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Swarming, diel movements, feeding and cleaning behavior of juvenile venomous eeltail catfishes, Plotosus lineatus and P. japonicus (Siluriformes: Plotosidae).

INTRODUCTION

Catfishes (order Siluriformes) are the largest monophyletic group of fishes, with more than 3,000 species in 36 families (Ferraris 2007). Primarily a freshwater group, a few species in the families Plotosidae (10 genera, 35 species) and Ariidae (26 genera, 133 species) are estuarine and/or marine (Arretia et al. 2003; Ferraris 2007). Plotosus and Paraplotosus (Plotosidae) are the only genera of catfishes found on coral reefs (Randall et al. 1997). In the genus Plotosus, six species were recognized as valid as of 2007, with Plotosus canius Hamilton, 1822 and Plotosus papuensis Weber, 1910, being freshwater and Plotosus nkunga Gomon and Taylor, 1986, from southern Africa being marine but also entering freshwater (Ferraris 2007). In Madagascar, Plotosus fisadoha Ng & Sparks, 2002, is also marine. Plotosus limbatus Valenciennes, 1840 (in Cuvier & Valenciennes 1840) is a freshwater, brackish and marine venomous catfish in the western Indian Ocean. The juveniles form dense aggregations (Sommer et al. 1996; Taylor & Gomon 1986).

In the Indo-Pacific and the Red Sea, Plotosus lineatus (Thunberg, 1787) and the newly described (the seventh known species) Plotosus japonicus Yoshino and Kishimoto 2008 (Plotosidae), recently separated from P. lineatus, are often seen by divers in coral reef areas, but they also occur on sand bottoms in tropical bays, lagoons and estuaries near reefs. Both species are venomous, have large swarms of juveniles and are known to be sympatric in the Ryukyu and Kyushu Islands of Japan (Yoshino & Kishimoto 2008). Plotosus lineatus extends southward from the Ryukyu Islands throughout the tropical Indo-Pacific, Australia (Siefert 2009, 2010), the Red Sea and has invaded the Mediterranean through the Suez Canal (Lessepsian migration) (Golani 2002). Plotosus japonicus is a more temperate species common in Japan, the Izu Peninsula and southern Japan. Range extensions may increase as more specimens are closely examined and molecular studies are initiated in these two species, which differ in some morphological structures, including fin counts and the structure of the dendritic organ. We could not distinguish between these two species in field observations or in our extensive collection of photographs and videos.

Compared with the widespread distribution of Plotosus lineatus in the Indo-Pacific, Pholidichthys leucotaenia, which is often confused with Plotosus by divers, has a much more restricted distribution. This pattern is typical in cases of Batesian mimicry, in which the mimic is relatively scarce, palatable and unprotected while the model is abundant and wellprotected. However, the mimic may be more abundant if the model is extremely venomous and therefore unpalatable, or if the mimic is unimportant as prey (Randall 2005). In our studies of the convict fish (Clark et al. 2006), we noted that juveniles of the venomous Plotosus lineatus appeared to be the model for the convict fish, Pholidichthys leucotaenia, which mimics Plotosus in its free-swimming juvenile stage. Our divers learned to identify Plotosus lineatus by their barbels and bottom-feeding behavior in contrast to the plankton-feeding behavior of Pholidichthys leucotaenia. We became interested, there-fore, in the juvenile catfish aggregations, which led to this present study to compare their behaviors with those of the juvenile convict fish.

ABBREVIATIONS

Diam: diameter; GPS: Global Positioning System; PNG: Papua New Guinea; SOL: Solomon Islands; TL: total length.

MATERIALS AND METHODS

Underwater observations: The world distribution of Plotosus lineatus, P. japonicus and Pholidichthys leucotaenia is shown in Fig. 1, with our study sites indicated. During the Israel South Red Sea Expedition to the Dahlak Archipelago in 1962 (Oren 1962), one of us (EC) spent 2+ h observing a small "catfish ball" 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 Solomon Islands and Papua New Guinea (PNG). In the latter three areas, our divers spent 5,000+ h studying and videoing the behavior and habitat of Pholidichthys leucotaenia, noting the presence of Plotosus lineatus whenever we came across them from before dawn to after dusk at the study sites (Clark et al. 2006).

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LOCATION            DATES    HOURS

Mabul, Malaysia   2001-2003    417

Solomon Islands   1997-1999   1931

Papua New Guinea  2000-2004   3244

Papua New Guinea       2007    273

TOTAL                         5865


In Japan, 1982, at Izu Peninsula (Fig. 1), the most northern and coldest but rich coral reefs (Clark 1984), David Doubilet and one of us (YK) photographed swarms of catfish then called Plotosus lineatus (now P. japonicus Yoshino and Kishimoto, 2008). Kobayashi made additional observations and photographs at Izu Peninsula in 1993, 1994 and 1996 (Kobayashi 1995, 1997; Kobayashi & Hakuta 2005).

In several areas throughout Indonesia (Fig. 1) in 2004, 2006, 2007, 2008 and 2009, one of us (MJS) spent 40+ h videoing Pholidichthys leucotaenia and Plotosus lineatus.

In Malaysia, off north-eastern Borneo, in 2001 (10 to 23 September) and 2003 (8 to 24 August), we stayed at the land-based dive resort, "Sipidan Water Village" on the island of Mabul and took day boats to research sites on the island and two other small islands (Kapalai and Sipidan). Our group of 17 divers spent 417 h underwater, studying both Pholidichthys leucotaenia and Plotosus lineatus.

In the Solomon Islands (Russell and Florida Islands) during 1997 (27 April to 8 May), 1998 (3 to 20 April), and 1999 (4 to 11 April), we chartered the live-aboard boat, Bilikiki, which served as our research base from which 54 divers spent a total of 1,931 h underwater, primarily to study Pholidichthys leucotaenia, which were sometimes initially mistaken for 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 h underwater making observations from the live-aboard boats Golden Dawn and Telita during our studies of Pholidichthys leucotaenia (Clark et al. 2006).

To concentrate our studies on Plotosus lineatus in PNG in 2007 (11 May to June 12), we chartered the live-aboard dive boat, Febrina, which served as our research base from which 21 divers spent a total of 273 h underwater in the Kimbe Bay area (Fig. 2) around Garove Island (4.40 S, 149.29 E) for 9 days and Vea Vea Bay of Lolobau Island (4.92 S, 151.158 E) (Figs 2-4a) for an additional 18 days (Doubilet 2008). Tidal ranges were slight, under 1 m.

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Our most intensive study site, Vea Vea Bay, Lolobau Island, PNG, is illustrated in Fig. 4a. The substrate was dark gray volcanic sand, high in organic material. A large strip of seagrass and algae extended from a depth of 1-20 m. On the south-east side of the bay were three patch reefs with sand chutes in between that extended from 10-21 m in depth. The top of the patch reefs were at 10 m depth. A wide sand patch extended between the algal bed and the most north-western patch reef, with a large (about 4 m diameter) stand of cabbage coral (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 of juvenile 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 a(Fig. 4a). Each swarm was identified by the size and estimated number of individuals and their location (depth and distribution) in the bay. A range of numbers in each swarm is given (Fig. 4a) since different divers reported slightly different numbers in the swarms observed at different times. During the 18 day study, from before dawn until after dusk, 10 pairs of divers followed the diel movements of separate swarms and recorded their behaviors on underwater slates or with video/still cameras. Swarm counts were estimated by divers in situ or afterwards by observations of photographs and/or videos.

Estimating large numbers of fish in photographs: We counted the number of fish in a photograph by laying a transparency sheet marked with columns over the photograph and using a permanent marker to mark a dot over the head of each fish. Columns were counted at least three times. To determine the number of fish in the swarm, we then estimated the length and 3-D shape (volume) of the swarm, the length of the fish and multiplied by the number of fish 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 catfish to a mirror image. One diver held the mirror to the side of the swarm or directly in front of the swarm, partially buried in the sand, while another diver recorded the response either with video, still photos, or on a slate. The diver also rolled the mirror along in the sand, beside the swarm, or attempted to maintain the mirror in front of the swarm.

Collection, measurements, and dissection of juvenile Plotosus lineatus: Three specimens in the "A" group of juveniles at Vea Vea Bay, PNG, were collected with a small three-pronged spear at night under a patch of cabbage coral (Turbinaria reniformis) (Fig. 4b). Onboard the ship they were photographed, measured, and then dissected by two of us (DRN and EC) (Fig. 5a, b). Stomach contents were examined and identified when possible.

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RESULTS

Studies in PNG in 2007: In PNG we first went to Garove Island (Fig. 2) for 9 days of diving. We found three widely separated, small (2 to 5 cm TL) swarms of juvenile catfish and two adults in separate but nearby caves. In Vea Vea Bay, Lolobau Island (Figs 2, 3, 4a), during 18 days of diving, our divers found and tracked five distinct swarms of 40 to <100 juveniles in each swarm, each with fish of similar size (>1 to 11 cm TL).

Size of swarms and individuals: In Vea Vea Bay, PNG, we determinated the range of numbers of individuals in the five swarms and estimated the size of 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) and swarm "E" had >100 individuals (>1 cm TL).

Diel movements of swarms: The five juvenile swarms in Vea Vea Bay (Fig. 4a) had pathways that extended from 40 to 70+ m from their nocturnal resting spots (under corals or in a hollow log). Swarm "A" returned each night to the same large patch of cabbage coral (Fig. 4b). Swarm "C" had the most extensive range, from shallow algal mats, over sand to the cabbage coral to the hollow log in the algal mat (16 m), where they retired for the night. The other swarms 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 the sand, the swarm was startled by sudden movements of the diver or mirror. When the diver placed the mirror in the sand and rolled it to keep it in front of the swarm, the juveniles showed no reaction but continued to feed parallel to the mirror (Fig. 6). Some individuals in the front of the swarm actually bumped into the mirror with their heads. When this occurred, the fish stopped and looked at the mirror, then turned away, and the group immediately turned and continued to feed. In a few cases, a fish bumped into the mirror, looked at it, swam behind the mirror, stopped, looked around, swam back to the front of the mirror, turned parallel to the mirror and began feeding again with the swarm.

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Photographic evidence of large swarms: In addition to our own images of small swarms in Vea Vea Bay, PNG, we obtained photographs of large swarms in other locations from divers not in our research group. The photograph of the largest swarm of P. lineatus that we examined was taken in Indonesia by John Ares (Fig. 7). We estimated the swarm consisted of over 2700 individuals based on our counts of the fish in the photograph and Ares' estimates of the length of the individuals and the length and 3-D shape of the swarm. The fish were about 10 cm in length and the swarm length ranged at any one time from about 0.5-1.5 m. Since the swarm was not as dense and tapered toward the end, we used a 3-D triangle, rather than an elongated box to represent the swarm. We noted that the fish did not line up head to tail; instead there was considerable overlap of the bodies, thus increasing the density of the fish in the swarm. The number of fishes that we counted in the front view in the photograph was 605, recognizing that not all fish in the photograph were in the same vertical plane. Based on the length of the swarm and the length of the fish, we estimated that the total number of fish in the swarm was in the thousands, at least 2700.

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One of the largest swarms of juvenile Japanese eeltail catfish, now classified as P. japonicus, was photographed at Izu Peninsula, Japan, by Kobayashi (1995) (Fig. 8). In analyzing this photograph, we estimated the swarm to consist of at least 400 individuals in the front layer of fish. The top and bottom of the swarm were cut off in the photograph, and we could not determine the number of fish in the layers behind the front fish, but we estimated there were well over 1000 in the swarm.

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Feeding behavior of swarms: We observed swarms of juveniles feeding over open sand (Figs 4a, 9a-d), algal (Caulerpa) beds (Fig. 10a-d), and occasionally on and in coral reef substrates (Fig. 11a-b). Plotosus juveniles fed over sand in a "steam-roller" fashion (Fig. 9) with the individuals close together and their barbels probing the substrate, stirring up invertebrates. During "steamroller" feeding in the sand, P. lineatus juveniles were sometimes followed by other groups of teleosts (Aeoliscus, Diploprion, Arothron, Goniistius, Parapercis, etc.) that fed on benthic organisms stirred up by Plotosus (Fig. 9a-b). Plotosus fed extensively on beds of Caulerpa serrulata f. spiralis, which has provide considerable surface area for invertebrates (epizoic and epibenthic) and epiphytes such as brittle stars, sea stars, quill worms, and polychaetes (Fig. 12). Juveniles were not observed feeding on another species of green alga, Caulerpa racemosa f. pelata (Fig. 13a), or in shallow water on the large seagrass Enhalus acoroides (Fig. 13b), or on the small sea-grass Halophila ovalis (Fig. 13c), which are smooth and have sparse epiphytic organisms. In the stomach contents of the three individuals we dissected (Fig. 5a-b), we found sand, organic debris, quill worms, polychaete worms, brittle stars, and other unidentifiable material, but no algae. Although we sent photographs of the tiny brittle star to experts, they were unable to identify it.

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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 of us (DRN) observed P. lineatus feeding on sediments that had settled on another diver's fins during the mirror trials (Fig. 6). One of our divers (Aya Konstantinou) rested on the sand in front of a feeding swarm of juvenile Plotosus. As the swarm went over her legs, she could feel some of the fish picking at her diveskin.

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Plotosus individuals also clean each other (intraspecific cleaning, Fig. 19). The host fish opens its operculum, and the cleaner puts its snout into the gill chamber, apparently removing parasites, commensals, 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 in PNG. The divers found one adult each in two separate caves, over 1 m apart, about 1 m back into the cave, at a depth of about 22.5 m. The solitary adults retreated deeper into the cave when divers entered with flashlights.

Mating/Spawning: One of us (MJS) videotaped group spawning of Plotosus lineatus (10+ individuals) under a coral ledge in Indonesia.

DISCUSSION

Species identification: Yoshino and Kishimoto (2008) separated as a new species, Plotosus japonicus from P. lineatus, by its having differences in certain morphological characters, including a more complex dendritic organ with two dermal folds. The original illustration of P. lineatus by Bleeker, 1862 (synonym "Plotosus arab") in Indonesia shows the dendritic organ below the anus (Fig. 20b), but the presence or absence of the dermal fold can not be determined. In Yoshino and Kishimoto (2008) the dendritic organ appears to be folded upward to show the underlying dermal folds in P. lineatus (absent in P. japonicus) (Fig. 21). In our Fig. 19 (Douglas Seifert, Indonesia), the dendritic organ of P. lineatus is visible but not clearly defined. The question of identification of these two similar species by divers can not be resolved based on photographs or videos, but at this time must be based on geographic location, except in areas of Japan where they are sympatric. In our study, the species shown in Figures 8, 15-17 is identified as Plotosus japonicus, based on the locality.

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Geographic range and dispersion:

The unique swarming behavior of the juveniles of Plotosus lineatus, Plotosus japonicus, and Pholidichthys leucotaenia may explain their apparently limited ability to reach certain areas isolated by deep water. In our studies, these three species were absent from Mary Island (SOL) and Sipidan (Borneo), both surrounded 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 similarity between juveniles of Plotosus lineatus, Plotosus japonicus and Pholidichthys leucotaenia is emphasized. Both have similar color patterns, form swarms, and swim long distances, often in huge formations (Fig. 22). However, Plotosus juveniles can be differentiated by their barbels and their bottom-feeding behaviors, whereas Pholidichthys juveniles lack barbels and are plankton-feeders. Even experienced divers often have difficulty distinguishing between juveniles of these two species in different genera.

In Batesian mimicry, the mimic (Pholidichthys leucotaenia) may be quite abundant throughout its distribution if the model (Plotosus lineatus) is extremely venomous and therefore unpalatable, or if the mimic is unimportant as prey (Randall 2005). Plotosus lineatus is notorious for being highly venomous. Three sharp, rigid spines, one in front of the first dorsal and each pectoral fin, can be locked into place when extended, making the fish especially dangerous. The venom glands, located along the dorsal and pectoral spines, inject venom (plototoxin) when the serrated spines penetrate a person's skin, causing great pain (Herre 1949; Halstead 1988). The venom is neurotoxic, hemolytic, vasoconstrictive, and dermonecrotic. In addition, proteinaceous crinotoxins are secreted by epidermal cells (Shiomi et al. 1988). These lethal, hemolytic and edema-forming toxins, produced when the fish is excited or threatened, provide Plotosus with additional protection from predation.

Numerous incidents of severe stings have been reported by those in the field (Burgess 1989). During our study, Capt. Sam Kivia reported that in his village of Ulamona, with 1000+ inhabitants, on the northeast side of Garove Island, PNG, a number of villagers have received painful stings from P. lineatus in shallow water but no deaths resulted. To alleviate the pain, the injured villagers drank juice from coconuts and wrapped the wound in young coconut leaves. This is the first report of using coconut juice and leaves to alleviate the symptoms. In Walindi, PNG, a diver and dive boat crew member, Nelson Lisian, told us that he remembers vividly as a young boy (8 or 9 years old) being stung on the bottom of his foot by a tiny lone catfish in a tide pool, after he dispersed a catfish "ball." His leg swelled up, he couldn't walk and stayed home in bed for a week.

Predators: We did not observe predators feeding on Plotosus (although pomacentrids, guarding their demersal eggs on dock poles or rocks, may attack and chase Plotosus swarms). In Okinawa, however, one of us (EC) learned from Minoru Toda, chief aquarist at the Okinawa Churaumi Aquarium, that they regularly feed their squid, Sepioteuthis lessoniana, on easily netted catfish balls common around Okinawa (Toda 1985). Also Dr. Tetsuo Yoshino confirmed this feeding behavior in his laboratory at the University of the Ryukyus where he is currently studying S. lessoniana, which is probably a complex of three species, all of which readily but carefully feed on Plotosus, avoiding the three venomous spines.

On rare occasions, predators have caught small, juvenile Pholidichthys. On one occasion at dawn, one of our videographers (M. Moltzer) was waiting for the emergence of a Pholidichthys swarm from its burrow and caught on film a shrimp, Periclimenes tenuipes, which apparently was also waiting for the juveniles to emerge, catch and eat a juvenile convict fish. Of the numerous swarms we observed, only once did one of us (EC) witness a serranid, Cephalopholis cyanostigma, watch a large, elongated swarm of juvenile Pholidichthys, then dart into the swarm, catch one fish and eat it. There is ample evidence that Pholidichthys leucotaenia swarms are protected by Batesian mimicry of the highly venomous juvenile swarms of Plotosus (Clark et al. 2006)..

Collective mimicry: Hass (1945) suggested the term "collective mimicry" for an "aggregation of numerous individuals" that acts as a "superindividual". In the Red Sea, Knipper (1955) reported an example of "collective mimicry" in which Plotosus appeared to mimic a sea urchin. Magnus (1967) also became fascinated with a catfish "ball" with the tails positioned outward and resembling a sea urchin, but disagreed with Knipper on calling this formation collective mimicry. In the Gulf of Mexico, Springer (1957) observed a compact "school" of Jenkinsia that resembled a ray. He referred to this phenomenon as an example of "collective mimicry" but noted that he used this term only to refer to the appearance of the aggregation to a human observer. We have seen collective group behavior ("superindividuals" per Hess 1945) in Pholidichthys when the swarm leaves the reef and forms changing shapes that resemble different large organisms such as giant fish, whales, or sea snakes. This group behavior may protect the swarm from open water predators. In Plotosus, we have not observed "collective mimicry" behavior in large swarms in open water, but the juveniles do form dense balls on or near the substrate (see "Swarming" below).

Swarming: In contrast to schooling behavior, few fishes form tight swarms of individuals, such as we found in Plotosus and Pholidichthys (Clark et al. 2006). Plotosus juveniles near the substrate can also form rounded aggregations that may resemble sea urchins ("collective mimicry"); these "catfish balls" (Fig. 23a-b) are called gonzai dama in Japanese. This dense ball-shaped swarm forms soon after hatching (Moriuchi & Dotsu 1973), indicating that the swarm formation is initiated by sibling recognition associated with olfactory and visual cues (Kinoshita 1975; Hayashi et al. 1994). A mixture of phos-phatidylcholine molecular species in the skin mucus, released into the seawater, is thought to be the 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 synchronously. Although some schools (e.g., sardines) may form "bait balls" that look like swarms, they do not touch each other. The difference between a "swarm" and a "school" is that in a swarm the individuals can be touching each other, whereas in a school the individuals are staggered, not lined up and 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: Sato (1938) studied the role of vision in the formation of aggregations of "P. lineatus" (now P. japonicus) in an aquarium. When a single fish was transferred into an aquarium with a mirror against one side, the fish swam to the mirror, zigzagging across the mirror surface with its face close to the glass. An increase in the number of fishes decreased the intensity of their reaction to the mirror. We observed this group behavior with a mirror in Vea Vea Bay. The actively-feeding swarm paid little attention to the divers or mirror until individual juveniles bumped into the mirror, looked at it and then changed their direction of movement. Then the entire swarm rapidly changed its direction, swimming parallel to the mirror (or away from it) and continued feeding. Until the fish physically contacted the mirror, they looked toward the swarm in the mirror and behaved as if the mirror image was part of the group.

Inter- and intraspecific cleaning: Plotosus juveniles feed primarily on epibenthic invertebrates in organically rich sand, in algal beds with extensive surface area covered with epizootic and epiphytic organisms, and occasionally on invertebrates on substrates between reef corals. They are also facultative cleaners of other fish and artificial surfaces. Although Cote (2000) reviewed cleaning symbioses in 97 species of fishes (and 34 species of crustaceans), Plotosus was not included as a facultative cleaner (one that gleans only a small part of its food by cleaning as juveniles). Obligate cleaners obtain an average of 85% of their food, primarily ectoparasites, from their symbionts and often are marked with bright lateral stripes. In Plotosus, the lateral stripe may be more important in swarming behavior and mimicry than in cleaning behavior.

Masuda et al. (1975) briefly mention that Plotosus "sometimes cleans other fish." This is the first reference world-wide to Plotosus as a cleaner. In the expanded version of the comprehensive list of fishes in Japan, Masuda et al. (1984), they do not mention this cleaning behavior. In our studies one of us (YK) photographed different species of fish being cleaned by Plotosus japonicus in Izu Peninsula, Japan (Figs. 15-17). This behavior may be common but may have been overlooked previously by divers.

In Indonesia, Douglas Seifert recently observed and photographed P. lineatus juveniles cleaning the gills of other juveniles (Fig. 19). In a tightly-packed aggregation, the snout of the cleaner is inserted into the gill chamber of the fish being cleaned, which has its mouth agape. Intraspecific cleaning is very rarely reported in fishes, although it is a common behavior in mammals, especially during grooming and courtship behavior. In this study we provide photographic evidence of intraspecific cleaning in Plotosus for the first time.

Adults and sub-adults: Plotosus lineatus adults are solitary or occur in small groups up to 20. Adults are nocturnal and known to hide under ledges during the day, unlike the juveniles and sub-adults that feed actively during the day and hide at night in natural or man-made objects. In Mabul, Malaysia, sub-adults retired into a tire at dusk and emerged again at dawn (Fig. 24a-d).

Spawning: According to Thresher (1984), Plotosus off Japan spawns in late spring and early summer, at which time the males construct nests under rocks and other large pieces of debris on a sandy bottom. After spawning, the male also guards the 300-700 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 larvae 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 just after spawning. This was the only record of predation on eggs that we observed in the natural environment.

After hatching, the juveniles stay on the bottom and start swarming within a week (Moriuchi & Dotsu 1973). When two schools are mixed, the juveniles return to the original school, indicating that the chemical cue is specific, allowing individuals to discriminate their own school from others (Kinoshita 1975). However, the sensitivity to the odor of swarm mates may be somewhat plastic, based on the genetic variation found within the school (Iwasaki 1995), indicating that individuals can 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 and other marine genera in Plotosidae (Cnidoglanis, Euristhmus, Paraplotosus) (Lanzing 1967). Plotosus papuensis Weber, 1910, apparently has recently entered freshwater rivers in New Guinea (formerly Irian Jaya) and still has a dendritic organ (Burgess 1989; Ferraris 2007). One morphological difference separating P. lineatus and P. japonicus is the complex structure of the dendritic organ. We have become interested in the dendritic organ and suggest that this structure be studied further in the catfishes.

ACKNOWLEDGEMENTS

We extend special thanks to our volunteer research divers, whose observations, photographs and video provided data for this study in PNG and Mabul: Anne Doubilet, Jessica Goldstein, Bob Halstead, Martha Kiser, Hanna Koch, Steve Kogge, Aya and Tak Konstantinou, Zen Kurokawa, Mopsy Lovejoy, Maya Moltzer, Jack Nelson, Val Palubok, John F. Pohle, Jann Rosen-Queralt, Judith Rubin, Pat and Susan Shaw, David Shen and Patty Sturtevant. John F. Pohle organized our dives and gave considerable help in mapping and GPS locations. Bob Halstead, the most knowledgeable diver and author of fishes in PNG waters, provided exceptional logistical help and many keen observations during and after our boat charters in PNG. We appreciate the good care of the crew of the Febrina in PNG, especially the valuable help of the crew divers, Captain Sam Kivia, Alfred George, Josie Waiwai, Martin Giru, and Nelson Lisian, who contributed data for our research and spent many hours assisting us underwater. The staff at the dive center at Sipidan Water Village, Mabul, Malaysia, was very helpful. Lawson Mitchell, Creative Director, Mote Marine Laboratory, produced the maps and the layout of the figures. John Ares provided photographs and observations of a large swarm of Plotosus lineatus in Indonesia. Yeang Ch'ng photographed P. lineatus swarming over to diver, Eric Cheng, in Raja Ampat, Indonesia. Eric Cheng provided close-up images of Plotosus. Douglas Seifert provided photographs of P. lineatus cleaning each other. Bill Macdonald sent valuable video of his independent observations. Diane and Mark Littler identified the green algae and seagrasses at Vea Vea, PNG. Carol Miller translated pertinent articles from German. Bev Rodgerson, Rachel Dreyer, Cathy Marine, Patricia Tuccio, Lance Ong and Joan Rabin gave valuable help with the editing and preparation of this manuscript. We thank the two reviewers and Helen Larson for their detailed comments and suggestions that considerably improved this final version of this paper. Susan Stover, Mote librarian, gave us much help in tracking down obscure references. Patricia Tuccio provided numerous references and discussions on swarming behavior. We appreciate the support of the Mote Scientific Foundation. East Tennessee State University provided partial travel support for DRN. This study was administered through the University of Maryland Foundation.

Received: 22 February 2011 - Accepted: 12 August 2011

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Eugenie Clark (1), Diane R. Nelson (2), Mary Jane Stoll (3) and Yasumasa Kobayashi (4)

(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: yoppe@mote.org

(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
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Author:Clark, Eugenie; Nelson, Diane R.; Stoll, Mary Jane; Kobayashi, Yasumasa
Publication:aqua: International Journal of Ichthyology
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Date:Oct 15, 2011
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