In Mexico, the tick Rhipicephalus microplus poses a serious risk to the livestock sector since it negatively affects both meat and milk production. It also threatens export of live cattle to the United States of America, activity that generates 700 million dollars annually¹. This tick vector is commonly controlled by applying chemical compounds, although these are expensive and can be toxic to livestock and their handlers. Excessive and inadequate use of chemical tick control methods has generated resistance among ticks and caused a rethink of these methods². Comprehensive pest management is considered the best option for controlling ticks but requires detailed knowledge of the interactions between the environment, the host and the parasite. However, this control method can maintain tick populations at low levels, keeping livestock healthy. These low levels are still sufficient to infect animals with hemotropic pathogens at an early age, thus generating immunity against them and achieving enzootic stability³.

Adequate control of ticks in livestock requires thorough knowledge of variations in annual tick populations and of the influence of climate and management practices on these populations. The present study objective was to evaluate the degree of natural Rhipicephalus microplus infestation in dual-purpose cattle, identify any correlations between infestation and climatological factors, and its effect on weight gain.

Field work was done at La Posta Research Station, which belongs to the National Institute for Forestry, Agricultural and Livestock Research (Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias - INIFAP), in the state of Veracruz, Mexico (19°00’49” N; 96°10’ W; 12 m asl). Regional climate is subhumid (Aw1), with a 25°C annual average temperature (35.3°C maximum, 15°C minimum), 1,641 mm annual average rainfall and 74.4% average relative humidity (RH).

Experimental animals consisted of 31 Bos taurus x Bos indicus cattle (13 heifers and 18 bulls), which were 11/16 Holstein x 5/16 Zebu (3.2%), 11/16 Brown Swiss x 5/16 Zebu (3.2%), 3/4 Holstein x 1/4 Zebu (16.1%), 3/4 Brown Swiss x 1/4 Zebu (25.8%), 5/8 Holstein x 3/8 Zebu (25.8%), 5/8 Brown Swiss x 3/8 Zebu (6.5%), undefined Holstein x Zebu crosses (16.1%), and undefined Brown Swiss x Zebu crosses (3.2%). At the beginning of the experiment average animal age was 307 d. Bulls and heifers were kept separate, under a rotational grazing system in contiguous pastures of established grasses: Tanzania (Megatyrsus maximus), Signal (Urocholoa decumbens), Pangola (Digitaria decumbes) and Mombaza (Megatyrsus maximus). Mineral salts and water were offered freely year round. During the dry season (December to May) sorghum (Sorghum vulgare) silage was provided ad libitum. The animals were vaccinated annually (August) against paralytic rabies and semi-annually (March and September) against clostridiasis. They were also treated for gastroenteric nematodes every 6 mo. A feed concentrate (18% crude protein, 70% total digestible nutrients) was provided at 1 kg per animal per day.

The population dynamics of R. microplus on the sampled animals was documented by counting all the semi-engorged ticks (4.5 to 8.0 mm in diameter) found on them. Samples were collected every 28 d for 15 mo, from August 2014 to October 2015. Tick collection and counting were done by the same field technician. Collections were done in the morning (08:00 h) by placing an animal in a covered handling pen and inspecting it from the head to the base of the tail, including the anterior and posterior limbs and the ventral region⁴. At each sampling, animal body weight was measured using an electronic scale. No chemical tick control methods were applied during the study period. As ticks were removed from the animals they were placed in a 70% alcohol solution. All were identified and taxonomically classified at La Posta’s Animal Health Laboratory, following established criteria⁵. Data on environmental temperature and relative humidity were obtained from La Posta’s weather station, which belongs to the National Network of Automated Agricultural Weather Stations of INIFAP. Rainfall data were not available for the study period.

The studied response variables were number of semi-engorged ticks (tick count) per animal, individual weight gain and average weight gain per animal. Tick count was the number of ticks collected from the left side of the animal after a period of 28 d. This variable has a high correlation (>0.90) with the number of ticks on the animal’s entire body⁶. Overall average tick count per animal was 39.4, with a range of 0 to 264. Individual average tick counts were used to classify tick infestation level: 1) low (0 to 30 ticks); 2) moderate (31 to 60 ticks); and 3) high (61+ ticks). Individual weight gain consisted of the body weight (kg) gained by an animal after a 28-d period. Average weight gain per animal was calculated by dividing the sum of individual weight gain results per 28 d by the total number of measurements.

All statistical analyses were run using the SAS statistical package⁷. Tick count per animal was analyzed with the GENMOD procedure (PROC GENMOD), using a repeated measurements model that included the fixed effects of sampling month (period), calf’s sex and breed group. For this variable, a Poisson distribution was declared as a subroutine in GENMOD, and a first-order autoregressive covariance structure [AR(1)] model was applied. Individual weight gain was analyzed with the MIXED procedure (PROC MIXED), using a repeated measurements model that included calf’s sex and breed group as categorical variables, and tick count, environmental temperature and RH as covariates; the previously mentioned covariance structure was applied. In the analysis of individual weight gain, environmental temperature and RH were included in the statistical model, rather than month (period) of sampling. This was done because the focus was not on differences in weight gain between months, but rather on more accurate adjustment for climatological factors and production of a linear regression coefficient of individual weight gain on tick count per animal. Average weight gain was analyzed with the GLM procedure (PROC GLM), using a model that included infestation level (high, medium and low). In a preliminary analysis, the effects of calf’s sex and breed group were found not to be significant (P>0.05), and were therefore not included in the definitive model. In the analyses of tick count per animal and average weight gain the differences between means were tested with the PDIFF option. A Pearson’s correlation coefficient, run with the CORR procedure (PROC CORR), was used to estimate degree of association between tick count per animal and environmental temperature and RH, as well as between average tick count and average weight gain.

Average tick count per animal varied widely from a low of 6 to a high of 94, and infestation level varied correspondingly (Table 1). Average individual weight gain also varied broadly from a low of 8 kg to a high of 18 kg, with an overall average of 11.9 kg.

Sampling month had a significant effect on tick count (P=0.0199), and the linear effect of tick count was significant for individual weight gain (P=0.0212). Infestation level (IL) had a significant effect on average weight gain (P=0.001). Average tick count was higher (P<0.05) in the hottest month (July) than in all other sampling months (Table 2).

For example, in the most extreme cases, in the month of July the animals exhibited 46.6 and 57.0 more ticks than in September (2015) and October (2015), respectively. Tick count did not differ (P>0.05) between April (45.0), May (43.0) and June (45.1), months which had similar values for environmental temperature and RH. Again, tick count did not differ (P>0.05) between January (20.7) and February (18.5), both months with relatively low temperatures. Of note is that the tick counts in these cooler months was lower (P<0.05) than in relatively warmer months such as April, May and June. This trend is supported by the corresponding Pearson’s correlation coefficient results, which indicated that tick count per animal was higher at higher temperatures (0.21; P<0.0001). There was a weaker correlation between lower RH and higher tick counts (-0.19; P<0.0001).

The annual fluctuations in tick population observed in the present data coincide with previous studies in which variations responded to regional climate conditions. For example, in a study using – Bos taurus x ¼ Bos indicus cattle R. microplus infestation (average ticks per animal) was found to be highest in May (93) and June (82) but lowest (<10) in November and March when RH was lower than in May and June⁸. A more recent study using Criollo Lechero Tropical cattle in central Veracruz found that tick (Amblyomma cajennense + Boophilus microplus) infestation (ticks per animal) was highest in August (11.1 ± 0.6) and October (12.0 ± 0.6), both high rainfall months (11.9 and 17.9 mm, respectively), but lowest (2.9 ± 0.6) in May which has low rainfall (1.4 mm); environmental temperatures did not differ between these months⁹. In a study done in the dry tropics of Mexico (Culiacán, Sinaloa), infestation levels (average number of ticks per animal) in cattle were affected by temperature, with high levels (50) during the hottest months from July to October and lower levels (30) as temperatures dropped in November and December¹⁰. This contrasts with a report on terminal cross calves in which B. microplus infestation levels (ticks per animal) were higher (155 ± 10) in February and March, which are cooler and drier (22°C average temperature; 49 mm rainfall), than levels (26 ± 15) in September and October, which are hotter and have more precipitation (26.4°C average temperature; 271 mm precipitation)¹¹.

Males tended to have more ticks than females (29.9 vs 22.1 ticks; Table 3), although the difference was not significant (P<0.055). This generally coincides with a study done in Australia in which tick count was 90% higher in male than in female cattle, suggesting that sex hormones exercise a strong effect on parasite resistance¹². However, the present results contrast slightly with the lack of difference in infestation levels between eight-month-old male and female calves under humid tropical conditions¹¹. Another study also reported a lack of difference in tick count between bulls and heifers (3.2 ± 0.6 vs 3.5 ± 0.4) of the Criollo Lechero Tropical breed in Mexico⁹.

Infestation levels did not differ between the evaluated breed groups (P>0.05), although 11/16 Brown Swiss x 5/16 Zebu calves tended to have fewer ticks than those of the other breed groups (Table 4). This lack of difference may be an artifact of sample size in the present study. If the overall sample size had been larger the means probably would have had lower standard errors, allowing identification of inter-breed group differences in tick count. Previous reports do identify inter-breed group variation in tick count. A study comparing – B. taurus x ¼ B. indicus to ½ B. taurus x ½ B. indicus cattle found that the former had higher tick counts than the latter in nine months of the year⁸; that is, the higher the proportion of genes from European breeds the higher the count. This is noteworthy since the 62.5 to 75.0% European breed percentage interval in the present study is lower than the 50 to 75% interval in the cited study⁸, which would imply greater genetic diversity in the latter. However, inter-breed group differences in tick count have been reported between crosses with uniform proportions of B. taurus versus B. indicus; one study found that ½ Braunvieh-¼ Holstein-¼ Zebu calves had higher natural tick infestation levels than ½ Black Angus-¼ Holstein-¼ Zebu and ½ Red Angus-¼ Holstein-¼ Zebu calves¹¹.

Zebu breeds (B. indicus) have been reported to be more resistant to ticks than European breeds (B. taurus)^13,14. For example, in one study with Nelore cattle counts for engorged B. microplus females increased progressively as the proportion of European genes increased: 3.3 in Nelore; 25.2 in ½ Nelore x ½ Fleckvieh; 22.5 in ½ Nelore x ½ Chianina; 21.0 in ½ Nelore x ½ Charolais; and 59.7 ticks in 3/8 Nelore x 5/8 Angus¹⁵. A study done in South Africa also reported higher tick counts in cattle as the proportion of European genes increased: 5.3 in Nguni (tropically adapted African breed, B. taurus x B. indicus); 24.1 in Bonsmara (5/8 Afrikaner and 3/8 Hereford or Shorthorn); and 37.4 in B. taurus (Hereford). A study in South Africa¹⁶ found that the average number of ticks was 37.4, 24.1 and 5.3 in Hereford, Bonsmara (5/8 Afrikaner and 3/8 Hereford or Shorthorn) and Nguni (tropically adapted African breed, product of the combination of breeds B. taurus and B. indicus), respectively.

In one study under field conditions (i.e. natural infestation) in Australia B. taurus x B. indicus cattle were found to carry fewer ticks than B. taurus (Shorthorn x Hereford) cattle¹². It has been argued that this disparity in IL may be due to Zebu breeds’ exhibition of behavior aimed at avoiding ticks, their greater skin sensitivity and more frequent and thorough grooming habits in comparison to exotic B. taurus breeds¹⁷. Differences in tick counts by breed have also been reported between B. indicus breeds; for instance, in a study of one-year-old animals, Brahman cattle were found to have twice as many B. microplus ticks as Nelore cattle¹⁸.

The linear regression coefficient for weight gain on tick count (-0.03442 kg/tick; P<0.05) represents a 34 g weight loss per tick during a 28-d period. Under the studied conditions this means that in the month of July each evaluated animal lost an average of 2.1 kg of body weight. This weight loss is only slightly higher than the 28 g per adult Amblyomma hebraeum tick reported in Brahman, Brahman x Simmental, Sanga and Hereford bulls¹⁹. However, the coefficient calculated here is lower than the -0.42 kg/tick/10 mo (i.e. 420 g weight loss over ten months) reported elsewhere²⁰. Of note is that the present results and those of the aforementioned studies are far in excess of the 4.4 g weight loss per engorged tick reported for Rhipicephalus appendiculatus in cattle²¹.

The Pearson’s correlation coefficient (-0.67; P<0.0001) supported the above findings in that it showed average weight gain to be negative as tick count increased. This coincides with the coefficient of -0.61 estimated between weight gain and cumulative tick count (Amblyomma americanum) in Angus x Zebu cattle in Texas²². A study done in Zambia in two herds of Sanga breed cattle found that weight gain was negative (-0.72 and -0.70) and moderately correlated to tick count (Amblyomma variegatum)²³. Another study reported a negative and moderate correlation (-0.52) between weight gain and tick count (A. variegatum) in the Gudali breed (B. indicus) in Cameroon²⁴.

Compared to the animals with a high IL, those with a medium level gained 2.88 kg more weight per sampling period while those with a low level gained 3.87 kg more (P<0.05; Table 5). A study done in Brazil with Holstein-Zebu cattle also reported greater weight gain at low infestation levels than at medium and high levels, although it did not specify the criteria for classifying infestation level²⁵. In an evaluation of the effects of engorged tick load (Boophilus microplus; diameter >5 mm) in Norman cattle, highly-infested animals (138 to 300 ticks) weighed 24 kg less at d 125 of the test than lightly-infested animals (0 to 33 ticks)²⁶. There are multifold reasons why some animals have higher tick counts than others in the same environment, although several authors suggest that an animal’s immunological response to ticks may affect their tick count^27-29.

The present results indicate a lack of adequate control of B. microplus infestation during the warmest months (April to July) in the study area. Calf’s sex and breed group had no effect on tick counts. The correlation between average tick count and average weight gain was negative and moderate, meaning animals with high infestation levels had lower weight gain than those with medium and low levels. Tick infestation clearly affects animal productive potential and needs to be effectively controlled.