Experimental and Applied Acarology 25: 899–908, 2001. © 2002 Kluwer Academic Publishers. Printed in the Netherlands.
A survey of ticks (Acari: Ixodidae) on dairy cattle on the island of Menorca in Spain J. CASTELLÀ1, A. ESTRADA-PEÑA2,∗, S. ALMERÍA1, D. FERRER1, J. GUTIÉRREZ1 and A. ORTUÑO1
1 Department of Parasitology, Veterinary Faculty, Bellaterra, 06019, Barcelona, Spain 2 Department of Parasitology, Veterinary Faculty, Miguel Servet 177, 50013, Zaragoza, Spain
(Received 27 March 2001; accepted 30 January 2002)
Abstract. A survey of ticks affecting dairy cattle under extensive management on Menorca island (off the Spanish Mediterranean coast) was performed through 1999–2000 on seven farms. The species collected were Rhipicephalus bursa, R. turanicus, Hyalomma m. marginatum, H. lusitanicum and Boophilus annulatus. The most abundant species were R. bursa and H. m. marginatum, with peaks of 10.7 (in summer) and 7.5 (in spring) ticks/cow, respectively. R. turanicus was scarcely encountered, while B. annulatus and H. lusitanicum were abundant only in a few localities. The mild climate and adequate vegetation on the island provide satisfactory habitat for extended periods of tick activity, as compared with other regions where these ticks have been collected. The competence of the ticks as vectors for pathogens and the difficulty of using acaricide treatments in the region are discussed. Key words: Boophilus, Hyalomma, Rhipicephalus, Menorca, dairy cattle, ticks
Introduction The control of ticks and tickborne diseases (TTBD) is a major component of animal health programmes for the protection of livestock, and enhances global food security (De Castro et al., 1997). The present methods for TTBD control rely on the application of acaricides based on the ecological and epidemiological knowledge of ticks and their associated diseases. A key challenge in this area is that control policies are sometimes implemented without the use of sound scientific knowledge on the distribution, associated pathogens and seasonal abundance of most common tick species. Ticks in the Mediterranean region are a major constraint on ruminant production because they affect livestock and are also responsible for the transmission of pathogens such as Babesia and Theileria (Papadopoulos et al., 1996). The mild Mediterranean climate, together with the adequate vegetation conditions in ∗ Author for correspondence (Fax: +34-976-761612; E-mail:
[email protected])
900 the region, provide adequate conditions for the survival of several xerophilic tick species. These species may also be associated with wild animals, ensuring wide dispersion rates. Knowledge of the distribution of ticks affecting domestic stock, together with their seasonal dynamics, would greatly refine acaricide application and, therefore, provide economic benefits. This study reports on the tick faunal composition in dairy cattle on Menorca Island, including data about seasonal dynamics.
Material and Methods Menorca island is located in the Mediterranean Sea, close to the Spanish coast, within 3◦ 45 –4◦ 17 E and 39◦ 45 –40◦ 10 N (Figure 1). It is a small island (approximately 741 km2 ) with vegetation dominated by Pinus halepensis and Olea europaea. Some small areas carry abundant Quercus spp., degraded with Cistus spp., Pistacia lentiscus, Erica spp. and Calluna spp. Pastures are interspersed within these forest formations, together with bush areas. Stone walls of variable height enclose most pasture fields (see Figure 2). Cattle are customarily kept within these enclosures while feed is available. Management methods include the rotation of the entire herd through different pasture plots according to the weather and grass availability. Elevations on the island are not higher than 400 m. The climate is Mediterranean, with an average yearly rainfall of 450 mm. The rainfall pattern is bimodal with maxima in spring
Figure 1. Map of the western Mediterranean region, showing the geographical location of Menorca island, together with the sampling localities (small stars).
901
Figure 2. Some aspects of the habitats and vegetation of the Menorca island, showing an overview of the island (A), the pastures extent and cover extension (B), a typical forest habitat with P. halepensis and O. europaea (C) and the typical stone walls surrounding properties (D).
(March–April) and winter (December–February). The average temperature in January is 10–12◦ C, and 24–26◦ C in July. The northern parts of the island are colder and have the highest evaporation levels as a consequence of the dominant north winds. The main domestic stock is dairy cattle. A small number of sheep (approximately 500) pasture on some parts of the island. Wild ungulates are absent. Neither deer nor wild boar is present on the island. However, rabbits are abundant throughout the island, mostly in open habitats. In 1997, seven farms were selected for tick sampling procedures (see Figure 1). These farms were selected as representative according to their vegetation and number of stocked animals. These farms were visited eight times in 1999–2000, and on each visit 10–20 cattle were sampled after the milking procedures in the afternoon or evening. Although the entire animal was explored for ticks, special attention was paid to the udder, perineum and the internal sides of the legs. After collection, ticks were separately stored in 70◦ C ethanol until species determination was performed in the laboratory, according to the keys by Estrada-Peña (2000).
902 Table 1. Species and stages of ticks collected on dairy cattle in Menorca island, in the period 1999–2000 Site
Rhipicephalus turanicus
Rhipicephalus bursa
Total
Males
Females
Nymphs
Binigaus Vell Binimetlla Binisequi Son Bonaventura Son Gornes Son Nadal Son Tema
2 12 33 6 1 0 4
1 4 16 2 0 0 0
0 8 17 4 1 0 0
1 0 0 0 0 0 4
Total
58
23
30
5
Site
Boophilus annulatus
Total
Males
Females
Nymphs
335 112 327 108 451 401 81
136 20 120 23 151 140 48
132 44 150 46 182 183 28
67 48 57 39 118 78 5
1815
638
765
412
Hyalomma m. marginatum
Total
Males
Females
Nymphs
Total
Males
Females
Nymphs
Binigaus Vell Binimetlla Binisequi Son Bonaventura Son Gornes Son Nadal Son Tema
81 1 204 87 34 0 16
12 1 34 18 5 0 0
68 0 162 65 29 0 6
1 0 8 4 0 0 10
127 43 222 40 176 21 343
84 28 150 25 103 15 216
43 15 72 15 73 6 127
0 0 0 0 0 0 0
Total
423
70
330
23
972
621
351
0
Site
Hyalomma lusitanicum Total
Males
Females
Nymphs
Binigaus Vell Binimetlla Binisequi Son Bonaventura Son Gornes Son Nadal Son Tema
12 15 4 72 47 2 204
6 8 4 71 28 2 149
6 7 0 1 19 0 55
0 0 0 0 0 0 0
Total
356
268
88
0
Sampling localities are included in the left column.
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Figure 3. Relative seasonal abundance of the five most prominent species collected on dairy cattle in Menorca.
Results A total of 3624 ticks was collected. The tick fauna of dairy cattle on Menorca Island is composed of Rhipicephalus bursa Canestrini et Fanzago, Hyalomma
904 m. marginatum Koch, H. lusitanicum Koch, Boophilus annulatus Say and R. turanicus Pomerantsev. Only one specimen of Haemaphysalis punctata was collected and is not included in the counts. Nymphs of both Hyalomma species were not encountered; furthermore, no larvae were present in our collections. Table 1 shows the total number of each species and the stages collected. R. bursa ranks first in abundance, comprising more than 50% of the total ticks captured. The relative abundance of the two Hyalomma species was clearly different in the Menorca cattle tick faunal composition, with 26.8% of H. m. marginatum and 9.8% of H. lusitanicum. However, H. lusitanicum was abundant on one farm, but scarce on the others. Figure 3 shows the relative abundance of the collected tick species according to the season of the year. More than 50% of the R. turanicus specimens were collected in autumn, although this tick species remains active, but in very low
Figure 4. Seasonal tick faunal composition on dairy cattle in Menorca. Rt: Rhipicephalus turanicus; Ba: Boophilus annulatus; Hm: Hyalomma m. marginatum; Hl: Hyalomma lusitanicum; Rb: Rhipicephalus bursa.
905 proportions, throughout the year. The highest proportion of R. bursa (74%) was collected in summer, together with B. annulatus (more than 90%). The two Hyalomma species recorded displayed different seasonal patterns. The majority of H. m. marginatum specimens were recorded in the spring and summer months (94%), whereas H. lusitanicum was more common in autumn. However, the activity of both species extended into summer (H. m. marginatum) and spring–summer (H. lusitanicum). Some 62% of the total ticks were collected in summer, with 18 and 19% in spring and autumn, respectively. The tick load in winter accounts for only 0.85% of the total ticks collected. The seasonal faunal composition is thus different (Figure 4). In spring (March–May), H. m. marginatum and R. bursa are the predominant species, with H. m. marginatum accounting for more than 60% of tick load. This proportion is inverted in summer (June–August), when R. bursa is the dominant species. Both H. lusitanicum and B. annulatus are present in these seasons, but in low numbers. In autumn and winter, R. bursa is again the most commonly collected species, with H. lusitanicum as the second ranked species in autumn (September–November). R. turanicus accounted for more than 25% of specimens in winter (December–February).
Figure 5. Relative abundance per host of the five most prominent tick species according the season of the year. Both adults and nymphs are included in calculations. Rt: Rhipicephalus turanicus; Ba: Boophilus annulatus; Hm: Hyalomma m. marginatum; Hl: Hyalomma lusitanicum; Rb: Rhipicephalus bursa.
906 However, this feature must be regarded with caution because of the low total number of ticks recorded in winter. The number of ticks per cow is also a very variable feature (Figure 5). H. lusitanicum, R. turanicus and B. annulatus remained at very low numbers throughout the year. Peaks of H. m. marginatum are recorded in spring and summer, with 7.5 and 4.5 ticks/cattle, respectively. As mentioned above, R. bursa is active throughout the year, with a peak of 10.7 ticks/cattle recorded in summer, approximately 4 ticks/cattle in autumn, and 2.2 and 1.8 ticks/cattle in spring and winter, respectively. Discussion The tick fauna on cattle in Menorca is typical of western Mediterranean regions (Morel, 1965). These are xerophilic species, well adapted to a dry environment with low rainfall most of the year. However, the accentuated Mesomediterranean environment prevents other species, such as Dermacentor marginatus (absent in our captures) and H. punctata (only 12 specimens collected), from colonizing the region. These species are more adapted to an oromediterranean climate (Gilot and Pautou, 1983; Gilot, 1985) and are, therefore, absent from the sampled area. In addition, the area is too dry to support adequate habitats for Ixodes ricinus. Although this species has been reported on other Mediterranean islands such as Corsica (Elfassy, 1993), the relative humidity in the surveyed habitat remains too low throughout the year to permit the existence of permanent populations of this important tick. The low prevalence of R. turanicus in our samples is surprising, because it prefers habitats similar to those sampled. Furthermore, it is a common parasite of cattle (Papadopoulos et al., 1996) meaning that the absence of adequate hosts cannot be ascribed as the main cause of its relatively low abundance. In agreement with previous reports (Ferrer and Castellà, 1999), R. turanicus is active later in the year than R. bursa. The latter species is well represented in our samples, being the most abundant tick on the dairy cattle of Menorca island. R. bursa is present in every type of Mediterranean habitat (Papadopoulos et al., 1996; Sahibi et al., 1998) and, therefore, the high prevalence in every sampled farm was expected. In this sense, both H. m. marginatum and H. lusitanicum have been collected in wide areas of the Mediterranean region (Manilla, 1998), although H. lusitanicum is geographically restricted to parts of the western Mediterranean and the Canary islands off the Atlantic African coast. H. m. marginatum prefers attenuated Mesomediterranean habitats, leading to the low relative abundance reported here. Most H. m. marginatum specimens were collected in spring, in accordance with the typical activity pattern of the species recorded in other
907 regions (Ghirotti and Maroli, 1997). Nearly all H. lusitanicum specimens were collected in autumn, indicating a clear seasonal pattern of activity, as previously reported by Habela et al. (1999). The management practices of the farmers on the island are responsible for the extended period of tick activity in some species over the entire year. The usual practice on these farms is to keep cattle stock enclosed while feed lasts, the duration of enclosure varying according to the prevailing climate and desiccation condition. However, the mild Mediterranean conditions, as well as the stone walls enclosing each plot that provide more humid conditions for flat ticks, ensure tick survival even in the absence of domestic stock or wild ungulates. Consequently, although a seasonal pattern may be inferred for some tick species, those better adapted to the prevailing conditions (e.g., R. bursa and H. m. marginatum) may be questing for long periods independent of the seasonal preferences observed for these species in other regions. The tick species reported in this study have previously been associated with pathogen transmission. A serological survey carried out on the island (Almería et al., 2000) demonstrated the existence of B. bigemina, B. bovis, T. annulata and T. buffeli. Both Hyalomma species reported herein have been incriminated in the transmission of T. annulata (Habela et al., 1999; Viseras et al., 1999), and B. annulatus is an acknowledged vector of cattle Babesia species. In addition, there exists a considerable risk of tick spread from Menorca to adjacent islands, as immature ticks of the Hyalomma species are common parasites of migratory birds (Osácar et al., 1998). This possibility has not been further studied, and studies on the topic are yet to be performed on nearby islands. Both Hyalomma species as well as R. bursa are also common parasites of wild ungulates; however, wildlife is almost absent from the island. Therefore, domestic stock is the only host available for these species making eradication of most important tick species a realistic possibility. However, acaricide treatments are performed without a scientific basis on tick seasonal activity. Treatments are carried out at the discretion of the owners, most commonly by spraying organophosphates and/or pyrethroids onto the back and udder. However, milking practices include the washing of the udder area twice daily before connection to the milking machine. This washing, although compulsory according to sanitary measures, renders the acaricide treatment almost useless, as the chemical is washed away soon after application. This practice greatly complicates the possibilities for control. In the same way, no control exists for tick-borne diseases, but only chemical treatment after the onset of clinical symptoms. Vaccination efforts using commercially available vaccines against concealed antigens (Willadsen and Jongejan, 1999) should provide a feasible framework for the eradication of, at least, Boophilus ticks, and should also cause some degree of damage to other ticks, as demonstrated previously (Preston and Jongejan, 1999).
908 Acknowledgement This work has received financial support from the project AGF1998-1097C02-02, CICYT (Spain).
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