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A review on the use of Ixodiphagus wasps (Hymenoptera: Encyrtidae) as natural enemies for the control of ticks (Acari: Ixodidae)
RENJIE HU^1, 2, K. E. HYLAND^2, & J. H. OLIVER^1, Jr.
1 Institute of Arthropodology and Parasitology, Georgia Southern
University, Statesboro, Georgia 30460, USA Accepted: 17 April 1998
Code Number:AA98003
Abstract
Ixodiphagus wasps (Hymenoptera: Encyrtidae) have been known as parasitoids of ticks since the beginning of the 20th Century. Currently, there are seven recognized species: Ixodiphagus texanus Howard, Ixodiphagus hookeri (Howard), Ixodiphagus mysorensis Mani, Ixodiphagus hirtus Nikolskaya, Ixodiphagus theilerae (Fielder), Ixodiphagus biroi Erdos, and Ixodiphagus sagarensis (Geevarghese). These wasps have been found parasitizing ticks belonging to the genera Ornithodoros, Amblyomma, Dermacentor, Hyalomma, Haemaphysalis, Ixodes, and Rhipicephalus. Parasitism by wasp parasitoids results in direct mortality of the tick hosts and appears to have potential for controlling them. This article reviews the taxonomy, life cycle, seasonality, host range and geographical distribution of these wasps, and their potential application to tick control.
Key words: Ixodiphagus, tick, wasp, parasitoid, natural enemy, biological control
Introduction
Ticks are obligate hematophagous ectoparasitic arthropods of significant medical and veterinary importance. Currently, there are more than 800 species described world-wide (Oliver 1989). During their life span, ticks have three post-embryonic active developmental stages, i. e. larva, nymph, and adult, and blood meals on vertebrate hosts are required for completion of their development. Due to their intimate association with humans and other animals, ticks are not only annoying pests but are well-known for their role in transmitting a number of disease-causing microorganisms of humans, wild, and domestic animals. In fact, ticks surpass all other groups of arthropods in the variety of pathogenic microorganisms which they transmit. This includes viruses, bacteria, rickettsiae, protozoa, and nematodes (Grist 1992; Hu & Hyland 1997a). Direct tick-host contact appears to be the major route for transmission of these pathogens and a reduction in the number of tick vectors would likely decrease the risk for acquiring tick-borne diseases. To this end, various ecological, chemical, and biological control methods have been evaluated for effectively reducing tick populations. Among these, biological control using predators, parasitoids, and pathogens of ticks would appear to be an ecologically and environmentally sound strategy. However, it has never been seriously considered in practice (Mwangi et al. 1991). In this article, we review the use of minute chalcid wasps as natural enemies for controlling ticks with focuses on the taxonomy, life cycle, host range and geographical distribution, seasonality, and application.
Taxonomy
Minute chalcid wasps (Order: Hymenoptera, Family: Encyrtidae) measuring about 2 mm in length are known to be parasitoids of ticks (Cooley 1927; Blagoveschensky 1947; Cole 1965; Davis 1986). Since the beginning of the 20th Century, seven confirmed wasp species known to parasitize ticks have been described: Ixodiphagus texanus by Howard (1907), Hunterellus hookeri by Howard (1908), Ixodiphagus mysorensis by Mani (1941), Ixodiphagus hirtus by Nikolskaya (1950), Hunterellus theilerae by Fielder (1953), Ixodiphagus biroi by Erdos (1956), and Hunterellus sagarensis by Geevarghese (1977). We spelled out both Ixodiphagus and Ixodes each time mentioned in this paper to avoid confusion. There were also other controversial reports on the taxonomy and classification of chalcid wasps. Du Buysson (1912) reported the discovery of a new species, Ixodiphagus caucurtei, in nymphal Ixodes ricinus (L.) collected in France. However, this species was later placed in synonymy with H. hookeri (Gahan, 1934). A Hunterellus sp. was found in engorged nymphal Amblyomma nuttalli Donitz from the Ivory Coast (Graf 1979). Even though this wasp appeared to be closely related to H. theilerae, it differed in certain morphological characters. It was then assumed to be a new species but with no taxonomic description available. Hunterellus sp. found in ticks collected in Queensland appeared morphologically similar to H. hookeri, however, the host range of the wasp was more similar to that of Ixodiphagus mysorensis (Doube & Heath 1975). Therefore, no confirmatory species identification was made. In 1947, Rao suggested that Ixodiphagus mysorensis was not a valid species but was a synonym of H. hookeri. However, this has not been resolved. Classification of wasp species has been mainly based on their morphological characters, especially the number of antennal segments and the number and location of ocelli (Gahan 1934). Trjapitzin (1985) suggested that Ixodiphagus is the only genus of wasp parasitoid of ticks, and that Hunterellus is therefore a synonym. This concept appears to have been widely accepted (Davis 1986; Mwangi et al. 1994; Stafford et al. 1996; Hu & Hyland 1997b). Therefore, all species noted in our paper will be assigned to Ixodiphagus as the currently accepted genus.
Life cycle
Among all Ixodiphagus spp.currently known, only Ixodiphagus hookeri and Ixodiphagus texanus have been successfully colonized under laboratory conditions (Wood 1911; Alfeev & Klimas 1938b; Bowman et al. 1979; Logan et al. 1985; Mwangi et al. 1994). Information on the biology of encyrtid wasps has gradually accumulated (Cole 1965; Davis 1986). They normally reproduce heterosexually and the female mates with the male immediately after emergence from the tick host. The fertilized female requires a live tick in which to oviposit and she normally deposits several eggs each time she inserts her ovipositor. Wood (1911) indicated that Ixodiphagus hookeri never oviposits more than twice in the same tick although some forms of polyembryony may exist. Wasp eggs develop only in the nymphal stage of ticks even though they can be deposited in engorged larvae (Wood 1911; Cooley & Kohls 1928; Alfeev & Klimas 1938a; Bowman et al. 1986; Hu 1990; Mwangi et al. 1994). Hu (1990) observed that embryonic development of Ixodiphagus hookeri begins only after the wasp-parasitized nymphal Ixodes scapularis Say attaches to an animal host. The larval stage of the wasp appears to consume the entire tissue contents of the engorged tick. Laboratory observations indicate that adult wasps emerge from ticks 30 to 57 days after the tick detaches from its host (Wood 1911, Geevarghese & Sreenivasan 1973; Davis & Campbell 1979; Hu 1990; Mwangi et al. 1994), resulting in mortality of the tick. Emergence of wasps from larval and adult ticks has never been reported. Solitary unmated Ixodiphagus texanus appear to be capable of thelytokous parthenogenetic reproduction when they are given access to engorged ticks and under certain conditions arrhenotokous parthenogenetic reproduction also occurs (Logan et al. 1985). Ixodiphagus wasps generally have a one-year life cycle (Larson & Green 1938, Hu & Hyland 1997b). However, laboratory experiments on the development of Ixodiphagus texanus and observations on the seasonal occurrence on wild-caught hosts indicate that this wasp has at least two generations per year in Nova Scotia (Davis & Campbell 1979).
Host range and geographical distribution
Ixodiphagus wasps are known to parasitize a wide range of ticks world-wide. Since being discovered from Ornithodoros sp. in India by Mani in 1941, Ixodiphagus mysorensis has also been found parasitizing other ixodid ticks. Parasitism by this wasp was detected in nymphal Ixodes tasmani Neumann collected from the ring-tailed possum (Pseudocheirus peregrinus laniginosus ) captured in Australia (Oliver 1964). Hoogstraal et al. (1968) found that one nymph of a Dermacentor auratus Supino-group tick fed on a Burmese ferret-badger (Melogale personata ) collected from Danang, Vietnam died from the infestation of 36 Ixodiphagus mysorensis . Ixodiphagus hirtus was only discovered in Russian Ixodes persulcatus Schulze (Nikolskaya 1950) and there is no further information on this species currently available. Ixodiphagus theilerae appears to be an African species. Since it was described as a parasitoid of nymphal Hyalomma truncatum Koch in Marienthal District, Southwest Africa (Fielder 1953), it has been found infesting another African tick, Hyalomma rufipes Koch on migrant birds in Egypt (Kaiser & Hoogstraal 1958; Hoogstraal & Kaiser 1961). Ixodiphagus sagarensis was also reported from nymphal Haemaphysalis spinigera Neumann, Haemaphysalis turturis Hoogstraal & Trapido, and Haemaphysalis kinneari Warburton in several areas in India (Geevarghese & Sreenivasan 1973; Kaul et al. 1978) besides in Haemaphysalis bispinosa Neumann. Geevarghese and Sreenivasan (1973) also indicated that this wasp did not oviposit on nymphal Boophilus microplus (Canestrini) which was a common tick species in the study area.
Ixodiphagus texanus and Ixodiphagus hookeri appear to have a wider host range and a broader geographical distribution than other encyrtid wasps. Since Howard (1907) first reported Ixodiphagus texanus in nymphal Haemaphysalis leporispalustris (Packard) feeding on a cotton tail rabbit in Jackson County, Texas, this wasp was also found parasitizing larval and nymphal H. leporispalustris that had fed on snowshoe hares (Lepus americanus ) from Minnesota (Larson 1937) and Nova Scotia (Davis & Campbell 1979). Ixodiphagus texanus was also recovered from H. leporispalustris collected in Oklahoma and subsequent laboratory colonization of the wasp was a success (Bowman 1979). In an attempt to select a suitable host for laboratory rearing of Ixodiphagus texanus, Bowman et al. (1986) reported that among unfed and engorged larval and nymphal Rhipicephalus sanguineus (Latreille), Dermacentor andersoni Stiles, Dermacentor variabilis (Say), Amblyomma maculatum Koch, and Amblyomma americanum (L.), all exposed to Ixodiphagus texanus, only R. sanguineus, D. variabilis, and D. andersoni were acceptable hosts. Furthermore, engorged larvae and unfed nymphs were best suited for wasp oviposition and development; engorged D. variabilis larvae appeared to be the most desirable species and stage for laboratory rearing of the wasp.
Since Howard (1908) described Ixodiphagus hookeri from nymphal R. sanguineus feeding on a dog in Corpus Christi, Texas, this wasp species has also been reported in engorged nymphal R. sanguineus collected in Loureco Marques, Portuguese East Africa, and Mexico (Wood 1911), in Rio de Janeiro, Brazil (da Costa Lima 1915), in India (Timerlake 1922), in Nigeria (Philip 1931), in Puerto Rico (Tate 1941), in Kenya (Philip 1954), in Uganda (Steyn 1955), in Indonesia (Munaf 1976), and in Malaysia (Cheong et al. 1978). In some areas, the percentage of ticks parasitized by wasps could exceed 90% (Philip 1931; Tate 1941).
Several studies of Ixodiphagus hookeri have also been conducted in the former Soviet Union. This wasp successfully survived the winter inside parasitized Ixodes ricinus nymphs (Alfeev & Klimas 1938a). Further extensive studies by the same authors (1938b) showed that Ixodiphagus hookeri imported from Montana, USA in nymphal D. andersoni appeared capable of parasitizing all the feeding stages of Ixodes ricinus in Russia, but only developed in the nymphs. The potential hosts used in their experiments were larval Ornithodoros sp., the flea Pulex irritans L., and nymphal Dermacentor marginatus (Sulzer). D. marginatus was the only suitable host. Subsequently, using nymphal Ixodes ricinus and D. marginatus, they established laboratory colonies. It was also reported that Ixodiphagus hookeri developed in nymphal Ixodes ricinus, Ixodes persulcatus, and Dermacentor pictus Herman [= Dermacentor reticulatus (Fabricius)] under natural conditions in the Province of Leningrad, Russia (Alfeev 1946). In additon, this wasp has been detected in nymphal Ixodes persulcatus, Ixodes crenilatus Koch, Haemaphysalis japonica Warburton, and Haemaphysalis concinna Koch in other areas of the former Soviet Union (Pervomalsky 1943 & 1947; Klyushkina 1958; Ushakova 1962).
Ixodiphagus hookeri was also found in Hyalomma aegyptium (L.) collected in the Transvaal, South Africa (Cooley 1930a). In the same study, it was also suggested that there was a wasp that attacks Amblyomma hebraeum Koch. However, a later study of this tick species collected from East London, South Africa did not reveal a wasp parasitoid (Rechav 1978). Doube and Heath (1975) indicated that larval and nymphal Haemaphysalis bancrofti Nuttall & Warburton and nymphal Haemaphysalis bremneri Roberts, Ixodes holocyclus Neumann and Ixodes tasmani engorged on the long-tailed short-nosed bandicoot (Isoodon macrourus ), the potoroo (Potorous tridactylus ), the eastern water rat (Hydromys chrysogaster ), and the brush-tailed possum (Trichosurus vulpecula ) collected in Queensland were parasitized by Ixodiphagus hookeri -like wasps. Ixodiphagus hookeri was also found in nymphal Ixodes ricinus collected in Czechoslovakia (Boucek & Cerny 1954). Other reports indicated the occurrence of Ixodiphagus hookeri in India (Timberlake 1922), Cuba, Indo-China (Cooley 1929), England, France, and Eastern Siberia (Larson 1937; Fielder 1953; Smith & Cole 1943; Cooley 1934a; Rao 1943). More recently, Mwangi et al. (1993) reported that Ixodiphagus hookeri parasitizes Amblyomma variegatum (Fabricius) collected in the Trans-Mara area, Kenya. Emergence of adult wasps was observed in approximately 49% of 140 nymphs collected from cattle. However, no Rhipicephalius appendiculatius Neumann (n= 650) nor Amblyomma cohaerens Donitz (n=31) collected in the same study were parasitized by the wasp.
In the United States, Ixodiphagus hookeri has been reported from widely scattered locations. In addition to parasitizing R. sanguineus in Texas (Howard 1908), the wasp was recovered from nymphal Dermacentor parumapertus Neumann feeding on a jackrabbit in Green Valley, California (Wood 1911). Cooley (1934b) reported in his studies of wasp parasitism in Colorado, Idaho, and Oregon that Ixodiphagus hookeri was found in nymphs of Ixodes cookei Parkard collected near Mayfield, Idaho. Additionally, Ixodiphagus hookeri has also been found in R. sanguineus in Florida, Montana, and South Carolina (Bishopp 1934; Gahan 1934). More recently, this wasp was found parasitizing Ixodes scapularis collected in Massachussetts, Rhode Island, New York, and Connecticut (Mather et al. 1987; Hu et al. 1993; Stafford et al. 1996; Hu & Hyland 1997b). These studies indicated that nearly one fourth of nymphal Ixodes scapularis collected by flagging at their study sites in the 1980s and 1990s contained eggs of Ixodiphagus hookeri . Mather et al. (1987) also reported that the prevalence of either Borrelia burgdorferi Johnson, Schmid, Hyde, Steigerwalt and Brenner (Lyme disease-causing spirochete) or Babesia microti Franca (human babesiosis-causing protozoan) in the host-seeking nymphs collected on Naushon Island was nearly 40% lower than that found in other sites where levels of wasp parasitism was either lower or absent. They suggested that wasp parasitism may render the tick inhospitable to both pathogens.
Seasonality
Seasonal activities of these wasps have been poorly understood and information on the subject is only available for Ixodiphagus texanus and Ixodiphagus hookeri. In Montana, Ixodiphagus hookeri tends to emerge from its tick host during late August and early September (Cooley & Kohls 1934). However, Ixodiphagus texanus was detected in H. leporispalustris feeding on hares in Minnesota nearly every month from April to October in 1935 with higher rates of wasp infestation recorded in May and June (Larson & Green 1938). Davis and Campbell (1979) conducted a similar field study from May through August, 1977 and 1978 in Nova Scotia. They also found higher numbers of Ixodiphagus texanus -parasitized nymphal H. leporispalustris feeding on hares in May. Moreover, they did not find either larvae or adults parasitized by the wasp. Logan et al. (1985) reported that Ixodiphagus texanus successfully overwintered under field conditions in parasitized engorged larvae and unfed nymphal D. variabilis in Oklahoma, while engorged nymphs were not suitable hosts for wasp overwintering. Alfeev and Klimas (1938a) reported that Ixodiphagus hookeri successfully survived the relatively harsh winter climate in the former Soviet Union inside Ixodes ricinus nymphs. Hu and Hyland (1997b) conducted a detailed study to elucidate the seasonality of Ixodiphagus hookeri in Rhode Island. In both 1988 and 1989, the prevalence of Ixodiphagus hookeri eggs in nymphal Ixodes scapularis collected on Prudence Island, Rhode Island reached its peak in May, approximately one month ahead of the peak for nymphal activity, then declined abruptly in June, July, and August. This suggested that the wasp overwinters as non-embryonated eggs inside the nymphs.
Application in tick control
Successful rearing of Ixodiphagus hookeri under laboratory conditions led to several attempted mass releases of this parasitoid for tick control in the late 1920s and early 1930s in the U. S. During the summer of 1926, Ixodiphagus hookeri wasps obtained from the forest of Fontainbleau, France were brought to the United States in parasitized nymphal D. reticulatus and R. sanguineus, and released onto Naushon Island, MA in an attempt to control the American dog tick, D. variabilis (Larrousse et al. 1928). This tick control effort apparently failed and both D. variabilis and Ixodes scapularis remained abundant on the island. However, the introduction of the parasitoid appeared to be successful and wasp eggs were found in field-collected nymphal D. variabilis and Ixodes scapularis. Adult stages of this wasp were also found on Naushon Island 12 years later (Cobb 1942), suggesting that the wasp had survived New England winters under natural conditions and had propagated itself. In 1937, 1938, and 1939, a total of 90,000 females of Ixodiphagus hookeri were released on nearby Martha's Vineyard, MA in an attempt to control D. variabilis (Smith & Cole 1943). This study indicated that neither wasp species was discovered in ticks collected in the areas from 1937 to 1942, nor was there a reduction in tick abundance attributable to the parasitoids. Wasps were also used for attempts in controlling ticks in the western United States. Beginning in 1927, approximately 4,158,600 Ixodiphagus hookeri wasps had been released in nature in Montana, and in 1932 in Colorado, Idaho and Oregon in attempts to control D. andersoni, the vector for the Rocky Mountain spotted fever in these areas (Cooley & Kohls 1934). Attempts to recover wasp parasitoids in these study sites were made each year until 1933 and results indicated that only at one site in Montana did a few adult wasps emerge from nymphs taken from Columbian ground squirrels (Spermophilus columbianus).
Similar field studies were also carried out in the former Soviet Union in the 1940s. Alfeev (1946) reported that in an effort to control Ixodes ricinus and Ixodes persulcatus in the Province of Leningrad, Russia, nearly 2,600 adult Ixodiphagus hookeri of both sexes were released together with 38,000 parasitized larval and nymphal Ixodes ricinus in an area of about 250 acres. Later, no parasitoids were discovered among 8,000 larval and nymphal Ixodes ricinus collected. It was assumed that the extremely cold weather probably caused the failure of the wasps' survival. Apparently, all of these earlier attempts were unsuccessful in noticeably reducing tick populations. This could be because of inadequate numbers of parasitoids released compared to the greater geographical areas covered by the releases and/or unsuitable hosts for these parasitoids. On the other hand, Ixodiphagus hookeri has been found in Ixodes scapularis only in areas where the population of this tick is extremely high, indicating that perhaps the establishment of a wasp population requires a certain threshold tick density (Hu et al. 1993; Hu & Hyland 1997b). In the 5 decades since the early attempts to control ticks by using encyrtid wasps little interest has been shown in using parasitoids for this purpose. However, in a recent report, Mwangi et al. (1997) indicated that in Kenya, by releasing Ixodiphagus hookeri on cattle over a period of one year, 51% of nymphal A. variegatum were found parasitized by the wasp and that tick numbers were reduced from 44 to 2 per animal. Their findings provided new insight into how this wasp species could be used strategically for tick control. Summary
Ixodiphagus wasps have been known as parasitoids of a number of ticks and are distributed world-wide. Parasitism by these wasps causes direct mortality of their tick hosts and may have potential as natural enemies for the control of ticks. Although many earlier attempts to use these wasps for tick control were unsuccessful, resulting in little interest being shown to seriously consider this strategy in tick control during the past several decades, it may still have a use in integrated tick control program. Information, especially on suitable host target and strategic release of these wasps, is urgently needed.
Acknowledgments
We thank L. A. Durden for his constructive comments and suggestions on an earlier draft. The senior author (R. H.) was supported in part by U. S. National Institutes of Health grant R 37AI-24899 (to J. H. O.) during the preparation of this review. References
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