Exp Appl Acarol (2014) 63:551–557 DOI 10.1007/s10493-014-9793-z
Analysis of the risk factors relating to cows’ resistance to Rhipicephalus microplus ticks during the peripartum Jenevaldo Barbosa da Silva • Charles Passos Rangel • Bruna de Azevedo Baeˆta • Adivaldo Henrique da Fonseca
Received: 1 July 2013 / Accepted: 5 March 2014 / Published online: 4 April 2014 Ó Springer International Publishing Switzerland 2014
Abstract This study aimed to evaluate season, breed, number of lactations and milk production as risk factors relating to Rhipicephalus microplus infestation in dairy cows during the peripartum. Eighty-four animals were randomly selected through proportional stratified sampling. All engorged and partially engorged female R. microplus specimens measuring 4.5–8.0 mm were counted during the 5 weeks before calving, calving week and 5 weeks after calving. The peripartum had a significant effect [calving (p \ 0.05; prevalence ratio (PR)= 3.12) and post calving (p \ 0.05; PR = 2.02)] on R. microplus infestation. Although the average tick count was higher during the rainy season than during the dry season, there was no significant difference (p = 0.055; PR = 0.63). The average R. microplus count was significantly higher (p \ 0.05; PR = 2.10) in Bos taurus animals, followed by F1 (p \ 0.05; PR = 1.64) and Girolando (p \ 0.05; PR = 1.39). The average R. microplus count was significantly higher (p \ 0.05; PR = 0.97) in first-lactation animals, followed by those at the second, third and, fourth or subsequent lactation. Milk production showed a negative correlation with R. microplus count, such that high-production animals were significantly (p = 0.003; PR = 2.04) more vulnerable to infestation than were low-production animals. First-lactation and high-production B. taurus animals had greatest vulnerability to R. microplus infestation over the peripartum period, and constituted the at-risk group in the dairy herd.
J. B. da Silva (&) Faculdade de Cieˆncias Agra´rias e Veterina´rias-UNESP, Rod. Carlos Tonanni, km 05, Jaboticabal, Sa˜o Paulo 14870-000, Brazil e-mail: [email protected] C. P. Rangel B. de Azevedo Baeˆta A. H. da Fonseca Universidade Federal Rural do Rio de Janeiro (UFRRJ), BR465, Km07, Serope´dica, Rio de Janeiro 23890-000, Brazil e-mail: [email protected] B. de Azevedo Baeˆta e-mail: [email protected] A. H. da Fonseca e-mail: [email protected]
123
552
Keywords
Exp Appl Acarol (2014) 63:551–557
Dairy cow Lactation Peripartum Pregnancy Ticks
Introduction In economic terms, Rhipicephalus microplus is the most important tick species for the tropical cattle industry (Piper et al. 2009). The damage done by this ixodid accounts for annual economic losses of approximately 13 billion dollars worldwide (Anon 2002). In Brazil, these costs may be over 800 million dollars per year (Martinez et al. 2006). Susceptibility to parasites is generally a multifactorial phenomenon in which different characteristics may be recognized. Among these is the host’s immunological response (Roche et al. 2000). The physical and metabolic stress factors of pregnancy, calving and lactation make important contributions towards decreasing the host’s resistance and consequently increasing disease incidence. The innate and acquired defense mechanisms of cattle are weaker during the peripartum (Mallard et al. 1998). Under tropical conditions, the level of infestation by R. microplus is notoriously influenced by the season of the year. Studies conducted in Brazil have shown quite different outcomes regarding tick infestation levels in relation to the period of the year. Oliveira et al. (1989) found higher infestation in the fall and winter, in Canchim cattle. Verı´ssimo et al. (1997) found from crossbred dairy cattle and Andrade et al. (1998) found from Gir cattle that there was greater infestation in the fall. Zebuines and taurines with no previous contact with R. microplus ticks are equally susceptible to primary infestation by the larvae of this ixodid (Wagland 1975). The higher level of resistance among zebuines becomes visible after a period of susceptibility to a primary infestation (Hewetson 1971). Many authors have demonstrated the greater resistance of zebuines to R. microplus ticks, in comparison with taurines (Wharton and Utech 1970; Oliveira et al. 1989). In dairy cows, the reproductive experience influence in immunological system during the peripartum. Primiparous cows do not have a fully matured immune system; thus, they usually produce poor quality colostrum in concentration and variety of antibodies (Donovan et al. 1986). Another variance of the immunological system that influence during the peripartum is the milk production. In low milk production animals, the mobilization of serum antibodies is usually lower due to the less activity of mammary glands fluids (Machado Neto and D’arce 1979). The purpose of the present study was to evaluate the impact of seasons, breed, number of lactations and milk production as risk factors relating to infestation by R. microplus in dairy cows during the peripartum.
Materials and methods The field activities were conducted in 2008 and 2009, in the dairy cow section at the Serope´dica Experimental Station, which belongs to the Agricultural and Livestock Research Company of the State of Rio de Janeiro (Empresa de Pesquisa Agropecuaria do Estado do Rio de Janeiro; Pesagro-Rio), located in the Rio de Janeiro Metropolitan microregion (latitude 22°450 S, longitude 43°410 W and altitude 33 m).
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Eighty-four cows were randomly selected to analyze risk factors relating to cows’ resistance to R. microplus ticks during the peripartum. Among these, 44 cows gave birth during the rainy seasons (spring and summer) and 40 during the dry seasons (fall and winter). Among the cows evaluated, 20 were pure Bos taurus (Holstein), 28 were half-blood F1 through crossbreeding (1/2 B. taurus 9 1/2 Bos indicus[Gir]), 21 were Girolando (5/8 B. indicus 9 3/8 B. taurus) and 15 were pure B. indicus. Regarding the number of lactations, 20 cows were at their first lactation, 25 at the second lactation, 24 at the third lactation and 15 at the fourth or subsequent lactation. In the milk production evaluation, the cows were classified according to their annual production. In the herd evaluated, 27 cows with milk production lower than 1,500 kg per year were classified as low-production animals, 37 with milk production between 1,500 and 3,000 kg per year were classified as having moderate milk production, and 20 cows with production higher than 3,000 kg per year were classified as high-production animals. In accordance with the routine management procedure at the experimental station, the pregnant cows were kept in an area of Brachiaria decumbens grass at an animal density of 5 AU/ha for the 30 days before calving. After birth and for the first 4 weeks of lactation, the animals were kept on B. decumbens and Panicum maximum pasture at an animal density of 3 AU/ha. During both of these periods, the animals received water and mineral salt ad libitum. During lactation, the cows were milked twice a day and received 3 kg of commercial concentrate a day, made up of citric pulp and commercial feed containing 22 % crude protein, in the proportions of 2:1. Rhipicephalus microplus ticks counts were weekly performed on all cows during the last 5 weeks of pregnancy, 1 week of calving and first 5 weeks of lactation. Each animal was put into an individual crate in order to count fully or partially engorged R. microplus females measuring 4.5–8.0 mm, from the right hemisphere of each cow, according to the procedure described by Wharton and Utech (1970). The result from each count was multiplied by two to calculate the monthly average for each animal. For the statistical analysis, the data were first subjected to the normality test (Kolmogorov–Smirnov) to ascertain whether the data conformed to normal distribution. Because the data did not show normal distribution even after logarithmic transformation to log10 (x ? 1), comparisons were made between averages by applying the parametric Kruskal–Wallis test at 5 % significance. The generalized linear model methodology was used, assuming Poisson distribution with a logarithmic link function. Lastly, interactions within the variance were investigated by means of the Spearman test. The operational procedures were done using the R Foundation statistical computing software, version 2.12.2 (2011).
Results The peripartum had an effect on infestation by R. microplus ticks (Fig. 1). The average tick count during the rainy season was 38 ticks/animal, while during the dry season, it was 33 ticks/animal (p [ 0.05; PR = 0.63). The infestation by R. microplus during the pre-calving, calving, and post-calving periods among the animals that gave birth during the rainy season were numerically higher than among those that gave birth in the dry season, but there was no statistically significant difference (Table 1). The average R. microplus count during the peripartum was 55 ticks/animal in Bos taurus animals, 39 ticks/animal in F1 B. taurus 9 B. indicus, 29 ticks/animal in Girolando
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Exp Appl Acarol (2014) 63:551–557
Counts of Rhipicephalus microplus
150 53±4.8
58±4.7 37±3.7
125
56±4.4
42±4.0 50±3.5
24±2.5 100
17±2.2
75
21±2.0 23±1.5
50 15±1.6 25 0
-5 week -4 week -3 week -2 week -1 week Calving 1 week 2 week 3 week 4 week 5 week
Pre calving Fig. 1
Calving
Post Calving
Rhipicephalus microplus tick counts during the peripartum period
Table 1 Evaluation of risk factors for infestation by Rhipicephalus microplus among cows during the peripartum, by means of Poisson regression Risk factors/variables
N
NS
X
PR
p
95 % CI
Pre calvinga
84
420
19
–
–
–
Calving
84
84
37
3.12
\0.001
[0.181–0.565]
Post calving
84
420
65
2.02
\0.001
[0.620–0.678]
Peripartum
Season Drya
44
484
33
–
–
–
Rain
40
440
38
0.63
0.055
[0.831–1.205]
Breed B. indicusa
15
165
18
–
–
–
F1
28
308
39
1.64
\0.001
[0.746–0.816]
Girolando
21
231
29
1.39
\0.001
[0.629–0.669]
B. taurus
20
220
55
2.10
\0.001
[0.442–0.510]
1° lactationa
20
220
60
–
–
–
2° lactation
25
275
44
0.97
0.045
[0.391–0.639]
3° lactation
24
264
19
0.91
\0.001
[0.871–0.958]
[3° lactation
15
165
16
0.97
0.030
[0.729–0.903]
No. of lactation
Milk prod (kg/year) \1,500a
27
297
19
–
–
–
1,500–3,000
37
407
28
0.91
0.125
[0.988–1.096]
[3,000
20
220
58
2.04
0.003
[0.852–0.969]
a
Value, N = number of animals evaluated, NS = number of samples evaluated, X = average tick count per animal, PR = prevalence ratio, CI = confidence interval, F1 = B. taurus x B. indicus
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and 18 ticks/animal in B. indicus. In all phases of the peripartum, the animals with higher levels of taurine blood were more vulnerable and had higher average populations of R. microplus (p \ 0.05; PR = 2.10). Among the crossbred animals, there was no statistically significant difference (p [ 0.05) in the tick counts (Table 1). In all three phases of the peripartum, the R. microplus counts were significantly higher (p \ 0.05) among the primiparous animals than among the multiparous ones (Table 1). The average R. microplus count during the peripartum was significantly higher (p \ 0.05) among first-lactation animals, which had an average of 60 ticks/animal, followed by second-lactation animals with an average of 44 ticks/animal. Among the animals that were at their third and fourth or subsequent lactations, the tick populations of ticks observed were 19 and 16 ticks/animal, respectively, which were not statistically significantly different from each other (p [ 0.05). The high-production animals were significantly (p \ 0.003; PR = 2.04) more vulnerable to infestation than were the low-production animals (Table 1). The average R. microplus count during the peripartum was 58 ticks/animal among high-production animals, 28 ticks/animal among moderate-production animals and 19 ticks/animal among lowproduction animals.
Discussion Although no study in the literature has evaluated tick infestation levels in relation to calving, it is known that the innate and acquired defense mechanisms of cattle are weaker during the peripartum period (Mallard et al. 1998). This reduced defense, together with changes to the immune system and the physical and metabolic weakening observed due to pregnancy and calving, contributes toward the fall in resistance and rise of incidence of ectoparasitism (Chorfi et al. 2004). According to Utech et al. (1978), pregnant animals are more susceptible to infestation by ticks than are nonpregnant animals, especially in the final third of pregnancy. Doube and Wharton (1980) claimed that a seasonal cycle of resistance to R. microplus tick might exist in cattle, due to oscillation in the animals’ immune ability against this parasite. These authors found that resistance to R. microplus ticks declined in the fall and early winter, regardless of the animals’ breed or nutritional state. Many authors have demonstrated that seasonal factors have an influence on the life cycle of ticks and consequently that differences in infestation dynamics exist in cattle, with possible variations according to the region, climate and period of the year (Oliveira et al. 1989; Doube and Wharton 1980). In the present study, the effect of the peripartum on R. microplus infestation was observed in both the dry and the rainy season, such that the parasite load increased from before to after calving. This demonstrated that, regardless of environmental conditions, the phenomenon of the peripartum had an important influence on R. microplus infestation levels. The average tick counts observed in this study demonstrated that there was a clear difference in resistance levels between the B. taurus and B. indicus animals. The half-blood F1 animals continued to be vulnerable and the Girolando animals became more resistant to infestations by R. microplus. These results demonstrate that to obtain animals with greater resistance, crossbreeding in which zebuine blood predominates is required. Tatchell and Moorhouse (1968) observed that B. taurus animals presented higher susceptibility to ticks than shown by B. indicus animals.
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The present study observed that primiparous animals were more susceptible while multiparous animals were more resistant. A wide variety of results concerning the influence of age on tick infestation can be seen in the literature. Andrade et al. (1998) found that older animals were more susceptible to ticks. The outcome from the present study corroborates the findings of Silva et al. (2013), who observed higher tick counts among primiparous cows than among multiparous cows. Bertrand et al. (1985) observed a direct relationship between milk production and disease incidence. In high-production dairy cows, the numbers of round neutrophils and mononuclear cells were significantly higher than in cows with intermediate productive potential (Detilleux et al. 1995). These results can be considered encouraging, considering that selection for high-production animals does not provide unfavorable responses relating to the functional ability of the immunological features. However, these animals are vulnerable to a higher number of diseases, especially during the peripartum (Detilleux et al. 1995).
Conclusion First-lactation and high-production B. taurus animals had greatest vulnerability to R. microplus infestation over the peripartum period. On the other hand, crossbred B. taurus and B. indicus animals presented satisfactory resistance and milk production. Thus, these animals are more efficient and cost-effective for tropical climates, and crossbreeding with predominance of zebuine blood is an ecologically sound way to control R. microplus ticks in cattle and to maintain good milk productivity in herds.
References Andrade ABF, Silva RG, Costa AJ, Rocha UF, Landim VJC (1998). Genetic and environmental aspects of the resistance of Zebu cattle to the tick Boophilus microplus. In: Proceedings of the 6th World congress on genetics applied to livestock production, 1998, Armidale: NSW, Austra´lia. Armidale, 27, 339–342 Anon (2002) Australian code of practice for the care and use of animals for scientific purposes. Australian Government Publishing Service, Canberra, ACT, Australia Bertrand JA, Berger PJ, Freeman AE, Kelley DH (1985) Profitability in daughters of high versus average Holstein sires selected for milk yield of daughters. J Dairy Sci 68:2287–2294 Chorfi Y, Lanevschi-Pietersma A, Girard V, Tremblay A (2004) Evaluation of variation in serum globulin concentrations in dairy cattle. Vet Clin Pathol 33:122–127 Detilleux JC, Kehrli ME Jr, Stabel JR, Freemad AE, Kelley DH (1995) Study of immunological dysfunction in periparturient Holstein cattle selected for high and average milk production. Vet Immunol Immunopathol 44:251–267 Donovan GA, Badinga L, Collier RJ, Wilcox CS, Braun RK (1986) Factors influencing passive transfer in dairy calves. J Dairy Sci 69:754–759 Doube BM, Wharton RH (1980) The effect of locality, breed and previous tick experience on seasonal change in the resistance of cattle to Boophilus microplus (Ixodoidea: Ixodidae). Experientia 36:1178–1179 Hewetson RW (1971) Resistance by cattle to the cattle tick Boophilus microplus. III. The development of resistance to experimental infestations by purebred Sahiwal and Australian Illawarra shorthorn cattle. Aust J Agric Res 22:331–342 Machado Neto R, D’arce RD (1979) Proteı´nas se´ricas nos perı´odos pre´ e po´s-parto de vacas da rac¸a Nelore. J Agric 53:13–19 Mallard BA, Dekkers JC, Ireland MJ, Leslie KE, Sharif S, Vankampen CL, Wagter L, Wilkie BN (1998) Alteration in Immune responsiveness peripartum period period and its ramification on dairy cow and calf health. J Dairy Sci 81:585–595
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Martinez ML, Machado MA, Nascimento CS, Silva MVGB, Teodoro RL, Furlong J, Prata MCA, Campos AL, Guimara˜es MFM, Azevedo ALS, Pires MFA, Verneque RS (2006) Association of BoLA-DRB3.2 alleles with tick (Boophilus microplus) resistance in cattle. Genet Mol Biol 5:513–524 Oliveira GP, Alencar MM, Freitas AR (1989) Resisteˆncia de bovinos ao carrapato Boophilus microplus. II. Infestac¸a˜o natural. Pesq Agropec Bras 24:127–1267 Piper EK, Jonsson NN, Gondro C, Lew-Tabor AE, Moolhuijzen P, Vance ME, Jackson LA (2009) Immunological profiles of Bos taurus and Bos indicus cattle infested with the cattle tick, Rhipicephalus (Boophilus) microplus. Clin Vaccine Immunol 16:1074–1086 Roche JF, Mackey D, Diskin MD (2000) Reproductive management of postpartum cows. Anim Reprod Sci 2:703–712 Silva JB, Rangel CP, Baeˆta BA., Fonseca AH ( 2013) Influence of the physiological state on infestation by Rhipicephalus microplus in dairy cows. Ticks Tick-Borne Dis 4:52–56 Tatchell R, Moorhouse D (1968) The feeding processes of the cattle tick Boophilus microplus (Canestrini). Parasitology 58:441–459 Utech KB, Wharton RH, Kerr JD (1978) Resistance to Boophilus microplus in different breeds of cattle. Aust J Agric Res 29:885–895 Verı´ssimo CJ, Silva RG, Oliveira AAD, Ribeiro WR, Rocha UF (1997) Resisteˆncia e susceptibilidade de bovinos leiteiros mestic¸os ao carrapato Boophilus microplus. Bol Ind Anim 54:1–10 Wagland BM (1975) Host resistance to cattle tick (Boophilus microplus) in Brahman (Bos indicus) cattle. I Responses of previously unexposed cattle to four infestations with 20,000 larvae. Aust J Agric Res 26:1073–1080 Wharton RH, Utech KBW (1970) The relation between engorgement and dropping of Boophilus microplus (Canestrini) (Ixodidae) to the assessment of tick numbers on cattle. J Aust Ent Soc 9:171–182
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Analysis of the risk factors relating to cows’ resistance to Rhipicephalus microplus ticks during the peripartum Jenevaldo Barbosa da Silva • Charles Passos Rangel • Bruna de Azevedo Baeˆta • Adivaldo Henrique da Fonseca
Received: 1 July 2013 / Accepted: 5 March 2014 / Published online: 4 April 2014 Ó Springer International Publishing Switzerland 2014
Abstract This study aimed to evaluate season, breed, number of lactations and milk production as risk factors relating to Rhipicephalus microplus infestation in dairy cows during the peripartum. Eighty-four animals were randomly selected through proportional stratified sampling. All engorged and partially engorged female R. microplus specimens measuring 4.5–8.0 mm were counted during the 5 weeks before calving, calving week and 5 weeks after calving. The peripartum had a significant effect [calving (p \ 0.05; prevalence ratio (PR)= 3.12) and post calving (p \ 0.05; PR = 2.02)] on R. microplus infestation. Although the average tick count was higher during the rainy season than during the dry season, there was no significant difference (p = 0.055; PR = 0.63). The average R. microplus count was significantly higher (p \ 0.05; PR = 2.10) in Bos taurus animals, followed by F1 (p \ 0.05; PR = 1.64) and Girolando (p \ 0.05; PR = 1.39). The average R. microplus count was significantly higher (p \ 0.05; PR = 0.97) in first-lactation animals, followed by those at the second, third and, fourth or subsequent lactation. Milk production showed a negative correlation with R. microplus count, such that high-production animals were significantly (p = 0.003; PR = 2.04) more vulnerable to infestation than were low-production animals. First-lactation and high-production B. taurus animals had greatest vulnerability to R. microplus infestation over the peripartum period, and constituted the at-risk group in the dairy herd.
J. B. da Silva (&) Faculdade de Cieˆncias Agra´rias e Veterina´rias-UNESP, Rod. Carlos Tonanni, km 05, Jaboticabal, Sa˜o Paulo 14870-000, Brazil e-mail: [email protected] C. P. Rangel B. de Azevedo Baeˆta A. H. da Fonseca Universidade Federal Rural do Rio de Janeiro (UFRRJ), BR465, Km07, Serope´dica, Rio de Janeiro 23890-000, Brazil e-mail: [email protected] B. de Azevedo Baeˆta e-mail: [email protected] A. H. da Fonseca e-mail: [email protected]
123
552
Keywords
Exp Appl Acarol (2014) 63:551–557
Dairy cow Lactation Peripartum Pregnancy Ticks
Introduction In economic terms, Rhipicephalus microplus is the most important tick species for the tropical cattle industry (Piper et al. 2009). The damage done by this ixodid accounts for annual economic losses of approximately 13 billion dollars worldwide (Anon 2002). In Brazil, these costs may be over 800 million dollars per year (Martinez et al. 2006). Susceptibility to parasites is generally a multifactorial phenomenon in which different characteristics may be recognized. Among these is the host’s immunological response (Roche et al. 2000). The physical and metabolic stress factors of pregnancy, calving and lactation make important contributions towards decreasing the host’s resistance and consequently increasing disease incidence. The innate and acquired defense mechanisms of cattle are weaker during the peripartum (Mallard et al. 1998). Under tropical conditions, the level of infestation by R. microplus is notoriously influenced by the season of the year. Studies conducted in Brazil have shown quite different outcomes regarding tick infestation levels in relation to the period of the year. Oliveira et al. (1989) found higher infestation in the fall and winter, in Canchim cattle. Verı´ssimo et al. (1997) found from crossbred dairy cattle and Andrade et al. (1998) found from Gir cattle that there was greater infestation in the fall. Zebuines and taurines with no previous contact with R. microplus ticks are equally susceptible to primary infestation by the larvae of this ixodid (Wagland 1975). The higher level of resistance among zebuines becomes visible after a period of susceptibility to a primary infestation (Hewetson 1971). Many authors have demonstrated the greater resistance of zebuines to R. microplus ticks, in comparison with taurines (Wharton and Utech 1970; Oliveira et al. 1989). In dairy cows, the reproductive experience influence in immunological system during the peripartum. Primiparous cows do not have a fully matured immune system; thus, they usually produce poor quality colostrum in concentration and variety of antibodies (Donovan et al. 1986). Another variance of the immunological system that influence during the peripartum is the milk production. In low milk production animals, the mobilization of serum antibodies is usually lower due to the less activity of mammary glands fluids (Machado Neto and D’arce 1979). The purpose of the present study was to evaluate the impact of seasons, breed, number of lactations and milk production as risk factors relating to infestation by R. microplus in dairy cows during the peripartum.
Materials and methods The field activities were conducted in 2008 and 2009, in the dairy cow section at the Serope´dica Experimental Station, which belongs to the Agricultural and Livestock Research Company of the State of Rio de Janeiro (Empresa de Pesquisa Agropecuaria do Estado do Rio de Janeiro; Pesagro-Rio), located in the Rio de Janeiro Metropolitan microregion (latitude 22°450 S, longitude 43°410 W and altitude 33 m).
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Exp Appl Acarol (2014) 63:551–557
553
Eighty-four cows were randomly selected to analyze risk factors relating to cows’ resistance to R. microplus ticks during the peripartum. Among these, 44 cows gave birth during the rainy seasons (spring and summer) and 40 during the dry seasons (fall and winter). Among the cows evaluated, 20 were pure Bos taurus (Holstein), 28 were half-blood F1 through crossbreeding (1/2 B. taurus 9 1/2 Bos indicus[Gir]), 21 were Girolando (5/8 B. indicus 9 3/8 B. taurus) and 15 were pure B. indicus. Regarding the number of lactations, 20 cows were at their first lactation, 25 at the second lactation, 24 at the third lactation and 15 at the fourth or subsequent lactation. In the milk production evaluation, the cows were classified according to their annual production. In the herd evaluated, 27 cows with milk production lower than 1,500 kg per year were classified as low-production animals, 37 with milk production between 1,500 and 3,000 kg per year were classified as having moderate milk production, and 20 cows with production higher than 3,000 kg per year were classified as high-production animals. In accordance with the routine management procedure at the experimental station, the pregnant cows were kept in an area of Brachiaria decumbens grass at an animal density of 5 AU/ha for the 30 days before calving. After birth and for the first 4 weeks of lactation, the animals were kept on B. decumbens and Panicum maximum pasture at an animal density of 3 AU/ha. During both of these periods, the animals received water and mineral salt ad libitum. During lactation, the cows were milked twice a day and received 3 kg of commercial concentrate a day, made up of citric pulp and commercial feed containing 22 % crude protein, in the proportions of 2:1. Rhipicephalus microplus ticks counts were weekly performed on all cows during the last 5 weeks of pregnancy, 1 week of calving and first 5 weeks of lactation. Each animal was put into an individual crate in order to count fully or partially engorged R. microplus females measuring 4.5–8.0 mm, from the right hemisphere of each cow, according to the procedure described by Wharton and Utech (1970). The result from each count was multiplied by two to calculate the monthly average for each animal. For the statistical analysis, the data were first subjected to the normality test (Kolmogorov–Smirnov) to ascertain whether the data conformed to normal distribution. Because the data did not show normal distribution even after logarithmic transformation to log10 (x ? 1), comparisons were made between averages by applying the parametric Kruskal–Wallis test at 5 % significance. The generalized linear model methodology was used, assuming Poisson distribution with a logarithmic link function. Lastly, interactions within the variance were investigated by means of the Spearman test. The operational procedures were done using the R Foundation statistical computing software, version 2.12.2 (2011).
Results The peripartum had an effect on infestation by R. microplus ticks (Fig. 1). The average tick count during the rainy season was 38 ticks/animal, while during the dry season, it was 33 ticks/animal (p [ 0.05; PR = 0.63). The infestation by R. microplus during the pre-calving, calving, and post-calving periods among the animals that gave birth during the rainy season were numerically higher than among those that gave birth in the dry season, but there was no statistically significant difference (Table 1). The average R. microplus count during the peripartum was 55 ticks/animal in Bos taurus animals, 39 ticks/animal in F1 B. taurus 9 B. indicus, 29 ticks/animal in Girolando
123
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Exp Appl Acarol (2014) 63:551–557
Counts of Rhipicephalus microplus
150 53±4.8
58±4.7 37±3.7
125
56±4.4
42±4.0 50±3.5
24±2.5 100
17±2.2
75
21±2.0 23±1.5
50 15±1.6 25 0
-5 week -4 week -3 week -2 week -1 week Calving 1 week 2 week 3 week 4 week 5 week
Pre calving Fig. 1
Calving
Post Calving
Rhipicephalus microplus tick counts during the peripartum period
Table 1 Evaluation of risk factors for infestation by Rhipicephalus microplus among cows during the peripartum, by means of Poisson regression Risk factors/variables
N
NS
X
PR
p
95 % CI
Pre calvinga
84
420
19
–
–
–
Calving
84
84
37
3.12
\0.001
[0.181–0.565]
Post calving
84
420
65
2.02
\0.001
[0.620–0.678]
Peripartum
Season Drya
44
484
33
–
–
–
Rain
40
440
38
0.63
0.055
[0.831–1.205]
Breed B. indicusa
15
165
18
–
–
–
F1
28
308
39
1.64
\0.001
[0.746–0.816]
Girolando
21
231
29
1.39
\0.001
[0.629–0.669]
B. taurus
20
220
55
2.10
\0.001
[0.442–0.510]
1° lactationa
20
220
60
–
–
–
2° lactation
25
275
44
0.97
0.045
[0.391–0.639]
3° lactation
24
264
19
0.91
\0.001
[0.871–0.958]
[3° lactation
15
165
16
0.97
0.030
[0.729–0.903]
No. of lactation
Milk prod (kg/year) \1,500a
27
297
19
–
–
–
1,500–3,000
37
407
28
0.91
0.125
[0.988–1.096]
[3,000
20
220
58
2.04
0.003
[0.852–0.969]
a
Value, N = number of animals evaluated, NS = number of samples evaluated, X = average tick count per animal, PR = prevalence ratio, CI = confidence interval, F1 = B. taurus x B. indicus
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and 18 ticks/animal in B. indicus. In all phases of the peripartum, the animals with higher levels of taurine blood were more vulnerable and had higher average populations of R. microplus (p \ 0.05; PR = 2.10). Among the crossbred animals, there was no statistically significant difference (p [ 0.05) in the tick counts (Table 1). In all three phases of the peripartum, the R. microplus counts were significantly higher (p \ 0.05) among the primiparous animals than among the multiparous ones (Table 1). The average R. microplus count during the peripartum was significantly higher (p \ 0.05) among first-lactation animals, which had an average of 60 ticks/animal, followed by second-lactation animals with an average of 44 ticks/animal. Among the animals that were at their third and fourth or subsequent lactations, the tick populations of ticks observed were 19 and 16 ticks/animal, respectively, which were not statistically significantly different from each other (p [ 0.05). The high-production animals were significantly (p \ 0.003; PR = 2.04) more vulnerable to infestation than were the low-production animals (Table 1). The average R. microplus count during the peripartum was 58 ticks/animal among high-production animals, 28 ticks/animal among moderate-production animals and 19 ticks/animal among lowproduction animals.
Discussion Although no study in the literature has evaluated tick infestation levels in relation to calving, it is known that the innate and acquired defense mechanisms of cattle are weaker during the peripartum period (Mallard et al. 1998). This reduced defense, together with changes to the immune system and the physical and metabolic weakening observed due to pregnancy and calving, contributes toward the fall in resistance and rise of incidence of ectoparasitism (Chorfi et al. 2004). According to Utech et al. (1978), pregnant animals are more susceptible to infestation by ticks than are nonpregnant animals, especially in the final third of pregnancy. Doube and Wharton (1980) claimed that a seasonal cycle of resistance to R. microplus tick might exist in cattle, due to oscillation in the animals’ immune ability against this parasite. These authors found that resistance to R. microplus ticks declined in the fall and early winter, regardless of the animals’ breed or nutritional state. Many authors have demonstrated that seasonal factors have an influence on the life cycle of ticks and consequently that differences in infestation dynamics exist in cattle, with possible variations according to the region, climate and period of the year (Oliveira et al. 1989; Doube and Wharton 1980). In the present study, the effect of the peripartum on R. microplus infestation was observed in both the dry and the rainy season, such that the parasite load increased from before to after calving. This demonstrated that, regardless of environmental conditions, the phenomenon of the peripartum had an important influence on R. microplus infestation levels. The average tick counts observed in this study demonstrated that there was a clear difference in resistance levels between the B. taurus and B. indicus animals. The half-blood F1 animals continued to be vulnerable and the Girolando animals became more resistant to infestations by R. microplus. These results demonstrate that to obtain animals with greater resistance, crossbreeding in which zebuine blood predominates is required. Tatchell and Moorhouse (1968) observed that B. taurus animals presented higher susceptibility to ticks than shown by B. indicus animals.
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The present study observed that primiparous animals were more susceptible while multiparous animals were more resistant. A wide variety of results concerning the influence of age on tick infestation can be seen in the literature. Andrade et al. (1998) found that older animals were more susceptible to ticks. The outcome from the present study corroborates the findings of Silva et al. (2013), who observed higher tick counts among primiparous cows than among multiparous cows. Bertrand et al. (1985) observed a direct relationship between milk production and disease incidence. In high-production dairy cows, the numbers of round neutrophils and mononuclear cells were significantly higher than in cows with intermediate productive potential (Detilleux et al. 1995). These results can be considered encouraging, considering that selection for high-production animals does not provide unfavorable responses relating to the functional ability of the immunological features. However, these animals are vulnerable to a higher number of diseases, especially during the peripartum (Detilleux et al. 1995).
Conclusion First-lactation and high-production B. taurus animals had greatest vulnerability to R. microplus infestation over the peripartum period. On the other hand, crossbred B. taurus and B. indicus animals presented satisfactory resistance and milk production. Thus, these animals are more efficient and cost-effective for tropical climates, and crossbreeding with predominance of zebuine blood is an ecologically sound way to control R. microplus ticks in cattle and to maintain good milk productivity in herds.
References Andrade ABF, Silva RG, Costa AJ, Rocha UF, Landim VJC (1998). Genetic and environmental aspects of the resistance of Zebu cattle to the tick Boophilus microplus. In: Proceedings of the 6th World congress on genetics applied to livestock production, 1998, Armidale: NSW, Austra´lia. Armidale, 27, 339–342 Anon (2002) Australian code of practice for the care and use of animals for scientific purposes. Australian Government Publishing Service, Canberra, ACT, Australia Bertrand JA, Berger PJ, Freeman AE, Kelley DH (1985) Profitability in daughters of high versus average Holstein sires selected for milk yield of daughters. J Dairy Sci 68:2287–2294 Chorfi Y, Lanevschi-Pietersma A, Girard V, Tremblay A (2004) Evaluation of variation in serum globulin concentrations in dairy cattle. Vet Clin Pathol 33:122–127 Detilleux JC, Kehrli ME Jr, Stabel JR, Freemad AE, Kelley DH (1995) Study of immunological dysfunction in periparturient Holstein cattle selected for high and average milk production. Vet Immunol Immunopathol 44:251–267 Donovan GA, Badinga L, Collier RJ, Wilcox CS, Braun RK (1986) Factors influencing passive transfer in dairy calves. J Dairy Sci 69:754–759 Doube BM, Wharton RH (1980) The effect of locality, breed and previous tick experience on seasonal change in the resistance of cattle to Boophilus microplus (Ixodoidea: Ixodidae). Experientia 36:1178–1179 Hewetson RW (1971) Resistance by cattle to the cattle tick Boophilus microplus. III. The development of resistance to experimental infestations by purebred Sahiwal and Australian Illawarra shorthorn cattle. Aust J Agric Res 22:331–342 Machado Neto R, D’arce RD (1979) Proteı´nas se´ricas nos perı´odos pre´ e po´s-parto de vacas da rac¸a Nelore. J Agric 53:13–19 Mallard BA, Dekkers JC, Ireland MJ, Leslie KE, Sharif S, Vankampen CL, Wagter L, Wilkie BN (1998) Alteration in Immune responsiveness peripartum period period and its ramification on dairy cow and calf health. J Dairy Sci 81:585–595
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Exp Appl Acarol (2014) 63:551–557
557
Martinez ML, Machado MA, Nascimento CS, Silva MVGB, Teodoro RL, Furlong J, Prata MCA, Campos AL, Guimara˜es MFM, Azevedo ALS, Pires MFA, Verneque RS (2006) Association of BoLA-DRB3.2 alleles with tick (Boophilus microplus) resistance in cattle. Genet Mol Biol 5:513–524 Oliveira GP, Alencar MM, Freitas AR (1989) Resisteˆncia de bovinos ao carrapato Boophilus microplus. II. Infestac¸a˜o natural. Pesq Agropec Bras 24:127–1267 Piper EK, Jonsson NN, Gondro C, Lew-Tabor AE, Moolhuijzen P, Vance ME, Jackson LA (2009) Immunological profiles of Bos taurus and Bos indicus cattle infested with the cattle tick, Rhipicephalus (Boophilus) microplus. Clin Vaccine Immunol 16:1074–1086 Roche JF, Mackey D, Diskin MD (2000) Reproductive management of postpartum cows. Anim Reprod Sci 2:703–712 Silva JB, Rangel CP, Baeˆta BA., Fonseca AH ( 2013) Influence of the physiological state on infestation by Rhipicephalus microplus in dairy cows. Ticks Tick-Borne Dis 4:52–56 Tatchell R, Moorhouse D (1968) The feeding processes of the cattle tick Boophilus microplus (Canestrini). Parasitology 58:441–459 Utech KB, Wharton RH, Kerr JD (1978) Resistance to Boophilus microplus in different breeds of cattle. Aust J Agric Res 29:885–895 Verı´ssimo CJ, Silva RG, Oliveira AAD, Ribeiro WR, Rocha UF (1997) Resisteˆncia e susceptibilidade de bovinos leiteiros mestic¸os ao carrapato Boophilus microplus. Bol Ind Anim 54:1–10 Wagland BM (1975) Host resistance to cattle tick (Boophilus microplus) in Brahman (Bos indicus) cattle. I Responses of previously unexposed cattle to four infestations with 20,000 larvae. Aust J Agric Res 26:1073–1080 Wharton RH, Utech KBW (1970) The relation between engorgement and dropping of Boophilus microplus (Canestrini) (Ixodidae) to the assessment of tick numbers on cattle. J Aust Ent Soc 9:171–182
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