froese and Pauly (2014) ＊＊＊＊: Leis (2006) suggested a possibility that fish from New Zealand is a different species

A B

Fig. 1. Adhesive demersal eggs of Allomycterus pilatus, 1.76 mm mean diameter (A), line drawing of hatched Allomycterus pilatus larva, 3.47 mm mean total length (B), adhesive demersal eggs of Diodon nicthemerus on pebble/sand substrate (red ellipse), 1.99 mm mean diameter (C), hatched Diodon nicthemerus larva, 3.98 mm mean total length (D). Head and trunk of both larvae covered with a “vesicular dermal sac” or “pliable shell”. Bars indicate 1 mm. Adhesive demersal eggs of porcupine puffers 359 relatively higher latitudes, representing four genera, References are known to spawn demersal eggs in shallow coastal Do i, H., T. Ishibashi and H. Sakai (2015a) Spawning and rearing of a porcupine puffer Cyclichthys orbicularis (Diodontidae, areas (Minami 1984). Pearcy (1963) suggested that Tetraodontiformes) in captivity. Aquacult. Sci., 63, 207-212. demersal flatfish eggs were an ecological adaptation Doi, H., Y. Zenke, H. Takahashi, H. Sakai and T. Ishibashi (2015b) acting to prevent dispersal by rapid coastal currents. Hybridization of burrfish (Chilomycterus spp.) in captivity revealed by AFLP and mtDNA sequence analyses. Ichthyol. However, ecological aspects of A. pilatus and D. nicthe- Res., 62, DOI 10.1007/s10228-015-0460-0. merus spawning sites are unknown. Froese, R. and D. Pauly (2014) FishBase, version 02/2014. Leis et al. (2013) discussed the trend within fami- http://www.fihbase.org, accessed 14 December 2014. Fujita, S. (1962) Lifecycle and aquaculture of main puffer fishes in lies in which species living at higher latitudes were Japan. Bull. Nagasaki Pref. Fish. Res. St., 2, 1-121, pls. 1-40 more likely to spawn demersal eggs with shorter (in Japanese). Fujita, S. and K. Matsuura (2014) Diodontidae. In “An Atlas pelagic larval duration and shorter dispersal dis- of Early Stage Fishes in Japan, 2nd edition” (ed. by M. tance. Allomycterus pilatus is distributed from south- Okiyama), Tokai University Press, Tokyo, pp. 1532-1534 (in ern Australia to New Zealand, and D. nicthemerus is Japanese). Leis, J. M. (1978) Systematics and zoogeography of the porcu- restricted to southern Australia (Leis 2006), being pinefishes (Diodon, Diodontidae, Tetraodontiformes), with relatively constrained compared to other diodontid comments on eggs and larval development. Fish. Bull., 76, 535-567. species distributed in lower latitudes and with wider Leis, J. M. (2006) Nomenclature and distribution of the species ranges (Table 1), the juveniles and young of which are of the porcupinefish family Diodontidae (Pisces, Teleostei). known to migrate to open pelagic waters (Nishimura Mem. Mus. Victoria, 63, 77-90. Leis, J. M., J. E. Caselle, I. R. Bradbery, T. Kristiansen, J. K. 1960; Fujita 1962; Leis 1978; Sakamoto and Suzuki 1978; Llopiz, M. J. Miller, M. I. O’Conner, C. B. Paris, A. L. Shanks, Fujita and Matsuura 2014). However, larval duration in S. M. Sogard, S. E. Swearer, E. A. Treml, R. D. Vetter and R. R. Warner (2013) Does fish larval dispersal differ between both A. pilatus and D. nicthemerus were similar to or a high and low latitudes? Proc. Royal Soc. B, 280, 1-9. little longer than those in other species, which spawn Minami, T. (1984) Early life history of flatfishes-III, characteristics pelagic eggs; 17 and 19 days in A. pilatus (Shimonoseki of eggs. Aquabiology, 6, 46-49 (in Japanese with English abstract). Marine Science Museum 2006a) and D. nicthemerus Nishimura, S. (1960) Some aspects of the natural history of por- (Shimonoseki Marine Science Museum 2010), respec- cupine puffers migrating to the Japanese waters I. spawning Japan. J. Ecol 10 - tively, and 17 and 13 days in Cy. orbicularis (Doi et and migration. ., , 6 11 (in Japanese with English abstract). al. 2015a) and D. holocanthus (Sakamoto and Suzuki Pearcy, W. G. (1963) Distributions and origin of demersal eggs 1978), respectively. within the order Pleuronectiformes. J. Cons. Perm. Int. Explor. Mer., 28, 232-235. Although the adaptive implications of the adhe- Sakamoto, T. and K. Suzuki (1978) Spawning behavior and early sive demersal eggs produced by A. pilatus and D. life history of the porcupine puffer, Diodon holacanthus, in nicthemerus remain somewhat ambiguous, adhesive aquaria. Japan. J. Ichthyol., 24, 261-270 (in Japanese with English abstract). non-dispersive eggs may be consistent with their Shimonoseki Marine Science Museum (2006a) Reports on the narrow distribution range. A fuller understanding of animal awarded a prize for breeding in captivity, 26. Deep- water burfish Allomycterus pilatus (natural). J. Japan. Assoc. diodontid reproductive adaptations is dependent upon Zoos Aquariums, 47, 68 (in Japanese). comparative studies of that family’s spawning ecology. Shimonoseki Marine Science Museum (2006b) Reports on the animal awarded a prize for breeding in captivity, 27. Birdbeak burfish Cyclichthys orbicularis (natural). J. Japan. Assoc. Zoos Acknowledgments Aquariums, 47, 68-69 (in Japanese). The authors are indebted to the staff of the Shimonoseki Marine Science Museum (2010) Reports on the animal awarded a prize for breeding in captivity, 22. Slender- Shimonoseki Marine Science Museum for technical spined porcupine fish Diodon nicthemerus (natural). J. Japan. assistance and Dr. G. S. Hardy for English corrections. Assoc. Zoos Aquariums, 51, 34-35 (in Japanese). Wolfsheimer, G. (1957) A spawning of porcupine puffers. Aquirium, 26, 288-290.