aqua International Journal of Ichthyology

Vol. 12 (2), December 2006

Aquapress ISSN 0945-9871 aqua - International Journal of Ichthyology Managing Editor: Scope aqua is an international journal which publishes original Heiko Bleher scientific articles in the fields of systematics, , Via G. Falcone 11, biogeography, ethology, ecology, and general biology of 27010 Miradolo Terme (PV), Italy fishes. Papers on freshwater, brackish, and marine fishes Tel.: +39-0382-754707/08 will be considered. aqua is fully refereed and aims at pub - Fax: +39-0382-754129 lishing manuscripts within 2-4 months of acceptance. In E-mail: [email protected] view of the importance of color patterns in iden - tification and ethology, authors are encouraged to submit color illustrations in addition to descriptions of Scientific Editor: coloration. It is our aim to provide the international sci - entific community with an efficiently published journal Friedhelm Krupp meeting high scientific and technical standards. Curator of Fishes Senckenberg Research Institute and Natural History Museum Call for papers Senckenberganlage 25 The editors welcome the submission of original manu - 60325 Frankfurt am Main, Germany scripts which should be sent in digital format to the scien - Tel: +49-69-7542.255 tific editor. Full length research papers and short notes will Fax: +49-69-7542.253 be considered for publication. There are no page charges E-mail: [email protected] and color illustrations will be published free of charge. Authors will receive one free copy of the issue in which their paper is published and an e-print in PDF format. Editorial Board: Subscription Notice Gerald R. Allen At least one volume (4 issues) of aqua is being published Department of Aquatic , per year, each issue comprising 48 pages (including cover). Western Australian Museum, Perth, Australia The subscription rate (for one volume = 4 issues) is from volume 12 on: Personal subscription: Euro 75,00 Nina G. Bogutskaya (incl. priority mail); Institutional subscription: Euro 140,00 Zoological Institute of the Russian Academy of (incl. priority mail) . Subscription enquires should be sent Sciences, St. Petersburg, Russia to the publisher at the address given below or by e-mail to: [email protected] Wilson J. E. M. Costa Laboratório de Ictiologia Geral e Aplicada, aqua binder Departamento de Zoologia, Binders for Volumes of aqua are available at cost price Universidade Federal do Rio de Janeiro, Brasil Euro 12,50 (US$ 15.00) plus postage Euro 8,00 (US$ 10.00). Notice: aqua Volumes 1(1)-5(4) = 1st. binder; Axel Meyer Volumes 6(1)-9(4) = 2nd. binder; Volumes 10(1)-13(4) Lehrstuhl für Zoologie und Evolutionsbiologie, = 3rd. binder. Universität Konstanz, Germany Special Publication Paolo Parenti Since 2003 Aquapress publishes a series of Special Publi - Department of Enviromental Sciences, cations, which are produced at irregular intervals. All Spe - University of Milano-Bicocca, cial Publications have about 100 or more pages and are Milan, Italy available separately from regular issues of aqua . Enquiries about subscriptions and prices should be sent to the pub - Mário de Pinna lisher at the address given here above or by e-mail to: Museu de Zoologia da USP, São Paulo, Brazil [email protected] John E. Randall Bishop Museum, Honolulu, Hawaii, U.S.A. ISSN 0945-9871 Publisher: Aquapress, Redazione aqua, Richard Winterbottom I-27010 Miradolo Terme (Pavia), Italy Centre of Biodiversity & Conservation Biology, Printer: SATE s.r.l. (Bergamo), Italy Royal Ontario Museum, Copyediting and layout: Rossella Bulla Toronto, Canada © 2006 aqua , International Journal of Ichthyology aqua, International Journal of Ichthyology

Burrow distribution and diel behavior of the fish Pholidichthys leucotaenia (Pholidichthyidae)

Eugenie Clark 1, Stephen N. Kogge 2, Diane R. Nelson 3, Thomas K. Alburn 4 and John F. Pohle 5

1) Department of Biology, University of Maryland, College Park, MD 20742-4415, U.S.A. Present address: Mote Marine Laboratory, Sarasota, FL 34236, U.S.A. E mail: [email protected] 2) 10600 Stoneyhill Ct., Silver Spring, MD 20901, U.S.A. 3) Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37614-1710, U.S.A. 4) 1488 Klines Run Rd., Wrightsville, PA 17368, U.S.A. 5) 61 Chinquapin Ave., Carlsbad, CA 92008, U.S.A.

Received: 28 August 06 – Accepted: 30 November 06

Abstract chsenen Tiere (bis 57 cm TL = Gesamtlänge) vor den We studied the behavior of adult and juvenile Pholidichthys Eingängen zu ihren Höhlen aufzuzeichnen. Mit Hilfe von leucotaenia on coral reefs in three areas of its range: the Solo - speziellen Video-Endoskopen konnten wir auch Einblick in mon (Russell and Florida Islands), Papua New Gui - das Innere der Höhlen gewinnen. Die Larven im Dotter - nea (Milne Bay Province), and Borneo, (Mabul, sackstadium (6-7 mm TL) und die Jungtiere, die sich von , and Sipadan). Using remote video for periods up to Plankton ernähren (7-11 mm), leben ortsgebunden. In der 55 h, we monitored diel behavior of adults (to 57 cm TL) at Morgendämmerung kamen die jungen Tiere in Schwärmen their burrow entrances. A customized miniature underwater zu Dutzenden bis Tausenden aus den Höhlen heraus. Die video endoscope enabled us to view inside the burrows. Larvenschwärme blieben in der Nähe der Eingänge, während Yolk-sac stage larvae (6-7 mm TL) and planktivorous juveni - die Jungfische ausschwärmten, um Plankton zu erbeuten. les (7-11 mm TL) are site-attached. At dawn young emerged Die jungen Tiere ähneln den sympatrischen giftigen Welsen from their burrows in swarms of dozens to thousands. Larval lineatus (Plotosidae) nach Erscheinungsbild und swarms stayed close to their burrow entrance, but swarms of unverwechselbarem Schwarmverhalten. Tagsüber reinigten juveniles swam away to feed on plankton. Juveniles resemble und pflegten die erwachsenen Pholidichthys leucotaenia ihre the sympatric, venomous , Plotosus lineatus (Plotosi - Höhlen, indem sie Sand und Korallenbruchstücke vor den dae), in appearance and unique swarming behavior. During Ausgang brachten und dort ausspuckten. In der Abenddäm - the day, adult Pholidichthys leucotaenia excavated and cleaned merung zogen sich die Larven und Jungfische zusammen mit their burrows by spitting out sand and rubble at the entrance. zwei, drei Erwachsenen in ihre Höhle zurück. Nachts kamen At dusk larvae and juveniles retired into their home burrows sie nie heraus. Die Larven und Jungtiere hingen in Trauben with two or three adults. None emerged from burrows at von der Decke herab, angeheftet mit einem Schleimsekret, night. Clusters of larvae or juveniles hung from the burrow das sie aus Kopfdrüsen ausscheiden; sie wurden von den ceiling by mucus secreted from glands on their heads and erwachsenen Tieren oft ins Maul aufgenommen, blieben often were scooped into mouths of adults and then released dabei aber offenbar unverletzt. Die Ernährungsgrundlage der apparently unharmed. The food source of adult P. leucotaenia erwachsenen P. leucotaenia ist nach wie vor unbekannt. Eine remains unknown. An undescribed galeommatid bivalve unbeschriebene Muschelart der Galeommatidae lebt in den lives in the fish’s burrows but apparently is not their food Höhlen, dient aber offensichtlich nicht als Nahrung. Die source. Our specimens raised at Mote Marine Laboratory on Exemplare, die wir im Labor (im Mote Marine Laboratory) standard fish food showed strong asymmetry in color pat - mit Standardfischfutter aufgezogen haben, zeigten während terns during development to the adult stage. ihrer Entwicklung zum erwachsenen Tier starke Unre - gelmäßigkeiten bei den Farbmustern. Zusammenfassung Wir untersuchten das Verhalten von Pholidichthys leucotae - Résumé nia verschiedener Altersstufen über Korallenriffen in drei Nous avons étudié le comportement de Pholidichthys leu - Gebieten ihres Vorkommens: Salomon-Inseln (Inseln Russell cotaenia adultes et juvéniles sur des récifs de corail, dans sa und Florida), Papua-Neuguinea (Provinz Milne Bay) und zone de distribution: les îles Salomon (les îles Russell et Flo - Borneo, Malaysia (Mabul, Kapalai und Sipadan). Dabei rida), la Papouasie-Nouvelle-Guinée (province de Milne verwendeten wir ferngesteuerte Videokameras mit Aufnah - Bay), Bornéo et la Malaisie (Mabul, Kapalai et Sipadan). En mezeiten von bis zu 55 Stunden, um das Verhalten der erwa - faisant usage d’une vidéo télécommandée sur des durées de

45 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the fish Pholidichthys leucotaenia (Pholidichthyidae)

55 H, nous avons observé le comportement alimentaire d’a - cibo. Gli esemplari allevati al Mote Marine Laboratory con dultes (jusqu’à 57 cm de LT), à l’entrée de leurs abris. Une cibo standard per pesci mostravano una forte asimmetria vidéo endoscope sous-marine, miniaturisée sur mesure, nous nella colorazione durante lo sviluppo nello stadio adulto. a permis de voir l’intérieur de leurs abris. Des alevins au stade du sac vitellin (6-7 mm LT) et des juvéniles mangeurs de INTRODUCTION plancton (7-11 mm LT) restent fixés dans leur site. Au cré - The behavior, size, and habitat of adult Pholidi - pucule, les jeunes sortent de leurs abris en bancs de douzai - nes à des milliers. Les bancs d’alevins au stade larvaire restent chthys leucotaenia Bleeker, 1856 in nature were près de l’entrée de leur abri, mais les groupes de juvéniles s’é - undescribed prior to our field studies. Juvenile P. loignent pour la chasse au plancton. Les juvéniles ressem - leucotaenia have long been popular in the aquarium blent au poisson-chat venimeux, sympatrique, Plotosus linea - trade, but the species has received little attention by tus (Plotosidae) pour leur aspect et leur comportement uni - field researchers. Since 1990, our diving teams have que en banc. Pendant le jour, les Pholidichthys leucotaenia been studying the behavior of several genera of coral adultes creusaient et nettoyaient l’entrée de leurs abris en sand fish; Malacanthus and (Mala - déplaçant le sable et le gravier à la bouche. Au soir, les alevins canthidae) , Trichonotus (Trichinotidae) , larvaires et les juvéniles se retirent dans leur habitation, en compagnie de deux ou trois adultes. Aucun d’entre eux n’en (Labridae), and Canthidermis (Balistidae) in the sort la nuit. Des grappes de larves ou de juvéniles pendent à Solomon Islands (SOL) and Papua New Guinea la voute de l’abri à l’aide de mucus sécrété par des glandes sur (PNG) (Clark & Pohle 1992, 1996; Clark & Pet - leurs têtes et étaient souvent observés dans la bouche d’adul - zold 1998; Clark et al. 1998). During these studies, tes, et alors apparemment intacts. Les sources de nourriture we came across swarms of juvenile P. leucotaenia and des P. leucotaenia adultes restent ignorées. Un bivalve galéom - discovered the entrances to tunnels in coral reefs matide vit dans l’abri du poisson, mais ne semble pas consti - where they spent the night with their cryptic adults tuer leur source d’alimentation. Nos spécimens élevés au (Anon. 2003, Kaufmann 2005). In this paper, we Mote Marine Laboratory, sur base de nourritures standards, report our findings on the distribution of burrows montraient une forte asymétrie dans les patrons de coloration pendant la croissance vers le stade adulte. and the diel activity of juvenile and adult P. leucotae - nia in SOL, PNG, and northeast Borneo, Malaysia. Sommario The family Pholidichthyidae consists of two È stato studiato il comportamento di adulti e giovani di known allopatric species restricted to the tropical Pholidichthys leucotaenia in ambiente di barriera corallina in Indo-western Pacific. Pholidichthys anguis Springer tre aree di distribuzione: le Isole Salomone (Isole Russell e & Larson, 1996 is known only from northern Florida), Papua Nuova Guinea (Provincia di Milne Bay) e Australia from specimens collected in coastal trawl Borneo, Malaysia (Mabul, Kapalai e Sipadan). Utilizzando hauls made over mud substrates (19-70 m depth) dispositivi video remoti per periodi fino a 55 h, è stato moni - not associated with coral reefs (Springer & Larson torato il comportamento diurno di adulti (fino a 57 cm TL) all’ingresso dei loro rifugio. Un endoscopio miniaturizzato e 1996). Pholidichthys leucotaenia was first described adattato all’utilizzo in ambiente subacqueo ci ha permesso di by Bleeker (1856) and is found in coral reefs in the visualizzare l’interno dei rifugi. È stato osservato che gli stadi , southeast to SOL, and west through larvali con sacco vitellino (6-7 mm TL) e gli stadi giovanili PNG and to Borneo. A reported third planctivori (7-11 mm TL) sono sito-dipendenti. All’alba, species, Pholidichthys anguilliformis Lockington, larve e giovani emergono dai rifugi in sciami di migliaia di 1881, has been designated invalid by Hastings & individui. Le larve rimangono in prossimità del rifugio, ma i Springer (2002) as a junior of Pholis ornata giovani si muovono alla ricerca di plancton. Per l’aspetto e (Girard 1854) in the unrelated family Pholidae. per la modalità con cui sciamano i giovani sono molto simili ai pesci gatto velenosi della specie Plotosus lineatus (Plotosi - Pholidichyids are of uncertain position within the dae), con cui sono simpatrici. Durante il giorno, gli adulti di perciform fish group (Springer & Freihofer 1976, Pholidichthys leucotaenia scavano e mantengono pulito il rifu - Springer & Johnson 2004, Springer & Orrell 2004). gio rimuovendo la sabbia e i detriti accumulati all’ingresso. In a detailed anatomical study of P. leucotaenia , All’imbrunire larve e giovani si ritirano nel rifugio in presenza Springer & Freihofer (1976) suggested it shared a di due o tre adulti. Nessun individuo emerge durante la similarity with certain tropical blennioids (suborder notte. Larve o giovani penzolano a grappoli dal soffitto del Blennioidei), although it also showed evidence of rifugio grazie al muco secreto dalle ghiandole presenti sul relationships with certain fishes not related to blen - capo e, spesso, per la loro incolumità, sono raccolti nella nioids such as labroids. The relationship with blen - cavità boccale degli adulti. La fonte di cibo degli adulti di P. leucotaenia rimane sconosciuta. Una specie di bivalve nioids, common in both the scientific literature (De galeommatide non ancora descritto abita i rifugi di questa Beauford & Chapman 1951, Günther 1961, Herre specie, ma apparentemente non rappresenta una fonte di 1951) and popular aquarium magazines was not aqua vol. 12 no. 2 - 2006 46 , Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle supported by DNA studies (of limited 12S and 16S Islands, SOL) at a dive location known as Mirror rRNA sequences) on our samples by James Garey Pond. In a narrow gully between two coral walls, we (pers. comm. 2001). Analysis of the 12S sequences found three BEs at a depth of 8 m, all less than 0.5 indicated that P. leucotaenia may appear within the m apart. We found a second site ca 60 m away in a Labroidei, but the relationship is unclear. Recently, shallow , 2.4 m from front to back, at a depth of a cladistic analysis based on the dorsal gill-arch 7.3 m. The head (ca 3 cm diameter) of an adult was musculature and skeletal characters of teleostome observed spitting out white sand from the BE. fishes indicated that the Labroidei are polyphyletic About 6 m outside this cave, we found a third site without the inclusion of the Pholidichthyidae with one BE under a coral head. In each case, there (Springer & Orrell 2004). More molecular and was a conspicuous area of white sand forming an morphological studies involving Pholidichthys and “apron” that spread about 30 cm from each BE. additional labroids and non-labroids are needed to Study sites: From 1996 to 2004, we dived in three discern the phylogenetic position of the Pholidi - areas of the Indo-Pacific, including the most eastern chthyidae (Springer & Johnson 2004). (SOL) and most western (Borneo) geographic ran - Schultz (1966) considered juvenile P. leucotaenia to ges for P. leucotaenia (Fig. 1, Table I). In central be related to gobies. Since the 1970s, juveniles of P. southwestern SOL, we studied 13 areas from the leucotaenia have been imported in the aquarium eastern New Georgia Islands to the northern coast of trade from the Philippine Islands and most often Guadalcanal (Fig. 1c, Table I c) with most of our referred to as a blenny (Brittan 1972) but sold under observations and mapping of burrows at Tanavula many common names such as “engineer fish”, “con - (Fig. 2b) in the Florida Islands and Mane in vict blenny”, “leopard blenny”, “Pacific neon goby”, the Russell Islands. In Milne Bay Province in “convict worm goby”, and “false catfish”. These southeastern PNG, we studied 11 areas (Fig. 1b, names refer to their pebble-moving and construc - Table I b), concentrating on Kwato (Fig. 2a), Obser - tion activities; the spots, stripes, blotches, and/or vation Point, Samarai, and Dale’s Reef. vertical bands on transitional pattern phases from We also surveyed three small islands (Fig.1a, Table I juvenile to adult; the juveniles’ resemblance to the a) off northeastern Borneo, Malaysia: Mabul, Kapa - Atlantic neon goby (Gobiosoma oceanops) or the lai, and Sipadan. worm gobies (microdesmids); and the strong resem - Underwater observations (5,592 h): In SOL blance in swarming behavior and appearance of the during 1997 (27 April to 8 May), 1998 (3 to 20 young to the sympatric venomous catfish, Plotosus April), and 1999 (4 to 11 April), we chartered the lineatus. The proper common name should be “con - live-aboard , Bilikiki , which served as our vict fish” (Springer 2001, Kaufmann 2005). research base from which our SCUBA divers (54) Abbreviations: BE: burrow entrance; GPS: Global spent a total of 1,931 h underwater. In PNG during Positioning System; LED: Light-emitting diode; 2000 (1 October to 1 November), 2001 (28 May PNG: Papua New Guinea; SOL: Solomon Islands; to 16 June), 2002 (25 April to 25 May), 2003 (8 TL: Total length; USNM: Division of Fishes, U. S. May to 8 Junne), and 2004 (7 May to 7 June), 48 National Museum of Natural History, formerly U. divers spent 3,244 h underwater making observa - S. National Museum. tions from the live-aboard dive boats, Golden Dawn Preliminary observations (1996-1997): In 1996 at and Telita . In Borneo, during 2001 (10 to 23 Sep - a coral reef at Observation Point, PNG, we first tember) and 2003 (8 to 24 August), we stayed at the observed and videoed a group of ca 20 large (ca 9 cm land-based dive resort, “Sipadan Water Village”, and TL) juvenile P. leucotaenia . took day boats to research sites, where 17 divers They were carrying pebbles and shell fragments out spent 417 h underwater. The unavailability of a of a burrow entrance (BE) in water ca 10 m deep. In live-aboard dive boat in Borneo limited our survey 1997, we saw the head of a large eel-like fish in a BE time, especially night dives, around these islands. with several juvenile P. leucotaenia. The head looked Tidal ranges were slight, under 1 m, and the varia - so unlike the juveniles’ that we thought we were bility in daily photoperiod length was considered observing a symbiotic relationship until further negligible for our study because of the proximity of observations revealed that they were the same spe - study sites to the equator. cies. Location and mapping of adult BEs: At dusk we In April 1997, we found five BEs of adult P. leuco - found the entrances to adult burrows by following taenia on the northeast side of Mane Island (Russell swarms of juveniles when they retired into their tun -

47 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae) nels for the night (Fig. 3a). During the day we often all owing the use of either video system there. found BEs by looking for the white sand “aprons” The black-and-white video camera was switched to (Fig. 3a). Divers mapped study sites using compass the image-intensified night-vision video camera that points and measuring tapes up to 30 m long, and was turned on at sunset and off at sunrise by a diver. many of the BEs were marked with a string attached A 4-watt Ikelite fluorescent , located ca 1 to a float at the surface where Global Positioning m from the burrow, provided sufficient light for the System (GPS) readings were taken by an observer in “starlight” camera to work during overcast nights. a small boat. Rare disruptions to continuous viewing occurred Juvenile swarms: Divers recorded behaviors of juve - when the video cable broke or when the boat had to niles on underwater slates or with video cameras move. After 2001, with technical improvements, we from before dawn (Fig. 3b) until after dusk. The size were able to record in color without a cable to the and number of individuals in a swarm (Figs. 4 and ship. 5a), depths and distribution of swarms on the reef, Watching the monitor onboard the ship, teams of and “wake-up times” and “bedtimes” were determi - two observers, working in 2-h shifts, recorded acti - ned during these observations. Wake-up and bedti - vity of P. leucotaenia at the BE in 1-min intervals. mes of juveniles were compared with sunrise and Observations that were tabulated and graphed inclu - sunset times calculated using a Garmin 75 GPS unit. ded: appearance of the adult, duration (sec) the “Wake-up time” was designated as the range of time adult was visible, how far the adult came out (as around sunrise from the emergence of the first juve - measured by the number of body “rings” visible), nile until the last of the swarm left the burrow with and the adult spitting out sand or moving rubble. only a few stragglers remaining. “Bedtime” was defi - We transcribed observations from seven recordings ned as the time interval around sunset from the first (90.7 h) at Mane, Tanavula, and Fonagho, SOL, to to almost the last individual of the swarm entering a PostgreSQL database for analysis, and grouped the the burrow. Swarm counts of juveniles were estima - data by 20-min intervals for graphing purposes. ted by divers in situ or more precisely by replaying In PNG we recorded inside the BE with a minia - the video in slow motion for five to seven persons ture video endoscope (“Burrow Cam”), assembled who counted the numbers of juveniles entering the by one of us (SNK) using a 6-mm diameter video BE. The highest and lowest counts were discarded, camera with a flexible 2-m long signal cable, contai - and the other estimates were averaged. ned in a custom housing with a light-emitting diode Video recordings: Divers used several types of (LED) illuminator. The self-illuminated video video cameras in underwater housings to record camera housing with a diameter of 2.5 cm and a 2 behaviors of adults and juveniles. For short unman - m long clear plastic tube connected the camera to ned runs (ca 2 h), a diver positioned a video cam - the electronics. A second housing contained the corder in an underwater housing held in place by a power supply for the camera, a small video monitor belt 1 to 2 m from the BE. turned used on site, and connectors to feed the video to the on the camera, left the site, and later retrieved the surface for recording and viewing through a moni - camera. Onboard the ship, we transcribed data tor onboard ship. This apparatus was flexible from the 2-h videotape played through a monitor. enough to maneuver into some burrows and allowed We made continuous live video camera observa - us to observe inhabitants up to 1 m inside. The Bur - tions of BEs (the longest of which was 55 h) using row Cam did not block juveniles’ access to the bur - one of two custom-designed systems: a low-light row, thus we were able to observe adults and juveni - black-and-white video camera from dawn to dusk les inside a burrow for entire nights albeit under the and then an ITT Image-Intensifier (“starlight”) artificial conditions of light from our endoscope. video camera at night. Before deploying these Collection of sand “aprons”: Quantitative estima - cameras, we stabilized the ship with stern and bow tes of bioerosion due to burrowing activities of adult anchors. Divers positioned the camera on a tripod P. leucotaenia were made by laying a collection cloth in front of a BE and deployed the video cable from outside the BE. After a specific amount of time (2- the camera to the ship along a stern anchor rope to 24 h), the sand spit onto the cloth by adults was keep the cable off the reef. The video cable was con - removed, dried, and weighed. nected to a monitor on the ship (Figs. 6a, b, and c). Collection and sizes of juveniles for P. leucotaenia The deep water close to shore at Tanavula, SOL, growth rates: Divers collected juveniles from a spe - prevented the ship from anchoring, thus not cific swarm near their BE by steering them into aqua vol. 12 no. 2 - 2006 48 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

a Fig. 1a-c. Dive sites surveyed for Pholidichthys leuco - taenia in the southwestern Pacific. All sites had thou - sands of juveniles and many adults except the islands of Sipadan (Borneo) and Mary (Solomons) isolated by deep water: (a) Islands of Mabul, Kapalai and Sipadan off NE Borneo; (b) coastal regions in Milne Bay Province, Papua New Guinea; (c) Solomon Islands. b

c

49 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

Table I. Latitude and longitude for sites surveyed for Pholidichthys leucotaenia in: a) Borneo, b) Papua New Guinea and c) Solomon Islands 1997-2004. Except for Sipidan and Mary Island, all sites had swarms of juvenile P. leucotaenia .

Country Map # Site Location Latitude Longitude (Fig. 1)

a – Borneo, Malaysia (Estimates from Maps) 1 Mabul 04° 14’ N 118° 37’ E 2 Kapalai 04° 13’ N 118° 37’ E 3 Sipadan* 04° 06’ N 118° 41’ E

b – Milne Bay Province, Papua New Guinea 1 Observation Point 09° 44.0’ S 150° 44.4’ E (GPS Readings) 2 Dale’s Reef 10° 15.8’ S 150° 43.5’ E 3 Cobb’s Cliff 10° 12.7’ S 150° 53.6’ E 4 Banana Bommie 10° 14.3’ S 150° 54.8’ E 5 Nuakata Island 10° 15.7’ S 151° 00.1’ E 6 Boirama Island 10° 17.0’ S 151° 02.8’ E 7 China Reef 10° 31.9’ S 150° 44.6’ E 8 Ito Reef 10° 34.3’ S 150° 44.7’ E 9 Sawasawaga 10° 37.4’ S 150° 45.4’ E 10 Samarai Wharf 10° 36.5’ S 150° 40.0’ E 11 Kwato Island 10° 36.9’ S 150° 38.0’ E c – Solomon Islands (GPS Readings) 1 Kokoana Passage 08° 30.5’ S 158° 09.4’ E New Georgia Group 2 Karanjou-Lionfish Point 08° 36.7’ S 158° 12.0’ E 3 Minjanga Island 08° 42.8’ S 158° 13.4’ E (Cave & Anemone Points) 08° 45.6’ S 158° 16.2’ E 4 Mbuolo Island (Lagoon Point) 5 Male Male Island 08° 47.1’ S 158° 15.1’ E Mborokua 6 Mary Island* 09° 01.1’ S 158° 43.9’ E Russell Islands 7 Mane Island (Pinnacle) 09° 01.4’ S 159° 02.6’ E Mane Island (Mirror Pond & East Point) 09° 02.6’ S 159° 05.5’ E Mane Island (St Mary’s Bay) 09° 01.3’ S 159° 02.2’ E 8 Karumolun Island 08° 58.6’ S 159° 06.9’ E 9 Samsaeon Island 08° 58.0’ S 159° 12.7’ E 10 Kaukau Island 09° 01.8’ S 159° 16.6’ E 11 Fonagho Island 09° 05.6’ S 159° 17.7’ E Florida Islands 12 Tanavula** 09° 02.5’ S 160° 04.1’ E Guadalcanal 13 Hirakawa Maru 09° 22.9’ S 159° 52.6’ E

* P. leucotaenia not found. ** Ranges from Tanavula Point (09° 02 37.4’ S, 160° 03 41.3’ E) to East Tabosi Island (09° 02 28.0 S, 160°04 25.8’ E) hand nets or plastic bags (Fig. 7). Onboard the dive ves living inside the P. leucotaenia burrows were col - boat they were placed into an aquarium. Each was lected with an improvised mini airlift (to suck them removed briefly to a glass plate where the total out of the burrows), constructed by one of us (SNK) length (TL) was measured using an electronic digi - with two 1-liter water bottles cut at the bottoms and tal caliper. They were then transferred to another joined with a fine mesh net in between, a 2.5-cm aquarium and returned by divers to their specific diameter corrugated plastic tube attached to each of swarm by the next day. After one to four weeks, the bottle necks, and an air tube connected to the these swarms were sampled again to estimate top bottle. growth. Juveniles were collected also incidentally Collection of adult specimens of P. leucotaenia: from inside the tunnels when we were collecting We collected and preserved six adults: three males symbiotic bivalves. and three females, one from SOL and five from Collection of symbiotic bivalves: Symbiotic bival - PNG (Table III). The first specimen, a female, was aqua vol. 12 no. 2 - 2006 50 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle caught with a small hook and line lowered into the in 10 % formalin and later transferred to 70 % ethyl BE and pulled directly into a large net bag that faci - alcohol. Some juveniles and a portion of muscle litated carrying the large, slippery, mucous covered from an adult were preserved in 95 % ethyl alcohol specimen to the surface. Additional specimens were for DNA analyses. collected with a small three-pronged spear when the The first specimen, collected in Tanavula, SOL, head of the fish appeared at the BE. These were also was deposited at the Smithsonian Institution in the transported in a net bag. Specimens were preserved Division of Fishes (USNM 348992). Two additional

2.7 m

7.6 m 3.0 m

14.9 m

a



b

Fig. 2a-b . Locations of burrow entrances (BE) for Pholidichthys leucotaenia: (a) nine BEs near dock on south side of Kwato Island, Papua New Guinea. Heavy circles around seven burrows indicate multiple year sightings, thin circles indicate single sighting (not present in other years); (b) Twenty-one burrow entrances along coast of Tanavula (Florida Islands), Solomon Islands. Scale in meters.

51 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

Table II. Depths of 21 burrow entrances (1.5 to 14.9 m) and, when noted, wake-up and bedtimes of juveniles in associated swarms at Tanavula, SOL, 1999 (see Fig. 2b).

BE # Depth (m) Juvenile Swarms Wake-up Sunrise Bedtime Sunset Number Size (cm)

1 16,5 500+ – – 06:22 – 18:19 2 9,1 2000-4000 1 ? To -8 06:22 – – 3 14,3 2000+200 3 ? To -2 06:22 – – 4 12,8 1000+ – – - – – 5 6,1 200+ 4 – 06:22 -6 to ? 18:21 6 11,9 500+ – ? to +12 - all in at 17:29 – 7 9,1 500+ 4 cm +8 to +23 06:22 - – 8 3,4 500-700 03. Feb 0 to +4 06:22 -21 to -17 18:22 9 3,4 500-700 03. Feb 0 to +4 06:22 -4 to+4 18:19 9 7,6 400 2.5 - 3.0 cm -3 to +12 06:22 -27 to +1 18:18 10 13,1 1000+ 2 @ 81-86’ – – – - 11 13,1 1500+ 3 -11 to 0 06:22 -12 to +8 18:18 12 11,6 600 3 -13 to +7 06:22 -20 to -13 18:19 13 7,6 1500+ 2 -11 to -5 06:22 -12 to +8 18:16 14 6,7 – – – – – – 15 1,5 – – – – – – 16 7,3 3000+ 1-2 -12 to -6 06:22 -9 to +6 18:19 17 12,5 – – – – – – 18 14,9 – – – – – – 19 10,7 1000+ 1-2 – – – – 20 12,2 – – – – – – 21 9,5 – –- –– –– specimens (Table III) collected from PNG were rium dealer, Seagrest Farms, Inc., in Ruskin, Florida, donated to the Florida State Museum. The remai - who is regularly supplied from the Philippines. We ning three specimens from PNG are at Mote Marine documented the pattern development of aquarium Laboratory (Eugenie Clark collection). juveniles raised to adults over a four-year period. Estimation of burrow size, configuration, and number of entrances: In order to determine if nearby Results BEs were connected, we injected concentrated beet Burrows: We compiled information on burrows of juice into the highest BE on the reef and noted the P. leucotaenia at depths of 1.2 to 17.7 m: 32 in SOL, other BEs where the vegetable dye came out. We 31 in PNG, and seven in Borneo. We found the measured a straight line across the surface of the sub - highest at Kwato, PNG (Fig. 2a) and strate between each of the connected BEs to obtain a Tanavula, SOL (Fig. 2b). At Tanavula we located 21 minimum estimation of the length of the tunnels. In BEs at depths of 1.5 to 16.5 m along a fringing reef an attempt to determine the actual configuration of extending 1100 m from the east side of Tabosi the labyrinthine tunnels between the BEs, we filled Island to Tanavula Point (Table II). At Kwato we one of the larger tunnel systems with uncooked rice, studied tunnel complexes, each with 1 to 4 entran - hoping it would set and allow us to excavate a mold ces, at depths of 1.2 to 14.9 m along a 150-m coas- of the tunnels. However, the adults inside very acti - tal reef (Fig. 2b, Table III). vely spit the rice out, undermining this attempt. Burrow entrances (BEs): BEs were approximately Color patterns observed in the field and in aqua - circular or ovoid with a diameter of 4 to 8 cm (rarely ria: Color patterns of larvae, juveniles and adults 10 cm). Entrances usually had 20 to more than 100 observed in the field were documented by video and pieces of coral rubble interlaced around the rim that photographs at study sites and from specimens col - hindered the collapse of the BE. The shape and size lected. In addition, we set up a series of aquaria (190, of the BE often changed when sand washed back 380, 1140 liters) at Mote Marine Laboratory, with into the tunnels due to physical disturbances, e.g. tunnel systems and mirrors, monitored by conti - modifications by adults, movements of other orga - nuous video. These fish were obtained from an aqua - nisms, or currents. Sometimes the BEs were almost aqua vol. 12 no. 2 - 2006 52 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle completely obstructed (with shell, rubble, and/or BEs connected in a system, the estimated two- sand), changed location, or disappeared, but they dimensional surface area between these BEs is an usually remained discernable for weeks and someti - artificially low measurement of the actual three- mes were in the same spot a year later. dimensional winding and branching tunnel com - Sand “aprons”: Adult P. leucotaenia formed sand plex since the total tunnel length is probably at least “aprons” as they spat out large quantities of sand twice as long as our measurements of the straight- (Fig. 3) while excavating their tunnels and removing line distances between the three BEs. sand that washed back in. Depending on shape and Undescribed bivalve: With the Burrow Cam, we slope of the substrate below the BE, the size of the found and videotaped over 40 specimens of an uni - sand “apron” varied from 0.5 to 3 m in width. In dentified small bivalve mollusk (10-15 mm TL; Fig. two cases, the steep slope of the reef (Observation 8) living symbiotically with P. leucotaenia in the first Point and Sawasawaga S-1) resulted in a highly con - two meters of most burrows in PNG. (The endo - spicuous sand “apron” about 1 m wide, cascading to scope was unavailable for our studies in SOL and over 3 m downslope. In four trials at one BE in Borneo.) In the light of the LED illuminator, the SOL, the dry weight of sand deposited on the sand amorphous shape of the bivalve appeared to be pale “apron” in a 3-h period during the day ranged from blue. Each was seen hanging by a thin appendage 730 to 850 g (mean = 795 g; S.D. = 55.1 g). Since from the ceiling of the burrow or crawling along the the adults actively spat out sand from dawn to dusk tunnel close to, but ignored by adult and juvenile (12 h), the mean amount of sand spat out was cal - fish. One of these bivalves attached itself to the culated to be ca 3.2 kg per day. Occasionally we camera cable and was collected, photographed alive observed larger juveniles (8-11 cm TL) also spitting (Fig. 8), and preserved in alcohol. We could see the sand and removing shells. small shell and larvae inside the translucent body. Burrow interiors: We inserted the Burrow Cam We sent this preserved specimen to Paula Mikkel - into 18 BEs in PNG. Just inside a BE, we typically sen, Curator of Malacology at the American found a large chamber with two or three side tunnels Museum of Natural History in New York, who con - which we estimated were at least 1 m and some pro - firmed it as a bivalve that was brooding thousands of bably over 4 m long. The chamber of one BE had larvae in its gills. She plans to describe it (P. Mikkel - two openings on opposite walls from which two dif - sen pers. comm. 2002) as a new species of bivalve ferent adults, spitting out sand and rubble, took mollusk belonging to the family Galeommatidae turns every three to 10 spits as they repaired and par - (Mikkelsen & Bieler 1989, 1992). We collected an tially closed the BE that we had widened for a better additional 15 specimens from a single tunnel system view. The sand “aprons” outside these BEs had two at Kwato with a mini airlift. We were able to keep peaks formed from the two adults alternately spitting some of these alive in an aquarium. in opposite directions. In another burrow, we found Diel behavior of adults: At the BE, adult P. leuco - three side tunnels off the inner chamber and identi - taenia showed much activity during the day and no fied a separate adult in each tunnel. In SOL, we mea - activity at night (Figs. 9a and b). The beginning and sured a cave-like chamber just inside the BE that was ending of adults’ activity coincides closely with the 9 to 12 cm wide, slightly less than 8 to 10 cm high, “wake-up times” and “bedtimes” of juveniles, respec - and ca 7 cm deep. Three tunnels with diameters of 3 tively. to 5 cm opened from this chamber. Based on differences in head markings, we could We found burrows with a single conspicuous BE identify one to three adults per BE taking turns clea - and sand “apron”, an inner chamber, and multiple ning out their burrow. Adults appeared at their BE tunnels. Other burrow complexes had as many as from zero to six times per minute from dawn to three BEs: one or two major ones each actively dusk. The number of seconds that the head appea - maintained with sand “aprons” and a third incon - red at the BE varied from about one to six. Usually spicuous one. In PNG, using beet juice at Dale’s just the head of the adult emerged or the head was Reef (Table I) and at Kwato (Fig. 2a), we recorded barely seen at the entrance (Figs. 10a, b, and c). tunnel systems with three BEs each. The three BEs Occasionally an adult stuck its head out of the BE of Kwato were 2 to 3 m apart, all of which opened without spitting (Figs. 6c and 10b). When the head into the same labyrinthine tunnel system under - protruded, we counted the number of dark irregular neath a surface area of ca 9 m 2. With multiple tun - rings on the head and body; the maximum number nels heading in different directions and multiple recorded was five (Fig. 10a). Once, an individual of

53 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

a

b

Fig. 3a-b. Bedtime and wake up time of Pholidichthys leucotaenia: (a) A swarm of thousands of juvenile Pholidichthys leuco - taenia (each ca 5 cm TL) streaming into their home burrow near sunset from a distant feeding area over 30 m away. White sand “apron” spreads from burrow entrance formed by the cryptic adults during daytime cleaning activity. Depth about 10 m. Observation Point, Papua New Guinea. Photo by , 2000; (b) Swarm of juvenile Pholidichthys leucotaenia emerging from their burrow at dawn. Depth about 8 m. Kwato, Papua New Guinea. Photo by Dinah Halstead, 2003. aqua vol. 12 no. 2 - 2006 54 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

Table III. Six adult Pholidichthys leucotaenia collected in Solomon Islands and Papua New Guinea 1998-2003.

1 2 3 4 5 6 Collection # USNM EC PNG #2 EC PNG #3 EC PNG#4 UF #159377 UF #159378 #348992 Collector T. Alburn B. Halstead B. Halstead B. Halstead B. Halstead B. Halstead Date 20 Apr 1998 26 Oct 2000 22 May 2002 20 May 2003 25 May 2003 5 Jun 2003 Time ~16:00 16:45 8:10 ~16:00 16:58 17:03 Location Tanavula, Dale’s Reef, Sawasawaga, Samarai, Samarai, Kwato SOL PNG PNG PNG PNG PNG, K-2 Depth ~8 m ~3 m ~12 m ~7 m ~5 m 1.2 m Sex Female Female Male Male Male Female No UG No UG Pink UG No UG No UG No UG Papilla Papilla Papilla Papilla Papilla Papilla Total length 47 cm 53 cm 56.5 cm 37 cm 48 cm 51 cm Gonad Size Both 7.2 cm Left: 5 cm x x 1.1 cm 0.8 cm. Right: 5.25 cm x 0.8 cm. Gonad Contents Thousands Thousands Small of small of tiny pale string-like eggs orange eggs beaded gonad Microscopic Gut Empty Empty Empty except Empty Empty Empty Contents except for for dark except for except for except for dark greenish greenish dark greenish dark greenish dark greenish chyme chyme chyme chyme chyme the smallest pair observed was videoed as it came par - sionally, large swarms of free-swimming juveniles, 9 tly out of its BE, then turned sharply and went back to 11 cm TL, (Fig. 4) stayed near the BE during the in headfirst before the tail came completely out. day. Large swarms separated into two, three, or rarely Although P. leucotaenia tolerated territorial damsel - four sub-swarms when feeding on plankton. During fish near their BE, we recorded them lunging at a strong , juveniles fed higher in the water transient small fish. Based on continuous surveillan - column. At slack , they stayed closer to the sub - ces over 24-h periods (with an endoscope as well as strate often near their BE where larger individuals (9- standard video and low light video cameras), neither 11 cm TL) cleaned out their burrows or simply tos - adults nor juveniles emerged from their burrow at sed around small amounts of sand and pieces of rub - night. We never observed adults feeding naturally, ble (Fig. 4, insert). Sometimes several juveniles went but we induced one individual to take a small piece in and out of the BE, undisturbed by the appearance of raw fish we left at the BE. of or contact with an adult’s head (Fig. 11), even Diel behavior of larvae and juveniles: We observed when an adult took several juveniles into its mouth over 120 swarms, each with hundreds to many thou - and released them seconds later. Some juveniles sands of larvae (0.7-1.2 cm TL) or juveniles (1.2- stayed deep in the burrow during the day, verified 11.0 cm TL). The exception was a swarm of only 25 when we collected juveniles in addition to bivalves juveniles (ca 3 cm TL each), belonging to the smal - with the mini airlift. lest pair of adults (ca 20 cm TL each) we ever obser - Usually the swarms stayed close to the reef, howe - ved. We saw all sizes of larvae and juveniles on each ver, sometimes swarms of many thousands formed expedition when we surveyed the reefs. Swarms were long streams, nearly 1.0 m wide, stretching away found at depths of 2 to 49 m. Swarms of endogenous from the reef and extending more than 20 m into larvae (yolks still visible) stayed close to the BE all open water in long snake-like formations. One such day, but swarms of juveniles fed on plankton in areas swarm at Observation Point (PNG) produced elon - as far as 52 m away from their home burrows. Occa - gated formations, completely leaving the reef to feed

55 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

Fig. 4. Swarm of thousands of juvenile Pholidichthys leucotaenia (9-11 cm TL), staying near and some entering their burrow (lower left) at 7.3 m depth under south side of Samarai Dock, Papua New Guinea. The insert shows a juvenile carrying a pebble. By this size, juveniles start pebble-moving construction activity, after which they make burrows, never swarm again, and are rarely seen. Photo by Dinah Halstead, 2003. aqua vol. 12 no. 2 - 2006 56 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

a

Fig. 5a. Swarms of juvenile Pholidichthys leucotaenia and Plotosus lineatus showing features of swarming (vs. schooling) beha - vior. Although individual fish in swarms are similar in size their orientation to each other, sometimes touching, is different from a school. Pholidichthys and Plotosus are the only marine fish known to form swarms: swarm of a few thousand juvenile P. leucotaenia, of which about 800 are in view, traveling and feeding on plankton under Samarai main dock, Papua New Gui - nea. Photo by Dinah Halstead, 2003.

57 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae) in the open water near the surface. In this unusual ding station every day for the four days we tracked case, divers took turns staying with them until dusk them. At Dale’s Reef we tracked a swarm for five and videoed them returning into a single BE located days that went 52 m away from its BE to feed in in the coral reef at 28 m. shallow water (3 m) on top of a coral head (“Bob’s Swarms changed shape during the day. Elongated Bommie”). On the sixth and seventh days we could swarms of larger juveniles took on ovoid shapes not find them, even though we looked on top of the when they reached their feeding station. At Kwato coral head and all over the sandy and rocky terrain PNG, we studied seven out of nine swarms and their in the area around the coral head. associated BEs (Fig. 2a), each went to their same fee - Large swarms often split into sub-swarms after they

b

Fig. 5b. Swarm of several hundred juvenile Plotosus lineatus in Mabul, Borneo showing close resemblance to swarm of juve - nile Pholidichthys leucotaenia . Barbels are inconspicuous at this distance but three individuals feeding in sand (front bottom of picture), is evidence that they are not the plankton-feeding P. leucotaenia. Photo by Susan Shaw 2003. aqua vol. 12 no. 2 - 2006 58 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle emerged from their BEs at dawn (“wake-up” times), at bedtime. Swarms that fed at depths from 1.8 to but at bedtime merged and went into their BE 32 m were traced to their BEs. The deepest swarm, together. In Tanavula, SOL (Fig. 2b), at BE #8, juve - at 49 m depth, was not traced to a BE. At Samarai niles emerged at dawn and divided into two sub- (PNG), two sub-swarms belonging to one burrow at swarms. More than 200 juveniles stayed at ca 14 m 10 m depth went far apart, more than 8 m, during depth, whereas the larger swarm of more than 2000 the day but converged at dusk and streamed into individuals went to a depth of 23.8 to 32.2 m. At their home BE together. BE #13, juveniles divided into three different sub- When rapidly streaming in or out of the BE, juve - swarms for the day but went back into the same BE niles were so close they appeared to be touching, sli -

c

Fig. 5c. Closer view of swarm of Plotosus lineatus swimming out of an abandoned tire showing the six long chin barbels that clearly distinguishes them from Pholidichthys leucotaenia . Photos b and c by Susan Shaw, Mabul, Borneo, 2003.

59 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

a b

Fig. 6a-f. Study site at Mane Island, Solomon Islands: (a) video cable from study site near shore to monitor on stern of boat; (b) tripod/video camera set-up at burrow entrance of Pholidichthys leucotaenia near coral reefs; (c) Diane Nelson with video camera on tripod, aimed at a burrow entrance with head of adult P. leucotaenia projec - ting from entrance; (d) swarm of juveniles in front of underwater slate (marked off in cm) near their burrow entrance; (e) juvenile, ca 4 cm TL showing luminous false eye and stripe; (f) swarm of juvenile venomous catfish, Plotosus lineatus , feeding in sand. Photos a, b, d, e, and f, by Stephen Kogge, 1998 and c by Ruth Petzold, 1998. d

e

c f

aqua vol. 12 no. 2 - 2006 60 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle ding against each other smoothly. A few juveniles, mucous thread. Within minutes of being exposed to usually at the end of the stream, entered the BE erra - light, most juveniles broke their attachments and tically and more slowly. Often one or two stragglers swam away. stayed out for several minutes after more than 98 % At dawn, the streaming of juveniles from BEs was of the main stream of hundreds or thousands had slightly slower than re-entry streaming at bedtime. entered the burrow. These stragglers (“sentries”) Wake-up times ranged from 23 min before sunrise looked around in all directions for several minutes to 46 min after sunrise. Most of the swarms began before finally entering the BE. Bedtimes averaged emerging shortly before sunrise (Fig. 12). The from 81 min before sunset to 38 min after sunset regression lines for depth versus sunrise and sunset (Fig. 12c). At Tanavula (SOL), eight of the twelve show weak correlation coefficients (R 2 = 0.03, P= observed swarms started entering the burrow prior 0.0301 for wakeup; R2 = 0.19, P=0.1777 for bed - to sunset. time; Fig. 12). At Tanavula (SOL), one of us (DN) During the night, with the Burrow Cam, we recor - observed that juveniles emerging from the BE at ded clumps of juveniles hanging from the ceiling dawn were disturbed by the bright lights of a video and wall crevices of the tunnels (Fig. 13a). Larvae camera and stopped coming out. But after a few and the smallest juveniles (0.8-1.1 cm TL) had four seconds they began streaming out from a hole in the small glands on the dorsal part of the head (Figs 14a, reef system, about 3 m away, with no obvious BE b, and c) that produced mucous threads used for and no sand apron. The videographer (J. Nelson) attachment (first described by Wirtz 1991). The recorded the emergence of the juveniles from the thread was as long as the length of a larva (ca 0.8 cm alternate hole, from a distance, so as not to disturb TL), but the thread became shorter as the juveniles their behavior. grew longer. Juveniles less than 2.0 cm TL attached Stomach contents of adults: The contents of the directly to the ceiling by their heads without a stomach and intestine contained chyme, which, in

Fig. 7 . Tak Konstantinou collecting juvenile Pholidichthys leucotaenia with hand nets. Photo by Stephen Kogge, 2002.

61 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

< byssus < posterior extension of the foot < feces produces the byssus digested microalgae

cowl

shell <

excurrent “siphon”

foot <

< papillae <

< posterior pallial tentacle incurrent “siphon” < mantle 1 cm

< cephallic tentacle a

bc1 cm

Fig 8a-c . New species of galeommatid bivalve living deep in burrows of Pholidichthys leucotaenia. (a) Two bivalves, collected 10 Jan. 2006 from one tunnel system (BE # 9) at Kwato, PNG, hanging on glass by byssus. They are kept alive at Mote Marine Laboratory and fed a mixture of flagellates, diatomes, and green algae. (b) & (c) First specimen collected at Ito 7 May 2002. Small internal shell and larval mass shows through transparent mantle from which foot and tentacles protrude out of cowl opening. Photo (a) by Debi Ingrao Aug. 2006; photos (b) and (c) aboard ship aquarium by Bob Halstead, May 2002. aqua vol. 12 no. 2 - 2006 62 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

a

b

Fig. 9a-b. Diel activity of adult Pholidichthys leucotaenia . Data summarized from 90.6 h of video at 12 burrow entrances at 3 study sites (Mane, Fonagho, and Tanavula) in the Solomon Islands: (a) “All activity” includes behaviors of adults observed at the burrow entrance (BE): spitting sand, moving rubble, and merely the appearance of the head. “Spits” refers only to beha - vior in which adult spits sand out of the burrow. “Seconds Head Visible at BE” is the average number of seconds that an adult appeared at the BE. “Observation Interval” is the number of minutes averaged for each data point; (b) 10 minute histo - gram of number of rings on the anterior part of the fish’s body indicating how far and how often a head is protruded.

63 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

b

a c

Fig. 10a-f. Adult Pholidichthys leucotaenia: (a) head moving an elongated (ca 10 cm) piece of coral rubble at burrow entrance; (b) head looking around, diver’s weight marked in cm; (c) head spitting out sand; (d) dorsal view of first adult captured, female 47 cm TL; deposi - ted in USNM 348922; (e) adult that escaped; (f) authors EC and TA examining female USNM 348922 when just captured in net. d Photos by Stephen Kogge, 1998.

e f

aqua vol. 12 no. 2 - 2006 64 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

a

b

Fig. 11a-b. False luminescent “eyes” of juvenile Pholidichthys leucotaenia: (a) Juveniles, 3-4 cm TL, hovering around the head of an adult at their burrow entrance. The anterior end of their white vertical stripe that extends forward to over the pupil of the eye, forms false luminescent “eyes.” Photo by Stephen Kogge, 1998; (b) Close-up of a juvenile ca 3.5 cm TL showing position of false eye on top of orbit above the pupil. Photo by Yoshi Hirata, Mabul, September 2001.

65 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

Figure 12a. Wakeup observations(33) of juveniles relative to sunrise and depth.

a

Figure 12b. Regression line of depth versus sunrise for juvenile wakeups.

P = 0.0301

b

Fig. 12a-b. Diel activity of juvenile Pholidichthys leucotaenia in relation to their “wake-ups” (times of emergence) from their burrow entrance (BE) and “bedtimes” (times they return into their BE): (a) Wakeup observations relative to sunrise and depth; (b) Regression line of depth versus wakeup time. aqua vol. 12 no. 2 - 2006 66 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

Figure 12c. Bedtime observations(55) of juveniles relative to sunset and depth.

c

Figure 12d. Regression line of depth versus sunset for juvenile bedtimes. e s i r n u s ) + ( r e

t P = 0.1777 f a r o ) - ( e r o f e b s e t u n i M

d

Fig. 12c-d. (c) “Bedtime” observations of juveniles relative to sunset and depth; ( d) Regression line of depth versus sunset for juvenile bedtimes. Regression lines b and d are weak but show trends that could be useful for future research in deeper water.

67 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae) five specimens examined microscopically, contained fusilier, Caesio xanthonotus (Caesionidae). no identifiable organisms except for one spicule of a Distribution of P. leucotaenia: We found P. leuco - tunicate and a few sand grains. The large swim blad - taenia swarms, and often their burrows, in every der in each was filled with gas. The rather flat liver coral reef area we surveyed except around isolated or was 9 cm long by 2.8 cm at its widest point, with a oceanic islands (Fig. 1, Table I). In SOL the excep - round gall bladder, ca 0.9 cm diameter. The male tion was the isolated but popular tourist dive location had a soft, pink urogenital papilla, 2.5 mm diameter of Mborokua (“Mary Island”) (Fig. 1c). In 1999, 17 and 2 mm long, located between the anus and the of our divers made 32 dives for a total of 33 h first anal fin ray. looking for swarms all around the island, but we This was the only evidence of external sexual found no swarms or BEs. We included a survey on dimorphism we observed in adults. the windward side of the island, where tourists on Predators of P. leucotaenia: We observed no pre - charters do not dive. During our diving in Milne Bay dators of adults. We did record one potential preda - Province, PNG, we located swarms and BEs at all tor: an octopus that came along the reef directly to a study sites (Fig. 1b, Table I), especially at Observa - BE we were watching on video. It quickly squeezed tion Point, Dale’s Reef, Samarai, and Kwato. In our its sizeable body into the BE, disappearing comple - survey of the three small islands off Borneo (Fig. 1a), tely into the burrow. It came out after four minutes our six highly experienced led us directly and continued moving down the reef. In less than to the relatively few P. leucotaenia burrows at Mabul one minute, the head of the adult P. leucotaenia we and Kapalai and confirmed our observation that this were studying appeared at the BE unharmed and species was absent from nearby Sipadan. spat out a puff of sand. We observed no planktivo - Color patterns of P. leucotaenia: Lar - res eating the small endogenous larvae (as many as vae and small juveniles (ca 1 cm TL) have two hori - more than 4000) that hung around their BE. zontal dark stripes separated by a silvery white or Although the reef had many small planktivorous pale yellow stripe (Figs. 3, 4, 5a, and 6e), whereas and predatory fishes of other species nearby, we saw adults have dark, wide irregular bands and blotches none attempt to eat the larvae. separated by narrow pale areas (Fig. 11). This ban - The smaller juveniles (1.2-6.0 cm TL) had inverte - ding pattern is asymmetric on the left versus right brate and vertebrate predators. The shrimp, Pericli - sides. In nature, we never saw transitional stages of menes tenuipes , was observed several times in small pattern development between the horizontally stri - groups around the BE, especially at dawn. One of ped juveniles and the vertically banded adults. We our videographers (M. Moltzer) recorded a shrimp have, however, studied this transition in aquaria at grabbing a juvenile (ca 3.0 cm TL) with its claw as Mote Marine Laboratory, especially the asymmetric the fish came out of the BE. The shrimp bit off the pattern development in aquarium-raised specimens fish’s head, and then fended off another shrimp that (Figs. 15 and 16). The six large adult specimens tried to snatch away the prey. Small groupers have (Table III) collected in SOL and PNG, one illustra - also been seen just outside a BE at dawn. A half- ted in Fig. 9d and five illustrated in Fig. 16, all hour midday videotape, sent to us by W. McDonald showed asymmetrical patterns. (taken in PNG in August 2002), showed a single large swarm (fewer than 2000) of P. leucotaenia (ca Discussion and conclusions 4.0 cm TL) as it traveled back and forth and strea - Geographic range and dispersion: Allen & Warner med into the water column above three groupers, (2002) have pointed out that Milne Bay Province, Cephalopholis cyanostigma (Serranidae) , that charged PNG, has the richest reef fish fauna and the most into the overhead swarm several times, catching and biologically diverse and extensive coral reefs, reflec - swallowing a juvenile P. leucotaenia each time until ting its tremendous habitat diversity, compared with the swarm moved out of the grouper’s territory. The other areas they surveyed in the Philippines and videotape also showed a trumpet fish, Aulostomus Indonesia. Since our studies were in the same region, chinesis (Aulostomidae), lunging and capturing P. it was unexpected that there are two areas we sur - leucotaenia . We observed other fishes often chasing veyed where P. leucotaenia is apparently absent: the and on rare occasions eating small juveniles: butter - rich coral reef areas on isolated Mary Island (SOL) flyfishes, Forcipiger flavissimus and Chaetodon sp. and the oceanic island of Sipadan (Borneo), both (Chaetodonidae); the , Oxycheilinus diagram - surrounded by deep water (up to 1200 m) and with mus (Labridae); an unidentified damselfish; and the plentiful reef-sand interfaces that would provide sui - aqua vol. 12 no. 2 - 2006 68 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

a

Fig. 13a. Nocturnal behavior of small juvenile Pholidichthys leucotaenia when they can hang by their heads with mucus: ren - dered for clarity from video taken by M. J. Stoll, 2002, of a view inside tunnel shows three groups of juvenile fish (each ca 2.0 cm TL): two clusters of juveniles hang from tunnel ceiling. A third group of four free-swimming juveniles (disturbed by lights of Burrow Cam endoscope) swim near the mid-body of a large adult with black and white irregular markings. Two galeomatid bivalves on left, one hanging from ceiling (artist: Lawson Mitchell).

69 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

b c

Fig. 13b-c. (b) Group of 18 juveniles (each ca 1 cm TL) in a small aquarium on board that had been darkened with a black cloth for two hours, swimming around after light introduced into the aquarium, having broken their mucous thread attach - ments; (c) One of these juveniles still attached is hanging by a mucous thread from a yellow plastic tube. Right side shows eye and mucus all over its body. Photos b and c by Stephen Kogge, 2002. table habitat for P. leucotaenia. sks. Pholidichthys leucotaenia appears to be the only The widely distributed Plotosus lineatus (Fig. 6f), fish known to excavate extensive burrows in coral common throughout the Indo Pacific and Red Sea reefs and may contribute substantially to bioerosion (Knipper 1955, Magnus 1967) and at Mabul and of reefs where it is found. Coral reef substrata are Kapalai also forms swarms and appears to be absent among the softest rocks in the world (Sale 1991: 7), from Sipadan and Mary Island. The unique swar - and P. leucotaenia probably excavates its way through ming behavior of these two unrelated species, the the path of least resistance, the softest sections of the only two known species with swarming rather than reef, resulting in its winding labyrinth of irregular schooling juveniles, may account for their apparen - tunnels. At Kwato, where we studied the tunnels of tly limited ability to reach areas isolated by deep K-1 in detail, the pair of adults had built a labyrinth water. We have made many deep dives in SOL and under an area of at least 10 m 2. The only macroor - PNG previously and never seen P. leucotaenia . ganisms we observed living inside the tunnels were Larvae and juveniles of P. leucotaenia are site-atta - adults and juveniles of P. leucotaenia and the galeom - ched, one of the few marine species of fish lacking a matid bivalve. Bivalves in this family are known to larval planktonic stage dispersed by currents. Lack of live in close association with other burrowing inver - larval dispersion is a major factor in the limited tebrates, e.g. in the tunnels of squillids and worms range of P. leucotaenia within the tropical southwe - (Boss 1965), but this is the first time they have been stern Pacific (Springer & Freihofer 1976, Springer found associated with fish. & Larson 1996). In their tunneling activity, the adults of P. leucotae - Bioerosion: Piscine bioerosion is an important nia , with their well-developed conical teeth (Sprin - agent of structural change on a coral reef (Choat ger & Freihofer 1976), excavate and spit out as 1991). Many herbivorous fishes, especially scarids much as 3.2 kg/day of sand and rubble from one and triggerfish, contribute to bioerosion by scraping tunnel opening, forming the characteristic sand the reef surface. Other small coral reef fishes live in “apron”. They clean out their tunnels when debris is short tunnels taken over from burrowing invertebra - introduced during physical disturbances created by tes such as squillids, worms, and burrowing mollu - currents, other organisms, and the artificial condi - aqua vol. 12 no. 2 - 2006 70 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

a b

c

Fig. 14a-c. Electron microscope photos of a Pholidichthys leucotaenia larva (1 cm TL): (a) Dorsal view of head with 4 ope - nings of mucous glands, two larger nostril openings and mouth; (b) Enlargement of openings of four mucous glands; (c) Head-on view showing large dark nostrils, part of anterior rim of one large eye and mouth with small canine teeth. Pho - tos by Tim Maugel, 2000.

71 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

RIGHT SIDE FEB 2003 LEFT SIDE

BOOT 1 OOM

SPOON 2 MOM

DIMPLES 3 ET

INLET 4 LEFT SPOT

RIGHT SPOT 5 NIPPLE

MULTI BLOTS 6 SEVEN BLOTS

FRONT SPLIT 7 MOOO

BLACK STREAK 8 INKY

Aquarium specimens in experimental tank Feb 2003

April 2004

2R 2L

3R 3L

5R 5L

7R 7L

8R 8L

Fig. 15a-b. Asymmetry of pattern development on aquarium specimens: (a) Juveniles ca 13 cm TL raised from juveniles ca 7 cm TL. Drawing by Lance Ong, February 2003; (b) Color patterns on same juvenile specimens above now adults (num - bers 2, 3, 5, 7 and 8), as in Fig. 15a. Nicknames given at various stages help identify individuals. Numbers 1, 4, and 6 all males killed (?) probably by other males. Sexes cannot be distinguished when alive. Drawing by Mary Louise Ringers, April 2004, based on hundreds of photos taken at feeding time by Tak Konstantinou. aqua vol. 12 no. 2 - 2006 72 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle tions of our experiments. Other fishes and a few reef areas do not appear harmed, and in fact the invertebrates feed in the fresh sand spit onto the bioerosion may provide microhabitats for other reef sand “apron”, e.g. bream, Scolopsis bilineatus organisms, enhancing biodiversity on the reef. (Nemipteridae), the signal goby, Coryphopterus signi - Diel activity of juveniles: Our data shows a strong pinnis (Gobiidae), , damselfishes, and several positive relationship between diel activity of adults species of shrimp. and juveniles (Figs. 9 and 12). In the morning, when From data gathered at Tanavula, we extrapolated most of the juveniles have gone off to feed on plank - that this could amount to ca 24,528 kg (24.5 metric ton, the adults start to appear at the burrow tons) of bioeroded reef structure in one year from entrance. In the evening, after all the juveniles return the 21 known burrows. Correcting for the normal to their burrow the adults do not appear. hiatus of one week every two months (see Repro - Diel activity of adults: Like the juveniles, the duction), a more conservative estimate would be ca adults show a definite day versus night pattern of 21,585 kg (21.6 metric tons) per year. In spite of activity. Fig. 9a and b shows the changes in activity this extensive bioerosion by P. leucotaenia , these rich at the BE, from the commencement of construction

Fig. 16. Aquarium specimens raised from juveniles ca 7 cm TL to mature adults ca 20 cm TL. Same individuals as in Fig. 15, for example, the two leftmost fish can be identified as 2L and 3L on Fig. 15. Photo by Tak Konstantinou, 2003.

73 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae) and cleaning activity at dawn and continuation cule of an ascidian, probably an incidental item throughout the day to complete cessation of activity taken in with sand. Since we never saw the adults at dusk. The two instances of night activity were come out during the day to feed, we thought they limited to a small puff of sand from the BE at 1:40 might feed at night, like moray eels. However, with a.m. and 5:20 a.m. These puffs could have been cau - our image-intensified night-vision video camera, we sed by a partial collapse of the burrow, as we obser - saw no evidence of adults leaving their burrows or ved on other occasions. We never observed any feeding at night, and their heads never appeared at adults coming completely out of the burrow except the BE, which was sometimes closed. This suggests once when a young adult came out for a few that the adult P. leucotaenia normally never leaves its seconds. Until we probed the burrow with the ligh - burrow, which leads to the question, “How do these ted endoscope, we did not know what went on cryptic adults obtain food?” The large muscular inside the tunnels. Then we observed adults moving adults must require substantial food energy sources around in the tunnels frequently (which may have for excavating and cleaning their tunnels as well as been an artificial response to the light) and the producing large numbers of young. Multiple sources young apparently resting at night by hanging from of food may be present within the tunnels. The only the ceiling of the tunnels by mucus from their heads. macrofauna in the tunnels, the galeommatid bivalve, Only in response to the endoscope light, did juveni - seems to live in harmony with P. leucotaenia, based les sometimes break the mucous attachment and on our endoscopic observations. We found no evi - swim around within the tunnels. dence that it was disturbed or eaten by the fish. We Possible food source of adults: Although juveniles have considered the following as possible food sour - and young adult P. leucotaenia raised in aquaria eat ces: live brine shrimp and guppies as well as chopped 1) Durophagy. Many herbivorous fishes (such as fish, shrimp, and mussels (Wirtz 1991; and our stu - scarids) graze on the surface of coral reefs by scra - dies at Mote Marine Laboratory), the food source of ping the substrate (Choat 1991), while other fish adults in their natural habitat is puzzling. The gut feed on soft-bottom zoobenthos and affect the stan - contents in the six adults we collected (Table III) ding crops of interstitial and infaunal communities consisted of greenish chyme. No remains of fish or (Jones et al. 1991). Meiofauna, microfauna, and/or other organisms could be identified except one spi - infauna inhabiting the tunnels may be consumed by

RIGHT SIDE FEB 2003 LEFT SIDE

7 57 cm TL

6 53 cm TL

6 51 cm TL

7 48 cm TL

7 48 cm TL

Fig. 17. Asymmetry of pattern on five adult Pholidichthys leucotaenia (Table III) collected (October 2000 – June 2003) in Papua New Guinea and preserved in formalin and ethyl alcohol. Photo by Jack Nelson, 2005. aqua vol. 12 no. 2 - 2006 74 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

a b

c

Fig. 18a-c. Mote Marine Laboratory Aquarium exhibit of Pholidichthys leucotaenia coral reef habitat. Exhibit constructed with glass bottom and mirror underneath showing how tunnels are excavated by six P. leucotaenia adults living inside: (a) 380 liter tank with cryptic adults. Looking down into a mirror reflection allows viewers to see through clear glass into the bottom of the reef tunnels; (b) Close-up of adult coming out at feeding time showing tiny pelvic fins near gill ope - ning; (c) Underside of tank (mirror view) with six adults crowded in one tunnel system. Even though this habitat is artifi - cial, we can learn much about the behavior of adults in tunnels that has never been seen in nature except by our research team. Photos by Tak Konstantinou, 2005.

75 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

Fig. 19. New 1140-liter acrylic tank at Mote Marine Laboratory Aquarium with two artificial coral reefs (August 2006), which replaced earlier 380-liter tank with one reef. This tank provides more space for fish (compared to the crowded condition seen in Fig 18. This is a unique exhibit permitting scientists to see live adults in a simulated natural habitat, and permits observation of cryptic fish behavior, otherwise only seen by authors with specially contrived camera-endoscopes on diving expeditions. It shows how the adult Pholidichthys leucotaenia excavates its tunnels in an effort to make deeper tunnels, keeping the bottom of the tank clear. Two viewing mirrors below at either end, and two Burrow Cams taking live video shown on monitors (in the exhibit and remotely for 24 hour obeservations in scientists’ offices) enable us to study the process of excavation and fish behavior that would otherwise be very difficult and has been seen only during research for this paper. Photo by Tak Konstantinou, August, 2006. aqua vol. 12 no. 2 - 2006 76 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

P. leucotaenia while burrowing and cleaning its tun - machs of the six adults we collected were basically nel. The sand and copious slime lining the walls of empty, except for green chyme. We have no evidence the t unnels provide abundant substrate for meio - of cannibalism. Manica (2002) reviewed filial canni - faunal populations and a microbial food loop. balism (the act of eating one’s own offspring) in 17 These food sources would be difficult to detect in families of teleost fish as an adaptive reproductive the fish’s stomach contents, especially when the strategy, and in these cases the cannibalistic parents prey are soft-bodied invertebrates. A study of these were eating their fertilized eggs. Cannibalistic micro-communities as a source of food, a good pro - parents may consume the entire larval clutch or blem to investigate, was beyond the scope of our brood (total filial cannibalism) or just a few eggs study. However an analysis of the stomach contents (partial filial cannibalism). Payne et al. (2002) repor - of adult # 2 for ciliate protozoa abundance was ted that filial cannibalism improves survival and negative. development of damselfish embryos. In the case of P. 2) Coprophagy/Scatophagy. Defecation by plank - leucotaenia , having the abundant juveniles do the tivorous fish provides nutrient and energy sources to foraging, and adults living cryptically, is a unique other fishes and invertebrates within the reef system survival strategy that would be interesting to investi - (Choat & Bellwood 1991, Hobson 1991). Organic gate further. The juveniles may be feeding their fecal matter from the juveniles may be eaten when parents by regurgitating their food, or the adults they return to the burrow at night and may provide may be eating the young. Our analysis of the sto - adults with essential nutrients and a rich energy mach contents of six adults is insufficient to draw source. In addition, adult and juvenile feces may fer - conclusions. tilize the microbial loop and meiofaunal populations Swarming of juveniles: Swarming behavior (some - within the tunnels. times included as an aspect of schooling) is consi - 3) Mucophagy. Juveniles produce mucus, which stently found only in juveniles of two species of could provide nutrition for the adult. Gorlick marine fish, P. leucotaenia and Plotosus lineatus . (1980) reported that a cleaner wrasse ingests consi - Swarming differs from schooling behavior (Breder derable amounts of mucus from the surfaces of its 1976) where adjacent individuals are never touching hosts as a reliable energy source. The mucous but approximately equidistant and heading in the threads secreted every night by so many juveniles of same direction. In a swarm, adjacent individuals are P. leucotaenia and the mucous accumulations lining not aligned or equidistant but may be in contact and the long tunnels, often seen by the endoscope as sta - swimming in multiple, even opposite, directions lactite-like hanging strands, might be eaten by adults (Figs. 5a, b, and c). In both swarming and schooling, and contribute to the slimy stomach contents of the the fish are dependent on vision as the swarm or six adults we dissected. The abundant slime hanging school moves. The lateral horizontal stripe on the on the surfaces of the tunnels may provide an energy body, common in schooling fishes, is characteristic source as well as a substrate “slime farm”, creating a of juveniles of both swarming species, and may be specialized ecosystem for meiofaunal populations the most important visual cue used to maintain the and a microbial food loop. Like most tunnel-dwel - swarm or school. This may explain why the stripe ling fish, the adults are heavily coated with slime. breaks up into bands and blotches during the tran - 4) Juvenile regurgitation. Regurgitation of food by sition from the swarming juvenile to the cryptic adults into the mouths of juveniles is well known in adult. birds (Ziswiler & Farner 1972) and bats (Wilkinson Often a swarm goes almost directly to a specific 1990), but the opposite case of vertebrate juveniles place on the coral reef each day, such as a large sea feeding adults is not known. In the burrow at night, fan or large sunken log, when they come out of the the plump juveniles of P. leucotaenia may regurgitate BE in the morning. Large swarms of thousands of P. plankton when they are scooped in and swim out of leucotaenia juveniles sometimes leave the reef and the mouths of the adults, a behavior we have also form changing shapes that from afar look like giant seen during the day at the BE. An alternate possibi - snakes, small whales or dugongs. Videotapes taken lity is that the adults protect their young by taking by M. Moltzer and J. Rubin show these swarms to them into their mouths when disturbed. be made up of considerably more than 4,000 juve - 5) Cannibalism. The adults could easily canniba - niles and possibly close to 10,000. Springer (1957) lize the many young that swarm into the burrow reported a mass of Jenkinsia (Clupeidae) that at first each night plump with plankton. However, the sto - was mistaken for a giant ray until it was caught in a

77 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae) net and broke up into tiny fish. This has been called Therefore, it is puzzling for cryptic fish such as the collective mimicry (Knipper 1955). The juveniles adult P. leucotaenia to develop such strong color pat - may be protected from open water predators not terns along the whole body when only the head is only by the apparent size of the mass, but also by seen from outside the BE and the body remains hid - their sheer numbers. den inside the burrow. Ontogenetic shifts in juvenile resource use: Onto - Mimicry of Plotosus lineatus by juvenile Pholidi - genetic shifts in resource use, well known among chthys leucotaenia: The striped stage, the color pat - fishes, are associated with predation avoidance, tern (Fig. 6e) and swarming behavior (Figs. 4 and trophic changes, reproductive strategies, or intraspe - 5a) of juvenile Pholidichthys leucotaenia strongly cific competition (Vagelli 2004). Although P. leuco - resemble that of juveniles of the venomous catfish, taenia adults appear to spend all their time inside Plotosus lineatus (Figs. 5b, c, and 6f). Field observers their burrows, their offspring show an ontogenetic may easily mistake swarms of P. leucotaenia for the shift in patterns and habitat use. On a few occasions catfish (Randall 2005). However, a closer view of the we observed tightly packed swarms of thousands of catfish juveniles reveals four pairs of chin barbels endogenous larvae (0.7-1.0 cm, with yolk) that (Fig. 5c). stayed at and around their BE apparently not yet Their swarming behavior is associated with their feeding. However, swarms of planktivorous juveniles benthic feeding habits and they usually form groups (2-11 cm TL) may stream to a particular feeding of less than 200 individuals. P. leucotaenia usually area, over 50 m away, and sometimes extend into forms much larger, more active swarms that feed in open water to feed. Individuals in these swarms the plankton. In rare cases at Observation Point and appear to be the same size; however, when samples Kwato we have seen P. lineatus and P. leucotaenia were measured from different swarms there was a juvenile swarms blending together so closely that a variation of over 15 % relative to the average TL size diver from above could miss the fact that the mass of the fish in the sample. Breder (1976) found a was two species. With its more extensive range from similar unexpected variation in size of individuals in eastern Pacific to the Red Sea, P. lineatus is sympatric schools of Jenkensia that appeared to be the same throughout the limited range of P. leucotaenia . Pho - size. lidichthys leucotaenia juveniles may have higher sur - Hobson (1991) has pointed out that diurnal vival rates because of Batesian mimicry of both the planktivores are most numerous along reef edges color pattern and swarming behavior of the veno - adjacent to deeper water. We encountered this con - mous P. lineatus. dition at Tanavula, SOL, and Observation Point and Reproduction and breeding: Breeding does not Kwato, PNG, where the major prey, transient holo - occur seasonally in P. leucotaenia , but appears conti - plankters from open water, are more accessible to nuously throughout the year. We came across many swarms of juvenile P. leucotaenia . Resident zoo - swarms of juveniles at different months. Each swarm plankters in dense swarms close to reefs are unavai - appeared to have individuals of about the same size lable to planktivorous fishes that may be overwhel - but the average size of swarms varied greatly at the med when confronted with multiple targets and same time (ca 1-11 cm TL) from smallest to largest have difficulty distinguishing individuals, i.e., ever seen in the field. Adult P. leucotaenia appear to plankton swarms protect each other from predators. be gonochoristic, with no external sexual Diurnal planktivores depend on water currents to dimorphism except for the small urogenital papilla supply them with transient plankton as food and are we found in the largest male (Table III). We do not able to feed in characteristic stationary aggregations, know whether fertilization is external or internal. which dissolve when currents slacken and the plank - One interesting series of observations by boat tivores are forced to swim about in search of prey. manager Scott Waring, of a BE at Mirror Pond, This may explain our observations on a large swarm Mane Island, SOL, over a period of 10 months that fed for five consecutive days around a huge (March to December 1999) indicated a possible coral bommie, 51 m from their BE, (Bob’s Bom - reproductive cycle of five to six months. He took his mie), but then disappeared to another feeding area divers every 10 days and checked the same burrow we could not find. at a depth of 8 m (pers. comm. May 20, 2001). He Color patterns (Figs 16 and 17): The adaptive reported that he watched thousands of small “juve - value of stripes and other disruptive coloration in niles” grow over a period of four or five months. The is usually associated with camouflage. swarm got smaller as the juveniles got larger. In late aqua vol. 12 no. 2 - 2006 78 Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle

August when he checked the burrow, there were no eggs began hatching. Over 80 tiny larvae (ca 2 mm juveniles and no sand “apron” and also no sign of an TL each) with large yolk sacs and wiggling tails were open BE. He thought the BE was deserted, but observed but disappeared in a few days even though when he returned in late September he found thou - all fish except the two adult P. leucotaenia were sands of tiny juveniles near the BE and a large sand removed from the tank. In December 2005, the “apron”. He continued to check the BE until Krulls reported a second egg mass from the same December when the juvenile had grown larger and pair that hatched in early or mid-January 2006 and then disappeared. Possibly the adults conserve had disappeared shortly after, but not until a photo - energy when the BE is closed and reproduction grapher friend, Steve McGehee, took video recor - takes place. dings that showed at least 100 larvae that swam Aquarium spawning and growth of larvae: Wirtz about erratically. The egg diameter was similar in (1991) first reported spawning of P. leucotaenia in an size to the yolk of the newly hatched larva that aquarium. His pair of adults spawned three times, looked like an egg with a wiggling tail. “seven months apart.” The adults’ size at the first Symbiotic bivalve mollusk (Fig. 8): The unidenti - spawning was 20 cm TL. The size of the larvae on fied small bivalve mollusk living symbiotically in the zero to one day after emergence was 0.60-0.61 cm burrows with P. leucotaenia appears to belong to the TL; at four to six days, they were 0.64 to 0.71 cm family Galeommatidae (Mikkelson & Bieler 1992). TL; at days 35 to 36, they were 1.26 to 1.55 cm TL; Other bivalves in this family have been reported to and at days 55 to 56, they were 1.9 cm TL (Trnsky live symbiotically with burrowing invertebrates, e.g., et. al. 1989). mantis shrimp and large polychaete worms (Boss At Atlantis Marine World (Riverhead, Long Island, 1965). This is the first report of symbiosis between NY), J. Yaiullo (pers. comm. 2002) reported three a galeommatid bivalve and a vertebrate. spawnings of small cryptic adults in their large com - Summary and future research : The puzzling syste - munity reef tank where assorted reef fishes apparen - matic position, behavior, anatomy, and life history tly ate the tiny (less than 1 cm TL) larvae. Some of of Pholidichthys leucotaenia present many areas for the juveniles were recovered in a net by divers and future research. We don’t even know to which family raised in a separate aquarium. or group of fishes P. leucotaenia is related. Its only Gessert in Frische & Gessert (2006) reported rai - relative, P. anguius (Springer & Larson 1996) is too sing a pair of this species in an aquarium for about rare to be helpful for classification purposes, espe - 14 years. He observed a swarm of about 50 young cially DNA. fish, each 5 to 6 mm long when he discovered them. When the complexities and new classification of the The authors were able to suck out 17 of these small present labroid fishes are worked out, Pholidichthys fish with a thick hose before the rest disappeared, may prove to be related to a subgroup of those apparently eaten by their parents. These young fish fishes. were kept in a separate aquarium where they always The unique life history of P. leucotaenia includes swam together and sometimes moved very close several extraordinary features: 1) the cryptic adults together and seemed to stick to each other with their that do not come out of their tunnels, not even to heads recalling the adhering behavior of suckerfish feed or mate or lay eggs; 2) site-attached juveniles, in (Echeneidae). Wirtz (1988) first described the adhe - groups up to many thousands, stream far away to sive glands on the heads of young convictfish that feed on plankton and form great balls that suddenly can stick to algae, but Gessert was the first to report explode like firework displays and then contract to juveniles sticking to each other with their head form tight dark masses that take on forms resem - glands. bling a dugong or a small whale. Steams of juveniles Eggs of P. leucotaenia were unknown until A. and can go completely away from the reef, taking on the H. Krull (pers. comm. July 2005) reported to us the shape of a giant snake opening and closing its presence of a bright yellow egg mass-produced by mouth, before dashing back to the reef; 3) the sym - two small adults (17.3 cm TL) in their home aqua - biotic relationship of both adults and juveniles with rium. They found the yellow egg mass in an under - the undescribed species of bivalve in the longest gravel filter by looking from the underside of a glass maze of tunnels made by any fish; 4) the unique bottom aquarium. “The two parents continually flu - behavior at night of hundreds or thousands of juve - shed the eggs in and out of their mouths” for two niles that hang by their heads from the tunnel cei - weeks until the egg mass broke apart and isolated lings, perhaps a practical way of conserving energy

79 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae) and in the long narrow tunnels with little ded observations on repeated field trips: John Bass circulation except the movements of the juveniles IV, Kathy Bass, Patrice Boeke, Marcey Carabelli, and adults; 5) mimicry of the color pattern and Glenn Gebler, Jeanne Grasso, Lil Hoffman, Chuck behavior of the only other fish that swarms, Plotosus Hull, Bruce A. Hunter, Ivi Kimmel, Eli Konstanti - lineatus, the venomous catfish. nou, Hera Konstantinou, Martha Kiser, Mopsy How the adults acquire food may offer another Lovejoy, Victoria Mills, Bev Rodgerson, Mary example of unique behavior. Do the big muscular Root, Jan Rosen-Queralt, Sabine Scherer, Pat Shaw adults feed on their plump juveniles’ mucus, feces, and Mark Vignola. Frank Sturtevant and Tony or regurgitated food when the juveniles return each Tucker assisted with interpreting statistical data. night? Is feeding a factor when the juveniles are gul - Bruce Carlson, Bill Macdonald, and Keith Moe ped into their parents’ mouth? Or is this a protective sent valuable videotapes of their independent obser - action by the adults from the bright lights of our vations. Lawson Mitchell and Traer Price, Art endoscope? Directors, laid out the color plates. John E. Randall, There is still much to learn about this unique fish. Joan S. Rabin, Norma Woodburn, and Deborah We hope others will continue to investigate the Danaher, reviewed versions of this manuscript and many, still unsolved, mysteries of Pholidichthys leu - made helpful suggestions. Bev Rodgerson, Claudia cotaenia . Whether further studies on this fish are Jackson and Ellen VanDernoot gave tremendous made diving underwater, in a laboratory, in an aqua - help with the editing and preparation of this manu - rium, or by innovative new methods, we hope future script. Special thanks to the two peer reviewers, researchers will enjoy studying these fish as much as whose suggestions improved with this manuscript. we have. Our work with aquarium specimens could not have been done without the staff and volunteers at ACKNOWLEDGEMENTS Mote Marine Laboratory and the Mote Aquarium: We are grateful to many who assisted this study. Kevin Curlee, Gail Case, Bert Barnes, Debi Ingrao, The help of the boat managers, captains, and crews Neil Labelle, Sue Ryan, and Elliott Dearborn; pho - of the “M.V. Bilikiki” in the Solomons. Scott tographers Tak Konstantinou, Joe Nickelson, and Waring provided valuable field information on P. Patricia Tuccio; artists Lawson Mitchell, Mary Lou leucotaenia reproductive cycle in SOL. The Chiefs of Ringers, and Lance Ong. Karen Burns and Chris the Solomon villages (Patrick Galua of Togha Vil - Higham analyzed stomach contents and Carol Mil - lage, Edwin Tutu of Haroro Village, and Patteson ler translated pertinent articles from German. We Barua of Mane Island) gave us permission to con - are grateful for the help of Joe Yaiullo and staff at duct our field research at Tanavula and Mane Island. Atlantis Marine World. We appreciate the support In PNG we thank the captains and crews and mana - of the Mote Scientific Foundation and the encoura - gers of the dive boats “Telita”, “Golden Dawn”, and gement of the National Geographic Society (grants “Paradise Sport”. The divemasters at Sipidan Water # 6877-00 and # 7015-01). East Tennessee State Village, Mabul (Yoshi Hirata, Hiro Arakai, Leonard University provided partial travel support for DRN. Lai, Miki Anaka, Soh Kian Tiong), were especially This study was administered through the University helpful. of Maryland Foundation, Inc. Most of all, we are grateful to our dedicated team We dedicate this paper to Victor G. Springer who of volunteer research divers, who, during this long inspired and encouraged this study. series of dive trips in SOL, PNG, and Borneo, made this study possible. They include video - REFERENCES graphers Don Blair, Dinah Halstead, Ben Kendall, ALLEN , G. & T. W ARNER 2002. Coral reef assessment in the Aya Konstantinou, Alice McNulty, Maya Moltzer, ‘coral triangle’ of southeastern Asia. Environmental Biology Jack Nelson, Judith Rubin, and Mary Jane Stoll; of Fishes 65: 209-214. photographers Bob Halstead, Ruth Petzold, and ANON . 2003. The Shark Lady and the Convict Fish. Mote Tak Konstantinou; supporting photographers Patty News Magazine 48(2): 14-15. Gergen, Dick Hull, Ginny Kendall, Colin BLEEKER , P . 1856. 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The Ecology of Fishes on Coral Reefs . liformis Lockington, 1881 (Teleostei: Pholidae), a junior Academic Press, San Diego, 754 pp. synonym of Pholis ornata (Girard, 1854). Proceedings of the SALE , P. F. 1991. Chapter 1. Introduction. In: P .F. Sale (ed.) Biological Society of Washington 115 (3): 543-545. The Ecology of Fishes on Coral Reefs , Academic Press, San HERRE , A. W. 1953. Check list of Philippines Fishes. United Diego. States Department of the Interior, Fish and Wildlife Service, SCHULTZ , L. P. 1966. Order Percomorphida, Suborder Research Report 20 :1-977. Gobiina, Superfamily Gobioidea. In: Fishes of the Mar - HERRE , A. W. & E. S. H ERALD 1951. Noteworthy additions shall and Marianas Islands. USNM Bulletin 202 (3): 1-13. to the Philippine fish fauna with description of a new SPRINGER , S. 1957. Some observations on the behavior of and species. The Philippine Journal of Science , 1950 79 (3): schools of fishes in the Gulf of Mexico and adjacent waters. 309-340. Ecology 38 (1): 166-171. HOBSON , E. S. 1991. Chapter 4. Trophic relationships of SPRINGER , V. G. 2001. Pholidichthyidae, convict fish (engi - fishes specialized to feed on zooplankters above coral reefs. neer fish). FAO Species Identification guide for fishery purpo - pp. 69-95. In: P .F. Sale (ed.) The Ecology of Fishes on Coral ses. The living resources of the Western Central Pacific 6: 3500. Reefs , Academic Press, San Diego. SPRINGER , V. G. & W. F REIHOFER 1976. Study of the JONES , G. P., F ERRELL , D. J. & P. F. S ALE 1991. Chapter 7. monotypic fish family Pholidichthyidae (). Fish predation and its impact on the invertebrates of coral Smithsonian Contributions to Zoology 216: 1-43. reefs and adjacent sediments. pp. 156-179. In: P. F. Sale SPRINGER , V. G. & G. D. J OHNSON 2004. Study of the dor - (ed.) The Ecology of Fishes on Coral Reefs , Academic Press, sal gill-arch musculature of teleostome fishes, with special San Diego. reference to the . Bulletin of the Biological

81 aqua vol. 12 no. 2 - 2006 Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae)

Society of Washington 27 Oct. 2004 (11): 1- 260 + plates TRNSKI , T., L EIS , J. M. & P. W IRTZ 1989. Pholidichthyi - 1.1-205.2. dae. pp. 259-262. In: J. M. Leis & T. Trnski (ed). The SPRINGER , V. G. & H. L ARSON 1996. Pholidichthys anguis , Larvae of the Indo-Pacific Shorefishes . University of a new species of pholidichthyid fish from Northern Ter - Hawaii Press, Honolulu. ritory and Western Australia. Proceedings of the Biological VAGELLI , A. 2004. Ontogenetic shift in habitat preference Society of Washington 109 (2): 353-365. by Pterapogon kauderni , a shallow water coral reef apogo - SPRINGER , V. G. & T. M. O RRELL 2004. Appendix: Phylo - nid, with direct development. Copeia 2004 (2): 364-369. genetic analysis of 147 families of acanthomorph fishes WILKINSON , G. S. 1990. Food sharing in vampire bats. based primarily on dorsal gill-arch muscles and skeleton. Scientific American Feb 1990 :76-82. Bulletin of the Biological Society of Washington 27 Oct. WIRTZ , P. 1991. Goby or blenny? Does the larva of Pholi - 2004 (11): 237-260. dichthys leucotaenia give a clue to the systematic position of the monotypic fish family Pholidichthyidae? Tropical Fish Hobbyist 40 (Oct.): 76-78, 80.

aqua vol. 12 no. 2 - 2006 82 aqua, International Journal of Ichthyology

Dactylanthias baccheti , a new species of anthiine fish (Perciformes: Serranidae) from the Tuamotu Archipelago

John E. Randall

Bishop Museum, 1525 Bernice St., Honolulu, HI 96817-2704, USA. E-mail: [email protected]

Received: 11 October 06 – Accepted: 03 November 06

Abstract INTRODUCTION The anthiine fish Dactylanthias baccheti is described from The serranid fishes of the subfamily Anthiinae are one 204-mm specimen collected from a depth of 200-250 among the most colorful fishes of our planet. With m off Takaroa Atoll, Tuamotu Archipelago. It is distinct the exception of species of a few genera of the sub - from the one other species of the genus , D. aplodactylus from Indonesia, in having a more oblique mouth, broader family, such as Pseudanthias Bleeker, 1871, they interorbital space, different shape of fins, slightly higher cannot be viewed alive in the sea by snorkelers or counts of dorsal soft rays, pectoral rays, and lateral-line divers because they occur on reefs at greater than scales, and in life color. normal SCUBA-diving depths. The lovely fish described here from one specimen could have been Zusammenfassung seen alive in its natural habitat only from a sub - Der Fahnenbarsch (Anthiinae) Dactylanthias baccheti mersible. It was caught at Takaroa Atoll in the wird nach einem 204 mm langen Exemplar beschrieben, northern Tuamotu Archipelago by a local fisher - das in einer Tiefe von 200 bis 250 m am Takaroa-Atoll im man who reported the depth of capture as between Tuamotu-Archipel gefangen wurde. Es unterscheidet sich 200 and 250 m. von der einzigen weiteren Art der Gattung: D. aplodactylus When first examined, the fish was believed to be von Indonesien, durch ein schrägeres Maul, breiteren Interorbitalraum, andersartige Flossenform, etwas gerin - a species of Plectranthias Bleeker, 1873. Although gere Zahl an weichen Rückenflossenstrahlen, Brustflossen - large for a Plectranthias at 204 mm standard strahlen und Seitenlinienschuppen sowie eine andere length, two of the 42 known species of the genus Lebendfärbung. attain this size. When the very different shape of the fins was noticed, especially the with Résumé no notch between the spinous and soft portions, Le poisson anthiine, Dactylanthias baccheti, est décrit à and the long pointed lobe of the soft portion, it partir d’un spécimen de 204 mm collecté à une profondeur was realized that is not a species of Plectranthias. de 200-250 m au large de l’Atoll Takaroa, archipel des The author then recalled having examined the Tuamotu. Il se distingue de l’autre espèce du genre, D. aplodactylus, d’Indonésie, par une bouche plus oblique, un holotype of Dactylanthias aplodactylus (Bleeker, esapce interorbital plus important, des nageoires de forme 1858), RMNH 5457, 170 mm in standard length, différente, un nombre de rayons mous légèrement plus at the Rijksmuseum van Natuurlijke Historie (now élevé à la dorsale, des rayons pectoraux, des écailles sur la the Nationaal Natuurhistorisch Museum) in Lei - ligne latérale et par la couleur in vivo. den. Bleeker (1858) described this species in the genus Anthias Bloch, 1792 from a single specimen Sommario 255 mm in total length collected off Ambon, Dactylanthias baccheti, un serranide della sottofamiglia Indonesia. In 1871 he created the new genus anthiinae, è descritto sulla base di un singolo esemplare di Dactylanthias for it. Comparison of the Tuamotu 204 mm raccolto a profondità di 200-250 m al largo specimen with Bleeker’s description of D. aplo - dell’atollo Takaroa, nell’arcipelago delle Tuamotu. Si di- dactylus , the painting of the fish that appeared in stingue dall’altra specie del genere, D. aplodactylus pre - sente in Indonesia, per avere la bocca più obliqua, un più volume VII of his “Atlas Ichthyologique” (repro - ampio spazio interorbitale, una differente forma della duced here as Fig. 1), and notes taken by the pinne, un numero di raggi dorsali molli, di raggi pettorali author of Bleeker’s holotype easily show that the e scaglie in linea laterale leggermente maggiore e per la co- two fishes are congeneric but not conspecific. lorazione. Dactylanthias hapolodactylu s Boulenger, 1895 is

83 aqua vol. 12 no. 2 - 2006 Dactylanthias baccheti , a new species of anthiine fish (Perciformes: Serranidae) from the Tuamotu Archipelago

Fig. 1. Holotype of Dactylanthias aplodactylus , RMNH 5457, 170 mm (after Bleeker, 1873-1876: Perc. Tab. IV, fig. 3). an unjustified emendation of D. aplodactylus Morphometric data are presented in Table I as per - (Eschmeyer, 1998). centages of the standard length. Proportional mea - surements in the text are rounded to the nearest MATERIALS AND METHODS 0.05. The holotype of the new species is deposited in The pectoral-ray count includes the slender first the Bernice P. Bishop Museum, Honolulu ray closely joined to the second ray. The lateral-line (BPBM). scale count is the total count of pored scales (none The length of the specimen is given as standard on this species extend beyond the caudal-fin base); length (SL), measured from the anterior end of the scales in transverse series are counted from the ori - upper lip to the base of the caudal fin (posterior gin of the anal fin obliquely upward to the base of end of the hypural plate); body depth is the great - the dorsal fin. No gill-raker counts are possible est depth from the base of the pelvic fins to the because the gill arches were removed by the fisher - base of the dorsal spines; body width is measured man. just behind the gill opening; head length from the upper lip to the posterior end of the opercular membrane, and snout length from the upper lip to Dactylanthias baccheti , n. sp . the fleshy edge of the orbit; orbit diameter is the (Figs. 2, 3; Table I) greatest fleshy diameter, and interorbital width the least fleshy width; upper-jaw length is measured MATERIAL EXAMINED from the upper lip to the posterior end of the max - Holotype: BPBM 40412, male, 204 mm SL, illa; caudal-peduncle depth is the least depth, and Tuamotu Archipelago, Takaroa Atoll, 14°30’S caudal-peduncle length the horizontal distance 144°58’W, between 200 and 250 m, local fisher - between verticals at the rear base of the anal fin and man, November, 2005. the caudal-fin base; lengths of spines and rays are Diagnosis: Dorsal rays X,17; anal rays III,7; pec - measured to their extreme bases; caudal-fin and toral rays 19, none branched; lateral line complete, pectoral-fin lengths are the length of the longest the pored scales 37; oblique rows of scales on cheek ray; caudal concavity is the horizontal distance 5; head completely scaled except mandible and between the tips of the longest and shortest caudal lips; accessory scales on head and nape; rounded rays; pelvic-fin length is measured from the base of corner and upper margin of preopercle with 30-36 the pelvic spine to the tip of the longest soft ray. serrae; lower margin without serrae or antrorse aqua vol. 12 no. 2 - 2006 84 John E. Randall spines; body depth 2.65 in SL; head length 2.8 in straight to above eye, becoming convex on upper SL; snout short, 4.0 in head length; interorbital part of nape; snout short, 4.0 in head length; orbit space slightly convex and broad, the width 3.7 in diameter 3.9 in head length; interorbital slightly head length; caudal-fin lobes and pelvic fins fila - convex and broad, the width 3.7 in head length; mentous; color in alcohol pale yellowish with no caudal-peduncle depth 2.7 in head length; caudal- dark markings; body when fresh with a posterior peduncle length 2.1 in head length. red bar, broadly edged in pinkish white; body ante - Mouth moderately large, the maxilla reaching rior to bar pinkish white with red vertical lines fol - slightly posterior to a vertical through center of lowing scale edges; spinous portion of dorsal fin eye, the upper-jaw length 2.1 in head length; lower mainly yellow. jaw strongly projecting; mouth strongly oblique, Description: Dorsal rays X,17; anal rays III,7, all forming an angle of about 55° to horizontal axis of dorsal and anal soft rays branched, the last to base; head and body; maxilla broadly expanded posteri - branched caudal rays 13, with 5 upper and lower orly, its greatest depth two-thirds orbit diameter; a segmented unbranched rays and 4 upper and lower dense band of small villiform teeth in jaws in about procurrent rays; pectoral rays 19, none branched; 7 to 8 irregular rows anteriorly; jaws with a pair of pelvic rays I,5, all soft rays branched; lateral line short stout canine teeth anteriorly, the upper pair complete, the pored scales 37; large scales above distinctly more lateral; side of upper jaw with an lateral line to origin of dorsal fin 3; scales below lat - outer row of about 20 slender incurved teeth, eral line to origin of anal fin 13; oblique rows of notably smaller posteriorly; a stout recurved canine large scales on cheek 5; circumpeduncular scales tooth on side of lower jaw about one-fourth dis - 21; branchiostegal rays 7; supraneural (predorsal) tance to end of jaw; a broad V-shaped patch of vil - bones 3, the first anterior to first neural spine, and liform teeth on vomer in about eight rows; an elon - the next two between the first and second neural gate oval patch of villiform teeth on palatines in spines; vertebrae 26. about eight rows where broadest; tongue strongly Body depth 2.65 in SL; body width 2.25 in body tapering to slender rounded tip; no teeth on depth; head length 2.8 in SL; dorsal profile of head tongue.

Fig. 2. Holotype of Dactylanthias baccheti , BPBM 40412, 204 mm. Photo by P. Bacchet.

85 aqua vol. 12 no. 2 - 2006 Dactylanthias baccheti , a new species of anthiine fish (Perciformes: Serranidae) from the Tuamotu Archipelago

Three flat spines on opercle, the middle most pos - out on membranes of all fins except pelvic fins, terior and clearly closer to blunt upper than lower spinous portion of anal fin, and first half of spin - spine; rounded corner and upper margin of preop - ous portion of dorsal fin; scales extending out on ercle with 36 small serrae (30 on right side), not soft portion of dorsal and anal fins a distance about counting ones missing in gaps; lower margin of equal to length of longest spines; scales on base of preopercle and edge of subopercle and interopercle caudal fin about half distance to posterior margin slightly irregular but without serrae or spines. (many small scales missing); scales on pectoral fins Nostrils small, the anterior in front of center of on about basal one-fourth of fins. eye, in a very short membranous tube with a pos - Origin of dorsal fin above upper end of gill open - terior flap; posterior nostril a short distance dorso - ing, the predorsal length 2.9 in SL; first dorsal posterior, in a depression one-half covered by a spine 5.25 in head length; third to tenth dorsal membrane ventroanteriorly. spines subequal, the sixth longest, 2.3 in head Scales finely ctenoid; head completely scaled length; no notch between spinous and soft por - except lips and mandible; head and nape with tions of dorsal fin; soft portion of dorsal fin with a numerous accessory scales; small scales extending prolonged pointed lobe centered on tenth and

Fig. 3. Head of holotype of Dactylanthias baccheti. Drawing by S. Mondon. aqua vol. 12 no. 2 - 2006 86 John E. Randall

Table I. Proportional measurements of holotype of Dacty - expand into spots; all of scale edges of body above lanthias baccheti (BPBM 40000) as percentages of the stan - lateral line red; head and chest pink with a faint dard length. oblique broad yellow band on side of snout and above eye, disappearing before origin of dorsal fin; Sex male Standard Length (mm) 204.0 spinous portion of dorsal fin pink with a broad yel - Body depth 37.8 low band covering most of anterior part of fin, nar - Body width 16.9 rowing as it passes to outer third of last spine; soft Head length 34.6 portion of dorsal fin light red in a broad basal band Snout length 8.7 Orbit diameter 8.9 the length of last spine, the rest of fin translucent Interorbital width 9.3 except for red continuing a short distance out on Upper-jaw length 16.3 rays, caudal fin red basally, the edges of lobes Caudal-peduncle depth 12.8 broadly tinged with yellow, becoming translucent Caudal-peduncle length 16.7 pale yellow on about outer third of fin, except for Predorsal length 34.7 Preanal length 70.5 pale pink upper and lower margins and filaments; Prepelvic length 39.4 anal and pelvic fins pinkish white (more pink prox - Dorsal-fin base 61.1 imally and more white distally); pectoral fins with Spinous dorsal base 31.0 pale pink rays and transparent membranes. First dorsal spine 6.6 Second dorsal spine 9.7 Etymology: This species is named in honor of Longest dorsal spine 15.1 Philippe Bacchet who provided the holotype and Longest dorsal ray 35.2 its color photograph. Anal-fin base 18.0 Remarks: The genus Dactylanthias is distinct First anal spine 7.0 Second anal spine 14.9 from Plectranthias (revision by Randall 1980, when Third anal spine 15.8 30 species were known) in the following characters: Longest anal ray 32.1 mouth strongly oblique, forming an angle of about Caudal-fin length 47.5 55° to horizontal axis of head and body (vs. less Caudal concavity 22.0 Pectoral-fin length 37.3 than 45°); interorbital space broad and slightly Pelvic spine length 16.7 convex (vs. narrower and flat to concave); no notch Pelvic-fin length 61.7 in dorsal fin between spinous and soft portions; third to tenth dorsal spines subequal (vs. one or eleventh rays, 2.85 in SL; origin of anal fin below two dorsal spines clearly longest); large pointed base of fourth dorsal soft ray, the preanal length 1.4 projection in soft portion of dorsal fin with the in SL; first anal spine 4.95 in head length; third tenth and eleventh rays longest; a similar lobe in anal spine slightly longer than second spine, 2.2 in anal fin with the third and fourth rays longest; cau - head length; third and fourth anal soft rays ending dal fin emarginate with the upper and lower two in a filament, its length 3.1 in SL; caudal fin emar - branched rays filamentous; pelvic fins extremely ginate with produced lobes and filamentous tips, long, the second ray filamentous (vs. short, usually the fin length 2.1 in SL; caudal concavity 1.55 in not reaching anus). Dactylanthias is separable from head length; pectoral fins pointed, the eleventh most species of Plectranthias by having the head and twelfth rays longest, 2.7 in SL; second pelvic fully scaled except for the mandible, and in having ray produced as a long filament, extending poste - numerous accessory scales on the head and nape. rior to caudal-fin base, 1.65 in SL. Dactylanthias baccheti may be distinguished from Color of holotype in alcohol pale yel - D. aplodactylus by having a broader interorbital lowish with no dark markings; only a faint dusky space (3.7 in head length compared to 5.2 for D. margin detected posteriorly on caudal fin. aplodactylus ), a shorter snout (4.0 in head length Color of holotype when fresh (Fig. 2): vs. 3.65); second anal spine longest (vs. third spine body with a red bar (scale edges red, centers pink) longest); 30-36 serrae on preopercle (vs. 18-20); on anterior half of caudal peduncle extending and in color, as may be seen by comparing Figs 1 upward to base of last seven dorsal rays, broadly and 2. There is a slight difference in meristics; D. bordered by pinkish white; body anterior to bar baccheti has 18 dorsal rays compared to 17 for D. pinkish white with red edges on scales, the red only aplodactylus , 19 pectoral rays compared to 18, and on posterior edges below lateral line, resulting in 37 lateral-line scales compared to 39; however, vertical red lines, except ventrally where red edges these differences might not hold if series of speci -

87 aqua vol. 12 no. 2 - 2006 Dactylanthias baccheti , a new species of anthiine fish (Perciformes: Serranidae) from the Tuamotu Archipelago mens were available. As mentioned, the gill arches REFERENCES of the holotype of D. baccheti were removed; the BLEEKER , P . 1858. Negende bijdrage tot de kennis der vis - count of the gill rakers of D. aplodactylus is 10 + 25 chfauna van Amboina . Acta Societatis Scientiarum Indo- (one or two upper-limb rakers might have been Neerlandicae 3: 1-4. overlooked due to damage). BLEEKER , P. 1873. Révision des espèces indo-archipélag - iques du groupe des Anthianini . Nederlandische Tijd - schrift voor de Dierkunde 4: 155-169. ACKNOWLEDGEMENTS BLEEKER , P. 1873-1876 . Atlas Ichthyologique des Indes Ori - Dr. Alexandre Champes and Philippe Bacchet of entalis Néêrlandaises. Percoïde s, vol. 7: 1-156. Amster - Papeete, Tahiti are gratefully acknowledged for dam: Fréderic Muller et Co. making this specimen of Dactylanthias available for ESCHMEYER , W. N. 1998 . , vol. 1: 1-958. study, the former for first recognizing it as a prob - San Francisco: California Academy of Sciences. able new species, and the latter for photographing, RANDALL , J. E. 1980. Revision of the fish genus Plectran - preserving, and shipping it to the Bishop Museum. thias (Serranidae: Anthiinae) with descriptions of 13 new Thanks are also due Susan Mondon for her draw - species. Micronesica 16 (1): 101-187. ing of the head of D. baccheti and William D. Anderson, Jr. and Phillip C. Heemstra for their review of the manuscript.

aqua vol. 12 no. 2 - 2006 88 Guidelines for Authors 1. Manuscript preparation : manuscripts must be sub - BLABER , S. J. M. 1980. Fish of the Trnity inlet system mitted in English. In exceptional cases aqua may pro - of North Queensland, with notes on the ecology vide translations of manuscripts written in French, Ger - of fish faunas of tropical Indo-Pacific estuaries. man, Italian, or Spanish. Australian Journal of Marine and Freshwater Research 31 :137-46. Manuscripts must be word-processed in Microsoft WORD and submitted in an electronic form. Generic, DAY , J. H., B LABER , S. J. M., & W ALLACE , J. H. 1981. specific, and sub-specific names must be italicised. All Estuarine fishes. In: Estuarine Ecology with Parti - papers must conform to the International Code of Zoo - cular Reference to Southern . (Ed. J.H. Day.): logical Nomenclature. Authors are strongly advised to 197-221. A. A. Balkema, Rotterdam. follow the format set out in previous publications of aqua . DIMMICH , W. W. 1988. Ultrastructure of North Ame - rican cyprinid maxillary barbels. Copeia 1988 (1) : 2. Title : the title must be short and should precisely 72-79. identify the main topic of the article. Names of genera TREWAVAS , E. 1983. Tilapiine Fishes of the Genera or species are followed by the systematic group to which Sarotherodon , Oreochromis and Danakilia. they belong. Author name(s) are given in full beneath British Museum (Natural History), London, 583 pp. the title, followed by the complete mailing and e-mail address(es). 7. Submission of manuscript and illustrations: The manuscript and illustrations must be submitted digi - 3. Abstract : the abstract should not exceed 250 words tally to the Scientific Editor: and draw attention to the principal conclusions. It should not contain any uncommon abbreviations or lit - Dr. Friedhelm Krupp erature citations. The inclusion of abstracts in other lan - Senckenberg Research Institute guages is optional. Senckenberganlage 25 60325 Frankfurt am Main, Germany 5. Subject matter : the text of the manuscript is usually E-mail: [email protected] arranged in four main sections: Introduction, Materials Tel: +49-69-7542.255, Fax: +49-69-7542.253 and methods (including a key to abbreviations), Results, and Discussion. Other subdivisions may be to whom all subsequent correspondence shall be chosen depending on the material presented. Acknowl - addressed. Texts, tables, and graphs should be in edgements should be placed between the text and refer - Microsoft-compatible electronic form. ences. After the paper has been accepted for publication, illus - Scientific names of genera, species, and subspecies trations as high-resolution TIF files or original pho - should be followed by the name(s) of author(s) and the tographs (ideally transparencies; otherwise glossy year of publication on first mention. A description of a prints, preferably in the size in which they will appear - new taxon must contain the following sections: Mater - the area of aqua is 158 x 224 mm, one column is ial, Diagnosis, Description, and Affinities. Holotype 76 mm wide) must be sent to: and paratypes must be clearly identified, the institution Aquapress, The Managing Editor in which they have been deposited named, and the cat - Via G. Falcone 11, alogue numbers given. Private collections are not 27010 Miradolo Terme (Pavia), Italy acceptable as repositories for holotypes. E-mail: [email protected] Synonyms must be arranged in chronological order. Authors should retain copies of all materials for refer - Identification keys must be dichotomous. ence. The metric system and SI units must be used. Proofs of accepted papers will be sent as PDF files by e- are given in °C. Fractions should not be mail attachment to the corresponding author. used. 8. Evaluation of manuscripts: manuscripts will be eval - 6. References to literature : the name-year system must uated by the editors and referees. Papers are accepted on be used. The list of references should be placed at the the understanding that they have not and will not be end of the paper, alphabetically arranged according to published elsewhere. author name. Only those publications cited in the paper may be included. Titles of journals must be given in 9. Reprints: Authors will receive one free copy of the full. issue in which their paper appears and an e-print in PDF format. Additional copies may be ordered from Examples of correct reference formats: Aquapress. aqua International Journal of Ichthyology Vol. 12 (2), December 2006 Contents:

Eugenie Clark, Stephen N. Kogge, Diane R. Nelson, Thomas K. Alburn and John F. Pohle : Burrow distribution and diel behavior of the coral reef fish Pholidichthys leucotaenia (Pholidichthyidae) ...... 45-82

John E. Randall: Dactylanthias baccheti, a new species of anthiine fish (Perciformes: Serranidae) from the Tuamotu Archipelago ...... 83-88

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

Cover photo: False luminescent “eyes” of juvenile Pholidichthys leucotaenia: close-up of a juvenile ca 3.5 cm TL showing position of false eye on top of orbit above the pupil. Photo by Yoshi Hirata, Mabul.

Adult Pholidichthys leucotaenia: dorsal view of first adult captured, female 47 cm TL; deposited in USNM 348922. See p. 64. Photo by Stephen Kogge .