Changes in hematological and biochemical parameters of tambaqui (Colossoma macropomum ) parasitized by metazoan species

Alterações nos parâmetros hematológicos e bioquímicos de tambaqui (Colossoma macropomum) parasitado por espécies de metazoários

Maria Juliete Souza Rocha Gabriela Tomas Jerônimo Oscar Tadeu Ferreira da Costa José Celso de Oliveira Malta Maurício Laterça Martins Patricia Oliveira Maciel Edsandra Campos Chagas About the authors

Abstract

The aim of this study was to evaluate the impacts of metazoan parasites on hematological and biochemical parameters and relative condition factor of tambaqui (Colossoma macropomum ) farmed in northern Brazil. A total of 32 juvenile fish were captured from a commercial fish farm located in the municipality of Rio Preto da Eva, Amazonas state, Brazil. Parasite prevalence was 100% for Anacanthorus spathulatus, Mymarothecium boegeri and Notozothecium janauachensis, 100% for Neoechinorhynchus buttnerae and 53.13% for Dolops geayi. The greatest mean parasite intensity was found in acantocephalans followed by monogeneans and branchiuran crustaceans. A negative correlation was observed between abundance of N. buttnerae and hematocrit percentage, hemoglobin concentration, total thrombocyte count and glucose and between abundance of the monogenean and glucose concentration. Parasitic infections caused damage in tambaqui in terms of the observed hematological parameters that were characterized by hypochromic anemia and thrombocytopenia, which are important parameters to be used in parasitic diagnosis. This study is the first record of the occurrence of Dolops geayi in farmed tambaqui in the Amazon.

Keywords:
Fish parasites; fish farming; Monogenea; Acanthocephala; Branchiura; hematology

Resumo

O objetivo deste estudo foi avaliar o impacto do parasitismo por metazoários sobre os parâmetros hematológicos, bioquímicos e fator de condição relativo de tambaquis (Colossoma macropomum) cultivados na região Norte do Brasil. Foram coletados 32 tambaquis em fase de engorda numa piscicultura comercial no município de Rio Preto da Eva, estado do Amazonas, Brasil. A prevalência de parasitos foi de 100% para Anacanthorus spathulatus, Mymarothecium boegeri e Notozothecium janauachensis, 100% para Neoechinorhynchus buttnerae e 53,13% para Dolops geayi. A maior intensidade média foi de acantocéfalos, seguida por monogenéticos e branquiúros. Correlação negativa significativa foi observada entre abundância de N. buttnerae e os parâmetros de hematócrito, concentração de hemoglobina, trombócitos totais e glicose, bem como entre a abundância de monogenéticos e glicose. A infecção por parasitos metazoários foi capaz de debilitar os tambaquis como observado por meio das alterações hematológicas; sendo este quadro de anemia hipocrômica e trombocitopenia importante para ser utilizado no diagnóstico destas parasitoses. Este estudo foi o primeiro registro da ocorrência de Dolops geayi em tambaquis cultivados na Amazônia.

Palavras-chave:
Parasitos de peixes; piscicultura; Monogenea; Acanthocephala; Branchiura; hematologia

Introduction

Colossoma macropomum, commonly known as tambaqui, is the most cultured native freshwater fish in Brazil at 137 thousand tons (27.0% of total production) ( IBGE, 2016 Instituto Brasileiro de Geografia e Estatística – IBGE. Produção da pecuária municipal. Rio de Janeiro: IBGE; 2016. ) due to its good zootechnical performance, rusticity, diet acceptance and number of fingerlings throughout the year ( GOMES et al., 2010 Gomes LC, Simões LN, Araújo-Lima CARM. Tambaqui (Colossoma macropomum ). In: Baldisserotto B, Gomes LC. Espécies nativas para piscicultura no Brasil. Santa Maria: UFSM; 2010. p. 175-204. ). In intensive culture of C. macropomum that uses aerators, production can lead to 18 tons per hectare and approximately 2.5 kg weight in 10 months of culture ( IZEL et al., 2013 Izel ACU, Crescêncio R, O’Sullivan FFLA, Chagas EC, Boijink C, Silva JI. Produção intensiva de tambaqui em tanques escavados com aeração . Manaus: Embrapa Amazônia Ocidental; 2013. ).

In addition to production intensification and inadequate animal care, the occurrence fish diseases can compromise part or all of the production of fish ( VALLADÃO et al., 2018 Valladão GMR, Gallani SU, Pilarski F. South American fish for continental aquaculture. Rev Aquacult 2018; 10(2): 351-369. http://dx.doi.org/10.1111/raq.12164.
http://dx.doi.org/10.1111/raq.12164 ...
). Economic impacts from diseases in Brazilian fish farms has totaled 25 thousand tons of production with U$ 5 million in economic losses ( TAVARES-DIAS & MARTINS, 2017 Tavares-Dias M, Martins ML. An overall estimation of losses caused by diseases in the Brazilian fish farms. J Parasit Dis 2017; 41(4): 913-918. http://dx.doi.org/10.1007/s12639-017-0938-y. PMid:29114119.
http://dx.doi.org/10.1007/s12639-017-09...
). Among the main parasites that affect tambaqui culture in northern Brazil, acanthocephalans must be highlighted because they cause significant damage to fish production due to their high parasitic loads ( CHAGAS et al., 2015 Chagas EC, Maciel PO, Aquino-Pereira SL. Infecções por acantocéfalos: Um problema para produção de peixes. In: Tavares-Dias M, Mariano WS. Aquicultura no Brasil: novas perspectivas. vol. 1. São Carlos: Pedro & João Editores, 2015. p. 305-328. ; GOMES et al., 2017 Gomes ALS, Coelho Filho JG, Silva WV, Oliveira MIB, Bernardino G, Costa JI. The impact of Neoechinorhynchus buttnerae (Golvan, 1956) (Eoacanthocephala: Neoechinorhynchidae) outbreaks on productive and economic performance of the tambaqui Colossoma macropomum (Cuvier, 1818) reared in pounds. Lat Am J Aquat Res 2017; 45(2): 496-500. http://dx.doi.org/10.3856/vol45-issue2-fulltext-25.
http://dx.doi.org/10.3856/vol45-issue2-...
; JERÔNIMO et al., 2017 Jerônimo GT, Pádua SB, Belo MAA, Chagas EC, Taboga SR, Maciel PO, et al. Neoechinorhynchus buttnerae (Acanthocephala) infection in farmed Colossoma macropomum: a pathological approach. Aquaculture 2017; 469: 124-127. http://dx.doi.org/10.1016/j.aquaculture.2016.11.027.
http://dx.doi.org/10.1016/j.aquaculture...
; PEREIRA & MOREY, 2018 Pereira JN, Morey GAM. First record of Neoechinorhynchus buttnerae (Eoacantocephala, Neoechinorhynchidae) on Colossoma macropomum (Characidae) in a fish farm in Roraima, Brazil. Acta Amaz 2018; 48(1): 42-45. http://dx.doi.org/10.1590/1809-4392201702411.
http://dx.doi.org/10.1590/1809-43922017...
). However, these studies also emphasized losses due to infection by the protozoans Ichthyophthirius multifiliis and Piscinoodinium pillulare and monogenean helminths.

Such obstacles are directly related to parasite damage of host tissue that can vary according to the parasitic species and the health status of the host ( TAVARES-DIAS, 2006 Tavares‐Dias M. A morphological and cytochemical study of erythrocytes, thrombocytes and leukocytes in four freshwater teleosts. J Fish Biol 2006; 68(6): 1822-1833. http://dx.doi.org/10.1111/j.1095-8649.2006.01089.x.
http://dx.doi.org/10.1111/j.1095-8649.2...
). Consequently, parasitism causes immune suppression and reduces fish resistance to diseases ( FAST, 2014 Fast MD. Fish immune responses to parasitic copepod (namely sea lice) infection. Dev Comp Immunol 2014; 43(2): 300-312. http://dx.doi.org/10.1016/j.dci.2013.08.019. PMid:24001580.
http://dx.doi.org/10.1016/j.dci.2013.08...
). Regular fish and facility assessments including hematological and biochemical parameters as stress indicators constitute a rapid assessment tool in fish diagnosis ( TAVARES-DIAS, 2015 Tavares-Dias M. Parâmetros sanguíneos de referência para espécies de peixes cultivados. In: Tavares-Dias M, Mariano WS. Aquicultura no Brasil: novas perspectivas. São Carlos: Editora Pedro & João; 2015. p. 11-30. ).

Elevated levels of parasitism by the monogenean Anacanthorus penilabiatus caused a significant decrease in the hematocrit percentage, red blood cells count, mean corpuscular hemoglobin concentration and number of circulating basophils in the characid fish pacu Piaractus mesopotamicus ( JERÔNIMO et al., 2014 Jerônimo GT, Pádua SB, Bampi D, Gonçalves ELT, Garcia P, Ishikawa MM, et al. Haematological and histopathological analysis in South American fish Piaractus mesopotamicus parasitized by Monogenean (Dactylogyridae). Braz J Biol 2014; 74(4): 1000-1006. http://dx.doi.org/10.1590/1519-6984.09513. PMid:25627614.
http://dx.doi.org/10.1590/1519-6984.095...
). The hybrid tambacu (Colossoma macropomum × Piaractus mesopotamicus) parasitized by the branchiuran Dolops sp. showed reduced hematocrit percentage and increased mean corpuscular hemoglobin concentration, glucose, total protein, sodium and chlorides indicating osmoregulatory damage to the host ( TAVARES-DIAS et al., 2007a Tavares-Dias M, Moraes FR, Onaka EM, Rezende PCB. Changes in blood parameters of hybrid tambacu fish parasitized by Dolops carvalhoi (Crustacea, Branchiura), a fish louse. Vet Arh 2007a; 77(4): 355-363. ). Nevertheless, little is known regarding the physiological alterations from parasitic infection in tambaqui ( TAVARES-DIAS et al., 2011 Tavares-Dias M, Neves LR, Santos EF, Dias MKR, Marinho RGB, Ono EA. Perulernaea gamitanae (Copepoda: Lernaeidae) parasitizing tambaqui (Colossoma macropomum ) (Characidae) and the hybrids tambacu and tambatinga, cultured in northern Brazil. Arq Bras Med Vet Zootec 2011; 63(4): 988-995. http://dx.doi.org/10.1590/S0102-09352011000400026.
http://dx.doi.org/10.1590/S0102-0935201...
).

The aim of this study was to evaluate the impact of parasitic metazoans on the hematological and biochemical parameters and relative condition factor of tambaqui cultured in northern Brazil.

Materials and Methods

Study site and fish collection

A total of 32 specimens of tambaqui (436.41 ± 177.7 g weight and 29.17 ± 3.8 cm long) were collected in December 2016 with nets in a fish farm in the municipality of Rio Preto da Eva, Amazonas State, Brazil. The fish were reared in ponds that were 8,000 m2 and an intensive system of culture, and they were fed twice a day with a commercial diet for omnivorous fish with 28% crude protein.

Water quality was measured at three different points in the ponds at the sampling time and were as follows: water temperature 30.40 ± 0.10 °C and dissolved oxygen 5.78 ± 0.67 mg L-1 measured with an oximeter YSI Pro20 (Ohio, USA), pH 6.30 ± 0.12 measured with a YSI Environmental pH100 (Ohio, USA) and ammonia 0.36 ± 0.17 mg L -1 measured by the indophenol method ( APHA, 1998 American Public Health Association – APHA. Standard methods for the examination of water and wastewater. 20th ed. Washington: American Water Works Association and Water Environmental Federation; 1998. ).

After capture, the fish were anesthetized in a benzocaine solution (100 mg L-1 ) for blood collection and biometry and were euthanized by a transversal section of the spinal cord for necropsy, and organs were collected for parasitological examination. All animal procedures were approved by the Animal Ethics Committee of Embrapa Pesca e Aquicultura, in Palmas, Tocantins state, Brazil (certificate no. 24, protocol 10/2016).

Hematological and biochemical analysis

Blood was withdrawn from the caudal vein with syringes containing a drop of EDTA 10% for determination of the hematocrit percentage by the microhematocrit method, the total erythrocyte count (RBC) in a Neubauer chamber after dilution 1:200 in a Natt & Herrick (1952) Natt MP, Herrick CA. A new blood diluent for counting the erythrocytes and leucocytes of the chicken. Poult Sci 1952; 31(4): 735-738. http://dx.doi.org/10.3382/ps.0310735.
http://dx.doi.org/10.3382/ps.0310735 ...
solution, and the hemoglobin concentration by the cyanmethemoglobin method ( COLLIER, 1944 Collier HB. Standardization of blood haemoglobin determinations. Can Med Assoc J 1944; 50(6): 550-552. PMid:20323122. ). The mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH) and mean corpuscular hemoglobin concentration (MCHC) were calculated according to Ranzani-Paiva et al. (2013) Ranzani-Paiva MJT, Pádua SB, Tavares-Dias M, Egami MI. Métodos para análise hematológica em peixes. Maringá: Ed. UEM; 2013. http://dx.doi.org/10.7476/9788576286530.
http://dx.doi.org/10.7476/9788576286530...
. Blood smears were stained with May Grünwald-Giemsa-Wright for a total count of leukocytes (WBC) and thrombocytes ( RANZANI-PAIVA et al., 2013 Ranzani-Paiva MJT, Pádua SB, Tavares-Dias M, Egami MI. Métodos para análise hematológica em peixes. Maringá: Ed. UEM; 2013. http://dx.doi.org/10.7476/9788576286530.
http://dx.doi.org/10.7476/9788576286530...
). A blood aliquot was used to obtain the plasma and centrifugation at 75 G , and the plasma was kept at -18 °C until the biochemical analysis. Glucose was determined by the glucose oxidase method, and total protein was determined by the biuret method with a commercial kit (Labtest, MG, Brazil).

Parasite collection an identification

Parasites were collected and fixed according to Eiras et al. (2006) Eiras JC, Takemoto RM, Pavanelli GC. Métodos de estudo e técnicas laboratoriais em parasitologia de peixes. Maringá: Ed. UEM; 2006. . The gills and intestines were removed and fixed in a 5% formalin solution, and the parasites were preserved in 70% alcohol for posterior identification and quantification under a stereomicroscope. The identification was based on Golvan (1956) Golvan YJ. Acanthocéphales d’Amazonie. Redescription d’Oligacanthorhynchus iheringi Travassos 1916 et description de Neoechinorhynchus buttnerae n. sp. (Neoacanthocephala-Neoechinorhynchidae). Ann Parasitol Hum Comp 1956; 31(5-6): 500-524. http://dx.doi.org/10.1051/parasite/1956315500.
http://dx.doi.org/10.1051/parasite/1956...
, Kritsky et al. (1979) Kritsky DC, Thatcher VE, Kayton RJ. Neotropical Monogenoidea. 2. The Anacanthorinae Price, 1967, with the proposal of four new species of Anacanthorus Mizelle & Price, 1965, from Amazonian fishes. Acta Amaz 1979; 9(2): 355-361. http://dx.doi.org/10.1590/1809-43921979092355.
http://dx.doi.org/10.1590/1809-43921979...
, Malta (1982 Malta JCO. Os argulídeos (Crustacea: Branchiura) da Amazônia brasileira, 2. Aspectos da Ecologia de Dolops geayi Bouvier, 1897 e Argulus juparanaensis Castro, 1950. Acta Amaz 1982; 12(4): 701-705. http://dx.doi.org/10.1590/1809-43921982124701.
http://dx.doi.org/10.1590/1809-43921982...
, 1984 Malta JCO. Os peixes de um lago de várzea da Amazônia Central (Lago Janauacá, Rio Solimões) e suas relações com os crustáceos ectoparasitas (Branchiura: Argulidae). Acta Amaz 1984; 14(3-4): 355-372. http://dx.doi.org/10.1590/1809-43921984143372.
http://dx.doi.org/10.1590/1809-43921984...
), Cohen & Kohn (2005) Cohen SC, Kohn A. A new species of Mymarothecium and new host and geographical records for M. viatorum (Monogenea: Dactylogyridae), parasites of freshwater fishes in Brazil. Folia Parasitol (Praha) 2005; 52(4): 307-310. http://dx.doi.org/10.14411/fp.2005.042. PMid:16405294.
http://dx.doi.org/10.14411/fp.2005.042 ...
and Belmont-Jégu et al. (2004) Belmont-Jégu E, Domingues MV, Martins ML. Notozothecium janauachensis n. sp. (Monogenoidea: Dactylogyridae) from wild and cultured tambaqui, Colossoma macropomum (Teleostei: Characidae: Serrasalminae) in Brazil. Zootaxa 2004; 736: 1-8. . Prevalence, mean intensity and mean abundance were calculated according to Bush et al. (1997) Bush AO, Lafferty KD, Lotz JM, Shostak AW. Parasitology meets ecology on its own terms: Margolis et al. revisited. J Parasitol 1997; 83(4): 575-583. http://dx.doi.org/10.2307/3284227. PMid:9267395.
http://dx.doi.org/10.2307/3284227 ...
.

Relative condition factor (Kn)

Weight and length data were used to calculate the relative condition factor (Kn). Standard length (Ls) in cm and total weight (Wt) in g of each host were adjusted to a weight-length curve by the formula: Wt = a.Lsb. With the coefficients a and b of the equation, the estimated weight values (We) were calculated with the relative condition factor (Kn) corresponding to a quotient between the observed and expected weight to determined length (Kn = Wt/We) ( LE CREN, 1951 Le Cren ED. The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). J Anim Ecol 1951; 20(2): 201-219. http://dx.doi.org/10.2307/1540.
http://dx.doi.org/10.2307/1540 ...
).

Statistical analysis

The results obtained were expressed as the mean ± standard error. Spearman (rs) correlation coefficient was used to determine the possible correlations among the parasites, hematological and biochemical parameters and condition factor (Kn). The significance level was p<0.05 ( ZAR, 1999 Zar JH. Biostatistical analysis. New Jersey: Prentice-Hall; 1999. ).

Results

Parasite prevalence was 100% for monogeneans, identified as Anacanthorus spathulatusKritsky et al. (1979) Kritsky DC, Thatcher VE, Kayton RJ. Neotropical Monogenoidea. 2. The Anacanthorinae Price, 1967, with the proposal of four new species of Anacanthorus Mizelle & Price, 1965, from Amazonian fishes. Acta Amaz 1979; 9(2): 355-361. http://dx.doi.org/10.1590/1809-43921979092355.
http://dx.doi.org/10.1590/1809-43921979...
, Mymarothecium boegeriCohen & Kohn (2005) Cohen SC, Kohn A. A new species of Mymarothecium and new host and geographical records for M. viatorum (Monogenea: Dactylogyridae), parasites of freshwater fishes in Brazil. Folia Parasitol (Praha) 2005; 52(4): 307-310. http://dx.doi.org/10.14411/fp.2005.042. PMid:16405294.
http://dx.doi.org/10.14411/fp.2005.042 ...
and Notozothecium janauachensis Belmont-Jégu, Domingues and Martins (2004) Belmont-Jégu E, Domingues MV, Martins ML. Notozothecium janauachensis n. sp. (Monogenoidea: Dactylogyridae) from wild and cultured tambaqui, Colossoma macropomum (Teleostei: Characidae: Serrasalminae) in Brazil. Zootaxa 2004; 736: 1-8. , 100% for acanthocephalans Neoechinorhynchus buttneraeGolvan (1956) Golvan YJ. Acanthocéphales d’Amazonie. Redescription d’Oligacanthorhynchus iheringi Travassos 1916 et description de Neoechinorhynchus buttnerae n. sp. (Neoacanthocephala-Neoechinorhynchidae). Ann Parasitol Hum Comp 1956; 31(5-6): 500-524. http://dx.doi.org/10.1051/parasite/1956315500.
http://dx.doi.org/10.1051/parasite/1956...
and 53.13% for branchiura crustaceans identified as Dolops geayiBouvier (1897) Bouvier MEL. Observations sur les Arugulides du genre Gyropeltis recueillis par M. Geay au Venezuela. Bull. Mus. Hist. Nat. 1897; 3: 13-19. ( Table 1 ). The fish were parasitized by two (46.88%) or three (53.13%) parasite groups (Monogenea, Acanthocephala, and Branchiura). A total of 1,762 monogenean parasites were collected in the gills, and from these, 296 monogeneans were identified as 282 A. spathulatus (95.27% prevalence), 3 M. boegeri (1.01%) and 11 N. janauachensis (3.72%). A total of 2,770 N. buttnerae were found in the intestine and 29 D. geayi in the gill cavity of C. macropomum. Also, 1,005 free living adult copepods non-parasite (Class Maxillopoda, Subclass Copepoda, Order Cyclopoida) were found in gill filaments.

Table 1
Parasitological indices of tambaqui (Colossoma macropomum).

Table 2 shows the condition factor values and hematological and biochemical parameters as well as the reference values for tambaqui according to Tavares-Dias (2015) Tavares-Dias M. Parâmetros sanguíneos de referência para espécies de peixes cultivados. In: Tavares-Dias M, Mariano WS. Aquicultura no Brasil: novas perspectivas. São Carlos: Editora Pedro & João; 2015. p. 11-30. , study in which non parasitized fish are similar in size and weight and maintained under reared conditions as registered in this study. Negative significant correlations among abundance of acanthocephalans, hematocrit, hemoglobin, thrombocytes and glucose as well as between abundance of monogeneans and glucose were found ( Table 3 ). Nevertheless, no correlation among the parasites was verified ( Table 4 ).

Table 2
Mean values ± standard deviation of condition factor, hematological and biochemical parameters of tambaqui (Colossoma macropomum), from Rio Preto da Eva, Amazonas state, Brazil.
Table 3
Spearman correlation coefficient values among parasites abundance, condition factor, hematological and biochemical parameters of tambaqui (Colossoma macropomum ).
Table 4
Spearman correlation coefficient values among parasites groups of tambaqui ( Colossoma macropomum).

Discussion

The municipality of Rio Preto da Eva is the greatest tambaqui producer in Brazil as a result of intensive management practices, the use of aeration and high stocking densities ( IZEL et al., 2013 Izel ACU, Crescêncio R, O’Sullivan FFLA, Chagas EC, Boijink C, Silva JI. Produção intensiva de tambaqui em tanques escavados com aeração . Manaus: Embrapa Amazônia Ocidental; 2013. ; IBGE, 2016 Instituto Brasileiro de Geografia e Estatística – IBGE. Produção da pecuária municipal. Rio de Janeiro: IBGE; 2016. ). However, the lack of implementation of best management practices in fish farming has favored outbreaks of mortality and disease dissemination ( MACIEL et al., 2016 Maciel PO, Benavides MV, Webber DC, Chagas EC, Brandão FR, Aquino-Pereira SL, et al. Caracterização sanitária em cultivos de tambaqui no Estado do Amazonas - polo de produção de Rio Preto da Eva. Palmas: Embrapa Pesca e Aquicultura; 2016. ). Fish cohabit with pathogens naturally in the environment, and increased parasite populations are attributed to high stocking densities and the lack of prophylactic measures. Protozoans, helminths, myxozoans and crustaceans are the main parasites found to cause fish diseases that compromise fish physiology ( JERÔNIMO et al., 2015 Jerônimo GT, Franceschini L, Zago AC, Silva RJ, Pádua SB, Ventura AS, et al. Parasitos de peixes Characiformes e seus híbridos cultivados no Brasil. In: Tavares-Dias M, Mariano WS. Aquicultura no Brasil: novas perspectivas. vol. 1. São Carlos: Pedro & João Editores; 2015. p. 283-304. ; MACIEL et al., 2018 Maciel PO, Garcia F, Chagas EC, Fujimoto RY, Tavares-Dias M. Trichodinidae in commercial fish in South America. Rev Fish Biol Fish 2018; 28(1): 33-56. http://dx.doi.org/10.1007/s11160-017-9490-1.
http://dx.doi.org/10.1007/s11160-017-94...
).

Neoechinorhynchus buttnerae is a unique acantocephalan species parasitizing tambaqui ( MALTA et al., 2001 Malta JCO, Gomes AL, Andrade SMS, Varella AMB. Infestações maciças por acantocéfalos, Neoechinorhynchus buttnerae Golvan, 1956, (Eoacanthocephala: Neoechinorhynchidae) em tambaquis jovens, Colossoma macropomum (Cuvier, 1818) cultivados na Amazônia Central. Acta Amaz 2001; 31(1): 133-143. http://dx.doi.org/10.1590/1809-43922001311143.
http://dx.doi.org/10.1590/1809-43922001...
; THATCHER, 2006 Thatcher VE. Amazon fish parasites. Sofia: Pensoft Publishers; 2006. ; DIAS et al., 2015 Dias MKR, Neves LR, Marinho RGB, Tavares-Dias M. Parasitic infections in tambaqui from eight fish farms in Northern Brazil. Arq Bras Med Vet Zootec 2015; 67(4): 1070-1076. http://dx.doi.org/10.1590/1678-4162-7592.
http://dx.doi.org/10.1590/1678-4162-759...
; PEREIRA & MOREY, 2018 Pereira JN, Morey GAM. First record of Neoechinorhynchus buttnerae (Eoacantocephala, Neoechinorhynchidae) on Colossoma macropomum (Characidae) in a fish farm in Roraima, Brazil. Acta Amaz 2018; 48(1): 42-45. http://dx.doi.org/10.1590/1809-4392201702411.
http://dx.doi.org/10.1590/1809-43922017...
). In the present study, the mean intensity of infection by N. buttnerae was lower than that found by Malta et al. (2001) Malta JCO, Gomes AL, Andrade SMS, Varella AMB. Infestações maciças por acantocéfalos, Neoechinorhynchus buttnerae Golvan, 1956, (Eoacanthocephala: Neoechinorhynchidae) em tambaquis jovens, Colossoma macropomum (Cuvier, 1818) cultivados na Amazônia Central. Acta Amaz 2001; 31(1): 133-143. http://dx.doi.org/10.1590/1809-43922001311143.
http://dx.doi.org/10.1590/1809-43922001...
, Lourenço et al. (2017) Lourenço FS, Morey GAM, Pereira JN, Malta JCO. Ocorrência de Neoechinorhynchus (Neoechinorhynchus) buttnerae Golvan, 1956 (Acantocephala: Neochinorhynchidae) em Colossoma macropomum (Cuvier, 1818) (Characiformes: Serrasalmidae) provenientes de uma piscicultura da Amazônia brasileira. Folia Amaz 2017; 26(1): 1-8. https://doi.org/10.24841/fa.v26i1.414.
https://doi.org/10.24841/fa.v26i1.414 ...
and Jerônimo et al. (2017) Jerônimo GT, Pádua SB, Belo MAA, Chagas EC, Taboga SR, Maciel PO, et al. Neoechinorhynchus buttnerae (Acanthocephala) infection in farmed Colossoma macropomum: a pathological approach. Aquaculture 2017; 469: 124-127. http://dx.doi.org/10.1016/j.aquaculture.2016.11.027.
http://dx.doi.org/10.1016/j.aquaculture...
in fish farms in the Amazon State. In contrast, no fish mortality was found in the present study, but other studies have related fish mortality ( MALTA et al., 2001 Malta JCO, Gomes AL, Andrade SMS, Varella AMB. Infestações maciças por acantocéfalos, Neoechinorhynchus buttnerae Golvan, 1956, (Eoacanthocephala: Neoechinorhynchidae) em tambaquis jovens, Colossoma macropomum (Cuvier, 1818) cultivados na Amazônia Central. Acta Amaz 2001; 31(1): 133-143. http://dx.doi.org/10.1590/1809-43922001311143.
http://dx.doi.org/10.1590/1809-43922001...
) and cachexia in cultured fish in Rondônia and the Amazon ( JERÔNIMO et al., 2017 Jerônimo GT, Pádua SB, Belo MAA, Chagas EC, Taboga SR, Maciel PO, et al. Neoechinorhynchus buttnerae (Acanthocephala) infection in farmed Colossoma macropomum: a pathological approach. Aquaculture 2017; 469: 124-127. http://dx.doi.org/10.1016/j.aquaculture.2016.11.027.
http://dx.doi.org/10.1016/j.aquaculture...
). Mechanical damage in intestinal tissues is associated with proboscis attachment into the mucosa that leads to an inflammatory reaction by macrophages, Langerhans cells and lymphocytes that result in thickening the intestinal wall ( JERÔNIMO et al., 2017 Jerônimo GT, Pádua SB, Belo MAA, Chagas EC, Taboga SR, Maciel PO, et al. Neoechinorhynchus buttnerae (Acanthocephala) infection in farmed Colossoma macropomum: a pathological approach. Aquaculture 2017; 469: 124-127. http://dx.doi.org/10.1016/j.aquaculture.2016.11.027.
http://dx.doi.org/10.1016/j.aquaculture...
). Histopathological findings showed a disappearance of the intestinal villi, hypertrophy of the goblet cells and leukocyte inflammatory infiltrate in the submucosa layer ( MATOS et al., 2017 Matos LV, Oliveira MIB, Gomes ALS, Silva GS. Morphological and histochemical changes associated with massive infection by Neoechinorhynchus buttnerae (Acanthocephala: Neoechinorhynchidae) in the farmed freshwater fish Colossoma macropomum Cuvier, 1818 from the Amazon State, Brazil. Parasitol Res 2017; 116(3): 1029-1037. http://dx.doi.org/10.1007/s00436-017-5384-3. PMid:28124738.
http://dx.doi.org/10.1007/s00436-017-53...
).

In this study, the negative correlation observed in acantocephalan parasitized fish with hematocrit and hemoglobin concentrations could be associated with a hypochromic anemia possibly explained by hemorrhages at the attachment site in the intestine, causing lower number of circulating erythrocytes in the parasitic tambaquis when compared to the reference values ( TAVARES-DIAS, 2015 Tavares-Dias M. Parâmetros sanguíneos de referência para espécies de peixes cultivados. In: Tavares-Dias M, Mariano WS. Aquicultura no Brasil: novas perspectivas. São Carlos: Editora Pedro & João; 2015. p. 11-30. ). Similar results were found in Seriola dumerili parasitized by the monogenean Zeuxapta seriolae in the gills ( MONTERO et al., 2004 Montero FE, Crespo S, Padrós F, Gandara F, Garcıa A, Raga JA. Effects of the gill parasite Zeuxapta seriolae (Monogenea: Heteraxinidae) on the amberjack Seriola dumerili Risso (Teleostei: Carangidae). Aquaculture 2004; 232(1-4): 153-163. http://dx.doi.org/10.1016/S0044-8486(03)00536-2.
http://dx.doi.org/10.1016/S0044-8486(03...
). On the other hand, the increased mean corpuscular volume observed in P. lineatus parasitized by acantocephalans ( BELO et al., 2013 Belo MAA, Souza DGF, Faria VP, Prado EJR, Moraes FR, Onaka EM. Haematological response of curimbas Prochilodus lineatus, naturally infected with Neoechinorhynchus curemai. J Fish Biol 2013; 82(4): 1403-1410. http://dx.doi.org/10.1111/jfb.12060. PMid:23557315.
http://dx.doi.org/10.1111/jfb.12060 ...
) suggests an advanced anemic response due to immature erythrocytes release in the blood stream.

The number of thrombocytes described for tambaqui in this study is within of the reference values described for the species by Tavares-Dias (2015) Tavares-Dias M. Parâmetros sanguíneos de referência para espécies de peixes cultivados. In: Tavares-Dias M, Mariano WS. Aquicultura no Brasil: novas perspectivas. São Carlos: Editora Pedro & João; 2015. p. 11-30. , however the negative correlation of N. buttnerae abundance with total thrombocyte count suggests that these cells were being recruited by the parasitized animals. Similar alterations were reported in P. lineatus parasitized by acantocephalans ( BELO et al., 2013 Belo MAA, Souza DGF, Faria VP, Prado EJR, Moraes FR, Onaka EM. Haematological response of curimbas Prochilodus lineatus, naturally infected with Neoechinorhynchus curemai. J Fish Biol 2013; 82(4): 1403-1410. http://dx.doi.org/10.1111/jfb.12060. PMid:23557315.
http://dx.doi.org/10.1111/jfb.12060 ...
), in P. mesopotamicus parasitized by the monogenean A. penilabiatus, the dinoflagellate P. pillulare ( TAVARES-DIAS et al., 2008 Tavares-Dias M, Moraes FR, Martins ML. Hematological assessment in four Brazilian teleost fish with parasitic infections, collected in feefishing from Franca, São Paulo, Brazil. B Inst Pesca 2008; 34(2): 189-196. ) and Argulus sp. ( TAVARES-DIAS et al., 1999 Tavares-Dias M, Martins ML, Kronka SN. Evaluation of the haematological parameters in Piaractus mesopotamicus Holmberg (Osteichthyes, Characidae) with Argulus sp. (Crustacea, Branchiura) infestation and treatment with organophosphate. Rev Bras Zool 1999; 16(2): 553-555. http://dx.doi.org/10.1590/S0101-81751999000200019.
http://dx.doi.org/10.1590/S0101-8175199...
). Fish thrombocytes are cells involved in not only coagulation ( TAVARES-DIAS & OLIVEIRA, 2009 Tavares-Dias M, Oliveira SR. A review of the blood coagulation system of fish. Rev Bras Biocienc 2009; 7(2): 205-224. ) but also phagocytosis ( TAVARES-DIAS et al., 2007b Tavares-Dias M, Ono EA, Pilarski F, Moraes FR. Can thrombocytes participate in the removal of cellular debris in the blood circulation of teleost fish? A cytochemical study and ultrastructural analysis. J Appl Ichthyology 2007b; 23(6): 709-712. http://dx.doi.org/10.1111/j.1439-0426.2007.00850.x.
http://dx.doi.org/10.1111/j.1439-0426.2...
; DOTTA et al., 2014 Dotta G, Andrade JI, Gonçalves ELT, Brum A, Mattos JJ, Maraschin M, et al. Leukocyte phagocytosis and lysozyme activity in Nile tilapia fed supplemented diet with natural extracts of propolis and Aloe barbadensis. Fish Shellfish Immunol 2014; 39(2): 280-284. http://dx.doi.org/10.1016/j.fsi.2014.05.020. PMid:24857767.
http://dx.doi.org/10.1016/j.fsi.2014.05...
). Coagulation can be influenced by parasitic infections, and thrombocytopenia in fish is related to the migration of thrombocytes to hemorrhagic lesions ( TAVARES-DIAS & OLIVEIRA, 2009 Tavares-Dias M, Oliveira SR. A review of the blood coagulation system of fish. Rev Bras Biocienc 2009; 7(2): 205-224. ; BELO et al., 2013 Belo MAA, Souza DGF, Faria VP, Prado EJR, Moraes FR, Onaka EM. Haematological response of curimbas Prochilodus lineatus, naturally infected with Neoechinorhynchus curemai. J Fish Biol 2013; 82(4): 1403-1410. http://dx.doi.org/10.1111/jfb.12060. PMid:23557315.
http://dx.doi.org/10.1111/jfb.12060 ...
).

Monogeneans are known as one of the most important ectoparasites in fish ( SANTOS et al., 2013 Santos CP, Borges JN, Fernandes ES, Santos EGN. Acanthocephala. In: Pavanelli C, Takemoto RM, Eiras JC. Parasitologia de peixes de água doce do Brasil. Maringá: Ed UEM; 2013. p. 333 - 352. ) provoking gills lesions, necrosis, edema, displacement of the gill epithelium and pillar cell rupture ( MARTINS & ROMERO, 1996 Martins ML, Romero NG. Efectos del parasitismo sobre el tejido branquial en peces cultivados: estudio parasitologico e histopatologico. Rev Bras Zool 1996; 13(2): 489-500. http://dx.doi.org/10.1590/S0101-81751996000200017.
http://dx.doi.org/10.1590/S0101-8175199...
). Such alterations compromise physiological processes such as breathing, nitrogenate excretion, acid-base equilibrium and osmoregulation ( BECKER & BALDISSEROTTO, 2014 Becker AG, Baldisserotto B. Regulação osmótica e iônica. In: Baldisserotto B, Cyrino JEP, Urbinati EC. Biologia e fisiologia de peixes neotropicais de água doce. Jaboticabal: FUNEP; 2014. p. 253-264. ; FERNANDES & MORON, 2014 Fernandes MN, Moron SE. Respiração e adaptações respiratórias. In: Baldisserotto B, Cyrino JEP, Urbinati EC. Biologia e fisiologia de peixes neotropicais de água doce. Jaboticabal: FUNEP; 2014. p. 203-232. ). Monogeneans (flatworms) are among the most host-specific of parasites in general and may be the most host-specific of all fish parasites ( WHITTINGTON et al., 2000 Whittington ID, Cribb BW, Hamwood TE, Halliday JA. Host-specificity of monogenean (platyhelminth) parasites: a role for anterior adhesive areas? Int J Parasitol 2000; 30(3): 305-320. http://dx.doi.org/10.1016/S0020-7519(00)00006-0. PMid:10719124.
http://dx.doi.org/10.1016/S0020-7519(00...
). The species found in this work were the same as those observed by Godoi et al. (2012) Godoi MMIM, Engracia V, Lizama MAP, Takemoto RM. Parasite-host relationship between the tambaqui (Colossoma macropomum Cuvier 1818) and ectoparasites collected from fish farms in the City of Rolim de Moura, State of Rondônia, Western Amaz, Brazil. Acta Amazon 2012; 42(4): 515-524. http://dx.doi.org/10.1590/S0044-59672012000400009.
http://dx.doi.org/10.1590/S0044-5967201...
in C. macropomum collected from fish farms in the Western Amazon, Brazil. The authors further point out that the specificity of monogeneans in a particular host can be influenced by numerous factors, as different fixing strategies related to mechanical and chemical factors that stimulate the permanence on their hosts. In the present study, no significant correlation was observed between abundance of monogeneans and hematological parameters in contrast to the results found by Montero et al. (2004) Montero FE, Crespo S, Padrós F, Gandara F, Garcıa A, Raga JA. Effects of the gill parasite Zeuxapta seriolae (Monogenea: Heteraxinidae) on the amberjack Seriola dumerili Risso (Teleostei: Carangidae). Aquaculture 2004; 232(1-4): 153-163. http://dx.doi.org/10.1016/S0044-8486(03)00536-2.
http://dx.doi.org/10.1016/S0044-8486(03...
and Tavares-Dias et al. (2008) Tavares-Dias M, Moraes FR, Martins ML. Hematological assessment in four Brazilian teleost fish with parasitic infections, collected in feefishing from Franca, São Paulo, Brazil. B Inst Pesca 2008; 34(2): 189-196. , possibly due to a low parasite load.

The fish louse Dolops geayi is widely distributed in South America, with reports of occurrences in Argentina, Brazil, Paraguay and Venezuela. The present study provides the first record of C. macropomum as a host for D. geayi . However, it should be emphasized that there are no records of tambaquis in natural environments as hosts for this species of Branchiura. Because fish farming consists of a confined environment, it allows these two species (parasite and host) to coexist, which possibly favors parasitism by D. geayi in tambaquis. According to some studies, the parasitic specificity of this species of Branchiura is low when they are in confined environments such as fish farms and aquariums ( RINGUELET, 1943 Ringuelet R. Revisión de los Argulídos Argentinos (Crustácea. Branchiura), con el catálogo de las especies neotropicales. Rev Museo de la Plata 1943; 3(19): 43-99. ; MALTA, 1982, Malta JCO. Os argulídeos (Crustacea: Branchiura) da Amazônia brasileira, 2. Aspectos da Ecologia de Dolops geayi Bouvier, 1897 e Argulus juparanaensis Castro, 1950. Acta Amaz 1982; 12(4): 701-705. http://dx.doi.org/10.1590/1809-43921982124701.
http://dx.doi.org/10.1590/1809-43921982...
1984). All the 29 specimens of D. geayi examined in this study were young and parasitizing the gill cavity, which was the same infestation site that Malta (1982) Malta JCO. Os argulídeos (Crustacea: Branchiura) da Amazônia brasileira, 2. Aspectos da Ecologia de Dolops geayi Bouvier, 1897 e Argulus juparanaensis Castro, 1950. Acta Amaz 1982; 12(4): 701-705. http://dx.doi.org/10.1590/1809-43921982124701.
http://dx.doi.org/10.1590/1809-43921982...
found in four other species of fish (Megalodoras sp., Crenicichla sp., Hoplias malabaricus and Astronotus ocellatus ), which were natural hosts for D. geayi in the Janauacá Lake. We did not find any correlations between parasitism by D. geayi and the hematological and biochemical parameters of tambaquis, which suggests that the mean parasite intensity of 1.7 that we found was insufficient to cause physiological changes. On the other hand, regarding the tambacu hybrid parasitized by Dolops sp., there have been reports of diminished hematocrit and increased concentrations of mean corpuscular hemoglobin, plasma glucose, serum protein, sodium and chlorides, thus resulting in osmoregulatory disorders in the host ( TAVARES-DIAS et al., 2007a Tavares-Dias M, Moraes FR, Onaka EM, Rezende PCB. Changes in blood parameters of hybrid tambacu fish parasitized by Dolops carvalhoi (Crustacea, Branchiura), a fish louse. Vet Arh 2007a; 77(4): 355-363. ).

The condition factor can also be used to detect parasitic species that affect host health ( LIZAMA et al., 2007 Lizama MAP, Takemoto RM, Ranzani-Paiva MJT, Ayroza LMS, Pavanelli GC. Relação parasito-hospedeiro em peixes de pisciculturas da região de Assis, Estado de São Paulo, Brasil. 1. Oreochromis niloticus (Linnaeus, 1757). Acta Sci Biol Sci 2007; 29(2): 223-231. http://dx.doi.org/10.4025/actascibiolsci.v29i2.594.
http://dx.doi.org/10.4025/actascibiolsc...
). However, in the present study there was no correlation between the condition factor and the hematological and biochemical parameters or between the condition factor and the parasite groups in tambaquis.

The variation amplitude of glucose levels in this study was higher than the reference values described for tambaqui by Tavares-Dias (2015) Tavares-Dias M. Parâmetros sanguíneos de referência para espécies de peixes cultivados. In: Tavares-Dias M, Mariano WS. Aquicultura no Brasil: novas perspectivas. São Carlos: Editora Pedro & João; 2015. p. 11-30. . However, the plasma glucose levels had negative correlation with Monogenoidea and Acanthocephala, suggesting that this index is altered in the parasitized fish. This result can be explained by the fact that high levels of parasite infestation promote a stress reaction in the host, with the occurrence of a series of physiological and behavioral responses ( URBINATI et al., 2015 Urbinati EC, Zanuzzo FS, Serra M, Wolkers CPB, Sabioni RE. Avanços da fisiologia do estresse e suas implicações em espécies nativas. In: Tavares‐Dias M, Mariano WS. Aquicultura no Brasil: novas perspectivas. São Carlos: Editora Pedro & João; 2015. p. 381-416. ), including secondary responses as well as changes in glucose and hematological parameters, as demonstrated in the current study. In pirarucus (Arapaima gigas) with polyparasitism, the same pattern was observed, with changes in glucose levels and no changes in total plasma protein levels ( MARINHO et al., 2015 Marinho RGB, Tostes LV, Borges M, Yoshioka ETO, Dias MT. Respostas hematológicas de Arapaima gigas (Pisces: Arapaimidae) parasitados naturalmente por protozoários e metazoários. Biota Amaz 2015; 5(1): 105-108. http://dx.doi.org/10.18561/2179-5746/biotaamazonia.v5n1p105-108.
http://dx.doi.org/10.18561/2179-5746/bi...
). In tambacus parasitized by Dolops sp. (Branchiura), there were increases in plasma glucose and serum protein levels ( TAVARES-DIAS et al., 2007a Tavares-Dias M, Moraes FR, Onaka EM, Rezende PCB. Changes in blood parameters of hybrid tambacu fish parasitized by Dolops carvalhoi (Crustacea, Branchiura), a fish louse. Vet Arh 2007a; 77(4): 355-363. ). In the present study, the range of glucose and total protein levels in tambaquis corroborated those that had previously been reported for tambaquis, tambacus and tambatingas ( TAVARES-DIAS, 2015 Tavares-Dias M. Parâmetros sanguíneos de referência para espécies de peixes cultivados. In: Tavares-Dias M, Mariano WS. Aquicultura no Brasil: novas perspectivas. São Carlos: Editora Pedro & João; 2015. p. 11-30. ; OBA-YOSHIOKA et al., 2017 Oba-Yoshioka ET, Costa R, Borges M, Tavares-Dias M. Blood variables of hybrid tambacu farmed in Amapá state, Northern Brazil. Vet Zootec 2017; 24(1): 201-208. ). It can also be highlighted that glucose and total protein levels may vary according to species, sex, state of gonad development, seasonality, diet and management ( MARINHO et al., 2015 Marinho RGB, Tostes LV, Borges M, Yoshioka ETO, Dias MT. Respostas hematológicas de Arapaima gigas (Pisces: Arapaimidae) parasitados naturalmente por protozoários e metazoários. Biota Amaz 2015; 5(1): 105-108. http://dx.doi.org/10.18561/2179-5746/biotaamazonia.v5n1p105-108.
http://dx.doi.org/10.18561/2179-5746/bi...
; OBA-YOSHIOKA et al., 2017 Oba-Yoshioka ET, Costa R, Borges M, Tavares-Dias M. Blood variables of hybrid tambacu farmed in Amapá state, Northern Brazil. Vet Zootec 2017; 24(1): 201-208. ).

In the present study, the tambaquis farmed in intensive system presented moderate infestation by Monogenoidea, Acanthocephala and Branchiura, and the correlations between parasitism and blood variables suggests worsening of fish health condition. The application of information on occurrences of hypochromic anemia, thrombocytopenia can be used to guide the diagnosis of these parasitosis. Assessing fish-farming facilities on a regular basis is strongly recommended as a prophylactic measure to avoid diminished fish performance and productivity indices among farmed tambaqui. The present study also provides the first record of D. geayi parasitizing tambaquis in captivity.

Acknowledgements

The authors thank Empresa Brasileira de Pesquisa Agropecuária - Embrapa (MP2 - 02.13.09.003.00.00) for financial support, Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq 305869/2014-0) for the grant to M.L. Martins, the technician Iraní Morais and PhD student Franmir Brandão for collection help and physiological analysis, and Kátia Sousa and Liliane Ferreira for their aid in parasite identification.

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Publication Dates

  • Publication in this collection
    08 Nov 2018
  • Date of issue
    Oct-Dec 2018

History

  • Received
    07 June 2018
  • Accepted
    11 Sept 2018
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