aqua Journal of Ichthyology and Aquatic Biology Vol. 8 (1), February 2004

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Daytime hunting behaviour of Echidna catenata (Muraenidae): why chain morays foraging at ebb tide have no followers

1 1, 2 Ivan Sazima and Cristina Sazima

1) Departamento de Zoologia and Museu de História Natural, Caixa Postal 6109, Universidade Estadual de Campinas, 13083-970 Campinas, São Paulo, Brazil. Fax: +55 (19) 3289 3124. E-mail: [email protected] 2) Departamento de Zoologia, Caixa Postal 199, Universidade Estadual Paulista, 13506-900 Rio Claro, SP, Brazil

Accepted: 17.11.2003

Keywords gar nicht folgen und das Beutefangverhalten zu ihrem Reef fishes, foraging behaviour, feeding specializa - Vorteil nutzen können. tion, prey handling, Muraenidae, heterospecific associ - ations, SW Atlantic Résumé La fouille en plein jour de la murène Echidna catenata Abstract pour capturer des crabes sur des écueils et dans les The daytime foraging of the chain moray (Echidna mares tidales a été étudiée dans l'archipel Fernando de catenata) on grapsid crabs on exposed reefs at ebb Noronha, Atlantique équatorial ouest (03° 50' S, 32° 25' tide and in tide-pools was studied in the Fernando de W). Quatre stratégies de chasse ont été observées Noronha Archipelago, western Equatorial Atlantic sous l'eau comme à l'air libre; (1) la fouille au bord des (03°50’S, 32°25’W). Four hunting tactics were mares et à la base des rochers, en sondant les fentes recorded both in and out of the water: (1) search at et les creux; (2) l'approche furtive de proies préalable - pool rims and rock bases, poking into crevices and ment ciblées; (3) la chasse à la proie; (4) en piégeant à holes; (2) stealthy approach to previously sighted partir de creux et de bases de rochers. Comme cette prey; (3) chasing of prey; (4) ambush from crevices murène se sert de plusieurs stratégies et que sa chasse and under rocks. As the chain moray uses varied aux crabes est le plus souvent orientée par la vue, sa hunting techniques and its crab hunting is mostly visu - fouille généralement discrète n'attire que peu l'attention ally guided, its generally unobtrusive foraging attracts de poissons des mares tidales. Une partie des fouilles little or no attention from tide-pool fishes. Part of the s'effectue hors de l'eau sur des récifs exposés; pour foraging is done out of the water on exposed reefs; cette raison, les poissons ne sont pas à même de suivre fish are therefore unable to follow the moray and take la murène et de profiter de ses activités de chasse. advantage of its hunting activities. Resumo Zusammenfassung O forrageamento diurno da moréia-listada (Echidna Untersucht wurde das tagaktive Verhalten der Ketten - catenata) sobre caranguejos grapsídeos, na parte muräne Echidna catenata beim Fang von Krabben exposta de recifes e nas poças durante a maré baixa, (Grapsiden) auf bei Ebbe frei liegenden Riffen und in foi estudado no Arquipélago de Fernando de Noronha, Gezeitentümpeln im Gebiet des Fernando-de-Noronha- Atlântico Oeste-equatorial (03°50’S, 32°25’W). Quatro Archipels im äquatornahen West-Atlantik (03°50‘S, táticas de caça foram registradas, tanto sob, como fora 32°25‘W). Vier Jagdtechniken konnten im Wasser und da água: (1) procura ativa em bordas de poças e bases außerhalb des Wassers festgestellt werden: (1) Suche de rochas, esquadrinhando frestas e tocas; (2) aproxi - an Tümpelrändern und auf Felsgrund, gezielte Kontrolle mação sorrateira à presa previamente avistada; (3) per - von Spalten und Löchern; (2) heimliche Annäherung an seguição da presa; (4) tocaia sob rochas e em frestas. vorher gesichtete Beutetiere; (3) Verfolgungsjagd; (4) A moréia-listada usa repertório variado de caça e sua Auflauern der Beutetiere vom Versteck in Spalten und procura por caranguejos é guiada principalmente pela unter Steinen. Wegen der Bandbreite der eingesetzten visão. Seu forrageamento discreto atrai pouca ou Techniken und der überwiegend optischen Kontrolle, all - nenhuma atenção dos peixes nas poças de maré. Parte gemein wegen der wenig auffälligen Form des da sua atividade é feita fora da água e, portanto, Nahrungserwerbs, ziehen die Kettenmuränen bei der nenhum peixe é capaz de seguir a moréia e tirar pro - Krabbenjagd kaum oder gar nicht die Aufmerksamkeit veito da sua atividade de caça. Gezeitentümpel bewohnender Fische auf sich. Ein Teil des Nahrungserwerbs erfolgt außerhalb des Wassers Sommario auf frei liegendem Riffgrund, sodass Fische der Muräne Il foraggiamento diurno della murena catenata

1 aqua vol. 8 no. 1 - 2004 Daytime hunting behaviour of Echidna catenata (Muraenidae): why chain morays foraging at ebb tide have no followers

(E chidna catenata) sui granchi grapsidi delle barriere lowed whole (see Miller, 1989, for handling behaviour in rocciose esposte durante il riflusso e nelle pozze di ma- captive chain morays feeding on large prey). rea è stato oggetto di studio nell’Arcipelago Fernando de Noronha, Atlantico occidentale equatoriale (03°50’S, Methods 32°25’W). Sono documentate ben quattro tecniche di Fernando de Noronha Archipelago (03°50’S, caccia, fuori e dentro l’acqua: (1) ricerca al margine della 32°25’W) lies about 345 km to the east of Cape São pozza e alla base delle rocce insinuando il muso tra Roque in north-eastern Brazil (see Maida & Ferreira, anfratti e crepe rocciose; (2) avvicinamento furtivo ad 1997 and Carleton & Olson, 1999, for map and descrip - una preda già individuata; (3) caccia della preda; (4) tion). Field observations were made on tide-pools and agguato teso tra gli anfratti e le rocce sommerse. Poiché areas of the reef exposed at ebb tide, in the Enseada la murena catenata usa varie tecniche di caccia e i das Caieiras, Buraco da Raquel, and Praia do Boldró, granchi che ne sono oggetto vengono individuati attra - during June and October 2001, June 2002, and May verso la vista, le sue abitudini innocue attirano scarsa and June 2003. attenzione da parte degli altri pesci della barriera. Inoltre Foraging chain morays were observed and followed at il foraggiamento avviene in parte fuori dell’acqua su bar - ebb tide during daylight hours, in sessions totalling 1105 riere esposte e, pertanto, i pesci sono impossibilitati a min over 17 non-consecutive days. In observation ses - seguire la murena e trarre vantaggio dalla sua attività. sions lasting from 10-55 minutes we used focal animal samplings, in which all instances of specified actions Introduction were recorded (Altmann, 1974). During these observa - Moray eels (Muraenidae) and snake eels (Ophichthi - tions, we focused on the foraging behaviour of the dae) forage mostly by poking about in holes and moray and the reaction of fishes towards it, as well as crevices, feeding on invertebrates and fishes (Dubin, on the hunting tactics and handling of prey by this crab 1982; Abrams et al ., 1983; Diamant & Shpigel, 1985). predator. We also recorded the feeding behaviour of Foraging morays usually disturb the substrate and flush other fishes while a moray was handling its prey. Live out fishes and crustaceans from their hiding places, an and dead sally lightfoot crabs (Grapsus grapsus) (great - activity that attracts several species of opportunistic car - est carapace width 2-7 cm) were released near foraging nivorous fishes which follow the morays to feed on the morays so as to observe hunting and handling behav - exposed prey both by day (Dubin, 1982; Diamant & iour during staged encounters. Dead crabs were gently Shpigel, 1985; Strand, 1988) and at night (Borges & squeezed to release presumed chemical cues to the Castro, 2003). Some of these opportunist predators are morays. To assess the importance of vision in the for - even attracted to a stationary moray and make contact aging behaviour of the chain moray, we used a nylon to induce it to move on (Dubin, 1982; DeLoach 1999; IS thread to drag decoy marine turtles in front of ambush - and CS, pers. obs.). ing or actively searching morays, both in and out of the The chain moray (Echidna catenata) inhabits shallow water. The miniature turtles were 4-5 cm long and made reef sites in the tropical Atlantic, preying especially on of acrylic (orange) or of rubber (green and black). In crab (Randall, 1967, 1999; DeLoach, 1999). The present some of the tests the decoy turtles were smeared with study describes the daytime foraging behaviour of the liquid squeezed from a dead crab so as to be able to chain moray in the Fernando de Noronha Archipelago compare the moray’s reaction to untreated decoys and (03°50’S 32°25’W), north-eastern Brazil. Because Böh - those smelling of crab. lke & Chaplin (1968) recorded a chain moray chasing a Initial estimates of the morays’ total length (TL), were Grapsus sp. crab out of the water, we thought that this later checked against measured live individuals. Nine moray might rely on vision to find its prey. (See Chave & morays were recognized by conspicuous individual Randall, 1971 for similar behaviour in the Pacific moray markings (white patches or black blotches and spots on Gymnothorax pictus .) If this assumption is correct, this particular body areas). Voucher moray specimens are type of foraging would disturb the substrate less than deposited at the Museu de Zoologia da Universidade de poking at it and stirring it up, which attracts opportunistic São Paulo (MZUSP 47479) and Museu de História Nat - followers (Dubin, 1982; Strand, 1988). Thus we also ural da Universidade Estadual de Campinas (ZUEC hypothesised that foraging by the chain moray would 5804). Colour photos of foraging and prey handling preclude following behaviour by most, if not all fishes, morays were scanned and filed in ZUEC; three of these especially since the hunting takes place in tide-pools and are available in FishBase (Froese & Pauly, 2003). on exposed reefs at ebb tide. We therefore addressed three main questions in our study: (1) what are the hunt - Results ing tactics of the chain moray ? (2) is vision important in Thirty-seven episodes of daytime foraging by chain its foraging? (3) is the moray followed by other fishes, as morays, involving at least 22 individuals (30-70 cm TL) are other eel species during their daytime foraging activ - were recorded in Fernando de Noronha. The morays ities? Since we found the remains of several crabs on moved over tide-pools and reef areas exposed at ebb the reef, we also addressed the question of how the tide (Figure 1). While actively foraging in the shallows or chain moray deals with prey that is too large to be swal - out of the water, they were extremely wary and quickly aqua vol. 8 no. 1 - 2004 2 Ivan Sazima and Cristina Sazima hid under rocks or fled to deeper water when (1) active search at pool rims and rock bases (visual approached (even a movement 2-3 m away from an inspection), including poking into crevices and holes alert moray caused it to flee). The morays were often (mostly tactile and/or chemical inspection?) One con - observed with the body partly or totally exposed when spicuous characteristic of this tactic (searching) is that on the move and searching for prey. The time spent out while poking about, the morays moved slowly and unob - of the water while foraging ranged from 3 to 24 min. We trusively, causing little disturbance in the substrate. This recorded four main hunting tactics for the chain moray, feature probably explains why chain morays have only both in the pools and out of the water: a few or no followers when hunting (see below).

Fig. 1. Above: Rocky reef exposed at ebb tide in Fernando de Noronha Archipelago. Below: A large (65 cm TL) chain moray, Echidna catenata, searching for a crab it had struck at and missed (seen on the rock above and to the left of the moray). Photos by I. Sazima.

3 aqua vol. 8 no. 1 - 2004 Daytime hunting behaviour of Echidna catenata (Muraenidae): why chain morays foraging at ebb tide have no followers

(2) stealthy approach to previously sighted prey; any of the other three tactics. A moray would hide under (3) pursuit of prey both in and out of the water; a rock in a pool ready to strike and catch an intended (4) ambush from beneath rocks or from concealment prey (Figure 2, Table I). If unsuccessful, it either pur - within crevices, the head sometimes barely visible (a sued its prey or left the pool and began to move over the tactic mostly employed in pools). exposed part of the reef, conducting a visual search for No regular or predictable sequence in these hunting the missed crab. If this crab or another was spotted, the tactics was perceived, except for chasing which mostly moray approached it stealthily and struck again, (Figure occurred after missing a strike (Figure 1) resulting from 3) with or without success. On missing a strike, the

Fig. 2. Ambush by a chain moray (60 cm TL) from under a rock in a pool. Above: Sally lightfoot crabs crossing a tide- pool towards a large rock. Below: The moray striking from the water at a crab which had climbed the rock near the ambush site (other crabs are visible on nearby rocks). Photos by J. P. Krajewski. aqua vol. 8 no. 1 - 2004 4 Ivan Sazima and Cristina Sazima

Table I. Hunting tactics and relative hunting success (%) of chain morays (Echidna catenata) (n=31) during daytime for - aging for sally lightfoot crabs (Grapsus grapsus) at ebb tide on reefs in the Fernando de Noronha Archipelago, off north- east Brazil.

Hunting tactic Strikes Missed *Snatched **Ingested n= (%) n= (%) n= (%) n= (%) Ambush 11 (35.5) 3 (27.2) 8 (72.7) 5 (45.4) Search 7 (22.6) 4 (57.1) 3 (42.8) 2 (28.5) Stealthy approach 7 (22.6) 1 (14.3) 6 (85.7) 5 (71.4) Pursuit 6 (19.3) 1 (16.6) 5 (83.3) 4 (66.6)

Total 31 (100) 9 (29.0) 22 (70.9) 16 (51.6)

*Crabs held after strike, even if prey sheds legs and escapes. ** Crab ingested mostly whole = successful tactic result. moray chased the crab if it was in sight and moving, or motionless treated decoys (n= 7) always attracted the searched around the spot where the strike had missed. morays after intervals varying between 15 and 70 sec, During this searching, the moray repeatedly followed its when they snatched the decoy and hid. exploratory path (in one case up to eight times). After Before striking, the anterior part of the moray’s body some time out of the water, the moray entered a pool assumed a sigmoid curve. The moray was able to strike and sought a hiding place, but it was not always clear with its body partly or entirely out of the water (Figure 2), whether it was ready to ambush again or was simply usually striking from a distance of about 5 to 10 cm. resting. Six individual morays (35-45 cm TL) observed When the moray struck at its prey from below or side - for 12-55 minutes, moved between 2.5 and 6 metres ways the crabs were seized by their legs, but when the while foraging. One of them (35 cm TL) explored three moray struck from above (Figure 3) they were seized by pools in succession and struck at crabs seven times their rear or the middle of the carapace. A crab snatched over a period of 55 minutes. Another of similar size by its leg often escaped by detaching the seized moved about 4 metres while inspecting the base of a appendage. When this happened, the moray would rock on the exposed reef, and struck only once during chase the crab for up to 5 m, even if the chase was com - this period. Results of the four different hunting tactics of pletely out of the water on the exposed part of the reef. the chain moray varied, with an overall foraging success Crabs crossed tide-pools either by walking on the of about 50% (Table I). bottom or by running up to 3 m on the surface of the Chain morays appear to rely heavily on vision to detect water. When walking, they could be seized either by a movement of their prey when foraging. Moving crabs moray in ambush or one in search of prey. They stimulated prompt orientation of the moray towards became an easier target, more visible to a moray them while motionless crabs went undetected even at when attempting to cross a pool by running across its very close quarters (2-5 cm). Movement appears to trig - surface (Figure 2). Indeed, an easy way to locate a ger the strike. Stealthily approaching a grazing crab, a moray in ambush would be to make a crab run over moray was distracted by a darting goby; it struck at the the surface of the water. Any moray present would fish, then failed to capture the crab. It then struck at a strike at the crab and try to seize it. snail, Nerita ascensionis (Neritidae), which was moving Live crabs released in staged encounters (n=8) were slowly near the now motionless crab. In another quickly perceived while moving, and were either instance, a moray was seen following a line of crabs approached stealthily if far from the moray, or if close, moving along the rim of a pool, obviously responding to struck at almost immediately. Dead crabs (n=5) were their movements. The moray suddenly struck at the located after from 10-50 seconds, but were seized and nearest crab, but missed, whereupon the crabs fled to a handled in the same way as live prey. In both natural higher part of the rock. and staged encounters small crabs were swallowed Simple field tests confirmed that morays rely on visual whole, whereas larger ones were torn apart by a combi - orientation when hunting. In all staged encounters nation of tugging, rotating, knotting and thrashing move - (n=11) the morays visually followed and approached ments of the moray (see Miller, 1989 for figures). Han - untreated decoy turtles as they were dragged along. In dling time was related to prey size, with the largest crabs 10 of the 11 encounters the decoys were snatched (Fig - (carapace width 2.3-3.2 times greater than moray’s ure 4) while in movement (in the other instance the head width) being broken up and swallowed in from 90 decoy was only briefly inspected). After seizing the to 240 sec. decoy, the morays tried to retreat with the “prey” in their Uneaten crab remnants attracted small, common tide- mouth. Motionless untreated decoys (n= 8) elicited no pool fishes such as the goby Bathygobius soporator and visible reaction from the morays. On the other hand juvenile damselfish, Abudefduf saxatilis . Small chain

5 aqua vol. 8 no. 1 - 2004 Daytime hunting behaviour of Echidna catenata (Muraenidae): why chain morays foraging at ebb tide have no followers morays (6-15 cm TL) were also attracted, taking rem - Bardach & Loewenthal, 1961; Chave & Randall, 1971), nants larger and heavier than themselves to a hiding but the relative importance of each cue is not known. place where they would be broken up and eaten. Our observations leave little doubt that stealthy In most instances, morays did not appear to be fol - approach and chase by chain morays are two visually lowed by other fishes. In 33 out of the total of 37 guided tactics used to catch crabs (see comments on observed foraging events no following took place. turtle decoys below). When lying in ambush in a tide- However, when a moray stirred the sandy bottom, pool, chain morays are obviously guided visually one or a few small or juvenile fishes (mostly gobies towards any moving object: even a moving shadow may and/or damselfishes) approached but moved away elicit a strike. The Pacific moray Gymnothorax pictus is shortly thereafter. another species that forages for crabs on exposed parts of the reef and relies mostly on vision to locate its prey Discussion (Chave & Randall, 1971). However, olfactory and/or tac - Mor ays active by day forage mostly by poking into tile cues probably prevail when the morays search in crevices and holes, and are presumably guided by olfac - crevices and holes in tide-pools. Simple field tests tory, tactile, and visual cues (e.g., Bardach et al ., 1959; performed with turtle decoys leave no doubt that the

Fig. 3. A chain moray (45 cm TL) foraging in tide pools. Above: Stealthily approaching a sally lightfoot crab, Grapsus grapsus, in a crevice (to the left of the moray). Below: Snatching a crab from above and behind following a stealthy approach. Photos by I. Sazima. aqua vol. 8 no. 1 - 2004 6 Ivan Sazima and Cristina Sazima hunting chain moray is guided by vision, especially while cessful hunting tactic. By contrast, stealthy approach out of the water, and probably also underwater. How - and pursuit seem to be the most successful, although ever scent also plays an important role, as demon - pursuit seems to occur mainly (if not exclusively) when strated by the attraction of morays to motionless decoys a moray misses a strike at the prey while hunting by any smelling of crab, and to squeezed dead crabs. The role of the other three tactics. Predators that hunt by ambush of scent orientation in the foraging behaviour of moray seldom chase their prey if the first strike misses (Keen - eels is documented for several species (e.g., Bardach et leyside 1979), thus the pursuit behaviour of the chain al. , 1959; Chave & Randall, 1971; Borges & Castro, moray is surprising, especially when it occurs out of the 2003). water. We suggest that the apparently lower success Our study shows that overall hunting success for the rate achieved while searching by poking about may be chain moray is surprisingly high (Table I), particularly in due to the moray grasping the crab mostly from the view of the keen eyesight, speed and agility of sally side, by the detachable legs. When the prey is lightfoot crabs (Meinkoth, 1981; IS & CS, pers. obs.). approached stealthily or chased, the moray will mostly Our records indicate that active searching (visual and/or grab it from behind or above, and the crab cannot free tactile and chemical inspection) may be the least suc - itself by shedding appendages.

Fig. 4. Foraging chain morays (35 and 50 cm TL) attracted to decoy turtles dragged nearby. Above: Emerging from under a rock to inspect a green and white rubber decoy. Below: Striking at an orange acrylic decoy. Photos by I. Sazima.

7 aqua vol. 8 no. 1 - 2004 Daytime hunting behaviour of Echidna catenata (Muraenidae): why chain morays foraging at ebb tide have no followers

Although foraging morays and other bottom-feeding receptors in fishes with special reference to moray eels are among the predators most sought by several eels ( Gymnothorax vicinus and G. moringa ). Copeia, opportunistic following fishes (Diamant & Shpigel, 1985; 1961 (1): 42-46. Strand, 1988; Borges & Castro, 2003; CS & IS, pers. Bardach, J. E., Winn, H. E. & D. W. Menzel. 1959. The obs.), we recorded no “true” followers for the diurnally role of senses in the feeding of the nocturnal reef foraging chain morays in Fernando de Noronha. The predators Gymnothorax moringa and Gymnothorax juvenile and small tide-pool fishes that benefit from the vicinus . Copeia, 1959 (2): 133-139. leftovers can hardly be called followers (e.g., Fricke, Böhlke, J. E. & C. C. G. Chaplin. 1968. Fishes of the 1975; Dubin, 1982; Diamant & Shpigel, 1985; Strand, Bahamas and adjacent tropical waters . Livingston 1988). The dietary specialization of the chain moray in Publications, Wynnewood, 771 pp. crabs is probably not related to the absence of follow - Borges, F. B. & R. M. C. Castro. 2003. Activity, habitat ers, since other tropical Atlantic eels that specialise in utilization, feeding behaviour, and diet of the sand crabs such as the snake eels Myrichthys breviceps and moray Gymnothorax ocellatus (Anguilliformes, M. ocellatus (Ophichthidae) are regularly followed by Muraenidae) in the South western Atlantic. Biota several species of opportunistic carnivorous fishes Neotropica, 3 (1): 1-7. (Dubin, 1982; DeLoach, 1999; IS & CS, pers. obs.). Chave, E. H. & H. A. Randall. 1971. Feeding behavior However, judging by their well-developed, downwards- of the moray eel, Gymnothorax pictus . Copeia, 1971 directed nostrils, and their hunting behaviour, it seems (3): 570-574. that ophichthid crab-eating eels are mostly oriented Carleton, M. D. & S. L. Olson. 1999. Amerigo Vespucci towards their prey by scent and/or touch. Habitually and the rat of Fernando de Noronha: a new genus and poking into holes and crevices and stirring up the sub - species of Rodentia (Muridae: Sigmodontinae) from a strate while foraging (Dubin, 1982; IS, pers. obs.), they volcanic island off Brazil’s continental shelf. American furnish the kind of stimuli that attract opportunistic fol - Museum Novitates , 3256 : 1-59. lowers (Fricke, 1975; Strand, 1988). Diamant, A. & M. Shpigel. 1985. Interspecific feeding When the chain moray pokes about in holes and associations of groupers (Teleostei: Serranidae) with crevices the virtual absence of followers may be octopuses and moray eels in the Gulf of Eilat (Aqaba). explained by the unobtrusive nature of the foraging Environmental Biology of Fishes, 13 (2): 153-159. depending as it does on visual cues and involving little DeLoach, N. 1999. Reef fish behavior: Florida, or no disturbance of the bottom. Additionally, the moray Caribbean, Bahamas . New World Publications, Jack - forages partly on the exposed part of the reef, where no sonville, 359 pp. fishes can follow to take advantage of its hunting activ - Dubin, R. E. 1982. Behavioral interactions between ity. We suggest that the Indo-Pacific muraenid Gym - Caribbean reef fish and eels (Muraenidae and nothorax pictus , which also forages on crustaceans and Ophichthidae). Copeia, 1982 (1): 229-232. fishes on reef areas exposed at ebb tide (Chave & Ran - Fricke, H. W. 1975. The role of behaviour in marine dall, 1971), also has few or no followers. symbiotic animals. Symposia of the Society of Experi - mental Biology, 1975 : 581-594. Acknowledgements Froese, R. & D. Pauly. (Eds.) 2003. FishBase . World We thank the Centro Golfinho Rotador (J. M. Silva-Jr.) Wide Web electronic publication. www.fishbase.org. and Projeto Tamar (C. Bellini) for logistic support; R. M. Keenleyside, M. H. A. 1979. Diversity and adaptation in Bonaldo and J. P. Krajewski for help with field work (the fish behaviour . Springer, Berlin, 208 pp. latter also for photographing morays); J. Zuanon for Maida, M. & B. P. Ferreira. 1997. Coral reefs of Brazil: suggestions for improving the manuscript; K. S. Brown, an overview. Proceedings of the International Coral Jr. and two anonymous reviewers for improving the Reef Symposium. 8: 263-274. English and the Ms as a whole; the IBAMA (C. Bellini Meinkoth, N. A. 1981. The Audubon Society Field and M. A. Silva) for permission to study reef fishes at the Guide to North American seashore creatures . Alfred A. Parque Nacional Marinho de Fernando de Noronha; the Knopf, New York, 799 pp. CNPq and FAPESP for essential financial support. This Miller, T. J. 1989. Feeding behavior of Echidna nebu - paper is dedicated to Ricardo Sazima for his continuous losa , Enchelycore pardalis , and Gymnomuraena zebra support, especially helping in the PC operations. (Teleostei: Muraenidae). Copeia, 1989 (4): 662-672. Randall, J. E. 1967. Food habits of reef fishes of the References West Indies. Studies on Tropical Oceanography, 5: Abrams, R. W., Abrams, M. D. & M. W. Schein. 1983. 665-847. th Diurnal observations on the behavioral ecology of Gym - Randall, J. E. 1999. Caribbean reef fishes .4 ed. T.F.H. nothorax moringa (Cuvier) and Muraena miliaris (Kaup) Publications, Jersey City, 368pp. on a Caribbean coral reef. Coral Reefs, 1: 185-192. Strand, S. 1988. Following behavior: interspecific for - Altmann, J. 1974. Observational study of behavior: aging association among Gulf of California reef fishes. sampling methods. Behaviour, 49 : 227-265. Copeia, 1988 (2): 351-357. Bardach, J. E. & L. A. Loewenthal. 1961. Touch aqua vol. 8 no. 1 - 2004 8 aqua, Journal of Ichthyology and Aquatic Biology

Historical overview of mugilid systematics, with description of Paramugil (Teleostei: Mugiliformes: Mugilidae), new genus

1 Javad Ghasemzadeh, Walter Ivantsoff and Aarn

1) Department of Biological Sciences, Macquarie University 2109, Australia. E-mail: [email protected]

Accepted: 17.11.2003

Keywords Introduction Mugilidae, osteology, Paramugil , systematics Mullets are spiny-rayed teleosts, distinguishable exter - nally by their distinctive body form and two well-sepa - Abstract rated dorsal fins, of which the first has one distinct spine, The history of the systematic relationships of the and three very closely-placed. Mullets are an ecologi - mugilids is reviewed, concluding with the modern con - cally diverse group, with a worldwide circumpolar distri - cept of Mugilidae comprising 17 genera with 80 species, bution, inhabiting the surface zone of oceans, estuaries one of five taxa comprising ‘Smegmamorpha’. Para - and some inland fresh waters. Fossil records of mullets mugil, new genus, is erected for P. georgii and P. par - date back to the Oligocene (Berg, 1940), lower mata , and 18 diagnostic morphological and osteological Oligocene (in France) (Berra, 1981), lower Oligocene, differences between Paramugil and Liza and/or Mugil upper Miocene and Pliocene (Svichenskaya, 1973). and/or Valamugil listed. The last author records fossils from France, Romania, Austria, Croatia, Majorca and from several former Zusammenfassung republics of the southern USSR. Nach einer historischen Übersicht zu den systema - Mullets occupy a relatively low position in the food tischen Beziehungen der Vertreter der Mugiliden wird web, and are thus relatively efficient secondary pro - das moderne Konzept der Mugilidae mit 17 Gattun - ducers of protein. Mullets are euryhaline and can be gen und 80 Arten dargestellt und als eines der fünf readily cultured under artificial conditions (Shehadeh Taxa verstanden, die zu den ‚Smegmamorpha‘ et al. , 1973). They comprise a large proportion of the gehören. Die neue Gattung Paramugil wurde an inshore fisheries of the world, meeting the subsis - Stelle von P. georgii und P. parmata eingerichtet. tence protein requirements of the peoples of the Genannt werden 18 morphologische und osteologis - Pacific basin, south-east Asia, India, the Mediter - che Unterscheidungsmerkmale zwischen Paramugil ranean, Eastern Europe, and many parts of Central und Liza und/oder Mugil und/oder Valamugil. and South America. Mullets form a lesser, yet valu - able, fishery resource in many European countries, Résumé the southern United States of America, Australia and On passe en revue l'historique des relations systéma - Japan. tiques des Mugilidés, pour aboutir au concept moderne The grey mullet Mugil cephalus Linnaeus is the only de Mugilidae comprenant 17 genres et 80 espèces, l'un cosmopolitan species, occurring between latitudes 42° des cinq taxons comprenant "Smegmamorphae". N and 42° S in all coastal waters of the world (Thomson, Pseudomugil, un genre nouveau, est créé pour P. 1963). Its physiological adaptations and behaviour allow georgii et P. parmata, sur base de 18 différences diag - it to move through all kinds of degraded habitats, nostiques morphologiques et ostéologiques entre Para - between fresh- and sea-water. Because of its ubiquity, mugil et Liza et/ou Mugil et/ou Valamugil. size and desirability as a food fish, M. cephalus is one of the most important fishery species, particularly for Sommario developing countries. La storia delle relazioni sistematiche dei Mugilidae With the increasing world demand for animal protein, viene rivisitata, portando ad un ridefinizione della any fish resource with the potential to contribute to this famiglia, comprendente 17 generi e 80 specie, e confer - need may be subject to future exploitation. There has mandola come uno dei cinque taxa facenti parte degli been considerable interest in the group (Oren, 1981) “Smegmamorpha”. Viene eretto un nuovo genere Para - and there is extensive literature on the biology of mullets mugil per le specie P. georgii e P. parmata; esso è and on their fisheries, (Thomson, 1963; Pillay, 1972). definito da 18 caratteri diagnostici morfologici e osteo - However, apart from taxonomic work, most studies logici che lo distinguono dai generi Liza e/o Mugil e/o have concentrated on commercial species, in particular Valamugil. M. cephalus . To assist planning for future sustainable

9 aqua vol. 8 no. 1 - 2004 Historical overview of mugilid systematics, with description of Paramugil (Teleostei; Mugiliformes; Mugilidae), new genus harvesting, it is appropriate to review the history of ence of a derived similarity between the pelvic girdle of mugilid systematics. mugilids and that of percomorph fishes contradicted the above alignment, suggesting an alternative alignment of The systematic position of Mugilidae mugilids with percomorphs, rather than atherinomorphs. Mullets are presently recognised as belonging to the Stiassny (1993) further investigated this character con - series Mugilimorpha with a single order Mugiliformes, flict, and examined the osteology and myology of the and a single family Mugilidae comprising two subfami - pelvic girdle (also Stiassny and Moore, 1992), branchial lies, Mugilinae and Agonostominae (Nelson, 1994). arches, primary and secondary pectoral girdle and fin Mugilidae was assigned to the suborder Percesoces, structure, extrascapular bones and opercular muscula - with Atherinidae, and Sphyraenidae (Jordan and Ever - ture in order to present more evidence in support of a mann, 1896a). Starks (1900) also considered these mugilimorph-atherinomorph alignment. The present three groups to be closely related, because of the simi - view of a close relationship between mugilids and lar branching of the posterior process of the epiotic, but Atherinomorpha follows Stiassny (1990, 1993) and questioned their homology. Although the skeleton of the Johnson and Patterson (1993). mugiloids and sphyraenoids superficially resembled Parenti (1993) rejected this view, suggesting that the that of atherinoids, Hollister (1937) noted an important atherinomorphs (excluding mugilids) were closer to the developmental difference between them. In Atherina the paracanthopterygians. It is thus concluded that mugilids lower hypural plate develops as a single entity, but in have some relationship to the last five families of Mugil and Sphyraena this plate forms from two distinct Gosline’s (1971) classification, but no close relationship elements. to the Sphyraenidae and Polynemidae. However, as On the basis of the abdominal position of pelvic fins, a indicated by Nelson (1994) (after Johnson and Patter - relatively primitive character, Berg (1940) recognised son, 1993), the best present summary of relationships Mugilidae as being closely related to Atherinidae, and places mugilomorphs, atherinomorphs, gasterostei- erected Mugiliformes (comprising Mugilidae and forms, synbranchiforms, and Elassoma in ‘Smeg - Sphyraenidae), distinct from Perciformes. Removal of mamorpha’, in an unresolved polytomy. Mugilidae from the suborder Percoidei was supported by studies of plasma proteins (Sulya et al ., 1960). Historical review of mugilid taxonomy Plasma proteins of mugilids were less complex than There are 281 nominal species of mullets, of which those of any other putative perciform family, and sug - approximately 80 are considered to be valid, assigned gested a relationship to some species of Cypriniformes to 17 genera (Thomson, 1964; Harrison and Howes, and Clupeiformes (Gunther et al ., 1961). In contrast, 1991; Nelson, 1994). plasma proteins of some species of the perciform fami - Mugil cephalus was recorded by Linnaeus in Systema lies Carangidae, Sciaenidae, and Scombridae, did not Naturae in 1758, presumably after Artedi [Artedi, Gen - differ greatly from those of Mugilidae. On this basis, era. Pisces. P. 32 (1738)]. Valenciennes (1836) pro - Mugilidae could be regarded either as a component, or posed the first worldwide revision, with the establish - derivative, of the most primitive perciform group. ment of five genera and 58 species, comprising “la The classification of Berg (1940) was widely accepted famille des Mugiloïdes”. Günther (1861) named this until Rosen (1964) assigned Atherinidae to Atherini - family Mugilidae, recognising three genera and 79 formes. On the basis of further morphological informa - species. Classification by these authors was mainly tion, Mugilidae, Sphyraenidae and Polynemidae were based on examination of external morphology, with an placed in Perciformes. Gosline (1968, 1971) grouped emphasis on shape of the mouth, dentition and lower Polynemidae, Sphyraenidae, Mugilidae, Melanotaeni - jaw characters. Although these ichthyologists implied idae, Atherinidae, Isonidae, Neostethidae and Phal - that there were a number of genera, due to the per - lostethidae in the perciform suborder of Mugiloidei, con - ceived paucity of useful taxonomic characters and a sidered to be one of the most primitive perciform taxa. wide range of similarity and overlapping features, many This classification was largely based on the absence of specialised forms were assigned to a single genus of a direct articulation between the pelvic girdle and the Mugil . cleithra in mugiloids (the two structures with an attach - Jordan and Swain (1884) reviewed the American ment in most other perciforms). Greenwood et al . (1966) species of marine Mugilidae, and identified three genera and Nelson (1984) concurred with Rosen (1964) in plac - and 12 species. Jordan and Evermann (1896a, b) ing Polynemidae, Sphyraenidae and Mugilidae in Perci - recognised two subfamilies, Mugilinae and Agonostom - formes, the other five families comprising the pre-acan - inae. Mugilinae were identified with flat labial teeth (dis - thopterygian Atheriniformes. tinguishable in juveniles, embedded in the flesh in Percomorpha was proposed as the sister group of a adults) connected to the jaws by elongate fibrous pedi - monophyletic Mugilomorpha plus a monophyletic cles, a ridged and grooved preorbital, and three anal Atherinomorpha, based on a series of derived similari - spines (in adults). Agonostominae were identified with ties in the branchial arches, jaw musculature and neural sessile teeth attaching directly to the jaws, a flat preor - arches (Stiassny 1990). On the other hand, the pres - bital, and two anal spines. Members of Mugilinae occur aqua vol. 8 no. 1 - 2004 10 Javad Ghasemzadeh, Walter Ivantsoff and Aarn in temperate waters worldwide, whilst Agonostominae genera (excluding fossils) worldwide, of which 13 gen - are confined to Central America, the western Indian era were recognised as valid, and described 17 species Ocean, tropical west Pacific, and south-west Indo- belonging to nine genera in Australia and the south Pacific. Pacific region. Thomson, in his subsequent revision of During the last century, numerous mullet genera and the mullets of the world (1981), considered 64 (of 282 species were described. Mohr (1927) reviewed the fam - nominal) species in 14 genera as valid, and presented ily, but did not consider all genera known at that time. a detailed description of distinctive characters and use - Popov (1931) divided the family into two subfamilies ful diagnostic features. (each consisting of eight genera): Mugilinae, inhabiting Senou (1988) reviewed the phylogenetic relationships inshore marine waters and estuaries; and Cestraeinae, of mullets, using osteological and morphological char - residing mainly in freshwaters. Some additional com - acters. He recognised 17 genera and 44 species in two prehensive regional revisions of this family were pub - subfamilies, Agonostominae (comprising three genera) lished by Weber and de Beaufort (1922) in the Indo- and Mugilinae (14 genera). Australian Archipelago; Oshima (1922), Liu and Shen The most recent worldwide account of Mugilidae was (1991a) and Shen (1994) in Taiwan; (1928, 1931, presented by Thomson (1997), who accepted 14 of 39 1934a) in Oceania; Roxas (1934) in the Philippines; described genera, and 64 of 282 nominal species, as Smith (1935, 1948) in South Africa; Fowler (1936), valid. A new species (Liza mandapamensis) was intro - Cadenat (1954) and Poll (1959) in West Africa; duced, and 18 species were classified as inquerenda . Athanassopoulos (1919) in the Mediterranean Sea; The identification and taxonomy of mullets has relied Popov (1929, 1930) in Russia and Europe; Borcea on external morphology, meristics, morphometrics and (1934) in the Black Sea; Trewavas and Ingham (1972) the structure of some internal organs. Characters which in the north-east Atlantic and the Mediterranean Sea; have been used by different authors include dentition Anderson (1982) in England; Whitehouse (1927), Deva- (Ebeling, 1957, 1961; Thomson, 1975; Farrugio, 1977), Sendaram (1951), Pillay (1962) and Day (1865a, scales (Cockerell, 1913; Jacot, 1920; Pillay, 1951; 1865b, 1878 and 1889) in India; Song (1981) in China; Thomson, 1981; Chervinski, 1984; Liu and Shen, Yoshino and Senou (1984) in Japan; Wongratana et al. 1991b), number of pyloric caeca (Perlmutter et al ., (1984) in Thailand; and Lee and Joo (1994) in Korea; 1957; Hotta and Tung, 1966; Luther, 1977), the alimen - and Harrison and Senou (2001) in the Western Central tary tract (Thomson, 1966), intestinal convolution Pacific. (Hotta, 1955), osteology (Ishiyama, 1951; Hotta and The most comprehensive generic revision of the fam - Tung, 1966; Sunny, 1971; Kobelkowsky and Resendez, ily (Schultz, 1946) drew attention to the taxonomic 1972; Luther, 1977; Mohsin, 1978 and Senou, 1988), importance of mouth parts and other qualitative charac - otoliths (Morovic, 1953), pharyngobranchial organ (Har - ters, and established criteria to distinguish the genera. rison and Howes, 1991), cranial lateral line patterns Of these, the more important were the nature of the (Song, 1981) and dentition, pigmentation and upper attachment of the maxilla, the curvature and melanophore patterns in identification of fry and juve - degree of exposure of the posterior angle of the maxilla, niles (van der Elst and Wallace, 1976; Cambrony, 1984; the relative thickness of the lips, the degree of coverage Reay and Cornell, 1988; Serventi et al ., 1996). by papillae and crenulations, the position (inferior or ter - Electrophoretic and molecular genetic studies (Peter - minal) of the mouth, the morphology and distribution of son and Shahadeh, 1975; Autem and Bonhomme, teeth, and the presence or absence of the symphysial 1980; Rosenblatt and Waples, 1986; Campton and knob. On the basis of these characters 13 genera were Mahmoudi, 1991; Menezes et al ., 1992; Crosetti et al ., recognised. 1993, 1994; Karunasinghe, 1995; Lee et al. , 1995, Smith’s (1948) generic revision of the South African 1996; Rossi et al ., 1996, 1998) have provided further mullets used Schultz’s (1946) characters, noting that insights in studies of population structure, but little Schultz did not examine worldwide representatives. insight into phylogeny. Smith (1948) confirmed the taxonomic value of the Mullets are speciose in the Indo-Pacific region (with 37 mouth parts, and erected four further genera. In a of 64 nominal species worldwide), but there is a dearth subsequent review Schultz (1953) accepted 14 valid of reliable taxonomic and descriptive information of genera. Indo-Pacific mullets at both generic and specific levels. Ingham’s (1952) comprehensive revision of the biol - Macleay (1880) presented an account of the Australian ogy and taxonomy of mullets (based principally on mullets, and subsequently described new genera and examination of the material in the British Museum of species of Indo-Pacific mullets (Macleay, 1884a, Natural History) recognised 13 genera and 64 species, 1884b). Ogilby, (1887) and Whitley (1930, 1941, 1945, and indicated that another 11 species were possibly 1948) described further genera and species. A compre - valid. Thomson (1954) conducted a revision of the mul - hensive guide to the mullets of the Indo-Australian Arch - lets of Australian waters and adjacent seas, based on ipelago was published by Weber and de Beaufort characters of mouth parts, dentition, digestive system, (1922). No further significant work appeared until Thom - morphometric and meristics. He listed 37 nominal son’s (1954) classic revision of the mullets of Australian

11 aqua vol. 8 no. 1 - 2004 Historical overview of mugilid systematics, with description of Paramugil (Teleostei; Mugiliformes; Mugilidae), new genus waters and adjacent seas. Thomson (1954) and Merrick thin, not papillate or crenulate, without fleshy lamellae and Schmida (1984) reported 17 species (of nine gen - between rami of lower jaw. Angle of dentary symphysis era) around Australia. Munro (1956) recorded 20 broadly obtuse. Lower lip thin, edentulous, directed for - species (eight genera) in Australian waters, and 16 wards, not folding down, and bearing a double sym - species (six genera) from New Guinea (Munro, 1967). physial knob at the tip. Teeth on both lips minute ciliform Since Thomson’s (1954) revision, there has been no or absent. Adipose eyefold moderately-developed, cov - comprehensive report concerning the phylogeny of mul - ering up to half of iris, and leaving a vertical oval space lets. Much of the research has been regional, concern - over the eye. Nostrils well-separated, posterior nostril ing aspects of the biology of one or more species. reaching above the upper rim of orbit. Interorbital flat to These studies include those of Harris (1968), Grant and slightly convex. Lacrimal with distinctly kinked anterior Spain (1975a, 1975b, 1975c, 1977), Grant et al. (1977), serrate margin, and squarish denticulate posteroventral Spain et al. (1980), Chubb et al. (1981), Lenanton et al. end. Maxilla slender, curving sharply posteroventrally (1984) and Langi et al. (1990). Some reasonable oste - (Fig. 2); maxilla posterior angle just posteroventral to ological information for Indo-Pacific mullets was corner of closed mouth, completely or partially con - reported by Luther (1977), and (to a lesser extent) cealed when mouth closed. Tongue raised and moder - Ishiyama (1951), Hotta and Tung (1966) and Mohsin ately keeled medially. Tongue, endopterygoid and basi - (1978), but none of these proposed phylogenies. Senou hyal dentigerous; palatine edentulous; vomer edentu - (1988) proposed a phylogenetic analysis, which lous or dentigerous. Gill rakers elongate. Scales ctenoid remains unpublished. Thomson (1997) presented an without membranous hind margin. evolutionary scheme for mullets, but not a substantiated First dorsal fin with stout spines, origin nearer to base phylogeny. of caudal fin than to snout tip. First dorsal and pelvic fins with long axillary scale. Origin of second dorsal fin at Genus Paramugil (New Genus) vertical through one to two-thirds of anal fin base; both Paramugil (Type species Mugil parmatus Cantor, fins slightly emarginate and scaled basally. Anal fin with 1850, by present designation). (Fig. 1) three spines and nine soft rays in adults. Dorsal inser - tion of pectoral fin horizontally at level of middle of pupil Diagnosis or slightly higher than its upper rim; pectoral fin usually Gross morphology: Characters distinguishing Para - not reaching to the origin of first dorsal fin; pectoral axil - mugil, Liza, Mugil and Valamugil are presented in lary scale rudimentary or absent. Pelvic fin shorter than Table I. Mouth terminal, oral cleft near-horizontal, lips pectoral.

1 cm m c 1

Fig. 1. Paramugil parmatus, NTM S.10469-014, 82.2 mm SL. Arrow indicates position of anus. aqua vol. 8 no. 1 - 2004 12 Javad Ghasemzadeh, Walter Ivantsoff and Aarn

Table I. Diagnostic differences between Paramugil and allied genera.

Paramugil Liza Mugil Valamugil adipose eyelid partially developed partially developed well developed partially developed maxilla slender, sharply curved stocky, sigmoid, slender, slightly curved slender, slightly curved posteromedially terminal hook posteromedially posteromedially maxilla posterior angle (usually) visible visible, forming a pad (usually) visible hidden visible or hidden when mouth closed basisphenoid present present absent present basioccipital absent absent absent present anteroventral process basioccipital rudimentary rudimentary rudimentary elongate posterolateral process intercalar reduced developed well developed well developed intercalar articulation simple complex complex complex with posttemporal urohyal posterior border simple simple produced as paired simple processes morphology of articular, distinct unremarkable unremarkable unremarkable palatine and lacrimal body scales posterior membranous, complete membranous, complete membranous, complete digitated margin pectoral axillary scale absent absent well developed well developed number of pyloric caeca 7-26 5-6 2 numerous predorsal pterygiophores simple simple forked and interlocked simple first dorsal pterygiophore straight or slightly curved straight or slightly curved distinctly curved straight or slightly curved anterior border proximal ribs anterior process moderately developed undeveloped moderately developed moderately developed anal rays/pterygiophores 9/10 9/10 8/9 9/10 abdominal vertebrae 10, present absent present present 11 haemal bridge

Pharyngobranchial organ with broad sulcus; its dentic - ulate area and valves variable in size. Stomach conical with well-developed gizzard-like muscle. Pyloric caeca unbranched and numerous. Intestine long with many convolutions. Two species: P. georgii and P. parmatus . Osteology: Articular elongate, approximately trape - zoid (Fig. 3); palatine elongate, with expanded anterior process (Fig. 4); lacrimal almost rectangular in lateral aspect, anterior serrate margin distinctly kinked, pos - teroventral angle squarish and denticulate (Fig. 5); eth - moid bilaminar; basisphenoid present and well devel - oped; intercalar reduced; articulation of intercalar and ventral arm of posttemporal simple; haemal arch pre - sent in vertebrae 10 and 11.

Discussion The holotype for Mugil georgii Ogilby is a 155 mm SL (190 mm TL) specimen. Ogilby (1897) commented that it was not a true Mugil and examination of further spec - imens was needed to clarify its status. The general Fig. 2. Paramugil georgii, AMS I.22722-052, 122 mm SL. appearance and characters, including the extent of adi - Scale bar: 1 mm. pose eyefold development, shape of maxilla, dentition,

13 aqua vol. 8 no. 1 - 2004 Historical overview of mugilid systematics, with description of Paramugil (Teleostei; Mugiliformes; Mugilidae), new genus scalation and scale structure, presence or absence of tion of specimens identified as L. parmata Cantor from rudimentary pectoral fin axillary scale, nine anal fin rays different localities suggests that this species is interme - and number of pyloric caeca, were equivocal. Thomson diate between Liza and Valamugil . Thomson (1997) (1978, 1997) assigned this fish to Valamugil on the commented on some characters of L. parmata including basis of the pectoral axillary scale, ctenoid scales with slight visibility of the maxilla below the corner of the membranous hind margin, concealed maxillary pad and closed mouth, long dorsal axillary scales, and relatively numerous pyloric caeca. Examination by the senior long pectoral and pelvic fins which superficially resem - author of the holotypes of M. georgii and M. nortoni bled Valamugil . It was also noted that L. parmata lacked Ogilby (135 mm SL) and a large number of specimens the long pectoral axillary scale and the fimbriate mem - of V. georgii strongly suggests that this species is sub - branous-edged scales, which are typical of Valamugil . stantially different from Mugil and Valamugil in many However morphological and osteological studies morphological and osteological characters. Examina - suggested a close affinity between L. parmata and

Anterior process

Fig. 3. Paramugil georgii, AMS I.22722-052, 122 mm SL. Articular in lateral aspect. Scale bar: 1 mm.

Fig. 4. Paramugil georgii, AMS I.22722-052, 122 mm SL. Fig. 5. Paramugil parmatus, ZMA 121.613, 59 mm SL. Palatine in lateral aspect. Scale bar: 1 mm. Lacrimal in lateral aspect. Scale bar: 1 mm. aqua vol. 8 no. 1 - 2004 14 Javad Ghasemzadeh, Walter Ivantsoff and Aarn

V. georgii . A phylogenetic analysis, based on computer Material examined - morphology analysis of extensive morphological characters, sepa - Institutional abbreviations follow Leviton et al. (1985). rated these two species as a distinct lineage genus from AMS B.8022 (55 mm SL), syntype of M. oligolepis , India, the rest of Indo-Pacific mullets (Ghasemzadeh, 1998). Calcutta; AMS I.22789-004 (74 mm SL), Queensland, Therefore Paramugil is erected for ‘Mugil’ parmatus and Norman River; AMS I.23941-005 (77 mm SL), Northern ‘Mugil’ georgii . Territory, Micket Creek; AMS I.5552-008 (4, 72-79 mm SL), Gulf of Carpentaria, mouth of Norman River; AMS Key to the species of Paramugil I.10475 (157 mm SL), Philippines, Negros Island; BMNH 1a. Scales in lateral series 24-26; pyloric caeca 7-15; 1974.5.25. 3640-3642 (3, 69-70 mm SL), New Guinea; vomerine teeth absent; urohyal anterior process BMNH 1894.1.19.41-2 (2, 66-71 mm SL), Sarawak; sharp; postzygapophysis of the second abdominal BMNH 1844.1.18 (88 mm SL), labelled as South Aus - vertebra elongate; pterotic with a lateral crest; pos - tralia, but originally from Northern Territory; NTM terolateral process of basioccipital rudimentary; S.10718-012 (10, 61-102 mm SL), Darwin, Pearl Raft more than five epipleural ribs ...... Creek; NTM S.10469-014 (3, 76-92 mm SL); Darwin, ...... Paramugil parmatus Channel Island; RMNH 6405 (7, 28-78 mm SL), holotype 1b. Scales in lateral series 28-32; pyloric caeca 18-26; and paratypes of M. oligolepis , Borneo; ZMA 121.613 (4, vomerine teeth present; urohyal anterior process 59-73 mm SL), Indonesia, Terentang, Sungai. blunt; postzygapophysis of the second abdominal vertebra short and blunt, expanded ventrolaterally; Material examined - osteology posterolateral process of basioccipital intermediate; All osteological drawings were done by the senior five epipleural ribs ...... Paramugil georgii author. AMS I.5552-008 (2, 72-79mm SL), Gulf of Car - pentaria, mouth of Norman River; AMS I.22789-004 (74 mm SL), Queensland, Norman River; AMS I.23941-005 Paramugil parmatus (Cantor, 1850) (77 mm SL), Micket Creek; NTM S.10718-012 (3, 61-72 mm SL); Darwin, Pearl Raft Creek; NTM S.10469-014 M. oligolepis Bleeker (RMNH 6405, holotype) is herein (3, 76-92 mm SL); Darwin, Channel Island; ZMA designated as the neotype of M. parmatus. 121.613 (59 mm SL), Indonesia, Terentang, Sungai. Mugil parmatus Cantor, 1850, p. 1076 (Penang Island, Malayan Archipelago); Bleeker, 1855, p. 400 (Java); Diagnosis 1859a, p. 276 (Indonesian Archipelago); 1860, p. 42 D1. IV; D 2. 9 ; A. III,9; Pec. I, 13-15; Pel. I,5; C. 8+7 (Borneo); 1861, p. 76 (Penang Island). (6+6); Ll. 24-26; Tr. 9-11; Pre D 1. 14-17; V. 11-13 (24). Mugil dussumieri Bleeker, 1848, p.637 (Sumbawa), non Body deep and compressed, more compressed at Valenciennes, 1836. caudal peduncle. Maximum depth at origin of first dorsal Mugil macrolepis: - Bleeker, 1852a, p. 422, (Borneo); fin 32-42 % standard length; depth at anus 28-34 % 1852b, p. 701 (Ceram), non Smith, 1849. standard length, and least depth at caudal peduncle 12- Mugil oligolepis Bleeker, 1859a, p. 275 (Sumbawa); 16 % standard length. Head deeper than wide, bluntly 1859b, p. 437 (Sumbawa); 1860, p. 40 (Borneo); Gün - pointed and flat or slightly convex dorsally; head length ther, 1861, p. 449, (Borneo, Sambawa); Dunker, 1904, 26-30 % standard length. Eye diameter 19-31 % head p. 166 (Malayan Archipelago); Weber, 1894, p. 451 length. Snout short and blunt in profile, snout length 18- (Indonesian Archipelago); Weber and Beaufort, 1922, 23 % head length and shorter than eye diameter. Mouth vol iv, p. 245 (Indo-Australian Archipelago); Roxas, appears transverse in ventral aspect. Upper lip slightly 1934, p. 413 (Philippines); Roxas and Martin, 1937, p. thickened, with a row of minute ciliform teeth present or 84 (Philippines); Smith, 1935, p. 635, fig. 17, pl. 21B lost. Adipose eyefold extending up to half of iris anteri - and 22 C, D (South Africa, Isipingo Lagoon); Fowler, orly, and more progressed posteriorly leaving a vertical 1925, p. 209 (Delagoa Bay); 1934, p. 399 (Oceania); oval space over the eye. Nostrils well-separated, poste - 1935, p. 134 (Thailand); 1939, p. 46 (Indo-China, rior nostril almost level to the upper rim of orbit; inter- Krabi); 1959, p. 156 (Fiji); Suvatti, 1981, p. 131 (Thai - nostril distance equal to or slightly greater than width of land); Pandey and Sandhu, 1992, p. 277 (India to posterior nostril. Vomer and palatine edentulous. Num - Malayan Archipelago). ber of gill rakers on lower part of gill arch 31-47. First Liza oligolepis: - Jordan and Richardson, 1908, p. 244 dorsal spine slightly convex proximally, higher and (Philippines); Herre, 1936, p. 95 (Fiji, Suva Harbour, much stronger than the second spine. Origin of second Viti Levu Island); 1953, p. 232 (Philippines); Smith, dorsal fin at vertical through half to two-thirds of anal fin 1948, p. 840, fig. 10 (Tropical Indo-Pacific); 1949; p. base; both fins slightly emarginate, densely-scaled 321, fig. 885 (Isipingo to Delagoa Bay); Matsubara, anterobasally, subequal to each other and higher than 1955 p. 491 (Japan), Munro, 1955, p. 94 (Ceylon); first dorsal fin. Pectoral fin I, 13-14 (usually 14, rarely Wongratana et al ., 1984, p. 18 (Thailand). 15), almost reaching origin of first dorsal fin; pectoral fin Valamugil parmatus: - Smith, 1975, p. 64 (South Africa) 20-25 % standard length, 74-88 % head length. Pelvic Liza parmata: - Thomson 1997, p. 528 (West Pacific). fin inserted at vertical nearer to origin of pectoral fin than

15 aqua vol. 8 no. 1 - 2004 Historical overview of mugilid systematics, with description of Paramugil (Teleostei; Mugiliformes; Mugilidae), new genus to origin of first dorsal fin. Scales in lateral series 24-26; Mugil georgii Ogilby, 1897, p. 77 (Georges River); 1915, in transverse series 9-11; predorsal scales 14-17; inter - p.13 (Queensland); Tosh, 1903, p. 19, pl. 2, fig. 4 dorsal scales 6-7; scales in lateral series anterior to ori - (Moreton Bay); Waite, 1904, p. 22 (Georges River); gin of first dorsal fin 7-8; scales anterior to origin of sec - Stead, 1908, p. 43 (New South Wales); Cockerell, ond dorsal fin 15-16; scales anterior to tip of pectoral fin 1913, p. 53 (Queensland); McCulloch, 1921a, p. 48 7-8; and 16 scales around caudal peduncle. Pharyngo - (New South Wales); 1921b, p. 129, pl. 22, fig. 1 (Port branchial organ with reduced denticulate area, bearing Hacking, Karuah River, Brisbane River); 1922, p. 38 fine, evenly-graded teeth; sulcus diagonal and broad. (New South Wales); 1927, p. 38 (New South Wales); Unbranched pyloric caeca 7-15. 1929, p. 114 (New South Wales, Queensland); 1934, Colour in alcohol: Greenish to olive brown dorsally, p. 38, fig. 139b (New South Wales); McCulloch and flanks silvery, abdomen white with a light yellowish Whitley, 1925, p. 141 (Moreton Bay, Brisbane River); tinge. Margin of caudal fin slightly darkish. Thomson, 1954, p. 94, pl. 1, fig. 2 (Queensland, New Largest recorded specimen 102 mm SL, but possibly South Wales); Munro, 1956, p. 103, fig. 706 (south may attain greater size, up to 150 mm SL. Queensland, New South Wales); Roughley, 1964, p. 37 (south Queensland, north New South Wales); Mar - Distribution shall, 1964. P. 407, pl. 54 (south Queensland, New Indo-Pacific from India, Ceylon and South Africa to South Wales); 1982. P. 87, pl. 126, fig. 1 (Queens - south China sea, Thailand, Philippines, Borneo, land); Grant, 1965, p. 46 (Queensland, New South Malayan and Indonesian Archipelago, Fiji, New Wales); 1982, p. 510, pl. 262 (south-east Australia); Guinea and tropical Australia in Queensland and 1987, p. 282, fig. 618 (south Queensland, New South Northern Territory. Wales); Lake, 1971. P. 42 (Australia). Mugil nortoni Ogilby, 1908, p. 22 (Brisbane River). Remarks Valamugil georgii. - Thomson, 1977, FAO identification The senior author (Ghasemzadeh, 1998) Thomson sheet; 1978, p. 106 (Queensland, New South Wales); (1997) and Ingham (1952) all recognise Cantor’s par - 1980, p. 165, fig. 29:5 (New South Wales, Port Hack - mata as a valid name despite the fact that Cantor’s ing; Queensland, Burnett River); 1997, p. 504 (eastern type for that species is unavailable. They all regard Australia, Port Hacking to Burnett River). Bleeker’s M. oligolepis (RMNH 6405, holotype and 6 paratypes, 28- 78 mm SL), (Rijksmuseum van Natu - Material examined - morphology urlijke Historie, Leiden) as indistinct from M. parma - AMS I.4936 (155 mm SL), holotype of M. georgii , tus on the basis of descriptions and examination of Georges River; AMS I.34341-004 (40, 24-41 mm SL), Bleeker’s types. The holotype M. oligolepis is con - Queensland, Mangrove Channel, Port Clinton; AMS sequently designated as the neotype of M. parmatus. I.24689-021 (2, 50-54 mm SL), Darwin, Buffalo Creek; AMS I.22722-052 (5, 39-70 mm SL), Queensland, Dain - Paramugil georgii (Ogilby, 1897) tree River mouth; AMS I.12843 (200 mm SL), Port Hacking; AMS I.12844 (195 mm SL), Port Hacking; Holotype: M. georgii AMS I.4936 (155 mm SL), , AMS I.12845 (145 mm SL), New South Wales, Karuah Georges River, Sydney. (Fig. 6). River; MQU F.1073 (5, 95-142 mm SL), Queensland,

1 cm

Fig. 6. Paramugil georgii, NTM S.10694-007, 90 mm SL. Arrow indicates position of anus. aqua vol. 8 no. 1 - 2004 16 Javad Ghasemzadeh, Walter Ivantsoff and Aarn

Townsville; MQU F.1013 (4, 54-87 mm SL), Queens - between origins of pectoral and first dorsal fins, or slightly land, Burnett River; MQU F.1012 (4, 92-159 mm SL), nearer the latter. Scales in lateral series 28-32; in trans - Queensland, St. Lawrence River; MQU F.1072 (6, 75- verse series 9-12; predorsal scales17-22; interdorsal 134 mm SL), Queensland, Mooloolaba; NTM S.11362- scales 8; scales in lateral series anterior to origin of first 028 (70 mm SL), Northern Territory, Darbilla Creek, dorsal fin 9-11; scales anterior to origin of second dorsal Millingimbi; NTM S.10429-013 (5, 16-45 mm SL), Dar - fin 17-20; scales anterior to tip of pectoral fin 8-11; and win, Channel Island; NTM S.11363-004 (11, 84-111 mm 16 scales around caudal peduncle. Pharyngobranchial SL), Northern Territory, Millingimbi, Rapuma Island; organ with large denticulate area, broad sulcus and no NTM S.10694-007 (90 mm SL), Northern Territory, valves. Unbranched pyloric caeca18-26. Gunn Point Beach; QM I.775 (135 mm SL), holotype of Colour when live : Pale olive brown dorsally, flanks M. nortoni , Queensland, Nerang River; QM I.28543 (11, silvery shading into white, with a light golden tinge ven - 75-110 mm SL), Queensland, Pine River mouth; QM trally when live. Second dorsal, anal and caudal fins I.12485 (2, 86-89 mm SL), Gulf of Carpentaria, with dusky margins Second dorsal membrane speckled Karumba; QM I.27032 (55 mm SL), Western Australia, with dark brown pigment spots. A dark purplish spot in Fitzroy River; QM I.15866 (2, 51-56 mm SL), Prince of the pectoral axilla. Iris golden. Wales Island, Smith Point; QM I.27012 (2, 77-79 mm Colour in alcohol : Same as above with golden colour SL), NE Queensland, Molongle Creek; QM I.22550 (48 washing out to white. Spot becoming black. mm SL), Western Australia, Pago Ruins Creek. Distribution Material examined - osteology This species is also confined to the temperate and AMS I.22722-052 (2, 39-59 mm SL), Queensland, tropical coastal waters of Australia. It is recorded from Daintree River mouth; AMS I.23941-005 (2, 48-51 mm Georges River and Port Hacking in New South Wales, SL), Northern Territory, Micket Creek; AMS I.22770-026 northwards in Queensland to the Gulf of Carpentaria, (2, 47-56 mm SL), Mackay, Queensland; AMS I.34341- northern Queensland and Northern Territory and adja - 004 (5, 37-41 mm SL), Queensland, Mangrove Chan - cent islands. Its distribution continues to the temperate nel, Port Clinton; AMS I.24689-021 (2, 50-54 mm SL), waters of Western Australia, where it has been recorded Darwin, Buffalo Creek; MQU F.1013 (2, 54-62 mm SL), down to the Fitzroy River delta. Queensland, Burnett River; MQU F.1072 (3, 75-96 mm SL), Queensland, Mooloolaba; MQU F.1013 (2, 62-75 Acknowledgements mm SL), Queensland, Burnett River; QM I.28543 (2, 93- Much of the work presented herein was part of the 97 mm SL), Queensland, Pine River mouth. senior author’s doctoral dissertation. The authors partic - ularly wish to thank Barbara Duckworth, the University Diagnosis artist, for the excellent illustrations, Dr. Ian Harrison for D1. IV; D 2. 9 ; A. III,9; Pec. I, 14-16; Pel. I,5; C. 8+7 many informative comments, and the staff of various (6+6); Ll. 28-32; Tr. 9-12; Pre D 1. 17-22; V. 11-13 (24). museums who kindly provided access to specimens dur - Body moderately robust. Maximum depth at origin of ing visits and facilitated loans during the period of study. first dorsal fin 28-33 % standard length; depth at anus 26-30 % standard length, and least depth at caudal References peduncle 13-15 % standard length. Head deeper than Anderson, M. 1982. The identification of the British wide, bluntly-pointed and flattened or slightly convex dor - grey mullets. Journal of Fish Biology, 20 : 33-38. sally; head length 25-33 % standard length. Eye diame - Athanassopoulos, G. 1919. Contributo alla distinzione ter 19-29 % head length. Snout short and blunt, 19-25 % delle specie Mediterranee del genere Mugil. Annali del head length and shorter than eye diameter. Upper lip Museo Civico di Storia Naturale (di Genova) Giacomo slightly thickened, with minute ciliform teeth. Adipose Doria, 3 (8): 254-269. eyefold extending up to half of iris anteriorly, and more Autem, M. & Bonhomme. 1980. Éléments de systema - progressed posteriorly leaving a vertical oval space over tique biochimique chez les Mugilides de Mediterranée. the eye. Nostrils well-separated, posterior nostril reach - Biochemical and Systematic Ecology, 8: 305-308. ing above the upper rim of orbit. Lacrimal with distinctly Berg, L. S. 1940. Classification of Fishes both Recent kinked anterior serrate margin, and squarish denticulate and Fossil. Tr. Zool. Inst. Akad. Nauk SSSR, 5 (2) (In posteroventral end. Tongue raised and moderately Russian). keeled medially. Vomer dentigerous. Number of gill rak - Berra, T. M. 1981. An Atlas of Distribution of the Fresh - ers on lower part of gill arch 38-58. Origin of second dor - water Fish Families of the World . University of sal fin at vertical through one-third to half of anal fin base; Nebraska Press, London, 197 pp. both fins slightly emarginate, scaled only anterobasally, Bleeker, P. 1852a. Zesde bijdrag tot de kennis der subequal to each other and higher than first dorsal fin. ichthyologische fauna van Borneo. Visschen van Pectoral fin I, 14-15 (rarely 16), not reaching origin of first Pamangkat, Bandjermassing, Braboekarta en Sampit. dorsal fin; pectoral fin 20-25 % standard length, 67-87 % Natuurkundik Tijdshjrift voor Nederlandsh Indië. head length. Pelvic fin inserted at vertical midway (Batavia), 3: 407-442.

17 aqua vol. 8 no. 1 - 2004 Historical overview of mugilid systematics, with description of Paramugil (Teleostei; Mugiliformes; Mugilidae), new genus

Bleeker, P. 1852b. Nieuwe bijdrag tot de kennis der coast of India. Pt 1. Acanthopterygii. Proceedings of ichthyologische fauna van Ceram. Natuurkundik Tijd - the Zoological Society of London, 1865 : 2-40. shjrift voor Nederlandsh Indië. (Batavia), 3: 689-714. Day, F. 1865b. The Fishes of Malabar . Bernard Bleeker, P. 1855. Verslag van eenige vischverzamelin - Quaritch, London, 293 pp. gen van visschen van Oost-Java. Natuurkundik Tijd - Day, F. 1878. The Fishes of India, being a Natural His- shjrift voor Nederlandsh Indië. (Batavia), 9: 391-414. tory of the Fishes known to inhabit the Seas and Fresh Bleeker, P. 1859a. Conspectus specierum Mugilis waters of India, Burma, and Ceylon (vol. 1). Today and Archipelagi indici analyticus. Natuurkundik Tijdshjrift Tomorrow’s Book Agency, New Delhi, 816 pp. voor Nederlandsh Indië. (Batavia), 16 : 275-81. Day, F. 1889. The Fauna of British India, including Bleeker, P. 1859 b. Derde bijdrag tot de kennis der Ceylon and Burma. Fishes (vol 2). Taylor and Francis, vischfauna van Soembawa. Natuurkundik Tijdshjrift London, 509 pp. voor Nederlandsh Indië. (Batavia), 19 : 434-440. Deva-Sundaram, M. P. 1951. Systematics of Chilka Bleeker, P. 1860. Diertiende bijdrag tot de kennis der Mullets with a key to their Identification. Journal of the vischfauna van Borneo. Acta Societatis Scientiarum Zoological Society of India, 3 (1): 19-25. Indo-Neérlandica (Batavia), 8: 1-64. Ebeling, A. W. 1957. The dentition of eastern Pacific Bleeker, P. 1861. Iets over de vischfauna van het mullets, with special reference to adaptation and eiland Pinang. Verslagen. Academie van. Amster - taxonomy. Copeia, 1957 (3): 173-185. dam, 12 : 64-80. Ebeling, A. W. 1961. Mugil galapagensis , a new mullet Borcea, I. 1934. Données pour servir à la systéma - from the Galapagos Islands, with notes on related tique et à la biologie des Mugilides Formes de la Mer species and a key to the Mugilidae of the eastern Noire (litoral Roumain). Annales des Sciences de Pacific. Copeia, 1961 : 295-304. l’Université. De Jassy, 19 : 247-286. Farrugio, H. 1977. Clés commentées pour la détermi - Cadenat, J. 1954. Notes d’ichthyologie ouest- nation des adults et des alevims de Mugilidae de rd africaine VIII. Sur les mulets de la côte occidentale Tunisie. Cybium, 3 Ser. (2): 57-73. d’Afrique. Bulletin de l’Institut Francais d’Afrique Fowler, H. W. 1925. Fishes from Natal, Zululand, and Noire, 16 : 584-591. Portuguese East Africa. Proceedings of the Academy Cambrony, M. 1984. Identification et périodicité du of Natural Sciences of Philadelphia, 77 : 187-268. recrutement des juvéniles de Mugilidae dans les Fowler, H. W. 1928. The Fishes of Oceania. Memoirs étangs littoraux du Languedoc-Roussillon. Vie Milieu, of the Bernice P. Bishop Museum, 10 : 1-546. 34 : 221-227. Fowler, H. W. 1931. The fishes of Oceania. Supple - Campton, D. E. & B. Mahmoudi. 1991. Allozyme vari - ment 1. Bernice P. Bishop Museum- Memoir, 10 (5): ation and population structure of striped mullet ( Mugil 313-81. cephalus ) in Florida. Copeia, 1991 (2) : 485-492. Fowler, H. W. 1934. The fishes of Oceania. Memoirs of Cantor, T. E. 1850. Catalogue of Malayan Fishes. Jour - the Bernice P. Bishop Museum Supplement, 2: 11 (6): nal of the Asiatic Society of Bengal, 18 (2) : 983-1043. 385-466. Chervinski, J. 1984. Using scales for identification of Fowler, H. W. 1935. Zoological Results of the Third de four Mugilidae species. Aquaculture, 38 : 79-81. Schauensee Siamese Expedition. Part 8- Fishes Chubb, C. F., Potter, I. C., Grant, C. J., Lenanton, R. Obtained in 1936. Proceedings of the Academy of C. J. & J. Wallace. 1981. Age structure, growth rates Natural Sciences of Philadelphia, 139 : 125-264. and movement of sea mullet Mugil cephalus L., and Fowler, H. W. 1936. The marine fishes of West Africa. yellow eye mullet, Aldrichetta forsteri (Valenciennes) in Bulletin of the American Museum of Natural History, the Swan Avon River system, Western Australia. 70 (1): 1-605. Australian Journal of Marine and Freshwater Fowler, H. W. 1939. Zoological Results of the Third de Research, 32 (4): 605-628. Schauensee Siamese Expedition, pt. IX. Additional Cockerell, T. D. A. 1913. The scales of some fishes obtained in 1936. Proceedings of the Academy Queensland fishes. Memoirs of the Queensland of Natural Sciences of Philadelphia, 91 : 39-76. Museum, 2: 51-9. Fowler, H. W. 1959. Fishes of Fiji . Government of Fiji. Crosetti, D., Avise, J. C., Placidi, F., Rossi, A. R. & Suva, 670 pp. L. Sola. 1993. Geographic variability in the grey mul - Ghasemzadeh, J. 1998. Phylogeny and Systematics of let Mugil cephalus : preliminary results of mt DNA Indo-Pacific mullets (Teleostei: Mugilidae) with special and chromosome analyses. Aquaculture, 111 : 95- reference to the mullets of Australia . Unpublished 101. Ph.D Thesis, Macquarie University, Sydney, 397 pp. Crosetti, D., Nelson, W. S. & J. C. Avise. 1994. Pro - Gosline, W. A. 1968. The suborders of perciform nounced genetic structure of mitochondrial DNA fishes. Proceedings of the United States National among populations of the circumglobally distributed Museum, 124 : 1-78. grey mullet ( Mugil cephalus). Journal of Fish Biology, Gosline, W. A. 1971. Functional morphology and 44 : 47-58. classification of teleostean fishes . University of Hawaii Day, F. 1865a. On the Fishes of Cochin, on the Malabar Press, Honolulu. 208 pp. aqua vol. 8 no. 1 - 2004 18 Javad Ghasemzadeh, Walter Ivantsoff and Aarn

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19 aqua vol. 8 no. 1 - 2004 Historical overview of mugilid systematics, with description of Paramugil (Teleostei; Mugiliformes; Mugilidae), new genus

Lee, S. C., Chang, J. T. & Y. Y. Tsu. 1995. Genetic re- McCulloch, A. R. 1934. The Fishes and Fish-Like lationships of four Taiwan mullets (Pisces: Percifor- Animals of New South Wales (third ed). Royal Zoo- mes: Mugilidae). Journal of Fish Biology, 46 : 159-162. logical Society of New South Wales, Sydney, 104 pp. Lee, S. C., Chang, H. L. & J. T. Chang. 1996. Allozyme McCulloch, A. R. & G. P. Whitley. 1925. Fishes variation in the large scale mullet Liza macrolepis (Per - recorded from Queensland. Memoirs of the Queens - ciformes: Mugilidae) from coastal waters of western land Museum, 8 (2): 125-82. Taiwan. Zoological Studies, 35 (2): 85-92. Menezes, M. R., Martins, M. & S. Naik. 1992. Inter - Lenanton, R. C. J., Potter, I. C., Lonergan, N. R., & P. specific genetic divergence in grey mullets from the J. Chrystal. 1984. Age structure and changes in Goa region. Aquaculture, 105 : 117-129. abundance of three important species of teleost in a Merrick, J. R. & G. E. Schmida. 1984. 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Svichenskaya, A. A. 1973. Mullet-like fossils in the Waite, E. R. 1904. Synopsis of the fishes of New South USSR. Trudi Paleontologii Instituta Akademii Nauk Wales. Memoirs of the New South Wales Naturalists’ (SSSR). Moscow, 138: 138:1-64. (In Russian). Club, 2: 1-59. Sunny, K. G. 1971. Morphology of the vertebral column Weber, M. 1894. Die Süsswasser-Fische des Indischen of Mugil macrolepis (Smith). Bulletin of the Department Archipels, Nebst Bemerkungen über den Ursprung der of Marine Oceanography, University of Cochin, Fauna von Celebes. Zoologische Ergebnis Indien, 2: 5: 101-108. 405-476. Suvatti, C . 1981. Fishes of Thailand . Rungsilpa Ltd., Weber, M. & L. F. de Beaufort. 1922. The Fishes of the Bangkok, 379 pp. Indo-Australian Archipelago (vol. 4). Leiden, 410 pp. Thomson, J. M. 1954. The Mugilidae of Australia and Whitehouse, R. H. 1927. The grey mullets of Tuticorin. adjacent seas. Australian Journal of Marine and Madras Fisheries Bulletin, 15 (3): 71-98. Freshwater Research, 5: 70-131. Whitley, G. P. 1930. Five new generic names for Thomson, J. M. 1963. Synopsis of Biological data on Australian fishes. Australian Zoology, 6 (3): 250-251. the grey mullet Mugil cephalus Linnaeus 1758. CSIRO Whitley, G. P. 1941. Ichthyological notes and illustra - Division of Fisheries and Oceanography, Fish Synop - tions. Australian Zoology 10 (1): 1-52. sis No. 1., Canberra, variable page numbers. Whitley, G. P. 1945. New sharks and fishes from West - Thomson, J. M. 1964. A Bibliography of Systematic ern Australia. Part 2. Australian Zoology 11 (1): 1-42. References to the Grey Mullets (Mugilidae) . CSIRO Whitley, G. P. 1948. New sharks and fishes from Division of Fisheries and Oceanography, Technical Western Australia. Part 4. Australian Zoology, Paper 16, Canberra, 127 pp. 11 (3): 259-276 Thomson, J. M. 1966. The grey Mullets. Annual Wongratana, T., Senou. H. & C. Vittayanon. 1984. Reviews of Oceangraphy and Marine Biology, First record of the stripped grey mullet Mugil cephalus 4: 301-335. (Pisces: Mugilidae) from Thailand, with a key to all Thomson, J. M. 1974. Mugilidae (mullets). In: Fischer, local species. Natural History Bulletin of the Siam W. and G. Bianchi (eds.) FAO Species Identification Society, 32 (1): 11-20. Sheets for Fishery Purposes. Fishing Area 57,71 (East Yoshino, T. & H. Senou. 1984. Family Mugilidae. Indian Ocean and West Central Pacific) Vol. 3. FAO, In: The Fishes of the Japanese Archipelago (Eds. Rome, variable page numbers. H. Masuda, C. Amoaka, T. Araga, T. Uyeno and Thomson, J. M. 1975. The dentition of grey mullets T. Yoshino) (English version). 119-121. Tokai Univer - (abstract). Aquaculture, 5: 108 sity Press, Tokyo. Thomson, J. M. 1978. A field guide to the Common Sea and Estuary Fishes of non-tropical Australia . Collins, Sydney, 144 pp. Thomson, J. M. 1980. Family Mugilidae. Grey Mullets. Pp 162-166. In: McDowall, R. M. (ed) Fresh- water Fishes of South Eastern Australia (New South Wales, Victoria and Tasmania) . Reed Pty. Ltd., Sydney, 208 pp. Thomson, J. M. 1981. The taxonomy of grey mullets. In: Aquaculture of grey mullets (Ed. O.H. Oren) 1-15. Cambridge University Press, London. Thomson, J. M. 1997. The Mugilidae of the world. Memoirs of the Queensland Museum , 41 (3): 457- 562. Tosh, J. R. 1903. Notes on the habits, development, etc., of the common food fishes of Moreton Bay. Queensland Harbour Marine Department Annual Report , Brisbane, pp. 17-24. Trewavas, E. & S. E. Ingham. 1972. A key to the species of Mugilidae (Pisces) in the north-eastern Atlantic, with explanatory notes. Journal of Zoology, London, 167 : 12-24. Valenciennes, A. 1836. Mugiloides. In: Histoire Naturelle des Poissons (vol. 11) (Eds. G. Cuvier and A. Valenciennes,) 1-127. F. G. Levrault, Paris. Van Der Elst, R. P. & J. H. Wallace. 1976. Identifica - tion of the juvenile mullet of the east coast of South Africa. Journal of Fish Biology, 9: 371-374. aqua vol. 8 no. 1 - 2004 22 aqua, Journal of Ichthyology and Aquatic Biology

Chaetodontoplus vanderloosi , A new species of angelfish (Pomacanthidae) from Papua New Guinea

1 2 Gerald R. Allen and Roger C. Steene

1) Conservation International, 1919 M. Street N.W. Suite 600, Washington, DC 20036, U.S.A. and Western Australian Museum, Perth, Australia; mailing address: 1 Dreyer Road, Roleystone, WA 6111, Australia. 2) P. O. Box 188, Cairns, Queensland 4870, Australia.

Accepted: 21.11.2003

Keywords Résumé Taxonomy, marine fishes, Chaetodontoplus , new On décrit ici une nouvelle espèce de Pomacanthidé, species, Pomacanthidae, Papua New Guinea Chaetodontoplus vanderloosi, sur base de 3 spéci - mens, 117,8-125,2 mm LS, collectés près de l'île Sama - Abstract rai, province de Milne Bay, Papouasie Nouvelle-Guinée A new species of pomacanthid fish, Chaetodontoplus en 1972 et 2003. L'espèce est très proche de vanderloosi , is described from 3 specimens, 117.8- C. dimidiatus et de C. melanosoma d'Indonésie et des 125.2 mm SL, collected at Samarai Island, Milne Bay Philippines, mais se distingue par le patron de col - Province, Papua New Guinea in 1972 and 2003. It is oration. L'espèce nouvelle est noire pour l'essentiel, closely related to C. dimidiatus and C. melanosoma mais la tête et la partie dorso-antérieure du corps est from Indonesia and the Philippines, but differs in colour gris clair à presque blanc, la caudale étant surtout noire pattern. The new species is mainly black except the (si ce n'est un large liseré postérieur jaune). Les petits head and adjacent dorsoanterior body is light grey to juvéniles sont surtout noirs avec une bande faciale nearly white, with a predominately black caudal fin médiane jaune, une bande diagonale jaune de juste (except broad yellow posterior margin). Small juveniles avant la dorsale jusqu'aux pelviennes, un large liseré are mainly black with a yellow median facial band, a yel - jaune occupant la majeure partie de la dorsale et une low diagonal band from just in front of the dorsal fin to caudale jaune avec une barre submarginale noire. the pelvic fins, a broad yellow margin covering most of the dorsal fin, and a yellow caudal fin with a black sub - Sommario marginal bar. Una nuova specie di pomacantide, Chaetodontoplus vanderloosi, è descritta sulla base di tre esemplari, Zusammenfassung 117.8-125.2 mm SL, raccolti all’Isola Samarai, Provincia Unter dem Namen Chaetodontoplus vanderloosi wird di Milne Bay, Papua New Guinea tra il 1972 e il 2003. Si eine neue Art der Kaiserfische auf der Grundlage von tratta di una specie molto vicina a C. dimidiatus e drei Exemplaren beschrieben, die an der Samarai-Insel C. melanosoma, presenti in Indonesia e nelle Filippine, in Papua-Neuguinea, Milne Bay Province, 1972 und dalle quali si differenzia per la colorazione. Essa è prin - 2003 mit 117,8 bis 125,2 mm SL gesammelt wurden. cipalmente di colore nero, eccetto il capo e la regione Die neue Art ist mit C. dimidiatus und C. melanosoma dorso-anteriore ad esso adiacente che sono grigio von Indonesien und den Philippinen eng verwandt, chiaro o quasi bianchi, come nera è pure la pinna cau - unterscheidet sich aber in der Farbgebung. Sie ist dale (tranne per una diffusa banda gialla al margine hauptsächlich schwarz, nur Kopf und vorderer Teil des posteriore). Gli individui giovani di piccola taglia sono Rückens sind hellgrau bis fast weiß gefärbt, auch die principalmente neri con una banda facciale mediana Schwanzflosse ist vorwiegend schwarz, bis auf einen gialla, una fascia diagonale anch’essa gialla che si breiten gelben Rand im hinteren Bereich. Kleine estende dal dorso anteriormente alla pinna dorsale fino Jungtiere sind ebenfalls überwiegend schwarz, zeigen alle pinne pelviche, un ampio margine giallo che ricopre aber in der Mitte des Kopfbereichs einen gelben la maggior parte della pinna dorsale e una pinna cau - Streifen, außerdem einen gelben diagonalen Streifen dale gialla con una banda submarginale nera. mit dem Ausgangspunkt kurz vor der Rückenflosse bis hin zu den Bauchflossen, einen breiten gelben Rand, Introduction der den Großteil der Rückenflosse einnimmt, sowie eine Angelfishes of the family Pomacanthidae are among gelbe Schwanzflosse mit einem submarginalen the most conspicuous inhabitants of coral reefs, occur - schwarzen Streifen. ring in both shallow and relatively deep water. Allen et al . (1998) reviewed the family, recognizing 83 species

23 aqua vol. 8 no. 1 - 2004 Chaetodontoplus vanderloosi , A new species of angelfish (Pomacanthidae) from Papua New Guinea worldwide, including 70 from the Indo-Pacific region. A measured just in front of the anal fin to the extreme base more recent (2003) treatment of the group by Debelius of the dorsal spines. The length of the caudal peduncle et al., recognized 75 Indo-Pacific species, including 14 was measured horizontally from a vertical at the rear members of the genus C haetodontoplus Bleeker, 1876. base of the anal fin to the caudal fin base. Measure - The present paper describes a new species in this ments of the dorsal and anal spines and soft rays were genus, which was originally collected at Papua New made from the distal tips to the extreme bases of these Guinea in 1972 and tentatively identified by the first elements (aided by x-rays). author as Chaetodontoplus melanosoma (Bleeker, Counts and proportions appearing in parentheses 1853). It belongs to a group of four closely-related apply to the paratypes if different from the holotype. Pro - species that is herein referred to as the “ melanosoma portional measurements expressed in thousandths of complex”. The taxonomic status of this assemblage has the standard length are provided in Table I. Type spec - long been a source of confusion, leading to frequent imens are deposited at the Bernice P. Bishop Museum, misidentifications. Subsequent observations of the true Honolulu (BPBM), United States National Museum of C. melanosoma and the closely-related C. dimidiatus Natural History, Washington, D.C. (USNM), and the (Bleeker, 1860) in Indonesian seas revealed important Western Australian Museum, Perth (WAM). Compara - colour pattern differences, as well as significant gaps in tive material of Chaetodontoplus dimidiatus and C. their allopatric distributions. melanosoma was examined at the Natural Museum of Natural History, Leiden, The Netherlands (RMNH) and Materials and Methods Museum of Victoria, Melbourne, Australia (NMV). Counts of pectoral rays, scales, and gill rakers were made on the left side of specimens. The scales of Chaetodontoplus vanderloosi n. sp. Chaetodontoplus are tiny (the smallest in the family, see (Figs 1-4) Shen and Liu, 1978) and occur in uneven rows, hence are very difficult to count accurately. Therefore, scale Holotype: WAM P.32263-001, 125.2 mm SL, wharf at row counts are approximations based on the average of Samarai Island (10°36.50’S, 150°39.64’E ), Milne Bay repeated counts for each specimen. The upper limb gill Province, Papua New Guinea, at depth of 6 m, collected raker count is given first; the raker at the angle is by spear, R. Vanderloos, 12 April 2003. included in the lower limb count. Paratypes (same locality as holotype): BPBM 13657, Standard length (SL) was measured from the front of 122.8 mm SL, at depth of 9 m, spear, G. R. Allen, 16 the upper lip to the base of the caudal fin (end of hypural June 1972; USNM 373887, 117.8 mm SL, same data as plate). Total length (TL) was measured from the front of BPBM paratype. the upper lip to the tip of the longest caudal fin ray. The head length was taken from the front of the upper lip to Diagnosis the end of the opercular membrane. The depth was A species of the pomacanthid genus Chaetodontoplus

Fig. 1. Chaetodontoplus vanderloosi, holotype, 125.2 mm SL, Milne Bay Province, Papua New Guinea. Photo by G. R. Allen. aqua vol. 8 no. 1 - 2004 24 Gerald R. Allen and Roger C. Steene

Fig. 2. Underwater photograph of Chaetodontoplus vanderloosi, adult, approximately 120 mm SL, Milne Bay Province, Papua New Guinea. Photo by R. Steene.

Fig. 3. Underwater photograph of Chaetodontoplus vanderloosi, subadult, approximately 80 mm SL, Milne Bay Province, Papua New Guinea. Photo by G. R. Allen.

Fig. 4. Underwater photograph of Chaetodontoplus vanderloosi, juvenile, approximately 30 mm TL, Milne Bay Province, Papua New Guinea. Photo by M. Strickland.

25 aqua vol. 8 no. 1 - 2004 Chaetodontoplus vanderloosi , A new species of angelfish (Pomacanthidae) from Papua New Guinea

Table I. Proportional measurements of type specimens with the following combination of characters: dorsal rays of Chaetodontoplus vanderloosi as percentage of the XIII,17; anal rays III,17; pectoral rays 16-17; scales tiny, standard length. about 105-116 diagonal scale rows from upper end of gill opening to base of caudal fin; gill rakers on first arch Character Holotype Paratyp e Paratype 4-5 +11; maximum body depth 1.9-2.0; length of preop - WAM BPBM BPBM ercular spine 2.7-4.1 in head length; adult mainly black P.32263 13657 13657 with pale grey head and adjacent dorsoanterior part of -001 body; caudal fin black with broad yellow margin posteri - Standard length (mm) 125.2 122.8 117.8 orly; juvenile mainly black with yellow median band from Body depth 50.7 51.5 53.4 snout to forehead, yellow diagonal band from front of Body width 20.8 22.6 22.5 dorsal fin origin to pelvic fin, broad yellow margin cover - Head length 26.5 28.7 27.4 ing most of dorsal fin, and a yellow caudal fin with black Snout length 9.5 10.5 8.6 submarginal bar. Orbit diameter 7.7 7.2 7.5 Interorbital width 8.1 8.0 8.4 Caudal peduncle depth 12.4 12.1 12.6 Description Caudal peduncle length 7.7 8.9 9.5 Dorsal rays XIII,17 (last divided to base); anal rays Predorsal length 33.5 32.3 33.9 III,17 (last divided to base); pectoral rays 17 (16 or 17) Preanal length 61.9 61.2 60.4 (upper two and lowermost unbranched); pelvic rays I,5; Prepelvic length 34.5 38.7 37.4 diagonal scale rows from upper end of gill opening to Length dorsal fin base 70.7 70.9 72.2 base of caudal fin about 115 (105-116); scale rows Length anal fin base 43.5 40.3 41.1 above lateral line to origin of dorsal fin about 20 (18-20); Length 1st dorsal spine 8.3 8.1 8.0 scale rows below lateral line to origin of anal fin about Length 2nd dorsal spine 12.5 12.9 12.3 56 (54-59); vertical scale rows on opercle about 14 (14- Length 3rd dorsal spine 17.3 17.8 16.7 15); gill rakers on first branchial arch 4 + 11 (4 or 5 +11), Length 4th dorsal spine 18.6 19.2 19.0 total rakers 15 (15 or 16); vertebrae 10 + 14. Length last dorsal spine 19.2 18.2 19.8 Length longest dorsal ray 18.5 16.7 19.0 Body ovate, the depth 2.0 (1.9) in SL, and com - Length 1st anal spine 10.5 10.3 9.5 pressed, the maximum width 2.4 (2.3-2.4) in depth; Length 2nd anal spine 16.9 16.3 16.3 head length 3.8 (3.5-3.6) in SL; dorsal profile of fore - Length 3rd anal spine 21.0 20.4 20.2 head relatively steep, forming an angle of about 50 Length longest anal ray 20.9 19.8 20.2 degrees to the horizontal; snout 2.8 (2.7-3.2) in head Length caudal fin 18.0 16.5 19.4 length, diameter of orbit 3.4 (3.7-4.0) in head length; Length pectoral fin 19.7 17.9 19.9 interorbital space slightly convex, the bony width 3.3 Length pelvic spine 16.3 16.4 17.4 (3.3-3.6) in head length; caudal peduncle deeper than Length pelvic fin 22.3 23.1 24.7 long, the least depth 2.1 (2.2- 2.4) in head length; length Length preopercular spine 10.0 7.0 7.6 of caudal peduncle 3.4 (2.9-3.2), in head length.

Fig. 5. Underwater photograph of Chaetodontoplus melanosoma, adult, approximately 150 mm TL, Komodo, Indonesia Photo by J. Randall. aqua vol. 8 no. 1 - 2004 26 Gerald R. Allen and Roger C. Steene

Mouth relatively small, terminal, the gape forming an pectoral and pelvic fins densely scaled at base, with tiny angle of about 28 degrees to the horizontal, the maxilla scales extending on surface of rays (but not on mem - reaching a vertical at front of anterior nostril. Upper lip branes) nearly to posterior margin. broader than lower, entirely scaled except anterior Lateral line relatively inconspicuous, its presence indi - edge, the maximum width contained 3.1 in diameter of cated by smaller scales (including tiny auxiliary scales), orbit. Teeth slender, elongate (the longest 2.9 in orbit of gently arching across back, originating at upper corner holotype), close-set, flexible, tricuspid (large central of gill opening and terminating below end of soft dorsal cusp notably longer than smaller lateral ones), in 4-5 fin; additionally, about 5-6 scattered tubed scales mid - rows in each jaw, 48 (45-48) in outer row of lower jaw laterally on caudal peduncle. and 52 (53-56) in outer row of upper jaw. No teeth on Caudal fin rounded, its length 5.6 (5.2-6.0) in SL. Ori - roof of mouth. Tongue short and broadly rounded. gin of dorsal fin slightly anterior to a vertical at upper end Nostrils anterior to centre of eye, the posterior opening of gill opening. Dorsal spines progressively longer to forming a vertical slit with thin flap-like rims, the slightly about sixth spine, remaining spines more or less sube - smaller anterior opening in a membranous tube with a qual, 1.4 (1.4-1.6) in head length; membranes between flap posterodorsally; distance between nostrils about first four dorsal spines and anal spines deeply incised; equal to half length of posterior opening; distance from posterior margin of soft portions of dorsal and anal fins edge of orbit to edge of posterior nostril about equal to rounded, the longest dorsal and anal rays reaching as length of posterior nostril slit. Head pores inconspicuous far posterior as base of caudal fin; origin of anal fin due to dense covering of tiny scales. Gill membranes below base of eleventh dorsal spine; third anal spine the narrowly attached to isthmus. Longest gill filament on longest, 1.3 (1.4) in head length; pectoral fins relatively first arch contained 1.8 times in orbit of holotype. Gill rak - short and moderately pointed, reaching a vertical ers short, the longest 8.1 in orbit of holotype. between base of pelvic fins and anal fin origin, slightly Opercle ending posteriorly in a single flat blunt spine. closer to pelvic fin base, their length 1.3 (1.4-1.6) in A prominent large spine at corner of preopercle, longer head length; pelvic fins reaching posterior to between than orbit, the spine length (measured along upper anus and anal fin origin, their length 1.2 (1.1-1.2) in edge) contained 2.7 (3.6-4.1) times in head length; mar - head length. gin of preopercle with 14 serrae; no serrae on margins Colour in life (from 35 mm colour transparency, see of opercular series, supracleithrum, and posttemporal. Fig. 2): body overall velvety black; head and nape region Scales coarsely ctenoid (up to 22 ctenii on posterior pale (nearly white) to medium grey except snout, interor - margins); auxiliary scales mainly confined to lateral line bital and apex of nape region yellowish with wavy blue and dorsoanterior portion of body; head fully scaled lines; mouth dark grey surrounded with yellow; all fins except lower lip and anterior edge of upper lip; dorsal blackish, with relatively broad yellow margin posteriorly and anal fins scaled nearly to margins except anteriorly on caudal, narrower yellow margin posteriorly on dorsal in spinous portion where fin membranes are deeply fin, and fine blue margin posteriorly on anal fin. The cau - incised; caudal fin scaled nearly to posterior margin; dal fin of subadults (approximately 80-100 mm SL,

Fig. 6. Underwater photograph of Chaetodontoplus melanosoma, juvenile, approximately 30 mm TL, Mabul, Sabah, Malaysia. Photo by R. Kuiter.

27 aqua vol. 8 no. 1 - 2004 Chaetodontoplus vanderloosi , A new species of angelfish (Pomacanthidae) from Papua New Guinea

Fig. 3) is yellow with a prominent crescent-shaped black snout, interorbital and nape regions. The larger marking in the centre. This central marking expands paratype has a large yellow area on the basal half of the with increased growth, until most of the fin is black. caudal fin, a remnant of the juvenile coloration. Small juveniles (Fig. 4) black with broad median yel - low facial band from chin to middle of nape, prominent Etymology yellow diagonal band from front of dorsal fin origin to The species is named vanderloosi in honour of Mr. pelvic fins, broad yellow margin covering most of dor - Robert (“Rob”) Vanderloos, owner and operator of the sal fin, and yellow caudal fin with broad black sub - live-aboard dive vessel Chertan . He also collected the marginal bar. holotype. Colour in alcohol : holotype (Fig. 1) overall black with head and dorsoanterior portion of body (above pectoral Remarks fin to below base of fourth dorsal spine) grey; fins black The genus Chaetodontoplus contains 14 species, except posterior margin of caudal broadly pale grey, which are mainly distributed in the Indo-Australian Arch - and posterior margins of dorsal and anal fin narrowly ipelago, ranging northward to Japan (Debelius et al. pale grey. After more than 30 years in preservative the 2003). A group of four closely-related species (referred paratypes are overall dark brown with the head and dor - to here as the “ melanosoma complex”) includes C. soanterior body tan. There are also indications of the cephalareticulatus Shen and Lim, 1974, C. dimidiatus wavy dark lines (bluish in life; see colour in life) on the (Bleeker, 1860), C. melanosoma (Bleeker, 1853), and

Fig. 7. Underwater photograph of Chaetodontoplus dimidiatus, adult, approximately 150 mm TL, Raja Ampat Islands, Indonesia. Photo by G. Allen.

Fig. 8. Underwater photograph of Chaetodontoplus dimidiatus, juvenile, approximately 30 mm TL, Lembeh Strait, Sulawesi, Indonesia. Photo by R. Kuiter. aqua vol. 8 no. 1 - 2004 28 Gerald R. Allen and Roger C. Steene

C. vanderloosi . Their similar appearance and paucity of the best means of separation of the remaining three specimens in museum collections has created confu - species. sion, resulting in misidentifications and the failure to rec - The new species is most similar to C. melanosoma . ognize some of the species as valid entities. For exam - Both species possess a black caudal fin with a broad yel - ple, Allen et al . (1998) misidentified a photograph of low margin. However, unlike C. melanosoma , which has C. cephalareticulatus as C. chrysocephalus (Bleeker, the entire dorsal half of the body light grey, C. vander - 1854), and following previous authors such as Fraser- loosi has a mainly jet black body with the light grey col - Brunner (1933) and Weber and de Beaufort (1936), did oration confined to the head and adjacent dorso-anterior not recognize C. dimidiatus as distinct from C. body. Moreover, the juvenile of C. vanderloosi has a yel - melanosoma. lowish diagonal band behind the head, compared with Colour pattern differences constitute the principal the white band of C. melanosoma . It also possesses a means of separation. All four species in the yellow tail with a relatively narrow black submarginal bar, melanosoma complex possess a yellowish area with which gradually expands with growth until the entire tail wavy blue lines on the front of the head. They also is black with the exception of the margin. In contrast, have a very similar juvenile colour pattern. C. juvenile C. melanosoma have a relatively broad black cephalareticulatus from southern Japan and Taiwan bar on the tail that fades with growth, with the black col - (see Masuda et al. 1988, Plate 177D-F) is perhaps oration of the body gradually expanding onto the caudal. the most readily distinguishable species, at least in Chaetodontoplus dimidiatus is similar in general body the adult stage. It has a series of wavy blue stripes on colour to C. melanosoma , particularly with respect to the the body and a blue reticulum on the head. However, proportion of black and light grey. However, the broad subadults (Masuda et al. 1988, Plate 177C; Debelius black bar on the caudal fin of juveniles gradually disap - et al., 2003, page 108, Figure J) are very similar in pears and adults are distinguished by a uniform yellow general appearance to C. dimidiatus . Differences in caudal. caudal fin coloration, in combination with the distribu - The three species appear to have non-overlapping tion of light grey on the head and body of adults, provide allopatric distributions (Fig. 9): C. melanosoma (Flores

Fig. 9. Known distributions of Chaetodontoplus dimidiatus, C. melanosoma, and C. vanderloosi.

29 aqua vol. 8 no. 1 - 2004 Chaetodontoplus vanderloosi , A new species of angelfish (Pomacanthidae) from Papua New Guinea and Solor Island westward to Bali, Indonesia and north - to use their excellent photographs. Glenn Moore of ward to the Philippines), C. dimidiatus (Raja Ampat WAM provided x-rays of the type specimens an d John Islands off western New Guinea, Halmahera, Moluccas, E. Randall critically reviewed the manuscript. and north-eastern Sulawesi), and C. vanderloosi (Milne Bay Province, Papua New Guinea). The record of C. References melanosoma from Japan by Masuda et al. (1988) is Allen, G. R. 1998. Reef and shore fishes of Milne Bay based on a misidentification of subadult C. cephalareti- Province, Papua New Guinea. in A rapid biodiversity culatus. Randall et al. (1997) included C. melanosoma assessment of the coral reefs of Milne Bay Province, from the northern Great Barrier Reef of Australia, but we Papua New Guinea (Werner, T. B. and Allen, G.R., now question this record as it appears to be unsubstan - eds.). RAP Working Papers 11, Conservation Interna - tiated. tional, Washington, DC: 39-49, 67-107. We have examined four of Bleeker’s five type speci - Allen, G. R., Steene, R. & M. Allen. 1998. Guide to mens of Holacanthus dimidiatus from Ambon, Indone - Angelfishes and Butterflyfishes. Odyssey Press, San sia (RMNH 5839, 3 specimens: 158-172 mm TL, and Diego. NMV A880, 136 mm TL) and the holotype of Holacan - Bleeker, P. 1853. Bijdrage tot de kennis der ichthyolo - thus melanosoma from Solor, Indonesia (RMNH 5828, gische fauna van Solor. Natuurkd. Tijdschrift Neder. 120 mm TL). The two species are also clearly illustrated Indië, 5: 67-96. in the Bleeker’s Atlas Ichthyologique (1877-1878, Vol. 9, Bleeker, P. 1860. Elfde bijdrage tot de kennis der vis - Plate 369, Figs. 1 and 4). chfauna van Amboina. Acta Soc. Sci. Indo-Neerl., The new species is apparently confined to a very lim - 8 (5): 1-14. ited area. Despite extensive searching in other parts of Bleeker, P. 1875-1878. Atlas ichthyologique des Milne Bay Province (which includes approximately Indes Orientales Néêrlandaises, publié sous les 265,000 km 2 of ocean) during five visits, it was only seen auspices du Gouvernement colonial néêrlandais. in a small area encompassing about 275 km 2, extending Tome IX. Toxotoidei, Pempheridoidei, Chaetodon - between Samarai Island (10°36.50’S, 150°39.64’E) and toidei, Nandoidei, etc. Atlas Ichthyol. v. 9: 1-80, Pls. the south-eastern corner of Basilaki Island (10°39.68’S, 355-360, 363-420. (Text published 1877-1878, 151°04.50’E). The species is apparently associated with plates published 1875-1878). relatively cool temperatures. Allen (1998) reported the Debelius H., Tanaka, H. & R. H. Kuiter. 2003. occurrence of lower water temperatures in this area, Angelfishes, A comprehensive Guide to Pomacanthi - between 22-24°C, compared with 26-28°C in other dae . TMC, Chorleywood, UK. parts of Milne Bay Province. Perhaps strong currents Fraser-Brunner, A. 1933. A revision of the chaetodont that sweep southward through narrow passes between fishes of the subfamily Pomacanthinae. Proceedings islands cause displacement of surface waters and con - of the Zoological Society of London 1933 (part 3, no. sequent upwelling of colder water from below. This phe - 30): 543-599. nomenon also occurs in the Komodo region and off Masuda, H., Amaoka, K., Uyeno T., & T. Yoshino. eastern Bali in Indonesia, where the closely-related C. 1988. The fishes of the Japanese Archipelago (2nd melanosoma occurs. Similarly, a species of surgeon - edition). Tokai University Press, Tokyo. fish, Prionurus chrysurus Randall, is restricted to cool Randall, J. E., Allen, G. R. & R. C. Steene. 1997 . upwelled seas at Komodo and Bali (Randall, 2001). Fishes of the Great Barrier Reef (2 nd edition). Crawford The new species is generally encountered alone or in House Press, Bathurst, Australia. pairs. Most individuals have been sighted in depths Randall, J. E. 2001. Prionurus chrysurus , a new ranging between 5 and 40 m. It is usually found on rocky species of surgeonfish (Acanthuridae) from cool bottoms with scattered hard and soft corals, or at Sama - upwelled seas of southern Indonesia. Journal of South rai Island in the vicinity of the wharf. Asian Natural History, 5 (2): 159-165. Shen, S.-C. & P.-C. Lim 1975. An additional study on Acknowledgements chaetodont fishes (Chaetodontidae) with description of We are greatly indebted to Rob Vanderloos for his gen - two new species. Bulletin of the Institute of Zoology erosity in providing numerous opportunities to join dive Academia Sinica (Taipei), 14 (2):79-105. cruises aboard Chertan . We also thank Walter Starck Shen, S.-C. & C.-S., Liu. 1978. Clarification of the gen - and Scott Michael for assisting with Papua New Guinea era of the angelfishes (Family Pomacanthidae). Taiwan fish collections, and Arnold Suzumoto of BPBM, for the Scientific Report, National Taiwan University: 57-77. loan of the paratypes of C. vanderloosi . Keiichi Matsuura Weber, M. & L. F. de Beaufort . 1936. The fishes of the and Kazuo Sakamoto successfully located and returned Indo-Australian Archipelago. VII. Perciformes (contin - the specimens to BPBM. They had been sent on loan in ued) families: Chaetodontidae, Toxotidae, Mon - 1974 to the late Yoshiaki Tominaga and were presumed odactylidae, Pempheridae, Kyphopsidae, Lutjanidae, lost. Dianne Bray (NMV) and Koos van Egmond Lobotidae, Sparidae, Nandidae, Sciaenidae, Malacan - (RMNH) provided information pertaining to Bleeker type thidae, Cepolidae . E. J. Brill Ltd., Leiden. Fish. Indo- specimens. Rudie Kuiter and Mark Strickland allowed us Aust. Arch. v. 7: i-xvi + 1-607. aqua vol. 8 no. 1 - 2004 30 aqua, Journal of Ichthyology and Aquatic Biology

Vampire catfishes seek the aorta not the jugular: candirus of the genus Vandellia (Trichomycteridae) feed on major gill arteries of host fishes

1 2 Jansen Zuanon and Ivan Sazima

1) CPBA, Caixa Postal 478, INPA-Instituto Nacional de Pesquisas da Amazônia, 69083-970 Manaus, Amazonas, Brasil 2) Departamento de Zoologia and Museu de História Natural, Caixa Postal 6109, Universidade Estadual de Campinas, 13083-970 Campinas, São Paulo, Brasil E-mail: [email protected] - Fax: +55 (19) 3289 3124

Accepted: 20.11.2003 Keywords Résumé Parasitic catfish, blood-feeding, Vandelliinae, Vandel - Les espèces de Trichomyctéridés du genre Vandel - lia cirrhosa , Vandellia sanguinea , fish host, tambaqui, lia (Candirus) se nourrissent du sang d'autres pois - Colossoma macropomum , Serrasalminae, Amazonia sons, généralement en pénétrant dans la chambre branchiale de leurs hôtes. Cependant, l'endroit précis Abstract où ces poissons vampires se fixent dans la branchie Species of the trichomycterid catfish genus Vandellia pour sucer le sang restait ignoré. A ce sujet, nous (candirus) feed on blood from other fishes, usually avons relevé clairement que deux espèces de Can - entering the gill chamber of their hosts. However, diru, Vandellia cirrhosa et V. sanguinea ciblent les exactly where these vampire fish attach themselves in artères principales des branchies. Les deux espèces the chamber to take blood remains unrecorded. Herein mordent surtout les artères ventrales et dorsales et le we present evidence that two candiru species, Van - sang leur parvient probablement par la pression san - dellia cirrhosa and V. sanguinea , seek the major gill guine de l'hôte. Nous pensons que les Candirus n'ont arteries. Both species bite mostly at the ventral or dor - pas besoin de mécanisme particulier de succion ou sal arteries, and the blood is presumably pumped into de pompage, mais se servent de leurs dents en aigu - their gut by the hosts’ blood pressure. We suggest that illes pour inciser l'artère. Si c'est le cas, la notion de candirus do not need any special sucking or pumping succion du sang par le Candiru est erronée. mechanism become rapidly engorged themselves with blood but simply use their needle-like teeth to make an Resumo incision in an artery. This being the case, the notion of As espécies do gênero Vandellia (candirus) alimen - blood-sucking by the candiru is misleading. tam-se de sangue de outros peixes, habitualmente entrando na câmara branquial de seus hospedeiros. Zusammenfassung Entretanto, o local exato onde estes peixes-vampiros Die Arten der Schmerlenwels-Gattung Vandellia se agarram dentro da câmara para obter sangue é ernähren sich vom Blut anderer Fische, wobei sie desconhecido. Apresentamos aqui evidências de que gewöhnlich in die Kiemenhöhle ihrer Wirtstiere eindrin - duas espécies de candirus, Vandellia cirrhosa e V. gen. Bisher wusste man jedoch nichts darüber, wo sanguinea , obtém sangue de artérias branquiais. genau sich diese „Vampirfische“ in der Kiemenhöhle Ambas as espécies mordem principalmente as festsetzen, um Blut aufzunehmen. Bei unseren Unter - artérias aorta ventral e dorsal, sendo o sangue pre - suchungen konnten wir nachweisen, dass zwei der sumivelmente bombeado no seu tubo digestivo pela Arten – Vandellia cirrhosa und V. sanguinea – die pressão sanguínea do seu hospedeiro. Sugerimos Hauptschlagadern aufsuchen. Beide Arten beißen am que os candirus não precisam de nenhum mecan - häufigsten in die ventralen oder dorsalen Arterien und ismo especial de sucção ou bombeamento para far - nutzen höchstwahrscheinlich den Blutdruck des Wirts- tar-se de sangue, porém simplesmente usam seus fisches, um das Blut in den eigenen Körper aufzuneh- dentes aguçados para fazer a incisão numa artéria. men. Nach unseren Ergebnissen benötigen die Schmer - Sendo este o caso, a noção do candiru sugador de lenwelse keinen speziellen Saug- oder Pumpmechanis - sangue é um conceito equivocado. mus, um sich das Blut des Wirtstiers möglichst rasch einzuverleiben, sie benutzen lediglich ihre nadelspitzen Sommario Zähne zu einem Einstich in eine Arterie. Die bisherige Le specie di pesci gatto tricomicteridi del genere Beschreibung, es handle sich um „blutsaugende“ Vandellia (comunemente noti come candirus) si Fische, erweist sich damit als missverständlich. nutrono del sangue di altri pesci, di solito penetrando

31 aqua vol. 8 no. 1 - 2004 Vampire catfishes seek the aorta not the jugular: candirus of the genus Vandellia (Trichomycteridae) feed on major gill arteries of host fishes nella camera branchiale dei loro ospiti. Tuttavia, il sito evidence that strengthens the suggestion of de Pinna esatto su cui questi pesci si attaccano non è mai stato & Wosiacki (2003) and weakens that of Spotte (2002) documentato. In questo articolo, viene illustrato come concerning the blood intake of the candirus of the due specie di candiru, Vandellia cirrhosa e V. san - genus Vandellia . guinea, vadano alla ricerca dell’arteria branchiale principale. Entrambe addentano soprattutto le arterie Methods dorsali e ventrali e il sangue viene così pompato nel The candirus we studied were caught with seine loro corpo dalla pressione sanguigna del loro ospite. nets in shallows with a muddy/sandy bottom in the Si conclude che i candiru non necessitano di nessun Solimões and Amazonas Rivers, near the Ilha do apparato atto a succhiare o a pompare sangue per Careiro (03°12’S, 59°60’W), Amazonas, northern ingurgitarne la maggior quantità possibile, ma sono Brazil. The net was dragged to the bank and its con - sufficienti i loro denti affilati per incidere la parete arte - tents emptied into a large plastic bowl. Fishes other riosa. Ne consegue che la denominazione di succhia - than candirus were released, and the candiru trans - tori di sangue attribuita ai candiru non risulta corretta. ferred with the water into plastic bags. In the labora - tory, 95 candirus were placed in two large aquaria Introduction (70-90 l) with aerated water from their habitat, and The candirus, neotropical freshwater Vandelliinae kept unfed for 2-5 days. Mortality over one week was catfishes, are known to feed on the blood of larger negligible (about 2%). Three laboratory-raised speci - fishes, usually entering the gill chamber of the host to mens of the tambaqui, Colossoma macropomum take the fluid there (Eigenmann, 1918; Kelley & Atz, (Characidae: Serrasalminae), 187-222 mm standard 1964; de Pinna, 1998; Spotte et al., 2001). Their feed - length (SL) were used in staged encounters to record ing habits were recently summarised by Spotte (2002), and included stories of attacks on humans, as well as conjecture on the mechanism by which blood is taken from fish hosts. The common names of van - delliine candirus, “bloodsucking catfishes”, and the presumptive descriptions of their feeding (Eigen - mann, 1918; Kelley & Atz, 1964; de Pinna, 1998; Spotte, 2002) imply that the blood is sucked from the host. In their account on the feeding of the minute Paravandellia oxyptera (as Branchioica bertonii), Machado & Sazima (1983) suggest that this candiru takes blood from its host by biting the proximal and medial parts of the gill filaments, which would then bleed freely into the alimentary tract of the catfish. In their account of feeding experiments with the larger Vandellia cirrhosa (as V. cf. plazaii), Spotte et al. (2001) found no evidence of gill damage on the fishes offered to this candiru. Spotte (2002) describes a hypothetical blood-pumping mechanism to explain how a larger candiru might quickly ingest a large vol - ume of blood. Published photographs of the larger species of Van - dellia feeding on captive goldfish show that this can - diru is attached somewhere at the upper or lower gill corners, under the gill cover of the host fish (Kelley & Atz, 1964; Spotte et al., 2001). Despite the fact that in these photos the candiru’s head is hidden, its position in the gill chamber and the very short time needed for the fish to become engorged with blood strongly indi - cate that the catfish seizes one of the major blood vessels, most probably an artery. Recently de Pinna & Wosiacki (2003) suggested that the larger species of Vandellia use their specialised teeth to lacerate a Fig. 1. Vandellia cirrhosa taking blood in the gill chamber major gill vessel of the host and feed on its blood, of a Colossoma macropomum host: positioned at the without damaging the gills. We recorded the feeding lower corner of the gill chamber (below), and somewhat behaviour in captivity of two candiru species, Vandel - higher (above). Note a little blood escaping from the gill lia cirrhosa and V. sanguinea , and here present chamber. Photos by I. Sazima. aqua vol. 8 no. 1 - 2004 32 Jansen Zuanon and Ivan Sazima the feeding behaviour of the candirus. The candiru the Instituto Nacional de Pesquisas da Amazônia attacking the tambaqui were observed directly, pho - (INPA) and the Museu de História Natural da Univer - tographed, and video-taped. In a few photographs sidade Estadual de Campinas (ZUEC). Vandellia cir - and video-records, the host fish was held in cotton- rhosa : INPA 21449 (81); ZUEC 6202 (1); 6203 (3); V. gloved hands. Occasionally, a submerged host fish sanguinea : INPA 21450 (2); 6204 (1); Vandellia sp.: was held belly up and its gill covers were gently lifted INPA 15599 (27); 15600 (14); Colossoma macropo - by hand to afford a better view of the candiru’s posi - mum : INPA 21451 (03). Digital images and the video- tion within the gill chamber. No tambaqui died from tape of feeding sequences are in the ZUEC fish photo attacks by the candirus or as a result of handling. The and video files (tape #16). host specimens were later anaesthetised and kept cool until death. A post-mortem inspection was car - Results ried out to discover wounds in the gill chamber and to In about half of the netted candirus blood in the verify which vessels had mostly been used by the digestive tract was visible through the body tissues; candiru for taking blood. some of them released blood from their cloacal open - The V. cirrhosa and V. sanguinea individuals ing on handling. The same behaviour was recorded observed measured 30.9-50.3 mm (n = 93) and 34.8- under aquarium conditions, but no candiru was 72.0 mm SL (n = 4) respectively. Focal animal and all observed to regurgitate any trace of blood even if occurrences samplings (Lehner, 1979) were used in roughly handled. Vandellia cirrhosa and V. sanguinea observation sessions lasting 10-30 min. Special atten - displayed similar feeding behaviour. The feeding tion was paid to the site where the candiru gained sequence began with the candiru approaching a host access to the tambaqui gill chamber, and to its sub - fish and swimming alongside it, aiming at the gill sequent position on the gills. The length of stay in the chamber. When close to the edge of the gill cover, the gill chamber and the time needed for a candiru to candiru attempted to penetrate the gill chamber by become engorged itself were measured with a hand- forcing itself underneath. The tambaqui displayed a held chronometer (the video-tapes were analysed and repertoire of defensive actions aimed at avoiding or the results pooled with the direct observations). hampering the candiru attacks (see below). After Avoidance behaviour of the host when attacked by some time the candiru generally succeeded in enter - the candiru was also recorded and video-taped. ing the gill chamber, usually through the lower angle Voucher specimens of the candirus and tambaquis (formed by the edge of the gill cover and the isthmus) used in the observations are in the fish collections of (N = 23). It also entered through the upper angle

Fig. 2. Vandellia cirrhosa in the gill chamber of Colossoma macropomum (gill cover abducted) showing its positioning at the angle formed by the gill arch and the upper part of the gill cover. The candiru abdomen is beginning to swell with blood. Photo by I. Sazima.

33 aqua vol. 8 no. 1 - 2004 Vampire catfishes seek the aorta not the jugular: candirus of the genus Vandellia (Trichomycteridae) feed on major gill arteries of host fishes

(N= 7), very rarely under the middle portion of the gill taking blood from there. After it left, two other individ - cover (N = 3), and only once entered through the uals entered in the same way to feed on the host’s host’s mouth (but see below). The host would often blood. The time required by the candiru to become shudder or jerk a little as the candiru entered and engorged with blood and leave the gill chamber var - moved within the gill chamber. Depending on the can - ied between 30 and 145 sec (x=58.2; n= 6): it seemed diru’s relative size, it either disappeared entirely into to be related to the relative size of the catfish and to the gill chamber or remained partly exposed. When a its success in attaching itself quickly to a large blood part of the candiru body remained visible, sinuous vessel. movements seemingly related to its positioning within The tambaqui was successful in circumventing or at the chamber were clearly seen; shortly afterwards least greatly hindering an attacking candiru by press - these movements ceased and the candiru hung limp ing it under the membranous gill cover flap, which (Fig. 1) rarely moving to reposition itself. caused the catfish to retreat, or by using its pectoral When the gill cover was spread so as to expose the fin to press it against its own flank or to sweep it from tambaqui’s gill chamber, the candiru could be seen the gill cover edge. Another method of defence was to positioned deep in the corner formed by the inner face slow down gill ventilation, making shallow breathing of the gill cover and the base of the gill arches, or in a movements, or even stopping ventilation entirely dur - similar position in the upper corner (Fig. 2), presum - ing the attack. Additionally, the tambaqui was able to ably taking blood from the ventral or dorsal aorta (see close the gill cover on the side under attack, and ven - below). The belly of the candiru was clearly seen to tilate through the opposite side. The most extreme swell quickly and continuously as the host’s blood defence recorded was shutting both gill covers and was taken. After a while the candiru made a few, short mouth, completely closing off the gill chamber. forward movements, curved its body and left the gill Post mortem inspection of the gill chamber of host fish chamber engorged with blood (Fig. 3). After the can - under a stereomicroscope revealed no observable diru attack, blood was sometimes observed to ooze or damage to the gill filaments. However, punctures and even pulse out of the gill chamber. cuts were evident, mostly in the angle formed by the The lower corner of the gill chamber was preferred base of the first gill arch and the inner face of the gill to the upper one (23 vs. 7; X 2 = 8.533; P< 0.003) irre - cover and/or in a similar spot in the upper angle. The spective of the host’s position in the aquarium. When cuts were relatively deep, wide, crescent-shaped or the candiru pushed itself under the middle portion of elliptical wounds with coagulated blood inside (Fig. 4). the gill cover and did not position itself in the lower or Close to the opposing ends of the cut were conspicu - upper angle, it usually left the host without taking ous puncture marks. Occasionally a small but obvious blood. However, it sometimes managed to attach cut was also seen on the median portion of the exter - itself to the gill arch and presumably took blood from nal face of the first gill arch. an afferent or efferent gill artery (N = 2). In the last session on the fifth day of observation, a previously Discussion used tambaqui host resorted to an extreme defence Our observations support the suggestion by de strategy (see below): it closed all breathing openings Pinna & Wosiacki (2003) that large candirus of the and ceased ventilation. However, a candiru forced its genus Vandellia take blood from their hosts through way into the host’s posterior nostril and succeeded in major gill vessels. The evidence obtained here sup -

Fig. 3. Vandellia cirrhosa swimming: it is engorged with blood after a feeding session. Actual size 37.2 mm SL (ZUEC 6202). Photo by I. Sazima. aqua vol. 8 no. 1 - 2004 34 Jansen Zuanon and Ivan Sazima ports the view that these vessels are the ventral and other structure apparently suited for an efficient intake dorsal aorta and/or the afferent and efferent gill arter - of fluids (e.g., the mandibular abductor muscles are ies. This view is strengthened by the observation of weakly developed). Some species of the order Perci - the candiru’s positioning, its quick engorging with formes have protrusible jaws and several of them are blood, and the blood spurting from the gill chamber able to suck water and prey into their oral chambers, Blood pulses from a damaged artery, not from a vein. but this behaviour is only intermittent (e.g., Lauder, We favour the view that the preferred vessels are the 1982; Liem, 1991), whereas the intake of blood by the ventral and dorsal aorta arteries, since these are candiru is continuous. The gut of species of Vandellia larger in diameter and are situated in the angle where is a straight tube, with loosely-spaced fibres within the the candiru bites (see figures of a fish’s main blood connective tissue lining the walls (see figures in vessels in Helfman et al., 1997). However, when the Spotte, 2002), features that most probably facilitate candiru is positioned under the middle of the gill the quick and considerable swelling of the candiru’s cover, it is likely to take blood from the afferent or belly during the intake of blood. efferent gill arteries. This latter positioning was The puncture-like wounds left by the candiru attack unusual and mostly occurred when experimentally are probably due to the fish using the interopercular exposing the gill arch by pulling back the host’s gill (and possibly opercular) spines to anchor itself in cover, or when another candiru was already taking position. The crescent-shaped or elliptical cuts blood at the upper or lower corners (this is probably through which the blood is taken are probably made rare under natural conditions). Entry into the nostril is by the sharp, well-developed, teeth on the medial pre- also rare and most probably due to the catfish having maxilla (see illustrations in Spotte, 2002). The wounds been starved for as long as five days. This may shed are most probably widened by lateral movements of some light on the occasional reports of candirus the candiru’s head and front end whilst in the host’s entering body openings (e.g. cloaca) other than the gill chamber. gill chamber of their fish hosts, and may perhaps also Since the candiru may be vulnerable to predation relate to the highly unusual penetration of the human and/or to mutilation of exposed parts while taking urethra or vagina by the candiru (see Spotte, 2002 for blood from its host, it may advantageous to keep the a few accounts). length of stay in the gill chamber to a minimum. Both We suggest that the blood pressure of the host fish the Vandellia species studied live in shallow water is sufficient to pump blood steadily into the digestive over a mud/sand bottom and have patchy distribution. tract of the candiru until it is gorged. That this parasitic Thus, if a host fish quickly moves into deeper water catfish employs a pumping mechanism while feeding while the candiru is still in the gill chamber, when the (e.g. Spotte, 2002) seems unlikely. Our view is sup - latter leaves the chamber it would be remote from its ported by the fact that the blood pressure of several usual territory and exposed to predators. fish species varies between 30 and 70 mm Hg, with The avoidance mechanisms here recorded for the highest values recorded at the ventral aorta artery Colossoma macropomum whilst under attack by the (Randall, 1970). This latter fact may explain the can - candiru (e.g., tightening its gill cover and using its diru’s preference for the anterior lower angle of the gill pectoral fins) strongly indicate that this species is one chamber. An alternative and not mutually exclusive of the potential hosts in the wild, and has therefore explanation is that the ventral angle is slightly more accessible than the dorsal angle. The high blood pressure in the aorta would also explain the speed with which the catfish becomes engorged. As a reverse pressure is presumably exerted by the cat - fish’s enormously swollen digestive tract, any further mechanism would probably involve some kind of valve or sphincter to prevent reflux of the ingested blood. The fact that under stress candirus only released blood via the cloacal opening lends support to this suggestion. Other trichomycterids under stress regurgitate recently ingested food, (pers. obs.). The idea that the candiru sucks blood is misleading, since the fish actually acts as a recipient for the blood enter - ing its digestive tract under the pressure of the car - diovascular system of its host. Fig. 4. The elliptical wound in the ventral aorta (centre, The view that the candiru does not suck blood is still bleeding) cut by Vandellia cirrhosa to feed on a supported by an inspection of its oral structures: the Colossoma macropomum host. Note the position of the oral chamber is of the generalised siluroid type ( our wound in the angle between the inner face of the gill pers. obs.), and the fish has no protrusible jaws or any cover and the base of the gill arches. Photo by I. Sazima.

35 aqua vol. 8 no. 1 - 2004 Vampire catfishes seek the aorta not the jugular: candirus of the genus Vandellia (Trichomycteridae) feed on major gill arteries of host fishes developed defensive measures. This view is strength - Helfman, G. S., B. B. Collette & D. E. Facey. ened by the fact that we only tested naïve, laboratory- 1997. The diversity of fishes . Blackwell . Science, raised tambaqui, which would not have learned Malden, 528 pp. defen sive behaviour. No special avoidance mecha - Kelley, W. E. & J. W. Atz. 1964. A pygidiid catfish that nisms other than flight were recorded for the exotic gold - can suck blood from goldfish. Copeia, 1964 (4): 702- fish (Carassius auratus), or for the relatively small native 704. cichlid (Cichlasoma amazonarum) whilst under attack Lauder, G. V. Jr. 1982. Patterns of evolution in the by the candiru (Spotte et al., 2001). Fish hosts reported feeding mechanisms of actinopterygian fishes. for vandelliine candirus under natural conditions include American Zoologist, 22 : 275-285. species of medium-sized to large characins, such as Lehner, P. N. 1979. Handbook of ethological meth - Piaractus brachypomus , Pygocentrus nattereri , Salmi - ods . Garland STPM Press, New York, 403 pp. nus maxillosus , Brycon sp., and large catfishes, such as Liem, K. F. 1991. Functional morphology. In: Cichlid Brachyplatystoma vaillanti and Pseudoplatystoma spp. fishes: behaviour, ecology and evolution. (Ed. M. H. (Eigenmann, 1918; Guimarães, 1935; Devicenzi & A. Keenleyside): 129-150. Chapman & Hall, London. Vaz-Ferreira, 1939; Miles, 1943). Machado, F. A. & I. Sazima. 1983. Comportamento Machado & Sazima (1983) suggested that the alimentar do peixe hematófago Branchioica bertonii minute Paravandellia oxyptera takes blood from its (Siluriformes, Trichomycteridae). Ciência e Cultura, hosts by biting the proximal and medial parts of the gill 35 (3): 344-348. filaments, which would then bleed freely into the ali - Miles, C. 1943. On three recently described species mentary tract of the candiru. This suggestion was and a new genus of pygidiid fishes from Colombia. supported by the presence of small scratches and fur - Revista da Academia Colombiana de Ciencias ther bleeding of the filaments seen after feeding by Exactas, Fisicas e Naturales, 5: 367-369. these candirus. However, this view remains untested, de Pinna, M. C. 1998. Phylogenetic relationships of even if it may apply to small species which attack very Neotropical Siluriformes (Teleostei: Ostariophysi); large hosts, such as the catfishes Pseudoplatystoma historical overview and synthesis of hypotheses. In: spp. (Machado & Sazima, 1983). Minute candirus are Phylogeny and classification of Neotropical fishes. unlikely to be able to cut through the relatively large, (Eds. L. R. Malabarba, R. E. Reis, R. P. Vari, Z. M. tough, major gill vessels of their large hosts; they S. Lucena & C. A. S. Lucena): 279-330. Edipucrs, most probably seek gill vessels of a diameter appro - Porto Alegre. priate to their own size. de Pinna, M. C. & W. Wosiacki. 2003. Family Tri - chomycteridae (pencil or parasitic catfishes). In: Acknowledgements Check list of the freshwater fishes of South and Cen - We thank the INPA staff fishermen for company and tral America. (Eds. R. E. Reis, S. O. Kullander & C. help in the field; R. Roubach and A. Storti Filho for J. Ferraris, Jr.): 270-290. Edipucrs, Porto Alegre. donating the Colossoma specimens; J. A. A. Gomes Randall, D. J., 1970. The circulatory system. In: Fish for allowing the use of the laboratory in his charge; the physiology Vol. IV. (Eds. W. S. Hoar & D. J. Ran - fish parasitology research group for access to the lab - dall): 133-172. Academic Press, New York. oratory in their care; F. Mendonça for stereomicro - Spotte, S., 2002. Candiru: life and legend of the scope photographs; E. Ferreira for digital video- bloodsucking catfishes . Creative Art Book, Berkeley, records; P. E. Gibbs for critical reading and improve - 322 pp. ment of the English; F. A. Bockmann for suggestions Spotte, S., P. Petry & J. A. S. Zuanon. 2001. Exper - and perceptive comments on the bucco-pharyngeal iments on the feeding behavior of the hemato- apparatus of candirus; the CNPq, FAPESP, and INPA phagous candiru, Vandellia cf. plazaii . Environmen - for financial support. tal Biology of Fishes, 60 (4): 459-464.

References Devicenzi, G. J. & R. Vaz-Ferreira. 1939. Nota pre - liminar sobre un pygidido hematofago del rio Uruguay. Archivos de la Sociedad de Biología de Montevideo, 9 (3): 165-178. Eigenmann, C. H. 1918. The Pygidiidae, a family of South American catfishes. Memoirs of the Carnegie Museum, 7 (5): 259-398. Guimarães, J. R. A. 1935. Contribuição para o con - hecimento de uma nova espécie de peixe hematophago, ectoparasita de “Characidae”, encon - trado em São Paulo (Rio Tietê). Revista de Industria Animal, 2 (3): 300-304. aqua vol. 8 no. 1 - 2004 36 aqua, Journal of Ichthyology and Aquatic Biology

Novaculoides , a new genus for the Indo-Pacific labrid fish Novaculichthys macrolepidotus John E. Randall and John L. Earle

Bishop Museum, 1525 Bernice St., Honolulu, HI 96817-2704, USA

Accepted: 19.09.2003

Keywords l’anale de taille équivalente; les ventrales des mâles Taxonomy, Labridae, Indo-Pacific, new genus souvent plus longues que la tête; 3.1-4.2 LS. Novac - ulichthys est désormais un genre monotypique pour Abstract l’espèce taeniourus (Lacépède). The new genus Novaculoides is proposed for one species of labrid fish previously classified as Novac - Sommario ulichthys macrolepidotus (Bloch). The genus is dis - Il nuovo genere Novaculoides viene proposto per tinct from Novaculichthys in possessing the following una specie di labride precedentemente classificato characters: anterior pair of canine teeth in jaws curv - come Novaculichthys macrolepidotus (Bloch). Il ing laterally; two or three oblique rows of small genere si distingue da Novaculichthys nel possedere embedded scales on cheek; head short, its length la seguente combinazione di caratteri: i due canini 3.4-3.65 in SL; body moderately elongate, the depth anteriori ricurvi lateralmente; due o tre file oblique di 2.8-3.0 in standard length; longest dorsal and anal piccole scaglie infossate sulle guance; capo breve, soft rays about equal in length; pelvic fins of males con lunghezza che sta 3.4-3.65 nella SL; corpo mo- often longer than head, 3.1-4.2 in standard length. deratamente allungato, l’altezza 2.8-3.0 volte nella Novaculichthys is now monotypic for the species tae - SL; il più lungo raggio molle dorsale circa uguale al niourus (Lacépède). più lungo raggio molle anale; pinne pelviche nei maschi generalmente più lunghe della testa, 3.1-4.2 Zusammenfassung nella SL. Novaculichthys diventa ora un genere Der neue Gattungsname Novaculoides wird für die monotipico con la sola specie taeniourus (Lacépède). eine Art vorgeschlagen, die bisher als Novaculichthys macrolepidotus (Bloch) bezeichnet wurde. Die neue Introduction Gattung unterscheidet sich durch folgende Merkmale Norman (1957) divided the fishes of the family Labri - von Novaculichthys: vorne liegendes Paar von Eck - dae, popularly called wrasses, into nine subfamilies, zähnen in seitlich gebogenen Kiefern; zwei oder drei one of which was the Hemipteronotinae in which he schräge Reihen kleiner Schuppen an den Wangen; classified three genera, Cymolutes Günther, Kopf kurz: 3,4 bis 3,65 in Standardlänge (SL); Rumpf Hemipteronotus Lacepède, and Iniistius Gill. He mäßig länglich, Tiefe 2,8 bis 3,0 in SL; die längsten included eight genera as synonyms of Hemipterono - weichen Flossenstrahlen dorsal und anal etwa gleich tus , among them Xyrichtys Cuvier and Novaculichthys lang; Bauchflossen der Männchen oft länger als der Bleeker. Randall & Bauchot (1993) explained that Kopf, 3,1 bis 4,2 in SL. Novaculichthys ist jetzt mono - Hemipteronotus was intended by Lacepède for the typisch für die Art taeniourus (Lacépède). Pilotfish ( Naucrates ductor ), the generic name Hemipteronotus in reference to its short dorsal fin. Résumé The razorfish now identified as Iniistius pentadactylus Le nouveau genre Novaculoides est proposé pour (Linnaeus) was included in the synonymy of une espèce de labridé préalablement classé comme Hemipteronotus , and the genus was later restricted to Novaculichthys macrolepidotus (Bloch). Le genre se it. Because both Naucrates and Xyrichtys were threat - distingue de Novaculichthys par les caracteristiques ened by Hemipteronotus , Opinion 1799 of the Inter - suivantes: la paire antérieure de canines dans national Commission on Zoological Nomenclature mâchoires courbées latéralement; deux ou trois rangs suppressed Hemipternonotus . Xyrichtys then obliques de petites écailles enchâssées sur la joue; la replaced Hemipteronotus , and the subfamily name tête courte, sa longueur étant de 3.4-3.65 en LS; le changed to Xyrichtyinae. corps modérément élancé, sa mauteur étant de 2.8- The majority of authors have not accepted Norman’s 3.0 LS; les plus longs rayons mous de la dorsale et de placement of Novaculichthys as a synonym of what is

37 aqua vol. 8 no. 1 - 2004 Novaculoides , a new genus for the Indo-Pacific labrid fish Novaculichthys macrolepidotus now Xyrichtys . Three species have long been classi - culichthys taeniourus , which occurs mostly on rubble- fied in Novaculichthys , the type species N. taeniourus sand areas near reefs, and the Seagrass Wrasse, N. (Lacepède), N. macrolepidotus (Bloch), and N. woodi macrolepidotus . The former can dive into sand as Jenkins. needed, while the latter relies on its protective col - Schultz in Schultz & collaborators (1960) erected a oration (green in seagrass) and cryptic behavior in new genus, Novaculops , for woodi . Some later dense benthic plant growth. authors, however, preferred to retain woodi in Novac - The authors have long been aware that Novac - ulichthys . ulichthys macrolepidotus seems too divergent from Randall & Earle (2002) discovered that woodi belongs the type species and the only other species of the in the genus Xyrichtys , the type species of which, X. genus, N. taeniourus , to remain in the genus. The pre - novacula Cuvier, is one of five Atlantic razorfishes sent study confirms that it warrants placement in a (reviewed by Randall, 1965, then placed in new genus. A brief diagnosis of the Xyrichtyinae is Hemipteronotus ). Xyrichtys is represented by three given below, followed by a key to the genera of the species in the eastern Pacific (Victor et al ., 2001). A subfamily, a diagnosis of the new genus, and a fourth eastern Pacific razorfish, Iniistius pavo (Valenci - species account of the one species of the genus. ennes), is also wide-ranging in the Indo-Pacific region. Gill (1862) erected the genus Iniistius , based on its Materials and Methods having the first two dorsal spines flexible, detached Specimens were examined at the Bernice P. Bishop from the rest of the fin, and elongate (especially in Museum, Honolulu (BPBM); California Academy of juveniles). Recent authors such as Yamakawa in Sciences, San Francisco (CAS, SU), and the U.S. Masuda et al. (1984), Randall in Smith & Heemstra National Museum of Natural History, Washington, (1986), Masuda & Kobayashi (1994), and Okamura & D.C. (USNM). Amaoka (1997) regarded Iniistius as a synonym of Xyrichtys . However, Randall & Earle (2002), following Novaculoides macrolepidotus material examined the unpublished PhD thesis on labrid osteology by Tri- Red Sea : Sinai Peninsula, Ras Muhammad, man - thuc Nguyen (1974), provided the following charac - grove channel, USNM 221762, 85 mm. ters to resurrect Iniistius as a valid genus for pavo and Seychelles : La Digue, BPBM 21651, 74.5 mm. Ami - other Indo-Pacific species that had previously been rantes, Alphonse, BPBM 35604, 2: 60-60.3 mm. placed in Xyrichtys : palatine bone overlaps the Aldabra, USNM 289765, 3: 39-68 mm. Indonesia : ectropterygoid in Iniistius , whereas it is separate in Lombok, BPBM 29800, 121.6 mm. Papua New Xyrichtys ; there are no dorsal pterygiophores Guinea : Admiralty Islands, USNM 114807, 82 mm. between the second and third neural species of Iniis - Santa Cruz Islands : Taumako Island (9°51’S, tius , but two in Xyrichtys ; the skull is notably higher in 167°9.5’E), USNM 357184, 24 mm. Philippines : adult Iniistius than in Xyrichtys . Externally, the origin Negros, Dumaguete, SU 38765, 2: 84-90 mm. Cebu, of the dorsal fin is more anterior in Iniistius , the space Cebu City market, BPBM 22094, 3: 118-126 mm. between the second and third dorsal spines is much Luzon, Sorsogon Province, Gubal, USNM 327866, 5: broader in Iniistius , and the membrane between these 52-101 mm. Cagayan Province, Santa Ana, USNM two spines is strongly incised, or in the case of I. pavo 309339, 4: 53-104 mm. San Vicente, USNM 309377, and I. dea (Temminck & Schlegel), completely absent. 45 mm. Batanes, USNM 332196, 47 mm. Palau : CAS Randall & Carlson (1997) described Ammolabrus 73622, 3: 68-102 mm. Lord Howe Island : BPBM dicrus as a new genus and new species of the sub - 35031, 125 mm. Fiji : Viti Levu, AMS I.222-32-014, 71 family Xyrichtyinae from the Hawaiian Islands, differ - mm. Tonga : Tongatapu, BPBM 37916, 128 mm. ing notably from the other species, which are benthic, in forming schools that feed on zooplankton well Subfamily Xyrichtyinae above the sandy substratum. The fishes of the Xyrichtyinae, many of which are Diagnosis called razorfishes because of their strongly com - Dorsal rays IX,12-15, the first one or more spines pressed bodies and the firm ridge anteriorly on the flexible; anal rays III (rarely II),12-13; branched caudal head, are able to escape approaching predators by rays 10-12; pectoral rays 12-13, the uppermost rudi - diving head-first into sand. Most live over open mentary; pelvic rays I,5; longitudinal scale series 72- stretches of sand away from the shelter of coral or 93 ( Cymolutes ) or 26 (all other genera); lateral line rocky reef or heavy plant growth because of their abil - interrupted; cheek naked or with a few rows of small ity to avoid predation in this unique way. Ammolabrus scales; opercle naked except for 1-4 scales dorsally; dicrus generally escapes predators by swiftly swim - gill rakers short, fewer than 26; branchiostegal rays 5- ming in elusive schools, but it will take refuge under 6; vertebrae 25; a single pair of large canine teeth sand as a last resort. Two species of the subfamily anteriorly in jaws, the lower pair fitting inside upper that do not live over open sand far from the shelter of when mouth closed (if a second pair of canines are reef or plant cover are the Rockmover Wrasse, Nova - present, they are about half length of anterior pair); no aqua vol. 8 no. 1 - 2004 38 John E. Randall and John L. Earle canine at corner of mouth; pharyngeal teeth bluntly and third dorsal spines much greater than spaces conical, nodular, or as very small molars; preopercu - between other spines; membrane between sec - lar edge free and without serration; body depth vari - ond and third dorsal spines deeply incised (or in able, but body always compressed, the width varying the case of two species, the first two spines com - from 2-3.5 in depth; no scales basally on dorsal or pletely separate) ...... Iniistius anal fins; caudal fin usually slightly rounded (slightly forked in Ammolabrus ). Future study may result in the removal of the genus Novaculoides , new genus Cymolutes , represented by three fine-scaled Indo- Type species: Labrus macrolepidotus Bloch, 1791 Pacific species, from the Xyrichthyinae. Diagnosis Dorsal and anal rays IX,13; lateral line interrupted, Key to the genera of Xyrichtyinae the pored scales 20 + 5-6; a pair of inwardly and lat - erally curving canine teeth anteriorly in jaws; no 1a. Scales small, the lateral line scales 48-68 + 15- canine tooth at corner of mouth; pharyngeal teeth 22; branched caudal rays 10; head naked ...... small and bluntly conical to nodular; two or three ...... Cymolutes oblique rows of small embedded scales from behind 1b. Scales not small, the lateral line scales 19-22 + 4- corner of mouth to behind lower part of eye; body 6; branched caudal rays 12 (rarely 11); some moderately elongate, the depth 3.5-3.65 in SL, and scales present on head (may be only one or two compressed, the width 2.8-3.1 in depth; head short, dorsally on opercle) ...... 2 3.4-3.65 in SL; dorsal profile of head about 45°; no 2a . Caudal fin slightly forked; all dorsal spines flexi - acute ridge anteriorly on head; origin of dorsal fin ble; body elongate, the depth 4.2-4.45 in standard nearly reaching to above upper end of preopercular length; upper jaw strongly protrusible, the median margin; first two dorsal spines flexible, the tips curving process of premaxilla extending to above anterior posteriorly; no broad gap between base of second edge of pupil ...... Ammolabrus and third dorsal spines; dorsal spines short (except 2b. Caudal fin truncate to slightly rounded; only the prolonged first two of juveniles), the longest soft rays first one or two dorsal spines flexible; body not nearly twice as long as longest spine; anal soft rays elongate the depth 2.3-3.9 in standard length; about equal in length to dorsal soft rays. upper jaw not protrusible ...... 3 3a. Pair of canine teeth anteriorly in jaws not curving Remarks laterally; anal soft rays notably longer than dorsal Novaculichthys is differentiated from Novaculoides soft rays ...... Novaculichthys by the following characters: anterior pair of canine 3b. Pair of laterally and inwardly curving canine teeth teeth in jaws not curved laterally; a single near-verti - anteriorly in jaws, the tips of lower pair overlap - cal row of small embedded scales behind and slightly ping base of upper pair when mouth closed; anal below eye; body depth 2.8-3.0 in standard length; soft rays about equal in length to dorsal soft rays head length 2.8-3.0 in standard length; longest anal ...... 4 soft rays about 1.2 times longer than longest dorsal 4a. A second pair of canine teeth in jaws half as long soft rays; pelvic fins of adults shorter than pectoral as first pair; no scales on cheek; head short, 3.4- fins, about 7 in standard length. 3.65 in SL; body moderately elongate, the depth Xyrichtys differs from Novaculoides in lacking a sec - 3.5-3.95 in SL; dorsal and anal soft rays 13; ond pair of canine teeth anteriorly in the jaws, half as longest dorsal soft ray about twice as long as long as the anterior canines; not having any scales on longest dorsal spine ..... Novaculoides , new genus the cheek or behind the eye; head not short, its length 4b . No second pair of canine teeth anteriorly in jaws; 3.1-3.4 in standard length; dorsal and anal soft rays small scales present on cheek; head not short, 12; longest dorsal soft ray at most 1.5 times longer 3.1-3.4 in SL; body not elongate, the depth 2.3- than longest dorsal spine. 3.4 in SL (except the Atlantic Xyrichtys martini - Although sharing some characters with Novacu- censis with depth 3.2-3.8 in SL); dorsal and anal lichthys and Xyrichtys , Novaculoides does not fit well soft rays 12; longest dorsal soft ray at most 1.5 in either genus. times longer than longest dorsal spine ...... 5 5a. Origin of dorsal fin more than an eye diameter behind eye; space between second and third dor - sal spines about equal to spaces between other spines; membrane between second and third dor - sal spines not incised ...... Xyrichtys 5b. Origin of dorsal fin over eye or less than half an eye diameter behind eye; space between second

39 aqua vol. 8 no. 1 - 2004 Novaculoides , a new genus for the Indo-Pacific labrid fish Novaculichthys macrolepidotus

Novaculoides macrolepidotus (Bloch, 1791) to 12 progressively smaller conical teeth; no canine Figs. 1-4 tooth posteriorly on upper jaw (at corner of mouth); a pavement-like band of small, close-set, discoid teeth Labrus macrolepidotus Bloch, 1791: 135, pl. 284, medial to conical teeth in each jaw in a maximum of fig. 2 (type locality unknown). three longitudinal rows; paired upper pharyngeal Labrus arago Quoy & Gaimard, 1824: 263, pl. 65, plates triangular, each with about 20 small teeth in fig. 2 (type locality, Iles des Papous). five or six anterior to posterior rows, the anterior teeth Labrus taenianotus Cuvier in Quoy & Gaimard, 1824: longest and bluntly conical, the remainder nodular 271 (type locality, Waigeo, Indonesia). and progressively smaller posteriorly; narrow median Julis trimaculata Valenciennes, 1839 (no locality; pre - limb of T-shaped lower pharyngeal plate with two to occupied by Julis trimaculata Quoy & Gaimard, 1834 three transverse rows of conical teeth, all but the first = Halichoeres trimaculatus ). few blunt; posterior limb broadly triangular with about Novacula julioïdes Bleeker, 1851: 354 (type locality, 50 nodular teeth in irregular transverse rows, the Banda Islands, Indonesia). largest teeth in posterior row. Body moderately elongate, the depth 3.5-3.95 in SL, Description and compressed, the width 2.8-3.1 in body depth; Dorsal rays IX,13; anal rays III,13; pectoral rays 12; head short, 3.4-3.65 in standard length; dorsal profile pelvic rays, I,5; principal caudal rays 12; upper and of head slightly convex, forming an angle of about 45° lower procurrent caudal rays 5; longitudinal scale to horizontal axis of body; no acute median edge on series 26; lateral line interrupted, the pored scales 20 front of head; snout length 2.80-3.2 in head length; + 5 or 6 (plus one pored scale on caudal fin base); eye diameter varying from 4.55 in head length in 60- scale rows above lateral line 1.5; scale rows below mm specimen to 6.3 in 128-mm specimen; fleshy lateral line to origin of anal fin 7.5; circumpeduncular interorbital width 4.2-4.9 in head length. scales 16; gill rakers 17-20; branchiostegal rays 5; Preopercular margin smooth and membranous, the vertebrae 9 + 16; tip of second neural spine ending posterior margin reaching above mouth but not to below ventral end of second dorsal pterygiophore; level of lower edge of eye, the ventral margin nearly third neural spine extending between second and reaching a vertical at corner of mouth. third dorsal pterygiophores. Nostrils small, in front of centre of eye, the anterior Mouth terminal to slightly ventral, the gape a little in a small short tubule, the posterior an oblique slit; oblique; upper jaw not protrusible; one pair of slender, suborbital pores 7. laterally and posteriorly curved canine teeth at front of Scales thin, cycloid, and adherent; largest scale on jaws, not fully covered by lips when mouth closed, the side of chest about half height of largest scale on side lower pair fitting inside upper pair when mouth closed, of body; no median predorsal scales; only two or three their tips overlapping base of upper pair; second pair embedded scales on side of nape anterior to origin of of teeth in jaws as small curved canines about half dorsal fin; two small partially embedded scales dor - length of anterior pair, each followed by a series of up sally on opercle; two or three oblique rows of small

Fig. 1. Mature female Novaculoides macrolepidotus , 60 mm SL, Alphonse Atoll, Seychelles. Photo by J. Randall aqua vol. 8 no. 1 - 2004 40 John E. Randall and John L. Earle

Fig. 2. Mature female Novaculoides macrolepidotus , 74.5 mm SL, La Digue, Seychelles. Photo by J. Randall

Fig. 3. Two male Novaculoides macrolepidotus , 120 and 126 mm SL, Cebu, Philippines. Photo by J. Randall

41 aqua vol. 8 no. 1 - 2004 Novaculoides , a new genus for the Indo-Pacific labrid fish Novaculichthys macrolepidotus embedded scales on cheek from just above corner of three dark markings with a submarginal orange line, mouth to behind lower edge of eye; no scales on fins the uppermost in large males may be replaced by two except basally on caudal fin; tubule of lateral line black lines, one of which continues dorsally on body; scales median and straight, the anterior series often a dark band or double line often present from eye to with a short, oblique, upper branch. front of snout; a narrow dark band extending Origin of dorsal fin nearly reaching a vertical at obliquely behind upper part of eye; a black spot on upper end of preopercular margin; first two dorsal first membrane of dorsal fin, edged anteriorly in white spines flexible, their tips curving posteriorly; space or pale blue; a large black spot usually present mid - between base of second and third dorsal spines only ventrally on chest; median fins often with pink mark - a little broader than that between the first two spines ings. A juvenile 5 cm in total length illustrated by or between third and fourth spines; dorsal spines Masuda & Kobayashi (1994: 288, fig. 8) is brown with short, only slightly longer posteriorly, the ninth 3.6- a few small black blotches midlaterally and anteriorly 3.85 in head length (except juveniles with prolonged on lateral line, three longitudinal rows of white first two dorsal spines); seventh to ninth dorsal soft blotches on body; head with brown, red, and white rays longest, 2.1-2.2 in head length; origin of anal fin bands extending from eye except ventrally; elevated below base of first dorsal soft ray; third anal spine 3.3- anterior part of dorsal fin mainly red. 3.8 in head length; seventh to ninth anal soft rays longest, 2.0-2.3 in head length; caudal fin slightly to Distribution moderately rounded, 1.25-1.45 in head length; pec - Red Sea and east coast of Africa to the Mariana toral fins short and broadly rounded, 1.8-2.0 in head Islands, Palau, Fiji, and Tonga; in the western Pacific length; pelvic fins of females 4.7-5.3 in SL; pelvic fins from the Ryukyu Islands to the Great Barrier Reef and of males often longer than head, 3.1-4.2 in SL. Lord Howe Island. Adults green to brownish yellow, the body of females with an irregular, midlateral, dark brown stripe or row Remarks of spots; body of males with small dark spots only Bloch‘s description of Labrus macrolepidotus was posteriorly; large females and males with two curved based on a single specimen. Paepke (1999: 90) listed black bands from eye across upper part of operculum the holotype in the Museum für Naturkunde der Hum - and a hemispherical black spot on opercular flap, all boldt Universität zu Berlin as ZMB 2633 and the stan -

Fig. 4. Underwater photograph of a large male Novaculoides macrolepidotus in seagrass, Cebu, Philippines. Photo by J. Randall. aqua vol. 8 no. 1 - 2004 42 John E. Randall and John L. Earle dard length as 71 mm. Although Bloch stated that the Smith, M. M. & P. C. Heemstra (eds.). 1986. Smiths’ locality of his specimen was not known, Paepke Sea Fishes. Macmillan South Africa, Johannesburg, apparently had reason to list it as the Indian Ocean. xx + 1047 pp. Novaculoides macrolepidotus has been collected Victor, B. C., Wellington, G. M. & C. Caldow. 2001. mainly from shallow seagrass beds and algal flats; A review of the razorfishes (Perciformes: Labridae) Bishop Museum specimens were collected from 1-2 of the eastern Pacific Ocean. Revista de Biologia m. In the seagrass this species is the same colour of Tropica 49, suppl. 1: 101-110. green as the surrounding plants. In addition to being difficult to see because of its protective coloration, it is difficult to approach underwater.a

References Bloch, M. E. 1791. Naturgeschichte der Ausländischen Fische. J. Morino & Comp., Berlin. Vol. 5, 152 pp. Gill, T. N. 1862. Catalogue of the fishes of Lower California in the Smithsonian Institution collected by Mr. J. Xantus. Proceedings of the Academy of Nat - ural Sciences of Philadelphia, 14 (3): 140-151. Masuda, H., Amaoka, K., Araga, C., Uyeno, T. & T. Yoshino (eds.). 1984. The Fishes of the Japanese Archipelago. Tokai University Press, Tokyo. Vol. 1 (text: xxii + 437 pp.) and vol. 2 (plates). Masuda, H. & Y. Kobayashi. 1994. Grand Atlas of Fish Life Modes (Color Variation in Japanese Fish). Tokai University Press, Tokyo. 465 pp. (in Japan - ese). Norman, J. R. 1957. A Draft Synopsis of the Orders, Families and Genera of Recent Fishes and Fish-like Vertebrates. British Museum (Natural History), Lon - don (unpublished photo offset copy, private circula - tion). 649 pp. Okamura, O. & K. Amaoka. 1997. Sea Fishes of Japan. Yama-kei Publisher, Tokyo. 783 pp. (in Japanese). Paepke, H.-J. 1999. Bloch’s fish collection in the Museum für Naturkunde der Humboldt Universität zu Berlin. A. R. G. Gantner Verlag KG, Ruggell / Liechtenstein. 216 pp. Randall, J. E. 1965. A review of the razorfish genus Hemipteronotus (Labridae) of the Atlantic Ocean. Copeia, 1965 (4): 487-501. Randall, J. E. & M. L. Bauchot. 1993. Case 2842 - Naucrates Rafinesque, 1810 an Xyrichtys Cuvier, 1814 (Osteichthyes, Perciformes): proposed conser - vation. Bulletin of Zoological Nomenclature, 50 (4): 277-281. Randall, J. E. & B. A. Carlson. 1997. Ammolabrus dicrus , a new genus and species of labrid fish from the Hawaiian Islands. Pacific Science, 51 (1): 29- 35. Randall, J. E. & J. L. Earle. 2002. Review of the Hawaiian razorfishes of the genus Iniistius (Perci - formes: Labridae). Pacific Science, 56 (4): 389- 402 . Schultz, L. P. & collaborators. 1960. Fishes of the Marshall and Marianas Islands. Bulletin of the United States National Museum, 202, vol. 2: ix + 418 pp.

43 aqua vol. 8 no. 1 - 2004 Index of aqua Vol. 7 (1-4) (Index by: 1. Author(s); 2. New Taxa; 3. Biology/Ecology/Biography/Reviews)

Author(s): Allen, Gerald R., Randall, John E. and Carlson, Bruce Allan: Cirrhilabrus marjorie, a new wrasse (Pisces: Labridae) from Fiji. aqua 7 (3): 113-118, October 2003. Allen, Gerald R. and Wright, Joan E.: Description fo a new species of damselfish (Pomacentridae: Pomacetrus) from Rodrigues Island, Indian Ocean. aqua 7 (4): 133-138, November 2003. Costa, Wilson J. E. M.: Rivulus paracatuensis n. sp. (Cyprinodontiformes: Rivulidae): a new rivuline species from the Rio São Francisco basin, Brazil. aqua 7 (1): 39-43, May 2003. Costa, Wilson J. E. M. and Nielsen, Dalton T. B.: Simpsonichthys reticulatus n. sp. (Cyprinodontiformes: Rivulidae): a new annual fish from the Rio Xingu flood - plains, Brazilian Amazon. aqua 7 (3): 119-122, October 2003. Feitoza, Bertran M., Rocha, Luiz A., Luiz-Junior, Osmar J., Floeter, Sergio R. and Gasparini, João L.: Reef fishes of St. Paul’s Rocks: new records and notes on biology and zoogeography. aqua 7 (2): 61-82, June 2003. Orlov, Alexei M.: Diets, feeding habits, and trophic relations of six deep-benthic skates (Rajidae) in the western Bering Sea. aqua 7 (2): 45-60, June 2003. Paschos, Ioannis, Nathanailides, cosmas, Kagalou, Ifigenia, Leka, Eufrosini, Tsoumani, Maria and Perdikaris, Costas: The prospects for restoring the nearly extinct population of the Adriatic sturgeon Acipenser naccarii Bonaparte 1836 (Acipenseridae) in Greece. aqua 7 (3): 123-132, October 2003. Randall, John E.: Thalassoma nigrofasciatum, a new species of labrid fish from the south-west Pacific. aqua 7 (1): 1-8, May 2003. Randall, John E. and Allen, Gerald R.: Paracheilinus rubricaudalis, a new species of flasherwrasse (Perciformes: Labridae) from Fiji. aqua 7 (3): 97-102, October 2003. Sanamyan, Karen and Schories, Dirk: Ascidians from the Strait of Magellan. aqua 7 (3): 89-96, October 2003. Soares, Marta S. C., Sousa, Luis and Barreiros, João Pedro: Feeding habits of the lizardfish Synodus saurus (Linnaeus, 1758) (Actinopterygii: Synodontidae) from the Azores. aqua 7 (1): 29-38, May 2003. Soares, Marta S. C. and Barreiros, João P.: Following associations with the striped red mullet Mullus surmuletus Linnaeus, 1758 (Perciformes: Mullidae) from the Azores. aqua 7 (4): 139-144, November 2003. Tokranov, Alexei M. and Orlov, Alexei M.: Some biological characteristics of the rare, little-studied gloved snailfish Palmoliparis beckeri Balushkin, 1996 (Liparidae, Teleostei), in the Pacific off the Northern Kuril Islands. aqua 7 (2): 83-88, June 2003. Triques, Mauro L., Vono, Volney and Caiafa, Emmanuelle V.: Astyanax turmalinesis, a new species of fish from the Rio Jequitinhonha basin, Minas Gerais, Brazil (Characiformes: Characida: Tetragonopterinae). aqua 7 (4): 145-150, November 2003. Williams, Jeffrey T. and Howe, Jeffrey C.: Seven new species of the triplefin fish genus Helcogramma (Tripterygiidae) from the Indo-Pacific. aqua 7 (4): 151-176, November 2003. Winterbottom, Richard: A new species of Trimma (Gobiidae) from the western Indian Ocean. aqua 7 (1): 9-12, May 2003. Winterbottom, Richard: Feja ranta, a new species of gobiid fish (Acanthopterygii; Perciformes) from Vietnam. aqua 7 (3): 97-102, October 2003. Winterbottom, Richard and Villa Cesar A.: A new species of the Trimma caesiura complex (Gobiidae, Teleostei) from the north-eastern margin of the Australian Plate, with a redescription of the other nominal species in the complex. aqua 7 (1): 13-28, May 2003.

New Taxa: Astyanax turmalinesis n. sp. A new species of fish from the Rio Jequitinhonha basin, Minas Gerais, Brazil (Characiformes: Characida: Tetragonopterinae). aqua 7 (4): 145-150, November 2003. Cirrhilabrus marjorie n. sp. A new wrasse (Pisces: Labridae) from Fiji. aqua 7 (3): 113-118, October 2003. Feja ranta n. sp. A new species of gobiid fish (Acanthopterygii; Perciformes) from Vietnam. aqua 7 (3): 97-102, October 2003. Helcogramma albimacula n. sp. Seven new species of the triplefin fish genus Helcogramma (Tripterygiidae) from the Indo-Pacific. aqua 7 (4): 151-176, November 2003. Helcogramma cerasina n. sp. Seven new species of the triplefin fish genus Helcogramma (Tripterygiidae) from the Indo-Pacific. aqua 7 (4): 151-176, November 2003. Helcogramma desa n. sp. Seven new species of the triplefin fish genus Helcogramma (Tripterygiidae) from the Indo-Pacific. aqua 7 (4): 151-176, November 2003. Helcogramma lacuna n. sp. Seven new species of the triplefin fish genus Helcogramma (Tripterygiidae) from the Indo-Pacific. aqua 7 (4): 151-176, November 2003. Helcogramma nesion n. sp. Seven new species of the triplefin fish genus Helcogramma (Tripterygiidae) from the Indo-Pacific. aqua 7 (4): 151-176, November 2003. Helcogramma nigra n. sp. Seven new species of the triplefin fish genus Helcogramma (Tripterygiidae) from the Indo-Pacific. aqua 7 (4): 151-176, November 2003. Helcogramma randalli n. sp. Seven new species of the triplefin fish genus Helcogramma (Tripterygiidae) from the Indo-Pacific. aqua 7 (4): 151-176, November 2003. Paracheilinus rubricaudalis n. sp. A new species of flasherwrasse (Perciformes: Labridae) from Fiji. aqua 7 (3): 97-102, October 2003. Pomacentrus rodriguesensis n. sp. Description fo a new species of damselfish (Pomacentridae: Pomacetrus) from Rodrigues Island, Indian Ocean. aqua 7 (4): 133-138, November 2003. Rivulus paracatuensis n. sp. A new rivuline species from the Rio São Francisco basin, Brazil. aqua 7 (1): 39-43, May 2003. Simpsonichthys reticulatus n. sp. A new annual fish from the Rio Xingu floodplains, Brazilian Amazon. aqua 7 (3): 119-122, October 2003. Thalassoma nigrofasciatum n. sp. A new species of labrid fish from the south-west Pacific. aqua 7 (1): 1-8, May 2003. Trimma lantana n. sp. A new species of the Trimma caesiura complex (Gobiidae, Teleostei) from the north-eastern margin of the Australian Plate, with a redescrip - tion of the other nominal species in the complex. aqua 7 (1): 13-28, May 2003. Trimma volcana n. sp. A new species of Trimma (Gobiidae) from the western Indian Ocean. aqua 7 (1): 9-12, May 2003.

Biology/Ecology/Biography/Reviews: A new species of the Trimma caesiura complex (Gobiidae, Teleostei) from the north-eastern margin of the Australian Plate, with a redescription of the other nominal species in the complex. aqua 7 (1): 13-28, May 2003. Ascidians from the Strait of Magellan. aqua 7 (3): 89-96, October 2003. Diets, feeding habits, and trophic relations of six deep-benthic skates (Rajidae) in the western Bering Sea. aqua 7 (2): 45-60, June 2003. Feeding habits of the lizardfish Synodus saurus (Linnaeus, 1758) (Actinopterygii: Synodontidae) from the Azores. aqua 7 (1): 29-38, May 2003. Following associations with the striped red mullet Mullus surmuletus Linnaeus, 1758 (Perciformes: Mullidae) from the Azores. aqua 7 (4): 139-144, November 2003. Reef fishes of St. Paul’s Rocks: new records and notes on biology and zoogeography. aqua 7 (2): 61-82, June 2003. Seven new species of the triplefin fish genus Helcogramma (Tripterygiidae) from the Indo-Pacific. aqua 7 (4): 151-176, November 2003. Some biological characteristics of the rare, little-studied gloved snailfish Palmoliparis beckeri Balushkin, 1996 (Liparidae, Teleostei), in the Pacific off the Northern Kuril Islands. aqua 7 (2): 83-88, June 2003. The prospects for restoring the nearly extinct population of the Adriatic sturgeon Acipenser naccarii Bonaparte 1836 (Acipenseridae) in Greece. aqua 7 (3): 123-132, October 2003. aqua vol. 8 no. 1 - 2004 44 Instructions to Authors al Indo-Pacific Estuaries. Australian Journal of Marine and Freshwater Research 31 :137-46. aqua is an international journal which publishes original sci- Day, J. H., Blaber, S. J. M., & J. H. Wallace. 1981. Estuarine entific articles in the fields of systematics, taxonomy, ethology, Fishes. 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Additional reprints may be ordered from Aquapress. aqua Journal of Ichthyology and Aquatic Biology Vol. 8 (1), February 2004 Contents:

Ivan Sazima and Cristina Sazim a: Daytime hunting behaviour of Echidna catenata (Muraenidae): why chain morays foraging at ebb tide have no followers ...... 1-8

Javad Ghasemzadeh, Walter Ivantsoff and Aarn: Historical overview of mugilid systematics, with description of Paramugil (Teleostei; Mugiliformes; Mugilidae), new genus ...... 9-22

Gerald R. Allen and Roger C. Steene: Chaetodontoplus vanderloosi , A new species of angelfish (Pomacanthidae) from Papua New Guinea ...... 23-30

Jansen Zuanon and Ivan Sazima: Vampire catfishes seek the aorta not the jugular: candirus of the genus Vandellia (Trichomycteridae) feed on major gill arteries of host fishes ...... 31-36

John E. Randall and John L. Earle: Novaculoides , a new genus for the Indo-Pacific labrid fish Novaculichthys macrolepidotus ...... 37-43

Index of aqua volume 7(1-4) ...... 44

Papers appearing in this journal are indexed in: Zoological Record; Biolis - Biologische Literatur Information Senckenberg; www.aquageo.com; www.Joachim-Frische.com

Cover photo: Vandellia cirrhosa taking blood in the gill chamber of a Colossoma macropomum host. Note a little blood escaping from the gill chamber. Photo by I. Sazima.

Underwater photograph of a large male Novaculoides macrolepidotus in seagrass, Cebu, Philippines. (See the Ms from John E. Randall and John L. Earle in this issue on pages 37-43). Photo by J. Randall.