(Acari: Ixodidae), the Karoo paralysis tick. L.Jo Fourie a, V.N. Belozerov b and D.J. Kok a a Department of Zoology and Entomology, University of the Orange ...
Experimental & Applied Acarology, 20 (1996) 477-481
477
Short Communication
Sex ratio characteristics in lxodes rubicundus (Acari: Ixodidae), the Karoo paralysis tick L.Jo Fourie a, V.N. Belozerovb and D.J. Kok a
a Department of Zoology and Entomology, University of the Orange Free State, PO Box 339, Bloemfontein 9300, South Africa b Biological Research Institute, St Petersburg University, Old Peterhoff198904, St Petersburg, Russia ABSTRACT The sex ratio is an important parameter which characterizes the state and dynamics of natural populations of animals. Although ixodid ticks are specialized ectoparasites, most species are bisexual and are characterized by a I: 1 sex ratio for their progeny. In natural populations and even in laboratory colonies, biased sex ratios are olten observed. Ixodes rubicundus, the Karoo paralysis tick, parasitizes domestic stock and wild ungulates in South Africa. Adults quest from vegetation, can mate off or on the host and males are seldom parasitic. We hypothesized that the sex ratio for/. rubicundus would be 1:1 when observed directly in the progeny but that it would be strongly biased towards females in samples of parasitic adults. The results mostly supported the hypothesis but it was also shown that unexplained and unpredictable variations can occur. On hosts, females dominated strongly, except on adult angora goats where the sex ratio was biased in favour of the males. This disparity may be related to a greater retention of males in the coarse, curly hair of angora goats compared to the other hosts. Monthly variations in the sex ratios of the tick on hosts are believed to be related to the large fluctuations in sex ratios of questing ticks. Key words: Ixodes rubicundus, ticks, Karoo paralysis, sex ratio.
The sex ratio is an important parameter which characterizes the state and dynamics of natural populations of animals. Information on the sex ratio and its distorters, the mechanism of sex determination and manifestation and sex ratio allocations is of fundamental importance (Wrensch and Ebbert, 1993) in understanding the biology of populations and is also of applied importance in terms of the biological control of pests (Davey and Cooksey, 1988). With more specific reference to ticks, the sexes are also differentially implicated in their potential to either cause diseases or act as vectors for pathogens (Bezuidenhout and Malherbe, 1981; Zaugg et al., 1986). An understanding of the dynamics of the sex ratio changes may therefore also be important in the epidemiology of tickborne diseases. Most ixodid ticks are bisexual and are characterized by a 1:1 sex ratio for their progeny (Oliver, 1989). This is, however, often contradictory to the actual situation in nature where biased sex ratios can occur in populations (V. N. 0168-8162 © 1996 Chapman & Hall
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L . J . FOURIE ETAL.
Belozerov, L. J. Fourie and D. J. Kok, unpublished). Data on the sex ratios of ixodid ticks are dispersed in the literature. There is, however, a great paucity of publications which specifically attempt to explain the sex ratio of particular ixodid species in relation to the sampling methods used and intrinsic factors which may influence the sex ratio. The objectives of this study are to present data on the sex ratios of Ixodes I UUI~Ut'IW~b
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domestic stock and natural hosts. Data on the sex ratios of parasitizing hosts were collected on the farm Preezfontein (29°50'S, 25°22'E), situated 10 km from the town of Fauresmith in southwestern Free State, South Africa. Information on the sex ratios of the progeny of I. rubicundus was obtained from two sources, namely laboratoryreared nymphs fed in the laboratory but maintained in the field and laboratory reared nymphs fed and maintained in the laboratory. Nymphs to be maintained in the field were fed in the laboratory on their natural host, Elephantulus myurus, each month from July to December 1988 (n = 360) and May to November 1989 (n = 240) and placed in observation containers under vegetation in the field (Fourie and Horak, 1994). After moulting, the sex ratio of the adults was determined. Nymphs to be maintained under laboratory conditions were also fed on their natural hosts. These nymphs (n = 511) were fed and maintained at 93% RH, 20°C and a light regime of 14L: 10D which led to non-diapause development (F. J. Van der Lingen, unpublished data). After moulting, the sex ratio of the adults was determined. Adult mountain reedbuck (Reduncafulvorufula) (n = 28) were shot during the winters of 1986 and 1989 and carefully searched, visually and by palpation, for the presence of ticks. All ticks (male I. rubicundus are rarely parasitic and thus remain mostly unattached; Fourie et al., 1988) were placed in labelled vials for identification and counting. Ticks were also collected from sheep and goats which consisted of between six and ten of each of the following age and sex categories: adult angora ewes; adult angora kapaters; young angora kapaters (approximately 16 months), angora kids (approximately 5 months), adult merino ewes, adult merino wethers, young merino wethers (approximately 11 months) and adult dorper ewes. From April to September during 1988 and 1989, on an approximately fortnightly basis, five animals belonging to each group were selected at random and subjected to a whole body search. Ticks were collected as indicated above. Angora kids were not available during 1988 and dorper ewes were only investigated during 1989. The counts of ticks for particular months were pooled. The data on the sex ratios are presented as a sex ratio (SR) index, i.e. the ratio of females to males in a sample. Comparisons between various samples were made with the use of a binomial test for proportions and X2 tests. An SR value of 1.52 (60%) was recorded for adults which moulted from nymphs in the field during 1988-1989 (n = 134). During the 1989-1990 season (n = 329) a preponderance of males was recorded with an SR value of 0.83 (45%
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479
females). Pooling of the data yielded an SR value of 1 (50% females). Nymphs fed and maintained in the laboratory (n=463) moulted into 53% females (SR= 1.12). This did not differ significantly from parity (Z2 = 1.57, p = 0.20). The sex ratio of/. rubicundus ticks collected on specific age and sex groups of hosts did not differ significantly (p > 0.05) between 1988 and 1989. The data for the 2 years were therefore pooled and are summarized in Table 1. With the eXUCp tlUll O l i i t I . U l t ttllgUt a gUi:lt:5, W l l f ~ l ~ lll~l,lt3 LIUK~ p r e u o m m a t e u , m e ~ t ~ l o t the ticks on all the other hosts was biased significantly in favour of females. The SR of/. rubicundus sampled from merino wethers and ewes differed significantly (p < 0.001). This was not the case for angora kapaters and ewes. In general the SR of the ticks on adult hosts differed significantly from those on the young animals. To serve as a representative example of monthly changes in the SR, the values for the ticks sampled from merino wethers during 1988 and 1989 are summarized in Table 2. From the results it is evident that the SR may vary markedly between months during the seasonal activity period of adult ticks. The sex ratio observed directly in the progeny of/. rubicundus ticks did not differ significantly from parity. A similar observation was made for/. hexagonus (Toutoungi et al., 1993) and Ixodes canisuga (Smith, 1972). A preponderance of females (62%) was, however, reported for Ixodes rugicollis (Aubert, 1981). In Ixodes ricinus (V. N. Belozerov, unpublished), Ixodes persulcatus (Arumova, 1988), Ixodes muris (Smith, 1944) and Ixodes rnatopi (Colborne and Norval, 1982) males usually dominated in the progeny. In some of these cases where the sex ratio differed markedly from parity, sample sizes were small and the validity of the results can be questioned. For/. ricinus and/. persulcatus it has been shown that developmental diapause affects the sex ratio in the progeny. Amongst those nymphs which underwent a developmental diapause male dominance was more pronounced compared to those that developed without diapause (Ammova, 1988; V. N. Belozerov, unpublished).
TABLE 1 SR index for adult I. r u b i c u n d u s ticks sampled from various hosts Host
SR
n
Z2 test
Adult merino wethers Adult merino ewes Young merino sheep (mixed sex) Adult angora kapaters Adult angora ewes Young angoras (mixed sex) Angora kids Dorper ewes Mountain reedbuck
3.89 2.33 3.57 0.68 0.84 1.19 3.07 4.10 3.62
1080 830 562 500 549 834 411 396 745
* * * * * * * * *
* Differs significantly (p < 0.05) from parity.
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L.J. FOURIE ETAL.
TABLE2 Seasonal changes in the SR ofL rubicundus ticks sampled from merino wethers during 1988 and 1989 (sample sizes of ticks are given in parentheses) Month
April May June July August September
1988
1.50(5) 3.39 (136) 2.48 (101) 14.00 (15) * *
1989
13.22(128) 2.94 3.67 8.50 8.00 6.00
(315) (266) (76) (27) (7)
* Sample size too small.
The type of host on which I. rubicundus was sampled had a significant effect on the sex ratio. On sheep and mountain reedbuck there was a strong preponderance of females (66-80%). On angora goats, on the other hand, the sex ratio was either biased in favour of females in kids, almost equal in young goats or males predominated on adult goats. This disparity in the sex ratios of ticks between hosts is most probably related to greater retention of the males in the long, coarse, dense and curly hair of adult angora goats compared to the other hosts. Females, being parasitic, may also be dislodged more easily by the horns of the goats during grooming. Age-related differences in pelage texture, the ability to dislodge attached ticks through grooming action or the behavioural differences between young and older animals may all be factors which affect the sex ratio of I. rubicundus on different hosts. The monthly variations in the sex ratio of/. rubicundus on hosts are most probably related to the large fluctuations in the sex ratio for questing ticks (De Jager, 1988; Fourie and Kok, 1995). The ratios of Ixodes ticks on hosts are almost exclusively characterized by a preponderance of females (Norval, 1974; Babenko et aL, 1977; Barnard, 1981). An exception is Ixodes dammini (=Ixodes scapularis) where a strong dominance of males (62-66%) occurred on American white-tailed deer (Kitron et aL, 1992). The data were collected at the end of the tick activity period and could possibly indicate that males are able to overwinter on deer. Biased sex ratios in the prostriate ticks are believed to be related to the ability to mate both on and off the host (Babenko et aL, 1977; Oliver, 1989). In the metastriate ticks, where mating usually occurs only on the hosts (Oliver, 1989), sex ratios are biased in favour of males (Horak, 1982). ACKNOWLEDGEMENTS We acknowledge the financial support of the University of the Orange Free State and the Foundation for Research Development.
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