FORUM Feasibility of Controlling Ixodes scapularis (Acari: Ixodidae), the Vector of Lyme Disease, by Parasitoid Augmentation

E. F. KNIPLING1 AND C. D. STEELMAN2

J. Med. Entomol. 37(5): 645Ð652 (2000)

ABSTRACT A theoretical analysis of the feasibility of controlling populations (Ixodidae) by Downloaded from https://academic.oup.com/jme/article/37/5/645/954424 by guest on 25 September 2021 the release of reared Ixodiphagus parasitoids in tick ecosystems yielded promising results. The analysis suggested that if reasonable progress could be made in mass-rearing the parasitoids, it would be possible to control the blacklegged tick, Ixodes scapularis (Say), the vector of Lyme disease, by this biological control procedure. Lyme disease has become the most important vector-borne disease in the United States. In a Þeld-release experiment conducted in Africa by members of the Inter- national Center for Physiology and Ecology, effective control of Amblyomma variegatum (F.) was obtained by the release of Ixodiphagus parasitoids in tick habitats. Encouraging theoretical results along with the encouraging results of a Þeld-release experiment indicate the need for civil and political leaders in countries where ticks are a major problem to sponsor strong and well- coordinated research initiatives focused on the development of this new method of dealing with tick problems.

KEY WORDS Ixodiphagus hookeri, Ixodes scapularis, Amblyomma variegatum, acaracide, parasitoid augmentation

TICKS ARE AMONG the most important pests that affect high rates of parasitism, but parasitoid populations the welfare of humanity. Disease causing organisms seldom provide adequate control of their hosts. transmitted to humans and livestock are a major ob- A comprehensive study of the role that parasitoids stacle to sound agricultural economies in many parts can play in controlling insect pests (Knipling 1992) of the world. In the United States, society is primarily indicated that if insect parasitoids were to play a prom- concerned with the role that ticks play in the trans- inent role in controlling pests it would be necessary to mission of diseases to humans. For the most part, this augment the number of parasitoids in pest host eco- concern involves the blacklegged tick, Ixodes scapu- systems by artiÞcial means. Nature imposes stringent laris (Say), which is the vector of Lyme disease (Den- limits on the rate of parasitism that natural populations nis 1995). This disease has emerged as a major health can cause. Therefore, if parasitoids were to play a problem in areas where high numbers of deer (Odoco- prominent role in managing ticks, the number of para- lieus virginianus Zimmerman) have developed (Ost- sitoids in the natural population must be augmented feld, 1997). Deer are the primary host for adult I. by artiÞcial means. The only feasible way to increase scapularis. the number of parasitoids in natural environments Acaracides have long been the chief method of would be to mass produce key species and release the controlling ticks in various parts of the world. Al- numbers required in the pest habitats. Currently, we though they play an important role in this regard, ticks have little information relative to the number of para- still cause billions of dollars in losses to agriculture sitoids required to achieve adequate control. There- production year after year. Like , ticks have fore, deductive procedures designed to estimate how developed resistance to chemical control agents. many parasitoids would have to coexist with their pest Acaracides are costly to use and they can also cause hosts to achieve adequate control were initiated. Such hazards to people and the environment. Therefore, estimates have been made for a wide range of insect there is continuing interest in the development of pest parasitoids previously discussed by Knipling more acceptable ways to cope with tick problems. This (1992). has included the possibility of controlling ticks by the This article presents the potential role that tick use of tick parasitoids. Ticks serve as hosts for a num- parasitoids can play directly in the management of ber of hymenopterous parasitoid species that belong ticks and indirectly in lowering the incidence of the to the family . The parasitoids cause fairly disease-causing organisms that they transmit. Specif- ically, the potential role of Ixodiphagus parasitoids for the control of Ixodes scapularis (Say), the primary vector of Lyme disease, is examined. However, the 1 Deceased. Former Director, Entomology Division, USDA-ARS, Beltsville, MD. fundamental principles apply for all ticks, including 2 Department of Entomology, Room 320, Agriculture Building, Uni- species that are major obstacles to livestock produc- versity of Arkansas, Fayetteville, AR 72701. tion in various parts of the world.

0022-2585/00/0645Ð0652$02.00/0 ᭧ 2000 Entomological Society of America 646 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 37, no. 5

Tick Parasitoids. Two species of tick parasitoids are behavior is important in the development of proce- known to exist in the United States. They are Ixo- dures for mass-rearing the parasitoids. diphagus (Hunterellus) hookeri, Howard (1907) and I. Ixodiphagus parasitoids are basically effective para- texanus, Howard (1908). A number of other closely sitoids and the natural rates of parasitism are quite related species exist in other parts of the world (Cole high. Data obtained by Mather et al. (1987), Hu et al. 1965). The biology and behavior of the two known (1993), and Stafford et al. (1996) indicated that max- species in the United States have been studied by a imum rates of parasitism of I. scapularis nymphs may number of investigators (Wood 1911, Cooley and exceed 40%. However, the average is probably closer Kohls 1928, Smith and Cole 1943, Bowman et al. 1986, to 25%, as observed by Lyon et al. (1998). In other Mwangi et al. 1993). areas and in other species, natural rates of parasitism Engorged tick larvae seem to be the preferred tick Ͼ50% have been observed in A. variegatum (F.) in stage parasitized by the parasitoids. However, as ob- Africa by Mwangi et al. (1993) and in Hyalomma- served by Cooley and Kohls (1928), the parasitoid anatolicum anatolicum (Koch) in India as recorded by Downloaded from https://academic.oup.com/jme/article/37/5/645/954424 by guest on 25 September 2021 eggs pass into the nymphs during the molting process Shastri (1984). Although these are rather high rates of and then complete their development in engorged natural parasitism, they are not high enough to achieve nymphs on the host. The immature parasitoids com- adequate tick control. plete their development in Ϸ45 d (Wood 1911). Most efforts made to control ticks by the use of The host-searching behavior of the parasitoids is not parasitoids have involved classical biological control clear. Whether the parasitoids actively search for the (Cooley and Kohls 1933, Smith and Cole 1943). But for hosts or wait for the hosts to come to the parasitoid is the most part these efforts have not been successful. not known. It is also not clear if the tick larvae or The feasibility of controlling ticks by releasing large nymphs are parasitized on or off the hosts. Some ob- numbers of parasitoids in tick habitats has received servers report that the parasitoids have been seen little consideration by researchers. However, Mwangi searching for hosts on . In the laboratory, how- et al. (1997) undertook a small augmentation exper- ever, many investigators have observed that the para- iment in Africa that yielded encouraging results. The sitoids will readily parasitize engorged larvae or un- results of that important experiment will be discussed engorged nymphs while off the hosts. in more detail later. Lyon et al. (1998) questioned whether the parasi- Estimating the Host-Finding Capability of Parasi- toids normally parasitize the larvae and nymphs when toids. To analyze the feasibility of controlling a pest by on the host. We raise the same question on theoretical the augmentation procedure it is important to know grounds. It is possible that most host searching by the how many hosts a female parasitoid normally parasit- parasitoids is for engorged larvae and unengorged izes during her lifetime. If that is known, it is possible nymphs while they are off the host. The adult para- by extrapolation to estimate the number and propor- sitoids are reported to be weak ßiers. They may be tion of coexisting host populations that can be para- incapable of readily getting on large hosts such as deer sitized by a given number of parasitoids. However, and cattle. In the investigations conducted by Shastri there is no data found relative to the host-Þnding (1984) and Mwangi et al. (1997) the implications are ability of any parasitoid species. Therefore, indirect that engorging nymphs are parasitized while on the procedures have been used to estimate the host Þnd- cattle. This, however, would be inconsistent with the ing of a wide range of parasitoid species (Knipling known parasitism behavior involving the larval and 1992). The assumption was made that a parasitoid unengorged nymphal stages. Thus, important ques- coexisted with its host when the two populations were tions remain about the behavior of tick parasitoids that stable. Thus, the female parasitoids under such con- could inßuence the way the parasitoids should be used ditions would, on average, produce one adult female for maximum effectiveness. progeny. A state of stability is a universal biological The behavior of tick parasitoids differs in several phenomenon for all populations. To estimate respects from the behavior of parasitoids of insects. the host-Þnding ability of the tick parasitoids, a life Most parasitoids have solitary parasitism behavior and table was developed (Table 1). The fecundity of Ixo- will deposit only one egg or larvae in a host, and only diphagus parasitoids is not well known; however, in- one parasitoid can normally mature in a host. In con- formation on I. hookeri indicates that the females de- trast, Ixodiphagus parasitoids deposit a number of eggs posit Ϸ100 eggs (Esther M. Mwangi, International in a host. Observations by Hu et al. (1993), Mather et Center for Insect Physiology and Ecology, Kenya, per- al. (1987), and Stafford et al. (1996) indicate that the sonal communication). Data obtained by Bowman et female parasitoids deposit 6Ð8 eggs in each I. scapu- al. (1986) indicate that I. texanus (Howard) females laris host. Observations made by Bowman et al. deposited Ϸ200 eggs. Information published by Shastri (1986), Shastri (1984), and Mwangi et al. (1994) in- (1984) indicated that females of the species of Ixo- dicate that more eggs were deposited in larger tick dipagus had the capability to depositing Ͼ100 eggs. species. Ixodiphagus parasitoids also readily super- Here we assume that female I. hookeri on average have parasitize hosts that have already been parasitized, the capability of producing 120 adult progeny. The sex and a large number of parasitoid progeny can develop ratio of Ixodiphagus parasitoids is normally 1:4 (male: in one host. In rearing investigations conducted by female). Therefore, when a population is stable the Bowman et al. (1986) they obtained a range of 40Ð50 females on average will produce only l.25 adults, 80% adult parasitoids from a single parasitized nymph. This of which are female. September 2000 KNIPLING:TICK MANAGEMENT BY PARASITOID AUGMENTATION 647

Table 1. Estimated fate of the life stages of an Ixodiphagus parasitoid and I. scapularis tick populations when the two populations coexist in a state of stability

I. parasitoid I. scapularis Adult females 1 Engorged females 1 Potential progeny, (fecundity) 120 Potential progeny 2,500 (fecundity) Adult survival, % 50 Adult survival, % 50 Parasitoid eggs deposited 60 Eggs deposited 1,250 Hosts parasitized per female 10 Eggs survival, % 50 Parasitoid eggs per parasitized 6 Unengorged larvae 650 host Immature parasitoids survival to 2 Unengored larva survival to 12 adults, % engorgement, % Adult parasitoid progeny, both 1.25 Engorged larvae 78 Downloaded from https://academic.oup.com/jme/article/37/5/645/954424 by guest on 25 September 2021 sexes Female parasitoids, % 80 Engorged larva survival to 16 engorged nymphs, % Female parasitoid progeny 1 Engorged nymphs, number 12.5 Accumulated mortality % 98.96 Engorged nymphs survival to 16 engorged adults, % Engorged adults, number 2 Engorged females 1 Accumulated mortality 99.92

The model shows the assumed fate of the different parasitoid populations. This in brief explains the the- life stages. Allowing for natural mortality the females ory of pest control by parasitoid augmentation. It is the are estimated to deposit 60 eggs. The observation that hypothesis that will be examined critically in the sec- each parasitized host normally has approximately six tions to follow. immature parasitoids becomes an important parame- How Tick Parasitoids and Ticks Coexist in Natural ter. It suggests that the female parasitoids in a stable Populations. To estimate the role that parasitoids can population will parasitize Ϸ10 tick hosts. play in controlling their hosts it is necessary to have Using the procedure described, with suitable mod- some indication of the relative number of parasitoids iÞcations, estimates have been made of the host-Þnd- and hosts that coexist in typical natural populations ing capability of Ͼ25 different parasitoid species. No and the rates of parasitism that will result from dif- doubt some of the estimates will be in error by a ferent parasitoid to host ratios. However, no data are considerable margin; however, we question if more available on these key parameters. Therefore, esti- accurate estimates could be made by the most sophis- mates must be made by indirect procedures. Table 2 ticated procedure that could be designed for actual shows the estimates made of the way that I. scapularis measurements in natural populations. and I. hookeri normally coexist in typical natural pop- General Discussion. According to the hypothetical ulations. In the case of I. scapularis, researchers have life table, the parasitoid in a stable population has an obtained information on the number of the different accumulative mortality of 98.96%. Yet it would repro- tick stages that exist in natural populations. But infor- duce successfully. The mortality experienced by the mation is completely lacking on the number of para- tick host is much higher. The estimate that engorged sitoids that coexist with the ticks and the rate of par- I. scapularis females on average can produce 2,500 asitism that will result from different parasitoid to host progeny is based on information obtained by Mount et ratios. These estimates must be made by deductive al. (1997a). Therefore, if an engorged female tick is procedures. expected to produce only two adult progeny, the ac- We have made a good start by estimating that fe- cumulated mortality would have to be Ϸ99.92%. Even male Ixodiphagus parasitoids must on average parasit- if the tick progeny were increasing at a twofold rate ize Ϸ10 host larvae or nymphs during their lifetime. per cycle, a probable normal maximum rate of increase This together with the knowledge that the parasitoids for ticks, the accumulated mortality would still be normally deposit approximately six eggs in the hosts 99.84%. are two important parameter values for estimating The procedure used to estimate the efÞciency of how the parasitoid and I. scapularis coexist in natural insect parasitoids in natural populations is of vital populations. importance. The only reason why parasitoids do not Another key parameter value is the number of hosts parasitize a higher proportion of their host popula- that normally occur in natural populations. Fortu- tions is that evolutionary processes have evolved to nately, a number of investigators have made estimates maintain the relative numbers of parasitoids and hosts of I. scapularis densities in natural populations includ- within safe limits for the survival of both organisms. ing Ostfeld (1996), Stafford et al. (1998), Mather et al. This is fundamental to natural parasitism processes. (1987), Lyon et al. (1996) and others. Mount et al. Through modern technology it is possible, however, to (1997a, 1997b) have reviewed much of the research on overcome that barrier by drastically altering the rel- the abundance of I. scapularis. We analyzed the de- ative number of parasitoids and hosts in favor of the tailed tick model (LYMESN) developed by Mount et 648 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 37, no. 5

Table 2. Estimated coexistence pattern of the I. hookeri parasitoid and I. scapularis tick population, coexisting in a stable natural population

Parameters, 1 km2 Period 15 JulyÐ15 Sept. Engorged tick larva 1,000,000 Normal rate of parasitism, % 25 No. of larva parasitized 250,000 Larva parasitized per female parasitoid 10 Female parasitoids coexisting with the tick population 25,000 Immature parasitoids per parasitized larva 6 Total immature parasitoids 1,500,000 % survival of immature parasitoids to adults 2.1 Adult parasitoids, next period 31,500 % female parasitoids 80 Downloaded from https://academic.oup.com/jme/article/37/5/645/954424 by guest on 25 September 2021 Female parasitoids next period 25,200 al. (1997a) efforts to decide what tick density to as- made for any desired release rate, but to ensure a high sume for this study. and decided that 1,000,000 en- rate of parasitism it was assumed that 300,000 female gorged larvae per square kilometer would be repre- parasitoids per square kilometer would be released sentative of a typical population in areas where the during the Þrst year. This would be 12 times the num- tick densities are high and Lyme disease is prevalent. ber of parasitoids estimated to cause 25% parasitism of Most of the engorged larvae were assumed to be the tick larvae and nymphs. present during 15 JulyÐ15 September in the northeast Because of the prolonged development time for the region. This would be in agreement with the infor- different tick life stages plus the overwintering period, mation that Mount et al. (1997a) developed. Some it would be difÞcult to estimate how soon the tick engorged larvae would be present before and after population would respond to the parasitoid releases. these dates but the numbers are small and are ignored So no effort was made to develop a model to indicate in this analysis. when and to what degree the population would de- Perhaps the most important parameter value in es- cline. However, the release of that number of parasi- timating the efÞciency of the parasitoids by the mod- toids would in theory cause 95% parasitism of the tick eling procedure used is the number of parasitoids that larvae and the nymphs and parasitized progeny would normally coexist with a typical host population. If the average rate of parasitism is 25%, which would be in be produced for several years. This in due time would agreement with the information obtained by Lyon et cause a sharp decline in all tick stages. There would be al. (1998), Ϸ25,000 female parasitoids will coexist with no inßuence observed on the number of ticks during 1,000,000 engorged tick larvae. year 1. Some reduction in the larvae and nymphs If a given number of hosts parasitized by a given might occur during year 2, but the reduction probably number of parasitoids was known, we could, by ex- would not be large. The full impact of the parasitoid trapolation, estimate the number parasitized by in- releases would not occur until year three and there- creasing the parasitoid population. after. Because of the long life of tick larvae and Influence of Parasitoid Releases. By indirect proce- nymphs in which the parasitoids live, a large number dures values for all of the parameters needed to esti- of parasitoid progeny would be expected to develop mate the inßuence of parasitoid releases on the rates for several years. In theory, enough parasitoid progeny of parasitism were established. The model devised for should develop to achieve on the order of 95% para- this estimate is shown in Table 3. Calculations could be sitism for several successive years.

Table 3. Estimated influence of I. hookeri releases on the rate of parasitism of I. scapularis larvae and nymphs in a natural population

Parameters, 1 km2 Period 15 JulyÐ15 Sept. Engorged tick larva 1,000,000 Female parasitoids released 300,000 Larva parasitized per female 10 Total larvae parasitized 3,000,000 Ratio, larvae parasitized to larvae presenta 3:1 Percent larval parasitism 95 Immature parasitoids per parasitized larvae 6 Total immature parasitoids 18,000,000 Percent survival of immature parasitoids to adults 2.1 Adult parasitoids next period, both sexes 378,000 Percent female parasitoids 80 Female parasitoids next period 302,400

a Formula for estimating the proportion of a pest population that will be parasitized depending on the ratio of hosts parasitized to hosts present is discussed by Knipling (1992). September 2000 KNIPLING:TICK MANAGEMENT BY PARASITOID AUGMENTATION 649

It would be mere speculation to estimate what The eventual cost of rearing the parasitoids in large would happen after year 4, if no additional parasitoids numbers will no doubt be the most important factor were released. But, if we make a conservative estimate that determines the feasibility of managing tick pop- that the tick population would be suppressed by 90% ulations by the parasitoid release technique. It should by year 4, it would require only Ϸ30,000 parasitoids be possible through research to develop procedures per square kilometers to achieve a parasitoid to host for rearing the parasitoids in large numbers at low cost. ratio that would again result in near 95% parasitism. This assumption was based on the investigations of And so long as a signiÞcant number of hosts were Bowman et al. (1986) who showed that up to 40Ð50 present we could also expect a signiÞcant number of parasitoids could be produced on one engorged parasitoid progeny to develop from such high rates of nymph. For this appraisal we assume that the parasi- parasitism. These are fundamental principles of pest toids could be reared at a cost of $1 per 1,000, if the nymphs were fed on host animals. Eventually, how-

parasitism that are unique to parasitism processes. Downloaded from https://academic.oup.com/jme/article/37/5/645/954424 by guest on 25 September 2021 It is apparent that a number of questions can be ever, it might be possible to rear the parasitoids on tick raised that might cast doubt on the validity of the larvae or nymphs that are engorged by membrane theoretical results that have been projected. We can feeding. If this could be done, it might be possible to be certain of one thing, however, no tick species dur- reduce the rearing costs well below the current esti- ing its long history has ever experienced the grossly mate as well as avoid some of operational and social distorted parasitoid-to-host ratio that would result if a problems created by maintaining large numbers of parasitoid population were increased by 10- to 12-fold animals on which to rear the ticks and the parasitoids. throughout its tick ecosystem. Natural constraints Another important variable is the number of deer in would not permit anywhere near such distorted ratios the natural population. This will largely determine the to occur naturally so no clues are available after ob- number of ticks that exist in these natural populations. serving natural populations. And, because no effort In many areas, deer populations have been permitted has ever been made to achieve such a distorted ratio to exist at abnormally high levels. However, deer man- by artiÞcial means, we can only speculate on what the agement procedures are being followed by wildlife impact would be. But we do know that we are dealing management agencies resulting in a reduction in the with a tenacious and resourceful organism that has size of deer herds and a corresponding decrease in the tick numbers. survived for many thousands of years on a variety of Thus, there are a number of factors and variables tick species and no doubt under various conditions. that would inßuence the feasibility of using parasitoids Two factors can account for the drastic effect that to manage tick populations and what the ultimate cost would be produced. One is the ability of the parasi- would be. But through research the chances seem toids to produce progeny at the expense of the tick. excellent that satisfactory tick control could be The other is the ability of the individual parasitoids to achieved at a low cost by the proposed biological Þnd and parasitize a certain number of hosts, even control procedure. though the host population may exist at a low level. No Current Tick Control Options and Probable Costs. other method of tick control has such suppressive People can protect themselves to some degree from actions. Although a high degree of conÞdence in the tick attacks by the use of repellents and protective theoretical results exists, it is recognized that the only clothing or by avoiding habitats where they might be way to determine for certainty what the results will be at risk of tick infestations. Immunization vaccines have is to test the technique on an area-wide basis in natural also been developed that will protect humans from populations Lyme disease. Although helpful, these procedures are Influence of Variables. A number of variables can not satisfactory because people often do not know if, inßuence the feasibility and efÞciency of tick control where, and when they will be subject to tick infesta- by parasitoid augmentation. Most of these variables tion. Rigid area-wide management of the ticks by the would be of little importance if the tick population parasitoid augmentation technique would make such were controlled by the use of acaracides. protective measures unnecessary. The assumed larval tick population is based on the Mount et al. (1997b) discussed in some detail the premise that the population is representative of the various options for controlling the blacklegged tick, average in high tick density habitats. It is probable, the primary vector of Lyme disease. The methods of however, that the average population density in large control discussed included the use of acaricides in areas would be lower than is assumed. If the average several ways, habitat modiÞcations, and the manage- tick population were only half that assumed, the para- ment of deer populations. One of the most promising sitoids required to achieve the rate of parasitism es- ways to control ticks involves the ingenious self-treat- timated could be reduced by about half. ment of deer with acaracides that has been developed The estimated rate of parasitism achieved would be by Pound et al. (1994, 1996). Mount et al. (1997b) Ϸ95%. It is probable, however, that parasitism as low estimated that the cost of tick control by the self- as 80% for 2Ð3 yr would reduce the tick population to treatment procedure would be about $9 per hectare a level that would provide satisfactory control of Lyme per year. disease. Only about half as many parasitoids would be This investigation indicated that the release of required to achieve 80% parasitism as is required to 300,000 parasitoids per square kilometer could achieve achieve 95%. a high degree of tick control. If the parasitoids could 650 JOURNAL OF MEDICAL ENTOMOLOGY Vol. 37, no. 5 eventually be reared in large numbers at a cost as low begin to decrease until Ϸ6Ð7 mo after the parasitoid as $1 per 1,000, the cost for the tick control would be releases began. It then gradually declined to Ϸ5% of only about $3 per hectare during the Þrst year. How- the original level. This lag in the decline of the adult ever, it is emphasized that this would be the initial cost. tick population could be attributed to the long life of The ability of the parasitoids to produce progeny at the adult ticks that had accumulated in the environ- the expense of the tick hosts introduces a suppression ment before the parasitoid releases began. The tick factor of great practical signiÞcance. In theory, population on an untreated control herd was some- enough parasitoid progeny would be produced to what variable, but in general it remained at a high achieve a high degree of tick control for at least 3 yr. level. Therefore, the average cost per year would be much However, the type of suppressive action that re- less than $3 per hectare. Once a tick population is sulted in good control is not clear. The marked de- reduced to a low level it should not require many crease in the nymph population on the experimental parasitoids to maintain that population at a low level. animals within 3Ð4 mo could not be attributed to the Downloaded from https://academic.oup.com/jme/article/37/5/645/954424 by guest on 25 September 2021 The lower the tick population the fewer the number direct action of the parasitoids on the nymphs while on of parasitoids needed to maintain low populations. the host animals because the adult tick population did The cost of tick control by the use of acaracides re- not decline during the Þrst 6Ð7 mo. Also, the rate of mains about the same whether the tick populations are parasitism of the engorged nymphs, which averaged high or low. only 51%, would have had little immediate inßuence The Economics of Tick Control Viewed in Perspec- on the adult tick population. Therefore, the marked tive. As a pest complex, ticks are responsible for large decline in the nymph population on the experimental losses to agriculture because of the disease organisms animals had to be the result of parasitoid action against that they transmit to cattle and other livestock. In the engorged tick larvae or the unengorged nymphs areas where ticks and the pathogens they transmit are that existed in the experimental area. prevalent they are a major obstacle to a highly pro- For a normal host, the parasitoid does not kill the ductive animal agriculture. This is especially true in engorged larvae or the unengorged nymphs. The para- some developing nations where effective tick man- sitoid eggs deposited in the larvae pass into the nymph agement at low cost would make a major contribution stage and the immature parasitoids then complete to the welfare of many people. their development in the feeding nymphs after they This estimate of the feasibility of managing I. scapu- Þnd a host. This process might require several months. laris by the parasitoid augmentation technique was To expect a 95% decline of the adult tick populations, based entirely on theoretical appraisals. Therefore, it the rates of parasitism of the nymphs on the cattle is necessary to conÞrm this theory. There are reasons should have been as high as 95% or more. Thus, the to believe, however, that the theoretical results reßect only way to account for the 95% decrease in the en- what can be achieved in practice. They are similar to gorged nymph and adult tick populations on the ex- results obtained in appraisals of the feasibility of man- perimental animals was that Ϸ95% of the engorged aging a wide range of insect pests by the use of para- larvae and unengorged nymphs present in the exper- sitoids as described by Knipling (1992). imental area were killed by the parasitoids before the Perhaps of equal importance, the theoretical results nymphs got on the cattle. It should be noted that the obtained against the blacklegged tick are in close estimate of 95% parasitism of the larvae and unen- agreement with the results obtained in a Þeld release gorged nymphs achieved in the Þeld release experi- experiment conducted by Mwangi et al. (1997) in ment would be consistent with the calculated 95% Africa against Amblyomma variegatum (F). Their ex- parasitism in the model developed for I. scapularis. periment is the only effort that has been reported that Based on the observations by Bowman et al. (1986), has tested the feasibility of controlling tick popula- parasitoids did not survive in the larvae and nymphs of tions by the parasitoid release technique. In their some tick species. In the experiment conducted by experiment 150,000 I. hookeri reared in the laboratory Mwangi et al. (1997) the parasitoids had no effect on were released during a 1-yr period for the control of Rhipicephalus appendiculatus (Newmann) ticks on the ticks on 10 head of cattle in a 4-ha pasture. Tick experimental animals. This tick species, therefore, is numbers were compared with animals having tick probably not a suitable host for the parasitoid used in parasitoids and those not having ticks subjected to I. their experiment. hookeri. Whereas much is unknown about tick parasitoids, The nymph and adult tick populations on the host they are highly specialized organisms that have existed animals were monitored at monthly intervals during with their hosts from cycle to cycle for many years and the parasitoid release period and for Ͼ1 yr after the no doubt under a wide range of conditions. Both in parasitoid releases were discontinued. Although this theory and practice the evidence is strong that re- was a rather small experiment and the parasitoid re- leased parasitoids could achieve effective control of lease rate was high, the results were favorable. The tick populations. engorged nymphs found on the experimental animals A Strong Research Initiative Needed. Ample evi- declined by Ϸ95% within 4 mo after the parasitoid dence has been presented to support the hypothesis releases began. The nymph population remained at that effective tick control can be achieved by using the that low level for Ͼ1 yr after the parasitoid releases parasitoid augmentation technique if it is used on an were discontinued. The adult tick population did not area-wide basis. It is evident, however, that the fea- September 2000 KNIPLING:TICK MANAGEMENT BY PARASITOID AUGMENTATION 651 sibility of doing this will depend entirely on the avail- Acknowledgments ability of technology and facilities for producing the Dr. Knipling expressed special thanks to his colleagues parasitoids in large numbers and at acceptable costs. with the U.S. Department of Agriculture including Karl It is also necessary to provide the resources required Narang, J. F. Carroll, J. E. George, and G. A. Mount. We also by scientists who will have to demonstrate that the thank Esther Mwangi (International Center of Insect Phys- parasitoids will perform as anticipated for each tick iology and Ecology, Nirobi, Kenya) for her helpful informa- species. This will require Þeld experiments, conducted tion. Special thanks are also due for J. P. Piesman (U.S. Public in habitats at least as large as the normal dispersal Health Service), K. C. Stafford (Connecticut Agricultural Experimental Station), and R. S. Ostfeld (Institute of Eco- range of the host animals. Considering that such ex- system Studies, NY). Dr. Knipling and I express also special periments must be conducted on a wide range of tick thanks to his daughter, Edwina K. Lake, who assisted us in a species and at different tick densities and parasitoid number of ways in conducting this investigation and prepar- release rates, it becomes apparent that considerable ing the manuscript. Published with the approval of the Di- Downloaded from https://academic.oup.com/jme/article/37/5/645/954424 by guest on 25 September 2021 funds will be needed to investigate and exploit the rector, Arkansas Agricultureal Experiment Station, manu- feasibility of managing ticks by the parasitoid augmen- script no. 00053. tation technique. It is probable that a number of parasitoid species or References Cited strains have evolved that are adapted for certain tick species. This requires research on the , bi- Bowman, J. L., T. M. Logan, and J. A. Hair. 1986. Host ology, and behavior of a number of parasitoid species suitability of Ixodiphagus texanus Howard on Þve species and certain information on the biology and behavior of hard ticks. J. Agric. Entomol. 3: 1Ð9. Cole, M. M. 1965. Biological control of ticks by the use of of ticks will be needed that has not been considered hymnopterous parasites. A review. WHO EBL 43: 65. important when they are to be controlled by acracides Cooley, R. 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