PARTHENOGENESIS AND OVERWINTERING BEHAVIOR IN IXODIPHAGUS TEXANUS HOWARD,,2
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1 PARTHENOGENESIS AND OVERWINTERING BEHAVIOR IN IXODIPHAGUS TEXANUS HOWARD,,2 Thomas M, Logan, Jerry L. Bowman and Jakie A. Hai,.' Department of Entomology Oklahoma State University Stillwater, Oklahoma Abstract: The tick parositoid, Ixodiphogus lexar/us Howard, successfully overwintered under field conditions in Dermacentor /Jar/ubilis (Say) ticks parasitized as replete larvae and unfed nymphs. Ticks parasitized as replele nymphs were unsuitable as ovenvintering hosts. Ixodiphagtts texanus emerging from D. variabilis parasitized IlS unfed larvae were monitored for parthenogenesis. Solitary unmated I. texarlus were given access to replete tick nymphs. Three of 50 groups exposed contained parasitized ticks find nil emerging parasitoids were male. Key Words: Tick parasitoid. l:wdiphagus lexallus biology, ticks, parthenogenesis, lxodiphagus (exarlll.'i overwintering, arrhenotoky in lxodiphagus texml1ls. J. Agric. Entomol. 2(3): (July 1985) The tick parasitoid, Ixodiphagus lexanus Howard, is similar to Hu.nterellus hookeri Howard, a parasitoid which has been the object of many attempts to effect some measure of biological control of ticks (Cooley 1930; Cooley and Kohls 1934; Kohls 1930; Parker and Butler 1928; Smith and Cole 1943). Earlier attempts were unsuccessful in noticeably reducing field populations of ticks. The encyrtid wasp, I. lexanus recovered from Haemaphysalis lepori.spalustris (Packard) in northeastern Oklahoma in 1978 and subsequently colonized (Bowman 1979), seems to offer potential for biological control of ticks. Research efforts have been diverted towards possible future mass releases of this parasitoid. The general laboratory biology or I. texanus has been reported (Bowman 1979), but many biological and behavioral traits that are prerequisites to successful release in the southwestern United States were unknown. Successful establishment of the parasitoid in Oklahoma is partially predicated upon its ability to survive our harsh winters in numbers large enough to maintain itself at population levels capable of suppressing tick populations. Larson and Green (I938) reported that 1. lexanus was able to overwinter in engorged or unengorged immature stages of H. lepol'ispaiustl'is located in Minnesota. Larrouse (1928) reported successful overwintering and maintenance of 1. caucurlei (= Hunl.erellus hookeri) in Massachusetts under field conditions. IxodipJwgus lexanus normally reproduces heterosexually with mating occurring soon after adult emergence from the tick. When unfed tick larvae are parasitized only a few or less often a single parasitoid will emerge (Bowman 1979). If these ~ l'iy~le!'op'n:ra: ~:nc)"rtidae ~,'CARINA: IxodidAe.,Iuurnnl article # 17if! of the Agriculturnl Experiment SUllion. Oklahoma Shlte Univer~il)", Stillwaler, 01\ i loi8. This rchclirch W1l8 sl'l'l'"rted in part by project ::; 1;02 lind Cooperalive AKrtll!'lIelll ~1:I-7~O!.I 66 from the Okl,.,homn AgricullurAI EJpcrimcnl Stntion 1I1id U.S. Dept, or Agrie. ARS. SOlllhern Hegioll. re~peetivel)". Hecci\"cd for IHlhlicAtioll 8 :\lart;h J!181i; IIccepled Zf, AugLisl 1981i. :1 Graduate He~eAr<;h Assi~tnl\l. Senior AgricullLlllllist nnd BeK,,"l~ Professor. resp,:<;ti"ely. Department of Enl"m"lo~y. OklahomA State University, Stillwater. OK
2 LOGAN el al: Irodiphagus lexonus Biology 273 tick carcasses contained unfertilized female wasps capable of parthenogenetic reproduction, other thon by arrhenatoky, it would seem likely that a larger population could be generated. The parthenogenic habits of I texanus are not known. Most of the parasitic Hymenoptera, including Encyrtidae, exhibit the arrhenotokous form of parthenogenesis (Clausen 1940, Doutt 1959). However, Ishii (1923) reported that virgin females of an encyrtid species, Microterys speciesis Ishii, produced only female progeny. Tests were devised to determine which developmental stage of the tick provided the most suitable overwintering host for 1. lexanus, and observations also were made on parthenogenesis in l. lexanus. MATERIALS AND METHODS Generalized Procedures Dermacentor variabilis (Say) was used as the parasitoid host in this study because it is one of the preferred species for I texanus in terms of host mortality and numbers of parasitoids emerging per tick (Bowman 1979). The ticks used to propagate parasitoids were maintained by procedures modified from Patrick and Hair (1975). Tick ISl'vae were fed on rabbit hosts restrained in wire cages inside rearing tubs. Adult and nymphal ticks were fed on sheep under orthopedic stockinette ceus placed over a shorn area of the skin of the animals. Large numbers of unifonnly aged ticks could be reared using these techniques. The 1. texanus colony was maintained following the procedure outlined by Bowman (1979). Groups of unengorged tick nymphs were exposed to parasitoids at a ratio of 1:10 parasitoid:tick for ca. 48 h. Exposed nymphs were then allowed to replete on sheep hosts. After tick detachment they were held in humidity chambers near 95% RH and were maintained at. 26 C with a photo-phase of 14L:10D. All tick samples retrieved and monitored far parasitism during the following observations were maintained under like conditions. lxodiphagus texanus Overwintering Behavior To detennine whether t. texanus would overwinter in central Oklahoma and if it survived which stage would be most successful, three immature tick stages, replete larvae, newly-molted nymphs and engorged nymphs of D. uariabilis, were tested. Tests were run in outdoor arenas situated in a grove of black locust, Robinia pseudoacacia, near Stillwater, Payne Co., Oklahoma. The grove had an existing canopy cover of ca. 90%. The humus layer was ca. L9 cm above a clayloam soil type. The arenas were made of 10.2 cm Diam Cresline DS@ white PVC pipe cut to 15 em lengths. The top of each arena was closed with a piece of organdy cloth secured by a rubber band. The arenas were driven 6 em into the ground leaving 9 em ahove ground. After the onset of donnancy in the ticks the top of each arena was removed to thoroughly present the ticks to the near natural environment. Three thousand unfed larvae were allowed to replete on a rabbit host On the day the engorged larvae dropped from the host, 1000 ticks per carton \vere placed in ,8.5 cm Diam paper cartons, and covered by clear Handi-Wrap@ Saran Wrap secured with a rubber band. Immediately after the replete larvae were placed in the paper carton, female parasitoids were introduced into the container at a ratio of 1 parasitoid per 10 ticks. The ticks remained exposed for 24 h to
3 2;4 J. Agric. Entomol. Vol. 2, No.3 (1985) ensure sufficient time for parasitism. The replete larvae then were separated into groups of 500 and placed in six different outdoor arenas. These ticks remained in their overwintering arenas from 10 October 1980 through retrieval on 16 March These overwintered ticks were then allowed to engorge on a sheep host and monitored for parasitoid development. In addition, within 5 d after their molting process was completed, 3,000 unfed D. variabilis nymp.,hs were placed inside paper cartons at the rate of 1,000 nymphs per carton. These ticks were exposed for 24 h to female parasitoids at a ratio of 1 parasitoid per 10 ticks. Ticks were separated into groups of 500 and on 10 October 1980 they were placed in the previously described overwintering arenas. After retrieval on 16 March 1981, the ticks were allowed to engorge on a sheep host and monitored for parasitoid development. Newly molted nymph hosts were also exposed to I. lexgnus as described above and then allowed [Q feed to replerion on a sheep host. After dropping from the host the ticks were separated into groups of 100 and immediately placed in three different outdoor arenas. A release of 300 newly exposed replete nymphs was continued on a weekly basis from 25 Sept.ember 1980 through 13 November Beginning on 20 November 1980 until 1 June 1981, samples of 10 engorged nymphs were retrieved from the arenas bi-weekly and held in II humidity chamber to more closely monitor when winter kill of parasitoids actually occuned, if at all Parthenogenesis Test Three t.housand unfed larvae were placed in paper cartons at the rate of 500 larvae per carton. The top of each carton was enclosed with clear Handi-Wrap@ Saran Wrap secured with a rubber band. Female parasitoids were introduced into each carton at a ratio of 1:10 parasitoid:tick. They were placed in a humidity chamber at ca. 95% RH and 26 c C for 24 h to allow sufficient time fol' parasitism. After exposure to parasitoids. the tick larvae were allowed to engorge on rabbit host.s and held in t.he humidity chamber for 21 d. The larvae which exhibited signs of parasitism after 21 d were placed singly in 12 X 75 mm culture tubes and held until parasitoid emergence occun ed. These isolated larvae were monitored closely during the emergence period and solitary emerged parasitoids were immediately given access to five freshly fed D. uariabijis nymphs. Host nymphs were monitored for panhenogenelic parasiloid development. RESULTS AND DISCUSSION /xodiphagus texannus Overwintering Behauior The nymphs emerging from the parasitized replete larvae and the parasitized unfed nymphs were allowed to engorge on a sheep host The number of ticks parasitized and the average number of parasitoids emerging per tick were recorded (Table I). Of 1,415 unfed nymphs which were retrieved and allowed to engorge, 153 ticks molted. The remaining 1,262 (89%) were successfully parasitized. A sample group of 100 nymphs originally parasitized as replcte larvae and 100 nymphs from the group parasitized as unfed nymphs wcre monitored for the average number of parasitoids emerging. The replete larvae group averaged Lex(lI1w; emerging per lick and the unfed nymph group yielded 15 parasitaids pel' lick.
4 LOGAN et ul: lxodiphagus lexotifls Biology 275 Table 1. Overwintering behavior of Ixodiphagus texmlus Howard in Dermacentor uariabilis (Say) ticks, Payne Co., Oklahoma, winter, Tick stage parasitized Replete Unfed Parameter larvae nymph # ticks released # ticks recovered # ticks parasitized parasitism x # parasitoids/tick These findings indicate that. I. texanus is capable of overwintering in central Oklahoma if the parasitoid is established in a natural tick population. Results obtained from newly molted nymphs that were parasitized and then allowed to feed to repletion showed that only the ticks placed in the arenas on 13 November 1980 had a large percentage of overwintering parasitoids. Availability of hosts at appropriat.e times seems to make unfed nymphs a better overwintering host than rel>!ele nymphal ticks (Sonenshine et al 1966; Atwood and Sonenshine 1967)_ ParlherlOgen.esis Test Three thousand unfed larvae were originally exposed for parasitism; 718 subsequently exhibited signs of parasitism. These host larvae were isolated and monitored. Fifty contained solitory l. texanus which, after emergence, were given access to five replete nymphs for oviposition. Of the 50 samples exposed and monitored, three contained parasitized nymphs. All of the parasitoids that emerged from these samples were males. These observations indicate that arrhenotokous reproduction may occur in l. texanus under certain conditions. REFERENCES CITED Atwood, E. L. t and D. E. Sonenshine Activit.y of t.he American dog t.ick, Dermacenlor variobilis (Acarina: Ixodidae), in relation to solar energy changes. Ann. Entomol. Soc. of Amer. 60: Bow11lnn, J. L Host suitability and laboratory biology of ixodiphagus lexallus Howard. :\1.S. Thesis. Depart.menl of Entomology, Oklahoma State University, 25 p. Clausen. C. P Entomophagolls Insects. J\ew York, NY, McGraw-Hili Book Co. Inc., pp Cooley, R. A Review of tick parasite work for 1929 find Eighth Biennial Report, It. lont SI.. Bd. of Entomol., pp Cooley, H. A., and G. M. l<ohi A summary on tick parasites. Proc. Fift.h Pac. Sci. Congr. ~~5: Doutt. R. L The biolob'y of pomsitic Hymenoptera. Ann. He\'. EntomoL 4: Ishii, T Observations all the Hymenopterolls parflsites of Ceroplast.es rubclis Mask.. with descriptions of new gclicrn lind species of the subfnmily Eflcyrlinae. Jupan Dept.. Agr. & Com. Imp. Plant Quar. Stn. Bull. 3: I(ohls. G. M A summary of porllsite liberations. Eighth Biennial Report, MOflL 51.. Bd. of Enlomal, pp Lurrouse. F.. G. A. King, and S. B. Wolbach The overwintering in 1\..lassachuselts of lxqdil)lw~us cuucureti. Science 67 (1735):
5 276 J. Agric. Entomol. Vol. 2. No.3 (1985) Larson, C. L., and R. G. Green Seasonal dist.ribution of tick parasites. J. ParasitoL 24: Parker. J, R, and W. J. Buller Tick parasite liberation in Montana during Seventh Biennial Reporl~ MonL St. Bd. of Enlomol., pp Patrick. C. D., and J. A. Hair. L975. Laboratory rearing procedures and equipment for multi-host ticks (Acarinn: Ixodidae). J. Merl. Entomol. 3: Smith, C. N., and M. M. Colc Studies of pamsiles of the American dog tick. J. Ecan. Entomol. 36: Sonenshine, D. E" E. L. Atwood. and J. T. Lamb, Jr The ecology of t.icks transmitting Rocky Mountain spotted fever in a study area in Virginia. Ann. Entornol Soc. of Amer., 59:
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