Introduction

The common snook, Centropomus undecimalis (Bloch, 1792), is distributed in tropical and subtropical areas of the west coast of the Atlantic Ocean, from Cape Canaveral, Florida, USA, to southern Brazil (^{ALVAREZ-LAJONCHERE & TSUZUKI, 2008}). It is considered to be a diadromous, euryhaline, stenothermic and estuarine-dependent fish found in rivers, estuaries and coastal lagoons and along rocky shores (^{McMICHAEL et al., 1989}; ^{POPE et al., 2006}). The common snook is considered to be the largest and also the fastest growing snook of all the species of the genus Centropomus in the Americas, and is a sporting fish of high market value (^{TUCKER, 2005}). The species has received high priority with regard to conservation and aquaculture issues, due to its ecological and economic characteristics (^{WINNER et al., 2010}).

With the intensification of fish farming, sanitary problems have become more frequent, making it necessary to periodically monitor fish health conditions. On this view, hematological investigations contribute to the evaluation of the organism’s state of defense for facing the common challenges in aquaculture, in which fish are exposed to high stocking densities, parasites, changes to environmental quality and to the physical-chemical parameters of the water, and unbalanced diet (^{RANZANI-PAIVA et al., 2013}).

Hematological parameters are recognized as secondary indicators of stress when increased red blood cell count, hematocrit, hemoglobin concentration and leukopenia are observed (^{WEDEMEYER et al., 1990}; ^{WOJTASZEK et al, 2002}; ^{PIERSON et al., 2004}). For C. undecimalis, studies relating to hematology under fish-farming conditions are scarce. However, some laboratory studies have been conducted on the congeneric species C. parallelus (^{RANZANI-PAIVA et al., 2008}; SANTOS et al., ²⁰⁰⁹, ²⁰¹²; ^{MARTINS et al., 2010}; ^{BARBOSA et al., 2011}; ^{SILVA et al., 2011}). Recently, ^{Dotta et al. (2015)}evaluated the hematological parameters of the mutton snapper (Lutjanus analis) reared in cages, and observed significant increases in the hematocrit and total numbers of leukocytes and monocytes after 30 days of rearing, in comparison with fish in their natural environment.

In South America, knowledge of the parasitic fauna of farmed marine fish can still be considered to be at an initial stage despite the great ichthyological diversity and number of potential host species. Most research has been in relation to taxonomic aspects of helminth species, mainly developed in Brazil, Chile, Peru and Argentina (^{LUQUE, 2004}).

Few studies have described and identified parasites in the common snook. ^{Tavares & Luque (2003)} identified a new species of Acantholochus (Copepoda: Bomolochidae) in the coastal zone of the state of Rio de Janeiro, Brazil. The trematode Acanthocollaritrema umbilicatum Travassos, Freitas & Bührnheim 1965 (Digenea: Acanthocollaritrematidae) was collected in the intestine of C. undecimalis reared in Itamaracá, Pernambuco (^{ROBALDO & PADOVAN, 1998}). The ecological community of metazoan parasites of the common snook in the coastal area of Rio de Janeiro was studied by ^{Tavares & Luque (2004)}, who found nine species of parasites in 79 fish analyzed. ^{Fujimoto et al. (2009)} evaluated the hematological parameters and parasitic fauna of C. undecimalis in the Bragantina region, state of Pará, Brazil, and reported a decrease in the RBC count, lymphopenia and neutrophilia in fish parasitized with Rhabdosynochus sp. (Monogenea), Bucephalus sp. (Digenea), Cucullanus sp. (Nematoda) and Lernanthropidae (Crustacea). Several studies have shown the influence of salinity on the growth and survival of marine fish (^{DENDRINOS & THORPE, 1985}; ^{McCORMICK et al., 1989}; ^{IMSLAND et al., 2001}). Additionally, temperature has been found to have a significant effect on numerous physiological processes in fish (^{BRETT & GROVES, 1979}). It is considered to be one of the most important environmental parameters, given that it directly affects the metabolism, oxygen consumption, growth and survival of marine organisms (^{JIAN et al., 2003}).

In this context, studies relating to sanitary aspects of the common snook are required in order to gain an understanding of the state of health of this fish under farmed conditions and in fluctuating environments. The aim of this study was to evaluate the relationship between hematological parameters and the mean abundance of gill parasites in the common snook reared at different temperatures and salinities in a recirculating aquaculture system.

Materials and Methods

Results

The water quality parameters were maintained at acceptable levels for the species. There were no significant differences among the treatments with regard to dissolved oxygen concentration (6.2 ± 1.0 mg.L^-1), pH (7.8 ± 0.2), N-NH₃ (0.1 ± 0.1 mg.L^-1), N-NO₂ (0.1 ± 0.1 mg.L^-1), N-NO₃ (0.6 ± 0.3 mg.L^-1) or PO₄ (1.3 ± 0.5 mg.L^-1). Significant differences were only observed in relation to the parameters that are directly affected by increased salinity, with higher values for higher salinities, such as alkalinity (0 ppt: 47.9 ± 5.3; 15 ppt: 66.0 ± 9.2; and 32 ppt: 76.6 ± 8.3 mg.L^-1 CaCO₃). The parameters obtained during this study were 28.0 ± 0.4 °C and 24.9 ± 0.9 °C for water temperature and 0.3 ± 0.1 ppt, 14.9 ± 1.5 ppt and 32.5 ± 3.5 ppt for salinity.

No parasites were found on the skin and fins but the monogenean Rhabdosynochus rhabdosynochus Mizelle and Blatz, 1941 (Dactylogyridae: Diplectanidae) was observed on the gills. The highest prevalence (100%) was observed in fish at 28 °C/15 ppt, 28 °C/32 ppt and 25 °C/15 ppt, being significantly different (p < 0.05) from the fish at 25 °C/32 ppt (75%). The mean intensity of infection differed significantly among the experimental conditions, such that the lowest values were among the fish at 28 °C/0 ppt (9.2 ± 10.2) and the highest were among those at 28 °C/15 ppt (27.1 ± 6.2). The mean abundance was lower (p < 0.05) among fish at 28 °C/0 ppt and 25 °C/32 ppt (7.7 ± 9.8 and 8.2 ± 7.3, respectively) (Table 1).

The average values for weight and length were greater from the fish maintained at higher temperature and did not differ with regard to salinity (Table 2). Significant difference on weight and length of examined fish could be associated with temperature and salinity conditions once no difference was observed among fish maintained in 28 and 25 °C. The hematological analysis showed that there were higher values for RBC, hematocrit and WBC in fish at 28 °C/15 ppt and 28 °C/32 ppt than among those at 25 °C/15 ppt (Table 2). Hemoglobin and MCHC were higher (p < 0.05) in the fish at 25 °C/0 ppt (11.4 ± 2.0 and 57.8 ± 20.8 respectively) than in the fish maintained at 28 °C/15 ppt and 28 °C/32 ppt. Total thrombocytes were lower in the fish at T6 (2.9 ± 1.8), being significantly different from those at 28 °C/0 ppt and 28 °C/15 ppt (7.1 ± 2.7 and 6.3 ± 3.1). No difference in MCV was found among the experimental conditions.

The mean abundances of R. rhabdosynochus, hematocrit and RBC showed positive correlations (p < 0.05) with temperature (ρ = 0.3908; ρ = 0.4771 and ρ = 0.2812 respectively) (Table 3). Mean abundance showed negative correlations with hemoglobin (ρ = -0.3567) and MCHC (ρ = -0.2684). There was no correlation between abundance and salinity among the experimental conditions (ρ = -0.0204).

Discussion

Monogenean parasites are mostly found parasitizing both wild and cultivated fish and are considered to be important pathogenic agents in aquaculture (^{TURGUT, 2012}). They feed on the epithelial cells from the body surface and gills, or blood in some cases (^{EIRAS, 1994}). The genus Rhabdosynochus was originally described by ^{Mizelle & Blatz (1941)} in C. undecimalis in East Florida, USA. In the present study, we recorded R. rhabdosynochus in the gills of common snook, but other species can be found in Brazil, such as R. hargisi, R. hudsoni and Rhabdosynochus sp. in common snook from Itamaracá, Pernambuco (^{KRITSKY et al., 2001}). ^{Abdallah et al. (2012)} described R. guanduensis on the gills of common snook examined in Guandu river, state of Rio de Janeiro. ^{Kritsky et al. (2010)} proposed a redescription of the genus based on the fish specimens examined from Centropomidae fish in Florida, USA, and ^{Mendoza-Franco et al. (2008)} described R. alterinstitus, R. lituparvus, R. volucris and R. siliquaus parasitizing the gills of Centropomus nigrescensand Centropomus robalito, collected on the coast of Mexico.

Several factors influence monogenean egg eclosion and depend on the parasite species. Turbulence, photoperiod, temperature and mucus released by the host can stimulate eclosion and determine the success of parasitism (^{EIRAS, 1994}).

Temperature is considered to be one of the most important factors in determining parasite abundance (^{OZTURK & ALTUNEL, 2006}). The fish examined in this study showed a positive correlation between monogenean abundance and temperature. Fish maintained at 28 °C were more parasitized than those kept at 25 °C, independently of the salinity.

In fact, several studies have focused on the correlation between temperature and parasite abundance and/or egg eclosion (^{GANNICOTT & TINSLEY, 1998}). These authors observed greater viability of eggs of Discocotyle sagittata in rainbow trout (Oncorhynchus mykiss) kept at 13-18 °C. Similarly, ^{Özer & Erdem (1999)} reported higher prevalence of Dactylogyrus anchoratus in Cyprinus carpio in summer (25.5-26.2 °C) than in winter (13.6-12.7 °C). Our results are also supported by the findings of ^{Barker & Cone (2000)}, who reported that prevalence and abundance had a positive correlation with water temperature (10-24 °C).

In this study, salinity did not influence parasite abundance, and this may have been related to the fact that the common snook is considered to be a euryhaline and diadromous species (^{McMICHAEL et al., 1989}; ^{POPE et al., 2006}). These fish can be found inhabiting environments of variable salinities (^{McMICHAEL et al., 1989}) and consequently the parasite species may have developed the same resistance over the years due to coevolution.

In the study by ^{Violante-González et al. (2010)}, parasite richness in C. nigrescens was evaluated at five different sites in a coastal lagoon located in Guerrero, Mexico. At sites where salinity was 15 ppt, the authors recorded greater diversity of the monogeneans R. alterinstitus and Cornutohaptor nigrescensi than at sites with salinity of 6 ppt.

Few studies on fish hematology in relation to sanitary issues have been conducted in Brazil, especially in relation to C. undecimalis. ^{Fujimoto et al. (2009)} reported that this metazoan parasite was found in common snook from Bragança, Pará, in northeastern Brazil. Nevertheless, other studies have focused on C. parallelus (^{RANZANI-PAIVA et al., 2008}; SANTOS et al., ²⁰⁰⁹, ²⁰¹²; ^{MARTINS et al., 2010}; ^{BARBOSA et al., 2011}; ^{SILVA et al., 2011}). The variations in the hematological parameters in freshwater and marine fishes may be related to length, gender or maturation (^{RANZANI-PAIVA & SOUZA, 2004}).

In analyzing the hematological parameters, the fish kept at a lower temperature (25 °C) showed decreased RBC counts and hematocrit levels without positive correlation with the abundance of R. rhabdosynochus. In contrast, ^{Fujimoto et al. (2009)} observed decreased values for RBC and hematocrit in parasitized common snook.

The relationships between hematocrit and RBC, and between hemoglobin and hematocrit, are known as hematimetric indices. These are used to classify anemia, which is an unpaired condition of the blood relating to transporting oxygen to tissues (^{RANZANI-PAIVA et al., 2013}). In this study, these parameters did not show any correlation with parasite abundance, except for hemoglobin, which that showed a negative correlation.

Hematological alterations can be related to the eutrophication level of the environment, as observed by ^{Seriani et al. (2013)} in common snook examined in Cananéia and São Vicente, state of São Paulo. Fish from São Vicente, which was the most eutrophicated region, showed the highest values for hematocrit, mean corpuscular volume, WBC and RBC.

In the present study, fish were maintained under good conditions in the recirculation system under controlled water quality. The low numbers of parasites observed (1 to 33) may have been strongly related to the experimental cultivation conditions. It can be inferred that a recirculation system is recommended for commercial maintenance of common snook, avoiding economic losses caused by monogeneans, since the water quality is monitored.