Ixodiphagus hookeri

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Ixodiphagus hookeri
Ixodiphagus-hookeri-Howard-hatched-from-an-Ixodes-ricinus-nymph-Photo-Oscar-Vorst.jpg

Ixodiphagus hookeri

Systematics
Class : Insects (Insecta)
Order : Hymenoptera (Hymenoptera)
Subordination : Waist Wasps (Apocrita)
Family : Encyrtidae
Genre : Ixodiphagus
Type : Ixodiphagus hookeri
Scientific name
Ixodiphagus hookeri
( Howard , 1908)
Feminine habitus, ventral, and enlarged genitals
Ixodiphagus hookeri Howard: Fig. 1, Parasites leave nymphs of Rhipicephalus sanguineus Latr .; FIG. 2, R. sanguineus nymphs with the striped appearance when parasitized; Figure 3, Ixodiphagus hookeri , male; Fig. 4, antenna of a female; Fig. 5, Excursion holes in tick nymphs, after Herbert P. Wood , 1911
Female habitus

Ixodiphagus hookeri is a wasp of the genus Ixodiphagus in the family Encyrtidae . The hyperparasite lays its eggs in the larvae and nymphs of various ticks . The hatching larvae feed ontheir hostas parasitoids . The potential use of Ixodiphagus hookeri for biological pest control has been studied for almost a century. Despite the initially promising successes in reproduction in the laboratory, no sustainable effect in the control of ticks as a vector of zoonoses has been achievedso far.

description

Ixodiphagus hookeri is a very small, black-colored wasp whose external appearance corresponds to that of other ore wasps . The body length is 0.8-0.9 millimeters in both sexes, the wingspan is 1.5 millimeters. The head is flattened at the top and twice as wide as it is long. There are large complex eyes on the side and three ocelli on the head , the distance between the rear ocelli and the edges of the complex eyes is significantly larger than their own diameter. At the front of the head there are two antennas that are close together . The antennae of the females have scapus, pedicellus and a funiculus divided into six limbs with a clavus of three limbs. The basal member of the clavus is separated from its distal neighbor by a furrow, so that the impression of a seventh flagellomer can arise on the funiculus. The males have antennae, the only two-parted end of which is not thickened.

The abdomen of the male wasps is clearly more pointed than that of the female in the dorsal view. It consists of eight segments in males and seven segments in females, one of which is fused with the thorax so that only seven or six segments are visible. The differentiation of the sexes takes place in the laboratory through the complexly designed genitalia of the female, which has been transformed into an ovipositor, and the simply structured genitalia of male wasps.

Way of life

Hosts

Ixodiphagus hookeri is a mandatory parasitoid of several types of ticks . Only a selection of the tick species present is parasitized in different habitats. Proven hosts are:

In searching for suitable hosts, Ixodiphagus hookeri follows odorous substances emitted by potential mammalian hosts of their preferred tick nymphs. In the laboratory test at the University of Hohenheim , for which wasps from German populations were used, they followed carbon dioxide and the species-specific smell of the faeces of deer and the smell of the hair of deer and wild boar . The droppings of cattle , rabbits and field mice and the hair of cattle and field mice had no effect. The droppings of the common trestle were only attractive at a distance of up to an inch. Experiments with odorous substances dissolved in n- hexane at various stages of development of the Amblyomma variegatum tick showed a strong attraction, and dummies of hosts were penetrated with the ovipositor . Previous research on wasps in Kenya found that they were attracted to the body of cattle by the smell of urine , feces and swab samples, as well as the smell of the feces of Amblyomma variegatum . The experimental setup could not show whether the smell of mammals or only the species-specific smell of cattle had an attractive effect. At close range, the wasps follow visual cues such as size and shape in order to distinguish suitable from unsuitable hosts. Due to the great geographical distance, the different host range and differences in the development of different populations, it cannot be ruled out that Ixodiphagus hookeri contains several species , subspecies or strains.

Egg laying

Egg-laying on a saturated nymph of the common wooden ram
Adult Ixodiphagus hookeri with dead nymph of the common wooden goat
Loophole in the dead nymph of the common ram

Counts of deer and wild boar nymphs of the common wooden ram revealed that the wasps in ticks can lay all their eggs on a single piece of game. A wasp ready to lay eggs runs around on the fur of a possible host of ticks and approaches the larva or nymph of a tick with strong movements of its antennae . Then the body surface of the potential host is felt with drumming feelers. Various species of the parasitic wasps , which are not closely related , have also been described as drumming on the ground when looking for suitable places to lay their eggs. These parasitic wasps use the self-generated vibrations of the body surface of a potential host to identify it and have developed special organs at the tips of the antennae. The wasp continues its search if it does not accept the larva or nymph as a host. If it accepts the host, it drills its ovipositor into the host's abdomen from above, or it bends its own abdomen under the host and inserts the ovipositor into its body from below. The egg-laying is followed by another short drumming with the antennae on the host. The entire egg-laying process, from the first drumming until the infected larva or nymph leaves, takes between two and twenty seconds, provided it is undisturbed.

The wasp does not lay eggs again in a host that it has attacked. However, eggs are laid in hosts that are already being used by other females to lay eggs, so that a nymph can be infested with larvae from various wasps. A female wasp can lay 100 to 200 eggs, according to other sources, it can parasitize more than 100 ticks. This contrasts with the results of observations in Kenya , which indicate two to a maximum of four parasitized nymphs per wasp. It is believed that Ixodiphagus hookeri adapts the number of eggs it sheds to both the type of tick being parasitized and its stage of development, with a larger volume associated with more food for the offspring and a larger number of eggs. The wasps of a German population preferred unfeeded nymphs of the common wood buck to larvae and fed nymphs when laying eggs. The alluvial forest tick was not accepted as a host.

Development cycle

After the eggs are laid in a tick larva, the parasite's eggs are carried along to the nymph stage. The larvae of Ixodiphagus hookeri , which feed on the meal and all of the nymph's internal organs, only begin to develop when the infected nymph of the tick takes its blood meal from a host . The number of Ixodiphagus hookeri in an infested nymph varies between one and 15, with an average number of 6.5 parasites. Under laboratory conditions, the development of the wasp larvae from hatching through the larval stage and pupa to hatching of the adult wasps takes an average of 28 to 70 days and a maximum of 102 days, with a longer development period in the second half of the year. In nature, the duration of development seems to depend heavily on climatic conditions, with shorter development times at higher temperatures, with the mortality of developing wasp larvae increasing from 23 ° C and reaching 100 percent at 30 ° C. After some time, the successfully parasitized tick nymphs can be recognized by the fact that their rear bodies are slightly swollen and not shimmering blue as usual, but brown or yellowish in color and appear blotchy or striped because of the translucent larvae. As the process progresses, the spots disappear. The droppings of the whitish wasp larvae are collected at the far end of the nymph's body cavity. At the end of development, the larvae align themselves parallel to the longitudinal axis in the front area and pupate in this position. Shortly after the wasps pupate, the nymph's body is black in front and the abdomen is yellowish translucent. The entire body of the host can be filled with the pupae of Ixodiphagus hookeri .

After development is complete, adult wasps hatch from the pupae and gnaw a hole in the back, at the weakest point, for the excursion into the shell of the tick nymph. Adult wasps can only be found for a short period of three to five weeks, in northern summer between late July and late September. Data collected in Germany and in Texas in the early 20th century led to the hypothesis that the development cycle of Ixodiphagus hookeri is adapted to that of its hosts. The appearance of adult wasps coincides with late summer, when the wild population has reproduced and has not yet been reduced by the winter. The tick population and thus the number of potential hosts are correspondingly larger. The goal of hatching the wasps during the short period of particularly high tick activity is achieved through three different developmental patterns:

  1. A wasp lays its eggs in a tick larva in late summer of the first year. The eggs rest while the tick's larva develops into a nymph. The development of the wasp larva begins with the nymph's blood meal in late summer of the second year. During the hibernation of the nymph, the development of the wasp also comes to a standstill. It only hatches in the late summer of the third year.
  2. The nymph, already infected as a larva, does not find a mammal host in the second year. After a hibernation, she takes a blood meal in the spring of the third year. This triggers the now shortened development of the wasp larva, here too the adult wasps hatch in the late summer of the third year.
  3. A wasp lays its eggs in a nymph in late summer, which then eats its blood meal. The wasp begins its development, interrupted by the hibernation of the nymph, and hatches in the late summer of the second year.

In populations in subtropical regions such as Kenya, no seasonality can be determined; adult ixodiphagus hookeri , like their hosts, can be found throughout the year.

Among the hatched wasps, female wasps are in the majority. Mating takes place immediately after hatching and lasts only seconds, then the female goes in search of a suitable host. Both sexes do not eat any food and have a lifespan of about three days, only in exceptional cases males live up to ten days.

Prevalence

Nymphs of the common wooden goat , left with millimeter scale

The investigation of German populations of the common wood buck for the infestation of the nymphs with Ixodiphagus hookeri showed an infestation rate of 1.9 to 3.8 percent over a period of three years. This apparently very low infestation rate can be explained by a number of factors. When the nymphs are caught by stripping them from the vegetation, the infested nymphs are those who are still looking for a host and who have brought their parasite load with them from the larval stage. The unaffected nymphs might have been parasitized at a later date, which was prevented by their capture. The larvae and nymphs are primarily parasitized by Ixodiphagus hookeri while they are on the host themselves and are looking for a suitable place to prick or are already sucking blood. The collection of larvae and nymphs that fall off the host after their blood meal could prove a significantly higher infestation rate with Ixodiphagus hookeri , but it is difficult to carry out. Studies from western France and Kenya which found no infestation in nymphs before the blood meal and a very high infestation in suckling nymphs on mammals support such considerations. An older study from Germany provided significantly different results. It detected an infestation in more than 90 percent of the tick nymphs, but it may contain methodological errors. Investigations in the United States also showed significantly higher infestation rates, but overall the figures indicate differences in the biology of European and American populations that still require clarification.

distribution

Group of white tailed deer

Ixodiphagus hookeri occurs worldwide with the exception of Australia and the Antarctic . Their presence in Germany seems to be linked to a dense game population with a strong infestation by the common wood tick. In any event, a dense population of suitable ticks is required. In the United States , a connection has been established between the population density of white-tailed deer , the deer tick parasitizing on it, and the occurrence of Ixodiphagus hookeri . Ten to twenty white-tailed deer per square kilometer seem to be necessary to ensure a sufficiently dense tick population.

Biological pest control

Robert A. Cooley at Rocky Mountain Laboratories , 1938

Ticks are mandatory blood-sucking parasites of vertebrates. Most species infest mammals including farm animals and humans. They are major vectors of a wide variety of pathogens, including those causing Rocky Mountain typhus , tularemia , early summer meningoencephalitis, and Lyme disease . Since their vector property was discovered, there has been great interest in controlling ticks. Ixodiphagus hookeri and other species of the genus were examined for the possibility of their use for biological pest control just a few years after their first description .

For the targeted control of ticks, in particular Dermacentor andersoni and Dermacentor variabilis , Ixodiphagus hookeri were bred in large numbers in the Rocky Mountain Laboratories in the 1920s under the direction of Robert A. Cooley . The breed was partly built up with Ixodiphagus hookeri , which were made available for this purpose by Émile Brumpt from France. Nymphs of Dermacentor andersoni served as hosts in the laboratory , which came from endemic areas of Rocky Mountain spotted fever and tularemia and could easily be reproduced on laboratory rabbits. First of all, laboratory rabbits or wild mice were populated with large numbers of nymphs. The available wasps were then brought near the suckling nymphs and laid their eggs.

The experiments to breed Ixodiphagus hookeri in the laboratory aimed to establish self-reproducing populations in nature and thus to eradicate Dermacentor andersoni and other ticks as vectors of zoonoses . The first attempts were very promising, also with regard to the wintering of the parasite. However, nymphs infected with spirochetes or Babesia microtis were not accepted as hosts. The parasitized nymphs were released in their natural environment where the control of Dermacentor andersoni was considered particularly important. Alternatively, the development was not waited for, but the mammals with the tick nymphs were brought into a natural environment after the wasps had laid their eggs. Extensive releases of Ixodiphagus hookeri have been made repeatedly in areas with dense tick populations:

  • Naushon Iceland , Massachusetts , 1926-1927: to combat the extremely dense population of deer ticks , and Dermacentor variabilis was Ixodiphagus hookeri released. At first it appeared that the measure had been successful. In 1940 and 1941 individual wasps were found. Both types of ticks remained frequent in the long term, but Ixodiphagus hookeri was able to establish itself. In 1987 it was found in a third of deer tick nymphs.
  • Montana , Colorado , Idaho, and Oregon , 1927–1933: in the largest mass release, more than four million Ixodiphagus hookeri were used to control Dermacentor andersoni . Neither a reduction in the tick population could be observed, nor an establishment of the wasps could be proven. Only in 1929 were some wasps found from the releases of the two previous years.
  • Leningrad Oblast , 1938: 2,600 wasps and 38,000 parasitized larvae and nymphs of the common wood tick were released to control Dermacentor variabilis . Two years later, no wasps could be detected, nor was a reduction in the tick population recognizable.
  • Martha's Vineyard , Massachusetts, 1937-1939: 90,000 female wasps were released in two locations on Martha's Vineyard to control Dermacentor variabilis . Two years later, no wasps could be detected, nor was a reduction in the tick population recognizable.
  • Trans Mara District , Kenya , 1993–1994: 150,000 Ixodiphagus hookeri were released over a period of one year in a four acre pasture with ten zebus . In the four months prior to the release of the wasps, 4,000 nymphs of the ticks Rhipicephalus appendiculatus and Amblyomma variegatum were released on the pasture . While no effect was found with regard to R. appendiculatus , the number of A. variegatum specimens found on the cattle fell by 95 percent and remained low even after the release. Only a small percentage of the tick nymphs collected after the end of the releases were parasitized by wasps.

The research did not lead to a successful use in tick control. The failure of such attempts is possibly due to the strong adaptation of the populations to local conditions and to certain hosts, which make the use of imported wasps of other origins fail. Measures such as the use of acaricides appear to be unsuitable because of the poisonous effect on the rest of the fauna and humans, the high costs and the observed development of resistance . Current research is aimed at the use of acaropathogenic fungi and nematodes , but is not yet operational. Regardless of the failure of previous efforts, biological tick control with the help of Ixodiphagus hookeri is therefore still the subject of research.

One aspect of the use of Ixodiphagus hookeri is the strongly decreased prevalence of the pathogenic spirochete Borrelia burgdorferi , the Lyme disease pathogen, and earlier than Babesia Microtis or Theileria Microtis known piroplasms in tick populations that are affected by the wasps. Nymphs infected by Ixodiphagus hookeri are never infected with Borrelia burgdorferi and only rarely with piroplasm. This also reduces the risk of infection for people in the area concerned.

Symbiotic or parasitic microorganisms

Wolbachia pipiens

The presence of bacteria of the Wolbachia pipientis group in the common wood tick has been demonstrated in several studies . These bacteria are widespread in insects , but have also been found in claw carriers and nematodes . Their observed influence ranges from obligatory mutualism in filariae , which are dependent on the presence of Wolbachia for development and reproduction , to commensalism to parasitism , with the prevalence ranging from low to complete, depending on the species. In infected insects, Wolbachia was able to demonstrate the diverse influence on the reproduction of their hosts, such as causing parthenogenesis , higher mortality or feminization of male individuals and cytoplasmic incompatibilities, but also strengthening the immune system. The prevalence of ticks is low and the route of infection has long been unclear.

Ixodiphagus hookeri are almost 100 percent infected with a strain of Wolbachia pipientis , whose close relatives have also been found in other hymenoptera . In a molecular genetic investigation of unfeeded nymphs in a natural French population of the common woodbuck, it was found that nymphs either did not contain any DNA from Ixodiphagus hookeri and Wolbachia pipientis , i.e. were free from parasites, or that both DNAs could be detected. Alleged infections of ticks with Wolbachia found in the past were probably an infestation with the infected larvae of Ixodiphagus hookeri . Nothing is known about the specific effects of the infection with Wolbachia pipiens on Ixodiphagus hookeri .

Arsenophonus nasoniae and Rickettsiae

In recent years, the more frequent use of molecular genetic methods has led to the detection of a number of microorganisms in ticks of various genera. Arsenophonus nasoniae was one of these microorganisms . This bacterium was first detected as an endosymbiont of the ore wasp Nasonia vitripennis , a member of the family Pteromalidae that parasitizes on flies . Since then, further evidence has been obtained from other wasps. Arsenophone nasoniae colonizes the tissue and body fluid around the germ cells and causes the death of about 80 percent of male offspring. To do this, it prevents the production of maternal centrosomes , which are required for the development of male wasps.

Nymphs from a natural population of the common wood tick in Slovakia were kept until Ixodiphagus hookeri hatched . Of 96 wasps (19 male, 69 female and 8 not determinable), 27 (4, 21, 2) or 28.1 percent were infected with Arsenophonus nasoniae , 13 (4, 8, 1) or 13.5 percent with Rickettsia helvetica and 2 (2, 6, 1) or 9.4 percent with Rickettsia monacensis . Arsenophonus nasoniae and rickettsiae were found in eight wasps . The molecular genetic investigation of nymphs of the common wood buck showed that DNA from Arsenophonus nasoniae could only be detected together with DNA from Ixodiphagus hookeri , i.e. in parasitized nymphs. About five percent of the nymphs contained only wasp DNA with no evidence of the bacterium, and ten percent contained the DNA of rickettsiae with no evidence of the bacterium. The infection with Arsenophonus nasoniae , but not that with Rickettsia, seems to be linked to the infestation with the parasite. However, DNA from Arsenophonus nasoniae was also detected in the eggs of ticks of the species Amblyomma americanum and Dermacentor variabilis , which cannot be explained by a transmission of Ixodiphagus hookeri .

Systematics and taxonomy

Leland Ossian Howard , 1911

Ixodiphagus hookeri was first described by Howard in 1908 as Hunterellus hookeri . The description was based on specimens that had hatched from several nymphs of ticks of the type host Rhipicephalus texanus . These ticks had been collected on a domestic dog in Corpus Christi , Texas ( 27 ° 45 ′  N , 97 ° 24 ′  W ) in April 1908 and kept alive for experiments by William Anson Hooker of the laboratory of the Bureau of Entomology in Dallas . Hooker is also honored with the specific epithet .

The year before, Howard had described a tick-parasitic insect for the first time, the wasp Ixodiphagus texanus , for which he established the genus Ixodiphagus . The French entomologist Robert du Buysson of the Muséum national d'histoire naturelle described another species, Ixodiphagus caucurtei , in 1912 , after specimens from nymphs of the common ram that were collected in France. In 1929 Robert A. Cooley suspected that all three of these parasitoids were the same species. Arthur B. Gahan showed in a publication in 1934 that the two species and genera described by Howard were different, but that Ixodiphagus caucurtei was a synonym of Hunterellus hookeri is. Trjapitzin proposed in 1985 Ixodiphagus as the only genus of these parasitic wasps and Hunterellus as a synonym. This view seems to be widely accepted, Hunterellus hookeri belongs to the genus Ixodiphagus as Ixodiphagus hookeri .

In Senegal copies were found in 1951 by Jean Risbec as Habrolepis caniphila described. Risbec himself placed his species in the genus Hunterellus in 1954 . David P. Annecke and H. Patricia Insley examined the type material Risbecs and synonymized the species with Hunterellus hookeri in 1971.

Howard's holotype was added to the collection of the National Museum of Natural History in Washington, DC under number 11,497 . Apparently this was no longer available in a later investigation, in 2010 John S. Noyes determined a lectotype from the material in the museum . The type material of Ixodiphagus caucurtei is in the Muséum national d'histoire naturelle in Paris.

Synonyms

Ixodiphagus hookeri is also known by the following synonyms:

  • Habrolepis caniphila Risbec , 1951
  • Hunterellus caniphila ( Risbec , 1951)
  • Hunterellus hookeri Howard , 1908
  • Ixodiphagus caucurtei Buysson , 1912

Web links

Commons : Ixodiphagus hookeri  - Collection of images, videos and audio files

Individual evidence

  1. ↑ a b c M. S. Quaraishi: Morphology of Two Chalcidoid Parasites of Ticks, Hunterellus hookeri Howard, 1908, and Ixodiphagus texanus Howard, 1907 . In: The American Midland Naturalist 1958, Vol. 59, No. 2, pp. 489-504, doi : 10.2307 / 2422494 .
  2. ^ A b John S. Noyes: Encyrtidae of Costa Rica (Hymenoptera: Chalcidoidea) 3. Subfamily Encyrtinae: Encyrtini, Echthroplexiellini, Discodini, Oobiini and Ixodiphagini, parasitoids associated with bugs (Hemiptera), insect eggs (Hemiptera, Lepidoptera, Coleoptera ) and ticks (Acari) . Memoirs of the American Entomological Institute Volume 84. Gainesville, FL 2010, ISBN 978-1-887988-28-5 , p. 656.
  3. ↑ a b c d e f g h i j k l m n o p Robert L. Zuparko: Annotated Checklist of California Encyrtidae (Hymenoptera) . Zootaxa 2015, Volume 4017, pp. 1–126, doi : 10.11646 / zootaxa.4017.1.1 .
  4. ↑ a b c Fanuel A. Demas et al .: Cattle and Amblyomma variegatum Odors Used in Host Habitat and Host Finding by the Tick Parasitoid, Ixodiphagus hookeri . In: Journal of Chemical Ecology 2000, Volume 26, No. 4, pp. 1079-1093, doi : 10.1023 / A: 1005497201074 .
  5. ↑ a b c d F. Larrousse , Arthur G. King and SB Wolbach : The Overwintering in Massachusetts of Ixodiphagus caucurtei . In: Science 1928, Volume 67, No. 1735, pp. 351-353, doi : 10.1126 / science.67.1735.351 .
  6. ^ A b c Herbert P. Wood : Notes on the Life History of the Tick Parasite Hunterellus hookeri Howard . In: Journal of Economic Entomology 1911, Volume 4, No. 5, pp. 425-431, digitizedhttp: //vorlage_digitalisat.test/1%3D~GB%3D~IA%3Djournalofeconomi04ento~MDZ%3D%0A~SZ%3Dn489~ double-sided%3D~LT%3D~PUR%3D .
  7. ↑ a b c d e f g Robert A. Cooley: A Search for Tick Parasites in South Africa . In: Onderstepoort Journal of Veterinary Science and Animal Industry 1934, Volume 3, No. 1, pp. 23-42, digitizedhttp: //vorlage_digitalisat.test/1%3Dhttps%3A%2F%2Frepository.up.ac.za%2Fbitstream%2Fhandle%2F2263%2F48340%2F2cooley1934.pdf%3Bsequence%3D1~GB%3D~IA%3D~MDZ% 3D% 0A ~ SZ% 3D ~ double-sided% 3D ~ LT% 3D ~ PUR% 3D .
  8. ↑ a b c d e f g h Jana Collatz et al .: A hidden beneficial: biology of the tick-wasp Ixodiphagus hookeri in Germany . In: Journal of Applied Entomology 2011, Volume 135, pp. 351-358, doi : 10.1111 / j.1439-0418.2010.01560.x .
  9. ↑ a b Kirby C. Stafford, Anthony J. DeNicola and Louis A. Magnarelli: Presence of Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in Two Connecticut Populations of Ixodes scapularis (Acari: Ixodidae) . In: Journal of Medical Entomology 1996, Volume 33, No. 1, pp. 183-188, doi : 10.1093 / jmedent / 33.1.183 .
  10. ↑ Marcos Antônio Bezerra Santos et al .: Larvae of Ixodiphagus wasps (Hymenoptera: Encyrtidae) in Rhipicephalus sanguineus sensu lato ticks (Acari: Ixodidae) from Brazil . In: Ticks and Tick-borne Diseases 2017, Volume 8, No. 4, pp. 564-566, doi : 10.1016 / j.ttbdis.2017.03.004 .
  11. ↑ Fanuel A. Demas et al .: Visual Evaluation and Recognition of Hosts by the Tick Parasitoid, Ixodiphagus hookeri (Hymenoptera: Encyrtidae) . In: Journal of Insect Behavior 2002, Volume 15, No. 4, pp. 477-494, doi : 10.1023 / A: 1016377132585 .
  12. ↑ a b Jana Collatz et al .: Being a parasitoid of parasites: host finding in the tick wasp Ixodiphagus hookeri by odours from mammals . In: Entomologia Experimentalis et Applicata 2010, Volume 134, No. 2, pp. 131-137, doi : 10.1111 / j.1570-7458.2009.00943.x .
  13. ↑ Keiji Takasu et al .: Host Recognition by the Tick Parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) . In: Environmental Entomology 2003, Volume 32, No. 3, pp. 614-617, doi : 10.1603 / 0046-225X-32.3.614 .
  14. ↑ Donald LJ Quicke: The Braconid and Ichneumonid Parasitoid Wasps. Biology, Systematics, Evolution and Ecology . John Wiley & Sons, Oxford and Hoboken, NJ 2015, ISBN 978-1-118-90705-4 , pp. 163-167.
  15. ↑ a b c N. I. Alfejew and Ja. W. Klimas: Experience in cultivating ichneumon flies, Hunterellus hookeri, obtained from United States, which destroy ixodid ticks of Soviet fauna . In: Priroda 1938, Volume 2, pp. 98-101. Translation 1674 by Naval Medical Research Unit Three , Cairo, Egypt, digitizedhttp: //vorlage_digitalisat.test/1%3Dhttp%3A%2F%2Fwww.nhm.ac.uk%2Fresources%2Fresearch-curation%2Fprojects%2Fchalcidoids%2Fpdf_X%2FAlfeevKl938b.pdf~GB%3D~IA%3D~MDZ 3D% 0A ~ SZ% 3D ~ double-sided% 3D ~ LT% 3D ~ PUR% 3D .
  16. ^ A b Esther N. Mwangi et al .: Predators, parasitoids and pathogens of ticks: A review . In: Biocontrol Science and Technology 1991, Volume 1, No. 3, pp. 147-156, doi : 10.1080 / 09583159109355195 .
  17. ^ A b Edward F. Knipling and Carrol Dayton Steelman: Feasibility of Controlling Ixodes scapularis Ticks (Acari: Ixodidae), the Vector of Lyme Disease, by Parasitoid Augmentation . In: Journal of Medical Entomology 2000, Volume 37, No. 5, pp. 645-652, doi : 10.1603 / 0022-2585-37.5.645 .
  18. ↑ a b c Keiji Takasu and Satoshi Nakamura: Life history of the tick parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) in Kenya . In: Biological Control 2008, Volume 46, No. 2, pp. 114–121, doi : 10.1016 / j.biocontrol.2008.04.013 .
  19. ↑ Renjie Hu and Kerwin E. Hyland: Effects of the Feeding Process of Ixodes scapularis (Acari: Ixodidae) on Embryonic Development of its Parasitoid, Ixodiphagus hookeri (Hymenoptera: Encyrtidae) . In: Journal of Medical Entomology 1998, Volume 35, No. 6, pp. 1050-1053, doi : 10.1093 / jmedent / 35.6.1050 .
  20. ^ A b c Robert A. Cooley : Preliminary Report on the Tick Parasite, Ixodiphagus caucurtei du Buysson . In: Montana State Board of Entomology (Ed.): Seventh Biennual Report. 1927-1928 . The Tribune, Great Falls, MT 1928, pp. 17-31, digitizedhttp: //vorlage_digitalisat.test/1%3D~GB%3D~IA%3Dbiennialre19271928mont~MDZ%3D%0A~SZ%3Dn19~ double-sided%3D~LT%3D~PUR%3D .
  21. ↑ a b c d e f Moses M. Cole: Biological Control of Ticks by the Use of Hymenopterous Parasites. A review . WHO / EBL 43.65. World Health Organization, Geneva 1965, digitizedhttp: //vorlage_digitalisat.test/1%3Dhttp%3A%2F%2Fwww.nhm.ac.uk%2Fresources%2Fresearch-curation%2Fprojects%2Fchalcidoids%2Fpdf_X%2FCole965.pdf~GB%3D~IA%3D~MDZ% 3D% 0A ~ SZ% 3D ~ double-sided% 3D ~ LT% 3D ~ PUR% 3D .
  22. ↑ AJ Davis: Bibliography of the Ixodiphagini (Hymenoptera, Chalcidoidea, Encyrtidae), parasites of ticks (Acari, Ixodidae), with notes on their biology . In: Tijdschrift voor Entomologie 1986, Volume 129, No. 6, pp. 181-190, digitizedhttp: //vorlage_digitalisat.test/1%3D~GB%3D~IA%3Dtijdschriftvoore128129198586nede~MDZ%3D%0A~SZ%3Dn511~ double-sided%3D~LT%3D~PUR%3D .
  23. ↑ Wladimir A. Trjapitzin and Enrique Ruíz Cancino: Los encírtidos del género Ixodiphagus Howard (Hymenoptera: Chalcidoidea: Encyrtidae), parasitoides de garrapatas (Acarina: Ixodidae) . In: Biotam 1996, Volume 8, No. 1, pp. 9-20.
  24. ↑ Kirby C. Stafford, Anthony J. DeNicola and Howard J. Kilpatrick: Reduced Abundance of Ixodes scapularis (Acari: Ixodidae) and the Tick Parasitoid Ixodiphagus hookeri (Hymenoptera: Encyrtidae) with Reduction of White-Tailed Deer . In: Journal of Medical Entomology 2003, Volume 40, No. 5, pp. 642-652, doi : 10.1603 / 0022-2585-40.5.642 .
  25. ^ A b Robert A. Cooley: Tick ​​Parasites - Executive Report . In: Montana State Board of Entomology (Ed.): Seventh Biennual Report. 1927-1928 . The Tribune, Great Falls, MT 1928, pp. 10-16, digitizedhttp: //vorlage_digitalisat.test/1%3D~GB%3D~IA%3Dbiennialre19271928mont~MDZ%3D%0A~SZ%3Dn12~ double-sided%3D~LT%3D~PUR%3D .
  26. ↑ Fred A. Morton: Quantity Production of Tick Parasites . In: Montana State Board of Entomology (Ed.): Seventh Biennual Report. 1927-1928 . The Tribune, Great Falls, MT 1928, pp. 32-35, digitizedhttp: //vorlage_digitalisat.test/1%3D~GB%3D~IA%3Dbiennialre19271928mont~MDZ%3D%0A~SZ%3Dn34~ double-sided%3D~LT%3D~PUR%3D .
  27. ^ JR Parker and WJ Butler: Tick ​​Parasite Liberation in Montana During 1928 . In: Montana State Board of Entomology (Ed.): Seventh Biennual Report. 1927-1928 . The Tribune, Great Falls, MT 1928, pp. 35-38, digitizedhttp: //vorlage_digitalisat.test/1%3D~GB%3D~IA%3Dbiennialre19271928mont~MDZ%3D%0A~SZ%3Dn37~ double-sided%3D~LT%3D~PUR%3D .
  28. ^ Andrew Spielman and Heinz Mehlhorn : Ticks as Vectors of Agents of Diseases, Man . In: Heinz Mehlhorn (Ed.): Encyclopedia of Parasitology. Fourth Edition . Springer, Berlin and Heidelberg 2016, ISBN 978-3-662-43977-7 , pp. 2729–2737, here p. 2736.
  29. ↑ Sidney Cobb: Tick ​​Parasites on Cape Cod . In: Science 1942, Volume 95, No. 2472, P. 503, doi : 10.1126 / science.95.2472.503 .
  30. ↑ Suzanne M. Lyon, Roy Van Driesche and John D. Edman: Ecology of Hunterellus hookeri (Hymenoptera: Encyrtidae) and Evaluation of Its Impact on Ixodes scapularis (Acari: Ixodidae) on Nonamesset Island in Massachusetts . In: Environmental Entomology 1998, Volume 27, No. 2, pp. 463-468, doi : 10.1093 / ee / 27.2.463 .
  31. ↑ a b Thomas N. Mather, Joseph Piesman and Andrew Spielman: Absence of spirochaetes (Borrelia burgdorferi) and piroplasms (Babesia microti) in deer ticks (Ixodes dammini) parasitized by chalcid wasps (Hunterellus hookeri) . In: Medical and Veterinary Entomology 1987, Vol. 1, No. 1, pp. 3-8, doi : 10.1111 / j.1365-2915.1987.tb00317.x .
  32. ↑ a b c Renjie Hu, Kerwin E. Hyland and James H Oliver: A review on the use of Ixodiphagus wasps (Hymenoptera: Encyrtidae) as natural enemies for the control of ticks (Acari: Ixodidae) . In: Systematic and Applied Acarology 1998, Volume 3, pp. 19-28.
  33. ^ Carroll N. Smith and Moses M. Cole, Studies of Parasites of the American Dog Tick . In: Journal of Economic Entomology 1943, Volume 36, No. 4, pp. 569-572, doi : 10.1093 / jee / 36.4.569 .
  34. ↑ Esther N. Mwangi et al .: The impact of Ixodiphagus hookeri, a tick parasitoid, on Amblyomma variegatum (Acari: Ixodidae) in a field trial in Kenya . In: Experimental & Applied Acarology 1997, Volume 21, No. 2, pp. 117-126, doi : 10.1023 / B: APPA.0000031790.30821.57 .
  35. ↑ Kathrin Hartelt et al .: Biological control of the tick Ixodes ricinus with entomopathogenic fungi and nematodes: Preliminary results from laboratory experiments . In: International Journal of Medical Microbiology 2008, Volume 298, Supplement 1, pp. 314-320, doi : 10.1016 / j.ijmm.2007.10.003 .
  36. ^ Richard S. Ostfeld et al .: Controlling Ticks and Tick-borne Zoonoses with Biological and Chemical Agents . In: BioScience 2006, Volume 56, No. 5, pp. 383-394, doi : 10.1641 / 0006-3568 (2006) 056 [0383: CTATZW] 2.0.CO; 2 .
  37. ↑ a b Ellen Tijsse-Klasen, Marieta Braks, Ernst-Jan Scholte, Hein Sprong: Parasites of vectors - Ixodiphagus hookeri and its Wolbachia symbionts in ticks in the Netherlands . In: Parasites & Vectors 2011, Volume 4, Article 228, doi : 10.1186 / 1756-3305-4-228 .
  38. ↑ a b Olivier Plantard et al .: Detection of Wolbachia in the Tick Ixodes ricinus is Due to the Presence of the Hymenoptera Endoparasitoid Ixodiphagus hookeri . In: PLOS ONE 2012, Volume 7, No. 1, Article e30692, doi : 10.1371 / journal.pone.0030692 .
  39. ↑ a b Geetha Subramanian et al .: Multiple tick-associated bacteria in Ixodes ricinus from Slovakia . In: Ticks and Tick-borne Diseases 2012, Volume 3, No. 5-6, pp. 406-410, doi : 10.1016 / j.ttbdis.2012.10.001 .
  40. ↑ a b Monika Bohacsova et al .: Arsenophonus nasoniae and Rickettsiae Infection of Ixodes ricinus Due to Parasitic Wasp Ixodiphagus hookeri . In: PLOS ONE 2016, Volume 11, No. 2, Article e0149950, doi : 10.1371 / journal.pone.0149950 .
  41. ↑ a b Jonathan Kagemann and Keith Clay: Effects of Infection by Arsenophonus and Rickettsia Bacteria on the Locomotive Ability of the Ticks Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis . In: Journal of Medical Entomology 2013, Volume 50, No. 1, pp. 155-162, doi : 10.1603 / ME12086 .
  42. ↑ Oleg Mediannikov et al .: Isolation of Arsenophonus nasoniae from Ixodes ricinus ticks in Slovakia . In: Ticks and Tick-borne Diseases 2012, Volume 3, No. 5-6, pp. 367-370, doi : 10.1016 / j.ttbdis.2012.10.016 .
  43. ↑ a b c Leland Ossian Howard: Another Chalcidoid Parasite of a Tick . In: The Canadian Entomologist 1908, Volume XL, No. 7, pp. 239-241, digitizedhttp: //vorlage_digitalisat.test/1%3D~GB%3D~IA%3Dcanadianentomolo40ento~MDZ%3D%0A~SZ%3Dn259~ double-sided%3D~LT%3D~PUR%3D .
  44. ↑ Leland Ossian Howard : A Chalcidid Parasite of a Tick . In: Entomological News 1907, Volume XVIII, No. 9, pp. 375-378, Plate XIV, digitizedhttp: //vorlage_digitalisat.test/1%3D~GB%3D~IA%3Dentomologicalnew18acaduoft~MDZ%3D%0A~SZ%3Dn421~ double-sided%3D~LT%3D~PUR%3D .
  45. ↑ a b Robert du BUYSSON : Un hymenoptera parasite of Ixodes . In: Archives de Parasitologie 1912, Volume 15, pp. 246–247, digitizedhttp: //vorlage_digitalisat.test/1%3Dhttp%3A%2F%2Fwww.nhm.ac.uk%2Fresources%2Fresearch-curation%2Fprojects%2Fchalcidoids%2Fpdf_X%2FBuysso912.pdf~GB%3D~IA%3D~MDZ% 3D% 0A ~ SZ% 3D ~ double-sided% 3D ~ LT% 3D ~ PUR% 3D .
  46. ^ A b c Arthur B. Gahan: On the Identities of Chalcidoid Tick Parasites (Hymenoptera) . In: Proceedings of the Entomological Society of Washington 1934, Vol. 36, No. 4, pp. 89-97, digitizedhttp: //vorlage_digitalisat.test/1%3D~GB%3D~IA%3Dproceedingsofent3536193334ento~MDZ%3D%0A~SZ%3Dn347~ double-sided%3D~LT%3D~PUR%3D .
  47. ↑ a b Jean Risbec : Les Chalcidoïdes d'AOF In: Mémoires de l'Institut français d'Afrique Noire 1951, Volume 13, No. 1, pp. 1–409, here pp. 170–172, ZDB -ID 974092- 2 (not viewed).
  48. ↑ a b c Jean Risbec: Chalcidoides Proctotrupides et de l'Afrique Tropicale Française (4e Supplement) . In: Bulletin de l'Institut français d'Afrique Noire 1954, Volume 16, pp. 1035-1092, here pp. 1070-1071, doi : 10.5281 / zenodo.24263 .
  49. ^ A b David P. Annecke and H. Patricia Insley: Catalog of Ethiopian Encyrtidae and Aphelinidae (Hymenoptera: Chalcidoidea) . Entomology Memoir No. 23. Department of Agricultural Technical Services, Pretoria 1971, p. 14 and p. 38.