research article metacercarial infection of wild nile

Research ArticleMetacercarial Infection of Wild Nile Tilapia(Oreochromis niloticus) from Brazil

Hudson A Pinto Vitor L T Mati and Alan L Melo

Laboratorio de Taxonomia e Biologia de Invertebrados Departamento de Parasitologia Instituto de Ciencias BiologicasUniversidade Federal de Minas Gerais PO Box 486 30123970 Belo Horizonte MG Brazil

Correspondence should be addressed to Hudson A Pinto hudsonalves13igcombr

Received 25 July 2014 Accepted 20 October 2014 Published 19 November 2014

Academic Editor Adriano Casulli

Copyright copy 2014 Hudson A Pinto et al This is an open access article distributed under the Creative Commons AttributionLicense which permits unrestricted use distribution and reproduction in any medium provided the original work is properlycited

Fingerlings of Oreochromis niloticus collected in an artificial urban lake from Belo Horizonte Minas Gerais Brazil were evaluatedfor natural infection with trematodes Morphological taxonomic identification of four fluke species was performed in O niloticusexamined and the total prevalence of metacercariae was 607 (3761) Centrocestus formosanus a heterophyid found in thegills was the species with the highest prevalence and mean intensity of infection (311 and 342 (1ndash42) resp) followed by thediplostomid Austrodiplostomum compactum (295 and 127 (1-2)) recovered from the eyes Metacercariae of Drepanocephalus spand Ribeiroia sp both found in the oral cavity of the fish were verified at low prevalences (82 and 16 resp) and intensities ofinfection (only one metacercaria of each of these species per fish) These species of trematodes are reported for the first time in Oniloticus from South America The potential of occurrence of these parasites in tilapia farming and the control strategies are brieflydiscussed

1 Introduction

The Nile tilapia Oreochromis niloticus (Linnaeus 1758) is acichlid species native to Africa that due to characteristicssuch as rapid reproduction rate and growth omnivorousfeeding and hardiness has been used in aquaculture indifferent parts of the world including America Africa andAsia In fact tilapia are the second most important fishgroup of farmed fish after carps with a global aquacultureproduction of more than 3 millions of tonnes in 2012 [1] Onthe other hand the intentional or accidental introduction ofO niloticus in urban aquatic environments has been reportedIn these places nonnative cichlids can contribute to the pro-cesses of eutrophication caused mainly by phosphorus excre-tion and resulting from bioturbation due to their bottom-feeding habits causing increase in total phosphorus andchlorophyll a concentrations as well as high cyanobacteriadensities [2] Moreover introduction of O niloticus may berelated to environmental impacts as competition with otheraquatic species including native fish species [3 4] Giventhe current economic importance of O niloticus worldwidestudies on its parasite fauna are desirable in order to prevent

economic losses In this context a diversity of protozoanand metazoan species has been reported in these hosts (bothwildlife and captive) in tropical and subtropical countries [5ndash11]

In Brazil O niloticus was introduced in the 1970s andcurrently it is the main fish used in fish farming [12] Thisinvasive alien species is now established in a great numberof Brazilian reservoirs where it has achieved high populationdensities and become the predominant species which is com-mon in sportive and subsistence fishing in the country [13ndash15] Records on the natural infection of this invasive cichlidwith Crustacea Monogenea and Protozoa species are recentin the country and in an increasing number (reviewed by[8]) However reports of infection ofO niloticuswith trema-todes are comparatively scarce In fact the only report oftrematodes inO niloticus from Brazil was performed by Silvaet al [16] who found metacercariae identified as Clinosto-mum complanatum Rudolphi 1814 a causative agent of theYellow Grub Disease

In the present study new reports of trematodes in Oniloticus are presented based on parasitological analyses ofwild specimens collected in an urban reservoir from Brazil

Hindawi Publishing Corporatione Scientific World JournalVolume 2014 Article ID 807492 7 pageshttpdxdoiorg1011552014807492

2 The Scientific World Journal

Table 1 Measurements of metacercariae of four species of trematodes found in naturally infected specimens of Nile tilapia (Oreochromisniloticus) collected in Pampulha reservoir Belo Horizonte Minas Gerais Brazil

Austrodiplostomum compactum Centrocestus formosanus Drepanocephalus sp Ribeiroia sp

Cyst 119871 mdash 220 plusmn 11 (191ndash239) 193 plusmn 7 (186ndash200) 432119882 mdash 145 plusmn 10 (123ndash171) 125 plusmn 3 (121ndash128) 205

Freeexcysted metacercaria 119871 1464 plusmn 70 (1375ndash1581) mdash mdash 623119882 702 plusmn 59 (602ndash808) mdash mdash 201

Oral sucker 119871 68 plusmn 7 (61ndash82) mdash mdash 85119882 70 plusmn 6 (61ndash82) mdash mdash 83

Ventral sucker 119871 NP mdash mdash 75119882 NP mdash mdash 77

Tribocytic organ 119871 345 plusmn 22 (300ndash375) NP NP NP119882 180 plusmn 17 (164ndash212) NP NP NP

119871= length119882 = width and NP = not present

Moreover the potential of occurrence of these parasites intilapia farming is discussed

2 Material and Methods

Sixty-one specimens of O niloticus fingerlings nonsexedmeasuring 2ndash45 cm in total length and weighing 015ndash149 g were collected in the Pampulha reservoir (19∘5010158401810158401015840S43∘5910158404010158401015840W) an artificial lake located in Belo HorizonteMinas Gerais Brazil in June 2013 Fish were caught withthe aid of a D-shaped nylon hand net (50 cm wide 40 cmhigh with a 30 cm opening and 1mm2mesh) and transportedto the laboratory Then they were measured weighed andkilled by means of cerebral concussion (in accordance withthe procedures recommended by the local ethics committeeon animal experimentation CETEA UFMG) and examinedfor the presence of parasites Initially the organs and tissues(gills intestine skin and musculature) were separated inPetri dishes containing saline (085 NaCl) and dissectedwith the aid of metal needles under a stereomicroscope Thegill arches were separated and transferred to glass slides andexamined under a light microscope After this preliminaryexamination the fish tissues were subjected to artificialdigestion by 1 pepsin solution in 085 NaCl and 1 HCl(pH 2) for 1 hour at 37∘C and reanalyzed using a stereoscopicmicroscope

The trematodes recovered were subjected to morpho-logical study in light microscope Photographs were takenon a Leica microscope coupled with a Leica ICC50 HDdigital camera Measurements were performed with the aidof a micrometer eyepiece Taxonomic identification untilthe lowest possible category was carried out according todifferent authors [17ndash21] The specimens were deposited inthe collection of the Department of Parasitology (DPIC) atFederal University of Minas Gerais Brazil The ecologicalterms were used according to Bush et al [22]

3 Results

From 61 specimens of O niloticus evaluated 37 (607) werefound infected with metacercariae A total of 94 metacer-cariae were recovered and four species of trematodes were

identified The species identified are listed below and themeasures (micrometers as themean followed by the standarddeviation and the range in parentheses) are presented inTable 1

Austrodiplostomum compactum (Lutz 1928)(Diplostomidae) (Figure 1(a))

Site of infection eyesPrevalence of infection 295 (1861)Mean intensity of infection 127 (1-2)Mean abundance of infection 041

Remarks This diplostomid species is an intestinal parasite ofcormorants (Phalacrocorax spp) in the American continent[23ndash26] In Brazil metacercariae of A compactum werereported in about forty native fish species (reviewed by [27])Nevertheless it had not yet been reported in O niloticusin the country Adult parasites were found in Phalacrocoraxbrasilianus (Gmelin 1789) in Brazil [26] and snails of thegenus Biomphalaria Preston 1910 are the first intermediatehosts [20] The infection of O niloticus with A compactumincluding reports of the occurrence of mortality was previ-ously reported in Mexico [28] and Panama [29]

Centrocestus formosanus (Nishigori 1924)(Heterophyidae) (Figure 1(d))

Site of infection gill filamentsPrevalence of infection 311 (1961)Mean intensity of infection 342 (1ndash42)Mean abundance of infection 103

Remarks Centrocestus formosanus is an intestinal hetero-phyid of Asian origin reported in birds and mammalsincluding human [18]The formation ofmetacercariae in gillsis related to the occurrence of asphyxia and mortality as wellas delayed development which cause damage to fish farming[30] In Brazil C formosanus was recorded firstly in its

The Scientific World Journal 3

(a) (b) (c)

(d) (e) (f)

Figure 1 Metacercariae found in naturally infected specimens of Nile tilapia (Oreochromis niloticus) collected in Pampulha reservoir BeloHorizonte Minas Gerais Brazil (a) Austrodiplostomum compactum recovered in the eyes (b) encysted Drepanocephalus sp found in oralcavity (c) mechanically excysted specimen of Drepanocephalus sp and detail of spines of cephalic collar (d) Centrocestus formosanus foundencysted in the gills (e) Ribeiroia sp recovered encysted in oral cavity and (f) mechanically excysted specimen of Ribeiroia sp All imagesobtained from unstained wet mount preparation Scale bar = 50 120583m

molluscan intermediary host the invader thiaridMelanoidestuberculata (Muller 1774) [31 32] and recently reported infish (Australoheros facetus (Jenyns 1842) and Poecilia reticu-lata Peters 1859) and bird (Butorides striata (Linnaeus 1758))from the Pampulha reservoir [19 33 34] This heterophyidwas previously reported in O niloticus from Egypt [35 36]Vietnam [37ndash39] and Saudi Arabia [40] but had not yetbeen reported in this cichlid in South America In additionthe occurrence of mortality in O niloticus experimentallyinfected with C formosanus was verified in Costa Rica [41]

Drepanocephalus sp (Echinostomatidae) (Figures 1(b)-1(c))Site of infection oral cavity and musculaturePrevalence of infection 82 (561)Intensity of infection 1Mean abundance of infection 0082

Remarks This 27-collar spined echinostomatid species par-asitizes cormorants (Phalacrocorax spp) in the AmericasTwo species Drepanocephalus spathans Dietz 1909 andDrepanocephalus olivaceus Nasir and Marval 1968 werereported in P brasilianus from Brazil [17 26] The life cycleof a species of this genus was recently elucidated and involvesplanorbid snails Planorbella trivolvis (Say 1817) (=Helisomatrivolvis) in North America [42] In South America Biom-phalaria spp are probably the first intermediate hosts ofDrepanocephalus spp The metacercariae of Drepanocephalussp recovered in O niloticus have spines of the cephaliccollar with general morphology and disposition compatiblewith those reported in adult parasites [16] Metacercariae ofDrepanocephalus spp were reported in fish fromMexico [43ndash46] and recently in the USA [42] This is the first report ofmetacercariae of Drepanocephalus in fish from South Amer-ica The potential association between the infection by these


echinostomids with mortality and delayed development ofNorth American fish was discussed [42]

Ribeiroia sp (Psilostomidae) (Figures 1(e)-1(f))

Site of infection oral cavityPrevalence of infection 16 (161)Intensity of infection 1Mean abundance of infection 0016

Remarks The trematodes of the genus Ribeiroia Travassos1939 are proventricular parasites of birds (with a few reportsin rodents) from the Americas and Africa In Brazil Ribeiroiainsignis Travassos 1939 considered by some authors as asynonymous of Ribeiroia ondatrae (Price 1931) was recordedin cormorants and herons [17 26] and the participationof the planorbid B straminea in transmission of Ribeiroiawas recently reported [47] These parasites have currentlyacquired great importance since R ondatrae is involved inmalformation andmortality of amphibians inNorthAmerica[48] a phenomenon not yet reported in South Americanhosts Moreover the natural infection of 15 species of fishincluding O niloticus with R ondatrae or Ribeiroia marini(Faust andHoffman 1934) was reported inNorth andCentralAmerica by a few authors (reviewed by [48]) To date fishwere not reported harboring metacercariae of Ribeiroia inSouth America Studies in order to determine other fishspecies involved in the transmission of Ribeiroia spp andthe potential pathological effects of these parasites in thesehosts are lacking Preliminary experimental infection studiesrevealed the occurrence of cutaneous alterations in fish dueRibeiroia sp from Brazil (unpublished results) likely a resultof the intense inflammatory process during the initial phaseof infection [49]

Most of the infected fish were found harboring onespecies of trematodes (3137 specimens 838) Coinfectionwas verified in 162 (637) of the parasitized fish in which4 specimens of O niloticus were found infected with C for-mosanus and A compactum 1 specimen with A compactumandDrepanocephalus sp and 1 specimen with A compactumand Ribeiroia sp

4 Discussion

The four species of trematodes found in O niloticus in thepresent study are generalists regarding their second inter-mediate hosts In fact A compactum have been reportedin several species of native fish from Brazil [27] whileDrepanocephalus spp and Ribeiroia sp were reported indifferent species of freshwater fish from North America [44ndash46 48] Given the wide distribution of species belonging tothese three genera in their respective definitive hosts mainlycormorants of the genus Phalachrocorax both parasites willsurely be found in O niloticus in other localities from SouthAmerica The same statement is valid for C formosanus aninvasive alien species that has been recorded widely in newlocations and fish species in the American continent

Prevalence and intensity of infection with trematodesmay be influenced by factors such as age of fish behavior andresistance to parasitism In fact the prevalence and intensityof infection by C formosanus observed in O niloticus in thePampulha reservoir are smaller than those previously verifiedfor A facetus a native cichlid from the same area of study(100 134 metacercariaefish resp) [19] On the other handlow intensities of infection for C formosanus and A com-pactumwere also reported inO niloticus by different authorsfrom other countries [35ndash40] which may suggest a relativeresistance of this fish to these parasites Indeed resistanceto parasites is a reason for the cultivation of tilapia howeverregarding trematodes this protection is not absolute and sothese parasites can be related to the occurrence of potentiallosses in the tilapia farming

The fact that the sample evaluated was composed offingerling may also be related to low values of intensity ofinfection observed in the present study Nevertheless theprevalence of infection is considerable in the case of finger-ling These two ecological data and also the diversity of para-sites may be higher in adult fish from the Pampulha reservoirprobably due to longer exposure to parasitic infective stagesas verified for other parasites species found in O niloticusfromUganda [7] Furthermore consideringDrepanocephalussp and Ribeiroia sp species only now reported in fish fromBrazil factors such as the small size and location of themetacercariae in the host (adhered to oral cavity and mus-culature) may have made it difficult to detect the parasites inprevious studies performed in the countryThus the artificialdigestion of host tissues which is not routinely used in studiesof parasite fauna of fish may have increased the sensitivity tothe detection of these metacercariae

The trematodes found in O niloticus in the present studyare transmitted by molluscsM tuberculata the intermediatehost of C formosanus and Biomphalaria spp the transmit-ters of Drepanocephalus sp Ribeiroia sp and A compactumThese mollusc species are widely distributed within water-sheds in South America and they are likely involved in thetransmission of these parasites to O niloticus both wild andcultivated The presence of these first intermediate hostsassociated with the occurrence of potential definitive hostsmainly aquatic birds may favor the introduction andmainte-nance of life cycle of trematodes in these places In this sensemonitoring the occurrence of aquatic molluscs in extensiveand semi-intensive tilapia farming is necessary for the pre-vention of outbreaks caused by these and other trematodeshaving fish including O niloticus as second intermediatehosts Among more than 20 species of digenetic trematodesinfecting O niloticus (mainly in Africa) metacercariae ofspecies belonging to the genera Apharyngostrigea Clinosto-mum Euclinostomum Prohemistomum and Tylodelphis [5 650 51] have been reported in vertebrate definitive hosts ornative fish from Brazil [17 52] In addition to the possibleeffects on fish production it is necessary to pay attention tospecies with zoonotic potential as C formosanus and Cli-nostomum spp which have already been reported infectinghumans in Asia

Taxonomic studies have revealed a wide diversity of par-asite species in fish includingO niloticus in Brazil [8 52ndash55]


and control measures have been discussed mainly in relationto parasite with direct transmission (Protozoa Monogeneaand Crustacea) However the potential impacts of trematodespecies in Brazilian fish farming are neglected and factorsrelated to parasitism and pathological changes caused bytrematodes in fish includingmortality are dependent on sev-eral variables related to the parasite biology and host intrinsicfactors [55] Although the infection with adult digeneansoften does not cause significant pathological changes in thefish hosts metacercariae of several species such as diplosto-mids andheterophyids whenpresent in high parasite burdenare known to cause developmental delay or death and sodamage to pisciculture In fact it is estimated that one of thespecies found in the present studyC formosanus is the causeof losses of 35million of dollars to pisciculture annually in theUSA [30] and diplostomid species including A compactummay be associated with mortality in catfish farming [56]Accordingly some strategies for the monitoring and controlof these trematodes and their transmitter molluscs have beentested in North America [30 56ndash58]

In South America and especially in Brazil the impact oftrematodes in fish farming is still unknown and the knowl-edge related to different fish-host susceptibility prophylaxisand control of these complex life cycle parasites needsadvance Thus in the field of Brazilian tilapia productionin extensive and semi-intensive conditions the presence ofaquatic molluscs and potential definitive hosts (aquatic birdssuch as cormorants herons and grebes) should serve as awarning about the possibility of maintaining the life cycle ofspecies of trematodes potentially involved in occurrence ofdamage to fish farming

Conflict of Interests

The authors declare that there is no conflict of interestsregarding the publication of this paper

Acknowledgment

The authors thank the National Council for Scientific andTechnological Development (CNPq) Brazil for financialsupport

References

[1] Food and Agriculture Organization of the United Nations(FAO) and Cultured Aquatic Species Information ProgrammeOreochromis niloticus FAO Fisheries and Aquaculture Depart-ment Rome Italy httpwwwfaoorgfisheryculturedspeciesOreochromis niloticusen

[2] F Starling X Lazzaro C Cavalcanti and R Moreira ldquoCon-tribution of omnivorous tilapia to eutrophication of a shallowtropical reservoir evidence from a fish killrdquo Freshwater Biologyvol 47 no 12 pp 2443ndash2452 2002

[3] G C Canonico A Arthington J KMccrary andM LThiemeldquoThe effects of introduced tilapias on native biodiversityrdquoAquatic Conservation Marine and Freshwater Ecosystems vol15 no 5 pp 463ndash483 2005

[4] I S T Vicente and C E Fonseca-Alves ldquoImpact of intro-ducedNile tilapia (Oreochromis niloticus) on non-native aquatic

ecosystemsrdquo Pakistan Journal of Biological Sciences vol 16 no3 pp 121ndash126 2013

[5] J H Landsberg ldquoParasites and associated diseases of fish inwarmwater culture with special emphasis on intensificationrdquo inFish Culture in Warm Water Systems Problems and Trends MShilo and S Sarig Eds pp 195ndash252 CRC Press Boca RatonFla USA 1989

[6] D Florio A Gustinelli M Caffara F Turci F Quaglio andR Konecny ldquoVeterinary and public health aspects in tilapia(Oreochromis niloticus niloticus) aquaculture in Kenya Ugandaand Ethiopiardquo Ittiopatologia vol 6 pp 51ndash93 2009

[7] P Akoll R Konecny W W Mwanja J K Nattabi C Agoe andF Schiemer ldquoParasite fauna of farmed Nile tilapia (Oreochromisniloticus) and African catfish (Clarias gariepinus) in UgandardquoParasitology Research vol 110 no 1 pp 315ndash323 2012

[8] W M F Pantoja L R Neves M K R Dias R G B MarinhoD Montagner and M Tavares-Dias ldquoProtozoan and metazoanparasites ofNile tilapiaOreochromis niloticus cultured in BrazilrdquoRevista MVZ Cordoba vol 17 no 1 pp 2659ndash2666 2012

[9] O O Ashade O M Osineye and E A Kumoye ldquoIsolationidentification and prevalence of parasites onOreochromis niloti-cus from three selected river systemsrdquo Journal of Fisheries andAquatic Science vol 8 no 1 pp 115ndash121 2013

[10] BWiriya J H Clausen T Inpankaew et al ldquoFish-borne trema-todes in cultured Nile tilapia (Oreochromis niloticus) and wild-caught fish from Thailandrdquo Veterinary Parasitology vol 198no 1-2 pp 230ndash234 2013

[11] N Penprapai and M Chumchareon ldquoBiodiversity of parasitesin red tilapia fishes (Oreochromis niloticus Linn) cultured cagein Trang River at Trang Provincerdquo Journal of Applied SciencesResearch vol 9 no 12 pp 6059ndash6062 2013

[12] Ministerio da Pesca e Aquicultura Boletim Estatıstico da Pescae Aquicultura MPA Brasılia Brazil 2011

[13] T Walter and M Petrere Jr ldquoThe small-scale urban reservoirfisheries of Lago Paranoa Brasılia DF Brazilrdquo Brazilian Journalof Biology vol 67 no 1 pp 9ndash21 2007

[14] J L C Novaes and E D Carvalho ldquoArtisanal fisheries ina Brazilian hypereutrophic reservoir Barra Bonita reservoirmiddle Tiete riverrdquo Brazilian Journal of Biology vol 71 no 4pp 821ndash832 2011

[15] J L C Novaes and E D Carvalho ldquoAnalysis of artisanalfisheries in two reservoirs of the upper Parana River basin(Southeastern Brazil)rdquoNeotropical Ichthyology vol 11 no 2 pp403ndash412 2013

[16] A S Silva S G Monteiro R L Doyle F A Pedron J E SFilipetto and J R Neto ldquoOcorrencia de Clinostomum com-planatum em diferentes especies de peixes de uma piscultura domunicıpio de SantaMariamdashRSrdquoVeterinaria e Zootecnia vol 15no 1 pp 27ndash32 2008

[17] L Travassos J F T Freitas and A Kohn ldquoTrematodeos doBrasilrdquoMemorias do Instituto Oswaldo Cruz vol 67 pp 1ndash8861969

[18] T Scholz and G Salgado-Maldonado ldquoThe introduction anddispersal of Centrocestus formosanus (Nishigori 1924) (Dige-nea Heterophyidae) in Mexico a reviewrdquo The American Mid-land Naturalist vol 143 no 1 pp 185ndash200 2000

[19] H A Pinto and A L Melo ldquoMetacercariae of Centrocestus for-mosanus (Trematoda Heterophyidae) in Australoheros facetus(Pisces Cichlidae) in Brazilrdquo Brazilian Journal of VeterinaryParasitology vol 21 no 3 pp 334ndash337 2012


[20] H A Pinto and A L Melo ldquoBiomphalaria straminea and Biom-phalaria glabrata (Mollusca Planorbidae) as new intermediatehosts of the fish eyefluke Austrodiplostomum compactum(Trematoda Diplostomidae) in Brazilrdquo Journal of Parasitologyvol 99 no 4 pp 729ndash733 2013

[21] P C Beaver ldquoThe morphology and life history of Psilostomumondatrae Price 1931 (Trematoda Psilostomidae)rdquo Journal ofParasitology vol 25 pp 383ndash393 1939

[22] A O Bush K D Lafferty J M Lotz and A W ShostakldquoParasitology meets ecology on its own terms Margolis et alrevisitedrdquo Journal of Parasitology vol 83 no 4 pp 575ndash5831997

[23] A Lutz ldquoEstudios sobre trematodes observados en Venezuelardquoin Estudios de Zoologia y Parasitologia Venezolanas A LutzEd pp 101ndash125 Universidad Central de Venezuela CaracasVenezuela 1928

[24] M Ostrowski de Nunez ldquoDie Entwicklungszyklen von Diplo-stomum (Austrodiplostomum) compactum (Lutz 1928) und D(A) mordax (Szidat und Nani 1951) n comb in SudamerikardquoZoologischer Anzeiger vol 208 pp 393ndash404 1982

[25] J Violante-Gonzalez S Monks S Gil-Guerrero A Rojas-Herrera R Flores-Garza and E Larumbe-Moran ldquoParasitecommunities of the neotropical cormorant Phalacrocoraxbrasilianus (Gmelin) (Aves Phalacrocoracidae) from twocoastal lagoons in Guerrero state Mexicordquo ParasitologyResearch vol 109 no 5 pp 1303ndash1309 2011

[26] C M Monteiro J F R Amato and S B Amato ldquoHelminthparasitism in the Neotropical cormorant Phalacrocorax brasil-ianus in Southern Brazil effect of host size weight sex andmaturity staterdquo Parasitology Research vol 109 no 3 pp 849ndash855 2011

[27] I P Ramos L Franceschini A C Zago et al ldquoNew host recordsand a checklist of fishes infected with Austrodiplostomum com-pactum (Digenea Diplostomidae) in Brazilrdquo Brazilian Journalof Veterinary Parasitology vol 22 no 4 pp 511ndash518 2013

[28] J Violante-Gonzalez M Garcıa-Varela A Rojas-Herrera andS G Guerrero ldquoDiplostomiasis in cultured and wild tilapiaOreochromis niloticus in Guerrero State Mexicordquo ParasitologyResearch vol 105 no 3 pp 803ndash807 2009

[29] D G Roche B Leung E F M Franco and M E TorchinldquoHigher parasite richness abundance and impact in nativeversus introduced cichlid fishesrdquo International Journal for Par-asitology vol 40 no 13 pp 1525ndash1530 2010

[30] J Mitchell R M Overstreet A E Goodwin and T M BrandtldquoSpread of an exotic fish-gill trematode a far-reaching andcomplex problemrdquo Fisheries vol 30 no 8 pp 11ndash16 2005

[31] H A Pinto and A L Melo ldquoMelanoides tuberculata (molluscaThiaridae) as an intermediate host of Centrocestus formosanus(Trematoda Heterophyidae) in Brazilrdquo Revista do Instituto deMedicina Tropical de Sao Paulo vol 52 no 4 pp 207ndash210 2010

[32] C Paula-AndradeH A Pinto D Coscarelli THDAVidigaland A L Melo ldquoThe natural infection of Melanoides tuber-culata (Muller 1774) (Mollusca Gastropoda) by Centrocestusformosanus (Nishigori 1924) (Platyhelminthes Trematoda) inParanoa lake Brasılia Brazilrdquo Brazilian Journal of Biology vol72 no 2 pp 419ndash420 2012

[33] H A Pinto and A L Melo ldquoInfeccao natural de Poeciliareticulata (Actinopterygii Poeciliidae) por metacercarias naRepresa da Pampulha Belo Horizonte Minas Gerais BrasilrdquoBoletim do Instituto de Pesca vol 38 no 3 pp 257ndash264 2012

[34] H A Pinto V L T Mati and A L Melo ldquoNew records and achecklist of trematodes fromButorides striata (Aves Ardeidae)rdquo

Revista Mexicana de Biodiversidad vol 84 no 4 pp 1100ndash11102013

[35] R A M Ramadan O A Saleh and R M El-Gamal ldquoPreva-lence and distribution of metacercariae of Centrocestus sp(Trematode Heterophyidae) on gills and other organs of Ore-ochromis niloticus fingerlingsrdquo Suez Canal Veterinary MedicineJournal vol 92 pp 657ndash667 2002

[36] A M Eissa H I Derwa M Ismail R A Ramadan M Zakiand N Mohamed ldquoUse of enzyme activities as biomarkers foroxidative stress induced by metacercarial affections in somecultured tilapia speciesrdquo Life Science Journal vol 11 no 3 pp228ndash233 2014

[37] J R Arthur and B Q Te ldquoChecklist of the parasites of fishesof Viet Namrdquo FAO Fisheries Technical Paper no 3692 FAORome Italy 2006

[38] N T Hop N V De D Murrell and A Dalsgaard ldquoOccurrenceand species distribution of fishborne zoonotic trematodes inwastewater-fed aquaculture in northern Vietnamrdquo TropicalMedicine and International Health vol 12 supplement 2 pp66ndash72 2007

[39] T T K Chi A Dalsgaard J F Turnbull P A Tuan and KD Murrell ldquoPrevalence of zoonotic trematodes in fish from aVietnamese fish-farming communityrdquo Journal of Parasitologyvol 94 no 2 pp 423ndash428 2008

[40] A M N Kalantan A H Al-Harbi and M Arfin ldquoOn themetacercaria of Centrocestus formosanus (TrematodaHetero-phyidate) Nishigori 1924 (DigeneaHeterophyidae) from Ore-ochromis niloticus in Saudi Arabia and its development in vari-ous definitive hostsrdquo Journal of Parasitology and Applied AnimalBiology vol 8 pp 83ndash94 1999

[41] D A Cortes G Dolz J J R Zuniga A E Jimenez andD LeonldquoCentrocestus formosanus (Opisthorchiida Heterophyidae)como causa de muerte de alevines de tilapia gris Oreochromisniloticus (Perciforme Cichlidae) en el Pacıfico seco de CostaRicardquo Revista de Biologıa Tropical vol 58 no 4 pp 1453ndash14652010

[42] M J Griffin L H Khoo SMQuiniou et al ldquoGenetic sequencedata identifies the cercaria of Drepanocephalus spathans (Dige-nea Echinostomatidae) a parasite of the double-crested cor-morant (Phalacrocorax auritus) with notes on its pathologyin juvenile channel catfish (Ictalurus punctatus)rdquo Journal ofParasitology vol 98 no 5 pp 967ndash972 2012

[43] I Jimenez-Garcıa ldquoFauna helmintologica de Cichlasoma fen-estratum (Pisces Cichlidae) del lago de Catemaco VeracruzMexicordquo Anales del Instituto de Biologia Universidad NacionalAutonoma de Mexico Serie Zoologıa vol 64 pp 75ndash78 1993

[44] T Scholz and M L Aguirre-Macedo ldquoMetacercariae of trema-todes parasitizing freshwater fish in Mexico a reappraisal andmethods of studyrdquo inMetazoan Parasites in the Neotropic Eco-logical Taxonomic and Evolutionary Perspectives G Salgado-Maldonado A N Garcıa-Aldrete and V M Vidal-MartinezEds pp 85ndash99 Universidad Nacional Autonoma de MexicoMexico City Mexico 2000

[45] G Salgado-Maldonado ldquoChecklist of helminth parasites offreshwater fishes from Mexicordquo Zootaxa vol 1324 pp 1ndash3572006

[46] G Perez-Ponce de Leon L Garcıa-Prieto and B Mendoza-Garfias ldquoTrematode parasites (Platyhelminthes) of wildlifevertebrates in Mexicordquo Zootaxa vol 1534 pp 1ndash250 2007

[47] H A Pinto R C Jadin S A Orlofske P T J Johnson and ALMelo ldquoBiomphalaria straminea (Mollusca Planorbidae) as an


intermediate host ofRibeiroia sp (Trematoda Psilostomidae) inBrazilrdquo Journal of Parasitology vol 99 no 5 pp 914ndash918 2013

[48] P T J JohnsonD R Sutherland JM Kinsella andK B LundeldquoReview of the trematode genusRibeiroia (Psilostomidae) ecol-ogy life history and pathogenesis with special emphasis on theamphibian malformation problemrdquo Advances in Parasitologyvol 57 pp 191ndash253 2004

[49] H W Huizinga and M J Nadakavukaren ldquoCellular responsesof goldfish Carassius auratus (L) to metacercariae of Ribeiroiamarini (Faust amp Hoffman 1934)rdquo Journal of Fish Diseases vol20 no 6 pp 401ndash408 1997

[50] A Taher ldquoSome studies on metacercarial infection in Ore-ochromis niloticus in Assiut Governorate and their role intransmission of some trematodes to dogsrdquoAssiutUniversity Bul-letin for Environmental Researches vol 12 no 1 pp 63ndash79 2009

[51] A Gustinelli M Caffara D Florio E O Otachi EMWathutaand M L Fioravanti ldquoFirst description of the adult stage ofClinostomum cutaneum Paperna 1964 (Digenea Clinostomi-dae) from grey herons Ardea cinerea L and a redescriptionof the metacercaria from the Nile tilapia Oreochromis niloticusniloticus (L) in Kenyardquo Systematic Parasitology vol 76 no 1 pp39ndash51 2010

[52] J C Eiras RM Takemoto and G C PavanelliDiversidade dosparasitos de peixes de agua doce do Brasil Clichetec MaringaBrazil 2010

[53] J C Eiras R M Takemoto G C Pavanelli and E A AdrianoldquoAbout the biodiversity of parasites of freshwater fish fromBrazilrdquo Bulletin of the European Association of Fish Pathologistsvol 31 no 4 pp 161ndash168 2011

[54] A Kohn BMM Fernandes and S C Cohen South AmericamTrematodes Parasites of Fishes Fiocruz Rio de Janeiro Brazil2007

[55] V EThatcherAmazon Fish Parasites Pensoft Publishers SofiaBulgaria 2006

[56] R M Overstreet and S S Curran ldquoDefeating diplostomoiddangers inUSA catfish aquaculturerdquo Folia Parasitologica vol 51no 2-3 pp 153ndash165 2004

[57] M Harvey E Wagner and C Wilson ldquoPotential impact onJune sucker and control of the digenetic trematodeCentrocestusformosanus and its intermediate hostMelanoides tuberculatardquoFinal Report to the Utah Reclamation Mitigation and Conser-vation Commission no 05ndash28 2005

[58] V Cantu TM Brandt and T L Arsuffi ldquoAn evaluation of threesampling methods to monitor a digenetic trematode Centroces-tus formosanus in a spring-fed ecosystemrdquo Parasitology vol 140no 7 pp 814ndash820 2013

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Table 1 Measurements of metacercariae of four species of trematodes found in naturally infected specimens of Nile tilapia (Oreochromisniloticus) collected in Pampulha reservoir Belo Horizonte Minas Gerais Brazil

Austrodiplostomum compactum Centrocestus formosanus Drepanocephalus sp Ribeiroia sp

Cyst 119871 mdash 220 plusmn 11 (191ndash239) 193 plusmn 7 (186ndash200) 432119882 mdash 145 plusmn 10 (123ndash171) 125 plusmn 3 (121ndash128) 205

Freeexcysted metacercaria 119871 1464 plusmn 70 (1375ndash1581) mdash mdash 623119882 702 plusmn 59 (602ndash808) mdash mdash 201

Oral sucker 119871 68 plusmn 7 (61ndash82) mdash mdash 85119882 70 plusmn 6 (61ndash82) mdash mdash 83

Ventral sucker 119871 NP mdash mdash 75119882 NP mdash mdash 77

Tribocytic organ 119871 345 plusmn 22 (300ndash375) NP NP NP119882 180 plusmn 17 (164ndash212) NP NP NP

119871= length119882 = width and NP = not present

Moreover the potential of occurrence of these parasites intilapia farming is discussed

2 Material and Methods

Sixty-one specimens of O niloticus fingerlings nonsexedmeasuring 2ndash45 cm in total length and weighing 015ndash149 g were collected in the Pampulha reservoir (19∘5010158401810158401015840S43∘5910158404010158401015840W) an artificial lake located in Belo HorizonteMinas Gerais Brazil in June 2013 Fish were caught withthe aid of a D-shaped nylon hand net (50 cm wide 40 cmhigh with a 30 cm opening and 1mm2mesh) and transportedto the laboratory Then they were measured weighed andkilled by means of cerebral concussion (in accordance withthe procedures recommended by the local ethics committeeon animal experimentation CETEA UFMG) and examinedfor the presence of parasites Initially the organs and tissues(gills intestine skin and musculature) were separated inPetri dishes containing saline (085 NaCl) and dissectedwith the aid of metal needles under a stereomicroscope Thegill arches were separated and transferred to glass slides andexamined under a light microscope After this preliminaryexamination the fish tissues were subjected to artificialdigestion by 1 pepsin solution in 085 NaCl and 1 HCl(pH 2) for 1 hour at 37∘C and reanalyzed using a stereoscopicmicroscope

The trematodes recovered were subjected to morpho-logical study in light microscope Photographs were takenon a Leica microscope coupled with a Leica ICC50 HDdigital camera Measurements were performed with the aidof a micrometer eyepiece Taxonomic identification untilthe lowest possible category was carried out according todifferent authors [17ndash21] The specimens were deposited inthe collection of the Department of Parasitology (DPIC) atFederal University of Minas Gerais Brazil The ecologicalterms were used according to Bush et al [22]

3 Results

From 61 specimens of O niloticus evaluated 37 (607) werefound infected with metacercariae A total of 94 metacer-cariae were recovered and four species of trematodes were

identified The species identified are listed below and themeasures (micrometers as themean followed by the standarddeviation and the range in parentheses) are presented inTable 1

Austrodiplostomum compactum (Lutz 1928)(Diplostomidae) (Figure 1(a))

Site of infection eyesPrevalence of infection 295 (1861)Mean intensity of infection 127 (1-2)Mean abundance of infection 041

Remarks This diplostomid species is an intestinal parasite ofcormorants (Phalacrocorax spp) in the American continent[23ndash26] In Brazil metacercariae of A compactum werereported in about forty native fish species (reviewed by [27])Nevertheless it had not yet been reported in O niloticusin the country Adult parasites were found in Phalacrocoraxbrasilianus (Gmelin 1789) in Brazil [26] and snails of thegenus Biomphalaria Preston 1910 are the first intermediatehosts [20] The infection of O niloticus with A compactumincluding reports of the occurrence of mortality was previ-ously reported in Mexico [28] and Panama [29]

Centrocestus formosanus (Nishigori 1924)(Heterophyidae) (Figure 1(d))

Site of infection gill filamentsPrevalence of infection 311 (1961)Mean intensity of infection 342 (1ndash42)Mean abundance of infection 103

Remarks Centrocestus formosanus is an intestinal hetero-phyid of Asian origin reported in birds and mammalsincluding human [18]The formation ofmetacercariae in gillsis related to the occurrence of asphyxia and mortality as wellas delayed development which cause damage to fish farming[30] In Brazil C formosanus was recorded firstly in its


(a) (b) (c)

(d) (e) (f)











4 Discussion











Acknowledgment


References







































































Volume 2014

Zoology






















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Virolog y



Volume 2014




Enzyme Research



Microbiology


(a) (b) (c)

(d) (e) (f)











4 Discussion











Acknowledgment


References







































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology







4 Discussion











Acknowledgment


References







































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology






Acknowledgment


References







































































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology



















































Volume 2014

Zoology






















Advances in

Virolog y



Volume 2014




Enzyme Research



Microbiology

research article metacercarial infection of wild nile

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