Color variation of the Puffer Arothron hispidus (Linnaeus) and comparison with A. reticularis (Bloch & Schneider).
The Whitespotted Puffer, Arothron hispidus (Linnaeus, 1758), type locality India, is the most wide-spread of the tetraodontid fishes, ranging from the Red Sea south to Western Cape, South Africa, east to the western Pacific from New South Wales to southern Japan, in Oceania to the Hawaiian Islands and islands of French Polynesia and in the eastern Pacific from Panama to the Gulf of California. It is a large species, attaining a total length of at least 48 cm.
The similar Arothron reticularis (Bloch & Schneider, 1801), also a large Indo-Pacific species with a type locality of India and ranging east to Fiji (Herre 1936), is much less common (for example, the Bishop Museum has 38 lots of A. hispidus, but only five of A. reticularis). It was not reported from the Red Sea until 1956, when Roux-Esteve identified a specimen, 197 mm in total length, from the island of Abulat (Abu Latt) in the Farasan Islands, southern Red Sea, as Tetraodon reticularis. Her record was included in three checklists of Red Sea fishes (Dor 1984; Goren & Dor 1994; Golani & Bogorodsky 2010). We cannot find a record of Arothron reticularis from the Indian Ocean west of the southern tip of India (Smith & Heemstra 1986; Fricke 1999; Manilo & Bogorodsky 2003). The westernmost locality appears to be Sri Lanka (Matsuura in Kimura et al. 2009). Also, A. reticularis is often found in estuaries and the young of Arothron reticularis are restricted to mangrove areas and the lower reaches of streams (Veeruraj et al. 2011). The Red Sea coast lacks permanent streams and well-developed estuaries. Roux-Esteve's Red Sea specimen (MNHN 52-252) was examined and photographed by the third author at the Museum National d'Histoire Naturelle in Paris (Fig. 1) and reidentified as A. hispidus.
Roux-Esteve is not alone in misidentifying specimens of Arothron hispidus as A. reticularis. Some Bishop Museum specimens were first mislabeled as A. reticularis, as well as some of the first author's photographs, and only three of the seven illustrations currently identified as A. reticularis in FishBase are correctly identified as this species. Shen et al. (1993: pl. 205, fig. 7) used an illustration of A. reticularis to represent A. hispidus. Adding to the confusion has been the extreme variation in color exhibited by what we believe to be one species, Arothron hispidus, in the Red Sea. The most perplexing are large individuals that have been photographed underwater with either a reticular or a linear pattern instead of a pattern of mainly white spots. We include here a diagnosis of A. hispidus, a comparison with A. reticularis and photographs of both species.
Specimens for the present study are from the Bishop Museum, Honolulu (BPBM), Museum National d'Histoire Naturelle, Paris (MNHN), Universitat Humboldt, Museum fur Naturkunde, Berlin (ZMB) and Uppsala Universitet Zoologiska Museet, Uppsala.
We asked representatives of the Senckenberg Museum in Frankfurt and the U. S. National Museum of Natural History in Washington, D.C., to see if their collections held any adult specimens of Arothron hispidus with a linear or reticular color pattern. None were found.
Figures 1-8 are specimen photographs of A. hispidus, in order west to east, from the Red Sea to the Line Islands in the Pacific. Figures 9-17 are underwater photographs of A. hispidus in the Red Sea, and Figures 18-22 are photographs of A. reticularis, one of which is a juvenile specimen in the Fisheries Research Laboratory of Mie University, Japan (FRLM).
Arothron hispidus (Linnaeus, 1758)
Tetraodon hispidus Linnaeus, 1758: 333 (type locality, India).
Tetraodon perspicillaris Ruppell, 1829: 63 (type locality, Red Sea).
Tetraodon semistriatus Ruppell, 1837: 58, pl. 16, fig. 3 (type locality, Massawa, Eritrea).
Tetrodon laterna Richardson, 1845: 124, pl. 61, fig. 2 (type locality, Canton, China).
Tetrodon pusillus Klunzinger, 1871: 645 (type locality, El Quseir, Red Sea).
Arothron hispidus Matsuura in Masuda et al. 1984: 364, pl. 331 H (Indo-Pacific).
Diagnosis: Dorsal fin rays 10 or 11; anal fin rays 9-11; pectoral rays 17-19; small spinules on head and body except for snout, posterior caudal peduncle and base of fins; snout length 4.6-6.1 in standard length (SL); nasal organ with two fleshy flaps bifurcating from common base; bony ridge above eye, interorbital space concave; bony interorbital width 4.8-7.0 in SL; anal fin origin below or posterior to rear base of dorsal fin; caudal fin rounded, posterior margin irregular, 2.6-3.8 in SL; color extremely variable, most often olivaceous with small white spots, white ventrally, with dark body color extending ventrally into the white ventral part of head and abdomen appearing as bars (three on head, three on abdomen); base of pectoral fin within vertically oval black spot containing a few white or yellow curved lines and/or small spots, often with one or more white lines encircling fin base; subadults with white spots often forming circle around eye and adults may have several complete white rings (Fig. 11 and Lieske & Myers 2004: 220, lower fig.). Subadults (Fig. 4) and juveniles (Fig. 6) sparsely spotted with white. With growth, white spots become more numerous. Some individuals with white lines, as shown in Figures 10 and 12, while others (Figs 11, 13, 14) remaining white-spotted, except for rings around eyes and gill openings; others developing reticular pattern (Figs 15 and 16) or a mainly linear pattern (Fig. 17). Base of dorsal fin usually with few white spots; anal fin generally none. Caudal fin varying from having only a few white spots on base to being almost completely white-spotted; some specimens with caudal fins having mixed spots and lines; still others with linear or reticular pattern. Largest specimen reported, 48 cm TL.
Comparison with Arothron reticularis: Because puffers are so variable in form, it is difficult to find morphological characters to distinguish some species from close relatives. We can confirm that the most important difference, as reported by Matsuura (1999), in separating A. hispidus from A. reticularis, is the distribution of the small dermal spinules on the body. They cover the entire body in A. reticularis, except for the region around the mouth and the base of the fins, whereas they are absent on the snout and at least the posterior half of the caudal peduncle of A. hispidus (see Fig. 4). Wheeler (1991: 192, Fig. 29) provided a photograph of Linnaeus' holotype of Tetraodon hispidus, ZMUU 102, 93 mm SL, at the University of Uppsala in Sweden. The spinules are clearly absent from the snout and all of the caudal peduncle. One of two syntypes of Tetrodon reticularis Bloch & Schneider at the Museum fur Naturkunde der Humboldt-Universitat, Berlin is lost (Paepke 1999). Figure 18 is a photograph of the remaining syntype, ZMB 4259, 185 mm SL, from Tranquebar, India. Spinules can be seen on the snout before the eye and over the caudal peduncle. Matsuura (1999) also reported that A. reticularis has a wider interorbital space than A. hispidus.
Like A. hispidus, A. reticularis is variable in coloration. It can be distinguished in color by having continuous dark brown bands that curve from below the eye across the abdomen and there are no ventral extensions of the dark body color into the pale ventral part of the head and body. Also, for any given size, the white spots posteriorly on the body and caudal fin are larger in A. reticularis and they more uniformly cover the caudal fin, whereas in A. hispidus they may be missing from the posterior part of the fin, if not the entire fin. We present color illustrations of an adult of A. reticularis (BPBM 28931, 355 mm SL) from the Great Barrier Reef (Fig. 19); a subadult (BPBM 7431, 153 mm SL) collected in fresh water from the Mizucho River, Babelthuap, Palau (Fig. 20), a first record for Micronesia; an underwater photograph of an adult taken by Robert F. Myers at Baie de Prony, New Caledonia (Fig. 21), a first record for the island; and a juvenile from the south-west coast of Thailand provided by Seishi Kimura (Fig. 22).
Arothron hispidus and A. reticularis are both well illustrated in color in Masuda et al. (1984: pl. 331), Masuda & Kobayashi (1994: 430), and Allen et al. (2003: 441).
Remarks: Arothron hispidus can be found in a variety of habitats from coral or rocky reefs to open sand or mud substrata, seagrass beds, algal flats, or estuaries, from depths of 1-99 m (Struhsaker 1973). It is more often seen in sheltered than exposed waters, and more often on soft than hard substrata. It may at times be seen at rest on sand, algal turf, or seagrass.
Bremert & Ormond (1981) reported Arothron hispidus feeding in the Red Sea on coral, tunicates, sea urchins and brittle stars, adding that it is a significant predator of the Crown-of-Thorns Starfish (Acanthaster). They described its mode of feeding on this venomous asteroid in detail. Randall (1985) wrote of the extremely varied diet: algae (including Jania and Halimeda), bivalves, gastropods, tunicates, sponges, corals, zoanthid anemones, crabs, tube worms, sea urchins, brittle stars, starfishes (including Acanthaster), hermit crabs, hydroids and detritus.
The different English common names reflect the variation in color pattern: Whitespotted Puffer, Stripebelly Puffer, Spiny Balloonfish, and Stars-and-Stripes Puffer.
One Hawaiian name, Makimaki, may be in reference to its toxicity (Titcomb 1972). This species is one of the most virulently poisonous of tetraodontid fishes (Halstead 1967). Yamada in Nakabo (2002) reported the skin, testes, liver and ovaries toxic, adding that there are conflicting reports on the toxicity of the flesh.
Ruppell (1829) described Tetraodon perspicillaris from the Red Sea, noting the white rings around the orbit and branchial opening. His species name is derived from the Latin perspicillum meaning spectacles, in obvious reference to the rings around the eyes. Ruppell (1837: 58, pl. 16, fig. 3) described a second species as Tetraodon semistriatus. His illustration is the same color form as shown here by Figure 12 (total length estimated as 32 cm when the photo was taken). The second Ruppell name (semistriatus) is in reference to the body being partly lined. Klausewitz (1960) and Tortonese (1968) treated the Red Sea population as a subspecies, Arothron hispidus perspicillaris. The Red Sea population of Arothron hispidus is more densely white-spotted at a given size (Figs 2, 3, 10-13) than that of the Indian Ocean (Figs 4, 5; Smith in Smith & Heemstra 1986: fig. 263; Debelius 1993: 308).
As noted by Matsuura in Masuda et al. (1984: 364, pl. 331, fig. H), Matsuura (1999: 130), and Figure 7 here, the Pacific Ocean population of Arothron hispidus differs in color from that of the Indian Ocean in having narrow wavy dark stripes ventrally on the body and fewer white spots. Figure 8 from Kiritimati in the Line Islands, however, is an exception in lacking the narrow dark stripes ventrally on the body and in having numerous white spots (as well as bright yellow pectoral fins).
We have no specimens of large individuals of Arothron hispidus from the Red Sea that exhibit such variable color pattern and express here the need for such specimens. Perhaps some of the variation is a result of sexual dichromatism. Molecular study would be most welcome. It would also be useful in deciding if taxonomic recognition is warranted for the apparent different populations within the Indo-Pacific region.
We thank Dr. Peter Bartsch of the Museum fur Naturkunde der Humboldt Universitat zu Berlin for his photograph of the existing syntype of Arothron reticularis, Dr. Seishi Kimura of the Fisheries Research Laboratory of Mie University for providing his photographs of juvenile specimens of Arothron hispidus and A. reticularis from the Andaman Sea, Jean Louis Rose and Richard Field for their underwater photographs of A. hispidus taken in the Red Sea, and Robert F. Myers for his underwater photograph of A. reticularis from New Caledonia. The most useful reference for this study was the review of the genus Arothron by Keiichi Matsuura (1999), and we thank him for additional information. We are grateful to Dr. Tilman Alpermann of the Senckenberg Museum, and Dianne Pitassy and Dr. Jeffrey T. Williams of the U. S. National Museum of Natural History for searching for adult specimens of Arothon hispidus for us. The second author acknowledges with gratitude the support for his fieldwork in the Red Sea from the Faculty of Marine Science of King Abdulaziz University, Jeddah, Saudi Arabia. The third author adds special thanks to Romain Causse, collection manager, Ichthyologie, Museum National d'Histoire Naturelle in Paris, for his assistance. Helen K. Larson, Robert F. Myers and Fareed Krupp reviewed the manuscript and provided very helpful comments.
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John E. Randall (1), Sergey V. Bogorodsky (2) and Jean Michel Rose (3)
(1.) Bishop Museum, 1525 Bernice St., Honolulu, HI 96817-2704, USA. E-mail: firstname.lastname@example.org
(2.) Station of Naturalists, Omsk, Russia. E-mail: email@example.com
(3.) Institut H.E. Sauvage, 56, rue du Dr. Brousse, 62360 St., Etienne-au-Mont, France.
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|Author:||Randall, John E.; Bogorodsky, Sergey V.; Rose, Jean Michel|
|Publication:||aqua: International Journal of Ichthyology|
|Date:||Jan 15, 2012|
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