Swarming, diel movements, feeding and cleaning behavior of ...4)_Plotosus-lineatus.pdf · Abstract...

AbstractJuveniles of the venomous striped eeltail catfishes, Plotosus

lineatus and Plotosus japonicus, were studied by scuba diversin Papua New Guinea, the Solomon Islands, Indonesia,Mabul (Malaysia), Japan and the Red Sea. Dozens, up tothousands, of juveniles form swarms or “balls”, often touch-ing each other, unlike typical fish schools where adjacentindividuals swim close but not touching. Feeding swarmscan move across large stretches of sand in a steamroller-likemovement as fish from the rear constantly speed up andadvance over those in front. Lead fish use head barbels toprobe the sand for food. Over algal beds and coral reefs, cat-fish swim in smaller and looser formations. Swarms may befollowed by other fishes: shrimpfish, Aeoliscus strigatus,barred soapfish, Diploprion bifasciatum, or the puffer,Arothron manilensis, which may enter and feed with theswarm. Pomacentrids, guarding their demersal eggs on dockpilings or rocks, may attack and chase Plotosus swarms away.At Izu Peninsula, Japan, juvenile P. japonicus clean the box-fish, Ostracion immaculatus, the zebra morwong, Goniistiuszebra, and the head and inside the mouth of the moray eel,Gymnothorax kidako. Plotosus lineatus juveniles also exhibitintraspecific cleaning behavior. This facultative cleaningseems to result from accidental encounters, not at estab-lished cleaning stations. Swarms of Plotosus juveniles canmove hundreds of meters in one hour while feeding oversand. Near sundown they retire for the night under a reefledge or into an artifact (e.g. hollow log, abandoned car tire),not necessarily to the same place on consecutive nights norinto home burrows with adult fish. In appearance andswarming behavior, juvenile Pholidichthys leucotaenia areBatesian mimics of the venomous Plotosus lineatus.

ZusammenfassungJungtiere der giftigen gestreiften Korallenwelse Plotosus linea-tus und Plotosus japonicus wurden in Papua-Neuguinea, anden Salomoninseln, in Indonesien, bei Mabul (Malaysien),

in Japan und im Roten Meer mit Hilfe von Tauchgerätenerforscht. Dutzende bis Tausende dieser Jungfische bildenSchwärme oder „Bälle” und berühren einander oft dabei, wasuntypisch ist für Fisch-Schulen, bei denen die benachbartenEinzeltiere zwar dicht beieinander schwimmen, sich abernicht berühren. Nahrung suchende Schwärme können überdem Sand weite Strecken zurücklegen und bewegen sichdabei walzenartig, indem die hinteren Fische immer wiederbeschleunigen und die vorderen überholen. Die führendenFische prüfen den Sand mit ihren Kopfbarteln, um Nahrungzu finden. Über Algenbetten und Korallenriffen schwimmendie Welse in kleineren und loseren Verbänden. Den Schwär-men folgen oft andere Meerestiere: Garnelen, Rasiermesser-fische (Aeoliscus strigatus), gebänderte Seifenfische Diploprionbifasciatum oder Kugelfische Arothron manilensis, die oft inden Schwarm eindringen und mit ihm zusammen Nahrungaufnehmen. Riffbarsche, die ihre auf Pfählen oder Felsenabgelegten Eier bewachen, greifen vielfach Plotosus-Schwärme an und jagen sie fort. An der Izu-Halbinsel, Japan,zeigen junge P. japonicus Putzverhalten am Kofferfisch Ostra-cion immaculatus, am Zebramorwong Goniistius zebra undan der Muräne Gymnothorax kidako, bei der sie den Kopfund die Innenseiten des Mauls säubern. Die Jungen von Plo-tosus lineatus zeigen auch innerartliches Putzverhalten. Dasfakultative Putzverhalten scheint sich aus zufälligen Begeg-nungen zu entwickeln, Putzstationen werden nicht gebildet.Die Schwärme aus jungen Plotosus-Fischen können sich beider Nahrungsaufnahme vom Sand Hunderte von Metern ineiner Stunde bewegen. Kurz vor dem Sonnenuntergangziehen sie sich für die Nacht unter einen Riffvorsprung oderin ein Artefakt (z.B. Pfahlhöhlung oder Autoreifen) zurück,wobei nicht zwingend jede Nacht derselbe Rückzugsortaufgesucht und die Wohnhöhle erwachsener Fischegemieden wird. Nach Erscheinungsbild und Schwarmverhal-ten sind jugendliche Pholidichthys leucotaenia als BatesscheMimikry der giftigen Plotosus lineatus aufzufassen.

aqua vol. 17 no. 4 - 15 October 2011211

aqua, International Journal of Ichthyology

Swarming, diel movements, feeding and cleaning behavior of juvenile venomous eeltail catfishes, Plotosus lineatus and P. japonicus

(Siluriformes: Plotosidae)

Eugenie Clark1, Diane R. Nelson2, Mary Jane Stoll3 and Yasumasa Kobayashi4

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. Email: [email protected]

2) Department of Biological Sciences, East Tennessee State University, Johnson City, TN 37614-1710 U.S.A. 3) 565 Bellevue Ave, #1702, Oakland, CA, 94610, U.S.A.4) 3-2-9 Kitaaoyama Minato-ku, Tokyo, 107-0061, Japan

Received: 22 February 2011 – Accepted: 12 August 2011

RésuméDes juvéniles des poissons-chats venimeux, Plotosus lineatus

et Plotosus japonicus ont été étudiés par des plongeurs en Pa -pouasie-Nouvelle-Guinée, aux îles Salomon, en Indonésie, àMabul (Malaisie), au Japon et en Mer Rouge. Des douzaines,et jusqu’à des milliers, de juvéniles forment des bancs, ou des« boules », souvent en se touchant mutuellement, au con-traire des poissons typiquement grégaires où les individusvoisins nagent près les uns des autres, mais sans se toucher.Pour se nourrir, les bancs peuvent parcourir de vastes éten-dues de sable à la manière d’un rouleau compresseur parceque les poissons de l’arrière se hâtent constamment pourdépasser ceux de l’avant. Les poissons de tête se servent deleurs barbillons pour tester la valeur nutritive du sable. Surdes étendues d’algues et de récifs coralliens, les poissons-chatsnagent en formations plus petites et plus lâches. Les bancspeuvent être suivis d’autres poissons : Aeoliscus strigatus, Di -plo prion bifasciatum ou Arothron manilensis, qui peuvententrer dans la formation et se nourrir avec elle. Des Poma-centridés qui gardent leurs oeufs démersaux sur des piles dequai ou sur des rochers peuvent attaquer et chasser les bancsde Plotosus. A Izu Peninsula, Japon, des P. japonicus juvénilesnettoient Ostracion immaculatus, Gonlistius zebra et la tête etl’intérieur de la bouche de Gymnothorax kidako. Les juvénilesde Plotosus lineatus montrent aussi un comportement de net-toyage intraspécifique. Ces nettoyages occasionnels semblentse faire lors de rencontres accidentelles, et non à des stationsde nettoyage déterminées. Les bancs de Plotosus junénilespeuvent couvrir, en une heure, des centaines de mètres en senourrissant sur le sable. Vers le coucher du soleil, ils se retirentpour la nuit sous un rebord de récif ou dans un artéfact (p.ex. un rondin creux, un pneu abandonné), pas nécessaire-ment à la même place pendant des nuits consécutives, nidans les creux avec les adultes. L’apparence et le comporte-ment grégaire de Pholidichthys leucotaenia en font des imita-teurs batésiens de Plotosus lineatus.

SommarioIndividui giovani delle specie velenose di pesce gatto dei

coralli, Plotosus lineatus e Plotosus japonicus, sono stati stu-diati in attività subacquee svolte a Papua Nuova Guinea, alleisole Salomone, in Indonesia, a Mabul (Malaysia), in Giap-pone e nel Mar Rosso. I giovani formano gruppi molto ser-rati (palle) di centinaia o anche migliaia di individui che sitoc cano spesso uno con l’altro, diversamente dai tipici ban -chi di pesci dove gli individui adiacenti nuotano vicini masenza toccarsi. Quando vanno a caccia di cibo i gruppi simuo vono lungo ampie distese di sabbia con una progres-sione che ricorda quella di un rullo compressore dove gliindividui che stanno dietro costantemente sopravanzanoquelli che si trovano davanti. Questi usano i barbigli postisul capo per sondare la sabbia alla ricerca del cibo. Sui lettidi alghe e sui tratti di barriera corallina i pesci gatti nuotanoin formazioni meno numerose e più rade. I gruppi possonoessere seguiti da altre specie come il pesce rasoio Aeoliscusstrigatus, la cernia sapone Diploprion bifasciatum o il pescepalla Arothron manilensis, che possono entrare nel banco enutrirsi con il gruppo. I pomacentridi, a guardia delle uova

deposte sul fondale roccioso o sui legni, possono attaccare escacciare i gruppi di Plotosus. Nella penisola di Izu, in Giap-pone, un giovane di P. japonicus è stato osservato ripulire ilpesce scatola Ostracion immaculatus, il morwong zebratoGoniistius zebra e il capo e l’interno della bocca della murenaGymnothorax kidako. I giovani di P. lineatus si dedicanoanche ad attività di pulizia intraspecifica. Questo serviziofacoltativo sembra essere il risultato di incontri accidentali,non un comportamento eseguito in stazioni prestabilite.Quando si nutrono sul fondale sabbioso i gruppi di giovanidi Plotosus possono compiere centinaia di metri in un’ora.All’approssimarsi del tramonto essi si ritirano per la nottesotto una sporgenza rocciosa o altro rifugio anche di origineantropica come un legno cavo o uno pneumatico abbando-nato, non necessariamente nello stesso posto della notteprecedente e mai in rifugi occupati da individui adulti. Perl’aspetto e il comportamento di gruppo i giovani di Pho-lidichthys leucotaenia rappresentano un caso di mimetismobatesiano di Plotosus lineatus.

INTRODUCTIONCatfishes (order Siluriformes) are the largest mono-

phyletic group of fishes, with more than 3,000species in 36 families (Ferraris 2007). Primarily afreshwater group, a few species in the families Ploto-sidae (10 genera, 35 species) and Ariidae (26 genera,133 species) are estuarine and/or marine (Arretia etal. 2003; Ferraris 2007). Plotosus and Paraplotosus(Plotosidae) are the only genera of catfishes foundon coral reefs (Randall et al. 1997). In the genus Plo-tosus, six species were recognized as valid as of 2007,with Plotosus canius Hamilton, 1822 and Plotosuspapuensis Weber, 1910, being freshwater and Ploto-sus nkunga Gomon and Taylor, 1986, from southernAfrica being marine but also entering freshwater(Ferraris 2007). In Madagascar, Plotosus fisadoha Ng& Sparks, 2002, is also marine. Plotosus limbatusValenciennes, 1840 (in Cuvier & Valenciennes1840) is a freshwater, brackish and marine ven-omous catfish in the western Indian Ocean. Thejuveniles form dense aggregations (Sommer et al.1996; Taylor & Gomon 1986).In the Indo-Pacific and the Red Sea, Plotosus linea-

tus (Thunberg, 1787) and the newly described (theseventh known species) Plotosus japonicus Yoshinoand Kishimoto 2008 (Plotosidae), recently separatedfrom P. lineatus, are often seen by divers in coral reefareas, but they also occur on sand bottoms in tropi-cal bays, lagoons and estuaries near reefs. Bothspecies are venomous, have large swarms of juvenilesand are known to be sympatric in the Ryukyu andKyushu Islands of Japan (Yoshino & Kishimoto2008). Plotosus lineatus extends southward from theRyukyu Islands throughout the tropical Indo-

aqua vol. 17 no. 4 - 15 October 2011 212


Pacific, Australia (Siefert 2009, 2010), the Red Seaand has invaded the Mediterranean through theSuez Canal (Lessepsian migration) (Golani 2002).Plotosus japonicus is a more temperate species com-mon in Japan, the Izu Peninsula and southern Japan.Range extensions may increase as more specimensare closely examined and molecular studies are initi-ated in these two species, which differ in some mor-phological structures, including fin counts and thestructure of the dendritic organ. We could not dis-tinguish between these two species in field observa-tions or in our extensive collection of photographsand videos. Compared with the widespread distribution of Plo-

tosus lineatus in the Indo-Pacific, Pholidichthys leuco-taenia, which is often confused with Plotosus bydivers, has a much more restricted distribution. Thispattern is typical in cases of Batesian mimicry, inwhich the mimic is relatively scarce, palatable andunprotected while the model is abundant and well-

protected. However, the mimic may be more abun-dant if the model is extremely venomous and there-fore unpalatable, or if the mimic is unimportant asprey (Randall 2005). In our studies of the convictfish (Clark et al. 2006), we noted that juveniles ofthe venomous Plotosus lineatus appeared to be themodel for the convict fish, Pholidichthys leucotaenia,which mimics Plotosus in its free-swimming juvenilestage. Our divers learned to identify Plotosus lineatusby their barbels and bottom-feeding behavior incontrast to the plankton-feeding behavior of Pho-lidichthys leucotaenia. We became interested, there-fore, in the juvenile catfish aggregations, which ledto this present study to compare their behaviors withthose of the juvenile convict fish.

ABBREVIATIONSDiam: diameter; GPS: Global Positioning System;

PNG: Papua New Guinea; SOL: Solomon Islands;TL: total length.


Eugenie Clark, Diane R. Nelson, Mary Jane Stoll and Yasumasa Kobayashi

Fig. 1. World map showing distribution of Plotosus lineatus, Plotosus japonicus, and Pholidichthys leucotaenia. Plotosus lineatusand P. japonicus are sympatric in southern Japan. Pholidichthys leucotaenia, a Batesian mimic of Plotosus lineatus, has a lim-ited distribution within the widespread range of Plotosus lineatus.

MATERIALS AND METHODSUnderwater observations: The world distribution

of Plotosus lineatus, P. japonicus and Pholidichthys leu-cotaenia is shown in Fig. 1, with our study sites indi-cated. During the Israel South Red Sea Expeditionto the Dahlak Archipelago in 1962 (Oren 1962),one of us (EC) spent 2+ h observing a small “catfishball” as it moved and fed over open sandy areas.From 1982-2009, we dived in five areas in the Indo-Pacific: Japan, Indonesia, Malaysia, the SolomonIslands and Papua New Guinea (PNG). In the latterthree areas, our divers spent 5,000+ h studying andvideoing the behavior and habitat of Pholidichthysleucotaenia, noting the presence of Plotosus lineatuswhenever we came across them from before dawn toafter dusk at the study sites (Clark et al. 2006). LOCATION DATES HOURS

Mabul, Malaysia 2001-2003 417Solomon Islands 1997-1999 1931Papua New Guinea 2000-2004 3244Papua New Guinea 2007 273TOTAL 5865

In Japan, 1982, at Izu Peninsula (Fig. 1), the mostnorthern and coldest but rich coral reefs (Clark1984), David Doubilet and one of us (YK) pho-tographed swarms of catfish then called Plotosuslineatus (now P. japonicus Yoshino and Kishimoto,2008). Kobayashi made additional observationsand photographs at Izu Peninsula in 1993, 1994and 1996 (Kobayashi 1995, 1997; Kobayashi &Hakuta 2005).

In several areas throughout Indonesia (Fig. 1) in2004, 2006, 2007, 2008 and 2009, one of us (MJS)spent 40+ h videoing Pholidichthys leucotaenia andPlotosus lineatus.

In Malaysia, off north-eastern Borneo, in 2001(10 to 23 September) and 2003 (8 to 24 August), westayed at the land-based dive resort, “Sipidan WaterVillage”on the island of Mabul and took day boatsto research sites on the island and two other smallislands (Kapalai and Sipidan). Our group of 17divers spent 417 h underwater, studying both Pho-lidichthys leucotaenia and Plotosus lineatus. In the Solomon Islands (Russell and Florida



Fig. 2. Google Earth photo showing location of Garove Island and Lolobau Island, both in the Bismark Sea, off northernNew Britain Island, Papua New Guinea.



Fig. 3. Google Earth photo of Lolobau Island, Papua New Guinea, showing location of Vea Vea Bay, our main study site.

1 Km

Islands) during 1997 (27 April to 8 May), 1998 (3to 20 April), and 1999 (4 to 11 April), we charteredthe live-aboard boat, Bilikiki, which served as ourresearch base from which 54 divers spent a total of1,931 h underwater, primarily to study Pholidichthysleucotaenia, which were sometimes initially mistakenfor Plotosus lineatus.In PNG (Milne Bay Province) during 2000 (1

October to 1 November), 2001 (28 May to 16 June),2002 (25 April to 25 May), 2003 (8 May to 8 June)and 2004 (7 May to 7 June), 48 divers spent 3,244 hunderwater making observations from the live-aboardboats Golden Dawn and Telita during our studies ofPholidichthys leucotaenia (Clark et al. 2006).To concentrate our studies on Plotosus lineatus in

PNG in 2007 (11 May to June 12), we chartered thelive-aboard dive boat, Febrina, which served as ourresearch base from which 21 divers spent a total of273 h underwater in the Kimbe Bay area (Fig. 2)around Garove Island (4.40 S, 149.29 E) for 9 daysand Vea Vea Bay of Lolobau Island (4.92 S, 151.158E) (Figs 2-4a) for an additional 18 days (Doubilet2008). Tidal ranges were slight, under 1 m.

Our most intensive study site, Vea Vea Bay,Lolobau Island, PNG, is illustrated in Fig. 4a. Thesubstrate was dark gray volcanic sand, high inorganic material. A large strip of seagrass and algaeextended from a depth of 1-20 m. On the south-eastside of the bay were three patch reefs with sandchutes in between that extended from 10-21 m indepth. The top of the patch reefs were at 10 mdepth. A wide sand patch extended between thealgal bed and the most north-western patch reef,with a large (about 4 m diameter) stand of cabbagecoral (Turbinaria reniformis) (Fig. 4b) on the north-west side. Video recordings: Our videographers (Mary Jane

Stoll, Judith Rubin, Maya Moltzer, Jack Nelson)used several types of digital video cameras in under-water housings to track and record the behavior ofjuvenile swarms and one group of mating adults(MJS). Mapping of swarms: We mapped the movements

of five swarms (“A” through “E”) at Vea Vea Bay,PNG (Fig. 4a). Each swarm was identified by thesize and estimated number of individuals and their

location (depth and distribution) in the bay. A rangeof numbers in each swarm is given (Fig. 4a) sincedifferent divers reported slightly different numbersin the swarms observed at different times. Duringthe 18 day study, from before dawn until after dusk,10 pairs of divers followed the diel movements ofseparate swarms and recorded their behaviors onunderwater slates or with video/still cameras. Swarmcounts were estimated by divers in situ or afterwardsby observations of photographs and/or videos.Estimating large numbers of fish in photographs:

We counted the number of fish in a photograph bylaying a transparency sheet marked with columnsover the photograph and using a permanent markerto mark a dot over the head of each fish. Columnswere counted at least three times. To determine thenumber of fish in the swarm, we then estimated thelength and 3-D shape (volume) of the swarm, thelength of the fish and multiplied by the number offish in the photographic plane. Reactions to mirror: During three daytime dives,

divers used a large (50 cm diam), round mirror from

the ship to determine the reaction of a swarm of cat-fish to a mirror image. One diver held the mirror tothe side of the swarm or directly in front of theswarm, partially buried in the sand, while anotherdiver recorded the response either with video, stillphotos, or on a slate. The diver also rolled the mir-ror along in the sand, beside the swarm, orattempted to maintain the mirror in front of theswarm.Collection, measurements, and dissection of juve-

nile Plotosus lineatus: Three specimens in the “A”group of juveniles at Vea Vea Bay, PNG, were col-lected with a small three-pronged spear at nightunder a patch of cabbage coral (Turbinaria reni-formis) (Fig. 4b). Onboard the ship they were pho-tographed, measured, and then dissected by two ofus (DRN and EC) (Fig. 5a, b). Stomach contentswere examined and identified when possible.

RESULTSStudies in PNG in 2007: In PNG we first went to

Garove Island (Fig. 2) for 9 days of diving. We



Fig. 4a-b. a) Diel movements of five swarms of juvenile Plotosus lineatus (A, B, C, D, E) in Vea Vea Bay, Lolobau Island,Papua New Guinea, May-June 2007. Swarms moved over the sand and extensive algal mats of Caulerpa serrulata f. spiralis,and under ledges in patch reefs and into a patch of cabbage coral (Turbinaria reniformis).

a

found three widely separated, small (2 to 5 cm TL)swarms of juvenile catfish and two adults in separatebut nearby caves. In Vea Vea Bay, Lolobau Island(Figs 2, 3, 4a), during 18 days of diving, our diversfound and tracked five distinct swarms of 40 to>100 juveniles in each swarm, each with fish of sim-ilar size (<1 to 11 cm TL). Size of swarms and individuals: In Vea Vea Bay,

PNG, we determinated the range of numbers ofindividuals in the five swarms and estimated the sizeof the individuals in each swarm (Fig. 4a). In swarm“A”, we counted <100 individuals of 11 cm TL.Swarm “B” had 47-60 individuals of 5.5 cm TL.Swarm “C” had 70-100 individuals of 6 cm TL.Swarm “D” had 43 individuals (2 cm TL) andswarm “E” had <100 individuals (<1 cm TL). Diel movements of swarms: The five juvenile

swarms in Vea Vea Bay (Fig. 4a) had pathways thatextended from 40 to 70+ m from their nocturnalresting spots (under corals or in a hollow log). Swarm“A” returned each night to the same large patch ofcabbage coral (Fig. 4b). Swarm “C” had the most

extensive range, from shallow algal mats, over sand tothe cabbage coral to the hollow log in the algal mat(16 m), where they retired for the night. The otherswarms rested at night under corals in shallow water.No Plotosus swarms were observed below 23 m. Reactions to mirror: When a diver held the mirror

in front of swarm “C” of P. lineatus as it fed in thesand, the swarm was startled by sudden movementsof the diver or mirror. When the diver placed themirror in the sand and rolled it to keep it in front ofthe swarm, the juveniles showed no reaction butcontinued to feed parallel to the mirror (Fig. 6).Some individuals in the front of the swarm actuallybumped into the mirror with their heads. When thisoccurred, the fish stopped and looked at the mirror,then turned away, and the group immediatelyturned and continued to feed. In a few cases, a fishbumped into the mirror, looked at it, swam behindthe mirror, stopped, looked around, swam back tothe front of the mirror, turned parallel to the mirrorand began feeding again with the swarm. Photographic evidence of large swarms: In addi-



The area with the seagrass Halophila ovalis slightly overlapped the upper region of the algal mats and extended into moreshallow water. b) Close-up of cabbage coral (Turbinaria reniformis) where Plotosus Group A spends the night, showing fourindividuals, in 17 m of water. Photo by S. Shaw, 2007.

b

length and 3-D shape of the swarm. The fish wereabout 10 cm in length and the swarm length rangedat any one time from about 0.5-1.5 m. Since theswarm was not as dense and tapered toward the end,we used a 3-D triangle, rather than an elongated boxto represent the swarm. We noted that the fish didnot line up head to tail; instead there was consider-able overlap of the bodies, thus increasing the den-sity of the fish in the swarm. The number of fishesthat we counted in the front view in the photographwas 605, recognizing that not all fish in the photo-graph were in the same vertical plane. Based on thelength of the swarm and the length of the fish, weestimated that the total number of fish in the swarmwas in the thousands, at least 2700.One of the largest swarms of juvenile Japanese

eeltail catfish, now classified as P. japonicus, was pho-tographed at Izu Peninsula, Japan, by Kobayashi(1995) (Fig. 8). In analyzing this photograph, weestimated the swarm to consist of at least 400 indi-viduals in the front layer of fish. The top and bot-tom of the swarm were cut off in the photograph,and we could not determine the number of fish inthe layers behind the front fish, but we estimatedthere were well over 1000 in the swarm.Feeding behavior of swarms: We observed

swarms of juveniles feeding over open sand (Figs4a, 9a-d), algal (Caulerpa) beds (Fig. 10a-d), andoccasionally on and in coral reef substrates (Fig.11a-b). Plotosus juveniles fed over sand in a “steam-roller” fashion (Fig. 9) with the individuals closetogether and their barbels probing the substrate,stirring up invertebrates. During “steamroller”feeding in the sand, P. lineatus juveniles were some-times followed by other groups of teleosts (Aeolis-cus, Diploprion, Arothron, Goniistius, Parapercis,etc.) that fed on benthic organisms stirred up byPlotosus (Fig. 9a-b). Plotosus fed extensively on bedsof Caulerpa serrulata f. spiralis, which has provideconsiderable surface area for invertebrates (epizoicand epibenthic) and epiphytes such as brittle stars,sea stars, quill worms, and polychaetes (Fig. 12).Juveniles were not observed feeding on anotherspecies of green alga, Caulerpa racemosa f. pelata(Fig. 13a), or in shallow water on the large seagrassEnhalus acoroides (Fig. 13b), or on the small sea-grass Halophila ovalis (Fig. 13c), which are smoothand have sparse epiphytic organisms. In the stom-ach contents of the three individuals we dissected(Fig. 5a-b), we found sand, organic debris, quillworms, polychaete worms, brittle stars, and otherunidentifiable material, but no algae. Although we



Fig. 5a-b. Three specimens of Plotosus lineatus from GroupA, Vea Vea, Lolobau Island, PNG. (a) Three individuals,collected at night with a 3-pronged spear, ready for dissec-tion. (b) Diane Nelson removes stomach and intestinefrom a specimen.

tion to our own images of small swarms in Vea VeaBay, PNG, we obtained photographs of largeswarms in other locations from divers not in ourresearch group. The photograph of the largestswarm of P. lineatus that we examined was taken inIndonesia by John Ares (Fig. 7). We estimated theswarm consisted of over 2700 individuals based onour counts of the fish in the photograph and Ares’estimates of the length of the individuals and the

a

b

sent photographs of the tiny brittle star to experts,they were unable to identify it. Inter- and intraspecific cleaning behavior: Plotosus

juveniles are facultative cleaners of other fishes(morays, boxfish, morwongs) (interspecific cleaning,Figs 14, 15, 16, 17) and even artificial surfaces (e.g.,wet suits or diveskins of divers) (Fig. 18a, b). One ofus (DRN) observed P. lineatus feeding on sedimentsthat had settled on another diver’s fins during themirror trials (Fig. 6). One of our divers (Aya Kon-stantinou) rested on the sand in front of a feedingswarm of juvenile Plotosus. As the swarm went overher legs, she could feel some of the fish picking ather diveskin. Plotosus individuals also clean each other (intraspe-

cific cleaning, Fig. 19). The host fish opens its oper-culum, and the cleaner puts its snout into the gillchamber, apparently removing parasites, commen-sals, or dead skin, possibly as a food source. Adults: Two adult Plotosus lineatus (TL 13-15 cm)

were seen by our divers at dusk on Garove Island inPNG. The divers found one adult each in two sepa-rate caves, over 1 m apart, about 1 m back into thecave, at a depth of about 22.5 m. The solitary adultsretreated deeper into the cave when divers enteredwith flashlights. Mating/Spawning: One of us (MJS) videotaped

group spawning of Plotosus lineatus (10+ individu-als) under a coral ledge in Indonesia.

DISCUSSION Species identification: Yoshino and Kishimoto

(2008) separated as a new species, Plotosus japonicusfrom P. lineatus, by its having differences in certainmorphological characters, including a more com-plex dendritic organ with two dermal folds. Theoriginal illustration of P. lineatus by Bleeker, 1862(synonym “Plotosus arab”) in Indonesia shows thedendritic organ below the anus (Fig. 20b), but thepresence or absence of the dermal fold can not bedetermined. In Yoshino and Kishimoto (2008) thedendritic organ appears to be folded upward to showthe underlying dermal folds in P. lineatus (absent inP. japonicus) (Fig. 21). In our Fig. 19 (DouglasSeifert, Indonesia), the dendritic organ of P. lineatusis visible but not clearly defined. The question ofidentification of these two similar species by diverscan not be resolved based on photographs or videos,but at this time must be based on geographic loca-tion, except in areas of Japan where they are sym-patric. In our study, the species shown in Figures 8,15-17 is identified as Plotosus japonicus, based on thelocality.Geographic range and dispersion: The unique swarming behavior of the juveniles of

Plotosus lineatus, Plotosus japonicus, and Pholidichthysleucotaenia may explain their apparently limitedability to reach certain areas isolated by deep water.In our studies, these three species were absent from



Fig. 6. Photograph showing Plotosus moving parallel to mirror soon after mirror was placed in front of the the swarm, VeaVea Bay, Lolobau Island, PNG. One diver (Aya Konstantinou) holds the mirror while another (Maya Moltzer) videos theswarm’s interaction with the mirror. Photo by S. Shaw, 2007.





Fig. 7. Juvenile Plotosuslineatus, part of a largeswarm estimated at 2,700+individuals, depth 12-15m, Pulau Putus Island nearLembeh Island (125°15’E,1°27’N), Indonesia. Photoby J. Ares, 2007.

Mary Island (SOL) and Sipidan (Borneo), both sur-rounded by deep water, up to 1200 m (Clark et al.2006). It is not known whether temperature,swarming behavior and/or deep water prevent P.japonicus from being present in the tropical Indo-Pacific. Batesian mimicry: In the present study the similar-

ity between juveniles of Plotosus lineatus, Plotosusjaponicus and Pholidichthys leucotaenia is empha-sized. Both have similar color patterns, form swarms,and swim long distances, often in huge formations(Fig. 22). However, Plotosus juveniles can be differ-entiated by their barbels and their bottom-feedingbehaviors, whereas Pholidichthys juveniles lack bar-bels and are plankton-feeders. Even experienceddivers often have difficulty distinguishing betweenjuveniles of these two species in different genera. In Batesian mimicry, the mimic (Pholidichthys leu-

cotaenia) may be quite abundant throughout its dis-tribution if the model (Plotosus lineatus) is extremelyvenomous and therefore unpalatable, or if the

mimic is unimportant as prey (Randall 2005). Plo-tosus lineatus is notorious for being highly ven-omous. Three sharp, rigid spines, one in front of thefirst dorsal and each pectoral fin, can be locked intoplace when extended, making the fish especiallydangerous. The venom glands, located along thedorsal and pectoral spines, inject venom (ploto-toxin) when the serrated spines penetrate a person’sskin, causing great pain (Herre 1949; Halstead1988). The venom is neurotoxic, hemolytic, vaso-constrictive, and dermonecrotic. In addition, pro-teinaceous crinotoxins are secreted by epidermalcells (Shiomi et al. 1988). These lethal, hemolyticand edema-forming toxins, produced when the fishis excited or threatened, provide Plotosus with addi-tional protection from predation. Numerous incidents of severe stings have been

reported by those in the field (Burgess 1989). Dur-ing our study, Capt. Sam Kivia reported that in hisvillage of Ulamona, with 1000+ inhabitants, on thenortheast side of Garove Island, PNG, a number of



Fig. 8. Swarm of juvenile Plotosus japonicus (TL 5 cm), estimated at >400 individuals, Izu Peninsula, Japan. Photo by Y.Kobayashi, 1995.

villagers have received painful stings from P. lineatusin shallow water but no deaths resulted. To alleviatethe pain, the injured villagers drank juice fromcoconuts and wrapped the wound in young coconutleaves. This is the first report of using coconut juiceand leaves to alleviate the symptoms. In Walindi,PNG, a diver and dive boat crew member, NelsonLisian, told us that he remembers vividly as a youngboy (8 or 9 years old) being stung on the bottom ofhis foot by a tiny lone catfish in a tide pool, after hedispersed a catfish “ball.” His leg swelled up, hecouldn’t walk and stayed home in bed for a week. Predators: We did not observe predators feeding

on Plotosus (although pomacentrids, guarding theirdemersal eggs on dock poles or rocks, may attackand chase Plotosus swarms). In Okinawa, however,one of us (EC) learned from Minoru Toda, chiefaquarist at the Okinawa Churaumi Aquarium, thatthey regularly feed their squid, Sepioteuthis lessoni-ana, on easily netted catfish balls common aroundOkinawa (Toda 1985). Also Dr. Tetsuo Yoshinoconfirmed this feeding behavior in his laboratory atthe University of the Ryukyus where he is currentlystudying S. lessoniana, which is probably a complexof three species, all of which readily but carefullyfeed on Plotosus, avoiding the three venomousspines. On rare occasions, predators have caught small,

juvenile Pholidichthys. On one occasion at dawn,one of our videographers (M. Moltzer) was waitingfor the emergence of a Pholidichthys swarm from itsburrow and caught on film a shrimp, Periclimenestenuipes, which apparently was also waiting for thejuveniles to emerge, catch and eat a juvenile convictfish. Of the numerous swarms we observed, onlyonce did one of us (EC) witness a serranid,Cephalopholis cyanostigma, watch a large, elongatedswarm of juvenile Pholidichthys, then dart into theswarm, catch one fish and eat it. There is ample evi-dence that Pholidichthys leucotaenia swarms are pro-tected by Batesian mimicry of the highly venomousjuvenile swarms of Plotosus (Clark et al. 2006).. Collective mimicry: Hass (1945) suggested the

term “collective mimicry” for an “aggregation ofnumerous individuals” that acts as a “superindivid-ual”. In the Red Sea, Knipper (1955) reported anexample of “collective mimicry” in which Plotosusappeared to mimic a sea urchin. Magnus (1967) alsobecame fascinated with a catfish “ball” with the tailspositioned outward and resembling a sea urchin, butdisagreed with Knipper on calling this formationcollective mimicry. In the Gulf of Mexico, Springer

(1957) observed a compact “school” of Jenkinsiathat resembled a ray. He referred to this phenome-non as an example of “collective mimicry” but notedthat he used this term only to refer to the appearanceof the aggregation to a human observer. We haveseen collective group behavior (“superindividuals”per Hess 1945) in Pholidichthys when the swarmleaves the reef and forms changing shapes thatresemble different large organisms such as giant fish,whales, or sea snakes. This group behavior may pro-tect the swarm from open water predators. In Ploto-sus, we have not observed “collective mimicry”behavior in large swarms in open water, but thejuveniles do form dense balls on or near the sub-strate (see “Swarming” below).Swarming: In contrast to schooling behavior, few

fishes form tight swarms of individuals, such as wefound in Plotosus and Pholidichthys (Clark et al.2006). Plotosus juveniles near the substrate can alsoform rounded aggregations that may resemble seaurchins (“collective mimicry”); these “catfish balls”(Fig. 23a-b) are called gonzai dama in Japanese. Thisdense ball-shaped swarm forms soon after hatching(Moriuchi & Dotsu 1973), indicating that theswarm formation is initiated by sibling recognitionassociated with olfactory and visual cues (Kinoshita1975; Hayashi et al. 1994). A mixture of phos-phatidylcholine molecular species in the skinmucus, released into the seawater, is thought to bethe chemical cue that elicits “turn behavior” of P.lineatus individuals (Matsumura et al. 2004). Paramo et al. (2010) have defined schools as

groups of fish that are characterized by polarized,equally spaced individuals swimming synchro-nously. Although some schools (e.g., sardines) mayform “bait balls” that look like swarms, they do nottouch each other. The difference between a“swarm” and a “school” is that in a swarm the indi-viduals can be touching each other, whereas in aschool the individuals are staggered, not lined upand they maintain their distance from each other,possibly by cupulae on their lateral line (Cahn &Shaw 1962; Cahn et al. 1968; McHenry et al.2008; Shaw 1962). Reactions to mirror: Satô (1938) studied the role of

vision in the formation of aggregations of “P. linea-tus” (now P. japonicus) in an aquarium. When a sin-gle fish was transferred into an aquarium with a mir-ror against one side, the fish swam to the mirror,zigzagging across the mirror surface with its face closeto the glass. An increase in the number of fishesdecreased the intensity of their reaction to the mirror.





Fig 9a-d. “Steamroller” feeding on the open sand by tightly-packed swarms of juvenile Plotosus lineatus. (a) “Steamroller”swarm followed by a puffer fish, Arothron manilensis, feeding on organisms stirred up by Plotosus, Mabul, Malaysia. Photo byS. Shaw, 2003. (b) “Steamroller” swarm followed by a large group of shrimpfish, Aeoliscus strigatus, Indonesia. Frame from

a

b


video taken by M. J. Stoll, 2003. (c) Close-up of “steamroller” swarm as they are beginning to feed in the sand, Vea Vea Bay,Lolobau Island, PNG. Photo by D. Nelson, 2007. (d) Close-up of leading edge of “steamroller” feeding, Indonesia. Imagecourtesy of E. Cheng/echeng.com, 2009.

c

d



Fig. 10a-d. Loose aggregations of Plotosus lineatus feeding over spiral algal mats (Caulerpa serrulata f. spiralis) spreading overdark volcanic sand, Vea Vea Bay, Lolobau Island, PNG. Unlike “steamrolling” on sand, the formation is looser and not in astraight line when they feed on the algal mat. (a) Small swarm (~70) over algal mats near shore, showing sloping habitat.Photo by V. Palubok, 2007. (b) Swarm C (~106 individuals, 6 cm TL), swimming over algal mat and starting to feed on

a

b



epibenthos and epizoans. Barbels are visible on some Plotosus specimens. Photo by Diane Nelson, 2007. (c) Some individu-als in Group C swimming horizontally, while others are going down into the algal mat to feed. Photo by S. Shaw, 2007.(d) Individuals in Group C feeding in an irregular pattern on invertebrates on the alga. Photo by S. Shaw, 2007.

c

d



Fig 20a-b. Plotosus lineatus (synonym, “Plotosus arab”) from Indonesia. From Bleeker, 1862. (a) Left lateral view of adult,showing location of dendritic organ posterior to base of pelvic fins. (b) Ventral view of base of pelvic fins, anus, and dendriticorgan.

Fig. 21. Dendritic organs of Plotosus lineatus (left) and Plotosus japonicus (right). A: pelvic fin, B: dendritic organ, C: dermalfold, D: anal fin. From Yoshino and Kishimoto, 2008.

a b

We observed this group behavior with a mirror inVea Vea Bay. The actively-feeding swarm paid littleattention to the divers or mirror until individualjuveniles bumped into the mirror, looked at it andthen changed their direction of movement. Thenthe entire swarm rapidly changed its direction,swimming parallel to the mirror (or away from it)and continued feeding. Until the fish physically con-tacted the mirror, they looked toward the swarm in

the mirror and behaved as if the mirror image waspart of the group.Inter- and intraspecific cleaning: Plotosus juve-

niles feed primarily on epibenthic invertebrates inorganically rich sand, in algal beds with extensivesurface area covered with epizootic and epiphyticorganisms, and occasionally on invertebrates onsubstrates between reef corals. They are also facul-tative cleaners of other fish and artificial surfaces.


Although Côté (2000) reviewed cleaning sym-bioses in 97 species of fishes (and 34 species ofcrustaceans), Plotosus was not included as a faculta-tive cleaner (one that gleans only a small part of itsfood by cleaning as juveniles). Obligate cleanersobtain an average of 85% of their food, primarilyectoparasites, from their symbionts and often aremarked with bright lateral stripes. In Plotosus, thelateral stripe may be more important in swarmingbehavior and mimicry than in cleaning behavior. Masuda et al. (1975) briefly mention that Plotosus

“sometimes cleans other fish.” This is the first ref-erence world-wide to Plotosus as a cleaner. In theexpanded version of the comprehensive list offishes in Japan, Masuda et al. (1984), they do notmention this cleaning behavior. In our studies oneof us (YK) photographed different species of fishbeing cleaned by Plotosus japonicus in Izu Penin-sula, Japan (Figs. 15-17). This behavior may becommon but may have been overlooked previouslyby divers. In Indonesia, Douglas Seifert recently observed

and photographed P. lineatus juveniles cleaning thegills of other juveniles (Fig. 19). In a tightly-packedaggregation, the snout of the cleaner is insertedinto the gill chamber of the fish being cleaned,which has its mouth agape. Intraspecific cleaning isvery rarely reported in fishes, although it is a com-mon behavior in mammals, especially duringgrooming and courtship behavior. In this study weprovide photographic evidence of intraspecificcleaning in Plotosus for the first time. Adults and sub-adults: Plotosus lineatus adults are

solitary or occur in small groups up to 20. Adultsare nocturnal and known to hide under ledges dur-ing the day, unlike the juveniles and sub-adultsthat feed actively during the day and hide at nightin natural or man-made objects. In Mabul,Malaysia, sub-adults retired into a tire at dusk andemerged again at dawn (Fig. 24a-d). Spawning: According to Thresher (1984), Ploto-

sus off Japan spawns in late spring and early sum-mer, at which time the males construct nests underrocks and other large pieces of debris on a sandybottom. After spawning, the male also guards the300-700 eggs. Eggs are spherical, non-adhesive,demersal, and roughly 3.1 to 3.5 mm in diameter,with a large bright yellow yolk. Newly hatched lar-vae are about 6.9 mm long and carry a large yolk sac. In Indonesia, one of us (MJS) videoed the Kai sole,

Aseraggodes kaianus, eating the eggs of P. lineatus justafter spawning. This was the only record of preda-

tion on eggs that we observed in the natural envi-ronment. After hatching, the juveniles stay on the bottom

and start swarming within a week (Moriuchi &Dotsu 1973). When two schools are mixed, thejuveniles return to the original school, indicatingthat the chemical cue is specific, allowing individu-als to discriminate their own school from others(Kinoshita 1975). However, the sensitivity to theodor of swarm mates may be somewhat plastic,


Fig. 11a-b. Plotosus lineatus juveniles feeding in patch reefsin Vea Vea Bay, Lolobau Island, PNG. (a) Juveniles feedingon organisms on flat surface of hard substrate in coralpatch reef. (b) Juveniles feeding on organisms in holes andcrevices in coral patch reef. Photos by P. Sturtevant, 2007.

a

b



based on the genetic variation found within theschool (Iwasaki 1995), indicating that individualscan join other swarms.Dendritic organs: Highly vascularized dendritic

organs, thought to be salt-secreting organs (Pucke &Umminger 1979), are present and equally developed

in adults and juveniles of both sexes in Plotosus andother marine genera in Plotosidae (Cnidoglanis,Euristhmus, Paraplotosus) (Lanzing 1967). Plotosuspapuensis Weber, 1910, apparently has recentlyentered freshwater rivers in New Guinea (formerlyIrian Jaya) and still has a dendritic organ (Burgess

Fig. 12a-b. The alga Caulerpa serrulata f. spiralis, with its “jungle” of coils that provide abundant surface area for prey items of Plo-tosus lineatus in Vea Vea Bay, Lolobau Island, PNG. (a) Commensal organisms on the algal spirals and rhizomes. Note unidenti-fied brittle star with a bright red central disk and striped arms in lower left. This brittle star was abundant in the stomach con-tents we examined. (b) Close up of algal spirals with unidentified quill worm, a tube-carrying epibenthic polychaete. This was oneof the common items we found in the stomach contents of the three Plotosus lineatus we dissected. Photos by D. Nelson, 2007.

a

b



Fig. 13a-c. Alga and sea grasses present in Vea Vea Bay, Lolobau Island, PNG, where feeding swarms of Plotosus lineatus werenever observed. The relatively smooth surfaces had few organisms that could be potential food for Plotosus. (a) Close up ofthe alga, Caulerpa racemosa f. peltata with sparse epiphytic organisms. (b) Close up of the large seagrass Enhalus acoroides, themost shoreward of the aquatic plants. A small brittle star is present near the upper part of the blade but only a few otherorganisms are visible. (c) Close up of dark volcanic sand grains and small seagrass Halophilia ovalis with no visible organismson the leaves. Photos by D. Nelson, 2007.

c

a b



Fig. 14. Gymnothorax kidako, a common moray eel, Izu Peninsula, Japan. Photo by D. Doubilet, 1982, in Clark, 1984.

Fig. 15. Plotosus japonicus juveniles (7 cm TL) cleaning Gymnothorax kidako (80 cm TL), depth 15 m, Izu Peninsula, Japan.Photo by Y. Kobayashi, 1996.



Fig. 16. Plotosus japonicus juveniles (7 cm TL) cleaningGoniistitis zebra, “zebra morwong,” family Cheilodactyli-dae (30 cm TL), 10 m depth, Izu Peninsula, Japan. Photoby Y. Kobayashi, 1993.

Fig. 17. Plotosus japonicus juveniles (7 cm TL) cleaningOstracion immaculatus (12 cm TL) under ledge, depth 5m, Izu Peninsula, Japan. Photo by Y. Kobayashi, 1982.

Fig. 18a-b. Diver encounter with swarm of >100 sub-adult Plotosus lineatus under dock, Raja Ampat, Indonesia. (a) Diver(Eric Cheng) was approached by the swarm that encircled him and cleaned the wet suit covering his legs. Photographer wasso transfixed that he did not photograph the actual cleaning. (b) Photographer regained his composure and photographedthe swarm returning to the dock. Photos by Y. Ch’ng, 2008.

a b



Fig. 19. Intraspecific cleaning by Plotosus lineatus. Center fish, with mouth agape, allows another fish to clean its gills. Pinkdendritic organ (arrows) posterior to pelvic fins, most visible on two fish in upper left. Secret Bay/Gilimanuk in North Bali,Indonesia. Photo by D. Seifert, 2008.

⬅⬅



Fig. 22a-b. Batesian mimicry. (a) Swarm of juvenile venomous catfish, Plotosus lineatus, the model for the mimic Pholidichthysleucotaenia (22b). Barbels are inconspicuous except on three individuals feeding in sand (front bottom of picture), Mabul,Malaysia. Photo by S. Shaw, 2003. (Reprinted with permission. First published 2006 in aqua 12 (2): 58.) (b) Swarm of juve-nile convict fish Pholidichthys leucotaenia, the mimic of Plotosus lineatus (22a). Barbels are absent in this plankton-feedingfish. Samurai, PNG. Photo by D. Halstead, 2003.

b

a



Fig. 23a-b. “Catfish balls” (gonzai dama), a non-feeding, slowly-moving, tightly-packed aggregation of Plotosus that mayresemble sea urchins (“collective mimicry”). (a) Plotosus japonicus, Izu Peninsula, Japan. Photo by Y. Kobayashi, 1995. (b) Plotosus lineatus sub-adults under dock, looking like a chorus, Lord Howe Island, Australia. Photo by D. Seifert, 1998.

b

aa



Fig. 24a-d. Plotosus lineatus sub-adults (~13 cm TL), depth 10 m, Mabul, Malaysia. (a) Retiring into a tire at dusk. (b) Intire, with measuring stick (5 cm increments). (c) In tire near dawn with a filefish, Paraluteres prionurus, the Batesian mimicof the poisonous puffer Canthigaster valentini. (d) Streaming away from tire at dawn. Photos by S. Shaw, 2003.

c d

a b

1989; Ferraris 2007). One morphological differenceseparating P. lineatus and P. japonicus is the complexstructure of the dendritic organ. We have becomeinterested in the dendritic organ and suggest thatthis structure be studied further in the catfishes.

ACKNOWLEDGEMENTSWe extend special thanks to our volunteer research

divers, whose observations, photographs and videoprovided data for this study in PNG and Mabul:Anne Doubilet, Jessica Goldstein, Bob Halstead,Martha Kiser, Hanna Koch, Steve Kogge, Aya andTak Konstantinou, Zen Kurokawa, Mopsy Lovejoy,Maya Moltzer, Jack Nelson, Val Palubok, John F.Pohle, Jann Rosen-Queralt, Judith Rubin, Pat andSusan Shaw, David Shen and Patty Sturtevant. JohnF. Pohle organized our dives and gave considerablehelp in mapping and GPS locations. Bob Halstead,the most knowledgeable diver and author of fishesin PNG waters, provided exceptional logistical helpand many keen observations during and after ourboat charters in PNG. We appreciate the good careof the crew of the Febrina in PNG, especially thevaluable help of the crew divers, Captain Sam Kivia,Alfred George, Josie Waiwai, Martin Giru, and Nel-son Lisian, who contributed data for our researchand spent many hours assisting us underwater. Thestaff at the dive center at Sipidan Water Village,Mabul, Malaysia, was very helpful. LawsonMitchell, Creative Director, Mote Marine Labora-tory, produced the maps and the layout of the fig-ures. John Ares provided photographs and observa-tions of a large swarm of Plotosus lineatus in Indone-sia. Yeang Ch’ng photographed P. lineatus swarmingover to diver, Eric Cheng, in Raja Ampat, Indonesia.Eric Cheng provided close-up images of Plotosus.Douglas Seifert provided photographs of P. lineatuscleaning each other. Bill Macdonald sent valuablevideo of his independent observations. Diane andMark Littler identified the green algae and seagrassesat Vea Vea, PNG. Carol Miller translated pertinentarticles from German. Bev Rodgerson, RachelDreyer, Cathy Marine, Patricia Tuccio, Lance Ongand Joan Rabin gave valuable help with the editingand preparation of this manuscript. We thank thetwo reviewers and Helen Larson for their detailedcomments and suggestions that considerablyimproved this final version of this paper. SusanStover, Mote librarian, gave us much help in track-ing down obscure references. Patricia Tuccio pro-vided numerous references and discussions onswarming behavior. We appreciate the support of

the Mote Scientific Foundation. East TennesseeState University provided partial travel support forDRN. This study was administered through theUniversity of Maryland Foundation.

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