Stranding of Masturus lanceolatus(Actinopterygii: Molidae) in the estuary ofthe Una River, Pernambuco, Brazil: naturaland anthropogenic causes

m.e. arau’ jo1

, e.c. silva-falca~o1

, p.d. falca~o2

, v.m. marques1

and i.r. joca3

1Departamento de Oceanografia, Universidade Federal de Pernambuco, 50730-540 Recife, Pernambuco State, Brazil, 2Veterinary(voluntary researcher) and 3Grupo de Ictiologia MarinhaTropical, 50730-540 Recife, Pernambuco State, Brazil

Molidae are tropical marine teleosts that occur in all oceans. Among the species described, Masturus lanceolatus is consideredrare on the Brazilian coast, with only four records found in scientific publications. The present study reports the first occur-rence of this species for the coast of the State of Pernambuco (north-eastern Brazil) and discusses the possible causes of itsbeing stranded. The specimen was found alive in the estuary of the Una River in the city of Sao Jose da Coroa Grande onthe southern coast of the state. The fish was unknown to the local community of fishermen, who considered it a ‘badomen’. The occurrence led to an environmental education project in the community carried out by members of theTropical Marine Ichthyology Group, which carried out an inspection, documentation, analysis of external injuries and collec-tion of viscera for the subsequent histological analysis. After undergoing taxidermy, the specimen was donated to the UnaMuseum. Analysis revealed that the fish suffered from an intense inflammatory process of the liver caused by polycystosisof nematodes and Trypanorhyncha, which resulted in malnutrition, as observed by the low body weight. Moreover, alikely stranding left the specimen more vulnerable to different species of shark, which mutilated it, hindering its locomotion.This fish appears to have drifted and was thrown against the reefs near the estuary before its stranding.

Keywords: sunfish, river, first record, fishermen, north-eastern Brazil

Submitted 9 March 2010; accepted 28 April 2010

I N T R O D U C T I O N

The family Molidae comprises species of epipelagic fish com-monly known as molas or ocean sunfish, which are distributedin warm, tropical waters in all oceans (Matsuura, 2002). Onlythree species were described for this family: Ranzania laevis(Pennant, 1776), Mola mola (Linnaeus, 1758) and Masturuslanceolatus Lienard, 1840. A recent genetic and biogeographi-cal study confirmed the existence of a fourth species, Molaramsayi (Giglioli, 1883), which is restricted to the southernhemisphere (Parenti, 2003; Bass et al., 2005). Despite theirbroad distribution, studies on the biology of these speciesare rare in Brazil and the majority involve the analysis ofindividuals stranded on the shore either dead or severelydebilitated (Lopes et al., 2004; Ahid et al., 2009).

Morphologically, molas are considered the heaviest livingmarine teleosts and have a very tall, laterally flat body. Thedorsal and anal fins are used for propulsion and the caudalfin is modified in a structure called a clavus. The mouth isvery small and the teeth are united in the form of a beak(Parenti, 2003). Molidae feed mainly on zooplankton, butalso jellyfish, algae, crustaceans and fish (Parenti, 2003);juveniles feed on benthic invertebrate (Matsuura, 2002).

These fish are frequently infected with the larvae of worms(Arru et al., 1991) and are well-known for their impressiveparasite load. Forty different genera of parasites have beenreported in a single species (Volgelinest, 2006).

Masturus lanceolatus, commonly known as the sharptailmola, has broad distribution in the western Atlantic, occurringfrom Nova Scotia to south-eastern Brazil (Klein-MacPhee,2002; Menezes, 2003). Records of occurrence in Brazil,however, are rare and the species is only cited for the statesof Sao Paulo, Ceara (Figueiredo & Menezes, 2000) andBahia. Only two specimens are deposited in ichthyologic col-lections in Brazil (Lopes et al., 2004).

Recently Ahid et al. (2009) published an article on a speci-men of Mola mola stranded in the Brazilian State of Rio Grandedo Norte. However, the photograph clearly shows the clavus inthe shape of a lance, which characterizes it as M. lanceolatus.

The aims of the present study are to analyse the possiblecauses of the stranding of a sharptail mola and record the firstoccurrence of M. lanceolatus for the coast of PernambucoState, Brazil.

M A T E R I A L S A N D M E T H O D S

Characterization of the areaThe estuary of the Una River is located at Sao Jose da CoroaGrande on the southern coast of the State of Pernambuco,

Corresponding author:M.E. AraujoEmail: elisabeth.araujo@ufpe.br

1

Marine Biodiversity Records, page 1 of 5. # Marine Biological Association of the United Kingdom, 2010doi:10.1017/S1755267210000588; Vol. 3; e69; 2010 Published online

123 km from Recife (State capital). Its margins are colonized bymangrove forests. Tidal plains form at the mouth of the river,along with a sandbar parallel with the coast. Reefs are abundantthroughout the coast and are located approximately 400 m fromthe mouth of the river. The stranding occurred on the left marginof the delta approximately 120 m from the coastline at the coor-dinates 8852′42.18′′S 35808′17.85′′W (Figure 1).

Description of specimen and external injuriesThe examination of the external injuries was initiallyperformed at the stranding site and subsequently throughphotographs taken on the day of the capture. Investigationswere made into the causes of the injuries through a compara-tive analysis of data published in scientific journals. Forthe identification of shark bites, specialist Dr PauloGuilherme Vasconcelos de Oliveira, adjunct professor of theUniversidade Federal Rural de Pernambuco, was consulted,along with bibliographic resources.

Preparation of histological slidesAfter being collected and fixed in 10% formalin, fragmentswere removed from the oesophagus, stomach, intestine, liverand heart (auricle and ventricle). The samples were submittedto routine histological techniques. Tissues were dehydrated inan increasing concentration of alcohol, diaphanized in xylol,embedded in paraffin, cut on a microtome to micro-sections5 mm in thickness and stained with haematoxylin–eosin(HE) (Maia, 1979) for mounting on slides.

R E S U L T S A N D D I S C U S S I O N

The specimen of Masturus lanceolatus was found by threelocal fishermen in the estuary of the Una River at about

0900 on 15 September 2006. The fish was being tossed bythe waves in the surf zone. It was quite debilitated, butstill alive. The fish was unknown to the fishermen and theircolleagues, who wanted to either burn or bury it, thinkingthat it was a ‘bad omen’. Native fishermen called theteam from the Tropical Marine Ichthyology Group (IMAT)to help them. Two researchers of IMAT, coordinated byM.E. Araujo, together with other researchers, including theauthors, went to the site to: (1) identify the specimen; (2) reas-sure the population; and (3) conserve the fish on ice until thearrival of the taxidermist (I.R. Joca). The IMAT acquired thespecimen and donated it to the Una Museum, where it is cur-rently on display (Figure 2).

The occurrence was reported by national newspapers andtelevision news due to the fact that this fish is rare, not onlyto the local population of the small beach, but also to thescientific community.

It is possible that the specimen described here died prema-turely, as its age was estimated at 20 years, using a calculationbased on the von Bertalanffy curve presented by Liu et al.(2009). According to the authors, M. lanceolatus longevity isestimated at 105 and 82 years for females and males, respect-ively. While molas have k-strategie characteristics, such asslow growth and late maturation, they also have the greatestfecundity among existing vertebrates, with as many as300,000,000 eggs (Parenti, 2003).

The specimen described here was male, measured 170 cmand weighed 78 kg. The three other specimens found inBahia (Lopes et al., 2004), Sao Paulo (Figueiredo &Menezes, 2000) and Rio Grande do Norte (Ahid et al.,2009) measured 112 cm, 170 cm and 93 cm and weighed50 kg, 119 kg and 24 kg, respectively. Comparing the bodymass index (BMI) of these specimens, the fish fromPernambuco was the thinnest (BMI ¼ 27) and the specimenfrom Sao Paulo was the fattest (BMI ¼ 41.2).

Along with the low body weight, a set of factors suggest thereasons for the stranding: (1) high parasite load in the liver; (2)net entanglement followed by stress; (3) susceptibility to sharkattacks, with mutilation of the fins; (4) locomotion difficultystemming from mutilated fins; and (5) body striking thereefs that form a barrier before arriving at the site where thespecimen was found.

The histopathological study of fragments from the oeso-phagus, stomach, intestine and heart revealed no noteworthyalterations. The liver had numerous cists from nematodes andcestodes from the order Trypanorhyncha in the hepatic

Fig. 1. Location of stranding of Masturus lanceolatus in the estuary of the UnaRiver, Pernambuco, Brazil.

Fig. 2. Specimen of Masturus lanceolatus on display at Una Museum (Sao Joseda Coroa Grande, PE) following taxidermy.

2 m.e. arau’ jo et al.

parenchyma, with perforation of the stroma of the organ,allowing a view of the cysts externally (Figure 3A). Onaverage, each cyst contained one parasite, as reported byRodrigues et al. (2002) in fish from the family Characidae.The liver exhibited parenchyma loss due to the presence ofworm polycytosis (Figure 3B). Several transversal concentrichyaline formations similar to nematodes were observed(Figure 3E). The cysts were enveloped by a fibrous capsuleof conjunctive tissue and some exhibited invasion of the

hepatic parenchyma, leukocyte infiltrates (Figure 3C) anddilation of arteries (Figure 3D).

Encysted nematodes inhabit different tissues in fish,causing cell disorganization and a variable amount of phago-cyte cells and lymphocyte infiltrates (Eiras & Rego, 1989). Theerratic migration of nematode larvae in viscera such as theliver is not uncommon (Roberts, 2001). In the intermediatehost, the larvae are found either floating freely or encapsulatedin the abdominal cavity or adhered to the liver (Moravec,

Fig. 3. Some results of the histopathological study of the specimen of Masturus lanceolatus, stranding on Una River, Pernambuco: (A) macroscopic view of liverwith numerous cysts from parasites; (B) worm polycytosis in hepatic parenchyma (magnification: 10×); (C) leukocyte infiltrate (magnification: 10×); (D) dilationof artery (left side) and encapsulated parasite (right side) (magnification: 10×); (E) transversal concentric hyaline formation similar to encapsulated nematode(magnification: 40×); (F) macroscopic view of cestode from the order Trypanorhyncha.

Fig. 4. External injuries on specimen of Masturus lanceolatus captured live in the estuary of Una River (Sao Jose da Coroa Grande, PE). (A, B) Scratches; (E & H)rashes; (G) x-shape mark and linear cut with knife; (C, D & F) shark bites.

stranding of sunfish in the una estuary, brazil 3

1998), as found in the liver of the specimen described here.Post mortem studies of the Mola mola revealed multifocalhepatic and renal granulomas and hepatic cysts of cestodes(Volgelnest, 2006). Digenetic hemiurid and plerocercoid para-sites from Trypanorhyncha were recorded in the specimen ofM. lanceolatus mistakenly identified as M. mola (Ahid et al.,2009). Adults and larvae of species from this order are oftenfound in the gastrointestinal apparatus of elasmobranchsand a number of teleost species (Campbell & Beveridge,1994; Knoff et al., 2004, Sao Clemente et al., 2004, Diaset al., 2009), as found in the specimen of M. lanceolatusdescribed here.

Although Campos et al. (2008) state that extensive eosino-philia is not usual with the inflammatory reaction of host fishto parasites, the intensity of encapsulated parasites in thespecimen of M. lanceolatus led to various points of leukocyteinfiltrates, thereby characterizing an inflammatory process.This condition may have led to the initial debility of the speci-men, making it an easy target for predation or fishing nets.

Fishing net marks in the form of an ‘x’ were found on theepidermis of the specimen (Figure 4G), revealing that the fishmust have been imprisoned in a fishing net and suffered stressand trauma, which further aggravated its state of health andenabled attacks from predators and parasites. Accidentalentanglement in fishing gear is one of the main threats tomola populations, as species from the family are oftenreported as by-catch in lone-line fisheries (Joung et al.,2005) and drift nets (Akiol et al., 2005).

Both recent and old shark bites of different shapes andorigins were found during the external analysis of the speci-men. One bite mark was typical of some species of cigarshark from the genus Isistius. The specimen had a circularorifice that was apparently recent, as the skin that coveredthe area was still attached to the upper margin of the injury(Figure 4D). The concentration of bites on the sides of thebody was likely due to the fact that these areas are thelargest and most easily accessed in this type of attack (Soutoet al., 2007). These sharks may be considered temporary ecto-parasites of oceanic fish, pinnipids and cetaceans (Perrin &Hohn, 1994; Miyazaki & Perrin, 1995; Heithaus, 2001; SilvaJr et al., 2007).

Other marks from sharks were much more violent: two onthe dorsal fin, with the basal bite more recent thare the upper(Figure 4C); and another mutilating bite on the anal fin(Figure 4F). In a period of 14 years, there have been 53shark attacks on humans along the coast of Pernambucoby the bull shark (Carcharhinus leucas) and tiger shark(Galeocerdo cuvier) that attacked the legs and buttocks ofswimmers (Hazin et al., 2008). It is likely that the attack onthe mola was from these species, as they are aggressive and ter-ritorial and are found throughout the entire coast ofPernambuco.

With its dorsal and anal fins mutilated by shark attacks, themola had swimming difficulties that caused profound rashesin the areas of the insertion of the caudal and pectoral fins(Figure 4E & H). Under these morpho-physiological con-ditions, the specimen must have remained adrift and, uponapproaching the coast, suffered a number of scratches(Figure 4A, B ) from the reefs near the estuary.

Although it can live at depths of 670 m (Lopes et al., 2004),M. lanceolatus is a pelagic species that spends most of itstime in depths of less than 200 m and prefers waters withtemperatures greater than 208C (Seitz et al., 2002). It is in

this marine zone where reefs are concentrated, over whichmolas pass when needing to clean off ectoparasites, which isperformed by fish from the families Chaetodontidae andPomacanthidae (Konow et al., 2006). Although the coast ofPernambuco has a large area of reefs, this is the first recordof this species for this area. Thus, it is believed that the injuriessupposedly caused by the specimen striking the reefs occurredafter the shark bites, which is the main factor attributed to itsstranding.

A C K N O W L E D G E M E N T S

The authors are grateful to the fishermen Amaro Tenorio,Amaro Junior and Valnencir Ferreira; to Luciano Silva whonotified us of the stranding, thereby keeping the mola frombeing buried or burned; to IMAT biologists Leonardo Brutoand Fernando Melo for having conserved the specimen,photographed it on the day of capture and interviewed thefishermen; to Bertrando Bernardino, Ricardo G. Ferreira, J.Barbosa de Andrade and his wife for the logistic and financialsupport; to J. Carlos Tenorio, Diogo Tenorio, Jailton Batistaand Lucilo Marinho for help with the transportation, main-tenance and taxidermy of the specimen; and to the Brazilianfostering agency CNPq for the grant given to the first author.

R E F E R E N C E S

Ahid S.M.M., Filgueira K.D., Fonseca Z.A.A.S., Soto-Blanco B. andOliveira M.F. (2009) Ocorrencia de parasitismo em Mola mola(Linnaeus, 1758) por metazoarios no litoral do Rio Grande doNorte, Brasil. Acta Veterinaria Brasilica 3, 43–47.

Akiol O., Erdem M., Unal V. and Ceyham T. (2005) Investigations ondrift-net fishery for swordfish (Xiphias gladius L.) in the Aegean Sea.Turkish Journal of Veterinary and Animal Sciences 29, 1225–1231.

Arru E., Garippa G. and Sanna E. (1991) Molicola horridus in Luvarisimperialis and Mola mola. Bollettino della Societa Italiana diPatologia Ittica 5, 89–91.

Bass A.L., Dewar H., Thys T., Streelman J.T. and Karl S.A. (2005)Evolutionary divergence among lineages of the ocean sunfish family,Molidae (Tetraodontiformes). Marine Biology 148, 405–414.

Campbell R.A. and Beveridge I. (1994) Order Trypanorhyncha Diesing,1863. In Khalil L.F., Jones A. and Bray R.A. (eds) Keys to the cestodeparasites of vertebrates. Cambridge: CAB International, pp. 51–148.

Campos C.M., Moraes J.R.E. and Moraes F.R. (2008) Histopatologia defıgado, rim e baco de Piaractus mesopotamicus, Prochilodus lineatus ePseudoplatystoma fasciatum parasitados por myxosporıdios, captura-dos no rio Aquidauana, Mato Grosso do Sul, Brasil. RevistaBrasileira de Parasitologia Veterinaria 17, 200–205.

Clemente S.C.S., Knoff M., Padovani R.E.S., Lima F.C. and Gomes D.C.(2004) Cestoides trypanorhyncha parasitos de congro-rosa, Genypterusbrasiliensis Regan, 1903 comercializados nos municıpios de Niteroi eRio de Janeiro, Brasil. Revista Brasileira de Parasitologia Veteterinaria13, 97–102.

Dias F.J.E., Clemente S.C.S. and Knoff M. (2009) CestoidesTrypanorhyncha parasitos de peroa, Balistes capriscus Gmelin, 1789comercializados no estado do Rio de Janeiro, Brasil. RevistaBrasileira de Ciencia Veterinaria 16, 19–21.

Eiras J.J. and Rego A.A. (1989) Histologia em peixes resultante de infec-coes parasitarias. Publicacoes do Instituto de Zoologia Dr. AugustoNobrega 208, 1–12.

4 m.e. arau’ jo et al.

Figueiredo J.L. and Menezes N.A. (2000) Manual de Peixes Marinhos doSudeste do Brasil, VI. Teleostei (5). Museu de Zoologia da Universidadede Sao Paulo, Sao Paulo, 116 pp.

Hazin F.H.V., Burgess G.H. and Carvalho F.C. (2008) A shark attackoutbreak off Recife, Pernambuco, Brazil: 1992–2006. Bulletin ofMarine Science 82, 199–212.

Heithaus M. (2001) Predator–prey and competitive interactions betweensharks (order Selachii) and dolphins (suborder Odontoceti): a review.Journal of Zoology 253, 53–68.

Joung S.J., Liu K.M., Liao Y.Y. and Hsu H.H. (2005) Observed by-catchof Taiwanese tuna longline fishery in the South Atlantic Ocean.Journal of the Fisheries Society of Taiwan 32, 69–77.

Klein-MacPhee G. (2002) Molidae. In Collette B.B. and Klein-MacPheeG. (eds) Bigelow and Schroeder’s fishes of the Gulf of Maine, 3rdedition Washington, DC: Smithsonian Institution Press, pp. 603–607.

Knoff M., Clemente S.C.S., Pinto R.M., Lanfredi R.M. and GomesD.C. (2004) Taxonomic reports of Otobothrioidea (Eucestoda,Trypanorhyncha) from elasmobranch fishes of the southern coastoff Brazil. Memoria do Instituto Oswaldo Cruz 99, 31–36.

Konow N., Fitzpatrick F. and Barnett A. (2006) Adult emperor angelfish(Pomacanthus imperator) clean giant sunfishes (Mola mola) at NusaLembongan, Indonesia. Coral Reefs 25, 208.

Liu K.M., Lee M.L., Joung S.J. and Chang Y.C. (2009) Age and growthestimates of the sharptail mola, Masturus lanceolatus, in waters ofeastern Taiwan. Fisheries Research 95, 154–160.

Lopes P.R.D., Oliveira-Silva J.T., Batista R.L.G., Esquivel M. andOlavo G. (2004) Registros da famılia Molidae (Actinopterygii:Tetraodontiformes) no litoral da Bahia, Brasil (Oceano AtlanticoOcidental). Revista de Biociencias 10, 205–207.

Maia V. (1979) Tecnica Histologica, 2nd edition Sao Paulo: Atheneu.

Matsuura K. (2002) Molidae. In Carpenter K.E. (ed.) The living marineresources of the Western Central Atlantic. Volume 3. Bony fishes,Part 2 (Opistognathidae to Molidae), sea turtles and marinemammals. Rome: FAO, pp. 2014–2015.

Menezes N.A. (2003) Molidae. In Menezes N.A., Buckup P.A., FigueiredoJ.L. and Moun R.L. (eds) Catalogo das Especies de Peixes Marinhosdo Brasil. Sao Paulo: Museu de Zoologia da Universidade de SaoPaulo, p. 111.

Miyazaki N. and Perrin W.F. (1995) Rought-toothed dolphin Steno bre-danensis (Lesson, 1828). In Ridgway S.H. and Harrison S.R. (eds)Handbook of marine mammals. London: Academic Press, pp. 1–21.

Moravec F. (1998) Nematodes of freshwater fishes of the neotropical region.Prague: Academia.

Parenti P. (2003) Family Molidae Bonaparte 1832—molas or ocean sun-fishes. Annotated Checklists of Fishes 18, 1–9.

Perrin W.F. and Hohn A.A. (1994) Pantropical spotted dolphin Stenellaattenuata. In Ridgway S.H. and Harrison S.R. (eds) Handbook ofmarine mammals. London: Academic Press, pp. 71–98.

Roberts R.J. (2001) Fish pathology, 3rd edition London: W.B. Saunders.

Rodrigues E.L., Ranzani Paiva M.J.T. and Santos A.A. (2002) Alteracoeshistopatologicas em fıgado de dourado Salminus maxillosusValenciennes, 1840, (Osteichthyes, Characidae) causadas porNeocucullanus neocucullanus Travassos, Artigas & Pereira 1828(Nematoda). Acta Scientiarum 24, 455–459.

Seitz A.C., Weng K.C., Boustany A.M. and Block B.A. (2002) Behaviourof a sharptail mola in the Gulf of Mexico. Journal of Fish Biology 60,1597–1602.

Silva Jr J.M., Silva F.J.L., Sazima C. and Sazima I. (2007) Trophicrelationships of the spinner dolphin at Fernando de NoronhaArchipelago, SW Atlantic. Scientia Marina 71, 505–511.

Souto L.R.A., Oliveira J.G.A., Nunes J.A.C.C., Maia-Nogueira R. andSampaio C.L.S. (2007) Analise das mordidas de tubaroes-charuto,Isistius spp. (Squaliformes: Dalatiidae) em cetaceos (Mammalia:Cetacea) no litoral da Bahia, nordeste do Brasil. Biotemas 20, 19–25.

and

Volgelinest L. (2006) The tale of two ocean sunfish (Mola mola)—anunusual mortality in an unusual species. Annual Conference of theWildlife Disease Association, Healesville, Victoria, 1–5 December2003, pp. 30–32.

Correspondence should be addressed to:M.E. AraujoDepartamento de OceanografiaUniversidade Federal de Pernambuco50730-540 Recife, Pernambuco State, Brazilemail: elisabeth.araujo@ufpe.br

stranding of sunfish in the una estuary, brazil 5