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aqua, International Journal of Ichthyology

Mimicry of a Bean Seed by the Amazonian Aspredinid hypsiura (Kner 1855), with Notes on Vegetative Camouflage by Fishes

Tyson R. Roberts Smithsonian Tropical Research Institute, Panama; and Institute of Molecular Biosciences, Mahidol University, Salaya, Thailand. E-mail [email protected]

Received: 16 January 2013 – Accepted: 22 April 2015

Abstract. Résumé can modify its typically bunocephalid or Amaralia hypsiura est en mesure de modifier sa forme typ- aspredinid-catfish shape, hiding many of its features includ- ique de Bunocéphalidé ou d’Asprédinidé, en cachant une sé - ing all of its fins, so that it resembles a large bean or seed of rie de ses caractéristiques, y compris toutes ses nageoires, de the spermatophyte family Leguminosae or Fabaceae. This is façon à ressembler à un grand haricot ou à une semence de la accomplished mainly by adpressing both pectoral fins and famille des Légumineuses ou Fabacées. Il y parvient surtout folding the tail and caudal fin tightly around one side of the en accolant ses deux pectorales et en repliant la queue et la body and head. In so doing, Amaralia radically transforms it- caudale fermement autour de la partie latérale du corps et de self from the bilaterally symmetrical form of a vertebrate an- la tête. Ce faisant, Amaralia se transforme radicalement, pas- imal into the radially symmetrical form of a seed. The fish sant de la forme de symétrie bilatérale d’un vertébré à then remains motionless until it unfolds itself. While mimic- celle de symétrie radiale d’une semence. Le poisson reste alors ry of plant parts and camouflage to resemble plants or woody im mobile jusqu’à ce qu’il se déploie. Alors que l’imitation de background is well known in fishes, mimicry of a seed appar- parties de plantes et le camouflage évoquant des plantes ou un ently has not been reported previously. It possibly facilitates fond de bois sont bien connus chez les poissons, l’imitation prey capture by Amaralia, which feed on the large yolky eggs d’une semence ne semble pas avoir été rapportée jusqu’ici. of orally-brooding or otherwise parentally-guarding loricariid Cela facilite peut-être la capture des proies pour Amaralia qui . It might also be involved in predator avoidance. se nourrit des grands oeufs de Loricariidés incubateurs buc- Mimicry and camouflage involving vegetation is now known caux ou protecteurs parentaux. Ce phénomène pourrait aussi in a wide variety of freshwater and marine fishes. concerner l’évitement des prédateurs. L’imitation et le camou- flage impliquant des végétaux sont à présent connus pour un Zusammenfassung grand nombre de poissons marins et d’eau douce. Amaralia hypsiura ist in der Lage, die für Asprenididen oder Bunocephaliden typische Form abzuwandeln; die Flossen Sommario und andere Merkmale sind dann verborgen, sodass der Wels Amaralia hypsiura può modificare la sua tipica forma di einer großen Bohne oder anderen Samen der Hülsenfrüchtler pesce gatto aspredinide o bunocefalide nascondendo molte (Leguminosen oder Fabaceen) ähnelt. Erreicht wird das dei suoi tratti morfologici, comprese tutte le pinne, così da as - dadurch, dass beide Brustflossen an den Rumpf gepresst und somigliare a un grande fagiolo o a un seme di leguminosa o Schwanz und Schwanzflossen dicht um Flanken und Kopf di fabacea. Questo avviene principalmente ripiegando stretta- gefaltet werden. Der Fisch bleibt dann so lange bewegungs- mente le pinne pettorali, la coda e la pinna caudale attorno ad los, bis er sich selber wieder entfaltet. Während Mimikry von un lato del corpo e alla testa. In questo modo Amaralia si tra- Pflanzenteilen und Tarnung durch Ähnlichkeit mit Pflanzen sforma da un animale vertebrato a simmetria bilaterale ad un oder hölzernem Untergrund von Fischen seit längerem es sere a simmetria radiale a forma di seme. Il pesce rimane poi bekannt sind, wurde über Mimikry von Samen bisher nicht im mobile fino a quando non si dispiega. Mentre l’imitazione berichtet. Möglicherweise wird der Beute-Erwerb von Amar- delle parti di piante e il camuffamento per assomigliare a alia hypsiura dadurch erleichtert, denn die Vertreter dieser Art piante o a uno sfondo legnoso sono ben noti nei pesci, il mi - ernähren sich von Eiern der maulbrütenden oder anderweitig metismo di un seme non è stato finora mai segnalato. Proba- von Eltern behüteten Vertreter der Loricariiden (Har- bilmente facilita la cattura delle prede da parte di Amaralia, nischwelse). Wahrscheinlich hilft es ihnen auch zu vermei- costuituite da grandi uova ricche di tuorlo dei pesci gatto den, dass sie selber zur Beute werden. Mimikry und Tarnung Loricaridi che hanno l’abitudine di covare le uova in bocca o in Bezug auf Vegetation ist jetzt von einer Vielzahl von Süß- di proteggere in altro modo la covata. Questo comportamen- und Salzwasserfischen bekannt. to potrebbe anche essere un meccanismo di difesa dai preda-

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Mimicry of a Bean Seed by the Amazonian Aspredinid Catfish Amaralia hypsiura (Kner 1855), with Notes on Vegetative Camouflage by Fishes

tori. Il mimetismo e il camuffamento in elementi vegetali è sometimes the ability to change coloration. The small diffuso in un’ampia varietà di pesci marini e d’acqua dolce. Amazonian characiform fish ele- gans turns bright green when it perches immobile on INTRODUCTION green plant stems or leaves so that it becomes nearly The aspredinid Amaralia Fowler 1944, gener- invisible (Zuanon et al. 2006). This again is best re- ally treated as including only a single , is widely garded as camouflage or protective coloration rather distributed in the Amazon and Plata basins. An un- than mimicry. described species reportedly occurs in the Parana and Young Amazonian pacu, Myleus sp., have modified Paraguay watersheds of the Plata basin (Friel 1994: coloration and behaviour and deep-bodied morphol- 83) and has even received a name, but the abstract in ogy enabling them to resemble darkened dead leaves which it is mentioned is not available for purposes of and fragments of branches. This has been interpreted zoological nomenclature (Friel 1992). The only avail- as protective camouflage. The coloration, similar to able nominal species taxon within the genus is Ama- that in juveniles of many Serrasalmidae, involves a ralia hypsiura (Kner 1855). The species is represented uniformly dark coloration of the entire head and by relatively few museum samples from widely scat- body and basal portions of the dorsal, anal, and pelvic tered localities in Bolivia, Brazil, Colombia, Ecuador, fins, while the rest of these fins, the pectoral fin, and and Peru. the caudal fin are entirely clear or colorless, thus ef- Biological camouflage is the ability of a plant or an fectively invisible. The little fish tend to occur as iso- animal to blend with its vegetable, animal, or inani- lated individuals rather than in schools characteristic mate background, usually to hide its presence from of the young of many species in other characoid taxa. potential predators or prey. In some instances both They remain relatively motionless, typically with the advantages are involved. Mimicry is when an animal head slightly down and the body slightly oblique, in or plant resembles another creature or inanimate ob- a rather uncharacteristic posture for fish (Zamprogno ject, for comparable advantages. Like camouflage, & Andrade 1986). mimicry often involves morphological and physio- Reported here for the first time is a fish that mimics logical modifications in body shape, coloration, color a seed. This came to my attention when a single spec- pattern and color change as well as in behavior, in- imen of Amaralia hypsyura was collected by seine in cluding but not limited to habitat selection, body the Rio de Las Piedras, a tributary of the Rio Madre posture, and locomotion or other movements. de Dios in the Upper Amazon of Peru near Puerto Resemblance to plants and plant parts is well docu- Maldonado. The specimen was collected in shallow mented in marine fishes and less well documented in water near the shore of the Rio de las Piedras a few freshwater fishes (Breder 1946; Randall & Randall km upstream from where it is entered by its tributary 1960; Randall 2005). The selective advantage of such the Rio Pariamanu, on 15 Sep 2010. camouflage apparently is most often defensive, i.e. to The specimen, now in the fish collection of the escape detection by predators, but it may also be of- Smithsonian Tropical Research Institute catalogued fensive, to hide a predator from its prey, or in some as STRI 08513, is 41.0 mm standard length. This is species, it could be both. The Amazon provides nu- far below maximum size for the species, and it is pre- merous examples of freshwater fishes that hide sumably immature. Sex undetermined. The portion among plants. At least three Neotropical catfish fam- of the fish that mimicked a bean, from snout tip to ilies, , Auchenipteridae, and Loricari- vent, is 25 mm long and 15 mm wide. Its stomach idae, include numerous species that partially resemble contents consisted of a uniform oval mass of partially tree trunks, branches or leaves. All or nearly all of digested orange colored yolk. these examples probably should be regarded as cam- ouflage rather than mimicry. The nandid Monocir- Amaralia Fowler 1954 rhus polyacanthus mimics dead leaves (Eigenmann & Allen 1921; Catarino & Zuanon 2010). So far as I Amaralia Fowler, 1954: 40 (type species by original am aware, no species or generic identification of the designation and monotypy hypsiura leaves mimicked has been made. Monocirrhus and Kner 1855). virtually all of the neotropical catfishes that hide among plants are essentially brown or brownish, of- Amaralia differs from all other aspredinids in that ten with a mottled or otherwise disrupted color pat- the abdomen is lengthened at the expense of the tail tern. Such fishes tend to have variable coloration, and and is distensible; dorsal fin greatly reduced with a

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very short stout spine and only 2 or 3 short rays (vs. logged dead seed completely fooled me. The incident dorsal fin relatively large with 3 or more rays) (Friel occurred following a seine haul on the Rio de las 1994: 47); and caudal peduncle deep and laterally Piedras, about an hour by motor boat upstream from compressed, with a low mid-dorsal tuberculated its mouth into the Rio Madre de Dios at Puerto Mal- ridge. Caudal fin with 5+4=9 principal fin rays and donado, Peru, on 19 January 2010. Felix Yucra, with procurrent rays thickened and S-shaped unlike whom I engaged to help me do an ichthyological sur- those in other aspredinids (Friel 1994: 82). Postab- vey of the Rio de Las Piedras and its tributary the Rio dominal part of body or tail exceptionally flexible. As Pariamanu, handed me a seemingly inanimate semi- in Bunocephalus (Friel 1994: 193, fig. 39) and most flattened oval object and asked “is this a fish?” I ex- aspredinids, body extensively covered with unculifer- amined the object closely, turning it over several ous tubercles. times, observing all aspects in good daylight at about Morphological modification of Amaralia are related 4 PM. Impressed by its symmetric oval shape and to two unusual adaptations, its characteristic egg-eat- strong resemblance to a dead water-logged seed, I ing or oophagy so far unknown in other aspredinids, pronounced it a seed. Noticing on the side of the oval and its ability to wrap the tail tightly around the sides what appeared to be the slightly raised edge of a seed of the abdomen, thus disguising its fish shape and coat and something lighter colored inside, I gently helping it to mimic a bean seed. Other buno- prized it open, fully expecting to reveal a seed leaf and cephalids have a less flexible tail that would prevent endosperm. To my amazement the prized edge them from doing this. straightened out into a fish tail complete with rayed In resting or immobilized Amaralia the dorsal fin is caudal fin, and only after that did the familiar shape depressed, so that it is virtually invisible and cannot of an aspredinid snout with its tiny eyes and short be detected by moving a finger gently forwards over barbels, and the dorsal, pectoral, pelvic, and anal fins the dorsal surface. When specimens are preserved the become apparent (Fig. 1). To avoid loss of the unique dorsal fin usually becomes erect and firmly locked in specimen it was immediately preserved. No pho- place. It is then obvious despite its very small size. It tographs were taken during the short time it resem- seems possible that in seed-mimicking mode the dor- bled a seed. sal fin with its spine may be withdrawn entirely below The following points should be noted with regard the skin. to the seed-like object I had held in my hands. Until Knobby skull ornamentation well developed, dorsal its tail was prized open, it remained completely im- surface of head rugose. This ornamentation pattern is mobile despite the handling it had been subjected to due to “bony knobs which often form above bifurca- by Felix and me. It was somewhat depressed or flat- tion points of the lateralis system of the skull.” tened but relatively thick and otherwise perfectly oval Among Aspredinidae this pattern is most highly de- in shape in its dorsal and ventral aspects (and thus veloped in Bunocephalus verrucosus and Amaralia hyp- completely unlike the relatively elongate shape of the siura (Friel 1994: 30). Coracoid processes of pectoral actual fish). What turned out to be the dorsal and girdle readily visible as prominent rib-like structures ventral or abdominal surfaces of the fish were nearly on the sides of the abdomen (typical for aspredinids). identical in their oval shape, coloration, and finely One of these coracoid processes apparently is covered granulated surface. There were no signs of eyes, when the tail is tightly wrapped around one side of mouth, barbels, epidermal knobs, or fins. The lateral the body. It is unclear how the process of the other surface of the head, abdomen and tail formed the side is hidden. It seems that the other bony knobs thick flattened circumference of the oval. The dull vary in the extent that they project from the body. brownish or tan seed-like color was similar dorsally Perhaps they also can be can be voluntarily exposed and ventrally. When gently squeezed the object felt or retracted below the skin. When the 41.0-mm alco- squishy or spongy like a dead waterlogged seed but hol preserved specimen was dried a bit, the tubercles remained immobile. on the dorsal surface of the head became much more Steps were taken after observation of this specimen pronounced than they are in Fig. 1b. to obtain additional relevant observations in the field. The large seine net in which the specimen was caught OBSERVATIONS (Fooled by a Fish) – Figs 1-3 was carefully searched for more specimens and for Only a single seed-mimicking A. hypsiura was ob- comparable seeds from actual plants, and several served by me, and it was not photographed in mim- more sweeps were made with it in the area to no avail. icry mode. Its initial resemblance to a large water- No additional specimens of Amaralia were collected

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Mimicry of a Bean Seed by the Amazonian Aspredinid Catfish Amaralia hypsiura (Kner 1855), with Notes on Vegetative Camouflage by Fishes

during the 14 days of the survey, nor were seeds re- Peeling back the abdominal wall of the Amaralia sembling the fish found. specimen from the Rio de las Piedras revealed an oval An attempt was made to recreate the bean mimicry mass of bright orange yolk 13 mm long and 15 mm position observed in the living fish by manipulation wide (Fig. 2). Horizontal hemisection of the mass of the preserved specimen. The part of the body, from with a scalpel revealed a uniform or homogeneous the snout tip to the vent, involved in mimicking a composition (with no sign of individual eggs). This bean, is 25 mm long, 15 mm wide, and a maximum presumably is the partially digested remains of a sin- of 11 mm deep. The tail, its full length from vent to gle meal of loricariid eggs. tip of caudal fin 23 mm, could be bent around one Twelve specimens 70-200 mm standard length were side of the abdomen and adpressed pectoral fin, effec- obtained from aquarium fish traders and maintained tively hiding them, until the tips of its caudal fin alive in my apartment in Iquitos for several weeks in reached the corner of the mouth. This left the pec- February and March 2010, in the hope of observing toral fin of the opposite fully exposed, but it was them mimicking seeds. They were kept in plastic somehow hidden when I observed it alive in bean lined wooden flat boxes 37x37x8 cm in standard use mimicry mode. Other problems of concealment ap- in the Iquitos aquarium trade in three groups of four parently solved by the fish in bean seed mimicry specimens according to their stated collection locali- mode involve the eyes, barbels, keratinous knobs, and ties Rio Itaya, Rio Momon, and Rio Uritiyacu. The the dorsal, pelvic, anal, and caudal fins. following observations were made on behavior of these three lots of A. hypsiura which was essentially similar. The Itaya lot included one Bunocephalus cora- coideus. None of the specimens was observed to change from its catfish form into the seed or bean form reported above. Immobility: Individually and collectively the fish in each flat would remain in fixed positions on the bot- tom, isolated from each other, lightly touching each other, or piled up on each other for periods as long as six to 12 hours. Occasionally the three or four fish in each lot would separate widely, sometimes one occu- pying each corner of the flat. More often they were scattered seemingly randomly or formed a pile. Sud- den splashes in the flat would indicate that at least one fish had made a sudden movement, but such oc- curred at infrequent intervals and were not visually observed. Movement of one or more fish would result invariably in a new immobile configuration of all of them. The Bunocephalus often remained immobile for equally long periods. Piling up: While individual fish often remained by themselves immobile on the bottom of a flat for pro- longed periods, as often two, three or four fish would pile up on each other and remain in the same posi- tion for periods of six to 12 hours. The piled-up con- figurations were very diverse, seemingly haphazard, but with substantial fin and body contact among in- dividuals. The Bunocephalus often participated in the pile-ups. Maintenance of upside-down position: When gen- Fig. 1. Amaralia hypsiura, 41.0 mm standard length, Rio de las Piedras near Puerto Maldonado, Peruvian Ama- tly overturned and released so that the belly was up- zonas. A. lateral view; B. dorsal view; C. ventral view. This wards, individual fish would remain immobile in up- is the specimen I mistook for a bean seed when it was col- side position for periods up to several hours. On one lected in the Rio de las Piedras. Photo by T. R. Roberts. occasion a group of three individuals left to their own

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devices piled up on top of each other with the upper- contrast was the response of the Bunocephalus, which most individual upside down (i.e., belly-up), and could only bend its tail partially compared to the maintained this position for at least six hours. Other- Amaralia, and when gently replaced in the water wise fish left on their own maintained upright posi- would dash about madly for several seconds. tions. When gently turned upside down, the Buno- Shedding of keratinized epidermis and color cephalus would immediately right itself. It was never change: Periodical shedding of the keratinzed epider- observed in an upside-down position. mis is characteristic of Aspredinidae (Friel, 1994). In- Thigmotropism: Thigmotropism is when an organ- dividual A. hypsiura fish occasionally shed a thin layer ism moves, remains stationary, or grows in response of the epidermis. Unlike in some amphibians and to touch or contact stimuli. Most fish are bottom snakes and reportedly in some other aspredinids in dwellers, and the commonest thigmotropism among which the epidermis is shed as a unit, the shedding them involves contact with the substrate. This prob- observed in my captive aspredinids resulted in nu- ably is true of A. hypsiura. In the specimens observed merous small flakes of discarded epidermis. The in captivity, this substrate was the plastic lined bot- process occurred at night and apparently required tom of a wooden flat. In nature the substrate presum- several hours. At the end of the shedding the fish was ably is often the wood of a tree trunk or branch. changed from an overall dark brown or chocolate Whether Amaralia stay inside hollowed out tree brown with some underlying darker markings to trunks, as do some ageneiosid, auchenipterid and loricariid catfishes, apparently is unrecorded. They may also seek contact with dead leaves, especially large broad ones. Catfish thigmotropism may be me- diated mainly by the barbels, the ventrally-located paired fins and caudal fin, or by the dorsal and ventral body surfaces as a whole. Many catfishes avoid body contact with other individuals of the same species, but intraspecific body contact thigmotropism is high- ly developed in A. hypsiura, which spend much of the time piled up on each other. In this species the struc- tures most important in thigmotropism or touch be- havior appear to be the pectoral and caudal fins and the body surface generally. The barbels apparently are Fig. 2. Amaralia hypsiura, 41.0 mm, with abdominal wall unimportant. peeled back to reveal an oval mass of digested yolk. Photo Tail-bending: Individual fish would sometimes re- by T. R. Roberts. main with the body fully extended for prolonged pe- riods of time, then respond to a light touch of the fin- ger by immediately coiling the tail loosely around the body. Bunocephalus can bend the tail, but not nearly so much as Amaralia, and they cannot bend it around the body like Amaralia. Amaralia but not Buno- cephalus are capable of bending the tail in an S-shape, or of bending the tail so that it nearly doubles around itself and is applied to one or the other side of the head and abdomen. In A. hypsiura this may con- tribute to the ability of a fish to disguise its true shape and enhance its camouflage without resulting in true mimicry. If lightly touched or gently removed from the water and immediately replaced, the response of Fig. 3. Seeds of Mucuna cf. fawcettii from the Upper Ama- zon of Peru. These resemble the specimen in Fig. 1 when all twelve A. hypsiura was to bend the tail. This had it was in seed-mimicking mode. The granular surface of the immediate effect of lessening their overall fishlike the seeds and the color of some of them as well as their outline. Sometimes the outspread pectoral fins were overall shape is closely similar to the tuberculation and adpressed, which also lessened the fishlike outline. coloration of the Amaralia. Photo courtesy of P. Mikkel- Otherwise the fish remained immobile. In marked son, SeaBean.com.

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Mimicry of a Bean Seed by the Amazonian Aspredinid Catfish Amaralia hypsiura (Kner 1855), with Notes on Vegetative Camouflage by Fishes

nearly black with prominent silvery or pale whitish groups of twig- and branch-mimicking insects that markings on the top of the head and on the tail. The evidently have evolved through a stage of camouflage four fish reportedly collected in the Rio Uritiyacu all to one of genuine mimicry. Camouflage usually is had the same black and silvery coloration when first possible only in the presence of the appropriate back- observed, so that initially they looked like they might ground. In mimicry the object resembled need not be belong to a different species. Only after a fish from present. Instances of camouflage in fishes evidently Momon shed its cuticle did it become clear that the greatly outnumber those of mimicry. Mimicry of a specimens from all three rivers were the same species. seed by a fish is perhaps very unusual. The Uritiyacu specimens did not attain the more The primary importance of camouflage and mimic- usual brown overall color associated with a mature ry in Amaralia may be to hide them from potential cuticle during the observation period. No short-term predators. The ability to hide may also contribute to color change was observed in any other of the indi- their success as predators on the eggs of egg-brooding vidual fish. loricariids. Observations in support of either hypoth- Sound production: is able esis are presently unavailable. Observations of stom- to make a fairly loud grating or grinding noise, appar- ach contents of A. hypsiura in museum collections in- ently by stridulation of its pectoral fin spines. Sound dicate that they may feed almost exclusively on the production was not observed in my captive Amaralia. eggs of loricariids (Friel 1994: 59, 197, fig. 43). It has not been determined whether the eggs are those of DISCUSSION the buccal egg guarding Loricariinae, of the substrate Given the lack of photographic evidence, this report laying Hypostominae, or of both kinds. If the seed of seed mimicry may be met with scepticism. Never- mimicry of Amaralia permits it to deceive the lori- theless, I prefer to report the phenomenon as it was cariids on the eggs of which it preys, then it represents observed and interpreted by me, with the expectation an instance of aggressive mimicry. Predators of Ama- that this unusual and possibly unique behaviour of ralia have not been identified but it seems likely that Amaralia will be fully confirmed and more adequate- the seed mimicry of Amaralia. also is defensive. ly documented by future investigations, which are Seed mimicry of Amaralia evidently is facultative, in more likely to occur if the facts are recorded. that the fish apparently can change rapidly from a My observations on captive specimens in Iquitos fish-like shape to a seed-like shape and back again. suggest that the usual cryptic behavior of Amaralia This statement is qualified because although the involves camouflage so that it resembles a back- rapid change from seed-like to fish-like was observed, ground of dead wood. Well known ichthyological ex- the change from fish-shape to seed-shape was not. amples of camouflage are provided by flatfishes, col- Immobility itself can serve to hide an organism oration of the dorsal surfaces of many of which from a potential predator or prey. In Amaralia it may changes to blend with differently colored substrates also be associated with a relatively low metabolic ac- on which they stay. The deceptive coloration of flat- tivity and prolonged fasting, with intermittent peri- fishes is effective partly due to their extremely flat- ods of activity, especially when taking food. Inactivity tened morphology and the behavior common to and fasting may be preadaptive for the evolution of many species of burying themselves in the substrate. camouflage and mimicry in many other fishes as well. Fishes with cryptic resemblances to plants or plant Loss of the alarm cells and fright reaction (Friel, parts are well known (Breder 1946; Randall & Ran- 1994: 59) might be another characteristic of Aspre- dall 1960: Randall 2005). Objects likely to provide dinidae related to their immobility and supposed re- the background for the camouflage of A. hypsiura are duced metabolic activity. Loss of sound production, tree trunks or branches and large broad dead leaves. otherwise widespread in Aspredinidae, might also be Judging from these limited observations on Amar- related to the excessive immobility and advanced hid- alia, camouflage may be a precondition, preadapta- ing behavior of Amaralia. tion or intermediate stage for evolution of more ad- Although the Amazonian leaffish Monocirrhus poly- vanced forms of mimicry, such as leaf mimicry and acanthus mimics leaves and not seeds, a brief compar- seed mimicry. From this perspective it seems that ison of the behavioral and other attributes contribut- many if not all resemblances of neotropical catfishes ing to its mimicry with those of Amaralia is instruc- to wood or leaves should be considered as examples tive. I observed several hundred Monocirrhus main- of camouflage rather than mimicry. There do not tained in a large aquarium in Iquitos in February seem to be any catfish equivalents of the various 2010. The most obvious similarity in behavior is im-

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mobility. In Amaralia this is achieved while the fish in the water, and ate the ants which had been dis- are resting on the substrate, while in Monocirrhus it lodged. occurs while the fish are suspended in the water or Death feigning is a common form of mimicry in with only their median chin barbel (resembling a leaf- many vertebrates including humans, and can be ag- stem) barely touching the bottom. While in Amaralia gressive or protective mimicry. It is not so well known the orientation of the body is extremely variable but among fishes, but probably more widespread than re- nearly always horizontal or nearly so, the leaf fish ori- ported. Tiago Carvalho advised me he has observed ent uniformly with the body at an angle of about Amaralia engage in apparent death feigning (pers. 60% with the head downwards. Hundreds of fish commun., 30 Jan 2015). This agrees well with my similarly oriented at once is a striking sight. Such observations on captive Amaralia reported above, large aggregations, however, probably do not occur particularly about individuals remaining immobile under natural conditions. Monocirrhus are able to re- for many hours while lying upside down. This could main quite stationary in mid water without any evi- be either aggressive or protective death feigning in dent swimming movements. While Amaralia hypsiu- Amaralia. A classical example of aggressive death ra actively seeks contact with conspecifics, M. polya- feigning in fishes is that of the predatory Malawi ci- canthus avoids contact. The mimicry of Monocirrhus chlid Haplochromis livingstonii reported by McKaye is obligatory, rather than facultative: it cannot change (1981). its leaf-like shape into any other shape. Since it is a Leaf mimicry apparently has not been reported pre- percomorph rather than an ostariophysan, Monocir- viously in any anabantoid fish. This is surprising, rhus – like Amaralia – does not have alarm cells or since the shape and coloration of Ctenopoma acu- fright reaction. tirostre and C. oxyrhynchus (both endemic to the Con- Another noteworthy character of Monocirrhus rele- go basin) are nearly as leaf-like as those of Monocir- vant to the present discussion is remarkable variation rhus polyacanthus and much more leaf-like than in C. in overall coloration of the entire head, body and fins. kingsleyae or any other West African species. No ex- These may be uniformly rich brown, reddish brown, ample of camouflage or plant mimicry is known gray, beige, or even yellow (never green), like the among the numerous Amazonian species of the per- changing shades of dead leaves. Part of this variation comorph fish family Cichlidae. None of them resem- may be due to individual ability to change color, but bles a dead leaf like Monocirrhus polyacanthus, and it might also have a genetic basis, therefore represent- none have young that are green in color like the green ing color polymorphism. Amaralia also varies consid- color phase of the small darterlike crenuchid erably in color, depending at least partially on how re- . I observed green young of cently it has molted, although it does not exhibit the a cichlid Etroplus sp. dwelling amidst green sea weed range of hues present in Monocirrhus on reef flats in Sri Lanka in 1970. Several of the col- It is opportune to report here an instance of leaf orful endemic cichlids of the spring-fed clear-water mimicry in fishes that might otherwise remain un- Rivière Fwa in SE Congo have bright green young published. The following observations on mimicry of that hide in large masses of large aquatic green plants a dead leaf by an anabantoid of the genus Ctenopoma (mostly Vallisneria aethiopica) (Roberts & Kullander were reported to me verbally by a Ghanaian limnol- 1994). It is surprising that young neotropical cichlids ogist many years ago whose name I regretfully cannot are unknown to exhibit similar green cryptic col- recall. The fish, possibly C. kingsleyae, was observed in oration for hiding in the midst of green plants. Ini- a mangrove area of the Abi lagoon in southwest tially I hypothesized that Amaralia was mimicking Ghana near the border with Ivory Coast. It was float- the seeds of a particular species of plant, presumably ing on the surface on its side, with the uppermost side of the family Leguminosae or Fabaceae. A survey of partially out of the water and dried, resembling a websites and literature on seeds in the STRI Library dead fish or a floating leaf. At first it appeared to be in Panama did not reveal any exactly similar seeds, immobile and floating passively, but it then made but those of the Mucuna fawcettii Urban 1908 are slight swimming movements so that it came to rest reasonably close (Fig. 3). This bat-pollinated bush of against the leafy branch of a mangrove tree. At this the family Fabaceae is widely distributed in the Ama- point a number of ants walked from the branch and zon basin. I am now inclined to consider the alterna- leaves onto the exposed surface of the fish and started tive hypothesis for Amaralia of generical mimicry, i.e. feeding on the dried mucus. The fish then swam mimicry of a general type of bean seeds, averaging the slowly away from the branch, suddenly righted itself characteristics of a variety of seeds without precisely

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Mimicry of a Bean Seed by the Amazonian Aspredinid Catfish Amaralia hypsiura (Kner 1855), with Notes on Vegetative Camouflage by Fishes

matching any of them. In this way Amaralia could ef- leaf fish Monocirrhus polyacanthus (Perciformes: Polycentri- fectively mimic bean seeds in areas where a particular dae) in a terra firme stream in the Brazilian Amazon. species of bean does not occur. Neotropical Ichthyology 8 (1): 183-186. Finally, Flávio Lima has communicated to me that a EIGENMANN, C. H. & ALLEN, W. R. 1921. A leaf mimicking fish. Biological Bulletin 41 (5): 301-305. large Bunocephalus verrucosus he observed and collect- FOWLER, H. W. 1954. Os peixes de água doce do Brasil. Vol. ed in an igapó forest tributary of Lago Amanã in the 2. Arquivos de Zoologia (São Paulo) 9: i-ix+1-400. middle. Solimões basin in March 2003 looked strik- FRIEL, J. P. 1992. A phylogenetic revision of Amaralia, a ingly like the pit of a drupe or a peachstone. He is go- genus of oophagous banjo catfishes. Abstracts, Annual ing to prepare an account of it, and suggests that Meeting of the American Society of Ichthyologists and Her- mimicry of plant seeds might occur in additional As- petologists 1992, University of Illinois at Urbana-Cham- predinidae. paign, p. 104. FRIEL, J. P. 1994. A phylogenetic study of the neotropical banjo catfishes (Teleostei: Siluriformes: Aspredinidae) ACKNOWLEDGEMENTS Ph.D.thesis, Duke University, Durham, NC, 256 pp. Much of the success of my Rio de Las Piedras and KNER, R. 1855. Ichthyologische Beiträge [Subtitles I-III]. Rio Pariamanu fieldtrip of September 2010 was due Sitzungsberichte der Kaiserlichen Akademie der Wis- to the enthusiasm and skill of Señor Felix Manani Yu- senschaften. Mathematisch-Naturwissenschaftliche Classe 17: cra of Puerto Maldonado, who collected the unique 92-162, pls. 1-6. specimen of Amaralia hypsiura balled up like a bean MCKAYE, K. R. 1981. Field observation on death feigning: a seed and promptly brought it to my attention. Per- unique hunting behavior by the predatory cichlid, Hap- mission to collect fish specimens and export them for lochromis livingstonii, of Lake Malawi. Environmental Biolo- gy of Fishes 6: 361-365. identification and scientific study was granted by the PIRES, T. H. S., CAMPOS, D. F., RÖPKE, C. P., SODRÉ, J., AMA- Instituto de Investigaciones de la Amazonía Peruana DIO, S. & ZUANON, J. 2014. Ecology and life-history (IIAP) in Puerto Maldonado. Angel Aguirre of the of Mesonauta festivus: biological traits of a broad ranged and Library, Smithsonian Tropical Research Institute, abundant neotropical cichlid. Environmental Biology of Fish- helped access the scientific literature. Ruth Gazela es DOI 10.1007/s10641-014-0314-z Reina, Curator of the STRI fish collection, kindly RANDALL, J. E. 2005. A review of mimicry in marine fishes. sent the specimen to me in Thailand so that this Zoological Studies 44 (3): 299-328. study could be completed at the Institute of Molecu- RANDALL, J. E. & RANDALL, H. A. 1960. Examples of Mim- icry and Protective Resemblance in Tropical Marine Fishes. lar Biosciences. Paul Mikkelson of SeaBean.com Bulletin of Marine Science 10 (4): 444-480. kindly provided the photograph of Mucuna repro- ROBERTS, T. R. & KULLANDER, S. O. 1994. Endemic cichlid duced in Fig. 3. Heiko Bleher and Flávio Lima pro- fishes of the Fwa River, Zaire: systematics and ecology. vided useful discussion and suggestions. Ichthyological Explorations of Freshwaters 5 (2): 97-154 ZAMPROGNO, C. & ANDRADE, G. V. 1986. Camuflagem em REFERENCES jovens de pacu, Myleus sp. (, Myleinae). Re- BREDER, C. M. 1946. An analysis of the deceptive resem- vista Brasileira de Biologia 46 (2): 415-418 blance of fishes to plant parts, with critical remarks on pro- ZUANON, J., CARVALHO, N. & SAZIMA, I. 2006. A cha mae - tective coloration, mimicry and adaptation. Bulletin of the leon characin: the plant-clinging and colour-changing Am - Bingham Oceanographic Collection 10 (2): 1-49. mocryptocharax elegans (Characidiinae: ). Ich- CATARINO, M. F. & ZUANON, J. 2010. Feeding ecology of the thyological Exploration of Freshwaters 17 (3): 225-232, pl. 1.

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