Biology of Ixodes Rubicundus Ticks under Laboratory Conditions: Observations on Oviposition and Egg Development

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  • Biology of Ixodes rubicundus ticks under laboratoryconditions: observations on oviposition and eggdevelopment

    F.J. VAN DER LINGENa, L.J. FOURIEa* D.J. KOKa and J.M. VAN ZYLba Department of Zoology and Entomology, University of the Orange Free State, PO Box 339,Bloemfontein, 9300, South Africab Department of Mathematical Statistics, University of the Orange Free State, PO Box 339,Bloemfontein, 9300, South Africa

    (Received 17 February 1998; accepted 6 October 1998)

    Abstract. Observations on oviposition and egg development of Ixodes rubicundus were made underlaboratory conditions. Engorged females were exposed to temperatures in the range 1025C and relativehumidities (RHs) of 33 and 93%. The pre-oviposition period, oviposition period, incubation period,conversion efficiency index (CEI) values and fecundity were determined. The mean pre-ovipositionperiod varied from 13.3 days (temperature 25C and RH 33%) to 68.3 days (temperature 10C and RH93%). Oviposition extended from a mean of 39 days (temperature 25C and RH 93%) to 201.7 days(temperature 10C and RH 93%). The developmental zero temperature for the pre-oviposition period was9.2C. The mean total number of eggs produced by engorged I. rubicundus females varied from 2045.7(temperature 10C and RH 93%) to 3777.7 (temperature 20C and RH 93%). Both female mass and RHsignificantly (p , 0.01) influenced the number of eggs produced. CEI values varied between 43.154.4%(RH 93%) and 34.142.5% (RH 33%). At 93% RH females produced between 14.2 and 17.7 eggs per mgbody mass compared to the 13.214.6 eggs per mg body mass at 33% RH. The shortest mean incubationperiod recorded was 164.3 days (temperature 25C and RH 93%). The developmental zero temperaturefor incubation was 6.5C. Both the pre-oviposition and oviposition periods of I. rubicundus are moreextended compared to other species of the genus. Ixodes rubicundus produces a large number of smalleggs compared to other prostriate ticks.Exp Appl Acarol 23: 513522 1999 Kluwer Academic Publishers

    Key words: Ixodes rubicundus, pre-oviposition period, oviposition period, egg yield, conversionefficiency index, fecundity, laboratory study.

    Introduction

    The Karoo paralysis tick Ixodes rubicundus is of considerable economic importancein South Africa because it causes paralysis in a variety of domestic stock and wildanimals (Spickett and Heyne, 1988; Fourie and Vrahimis, 1989). It inhabits mainlyrocky outcrops and occurs in close association with certain plant species (Stampa,1959; Fourie et al., 1991).

    * To whom correspondence should be addressed.

    Experimental and Applied Acarology 23: 513522, 1999. 1999 Kluwer Academic Publishers. Printed in the Netherlands.

  • The ticks geographic distribution range is characterized in some regions by winterand in others by equinoctial rainfall, with mean annual rainfall varying from 100 to600 mm. Mild to severe droughts occur periodically. Air temperatures show majordiurnal and seasonal variations with temperatures as low as 214C or as high as41C during winter and summer, respectively. A difference of 25C betweenmaximum day and minimum night temperatures may occur (Venter et al., 1986). Itis evident that I. rubicundus, in its natural habitat, is subjected to adverse conditionsduring large parts of the year. A field study on the life cycle of the tick has shownthat it extends over 2 years. The two regulating phases in the life cycle of the tick,which undergoes a developmental diapause during the hot and often dry summermonths, are the egg and engorged nymph (Fourie and Horak, 1994).

    Comparatively little research on the life cycle of I. rubicundus under controlledlaboratory conditions has been conducted. A better understanding of certain aspectsof its life cycle could contribute towards elucidating its current and potentialbiogeographic distribution, seasonality and mortality factors. The purpose of thepresent controlled laboratory study was to investigate the effect of selected tem-perature and relative humidity regimes on the duration of the pre-oviposition andoviposition periods, egg yield and eclosion in I. rubicundus.

    Material and methods

    Engorged, female I. rubicundus ticks were collected from Angora goats during Apriland May 1993 and 1994 on the farm Preezfontein, situated 10 km from the townFauresmith (29 46'S, 25 19'E) in the south western Free State province of SouthAfrica. Only fully engorged, recently detached females that were still retained in thedense and curly hair of the goats were used. Limited numbers of such ticks wereavailable for the study. The ticks were weighed and placed individually intonumbered cylindrical (15 3 30 mm) Perspex containers (UOFS, instrumentationworkshop). The open ends of the containers were sealed with nylon gauze (Nyboltbolting cloth with pores of 200 mm). Each container consisted of two equally-sizedparts which were screwed together. The small, Perspex containers with ticks wereplaced in larger containers in which the relative humidity (RH) could be controlledthrough the use of saturated salt solutions (Winston and Bates, 1960). Temperature-controlled incubation cabinets were used to expose females in groups of three or fourto temperatures in the range 1025C (5C intervals) and RHs of 33 and 93 6 2% foreach temperature interval. The containers were kept in constant darkness.

    Each engorged female was examined every second day to determine the onset ofoviposition, following which each female was examined daily. The eggs depositedby each female were counted with the aid of a stereomicroscope and then transferredto a correspondingly numbered, 7 ml glass vial, covered with 200 mm pore size nylongauze (Nybolt bolting cloth) to ensure sufficient circulation. These vials were placed

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  • in the same container as the females. At the completion of egg laying, egg batcheswere weighed to the nearest 0.01 mg. Because of the range of conditions to whicheggs were exposed during the extended oviposition period some egg batches driedout or became infected with fungi. These batches, although counted, could not beweighed. This affected the number of egg batches available for the calculation of theconversion efficiency index (CEI) (see below).

    Egg batches used to determine the time to eclosion were not counted or weighedin order to leave them undisturbed. Three to seven egg batches were available for thedetermination of incubation period. Egg batches were monitored twice a week andthe incubation period was taken as the time (in days) from laying of the first egg toeclosion of the first larva. The experimental conditions were extended to include30C also.

    The CEI (Drummond and Whetstone, 1970) was expressed as a percentage torepresent the percentage body mass (engorged female) converted to egg mass.Because some egg batches dried out or became infected with fungi (see above) datawere limited for some of the temperature and humidity regimes (see column n inTable 3).

    CEI (%) 5 (m1/m2) 3 100

    where m1 is the egg batch mass (g) and m2 is the engorged female mass (g).Fecundity, expressed as the mean number of eggs per mg female engorged mass,

    was determined for females at each temperature and RH.The data obtained are presented as mean values. An ANOVA was used to

    determine the influence of engorgement mass, temperature and humidity on the pre-oviposition and oviposition periods. A multiple regression analysis and ANOVAwere used to determine the effect of female engorgment mass, temperature andhumidity on the number of eggs laid. A critical low temperature (developmentalzero) for each developmental stage was calculated from the regression equationbetween temperature and the developmental velocity (reciprocal of days of pre-oviposition or incubation period).

    Results

    Because limited numbers of fully engorged female ticks were available for exposureto a wide range of experimental conditions, only three to four ticks were used at eachtemperature/RH regime. Furthermore, some egg batches were affected by lowhumidity, high temperature, fungal growth or combinations of these, particularly inthose cases where the eggs had to be kept under experimental conditions forextended periods. Therefore, although at least three to four ticks were used for eachcondition in a few cases the results were based on more limited observations.

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  • The mean pre-oviposition period varied from 13.3 (temperature 25C and RH33%) to 68.3 (temperature 10C and RH 93%) days with minimum and maximumpre-oviposition periods of 12 (temperature 25C and RH 93%) and 75 days(temperature 10C and RH 93%) respectively (Table 1). Oviposition extended froma mean of 39 (temperature 25C and RH 93%) to 201.7 (temperature 10C and RH93%) days (Table 1). The minimum and maximum oviposition periods were 34(temperature 25C and RH 33%) and 288 (temperature 10C and RH 93%) days,respectively (Table 1).

    Temperature significantly (p , 0.05) influenced the pre-oviposition and oviposi-tion periods. Mass and RH, however, had no significant effect. The relationship(r 5 0.8059) between temperature and the reciprocal of the pre-oviposition period isgiven by the following equation:

    y 5 b 3 log(x 2 a)

    where a 5 8.15, b 5 2.68, y is 1/pre-oviposition period (days) and x is the tem-perature (C). A developmental zero temperature of 9.2C was calculated.

    The oviposition pattern of females maintained at 20C and 93% RH is presentedin Fig. 1. The number of eggs deposited rose sharply to reach a mean peakproduction of 174 eggs day1 on day 10, after which it decreased gradually up to day45. Few eggs (, 25) were deposited daily from day 45 up to day 67 (Fig. 1). Themean total number of eggs produced by engorged I. rubicundus females varied from2045.7 (temperature 10C and RH 93%) to 3777.7 (temperature 20C and RH 93%).The absolute minimum and maximum numbers of eggs produced were 1717 and5092, respectively (Table 2). Both female mass and RH significantly (p , 0.01)influenced the number of eggs produced. The relationship (r 5 0.83) between femalemass and number of eggs is reflected by the following linear regression equation:

    y 5 a 1 bx

    Table 1. Pre-oviposition and oviposition periods (days) of engorged I. rubicundus females exposed todifferent temperature and RH regimes

    Pre-oviposition period (days) Oviposition period (days)Temperature(C)

    RH(2%)

    Femalex mass

    (g) x Minimum Maximum x Minimum Maximum n10 93 0.116 68.3 64.0 75.0 201.7 133 288 310 33 0.180 58.3 57.0 60.0 116.3 105 136 315 93 0.205 16.0 15.0 17.0 49.7 46 52 315 33 0.195 19.7 16.0 23.0 50.7 46 59 320 93 0.112 17.0 15.0 19.0 61.3 51 67 320 33 0.166 18.3 16.0 22.0 48.0 42 57 325 93 0.187 14.0 12.0 20.0 39.0 36 44 425 33 0.170 13.3 13.0 14.0 60.7 34 108 3

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  • where a 5 2989.602, b 5 20324.95, y is the number of eggs and x is the femalemass (g).

    The number of eggs produced by females exposed to different temperature and RHregimes can be calculated by using the following multiple regression equation:

    y 5 ax1 1 bx2 1 cx3 1 d

    where a 5 21.8, b 5 400.8, c 5 19 138.07, d 5 21342.419, y is the number of eggs,x1 is the temperature (C) (r 5 0.006), x2 is the RH (%) (r 5 0.1849) and x3 is thefemale mass (g) (r 5 0.8678).

    CEI values for females exposed to the different temperatures and RHs are given inTable 3. RH and CEI values were significantly (p 5 0.0266) correlated (r 5 0.7662)whereas temperature and CEI values were not significantly (p 5 0.8549) correlated(r 5 0.0777). At an RH of 93% between 43.1 and 54.4% of the engorged body mass

    Figure 1. Mean (S.E.) number of eggs laid per day by I. rubicundus females at 20C and 93% RH.

    Table 2. Total numbers of eggs laid and fecundity of I. rubicundus females

    Egg number

    Temperature (C) RH (2%)Female xmass (g) x Minimum Maximum Fecundity n

    10 93 0.144 2045.7 1717 2590 14.20 310 33 0.180 2382.7 1869 2985 13.20 315 93 0.198 3501.0 3111 3858 17.70 315 33 0.189 2661.7 1879 3520 14.10 320 93 0.221 3777.7 1791 5092 17.10 320 33 0.166 2277.7 2074 2385 13.72 325 93 0.187 2805.0 2592 3224 15.00 425 33 0.170 2477.0 2267 2719 14.60 3

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  • was converted into eggs. At an RH of 33% this conversion varied between 34.1 and42.5%. The fecundity (x number of eggs/x mg body mass) for females exposed to thedifferent temperatures and RH is given in Table 2. Engorged females at an RH of93% produced between 14.2 and 17.7 eggs per mg body mass. At an RH of 33% thefecundity varied between 13.2 and 14.6. Neither temperature (p 5 0.6203 andr 5 0.2085) nor RH (p 5 0.0557 and r 5 0.6951) were significantly correlated withfecundity.

    The relationship between temperature, RH and mean egg incubation period issummarized in Table 4. No eggs hatched at either an RH of 33% or a temperature of30C. Only one out of six egg batches exposed at temperature 10C and RH 93%hatched after 562 days. The shortest mean incubation period recorded was 164.3 daysat 25C. The relationship (r 5 0.3964) between temperature and the reciprocal of theincubation period of eggs is described by the following equation:

    y 5 b 3 log(x 2 a)where a 5 6.53, b 5 2.19, y is 1/incubation time (days) and x is the temperature (C).The developmental zero temperature for incubation was calculated as 6.5C.

    Table 3. Engorged I. rubicundus female mass, egg mass and CEI values (%)Female Mass (g) Egg Mass (g)Temperature

    (C)RH(2%) x Minimum Maximum x Minimum Maximum CEI (%) n

    10 93 0.116 0.116 0.050 0.050 43.1 110 33 0.180 0.169 0.200 0.061 0.044 0.082 34.1 315 93 0.205 0.202 0.208 0.112 0.111 0.112 54.4 215 33 0.195 0.155 0.235 0.083 0.072 0.093 42.5 220 93 0.112 0.112 0.054 0.054 48.1 120 33 0.166 0.170 0.174 0.057 0.052 0.062 34.2 325 93 0.187 0.166 0.218 0.083 0.075 0.096 44.5 425 33 0.170 0.159 0.192 0.069 0.060 0.076 40.5 3

    Table 4. Incubation period of I. rubicundus eggs

    Incubation period (days)Temperature (C) RH (2%) x Minimum Maximum n10 93 562 562 110 33 a 615 93 180.0 131 201 615 33 620 93 170.5 138 190 620 33 625 93 164.3 150 179 725 33 630 93 330 33 3a No hatching of eggs.

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  • Discussion

    A decrease in pre-oviposition time for I. rubicundus with an increase in temperatureis in accordance with that generally found for ixodid ticks (Fujimoto, 1992;Guglielmone, 1992). In comparison to other Ixodes species the mean pre-ovipositionperiod of 14 days recorded for I. rubicundus at 2225C is long. The mean pre-oviposition periods recorded for Ixodes persulcatus (Fujimoto, 1992), Ixodes hex-agonus (Toutoungi et al., 1995) and Ixodes ricinus (MacLeod, 1935) were 5.8, 8.4and 10 days, respectively. A possible explanation for the longer than expected pre-oviposition period is perhaps the fact that I. rubicundus eggs undergo a devel-opmental diapause (Fourie and Horak, 1994). The delay in onset of oviposition maybe a reflection of reduced metabolic activity in engorged females. The developmentalzero or critical low temperature for the onset of oviposition in I. rubicundus is high(9.2C) compared to the 5.6 and 2.9C for Ixodes nipponensis and I. persulcatus,respectively (Fujimoto, 1992). A value of 8.2C for Ixodes ovatus, which occurs inmore moderate en...

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