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Parasitos protozoarios y metazoarios de la tilapia del Nilo Oreochromis niloticus criadas en Brasil.

Protozoan and metazoan parasites of Nile tilapia Oreochromis niloticus cultured in Brazil

INTRODUCTION

The freshwater aquaculture in Brazil has been growing, driven especially by fish farming, which represents the bulk of the domestic production. The Nile tilapia Oreochromis niloticus is the species making the greatest contribution to the growth of this production, representing 39% of all fish from freshwater fish farming (1). Culture of this fish occurs mainly in the Northeastern, Southern, Midwestern and Southeastern areas, but the largest production is found in the Northeast (1). This production at high stocking densities is done mainly in tanks, besides ponds.

In northern Brazil, the production of Nile tilapia is small, since it is cultured only in the States of Rondonia, Acre, Para and Amapa. In the state of Amapa, the Nile tilapia was introduced in the early 90's by the former Aquiap (Aquaculturers of Amapa Association). The choice for the cultivation of this non-native fish in the state of Amapa was due to its rapid reproduction rate which allows the quick replenishment of the tanks of the pirarucu Arapaima gigas. Thus, the production of the Nile tilapia grew from 2004 to 2007, going from 10 to 30 tons (1).

The fish live in balance with the parasites, but this balance can be broken, mainly by environmental disturbances, among which the changes in the water quality have a relevant role (2,3), as well as inadequate management and high stocking densities of fish (3,4). Therefore, in systems of intensive culture, problems of infections caused by protozoan and metazoan are quite frequent. Protozoan parasites are common in farmed fish and can cause economic losses in fish farms. Metazoan are parasites that can cause gill infections, damage to eyes and internal organs, starvation, inflammation of the swim bladder, and inhibited oxygen exchange across gill lamella. They provide portals of entry for bacteria in fish. Therefore, these parasites can be limiting factors for the development of fish farm as they cause low growth of fish and diseases, reducing profitability and increasing the costs of production due to treatments. Thus, epidemiological studies in fish farms are important for adapting the management techniques and providing sanitary guidelines.

In Brazil, the parasitic fauna in Nile tilapia has been studied primarily in fish farms in the states of Sao Paulo, Santa Catarina and Parana, but the information are scattered in the literature. In addition, there is no information about the parasitic fauna in this cichlid cultured in the North, so some important issues remain open. Thus, the objectives of this study were to determine the prevalence rate and mean intensity of protozoan and metazoan parasites, as well as the condition factor in O. niloticus cultured in the State of Amapa (Northern region).

MATERIAL AND METHODS

Study site. Specimens of Nile tilapia were collected from August 2009 to March 2010 in four fish farms in the city of Macapa, state of Amapa (Brazil) for parasitological analysis.

Conservation fishes. In ponds of different sizes, the fish were maintained with an artificial diet and ignored stocking density, since they were not sexually reversed.

Parasitological analysis. All fish were collected with net, weighed (g) and measured (cm). Then, they were necropsied for parasitological analysis. Each specimen had its mouth, opercula, gills and gastrointestinal tract examined. The methodology used for collection, fixation and quantification of parasites followed previous recommendations (5,6). Identification of parasites was done in accordance to suggestions from the literature (7-9). The ecological terms were according to Bush et al (10) and Rhode et al (11).

Data analysis. With the weight and total length data, the relative condition factor (Kn) of the parasitized and non-parasitized fish was determined. The differences between parasitized and non-parasitized fish were compared through the test t (p<0.05). Spearman's rank (rs) correlation coefficient was used to determine possible correlations between the total length and weight of the hosts and the number of parasites. At each fish collection, the potential for hydrogen (pH), the temperature and dissolved oxygen concentration (DO) of the nurseries were measured with digital (YSI) equipments, respectively.

RESULTS

The temperature and the pH of ponds water were similar; however, the dissolved oxygen levels were lower in the fish farm 2 and 3 (Figure 1).

A total of 123 Nile tilapia were examined in four fish farms in Macapa (State of Amapa) and weigh and total length mean [+ or -] standard deviation are described on Table 1. In the four fish farms, 64.2% of fish were parasitized by one or more parasites (Table 1), such as: Ichthyophthirius multifiliis Fouquet, 1876 (Protozoa), Paratrichodina africana Kazubski & El-Tantawy, 1986 (Protozoa: Trichodinidae), Trichodina Ehrenberg, 1830 (Protozoa: Trichodinidae) and Cichlidogyrus tilapiae Paperna, 1960 (Monogenoidea: Dactylogyridae). The highest prevalence of parasitic infection was observed in the fish farm 2 and the lowest prevalence in the fish farm 4. In the other fish farms (1 and 3) there was not a significant difference in the prevalence, which was of 73.6% and 76.0% respectively (Table 1).

[FIGURE 1 OMITTED]

Infections by I. multifiliis were observed in Nile tilapia cultured in three of the four fish farms investigated. However, the lowest rates of parasitism occurred in the fish farm 1 and the highest in the fish farm 3. The rates of infection by Trichodinidae were similar in the three fish farms in which there was parasitism (Table 2) and two species were identified. P. Africana was found in the fish farm 1 and Trichodina sp. was found in the fish farms 2 and 3.

In tilapia from the fish farms 3 and 4, infection rates for C. tilapiae were lower than the ones from the fish farms 1 and 2 (Table 3).

The Protozoan I. multifiliis was the parasite with the greatest abundance and relative dominance (Table 4) and it showed a positive correlation with the weigh and length of O. niloticus (Figure 2).

[FIGURE 2 OMITTED]

On the other hand, Trichodinidae P. africana and Trichodina sp. were the less prevalent parasites and showed a higher relative dominance when compared to C. tilapiae (Table 4).

Kn of parasitized (0.999 [+ or -] 0.012) and non-parasitized (1.00 [+ or -] 0.03) O. niloticus showed no significant difference (p=0.676).

DISCUSSION

In Brazil, Trichodinidae are the most common protozoan affecting cultivated Nile tilapia, especially in the South where their culture has been intensified (Table 5). However, few species are described in Brazil, since in general, they are described as Trichodina sp (3,5,12-23). These parasites are important agents causing diseases in Nile tilapia and most Trichodinidae species do not show host specificity (24). In Nile tilapia grown in Bangladesh, Trichodinidae were the most frequent parasites, with a prevalence ranging from 24.2-90.2%, depending on the fish farm and the time of the year. In addition, the high prevalence proved to be correlated with the high stocking density of fish and with the physicochemical parameters of the water (2). Therefore, these results indicate the aggregate pattern of distribution of the Trichodinidae, causing these high prevalence rates when fish are kept in high stocking densities during culture.

Several species of Trichodinidae are distributed worldwide due to the transcontinental introduction of fish (24). Martins & Ghiraldelli (22) mention that the Trichodina, Trichodinella and Paratrichodina have been described parasitizing tilapia. Trichodina compacta is common in the skin and gills of several families of freshwater fish from Africa, Taiwan and Philippines, but it has a clear preference for Cichlid species (24). Paratrichodina africana occurs in 100% of tilapia from Lake Vitoria in Kenya and in 64.7% of tilapia from the Nile Delta in Egypt (8,9). In tilapia O. niloticus from three fish farms in the state of Amapa, rates of infection by Trichodina sp. and P. Africana were similar. However, the prevalence was lower than that reported for the same host grown in other regions of Brazil, while the intensity was higher (Table 5). Trichodinidae reproduction is favored by the excess of organic matter in the culture ponds (3,21,22) and by the high temperatures (2,3) such as the ones that occur in the region of this study.

Ichthyophthirius multifiliis is one of the biggest responsible for significant economic losses in fish farms worldwide (28). In Nile tilapia reared in several localities in Brazil, it is the second protozoan causing infections (Table 5), which proves its great adaption also in tropical areas. In the gills of O. niloticus cultivated in the State of Amapa, the intensity of I. multifiliis was positively correlated with weigh and length, which indicates an increase of parasitism according to the growth of fish. An increase in the number of parasites is due to cumulative process since the gills increase their surface area in proportion to an increase in fish growth (25). There is a proportional increase in habitat for reproduction of this protozoan.

The ichthyophthiriasis often manifests itself after handling operations during cold seasons and in other stressful situations (5). High rates of infections by I. multifiliis were found in tilapia from three fish farms in the state of Amapa, in the eastern Amazon, where temperatures are higher and more constant than in other Brazilian regions. However differences in the abundance and prevalence for the same host in different regions may be due to the balance between the host immune system and the performance of the parasite.

Monogenoidea is the main metazoan parasite infecting cultured tilapia in Brazil, mainly Cichlidogyrus Paperna, 1960 (Table 5). However there are few records of mortality caused by severe infections in cichlid fish. These parasites have been responsible for 80.0% of the infections in Nile tilapia grown in the state of Santa Catarina; 40.0% in the ones grown in the state of Sao Paulo and 16.0% in the ones grown in the state of Parana (29).

Parasitism by C. tilapiae was high only in tilapia from two of the investigated fish farms. However the indices were similar to the ones described for this same host grown in the southern Brazil (Table 5). Banu & Khan (2) have demonstrated that in tilapia grown in Bangladesh, Monogenoidea was the second most frequent parasite throughout the year and that their prevalence was correlated with the physicochemical parameters of the water. In a polluted environment, there is a decrease in the abundance of Cichlidogyrus sclerosus, as well as in the immunological resistance of tilapia, thereby increasing the persistence of this infection. Therefore, in tropical environments, this parasite and its host are useful bio indicators of the impact of environmental quality (30). Nevertheless, the severity of the disease also depends on the pathogenicity of the Monogenoidea species (3) and the nutritional conditions of the host.

In Nile tilapia from the states of Sao Paulo, Rio de Janeiro and Santa Catarina (Brazil), the emerging parasite Lamproglena sp. (Table 5) has been found since 2000. In the southeast, this crustacean parasite has arisen with the intensification in tilapia culture in cages. However, Lamproglena sp. has not been reported in the Brazilian Amazon, including the state of Amapa. Besides, other parasites have been known to infect this cichlid species in Brazil (Table 5). In Brazil, the diversity of digenean and other crustacean parasitizing Nile tilapia is low (Table 5), but it has also acquired parasites common in native fish, such as o Clinostomum sp., Diplostomum sp., Ergasilus sp., Argulus spinulosus and Dolops carvalhoi.

In conclusion, this study highlights that the diversity of parasites reported for O. niloticus grown in Brazil was higher than the one found in the state of Amapa, probably due to differences in size and age of fish, water quality, management and culture system for each fish farm. In Brazil, the parasitic fauna in tilapia is composed by protozoans, monogenoideans, crustaceans and digeneans. However, Trichodinidae are the most frequent protozoan in fish in the south and southeast, while I. multifiliis was more abundant in the state of Amapa, in the north. This was the first report of P. africana in O. niloticus in the eastern Amazon, what broadens its distribution and confirms the presence of this protozoan in Brazil.

Acknowledgements

We are grateful to CNPq by financial support (grants # 578159/2008-2 and 556827/2009-0) and for supporting a fellowship to M. Tavares-Dias (grant # 300472/2008-0).

REFERENCES

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(13.) Ghiraldelli L, Martins ML, Yamashita MM, Jeronimo GT. Ectoparasites influence on the hematological parameters of Nile tilapia and carp cultured in the State of Santa Catarina, Brazil. J Fish Aquatic Science 2006a; 1:270-276.

(14.) Onaka EM. Acompanhamento do estado parasitologico de peixes mantidos em tanques-rede e em ambiente natural nos reservatorios de Nova Avanhandava e Ilha Solteira (SP). Em: Castellani D., editor. I Workshop de Piscicultura do Noroeste Paulista; Votuporanga 13 marco de 2009 March 13; Votuporanga, Sao Paulo; 2009.

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(16.) Vargas L, Povh JA, Ribeiro RP, Moreira HLM, Loures BTRR, Maroneze MS. Efeito do tratamento com cloreto de sodio e formalina na ocorrencia de ectoparasitos em alevinos de tilapia do Nilo (Oreochromis niloticus) revertidas sexualmente. Arq Cien Vet Zool Unipar 2003b; 6: 39-48.

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(19.) Braccini LG, Vargas L, Ribeiro RP, Alexandre-Filho L, Digmayer M. Ectoparasitos de tilapiado-nilo (Oreochromis niloticus) cultivados em tanques-rede nos rios do Corvo e Guairaca, Parana, Brasil. Rev Bras Parasitol Vet 2008; 17:24-29.

(20.) Azevedo TMP, Martins ML, Bozzo FR, Moraes FR. Haematological and gills response in parasitized tilapia from valley of Tijucas River, SC. Brazil. Sci agric 2006; 63:115-120.

(21.) Ghiraldelli L, Martins ML, Jeronimo GT, Yamashita MM, Adamante, WB. Ectoparasites communities from Oreochromis niloticus cultivated in the State of Santa Catarina, Brazil. J Fish Aquatic Sci 2006b; 1:181-190.

(22.) Martins ML, Ghiraldelli L. Trichodina magna Van As and Basson, (Ciliophora: Peritrichia) from cultured Nile tilapia in the State of Santa Catarina, Brazil. Braz J Biol 2008; 68:169-172.

(23.) Ghiraldelli L, Martins ML, Adamante WB, Yamashita MM. First record of Trichodina compacta Van As and Basson, 1989 (Protozoa: Ciliophora) from cultured Nile tilapia in the State of Santa Catarina, Brazil. Int J Zool Res 2006c: 2:369-375.

(24.) Basson L, Van As J. Trichodinidae and other ciliophorans (Phylum Ciliophora In: Woo, P.T.K., editor. Fish diseases and disorders: Protozoan and metazoan infections. UK: Biddles, King's Lyn; 2006.

(25.) Alves DR, Luque JL, Paraguassu AL. Ectoparasitas da tilapia nilotica Oreochromis niloticus (Osteichthyes: Cichlidae) da estacao de piscicultura da UFRJ. Rev Univ Rural Ciencias e Vida 2000; 22:81-85.

(26.) Marengoni NG, Santos RS, Goncalves-Junior AC, Gino DM, Zerbinatti DCP, Lima FS. Monogenoidea (Dactylogyridae) em tilapiasdo-nilo cultivadas sob diferentes densidades de estocagem em tanques-rede. Arq Bras Med Vet Zootec 2009; 61:393-400.

(27.) Silva AS, Monteiro SG, Doyle RL, Pedron FA, Filipetto JE, Radunz-Neto J. Ocorrencia de Clinostomum complanatum em diferentes especies de peixes de uma piscicultura do Municipio de Santa Maria - RS. Vet Zootec 2008; 15:27-32.

(28.) Dickerson HW. Ichthyophthirius multifiliis and Cryptocaryon irritans (Phylum Ciliophora), In: Woo, P.T.K., editor. Fish diseases and disorders: Protozoan and metazoan infections. UK: Biddles, King's Lyn; 2006.

(29.) Goncalves ELT, Jeronimo GT, Martins ML. On the importance of monogenean helminthes in Brazilian cultured Nile tilapia. Neotrop Helminthol 2009; 3:53-56.

(30.) Sanchez-Ramirez C, Vidal-Martinez VM, Aguirre-Macedo ML, Rodrigues-Canul RP, Gold-Bouchot G, Sures B. Cichlidogyrus sclerosus (Monogenea: Ancyrocephalinae) and its host, the Nile tilapia (Oreochromis niloticus), as bioindicators of chemical pollution. J Parasitol 2007; 93:1097-1106.

Wanderson Pantoja MF, [1] Fishing Engineer, Ligia Neves R, [1] Fishing Engineer, Marcia Dias RD, [1,2] Biologist, Renata Marinho GB, [1,2] Zoo Technician, Daniel Montagner, [1] M.Sc, Marcos Tavares-Dias, [1] * Ph.D.

[1] Embrapa Amapa, Laboratorio de Aquicultura e Pesca, Macapa, AP, Brasil. [2] Universidade Federal do Amapa (UNIFAP), Programa de Pos-Graduacao em Biodiversidade Tropical, Macapa, AP, Brasil.

Correspondence: marcostavares@cpafap.embrapa.br

Recibido: Marzo de 2011; Aceptado Diciembre de 2011.
Table 1. Mean values [+ or -] standard deviation of weigh and total
length of Nile tilapia collected in four fish farms from the state of
Amapa. EF: examined fish; PF: parasitized fish, P: Prevalence.

Fish              Geographic coordinates
farms

1       0[degrees]02'31.4"S, 051[degrees]07'34.4"W
2       0[degrees]00'58.1"S, 051[degrees]06'31.8"W
3       0[degrees]00'36.8"S, 051[degrees]06'13.7"W
4       0[degrees]00'04.5"N, 051[degrees]05'52.1"W
Total                       --

Fish        Weight (g)           Length (cm)       EF      PF     P (%)
farms

1        44.0 [+ or -] 31.7   12.6 [+ or -] 2.7    38      28     73.6
2        51.1 [+ or -] 44.9   12.9 [+ or -] 3.7    32      29     90.6
3       135.8 [+ or -] 36.7   19.1 [+ or -] 2.0    25      19     76.0
4        55.2 [+ or -] 68.8   12.6 [+ or -] 4.2    28       3     10.7
Total           --                   --            123     79     64.2

Table 2. Parasitological indices of Ichthyophthirius
multifiliis and Trichodinidae on the gills of Nile
tilapia from four fish farms from the state of
Amapa.

Parasites           Ichthyophthirius multifiliis

Fish farms      1             2               3           4

EF              38           32               25         28
PF              13           17               19          0
P (%)          34.2         53.1             76.0         0
MI            700.8        7183.9          75.198,4       0
MA            239.7        3816.5          57.150,8       0
Range        120-2550   4,100-14,800    13,108-282,785    0
TNP            9110        122.127        1.428.770       0

Parasites                 Trichodinidae

Fish farms      1         2        3       4

EF              38        32       25     28
PF              3         1        1       0
P (%)          7.9       3.1      4.0      0
MI            1957.3     6800     9894     0
MA             1545     206.1    395.7     0
Range        735-3180                      0
TNP            5872                        0

EF: examined fish; PF:parasitized fish; P:Prevalence; MI:Mean
intensity of infection; MA:Mean abundance; TNP:Total number of
parasites.

Table 3. Parasitological indices of Cichlidogyrus tilapiae
on the gills of Nile tilapia from four fish farms in
the state of Amapa.

Fish farms     1       2       3       4

EF            38      32      25      28
PF            28      22       2       3
P (%)        73.7    68.7     8.0    10.7
MI           12.3     7.6     3.5    11.0
MA            9.0     5.2    0.28     1.2
Range        2-51    3-17     1-6    4-23
TNP           343     168      7      33

EF:examined fish; PF:parasitized fish; P:Prevalence; MI:Mean intensity
of infection; MA:Mean abundance; TNP:Total number of parasites.

Table 4. Total parasitological indices in Nile tilapia in the
state of Amapa.

Parasites    C. tilapiae   I. multifiliis    Trichodinidae

EF               123             123              123
PF               55              49                5
P (%)           44.7            39.8              4.1
MI              10.0          31.836,9          4513.2
MA               4.5           12.683            183.5
TNP              551          1.560,007         22.566
MRD            0.0003          0.9854           0.01425

EF: examined fish; PF: parasitized fish; P: Prevalence; MI: Mean
intensity of infection; MA: Mean abundance; TNP: Total number of
parasites; MRD: Mean relative dominance.

Table 5. Parasites of Nile tilapia cultured in different Brazilian
states.

Group/Species                      Culture/State

PROTOZOA

I. multifilis                     Feefishing (SP)
I. multifilis                      Net cage (SP)
I. multifilis              Fish farm and Feefishing (PR)
I. multifilis                     Feefishing (PR)
I. multifilis                      Fish farm (PR)
Trichodina sp.                    Feefishing (PR)
Trichodina sp.                     Fish farm (PR)
Trichodina sp.                     Fish farm (PR)
Trichodina sp.                     Fish farm (PR)
Trichodina sp.                     Net cage (PR)
Trichodinidae                      Net cage (PR)
Trichodina sp.                     Net cage (SP)
Trichodina sp.                     Fish farm (SP)
Trichodina sp.                    Feefishing (SC)
Trichodina magna                   Fish farm (SC)
Trichodina compacta                Fish farm (SC)
T. compacta and T. magna           Fish farm (SC)
T. compacta and T. magna           Fish farm (SC)
T. compacta and T. magna   Fish farm and Feefishing (SC)

MONOGENOIDEA

Cichlidogyrus sp.                  Fish farm (RJ)
Dactylogyrus sp.                   Net cage (SP)
Cichlidogyrus sclerosus            Fish farm (SP)
  and Cichlidogyrus sp.
Dactylogyridae                     Fish farm (PR)
Dactylogyridae                    Feefishing (PR)
Dactylogyrus sp.                   Fish farm (PR)
Gyrodactylogyridae                Feefishing (PR)
Cichlidogyrus sp. and             Feefishing (SC)
  C. sclerosus
Cichlidogyrus sp., C.              Fish farm (SC)
  sclerosus and
  Gyrodactylus sp.
Cichlidogyrus sp.,  C.             Fish farm (SC)
  sclerosus and
  Gyrodactylus
Cichlidogyrus sp. And             Feefishing (SC)
  C. sclerosus

DIGENEA

Clinostomum complamatum            Fish farm (RS)
Diplostomum sp.                    Net cage (SP)
CRUSTACEA
Ergasilidae                        Fish farm (SP)
Ergasilus sp.                      Fish farm (RJ)
Lamproglena sp.                    Fish farm (RJ)
Lamproglena sp.                    Fish farm (SP)
Lamproglena sp.                   Feefishing (SC)
Lamproglena sp.                    Fish farm (SC)
Lamproglena sp.                    Fish farm (SC)
Lamproglena sp.                    Fish farm (SC)
Argulus spinulosus                 Fish farm (SC)
Dolops carvalhoi                   Net cage (SP)

Group/Species              Prevalence (%)   Mean Intensity   References

PROTOZOA

I. multifilis                   4.0              76.0            5
I. multifilis                   3.2               --             14
I. multifilis                21.3-25.0            --             15
I. multifilis                 1.8-2.5             --             12
I. multifilis                   26.0              --             16
Trichodina sp.               15.8-18.3            --             12
Trichodina sp.                  43.0              --             16
Trichodina sp.               62.5-72.5            --             15
Trichodina sp.               17.0-72.0            --             17
Trichodina sp.               13.3-50.0            --             18
Trichodinidae                13.9-17.4            --             19
Trichodina sp.               24.0-38.1            --             14
Trichodina sp.                  8.0              243             5
Trichodina sp.                  1.6               --             20
Trichodina magna                24.7              --             22
Trichodina compacta             24.7              --             23
T. compacta and T. magna     10.0-51.0        55.1-621.9         21
T. compacta and T. magna        81.0              --             13
T. compacta and T. magna      0.6-1.7             --             3

MONOGENOIDEA

Cichlidogyrus sp.               12.8             1.1             25
Dactylogyrus sp.             52.8-83.3        65.6-112.8         26
Cichlidogyrus sclerosus       6.7-43.8         3.6-7.3           4
  and Cichlidogyrus sp.
Dactylogyridae                3.3-10.0            --             18
Dactylogyridae               25.8-53.3            --             12
Dactylogyrus sp.                49.0             0.8             16
Gyrodactylogyridae              0.8               --             12
Cichlidogyrus sp. and           13.3             4.2             20
  C. sclerosus
Cichlidogyrus sp., C.         28.0-83          1.3-34.5          21
  sclerosus and
  Gyrodactylus sp.
Cichlidogyrus sp.,  C.          76.0              --             13
  sclerosus and
  Gyrodactylus
Cichlidogyrus sp. And        13.2-16.5         0.8-2.6           3
  C. sclerosus

DIGENEA

Clinostomum complamatum         100               --             27
Diplostomum sp.                 4.8               --             14
CRUSTACEA
Ergasilidae                     18.0             3.4             6
Ergasilus sp.                   18.2             2.0             25
Lamproglena sp.                 60.0             3.4             25
Lamproglena sp.                 67.4             5.2             4
Lamproglena sp.                 3.3              1.5             20
Lamproglena sp.               3.0-22.0         0.3-0.8           21
Lamproglena sp.                 9.0               --             13
Lamproglena sp.               0.5-1.7          0.1-0.2           3
Argulus spinulosus              33.0             1.7             21
Dolops carvalhoi                1.6               --             14
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Title Annotation:ORIGINAL
Author:Pantoja M.F., Wanderson; Neves R., Ligia; Dias R.D., Marcia; Marinho G.B., Renata; Montagner, Daniel
Publication:Revista MVZ (Medicina Veterinaria y Zootecnia)
Date:Jan 1, 2012
Words:4168
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