aqua, International Journal of Ichthyology

Fooled by a fish: seed camouflage by an Amazonian banjo , verrucosus (Siluriformes: )

Flávio C. T. Lima1 and Gilberto N. Salvador2

1) Museu de Zoologia, Universidade Estadual de Campinas, Caixa Postal 6109, 13083-863, Campinas, SP, . E-mail: [email protected] 2) Laboratório de Ecologia e Csonservação, Universidade Federal do Pará, Rua Augusto Côrrea, 1, Belém, PA, Brazil. E-mail: [email protected]

Accepted: 05 February 2018

Keywords mentada baseada em observações de dois espécimes que hypsiura, Couepia, Chrysobalanaceae, flooded dobraram seu pedúnculo caudal contra o lado do corpo forest, Chromolucuma rubriflora. após serem capturados, na região de Tefé, Amazônia cen- tral, Brasil. Este é o segundo registro de camuflagem de se- Abstract mentes em bagres aspredinideos, o primeiro sendo para Seed camouflage (masquerade) by Bunocephalus verruco- . Tipos de camuflagem entre bagres as- sus, an aspredinid catfish, is herein reported based on two predinideos são aqui reportados como variando entre observations of specimens that folded their caudal pedun- “masquerade”, imitação do substrato, e colorido disruptivo. cle against the side of the body after being captured, in the Muitas sementes (tipicamente drupas) da foresta inundada region of Tefé, Central Amazon, Brazil. This is the second podem servir como modelos potenciais para Bunocephalus report of seed camouflage for aspredinid , the first verrucosus, através de sua área de distribuição, em destaque being reported for Amaralia hypsiura. Types of camouflage sementes de Chrysobalanaceae. among aspredinid catfishes are herein reported to range from masquerade, background matching, and disruptive Résumé coloration. Many seeds (mostly drupes) of the flooded for- Camouflage de semences (masquerade) par un aspredinid est may serve as potential models for Bunocephalus verruco- Bunocephalus verrucosus, poisson-chat, est rapporté dans le sus across its range, particularly seeds of Chrysobalanaceae. présent document en se fondant sur deux observations de spécimens que leur pédoncule caudal pliée contre le côté Zusammenfassung du corps après sa capture, dans la région de Tefé, Central Berichtet wird hier von einer Samenmimese (Maskierung) Amazon, au Brésil. C'est le deuxième rapport du camou- bei Bunocephalus verrucosus, einem Wels der Aspredinidae; flage des semences pour aspredinid poissons-chats, le pre- der Bericht gründet sich auf Beobachtungen in der Gegend mier étant déclaré pour Amaralia hypsiura. Types d'aspre- von Tefé, Zentralamazonien, Brasilien, an zwei Exemplaren, dinid camouflage chez les poissons-chats sont présentes de die nach dem Fang ihren Schwanzstiel an die Körperseite mascarade, d'arrière-plan, correspondance et perturbateurs legten. Es ist der zweite Bericht von Samenmimese bei de la couleur. Beaucoup de graines (surtout les drupes) de Welsen der Aspredinidae; der erste bezog sich auf Amaralia la forêt inondée peuvent servir de modèles potentiels pour hypsiura. In diesem Bericht wird ein Überblick über die Tar- Bunocephalus verrucosus dans toute son aire de répartition, nungstypen bei Welsen der Aspredinidae gegeben: Sie re- notamment les semences de Chrysobalanaceae. ichen von Mimese (Maskierung) und Somatolyse (Ver- schmelzung mit dem Hintergrund) bis zur auffälligen Fär- Sommario bung (Schrecktracht). Viele Samen (meistens Steinfrüchte) Il criptismo (mascheramento) a forma di seme di Buno- in einem überfluteten Waldstück eignen sich als Modell für cephalus verrucosus, un pesce gatto aspredinide, è qui ripor- die Tarnung von Bunocephalus verrucosus innerhalb seiner tato in base a due osservazioni di esemplari che hanno ri - mimetischen Möglichkeiten, insbesondere Samen der piegato il loro peduncolo caudale contro il lato del corpo Chrysobalanaceae (Goldpflaumengewächse). dopo essere stati catturati, nella regione di Tefé, nell'Amaz- zonia centrale, in Brasile. Questo è la seconda segnalazione Resumo di criptismo a seme per i pesci gatto aspredinidi, dopo Camuflagem de sementes (“masquerade”) por Buno- quello riportato per Amaralia hypsiura. I tipi di mimetiz- cephalus verrucosus, um bagre aspredinideo, é aqui docu- zazione qui riportati tra i pesci gatto aspredinidi compren-

137 aqua vol. 23 no. 4 - 15 March 2018 Fooled by a fish: seed camouflage by an Amazonian banjo catfish, Bunocephalus verrucosus (Siluriformes: Aspredinidae) dono il mascheramento, il camuffamento con il fondale e November 2017. Data for the map of distribution la colorazione distruttiva. Molti semi della foresta allu- of Bunocephalus verrucosus was obtained from the vionale (principalmente drupe, in particolare di literature (Mees 1988; Mol 2012; Le Bail et al. Chrysobalanaceae) possono servire come potenziali model- 2012) complemented with the records available li per Bunocephalus verrucosus. through two online databases, Link (splink.cria.org.br) and Global Biodiversity Infor- INTRODUCTION mation Facilit (GBIF) (www.gbif.org). Specimens Visual camouflage (of which crypsis is the best deposited in two collections (MZUSP and ZUEC) known example: Stevens & Merilaita 2009) is a were checked to confirm their identity (see Appen- widespread, although relatively poorly document- dix). Bunocephalus verrucosus is a very distinctive ed, evolutive strategy present in several freshwater aspredinid and misidentifications in collections are and marine fishes (see, e.g., Randall 2005, Roberts very likely non-existent or negligible in number. 2015, Sazima 2017). Several fishes from the Institutional acronyms follow Sabaj (2016). Distri- Greater Amazonia region (used herein to include, bution data of Couepia paraensis was obtained besides the , the Orinoco basin and through the above-mentioned databases. A sample the several relatively small guyanese river systems; of the Chromolucuma rubriflora was de- cf. Van der Sleen & Albert 2017) are known to use posited at the UEC (Universidade Estadual de camouflage with its surroundings or inanimate ob- Campinas) herbarium. jects, typically to avoid predation (e.g., Zuanon et al. 2006; Sazima et al. 2006). Camouflaged color RESULTS patterns of fishes from the Pan-Amazon region typ- The first Bunocephalus verrucosus specimen ob- ically imitates either fallen, dead, soaken leaves or served imitating a large seed was collected with a leaves remnants (e.g., juvenile pacus; Zamprogno small handnet at a tributary of the Lago Amanã, at & Andrade 1986; the catfishes Helogenes marmora- the shoreline of a flooded igapó forest with a deep tus and Tetranematichthys quadrifilis, and the knife- layer of dead leaves and other vegetal debris. This fish Steatogenys duidae; Sazima et al. 2006), dead large (c. 10 cm SL) specimen was taken to be at twigs (e.g., suckermouth catfishes; Ret- first a large seed by the first author, and only a zer & Page 1996: 34), or living aquatic vegetation closer look revealed it to be a fish. This observa- (e.g., the crenuchid elegans; tion was previously reported by Roberts (2015: Zuanon et al. 2006; the suckermouth catfishes 127). The second Bunocephalus verrucosus ob- Acestridium spp.; Retzer et al. 1999). The most fa- served (ZUEC 15094, 72.1 mm SL) was collected mous example of cryptic camouflage among fishes by the first author with a handnet at the mouth of from the Greater Amazonia region, and in fact one a small igarapé emptying into the Lago Tefé, a of the most famous among all , is of course large ria-lake of the middle Amazon basin, in No- the leaffish, Monocirrhus polyacanthus (Britz & vember 2017. Although the specimen was identi- Kullander 2003; Catarino & Zuanon 2010; Skel- fied immediately as a Bunocephalus verrucosus, it horn et al. 2010). Recently, Roberts (2015) argued was initially mistaken as a seed during its subse- that the aspredinid catfish Amaralia hypsiura imi- quent handling by the two authors, a few hours af- tate large seeds. The present contribution reports a ter being collected. The specimen kept its caudal second case of putative seed camouflage, this time peduncle bent against the side of the body (Figs by another aspredinid catfish, Bunocephalus verru- 1a-b), in the same way as described by Roberts cosus, furthering the case that some aspredinid cat- (2015: 122) for a living Amaralia hypsiura. In fact, fishes do indeed imitate large seeds. the bent caudal peduncle, with the erect caudal fin, gave the impression of a sprout coming out of MATERIALS AND METHODS the seed, and contributed for the overall similarity Ad libitum observations were made from two alive of the fish to a seed. The specimen only straight- Bunocephalus verrucosus specimens, one collected at ened after being anesthesized and euthanized prior a tributary of the Lago Amanã (which is connected to fixation (Fig. 2). to the lower rio Japurá, Amazonas state, Brazil; IN- PA uncat.) in March 2003 and another at the DISCUSSION mouth of a small igarapé tributary to the Lago Tefé, As noticed in the introduction, Roberts (2015) Alvarães, Amazonas state, Brazil; ZUEC 15094) in was the first to call attention to the possibility that aqua vol. 23 no. 4 - 15 marzo 2018 138 Flavio C. T. Lima and Gilberto N. Salvador

Figs 1a-f. a-b) Bunocephalus verrucosus, ZUEC 15094, 72.1 mm SL, living specimen, in the “seed-camouflage mode”, with caudal peduncle bent over the side of the body. c) Seed of Couepia sp. from rio Cristalino, Alta Floresta, Mato Grosso, Brazil; d) Seeds of Virola surinamensis from an unspecified locality in the Brazilian Amazon. e-f) Fruits of maiá, Chromolucuma rubri- flora from Igarapé Uacatuna, São Gabriel da Cachoeira, Amazonas, Brazil, February 2018, showing different degrees of shrink- age (e) and different sizes (f). Photos a-b) by G. N. Salvador, photo c) by D. Sasaki, photo d) by P. S. Sena (available at: www.commons.wikimedia.org/wiki/File%3AUcuuba_casca.JPG), photo e) by F. C. T. Lima, and photo f) by G. C. Bortolo.

139 aqua vol. 23 no. 4 - 15 March 2018 Fooled by a fish: seed camouflage by an Amazonian banjo catfish, Bunocephalus verrucosus (Siluriformes: Aspredinidae)

Fig. 2. Bunocephalus verrucosus, ZUEC 15094, 72.1 mm SL, preserved specimen, in dorsal, lateral, and ventral views. Photo by E. G. Baena. aqua vol. 23 no. 4 - 15 marzo 2018 140 Flavio C. T. Lima and Gilberto N. Salvador aspredinid catfishes – specifically Amaralia hypsiu- over the side of the body (Roberts 2015; present ra – imitate seeds. Although Roberts (2015) called study). In addition, Bunocephalus verrucosus is a rel- the similarity between Amaralia hypsiura and a seed atively robust, high-bodied aspredinid, contrasting as constituting mimicry, we herein use the term with the typically more depressed body shape pre- “camouflage”, to be more consistent with the cur- sent in most of the remaining aspredinids, includ- rent terminology on the subject, where most au- ing the remaining Bunocephalus species (cf., e.g., thors consider them to be distinct (e.g. Stevens & Mees 1989; Carvalho et al. 2015), which reinforces Merilaita 2009), even though somewhat related a seed-shape overall appearance for the species. (e.g., Endler 1981), phenomena. More specifically, Other Bunocephalus species present a cryptic color seed imitation by Amaralia hypsiura and Buno- pattern, overall appearance, and behavior; B. aleu- cephalus verrucosus constitute a type of visual cam- ropsis and B. coracoideus are typically found near ouflage called “masquerade”, where a specific ob- vegetal debris and when captured remain immo- ject, such as a leaf, a twig, a stone, or a bird-drop- bile, imitating the background where they are ping, is imitated, instead of a general background found (F. C. T. Lima, pers. obs.). Some other (Stevens & Merilaita 2009: 424). Bunocephalus species, as the recently described B. It might be questioned whether this putative case hartti and B. minerim, as well as some hoplomy- of camouflage is indeed real. One of the arguments zontini aspredinids as , and the pointed against the identification of examples of species of Ernestichthys (for pictures-drawings of camouflage (or else mimicry) is that we, humans, these aspredinids, see respectively Carvalho et al. are not the “targeted receivers” of the visual infor- 2015, and Stewart 1985), present a saddled color mation and as such might not be in a good posi- pattern, a disruptive color signal occurring in ben- tion to assess them in the first place (Stevens & thic fishes living in flowing environments with un- Merilaita 2009). This argument is, however, self- even substrates (Armbruster & Page 1996). Clear- defeating, because there is no way other than to re- ly, different aspredinind taxa rely in distinct modes ly on our own visual senses to identify putative ex- of camouflage: ‘masquerade’ for Amaralia species amples of camouflage or mimicry. We do not con- and Bunocephalus verrucosus, ‘background match- sider a coincidence that on two separate occasions, ing’ for B. aleuropsis and B. coracoideus, and ‘dis- two ichthyologists could be fooled into thinking ruptive coloration’ for B. hartti, B. minerim, that a fish was a seed, to the point of feeling Dupouyichthys sapito, and Ernestichthys species (ter- awestruck when finding out the truth (undoubted- minology follows Stevens & Merilaita 2009). ly the same feeling experienced by Roberts 2015). The flooded forests of the Amazon basin provide We have little doubt that this similarity is no mere a great number of possible seed models for Buno- coincidence, but instead a type of camouflage ac- cephalus verrucosus. The species occur across the quired during the course of evolution. Four main lowlands of the Amazon basin, as well as in rivers questions then arise: 1) how widespread might be from , Suriname, and French Guyana this type of camouflage among aspredinids; 2) (Mees 1988; Mol 2012; Le Bail et al. 2012) (Fig. what types of seeds are potentially serving as mod- 3), and most of its known localities lie within els; 3) what predators are potentially being fooled black- or clear-water rivers, typically in flooded by this camouflage; and 4) if this camouflage may forests. Drupe pits and arillated seeds are the types be serving to a purpose other than to disguise the of seeds that most likely serve as models for Buno- fish against predators. We will address each of these cephalus verrucosus, because of their size, hardness, questions in that . ornamented surfaces, and imperishability in the Among aspredinids, seed camouflage is presum- submerged leaf litter. Examples of trees occurring ably only present in Amaralia (a previously mono- in flooded forests of the Amazon basin that pro- typic , now containing two species, A. hypsiu- duces seeds (mostly drupes) that are potentially im- ra and A. oviraptor; Friel & Carvalho 2016) and itated are the seeds of Virola spp. (Myristicaceae), Bunocephalus verrucosus. Both taxa share the pres- several Chrysobalanaceae, as species of the genera ence of conspicuous bony knobs over the skull, Couepia, Licania, and Parinari, Caryocar micro- supracleithrum, and middle nuchal plate (Roberts carpum (Caryocaraceae), Andira inermis (Faba - 2015; Friel & Carvalho 2016), which imparts ceae), Buchenavia spp. (Combretaceae), among some similarity to the irregular surface of many other examples. The ucúuba, Virola surinamensis, is seeds, and the ability of flexing the caudal peduncle a widespread and common tree occurring in flood-

141 aqua vol. 23 no. 4 - 15 March 2018 Fooled by a fish: seed camouflage by an Amazonian banjo catfish, Bunocephalus verrucosus (Siluriformes: Aspredinidae) ed forests, especially white-water flooded forests ring in flooded forests, as V. elongata, which prefer (Wittmann et al. 2010), and its seeds, although rel- black-water flooded forests (Prance 1979; Worbes atively small (the whole fruits reaches up to 3 cm 1997). Even more similar are the drupes of several in diameter), may serve as a possible model for Chrysobalanaceae, which are larger and present small-sized Bunocephalus verrucosus specimens (Fig. conspicouous striae over their surfaces (e.g., 1d), as well as the seeds of other Virola trees occur- Couepia sp.; Fig. 1c). Chrysobalanaceae trees are

Fig. 3. Map of northern , showing the distribution of Bunocephalus verrucosus (above) and Couepia paraensis (below), exemplifying the co-occurrence of the fish with a putative seed model. aqua vol. 23 no. 4 - 15 marzo 2018 142 Flavio C. T. Lima and Gilberto N. Salvador among the dominant elements from black- and cently fallen, floating fruits with fleshy mesocarps clear-water flooded forests (Ayres 1993; Wittmann are taken, so its resemblance to drupes most likely et al. 2011). Particularly, Couepia paraensis, a does not put in jeopardy the seed-imitating Buno- species widespread in central and western Amazon cephalus verrucosus of being accidentaly eaten by (Prance 1972), is one of the most common trees these and other frugivorous fishes. occurring in igapó (black-water flooded forest) (Prance 1979; Kubitzki 1989), and remarkably, ACKNOWLEDGEMENTS with a distribution largerly overlapping with B. The first observation of a Bunocephalus verrucosus verrucosus (Fig. 3). In addition, fruits of maiá, imitating a seed was made by the first author dur- Chromolucuma rubriflora (Sapotaceae), a tree oc- ing a field collection trip at the invitation of curring in the forests of the Rio Negro basin as well Michel F. Catarino, then at the Instituto de Desen- as in the lower Amazon basin (Pennington 1990; volvimento Sustentável Mamirauá, Tefé, Brazil. We Pennington & Edwards 2005) might serve as mod- are grateful to him for the opportunity, as well as to els as well. The relatively large (90-150 mm) fruits Jansen S. Zuanon, Leandro M. Sousa, and Jonas A. have a mesocarp that shrink after desiccation or a Oliveira, for help and comradeship in the field. long immersion in water (Fig. 1e-f), when it sinks The second observation was made during a trip of (fresh fruits float in the water; F.C.T. Lima, pers. the project “Systematics of the tetras (genera Hemi - obs.). However, in the same way as Roberts (2015: grammus, Hyphessobrycon, Thayeria, Parapristella e 126-127) remarked for Amaralia hypsiura, we do Bryconella), with emphasis on the species from cis- not consider likely that Bunocephalus verrucosus andean South America” (FAPESP grants # evolved a resemblance to a specific seed, but actu- 2011/51532-7 and 2013/20936-0 to the first au- ally present a overall similarity to seeds, allowing it thor). We are grateful to Nelson Flausino Junior, to imitate available seeds present at the submerged and again to Jonas A. Oliveira, as well as to leaf litter of a given locality. Danielle Pedrociane Cavalcante (Instituto de De- Potential predators that may be fooled by the sim- senvolvimento Sustentável Mamirauá) for the help ilarity of Bunocephalus verrucosus to a seed are evi- at Tefé. Observations of the fruits of Chromolu- dently diurnal predators present in flooded forests, cuma rubriflora at São Gabriel da Cachoeira in relying on visual cues to identify their prey. These February 2018 were funded by the same grants. include ichthyophagous birds that hunt in shallow Denise Sasaki (Programa Flora Cristalino) kindly water, as herons, finfoot, sunbittern, and kingfish- provided Fig. 1c. Eduardo G. Baena prepared Fig. ers, and some middle to large-sized ichthyo pha - 2. We thank Alessio Datovo and Osvaldo T. Oy- gous fishes, as the cichlids Cichla spp. and the akawa (MZUSP) for allowing access to specimens large-sized pike cichlids of the Crenicichla lugubris under their care. The second author was funded by group. However, we are not aware of records of Coordenação de Aperfeiçoamento Pessoal de Nível predation on aspredinids by any of these potential Superior (CAPES). We dedicate this paper to Ivan predators. 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APPENDIX Caracaraí, igarapé do Bota Panela, cachoeira do Material examined. Bunocephalus verrucosus: Bem-Querer, c. 1˚55’N, 61˚1’W; M. Goulding, 9 Brazil, Amazonas: MZUSP 7362, 15; MZUSP Jan 1984. Pará: MZUSP 23678, 1, Lago Jacaré, rio 7363, 4; Maués, igarapé Limãozinho, 3˚24’S, Trombetas; EPA, 7-11 Oct 1969. Peru, Loreto: 57˚42’W; EPA, 4 Dec 1967. MZUSP 6208, 1, MZUSP 15296, 1, Río Nanay, Iquitos, 3˚44’S, Manaus, igarapé Jaraqui, trib. rio Negro, above 73˚18’W; M. Villacorta, 26 Sept 1979. Manaus; EPA, 22-24 Apr 1967. MZUSP 42809, 2, Manaus, igarapé Tarumãzinho; EPA, 17-18 Nov 1967. MZUSP 58966, 2, rio Negro, Anavilhanas, igapó; M. Goulding, March 1982. MZUSP 54514, 2; MZUSP 31254, 1; MZUSP 64941, 1, Barcelos, lake on island; M. Goulding, 29 Feb 1980. MZUSP 31253, 1, Rio Negro, central lake at ilha de Buiu-Açu, above rio Urubaxi; M. Gould- ing, 6 Feb 1980. MZUSP 63310, 1, Rio Negro, downstream mouth of rio Daraá, central lake; M. Goulding, 17 Feb 1980. MZUSP 59173, 1, Can- tagalo, rio Negro; EPA, 28 Jan 1972. MZUSP 61915, 3; MZUSP 84754, 1; Santa Isabel do Rio Negro, rio Aiuanã, 0˚24’S, 65˚ 2’W; EPA, 22 Oct 1972. MZUSP 62052, 6, Santa Isabel do Rio Ne- gro, rio Negro, Tapera, 0˚12’S, 64˚4’W; EPA, 2 Nov 1972. MZUSP 55117, 7, Santa Isabel do Rio Negro, igarapé em São João, 0˚24’S, 65˚2’W; EPA, 27 Oct 1972. MZUSP 109555, 1, Santa Isabel do Rio Negro, igarapé do Bitiana, próximo a boca do rio Neuixi, 0˚34’3’’S, 65˚4’5’’W; M. T. Piza et al., 8 Feb 2011. MZUSP 30699, 1, Rio Tefé, Jauar- iatuba; M. Goulding, 7 Ag 1979. ZUEC 15094, 1, Alvarães, small igarapé into Lago Tefé, 3˚ 20’00’’S, 64˚49’8’’W; F. C. T. Lima, G. N. Salvador, N. Flausino Jr. & J. A. Oliveira, 28 Nov 2017. MZUSP 6350, 2; MZUSP 6351, 2; lago Castro, mouth of rio Purus; EPA, 7-8 Nov 1967. MZUSP 23349, 7, Rio Solimões, in front of Jacaré, near- Fonte Boa; EPA, 7 Oct 1968. Acre: MZUSP 30701, 9; MZUSP 30968, 3; Tarauacá, rio Ta- rauacá, c. 8˚11’S, 70˚46’W; M; Goulding, Jul 1984. ZUEC 13501, 7, Cruzeiro do Sul, Lago Ver- melho (rio Moa), 7˚36’48’’S, 72˚48’10’’W; T. Jacó et al., 15 Jul 2015. : MZUSP 23569, 2, Caracaraí, igarapé 1 km. N of Caracaraí, c. 1˚51’N, 61˚7’W; T. R. Roberts, 5 Feb 1969. MZUSP 112954, 1; MZUSP 112777, 1; Caracaraí, igarapé Pretinho, below mouth of igara- pé Branquinho, 0˚56’32’’S, 62˚6’19’’W; O. T. Oy- akawa et al., 9 Sept 2011. MZUSP 112911, 1, Caracaraí, praia do Paricá, rio Jufari, 1˚8’41’’S, 61˚59’57’’W; O. T. Oyakawa et al., 10 Sept 2011. MZUSP 113561, 1, Caracaraí, igarapé Caicubi, trib. rio Jufari, 1˚0’54’’S, 62˚6’30’’W; O. T. Oy- akawa et al., 30 Aug 2011. MZUSP 30700, 3,

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