aqua, International Journal of Ichthyology

Deception, protection, and in the mangrove: three juvenile fishes and floating leaves in Southeast Brazil

Ivan Sazima1, 2

1) Museu de Zoologia, Universidade Estadual de Campinas, Caixa Postal 6109, 13083-863 Campinas, SP, Brazil. E-mail: [email protected] 2) Projeto Dacnis, Estrada do Rio Escuro 4754, 11680-000 Ubatuba, SP, Brazil.

Received: 01 April 2017 – Accepted: 04 April 2017

Keywords blätter in mangroven-ähnlichen Habitaten zu verwenden. Masquerade, cover, Lobotes surinamensis, Mugil liza, Ohne Frage gibt es weitere Verwendungsmöglichkeiten, Oligoplites saurus doch sind es meistens solche, die mögliche Beutegreifer in einem der empfindlichsten Lebensabschnitte der Fische Abstract fernhalten sollen. Mangroves and similar habitats generally harbour rich and varied fish assemblages composed mostly of juvenile Resumo individuals (nurseries). I report here on juveniles of three Manguezais e ambientes semelhantes geralmente abrigam fish species that make use of floating leaves in mangroves, conjuntos ricos e variados de peixes, compostos principal- tidal creeks, and beaches with freshwater influence. The mente por indivíduos juvenis (“berçários”). Descrevo o uso tripletail Lobotes surinamensis uses leaves as a form of mas- de folhas flutuantes por três species de peixes em querade (resemblance to decaying leaves) both as protec- manguezais, estuários e praias sob influência de água doce. tion against potential predators and as disguise to ap- A prejereba Lobotes surinamensis usa as folhas como dis- proach prey (aggressive ). The mullet Mugil liza farce (semelhança com folhas em decomposição) como uses leaves as shelter against potential predators. The proteção contra predadores potenciais e como dissimu- leatherjacket Oligoplites saurus uses leaves mostly as cover lação para se aproximar de presas (mimetismo agressivo). A to approach its prey. These three fish species illustrate the tainha Mugil liza usa as folhas como abrigo contra variety of opportunities to use floating leaves in mangrove- predadores potenciais. A guaivira Oligoplites saurus usa as like habitats. No doubt there are additional uses, but the folhas principalmente como cobertura para se aproximar majority of them would likely be a way to elude potential de presas. As três species de peixes ilustram a variedade de predators in one of the most vulnerable life stages of a fish. oportunidades de uso de folhas flutuantes em manguezais e ambientes semelhantes. Sem dúvida há usos adicionais, Zusammenfassung mas a maioria deles possivelmente seria uma forma de es- Mangrovenwälder und ähnliche Habitate beherbergen im capar de predadores potenciais na que é uma das fases mais allgemeinen reiche und vielfältige Fischgesellschaften, die vulneráveis na vida de um peixe. meistens aus jungen Tieren bestehen („Kinderstuben“). Ich berichte hier von den Jungtieren dreier Fischarten, die sich Résumé in Mangrovenwäldern, saisonalen Bächen und an Stränden Les mangroves et les habitats analogues abritent générale- mit Süßwasser-Einfluss Schwimmblätter zunutze machen. ment des communautés riches et variées de poissons, com- Der Dreischwanzbarsch Lobotes surinamensis nutzt Blätter posées surtout de juvéniles (pouponnières). Il est question als eine Art Maskerade (Ähnlichkeit zu moderndem Laub), ici de juvéniles de trois espèces de poissons qui utilisent des sowohl als Schutz gegen mögliche Beutegreifer als auch als feuilles flottantes dans des mangroves, des criques de Tarnung, um sich Beute annähern zu können (aggressive marées et des plages sous influence d’eau douce. Lobotes Mimikry). Die Meeräsche Mugil liza benutzt Blätter als surinamensis se sert de feuilles pour se masquer (ressem- Schutz vor möglichen Beutegreifern. Der Feilenfisch Oligo- blance avec des feuilles mourantes) à la fois pour se pro- plites saurus verwendet Blätter meistens als Tarnung, um an téger des prédateurs éventuels et se déguiser pour ap- die Beute näher heranzukommen. Diese drei Fischarten ve- procher des proies (mimétisme agressif). Mugil liza utilise ranschaulichen die Vielfalt der Möglichkeiten, Schwimm- des feuilles comme abri contre des prédateurs potentiels.

41 aqua vol. 23 no. 2 - 28 April 2017 Deception, protection, and aggression in the mangrove: three juvenile fishes and floating leaves in Southeast Brazil

Oligoplites saurus se sert de feuilles surtout comme couver- mullet Mugil liza Valenciennes, 1836 (Mullidae), ture pour approcher ses proies. Les trois espèces de pois- and the leatherjacket Oligoplites saurus (Bloch & sons illustrent la variété de moyens de se servir de feuilles Schneider 1801) (Carangidae). These three fishes flottantes dans les habitats analogues aux mangroves. Sans used floating leaves for different functions, which aucun doute, il doit y avoir d’autres utilisations, mais la majorité d’entre elles doit probablement servir à éviter included masquerade to elude potential predators d’éventuels prédateurs lors d’un des stades les plus vul- and approach prey, shelter against potential preda- nérables de la vie des poissons. tors, and cover to approach prey.

Sommario MATERIALS AND METHODS Mangrovie e habitat simili ospitano in genere ricche e I observed and recorded the three fish species as- varie comunità di pesci composte per lo più da individui sociated with floating leaves whenever found, giovani (vivai). Si riportano qui come giovani di specie it- tiche facciano uso di foglie galleggianti in zone di man- mostly in shallow mangroves, but also in tidal grovie, in insenature di marea e in spiagge bagnate da creeks and adjacent beaches under freshwater influ- acque dolci. Il pesce foglia Lobotes surinamensis utilizza le ence. All surveyed habitats were in the area of the foglie sia come forma di travestimento (somiglianza con Ubatuba town (23°22’14.75”S, 44°49’48.65”W to foglie in decomposizione) sia come protezione contro 23°29’27.12”S, 45°09’50.40”W), São Paulo, potenziali predatori e per avvicinare la preda (mimetismo Southeast Brazil. The behaviour of the fishes was aggressivo). Il cefalo Mugil liza utilizza foglie come rifugio observed during daylight hours through above sur- contro i potenziali predatori. Il carangide Oligoplites saurus face sessions by slowly wading in the water, and utilizza foglie per lo più come copertura per avvicinare la sua preda. Queste tre specie di pesci illustrano la varietà di underwater sessions by snorkeling. During the ob- opportunità offerte dall’utilizzo di foglie galleggianti in servation sessions I used “ad libitum” and “se- habitat di mangrovie e simili. Senza dubbio ci sono altri quence” samplings (Altmann 1974), which are ad- usi, ma la maggior parte di loro sarebbe probabilmente un equate to record fortuitous events. The identifica- modo per eludere i potenziali predatori in una delle fasi di tion of the mullet followed Menezes et al. (2011, vita più vulnerabili di un pesce. 2015). The sizes of the observed fishes were esti- mated against objects of known size, or measured INTRODUCTION on actual collected specimens: total length (TL) or Mangroves and similar habitats are recognised as standard length (SL). Collected individuals are de- fundamental fish nurseries worldwide and general- posited in the Museu de Zoologia da Universidade ly harbour rich and varied fish assemblages com- Estadual de Campinas (ZUEC). posed mostly of juvenile individuals (Odum et al. 1982; Nagelkerken et al. 2008; Nip & Wong RESULTS 2010; Gajdzik et al. 2014). Mangrove trees and I found the tripletail Lobotes surinamensis near or treelets, including those from adjacent habitats, among floating leaves and other flotsam after shed leaves throughout, or for most of, the year winds or storms (three individuals 35.6-48 mm (Odum et al. 1982; Nagelkerken et al. 2008; pers. TL), but also on calm days (one individual 41.6 obs.). Leaves that fall into the water may float for a mm). The fish fluttered their transparent pectoral while and are carried to and fro by the currents and fins only and hovered near the leaves, drifting as if tidal movements until sinking, fragmenting, and carried by the wave movements or tidal currents. decomposing (Odum et al. 1982; Nagelkerken et The tripletails adopted a slightly oblique posture, al. 2008; Sazima & Uieda 1979). Several brackish head down, but horizontal postures were used as water and marine fish species associate with float- well (Fig. 1). When approached closely, they ing or sunken leaves and other debris, mostly sought closer proximity to a leaf and the leaf-like as a (Breder 1946; Randall & Randall behaviour was kept even in presence of snowy 1960; Sazima & Uieda 1979; Randall 2005; egrets Egretta thula (Molina, 1782) wading nearby. Queiroz et al. 2016). When the fish itself resembles Only once I observed a event by a triple- a leaf, it exemplifies a form of camouflage called tail on a guppy (Poecilia sp.). A tripletail about 40 masquerade (Endler 1981; Stevens & Merilaita mm TL was close to two or three floating leaves 2009). near the marginal vegetation of the mangrove I report here on the use of floating leaves by juve- when a small group of guppies moved niles of three fish species: the tripletail Lobotes suri- along the vegetation and approached the leaves. namensis (Bloch 1790) (Lobotidae), the lebranche The tripletail stealthily moved towards the guppies aqua vol. 23 no. 2 - 28 April 2017 42 Ivan Sazima and suddenly made a dash forwards and gulped leaf side. Two of the attacks were directed towards down an individual about 15 mm TL. juvenile Brazilian silversides Atherinella brasiliensis The lebranche mullet Mugil liza I found near or (Quoy & Gaimard 1825) and one towards juvenile on floating leaves twice (both individuals 18.2 mm mullets (Mugil sp.) about 50 mm TL. On all occa- SL). The fish swam close to a leaf, aligned with it sions the leatherjackets kept their position close to and adjusted its swimming speed according to the the leaf, partly concealed by its edge (Fig. 3). When leaf drifting in the wave movements or tidal cur- a leatherjacket and its leaf drifted near a small rents. When approached closely, it jumped on the group of prey fish swimming slowly at the water leaf and remained in the water sheet accumulated surface, it positioned itself towards a given individ- on the upper surface of the leaf (Fig. 2). The fish ual, curved the body in a sigmoid posture, and sud- remained on, or in close proximity of, the leaf for denly dashed forwards and scrapped the flank of about 30 min, after which I collected them for the intended prey with its mouth open. Scales re- identification. moved in such an attack were swallowed and the I found the leatherjacket Oligoplites saurus closely few ones scattered in the water column were picked associated to floating leaves drifting with incoming up. tide (six individuals 19.3-30.5 mm TL). The fish aligned with the leaves and adjusted their swim- DISCUSSION ming speed accordingly to the tidal currents. They From the above described events, I deduce that kept their closeness to the leaves moving slowly the tripletail L. surinamensis uses decaying and and inconspicuously. When approached closely, floating leaves as a form of masquerade both as they sometimes sunk and swam away, only to re- protection against potential predators and as dis- turn soon after to the same or similar floating leaf. guise to approach prey, the lebranche mullet M. I observed preying attacks (two of them successful) liza uses floating leaves as a shelter against potential on three occasions by individuals aligned with the predators, and the leatherjacket Oligoplites saurus

Fig. 1. A tripletail (Lobotes surinamensis) juvenile lies on its right side, hovering near a decaying leaf that floats at the water surface in the shallow portion of a beach under freshwater influence. Note the overall similarity of shape and colour of the fish and a leaf. Standard length 41.6 mm (ZUEC 892), 29 March 1983. Photo by I. Sazima.

43 aqua vol. 23 no. 2 - 28 April 2017 Deception, protection, and aggression in the mangrove: three juvenile fishes and floating leaves in Southeast Brazil uses floating leaves mostly as cover to approach its commonly seen lying on its side at or near water prey, even if the leaves may confer some protection surface and often among floating leaves (Breder against potential predators. 1949; Randall 2005), which is a behaviour that en- The tripletail has a leaf-like appearance and is hances its leaf-like resemblance and may elude po-

Fig. 2. A lebranche mullet (Mugil liza) shelters in the sheet of water it jumped into, on a decaying leaf that floats at the water surface in a beach under freshwater influence. Note that the dorsal colour of the fish is similar to that of the microorganisms that line a portion of the leaf. Standard length 18.2 mm (ZUEC 5298), 2 June 2001. Photo by I. Sazima.

Fig. 3. A leatherjacket (Oligoplites saurus) aligns with a decaying leaf that floats at the water surface in a shallow mangrove while approaching a small group of Brazilian silversides (Atherinella brasiliensis) – not visible on the photo. Note that the fish is partly covered by the leaf edge when viewed from a horizontal perspective. Total length about 30 mm, 3 February 1981. Photo by I. Sazima. aqua vol. 23 no. 2 - 28 April 2017 44 Ivan Sazima tential predators. Additionally, as the tripletail that improved the paper, and also thank to the feeds mainly on crustaceans and fishes, including CNPq for past grants that allowed me to study nat- those that dwell near the surface (Carvalho-Filho ural history of mangrove fishes in Southeast and 1999; Franks et al. 2003), its association with float- South Brazil. ing leaves plus the leaf-like behaviour are helpful to stealthily approach this prey type. Mullets generally school (Carvalho-Filho 1999; REFERENCES Carvalho et al. 2007), but the two leaf-associated ALTMANN, J. 1974. Observational study of behaviour: individuals I observed were alone. They possibly sampling methods. Behaviour 49 (3): 227-267. ARONSON, R. B. 1983. Foraging behavior of the West At- became isolated from their group and sought shel- lantic trumpetfish, Aulostomus maculatus: use of large ter close to, or on, floating leaves. When jumping herbivorous reef fishes as camouflage. Bulletin of Marine on the leaf, the fish would be protected from po- Science 33 (1): 166-171. tential predators that attack from below (Baylis BAYLIS, J. R. 1982. Unusual escape response by two 1982; Sazima & Machado 1989). cyprinodontiform fishes, and a bluegill predator’s coun- Juvenile leatherjackets are known for their leaf re- terstrategy. Copeia 1982 (2): 455-457. semblance and associated leaf-like behaviour: this BREDER C. M. 1942. 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A., OLIVEIRA, C. & NIRCHIO, M. 2010. An

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