Hematological changes in Eleginops maclovinus during an experimental Caligus rogercresseyi infestation

Alterações hematológicas em Eleginops maclovinusdurante uma infestação experimental com Caligus rogercresseyi

Patricio Peña-Rehbein Karin Ruiz Alexander Ortloff María Isabel Pizarro Carolina Navarrete About the authors

Abstracts

Eleginops maclovinus has been an important fishery resource in Chile since 1957. Caligus rogercresseyi is one of the most prevalent ectoparasite species found on E. maclovinus. Hematocrit, hemoglobin level, red blood cell count (RBC), white blood cell count (WBC), mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC) and differential white blood cell count were determined before and after an experimental infestation withC. rogercresseyi. We found significant differences in the hemoglobin level, WBC, MCV, MCH, MCHC, hematocrit level and RBC between infested and uninfested fish. Furthermore correlations between number of C. rogercresseyi with hematocrit, MCHC, neutrophil, eosinophil and lymphocyte counts were found. Hematological reference ranges of E. maclovinus in captivity conditions were also established.

Blood parameters; erythrocytes; leukocytes


Eleginops maclovinus tem sido um importante recurso pesqueiro no Chile desde 1957. Caligus rogercresseyi é uma das espécies ectoparasitas mais comumente encontradas em E. maclovinus. Hematócrito, nível de hemoglobina, contagem de eritrócitos, contagem de leucócitos, volume corpuscular médio (VCM), hemoglobina corpuscular média (HCM), concentração de hemoglobina corpuscular média (CHCM) e contagem diferencial de leucócitos foram determinadas antes e após uma infestação experimental comC. rogercresseyi. Foram encontradas diferenças significativas no nível de hemoglobina, leucócitos, VCM, HCM, CHCM, hematócrito e eritrócitos entre peixes infestados e não infestados. Além disso, foram encontradas correlações entre o número de C. rogercresseyi com hematócrito, CHCM, neutrófilos, eosinófilos e linfócitos. Foram estabelecidos intervalos de referência para E. maclovinus em condições de cativeiro.

Parâmetros sanguíneos; eritrócitos; leucócitos


Introduction

The Chilean rock cod, also known as robalo (Eleginops maclovinus), is a common fish in littoral zones, estuaries and rivers (under tidal effects) of southern South America, including the Falkland islands (PEQUEÑO et al., 2010). Although this species is traditionally considered an opportunistic benthic omnivore, recent research indicates that juveniles and adults are opportunistic carnivores capable of feeding in both marine and freshwater environments (EASTMAN; LANNOO, 2008Eastman JT, Lannoo MJ. Brain and sense organ anatomy and histology of the Falkland Islands mullet, Eleginops maclovinus (Eleginopidae), the sister group of the Antarctic notothenioid fishes (Perciformes: Notothenioidei). J Morphol 2008; 269(1): 84-103.).E. maclovinus is a coastal species generally associated with estuarine systems, has been exploited as a fishery resource in Chile since 1957 (GACITÚA et al., 2008Gacitúa S, Oyarzún C, Veas R. Análisis multivariado de la morfometría y merística del robalo Eleginops maclovinus (Cuvier, 1830). Rev Biol Mar Oceanogr 2008; 43(3): 491-500. http://dx.doi.org/10.4067/S0718-19572008000300008
http://dx.doi.org/10.4067/S0718-19572008...
) and also has a great potential to be farmed (VALENZUELA et al., 1999Valenzuela A, Silva V, Oyarzún C. Caracterización cualitativa y cuantitativa de células sanguíneas de robalo Eleginops maclovinus (Valenciennes, 1830) (Pisces, Eleginopsidae) en la desembocadura del río Biobio. Rev Biol Mar Oceanogr 1999; 34(2): 261-267.).

Caligus species is found in continental waters on native fish (E. maclovinus) as well as on a cultured species,Oncorhynchus mykiss, from the south of Chile (CARVAJAL et al., 1998). C. rogercresseyi (Copepoda: Caligidae) is one of the most prevalent ectoparasite species found on E. maclovinus (CARVAJAL et al., 2001Carvajal J, Ruiz G, Sepúlveda F. Symbiotic relationship between Udonella sp. (Monogenea) and Caligus rogercresseyi (Copepoda), a parasite of the chilean rock cod Eleginops maclovinus. Arch Med Vet 2001; 33(1): 31-36. http://dx.doi.org/10.4067/S0301-732X2001000100003
http://dx.doi.org/10.4067/S0301-732X2001...
; HENRIQUEZ et al., 2011Henriquez VP, Gonzalez MT, Licandeo R, Carvajal J. Metazoan parasite communities of rock cod Eleginops maclovinus along southern Chilean coast and their use as biological tags at a local spatial scale. J Fish Biol 2011; 79(7): 1851-1865. http://dx.doi.org/10.1111/j.1095-8649.2011.03126.x
http://dx.doi.org/10.1111/j.1095-8649.20...
). Parasites negatively influence host fitness, and in response, hosts develop anti-parasitic defenses, for example, a functional immune system, to reduce the fitness cost induced by parasitism (SHELDON; VERHULST, 1996Sheldon BC, Verhulst S. Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 1996; 11(8): 317-321. http://dx.doi.org/10.1016/0169-5347(96)10039-2
http://dx.doi.org/10.1016/0169-5347(96)1...
). Sea louse cause a local inflammatory response and blood loss at the site of attachment but do not appear to suppress host defense mechanisms during the early stages of infestation (TAVARES-DIAS et al., 2007Tavares-Dias M, Moraes FR, Onaka E, Rezende PCB. Changes in blood parameters of hybrid tambacu fish parasitized by Dolops carvalhoi (Crustacea, Branchiura), a fish louse. Vet Arhiv 2007; 77(4): 355-363.; WAGNER et al., 2008). Parasitic infestations can influence blood parameters, such as anemia and white cells count unbalances in other host fishes (HORTON; OKAMURA, 2003; MARTINS et al., 2004Martins ML, Tavares-Dias M, Fujimoto RY, Onaka EM, Nomura DT. Haematological alterations of Leporinus macrocephalus (Osteichtyes: Anostomidae) naturally infected by Goezia leporini (Nematoda: Anisakidae) in fish pond. Arq Bras Med Vet Zootec 2004; 56(5): 640-646. http://dx.doi.org/10.1590/S0102-09352004000500011
http://dx.doi.org/10.1590/S0102-09352004...
; SILVA-SOUZA et al., 2000;TAVARES-DIAS et al., 1999Tavares-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/S0101-81751999...
, 2002Tavares-Dias M, Moraes FR, Martins ML, Santana AE. Haematological changes in Oreochromis niloticus (Osteichthyes: Cichlidae) with gill ichthyophthiriasis and saprolegniosis. Bol Inst Pesca 2002; 28(1): 9., 2007Tavares-Dias M, Moraes FR, Onaka E, Rezende PCB. Changes in blood parameters of hybrid tambacu fish parasitized by Dolops carvalhoi (Crustacea, Branchiura), a fish louse. Vet Arhiv 2007; 77(4): 355-363.; WAGNER et al., 2008).

The aim of this work is to study the hematological changes in E. maclovinus caused by C. rogercresseyi-induced experimental infestation.

Materials and Methods

The experimental hatchery of Fundación Chile in Quillaipe (Región de los Lagos, Chile) has E. maclovinus stocks that were grown since hatching. In this study 160 E. maclovinus (weight = 488 ± 138 g, length = 32.9 ± 2.89 cm) belonging to this group were used. They have always been fed with an Ewos transfer commercial diet. Prior to the experiment fish were acclimatized to the experimental tank for two weeks. During acclimatization and experimental periods, fish were maintained in a 3 m3 tank with a density of 26.03 kg m–3. The maximum density for E. maclovinusfarming is 30 kg m–3 (Fundación Chile unpublished results). The water temperature during the experiment was 12.7 ± 0.8 °C. Fish were infested with copepodid stage C. rogercresseyi parasites (150 copepodid/fish), and infestation was maintained up to 4 weeks post-infestation (wpi).

Blood samples were taken from the caudal vessel (WEISS; WARDROP, 2010Weiss D, Wardrop K. Schalm's Veterinary Hematology. 6th ed. Singapore: Wiley-Blackwell; 2010.) one week pre (basal) and 2, 3 and 4 weeks post infection (wpi) (n=40 per each sample time). The fish were sedated using benzocaine (50 mg L–1) prior to bleeding. Once the fishes were sampled (n=40) they were placed in a different tank to avoid fish reuse; afterwards water level corrections were performed to keep a constant density during the experiment.

Blood samples were stored in heparinized Eppendorf tubes that were transported at 4 °C and analyzed within 12 h of collection at the Catholic University of Temuco. The hematocrit, hemoglobin level, red blood cell count (RBC), white blood cell count (WBC), mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), mean corpuscular hemoglobin concentration (MCHC) and differential white cell count were determined using standard methods (BAIN et al., 2011Bain BJ, Bates I, Laffan MA, Lewis SM. Dacie and Lewis Practical Haematology. 11th ed. Philadelphia: Churchill Livingstone; 2011.; TODD et al., 1979Todd J, Sanford A, Davison I. Clinical Diagnosis and Management by Laboratory Methods. 16th ed. Philadelphia: Saunders; 1979.).

Statistical analysis was performed using a one-way ANOVA and the Bonferroni post-test to make comparisons between the groups infested and uninfested. Associations of parasite count with neutrophil, eosinophil, and lymphocyte counts; hematocrit; and MCHC levels were tested using the Spearman correlation (rs) and linear regression. Statistical significance between the groups was indicated by p<0.05. All statistical analyses were performed using GraphPad Prism v5.0 (GraphPad Software Inc, CA, USA).

Results

The C. rogercresseyi infestation site was the skin ofE. maclovinus. The mean parasite number ± standard deviation per fish at 2nd wpi was 6.73 ± 5.71, at 3rd wpi was 4.14 ± 3.58 and at the end of experiment was 1.11 ± 1.06.

The mean values and ranges of the blood parameters and white blood cells counts for uninfested and C. rogercresseyi-infested E. maclovinus are shown in Table 1. Table 2 describes the hematological reference ranges in E. maclovinus under cultivation.

Table 1.
Hematological parameters of uninfested and Caligus rogercresseyi-infested Eleginops maclovinus. Mean ± standard deviation (SD). Different lowercase letters indicate significant differences.

Table 2.
Reference ranges of hematological parameters in Eleginops maclovinus (n=40) under farm conditions. Lower (25th) and upper percentiles (75th).

Our results showed significant differences between infested and uninfested fish in hemoglobin levels (p=0.0104; df=154; F=3.883), WBC counts (p=<0.0001; df=154; F=37.12), MCV (p=<0.0001; df=154; F=8.3), MCH (p=<0.0001; df=154; F=21), MCHC (p=<0.0001; df=154; F=25), hematocrit (p=<0.0001; df=154; F=9.935) and RBC counts (p=<0.0001; df=154; F=14.47). No significant differences were observed in lymphocyte, neutrophil, eosinophil, basophil and monocyte counts.

Infested fish show an increase in WBC counts up to the 3rd wpi and an increase in eosinophils and basophils in the second week, with a subsequent decline to the 4th wpi, a decrease in neutrophils over all 4 wpi, an increase in lymphocytes at 4 wpi, and a decrease in monocytes up to the 3rd wpi followed by a slight increase in the last wpi. Red blood cell parameters (hemoglobin, MCV, MCH and MCHC) increased during infestation; however, RBC count and hematocrit decreases during infestation. The most common leukocytes in uninfested group (basal) were lymphocytes, followed by neutrophils, monocyte, basophils and a small perceptual of eosinophils. However, in the infested group, the most abundant cell types were lymphocytes, neutrophils and eosinophils (Table 1).

Our results demonstrate that the number of C. rogercresseyi in the body was correlated with the neutrophil counts (r=0.4612; p=0.0007), eosinophil counts (r=0.3628; p=0.0082), hematocrit levels (r=0.2333; p=0.0195), MCHC (r=−0.2866; p=0.053) and lymphocyte counts (r=−0.3043; p=0.0226). No correlation was observed between the C. rogercresseyinumber and red blood cell counts, hemoglobin levels, MVC, MCH, and white blood cell, monocyte and basophil counts (Figure 1).

Figure 1.
Correlations between Caligus rogercresseyi number and hematological parameters of Eleginops maclovinus.

Discussion

Studies performed by Valenzuela et al. (1999)Valenzuela A, Silva V, Oyarzún C. Caracterización cualitativa y cuantitativa de células sanguíneas de robalo Eleginops maclovinus (Valenciennes, 1830) (Pisces, Eleginopsidae) en la desembocadura del río Biobio. Rev Biol Mar Oceanogr 1999; 34(2): 261-267. and Valenzuela et al. (2003) have characterized blood cells from wild fish native to Chile. To date there are no studies of the differences in the hematologic parameters between uninfested and infested captive robalo E. maclovinus with C. rogercresseyi.

The infestation site by C. rogercresseyi was the skin ofE. maclovinus, this is consistent with Nolan et al. (2000)Nolan DT, Ruane NM, Van Der Heijden Y, Quabius ES, Costelloe J, Bonga SEW. Juvenile Lepeophtheirus salmonis (Krøyer) affect the skin and gills of rainbow trout Oncorhynchus mykiss (Walbaum) and the host response to a handling procedure. Aquacult Res 2000; 31(11): 823-833. http://dx.doi.org/10.1046/j.1365-2109.2000.00515.x
http://dx.doi.org/10.1046/j.1365-2109.20...
, Costello (2006), Hamilton-West et al. (2012) and Venmathi Maran et al. (2012).

When compared our infested fish with data from Valenzuela et al. (1999)Valenzuela A, Silva V, Oyarzún C. Caracterización cualitativa y cuantitativa de células sanguíneas de robalo Eleginops maclovinus (Valenciennes, 1830) (Pisces, Eleginopsidae) en la desembocadura del río Biobio. Rev Biol Mar Oceanogr 1999; 34(2): 261-267., no differences was found in lymphocyte, eosinophil and monocyte counts, this suggests that the study by Valenzuela et al. (1999)Valenzuela A, Silva V, Oyarzún C. Caracterización cualitativa y cuantitativa de células sanguíneas de robalo Eleginops maclovinus (Valenciennes, 1830) (Pisces, Eleginopsidae) en la desembocadura del río Biobio. Rev Biol Mar Oceanogr 1999; 34(2): 261-267. was made with wild infested E. maclovinus. On the other hand, we found statistically significant differences in lymphocyte (p<0.0001, df=185, F=23.1), eosinophil (p<0.0001, df=185, F=15.1) and monocyte counts (p<0.0001, df=185, F=78.9) when compared Valenzuela et al. (1999)Valenzuela A, Silva V, Oyarzún C. Caracterización cualitativa y cuantitativa de células sanguíneas de robalo Eleginops maclovinus (Valenciennes, 1830) (Pisces, Eleginopsidae) en la desembocadura del río Biobio. Rev Biol Mar Oceanogr 1999; 34(2): 261-267. results with our uninfested (basal) fish group. The values of uninfested group are proposed as reference ranges for uninfested E. maclovinus maintained in captivity (Table 2). Blood parameters, although not regularly used in fish medicine, can provide substantial diagnostic information once reference intervals are established.

In both the infested and basal (uninfested) groups, we found that lymphocytes are the most abundant leukocytes in the peripheral blood; however, eosinophils were scarce in the uninfested fishes but abundant in the infested ones, which correlates with other studies in fishes (ALVAREZ-PELLITERO, 2008; EZE EVELYN et al., 2012; PIERRARD et al., 2012; RUANE et al., 2000Ruane NM, Nolan DT, Rotllant J, Costelloe J, Wendelaar Bonga SE. Experimental exposure of rainbow trout Oncorhynchus mykiss (Walbaum) to the infective stages of the sea louse Lepeophtheirus salmonis (Krøyer) influences the physiological response to an acute stressor. Fish Shellfish Immunol 2000; 10(5): 451-463.; SILVA-SOUZA et al., 2000). Neutrophils decrease steadily during the 4 weeks of infestation, which is consistent with a study by 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. Bol Inst Pesca 2008; 34(2): 189-196.. This decrease indicates that neutrophils are often the first leukocytes to migrate to the site of parasite infestation (TAVARES-DIAS et al., 2008Tavares-Dias M, Moraes FR, Martins ML. Hematological Assessment in Four Brazilian Teleost Fish with Parasitic Infections, Collected in Feefishing from Franca, São Paulo, Brazil. Bol Inst Pesca 2008; 34(2): 189-196.; WITESKA et al., 2010Witeska M, Kondera E, Lugowska K. The effects of ichthyophthiriasis on some haematological parameters in common carp. Turk J Vet Anim Sci 2010; 34(3): 267-271.). WBC counts increase significantly in infested E. maclovinus at 2, 3 and 4 wpi, correlating with the studies by Jori and Mohamad (2008)Jori MM, Mohamad ET. The effect of Hamatopeduncularia sp. and Caligus sp. on some blood parameters of Arius bilineatus (Val., 1840). Mesopot J Mar Sci 2008; 23(2): 269-277. and Harikrishnan et al. (2012). The RBC counts decrease during theC. rogercresseyi infestation, which is similar to studies of other parasites (HORTON; OKAMURA, 2003; MARTINS et al., 2004Martins ML, Tavares-Dias M, Fujimoto RY, Onaka EM, Nomura DT. Haematological alterations of Leporinus macrocephalus (Osteichtyes: Anostomidae) naturally infected by Goezia leporini (Nematoda: Anisakidae) in fish pond. Arq Bras Med Vet Zootec 2004; 56(5): 640-646. http://dx.doi.org/10.1590/S0102-09352004000500011
http://dx.doi.org/10.1590/S0102-09352004...
; TAVARES-DIAS et al., 2002Tavares-Dias M, Moraes FR, Martins ML, Santana AE. Haematological changes in Oreochromis niloticus (Osteichthyes: Cichlidae) with gill ichthyophthiriasis and saprolegniosis. Bol Inst Pesca 2002; 28(1): 9.). Hematocrit and electrolyte levels are secondary indicators of chronic stress, indicating the osmoregulatory status of the fish (TAVARES-DIAS et al., 2007Tavares-Dias M, Moraes FR, Onaka E, Rezende PCB. Changes in blood parameters of hybrid tambacu fish parasitized by Dolops carvalhoi (Crustacea, Branchiura), a fish louse. Vet Arhiv 2007; 77(4): 355-363.). The hematocrit reduction in infested fish can be explained by osmoregulatory failure as a result of exposed lesions (GRIMNES; JAKOBSEN, 1996Grimnes A, Jakobsen PJ. The physiological effects of salmon lice infection on post-smolt of Atlantic salmon. J Fish Biol 1996; 48(6): 1179-1194. http://dx.doi.org/10.1111/j.1095-8649.1996.tb01813.x
http://dx.doi.org/10.1111/j.1095-8649.19...
) or blood ingestion (JONES; GRUTTER, 2005Jones CM, Grutter AS. Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. J Fish Biol 2005; 66(3): 860-864. http://dx.doi.org/10.1111/j.0022-1112.2005.00640.x
http://dx.doi.org/10.1111/j.0022-1112.20...
).

Higher values of MCV, MCH and MCHC was found in infested fish when compared to uninfested fish, this is probably due to the continued development in RBC which increase in size and hemoglobin content with time (WEISS; WARDROP, 2010Weiss D, Wardrop K. Schalm's Veterinary Hematology. 6th ed. Singapore: Wiley-Blackwell; 2010.).

Positive correlations found between C. rogercresseyinumber and neutrophil count, could be explained by the hyperplastic and inflammatory responses involving rich neutrophil infiltration as response toLepeophtheirus salmonis observed in salmonids (WOO; BUCHMANN, 2011Woo P, Buchmann K. Fish Parasites: Pathobiology and Protection. CAB International; 2011.). The positive correlation with eosinophils counts is due to that eosinophils are frequently involved in parasite disease responses (ALVAREZ-PELLITERO, 2008; THRALL et al., 2012Thrall MA, Weiser G, Allison RW, Campbell TW. Veterinary Hematology and Clinical Chemistry. 2nd ed. Ames: Wiley-Blackwell; 2012.). So, hematocrit positive correlation with parasite number is consistent with osmoregulatory failure as a result of exposed lesions or blood ingestion (GRIMNES; JAKOBSEN, 1996Grimnes A, Jakobsen PJ. The physiological effects of salmon lice infection on post-smolt of Atlantic salmon. J Fish Biol 1996; 48(6): 1179-1194. http://dx.doi.org/10.1111/j.1095-8649.1996.tb01813.x
http://dx.doi.org/10.1111/j.1095-8649.19...
;JONES; GRUTTER, 2005Jones CM, Grutter AS. Parasitic isopods (Gnathia sp.) reduce haematocrit in captive blackeye thicklip (Labridae) on the Great Barrier Reef. J Fish Biol 2005; 66(3): 860-864. http://dx.doi.org/10.1111/j.0022-1112.2005.00640.x
http://dx.doi.org/10.1111/j.0022-1112.20...
). Negative correlation between number of C. rogercresseyi and MCHC is probably an indication of RBC swelling and/or a decrease in hemoglobin synthesis (KUMAR; RAMULU, 2013Kumar MP, Ramulu KS. Haematological changes in Pangasius hypophthalmus infected with Aeromonas hydrophila. Int J Food, Agriculture Vet Sci 2013; 3(1): 70-75.). The negative correlation of lymphocytes count with C. rogercresseyi is explained by the migration of lymphocytes into peripheral tissues such as skin and gills which has been reported in Atlantic salmon infected with adult L. salmonisand other salmonids (RUANE et al., 2000Ruane NM, Nolan DT, Rotllant J, Costelloe J, Wendelaar Bonga SE. Experimental exposure of rainbow trout Oncorhynchus mykiss (Walbaum) to the infective stages of the sea louse Lepeophtheirus salmonis (Krøyer) influences the physiological response to an acute stressor. Fish Shellfish Immunol 2000; 10(5): 451-463.).

In conclusion, this study has demonstrated differences betweenCaligus rogercresseyi-infected and uninfected E. maclovinus in the hematological parameters RBC and WBC counts, hemoglobin, MCV, MCH, MCHC and hematocrit. The WBC count increased during infection and were mainly composed by lymphocytes, neutrophils, and eosinophils. Neutrophils, eosinophils and hematocrit increased with parasites number, confirming the importance of these leukocytes in the response against C. rogercresseyi. The Chilean rock cod, also known as robalo

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Publication Dates

  • Publication in this collection
    Jul-Sep 2013

History

  • Received
    14 Apr 2013
  • Accepted
    14 Aug 2013
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