Ewerimental & Applied Acarology, 18 (1994) 23-35 23

The life cycle of Ixodes rubicundus (Acari: Ixodidae) and its adaptation to a hot, dry

environment

L.J. Four i e ~ and I.G. H o r a k ~

"Department ~fZoology and Entomology, Univer~'ity of the Orange Free State, P.O. Box 339. Bloemfontein 9300, South Africa

I'Faculty of Veterinar T Science, University of Pretoria. Onderstel)oort 0110. South Afiica

(Accepted 25 November 1993)

ABSTRACT

Fourie, L.J. and Horak. I.G., 1993. The life-cycle oflxodes rubwundus t Acari: lxodidae) and its adap- tation to a hot, dry environlnent. Exp. Appl. Acarol., 18: 23-35.

The life cycle of lxodes rubicumhls, the Karoo paralysis tick. was studied under field conditions in the south-western Orange Free State, South Africa, by placing freshly engorged ticks in small con- tainers. The life cycle extends over 2 years. The two regulating phases in the life cycle, which undergo a morphogenetic diapause during the hot and d~' summer months, are the egg and engorged nymph. Possible behavioural diapause in adults which suppresses questing activity before the end of March. can also serve as a third regulating phase. Temperature affects the duration of the pre-ovilx~sition perkxt of engorged females and the pericxt between detachment of engorged larvae from hosts and ecdysis. Commencement of larval hatch is reasonably synchronized, irrespective of the month dur- ing which oviposition occun'ed. Peak activity periods of larvae (April or May) occur during a period of high rainfall and decreasing daily maximum temperatures. The peri(nl between detachment of engorged nymphs from hosts and ecdysis is highly variable (8--36 weeks). All developmental stages of the tick occur mainly during autumn and winter and no ticks are active during the hot summer months of December to February. Larvae. nymphs and adults each survive for only one season.

INTRODUCTION

Tick life cycles are subject to a great deal of variability. The nature of the area of geographic distribution, environmental associations within it. habitat type and host relationships rnm'kedly affect the duration and phenology of the cycle (Balashov, 1972). For the synchronization of their life cycles with favourable climatic seasons and the enhancement of survival, ticks make use of various types of diapause (Belozerov, 1982). The identification of diapausing stages and peculiarities of the life cycle are important in understanding the habitat- and host relationships of ticks. This is of particular relcvancc for medically or veterinary important species.

© Science and Technology Letters. All rights reserved.

24 L.J. FOURIE AND I.G. HORAK

The Karoo paralysis tick, Ixodes rubicundus, is of considerable economic impor- tance in South Africa since it causes paralysis in a variety of domestic and wild animals (Stampa, 1959; Spickett and Heyne, 1988; Fourie et al., 1989; Fourie and Vrahimis, 1989). Its host preference is similar to that of other three-host species (Balashov, 1972) with larvae and nymphs feeding on small mammals (elephant shrews and rock rabbits) and adults mainly on wild and domesticated artiodactylids (Stampa, 1959; Horak et al., 1987; Fourie et al., 1992). The tick inhabits mainly hilly or mountainous terrain and occurs in close association with certain plant species (Stampa, 1959; Fourie et al., 1991). It is widely distributed in the Orange Frec State and Eastern Cape Province and occurs at several localities in the south- ern as well as western Cape Province, the Transvaal and Natal (Howell, 1983; Horak and Fourie, 1992). A recent survey has shown that the distribution range of the tick is increasing (Spickett and Heyne, 1988).

The Karoo paralysis tick occurs in regions characterized by winter or equinoc- tial rainy seasons, with mean annual rainfall varying from 100 to 600 mm. Because of the irregular rainfall within its distribution range, mild to severe droughts occur periodically. Air temperatures show major diel and seasonal fluctuations. Maxi- mum temperatures may reach 41°C and minimum temperatures may be as low as - 14°C. A range of 25°C between maximum day and minimum night temperatures within 24 hours is not unusual (Venter et al., 1986). The potential duration of the frost period (period from first to last occurrence) may be as long as 183 days. It is therefore evident that the tick occurs in regions where, for a large part of the year, it is exposed to unfavourable and even adverse climatic conditions within its macro- habitat.

The purpose of this study was to investigate the life cycle of/. rubicundus under field conditions, to identify diapausing stages and to ascertain the various features of the life cycle which enable it to survive and even extend its range.

M A T E R I A L S A N D METH O D S

The study was conducted on the farm Preezlbntein which is situated 10 km from the town of Fauresmith (29°46'S; 25°19'E) in the south-western Orange Free State, South Africa. The area falls within the Karoo biome biotic formation and the vege- tation is defined as false upper Karoo (Acocks, 1975). Intensive investigations on various aspects of the biology of the Karoo paralysis tick and epidemiology of Karao paralysis have been conducted at this site since 1985 (Fourie et aL, 1989; Petney and Fourie, 1990; Fourie and Van Zyl, 1991; Fourie et al., 1991).

Meteorological data were obtained from a weather station at Fauresmith. Within the study area L rubicundus is closely associated with certain shrubs and trees, par- ticularly wild olive trees (Olea europaea africana) (Fourie et al., 1991 ). Temper- ature changes in the litter beneath an olive tree on each of a distinct south- and an opposing north facing hill slope were recorded with a data logger (MC Systems: Cape Town) programmed to record daily minimum, maximum and mean temper-

THE LIFE CYCLE OF IXOOES RUBICUNDUS (ACAR[: IXODIDAI':} 25

atures. Temperature sensors were placed at a depth of 2 cm within the litter and for comparative purposes temperature changes beneath rooigras (Themeda triandra) tufts about 2 m from the edge of the canopy cover of the olive trees, were also recorded.

The life cycle of L rubicundus was investigated by observations made on ticks in containers placed 2 cm deep in litter under the olive trees where the temperatures were being recorded. The open ends of the cylindrical perspex con- tainers (30 X 15 ram) were scaled with Nybolt bolting cloth with apertures of 250 b~m. Each container consisted of two equally-sized paris which were screwed together.

Engorged female ticks were collected from Merino sheep on Preezfontein. Depending on their availability between 3 and 23 ticks (n = 57) were collected on a monthly basis from May to July 1988 and were individually placed in marked containers buried below olive trees growing on opposing hill slopes. Except for August when only one tick was collected a similar procedure was followed from April to September 1989 and on each occasion 4 to 7 engoged females (n = 62) were buried under the olive trees.

Larvae and nymphs used in the experiments originated from females which engorged on sheep. These ticks were placed in 10 mL glass vials, plugged with cot- ton wool and kept in a closed glass container {85 _+ 5% RH) in the laboratory at 18-25°C to oviposit. Eggs, fiat and engorged lar~,ae and fiat and engorgcd nymphs were maintained under similar conditions. The engoged larvae and nymphs used in the experiments had all been fed on elephant sbaews (Etephantulus myurus) in the laboratory at temperatures of 18-25°C and a natural light regime correspond- ing to that of specific months. Separate batches of larvae were l}d each month from March to July 1989, and after detachment were placed in groups of 15 (n = 270) in lbttr containers. Two containers were each placed under the olive trees on north and south lacing slopes. Nymphs were fed cach month from July to Dccember 1988 (n = 360) and May to November 1989 (n = 240). Duplicate batches of 10-15 nymphs were placed in the observation containers under the olive trees as before.

The various containers were inspected at approximately 14 day intervals from May 1988 to October 1990. Data recorded included pre-oviposition period, time of egg cclosion, moults to nymphs and adults and survival of larvae, nymphs and adults. The term premoult period used in this study designates the period between detachment of engorged larvae or nymphs from the host and ecdysis. In the case of larvae that hatched, survival was categorized on a subjective scale from 4 to 0 (4 = all larvae alive; 0 = all dead).

In order to determine the presence of adults in the field before the onset of sea- sonal activity (end of March or April), litter and grass tufts under or close to trees or shrubs with which the tick is known to be associated, were collected during Feb- mary and placed in plastic bags. The contents of these bags were examined in the laboratory for engorged nymphs or adults.

26 l , . J . FOURII ' I A N D I .G. H O R A K

RESULTS

Climatic data for the Fauresmith rcgion are graphically illustrated in Fig. 1. Rain during the study period fell mainly from Novembcr to March. The mean total annual rainfall for the period 1980-89, excluding 1988 when abnormally high rain- tall occurred (total rainfall 1,048 mm), was 371 mm. Mean monthly temperatures showed a steady decline from January, the hottest month of the year, to June and July. Daylight length (sunrise to sunset) increased from 10.25 hours during June to about 14 hours during December (Fig. 1). Seasonal temperature changes in the litter under trecs and under exposed grass tufts are summarized in Table 1. Higher mean temperatures were recorded under trccs on northern than on southern slopes. The differences were more pronounced during late winter and spring (July to October).

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THE Ell,15 CYCLE OF IXODES RUBICUNI)US (ACARI: IXODn)AE) 27

TABLE l

Comparison between temperature recordings made under trees and grass tufts on mwthern and southern slopes.

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Trt~(~ July 1988 11.4 1.3 6.6 17.8 9.5 2,9 6.3 14,3 August 12.2 1.5 8.0 17.7 11.2 1.4 7.8 15.6 September 12.7 3.8 86 18,8 11.5 2.5 9.2 13.9 October 14.6 3.9 10.0 21,0 12.9 2.8 10.4 16.5 November 17.7 2.8 13.2 24.7 17.0 2,4 13.2 22.4 December 17.9 2. l 14.5 22.4 17.4 1,5 15.(1 20,9 Janua~" 1989 19.2 1.5 16.3 23.8 19.0 0.9 17.4 21.8 Februat,y 17,4 1,5 15.2 21.5 17,4 0.9 16.(I 19.7 March 16,9 2.6 14.0 2(I,9 17.0 2.3 15,0 20.7 April 14.9 2.8 12.1 18.5 14.7 2.(1 12.4 17.9

Grass tuft July 1988 12.1 1.6 1.7 30.4 9.4 3.3 2.5 23.8 August 14.1 1,6 3.4 31.3 12.4 1.8 5.3 27.2 September 16.0 4.2 6.9 30.3 14.8 3.5 9.4 24.9 October 18.5 4.5 7.5 16.7 4.0 11.3 26.8 November 23.3 3.1 13.5 39.6 20.6 2.1 15.5 29.9 December 23.6 3.2 14,4 38.5 20.8 2.0 15.8 29.6 January 23.7 2.8 16.8 35.1 21.7 1.8 18.2 29.0 Februa~ 1989 20,3 2.4 15.6 28.9 19.l 1,6 16.7 24.1 March 20.3 3.6 11.5 .M-.8 18.3 2,9 11,7 31.0 April 17.0 3.4 9.8 29.3 14.5 2.8 9.5 23.7

Except that diel and seasonal fluctuations were more pronounced, a sinfilar situation was true for temperatures recorded under grass tufts. Mean monthly maxi- mum temperatures as high as 39.6°C were recorded under tufts on northern slopes at the bcginning of summer (Table I ).

The duration of the pre-oviposition period of engorged females varied from 1 to 4 months (Fig. 2) and was related to the time of engorgement. Females which engorged during August and September, a time characterized by increasing monthly temperatures (Fig. 1 ) had the shortest pre-oviposition periods. There was also a ten- dency towards shorter pre-oviposition periods for females on the warmer northern than on the southern slopes. The commencement of oviposition for females which engorged during the same period was asynchronous and variation of up to 8 weeks between individuals was observed (Fig. 2).

Eggs took 3½ to 7½ months to hatch (Fig. 2). The commencement of hatching was reasonably synchronized, irrespective of the time of oviposition, and took place from early February or early March until April (Fig. 2). This period is character- ized by relatively high rainfall, and decrcasing daylength and temperatures (Fig. 1;

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Table 1). Larval survival was high from March to mid-May (4-3.7 on subjective scale), after which a rapid decrcase occurred (1.3 for June). All larvae were dead towards the end of September (Fig. 6). The time from detachment of engorged lar- vae until ecdysis was dependent on temperature and varied from 7 to 18 weeks. Larvae engorging at the beginning of April, with mean monthly air temperatures above 15°C (Fig. 1), had the shortest premoult period and those engorging during June or July, the coldest months of the year, the longest (Fig. 3). The moulting of larvae into nymphs was synchronized within batches. Towards the end of December all flat nymphs in the observation containers were dead (Fig. 6).

There were major differences in the premoult periods of engorged nymphs into adults between the 1988/89 and 1989/90 seasons. During 1988/89 this period var- ied from 8 to 30 weeks (Fig. 4) compared to 21 to 36 weeks in 1989/90 (Fig. 5). During March of 1989 about 70% of the engorged nymphs had moulted compared to 4% in 1990 (Figs 4 and 5). The mean maximum temperature for the period August 1988 to March 1989 was significantly lower (t = 3.4; p = 0.01) compared with the same period during 1989/1990. Mean minimum temperatures did not dif- fer significantly. The numbers of live adults in the observation containers reached

rilE I,IFE CYCLE OF IXODES RUBICUNDUS (ACARI: IXODIDAE) 29

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a peak in April and in May during 1989 and 1990 respectively (Figs 4 and 5). There- after mortality increased gradually and no adults survived until November.

No adults or engorged nymphs were found in the litter or grass tufts that were examined.

Figure 6 is a graphical representation of the life cycle of l x o d e s r u b i c u n d u s as well as the seasonal abundance of the various life stages on hosts (adapted from Fourie et al., 1989; Fourie et al., 1992; Fourie and Kok, 1992; Horak and Fourie, 1992). The life cycle probably extends over a period of 2 years.

DISCUSSION

Considering the economic importance of Karoo tick paralysis there is a surprising paucity of knowledge on the life cycle of 1. r u b i c u n d u s . Available information is of a fragmented nature (Stampa and Du Toit, 1958), or can only be deduced from studies on hosts (Horak e t al. , 1987), or was obtained under laboratory conditions (Neitz et al. , 1971). None of these studies addressed the importance of photoperiod in influencing the nature and duration of tick ontogeny (Belozerov. 1982). Nevertheless the present results support those of Stampa and Du Toit (1958) and Horak et al. (1987) that the life cycle of I. r u b i c u n d u s extends over 2 years. The two regulating phases in the life cycle which undergo a morphogenetic (develop- mental) diapause are the eggs and engorged nymphs. Since adults intbst hosts in

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THE LIFE CYCI.E OF IXODES RUBICUNDUS (ACARI: IXODIDAE) 3 ]

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3 2 L.J. FOURIE AN'[) I.G. I IORAK

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Fig. 6. Diagrammatic representation of the life cycle of Ixodes rubicundrs and seasonal abundance on hosts of larvae, nymphs and adults (lower graph). A: Pre-oviposition: B: Oviposition; C: Eggs undergo a morphogenetic diapause; D: Larvae; E: Nymphs; F: Adults; G: Adults undergo bchavioural diapause; H: Morphogenetic diapausc - engorged nymphs (for further details scc text).

THt- l.lI"g CYCLE OF IXODI-TS RL,FHf'UNDUS (..\CARl: IXOL)II)AEJ 33

the southern Orange Free State from the end of March at the earliest, the data strongly suggest that adults which moult early in the season undergo a behavioural diapause which suppresses questing activity. Larvae, nymphs and adults each sur- vived for only one season and no ticks are active during the hot summer months of December to February.

Since unfed larvae are the most prone to die because of adverse climatic condi- tions (Stampa. 1959; De Jager, 1988) their hatching is the most critic',.d stage in the life cycle. Although the commencement of lar~'al hatch was reasonably synchro- nized, irrespective of the month during which oviposition occurred, not all the egg batches deposited during a particular month hatched simultaneously. During the 1989/90 season the difference between the commencement of hatching for batches deposited during the same month varied by up to 2 months. Decreasing mean monthly temperatures from February onwards most probably slow down the rate of embryogenesis and hence eclosion. This may be the reason why larvae are active and attach to hosts over an extended period lasting from March to October (Horak et al., 1987; Fourie et at., 1992).

Peak activity periods (April or May) for larvae (Stampa. 1959; Fourie et al., 1992) correspond to the time of the year during which the population density of their main natural host (E, myurus) is highest (Du Toit, 1993). These territorial, small, insectiw)rous mammals, which inhabit rocky terrain, have little resistance to L rubicundus infestation (Du Toit, 1993) ~md consequently a large percentage of immature ticks are able to engorge successfully.

The rate at which engorged larvae moult to nymphs is dependent on tempera- ture. The premoult period increases with decreasing mean monthly temperature. This relationship is supported by the observation that there is a tendency for the period from detachment of engorged larvae from hosts up to ecdysis to be shorter for engorged larvae on the warmer northern slopes than for thosc on the southern slopes. The present results support the observations of Stampa (19591) and Fourie et al. (1992) of a 3 to 4 month difference in the peak period of larval (April or May) and nymphal (August) infestations of hosts. Although nymphs may also occur on hosts during early or mid-summer (November to January), infestation levels are usually very low (Stampa, 1959: Horak et al., 1991: Fourie et al., 1992). The present findings support those of Horak el al. (1987) and Fourie et at. (1992) that nymphs are active and survive for only one season.

The premoult period of nymphs into adults is highly variable between years and this is difficult to explain. The complex interplay between photoperiod and tem- perature in inducing diapause (Belozerov, 1982) in engorged nymphs is currently being investigated. Most nymphs oversummer in the engorged state.

Since adult seasonal activity begins near the end of March or in April in the southern Orange Free State (Fourie et al., 1989: Fourie and Kok, 1992) this sug- gests that adults, originating from nymphs which moulted early in summer, undergo a behavioural diapause. The results of De Jager (1988) on the total energy content of adult lxodes rubicun&ts at the beginning of the season, indicate that a certain

34 L.J. FOURIE AND I.G. HORAK

proportion (3-26%) have significantly lower energy levels than other ticks of this species sampled at the same time. Investigations made over a 4 year period during the onset of seasonal activity of adults have also shown that between 4 and 82% of the females examined had been inseminated preprandially (Fourie, unpublished data). These findings suggest that adults may display some form of activity e.g. mate-seeking and copulation betbre the onset of seasonal activity at which time vertical migration and hence questing commences.

The onset of seasonal activity of adults varies within and between regions and may occur from February to April (Stampa, 1959; Fourie et al., 1989; Fourie and Kok, 1992; Horak and Fourie, 1992). The available data suggest that it is related to temperature. Seasonal activity commences sooner in areas where the tempera- tures are lower during late summer than in areas where temperatures are higher (Fourie, unpublished data). The seasonal activity of adults peaks during April to June (Stampa, 1959; Fourie et al., 1989; Fourie and Kok, 1992). The number of living adults present in the observation containers in the current study is in accor- dance with field observations. All engorged nymphs have moulted by May. Since adults survive until October this suggests a maximum longevity of about 5 months, Adults are found attached to hosts until September or October (Stampa, 1959; Fourie et al., 1989; Fourie and Kok, 1992).

Most adult tick activity occurs during autumn or winter (Stampa, 1959; Fourie et al., 1989), periods characterized by decreasing mean monthly rainfall and tem- perature. The critical equilibrium activity (0.93) of adults is similar to that of other members of the genus, but transpiration rates are lower (De Jager, 1988). Survival of the tick is enhanced through its association with certain grasses, shrubs and trees which provide it with a favourable microhabitat (Stampa, 1959; Fourie et al., 1991).

In summary, the semivoltinc life cycle ofL rubicundus is synchronized with sea- sonal climatic changes through morphogenetic diapause (egg and engorged nymph) and most probably behavioural diapause of adults. Temperature most probably modulates the induction of diapause, influences the rate of embryogenesis and the rate of moulting and therefore affects the activity period of larvae, nymphs and adults. The tick is a true winter tick with most of the seasonal activity of the vari- ous developmental stages occurring during winter months. Periods in major larval activity, the most abundant and sensitive developmental stage, are correlated with peak abundance of their preferred hosts, decreasing temperatures and relatively high rainfall.

A C K N O W L E D G E M E N T S

We wish to thank Mr. J. van Niekerk, owner of the farm Preezfontein, for the use of the facilities on his farm and Prof. V.N. Belozerov (Biological Research Insti- tute, St. Petersburg University, Russia) for constructive comments on the manu- script. The technical assistance of Mrs. C. Human is gratefully acknowledged. This

THE LII;E CYCI.E OF IXODES RUBICUNDUS (ACARI: IXODIDAE) 35

research was funded by the Depa r tmen t of Agr icu l ture and Water Supply, the Mea t

Board and Bayer A n i m a l Health,

REIZERENCF~S

Acocks, J.P.H., 1975. Veld types of South Africa. Mem. Bot. Surv. S. Aft.. 18 pp. Balashov Yu.S., 1972. Bloodsucking ticks (lx~oidea) - Vectors of Diseases of Man and Animals.

Misc. Publ. Entomol. Soc. Am., 8(5): 376 pp. Belozerov, V.N., 1982. Diapause and biological rhythms in ticks. In: F.O, Obenchain & R. Galun

(Editors), Physiology of Ticks. Pergamon Press, New York, pp. 469-500. De Jager, C., 1988. Water- en cnergieverhoudings by die Karooverlammingsbosluis, lxodes rubi-

cundus Neumann, 1904 tAcari: Ixodidac). M.Sc. Thesis, University of the Orange l"ree Stale, South Africa, 171 pp. (unpubl.).

Du Toil, S.J., 1993. Ecophysiology and host status of the lOCk elephant shrcw Elephantulus myurus (Thomas & Schwann. 1906). M.Sc. thesis, University of the Orange Free State. South Africa, 200 pp. (unpubl.).

Fourie, L.J. and Kok, O.B., 1992. The role of host behaviour in tick-host interactions: a domestic host-paralysis tick model. Exp. Appl. Acarol., 13: 213-225.

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