Brazilian Journal of Animal and Environmental Research 625 ISSN: 2595-573X
Production Performance and hematological analysis of Zapteryx brevirostris in a Closed System
Desempenho Produtivo e Hemograma da Zapteryx brevirostris em Sistema Fechado
DOI: 10.34188/bjaerv4n1-053
Recebimento dos originais: 20/11/2020 Aceitação para publicação: 20/12/2020
Tais Pereira de Sousa Lima Mestre em Aquicultura e Pesca pelo Instituto de Pesca/APTA/SAAESP Instituto de Pesca/APTA/SAAESP Av. Bartolomeu de Gusmão, 192 - Ponta da Praia, Santos-SP, Brasil [email protected]
Carlos Eduardo Malavasi Bruno Doutor em Ciências pela Universidade de São Paulo/Departamento de Anatomia dos Animais Domésticos e Silvestres da Faculdade de Medicina Veterinária e Zootecnia. Instituto Pau Brasil de História Natural Rua Bolívia, 545, Guararema - SP, Brasil [email protected]
Venâncio Guedes de Azevedo Doutor em Ciências pela Universidade de São Paulo/ Instituto Oceanográfico Instituto de Pesca/APTA/SAAESP. Núcleo Regional de Pesquisa do Litoral Norte Estrada Joaquim L. M. C. Neto, 2275. Itaguá, Ubatuba-SP, Brasil [email protected]
Alberto Ferreira de Amorim Doutor em Ciências Biológicas pela Universidade Estadual Paulista/ Instituto de Biociências/Campus de Rio Claro Instituto de Pesca/APTA/SAAESP Av. Bartolomeu de Gusmão, 192 - Ponta da Praia, Santos-SP, Brasil [email protected]
ABSTRACT The shortnose guitarfish ray, Zapteryx brevirostris, is constantly hauled by seven-beard-shrimp trawl nets are currently within the endangered species category. One means of preserving some aquatic species is to maintain them in a captive system such as tanks and aquariums, where it is possible to know their behaviors, as well as hematology and their well-being. The objective of this study was to analyze the productive performance and hematological analysis of Zapteryx brevirostris when submitted to different sediments in a captive system of water recirculation. For this, four treatments were used: Treatment 1 (gravel), treatment 2 (coarse sand), treatment 3 (medium sand) and treatment 4 (control) without sediment. At the end of the experiment, growth and weight data were taken for calculations of productive performance. Further, the hematological analysis was performed. The results showed that the species showed no significant difference for productive performance and hematological analysis in all treatments. However, treatment 3 (medium sand) was the only one to demonstrate weight gain, but the hematological analysis proved
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Brazilian Journal of Animal and Environmental Research 626 ISSN: 2595-573X that the rays of all treatments were with hypochromic microcytic anemia. Thus, none of the treatments contributed to the productive performance and well-being of the rays.
Key words: ray, sediment, hematological analysis.
RESUMO A raia-viola, Zapteryx brevirostris, é constantemente capturada pela pesca de arrasto do camarão- sete-barbas, atualmente está na categoria de espécies ameaçadas de extinção. Uma forma de preservar algumas espécies aquáticas é mantê-las em sistema cativo, como tanques e aquários, onde é possível conhecer seu comportamento, sua hematologia e seu bem-estar. O objetivo deste estudo foi analisar o desempenho produtivo e o hemograma da Zapteryx brevirostris quando submetida a diferentes sedimentos em um sistema cativo de recirculação de água. Para isso, foram utilizados quatro tratamentos: Tratamento 1 (cascalho), tratamento 2 (areia grossa), tratamento 3 (areia média) e tratamento 4 (controle) sem sedimento. No final do experimento, os dados de crescimento e peso foram tomados para cálculos de desempenho produtivo. Posteriormente, foi realizada a análise hematológica. Os resultados mostraram que as espécies não apresentaram diferença significativa para desempenho produtivo e hemograma em todos os tratamentos. No entanto, o tratamento 3 (areia média) mostrou ganho de peso, porém a análise hematológica demonstrou que todas as raias dos quatro tratamentos estavam com anemia microcítica hipocrômica. Assim, nenhum dos tratamentos contribuiu para o desempenho produtivo e o bem-estar das raias.
Palavras-chave: raia, sedimento, hemograma.
1 INTRODUCTION Aquatic animals such as fish and shrimp can be kept in a captive system, such as tanks and aquaria, but it is important to control water parameters (temperature, pH, salinity, ammonia, nitrite and nitrate) in order to maintain water quality and reduce the risk factors that could harm the health of the animal and, consequently, its death. (SMITH et al., 2004; PEDRAZZANI et al., 2007; NORONHA et al., 2008; DIAS, 2009; OBA et al., 2009). Aquarium sediments may also contribute to the welfare of these animals (FRANDSEN and DOLMER, 2002; STUART et al., 2006; MENDONÇA, 2010). Galhardo et al., (2008), observed that the absence of substrate in the aquarium can influence the territorial inactivity of the male Mozambique tilapia, Oreochromis massambicus, since it is a species that presents a territorial behavior for copulation. Mendonça, (2010), studying Nile tilapia, Oreochromis niloticus, found that the type of substrate interferes with reproduction, behavior and hormonal levels that affect well- being. For elasmobranches, the sediment within a captive system is important for the well-being of the animal. According to Maracini et al., (2009), when reporting the birth of bamboo shark, Chylloscyllium punctatum, the use of fine granulometry sand as the dolomite in order to keep the fish in a suitable environment. Rezende, (2017), stated that aquaria maintained with Potamotrygon
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Brazilian Journal of Animal and Environmental Research 627 ISSN: 2595-573X sp. rays should contain sand of fine granulometry so that it does not provoke injuries in the ventral region of the animal and, consequently, entrance of invading microorganisms. Greenway et al., (2016), comparing the sediments, sand and gravel, and the absence of the same, verified the preference of the ray, Raja clavate, for the sand. Gonzalez, (2004), when reporting the birth of Zapteryx brevirostris kept in an aquarium, observed that the species tended to bury itself in the sand. When the fish is in an environment that provides well-being, it swims normally, feeds itself, as well as displays other natural behaviors of the species. However, when the fish is exposed to a stress situation by parasites or by diseases or poor water quality, it displays responses such as: a lack of appetite, erratic swimming, aggressive behavior and increase of cortisol in the blood which is an element considered as a stress indicator (LIMA et al., 2006; NORONHA et al., 2008; DIAS 2009; OBA, 2009; SILVEIRA et al., 2009). In addition to cortisol, Ranzani-Paiva et al., (2013), stated that the hematological analysis, both of the red blood cells and of the white blood cells, is used to verify if the fish is in a state of stress, and it is possible to verify changes in: erythrocytes, hematocrits, Mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), and mean corpuscular hemoglobin concentration (MCHC). For example, low values of MCV can show if the fish is anemic, this occurs when the environment causes some type of stress, consequentially, the fish ceases to feed causing the physiological alteration. Takatsuka et al., (2017), found that Zapteryx brevirostris, when kept in a closed system and with long periods of food deprivation, demonstrated anemia which was different from rays fed every day. However, when fed regularly and deprived of food for a short period they did not present anemia and tended to gain weight as well as improve productive performance. Zapteryx brevirostris is a species of the Trygonorrhinidae family that comprises three genera, and the genus, Zapteryx, has three species: Zapteryx brevirostris, Zapteryx xyster and Zapteryx exasperata (LAST et al., 2016). Zapteryx brevirostris has a short muzzle and can be called a tuiuiú, mandolin or shortnose ray (BORNATOWISK and ABILHOA, 2012). According to Figueiredo, (1977), the species can be found from Fernando de Noronha to the Rio de la Plata in Argentina. It is considered an endangered species by the IUNC (International Union for Nature Conservation) due to being a trawling bycatch, and studies of this species are necessary in order to contribute to its preservation. The objective of this study was to analyze the productive performance and hematological analysis of Zapteryx brevirostris, when submitted to different sediments in a captive system of water recirculation.
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2 MATERIAL AND METHODS The experiment was carried out in December 2016, with a duration of 18 days. The parameters of the water were measured daily with a HANNA HI 9829 multiparameter water meter.
2.1 EXPERIMENTAL ANIMALS A total of 36 shortnose guitarfish rays, Zapteryx brevirostris, were obtained, comprised of 17 males and 19 females, randomly captured by trawling of seven-beard-shrimp (Xiphopenaeus kroyeri) in Itaguá bay, Ubatuba, São Paulo. Since the species is classified as endangered by the International Union for Nature Conservation (IUNC), the material was obtained by means of a permit issued by the Brazilian Institute for the Environment and Natural Renewable Resources (IBAMA) (SISBIO No. 49.980-4). The specimens were taken to the Marine Fisheries Laboratory of the Fisheries Institute in Ubatuba. Initially the rays were randomly distributed in three 3,000-liter fiberglass tanks, containing no sediment and possessing individual salt-water recirculation systems. The animals remained in this system for a period of 40 days for acclimatization until they reached stability. Biometry was performed on the first and last day of the experiment and the microchip implantation was performed on the first day. The procedures were performed on a manipulation table in the following steps: each specimen was removed from the tank and placed in a plastic box with a 40-liter capacity to be anesthetized by immersion in eugenol (63 mg/L1) diluted in 10 liters of water, the average time of anesthetic induction was three to four minutes for each ray. After inducing the anesthesia, the animal was removed from the box and positioned on an ichthyometer and then the weight was gauged on a digital scale. Subsequently, a microchip (ray identification number) applicator was used on the right side at the base of the second dorsal fin, and the identification number was checked through the digital microchip reader.
2.2 TREATMENT SYSTEM Twelve glass fiber tanks with a capacity of 500 liters each were used in a single salt-water recirculation system with a 200% capacity of water recirculation per day.
The system was composed of a sump (filtration box), with a 100-liter capacity, containing a skimmer (filtration of particles); filter bag/perlon (retains the coarser particles); thermostat (controls temperature) and pump (conducts and distributes sump water to the tanks). The programmed photoperiod was 12 h (light) and 12 h (dark).
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The experiment was composed of four treatments and three replicates, treatment T1 (gravel), treatment T2 (coarse sand), treatment T3 (medium sand) and treatment T4 (control) absent of sediment. The sediments were collected at different points on the beaches of the municipality of Ubatuba, those sites being: gravel collected in Itaguá Bay, coarse sediment at Vermelha beach and medium sediment in front of the Fisheries Institute. The granulometry of the sediments was verified with the aid of a sediment agitator in the laboratory of the Santa Cecília University, in Santos, and classified through the Wentworth table (1922) as: gravel (2-4 mm) = 2 mm; coarse sand (0.5-1 mm) = 0.6 mm and medium sand (0.25-0.5 mm) = 0.5 mm.
2.3 FEEDING The biomass in each tank had the following values: (t-1) 1,891.1 g; (t-2) 1,673.1 g; (t-3) 1,576.6 g; (t-4) 1,605.9 g; (t-5) 1,374.5 g; (t-6) 1,196.2 g; (t-7) 1,408.6 g; (t-8) 1,331 g; (t-9) 942.3 g; (t-11) 1,127.8 g, and (t-12) 763.3 g. Initially, 3% of the biomass of each tank was supplied, being a combination of 70% diced frigate tuna, Auxis thazard, and 30% headless seven-beard-shrimp, Xiphopenaeus kroyeri. The food was given once in the morning every day and was distributed in tanks two by two remaining in the water for five minutes so that the water of the system was not impaired, and the leftovers were removed with the aid of a sieve. Food leftovers were weighed, still moist, to check daily food intake and started to be distributed to other tanks using the same procedure. Subsequently, due to the rejection of fish feed, betara, Menticirrhus sp., which are less than 5 cm of average total length, was provided as a food stimulus. However, the consumption of betara was disregarded due to the small quantity offered since it was used only as a food stimulus.
2.4 PARAMETERS OF PRODUCTIVE PERFORMANCE The following performance parameters were calculated through the initial and final biometry, as well as the feed consumption: final biomass (sum of tank fish weights); specific growth rate (SGR) (ln final weight - ln initial weight/number of days of the experimental period x 100); daily weight gain (DWG) (final weight - initial weight/number of days of the experimental period); feed conversion (FC) (total amount of feed supplied in the period/weight gain in the experimental period); and survival rate [(rays alive at the end of the experimental period/initial number of individuals) x 100] (Takatsuka et al., 2017).
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2.5 HEMATOLOGICAL ANALYSIS Blood samples were collected from each individual to analyze the red blood cells and the hematometric indices at the end of the experiment. The fish were anesthetized by immersion in eugenol (63 mg.L-1) and 10 liters of water, with an average anesthetic induction time of three minutes for each ray. Then, with the aid of a 3 ml disposable syringe, a needle was inserted perpendicularly at 5 cm of the cloaca in the caudal vein, removing about 2 ml of blood and distributing them into polypropylene collecting tubes.
Blood was diluted 1:100 in methyl violet dye solution (Natt and Herrick, 1952) for the erythrocyte count in the Neubauer chamber. For the hematocrit analysis, the microhematocrit method with microcapillary aid was used in a centrifuge at 12,000 rpm of rotation for three minutes. The total plasma protein concentration (TPP) was measured using a manual refractometer and the hemoglobin concentration was determined by the photometric method using an automatic hematology analyzer.
Through the Wintrobe method (1934) hematometric indices were calculated, such as: Mean Corpuscular Volume (MCV); Mean Corpuscular Hemoglobin (MCH); and the Mean Corpuscular Hemoglobin Concentration (MCHC).
2.6 STATISTICAL ANALYSIS Statistical analysis ANOVA (p <0.05) was applied in the Past 3.0 program.
3 RESULTS The mean water parameters obtained were: temperature of 26.7ºC; salinity 29.3 ppm; pH 7.9 and 99.9% dissolved oxygen.
3.1 PARAMETERS OF PRODUCTIVE PERFORMANCE The parameters of the productive performance did not present a significant difference between the treatments (ANOVA; p <0.05). However, it was observed that the T3 treatment (medium sand) produced a higher final weight, daily weight gain (DWG), feed conversion (FC), and, consequently, a higher specific growth rate (SGR) compared with other treatments that demonstrated low and negative values. In relation to the survival rate of Z. brevirostris, treatment 4 (control) was the only one that obtained a 100% survival of the rays, however, the rays lost weight (Table 1).
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Table 1. Parameters of productive performance of shortnose guitarfish (Zapteryx brevirostris) submitted to different substrates for 18 days. Mean and standard deviation. There was no significant difference (p <0.05) according to the ANOVA test in the Past 3 program. T1 T2 T3 T4 Parameters Gravel Coarse sand Medium sand Control Starting weight (g) 462.8 ± 166.8 470.1 ± 139.0 475.7 ± 42.60 411.1 ± 142.40
Final weight (g) 453.3 ± 117.90 422.2 ± 96.90 544.1 ± 96.30 390 ± 135.9
Starting length (cm) 43.2 ± 4.42 43.2 ± 4.70 44.9 ± 2.35 41.4 ± 4.92
Final lenght (cm) 43.2 ± 3.80 43.3 ± 4.80 45.1 ± 1.39 41.4 ± 4.20
Starting disk width (cm) 19.9 ± 1.90 20.3 ± 1.94 20.5 ± 0.73 19.4 ± 1.81
Final disk width (cm) 20.3 ± 1.93 20.3 ± 1.94 21.1 ± 0.98 19.4 ± 1.81
Final Biomass (g) 3,173.1 1,688.9 2,720.6 3,509.7
Survival rate (%) 77.8 44.4 55.6 100
SGR weight (%VW day-1) 0 ± 1.4 -0.5 ± 0.8 0.7 ± 0.9 -0.3 ± 1.1
DWG (g day-1) -0.5 ± 5.6 -2.7 ± 3.8 3.8 ± 5.1 -1.2 ± 4.4
Feed Conversion -72.4 -23.7 6.6 -22.1
SGR = Specific Growth Rate; DWG = Daily Weight Gain.
Moreover, it was observed that the daily weight gain (DWG) and the specific growth rate (SGR) of all treatments demonstrated low values. However, the T3 treatment (medium sand) was the only treatment that demonstrated higher and positive values. The T4 treatment (control) had less variability, but with negative values, and the other treatments demonstrated a greater variability of positive and negative values.
3.2 HEMATOLOGICAL ANALYSIS Data from the red blood cells and the hematometric indices showed that there was no significant difference between the treatments (ANOVA; p <0.05). However, T3 (medium sand) presented higher values for mean corpuscular volume (MCV), mean corpuscular hemoglobin concentration (MCHC) and total plasma protein (TPP) compared with other treatments (Table 2). It was also observed that T2 (coarse sand) and T4 (control) treatments displayed greater variabilities of hematocrit percentage. However, T1 (gravel) and T3 (medium sand) presented lower variabilities.
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Table 2: Hemogram (red blood cells) of shortnose guitarfish (Zapteryx brevirostris) submitted to different sediments, for 18 days. Mean and standard deviation. There was no significant difference (p <0.05) according to the ANOVA test in the Past 3 program. Parameters T1 T2 T3 T4 Gravel Coarse sand Medium sand Control Erythrocytes (106/mm3) 0.49 ± 0.06 0.54 ± 0.12 0.49 ± 0.05 0.50 ± 0.05
Hematocrit % 16.7 ± 2.50 18.3 ± 3.40 18.2 ± 1.30 18.4 ± 2.35
Hemoglobin (mg/dL) 5.6 ± 0.82 6.1 ± 1.06 6.3 ± 0.41 6.0 ± 0.82
Mean Corpuscular Volume (MCV) 346.66 ± 30.56 349.14 ± 64.06 376.99 ± 32.94 378.60 ± 62.16 (fL) Mean Corpuscular Hemoglobin 33.85 ± 2.30 33.54 ± 1.23 34.74 ± 0.46 32.63 ± 1.06 Concentration (g/dL) Mean Corpuscular Hemoglobin (pg) 117.42 ± 13.38 116.74 ± 18.72 130.77 ± 10.16 123.66 ± 0.15
Total Plasma Protein (g/dL) 4.14 ± 0.66 4.65 ± 0.41 5.12 ± 0.46 4.33 ± 0.41
In relation to the Mean Corpuscular Volume (MCV), the T3 treatment (medium sand) was the one that presented smaller variations of values with a smaller amplitude of data. However, T2 (coarse sand) and T4 (control) presented higher variation values with higher data amplitudes.
Mean Corpuscular Hemoglobin Concentration (MCHC) had a lower variability of values and lower amplitude in the T3 treatment (medium sand), but T1 (gravel), T2 (coarse sand) and T4 (control) presented higher value variations. On the mean corpuscular hemoglobin (MCH), the T3 treatment (medium sand) presented smaller variations of values with a lower amplitude, but T1 (gravel), T2 (coarse sand) and T4 (control) displayed greater variabilities. Regarding Total Plasma Protein (TPP), T3 (medium sand) had higher values, but T1 (gravel), T2 (coarse sand) and T4 (control) had lower values.
4 DISCUSSION 4.1 PARAMETERS OF PRODUCTIVE PERFORMANCE The Zapteryx brevirostris ray did not show any productive performance in any of the four treatments since there was no significant difference when applying ANOVA. A possible factor for the lack of productive performance is that the experiment was carried out within a very short period, because this group displays slow growth and is considered K strategists (VOOREN et al., 2006; MARION et al., 2011; BORNATOWSKI and ABILHOA, 2012). The largest ray was 48 cm in length. Figueiredo, (1977), reported that Z. brevirostris can reach up to 66 cm in total length. Probably, the productive performance could have been achieved if the period of the experiment were longer, for example a year, and/or if the food was supplied with periods of fasting, according to Takatsuka et al., (2017).
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However, the rays submitted to treatment T3 (medium sand) showed an increase in mean GDP, SGR and feed conversion. Although T4 treatment (control) showed 100% survival of the rays, weight loss was observed in the individuals. It is possible that the T3 treatment (medium sand) rays adapted more effectively to medium sand, even though there were four rays the died. This type of sediment likely provides a more favorable environment for Z. brevirostris by avoiding injuries in the ventral region of the rays, thus, it is a suitable element for the maintenance of rays according to Rezende, (2017). Gonzalez, (2004), observed the behavior of newborn Z. brevirostris rays and reported that they tend to bury themselves, which is considered an important component for shelter and safety of the fish. Therefore, this demonstrates that the proper sediment in the captive environment of the stingrays may be an important component for rays to bury themselves. According to Takatsuka et al., (2017), Z. brevirostris can obtain a compensatory gain in productive performance if submitted to food deprivation for a certain period of time. If the rays are fed daily, and/or the feeding occurs for a long period of time, they do not display compensatory gain. The same occurs when the feeding is performed at appropriate levels, the species and its physiology must be considered so that the food is absorbed by the body of the animal and there is no food waste in the water (KUBTIZA, 2010). According to Gomiero et al., (2010), and Araújo, (2013), the growth and weight of the fish can be affected due to some stress factors, such as: water quality, disease, endoparasites, ectoparasites, which cause weight loss in fish, as well as death. One of the factors that can be considered for the weight loss and death of the rays of this experiment were the treatment system with fiberglass tanks and the sediments that may have caused injuries in the ventral region of the rays. REZENDE, (2017), states that the type of sediment and the environment can impair the well- being of the rays.
4.2 HEMATOLOGICAL ANALYSIS The red blood cells and the hematometric indices did not show a significant difference. However, according to Takasuka et al. (2017) study, the values of Mean Corpuscular Volume (MCV), Mean Corpuscular Hemoglobin (MCH) and Total Plasma Protein (TPP) of all treatments were low compared to the control group (fed daily) in which the values were 545.58±114.15 (MCV); 176.15±29.68 (MCH); 5.30±0.46 (TPP). According to Ranzani-Paiva et al., (2013), low MCV values indicate hypochromic microcytic anemia. Moreover, Wintrobe (1934) affirmed that the causes of the anemia may be due to injuries by diseases, deficiency of vitamins C and K or endo- and ectoparasites. Therefore, the rays of this experiment likely had hypochromic microcytic anemia, recurrent vitamin deficiency, injuries caused by the treatment system or by parasites.
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The hematocrit, Mean Corpuscular Volume (MCV), Mean Corpuscular Hemoglobin (MCH), and Mean Corpuscular Hemoglobin Concentration (MCHC) graphs of the T3 treatment (medium sand) displayed values with lower variability. Therefore, treatment T3 (medium sand) was able to maintain more balanced hematometric parameters compared with the other treatments. Moreover, the volume of the tank should not have caused stress in the rays, since three rays were distributed in 500L of water in each tank. According to Maciel et al., (2013), high fish density can affect well-being and alter the values of hemoglobin, hematocrit and total plasma protein for fish species, but there are species such as Piaractus mesopotamicus, which are not influenced by high density.
5 CONCLUSIONS In the productive performance, the rays did not demonstrate significant differences. The T3 rays (medium sand) obtained a greater weight gain. Regardless of the presence of the sediment, the rays may have been stressed, resulting in low weight. The hemogram showed that the rays of all treatments presented hypochromic microcytic anemia. Therefore, it is considered necessary to carry out more studies, such as this one, on the productive performance, hemogram, as well as the analysis of the well-being of Z. brevirostris.
ACKNOWLEDGMENTS Thank you Dr. Maria Letizia Petesse, Dr. Carlos Alberto Arfelli, and the students of the Marine Fish Laboratory at the Fish Institute in Ubatuba, SP; especially, Verônica Takatsuka (M.Sc.). We also thank CAPES for the scholarship from 2016 to 2018.
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Brazilian Journal of Animal and Environmental Research, Curitiba, v. 4, n. 1, p. 625-636 jan./mar. 2021