ECOLOGY AND BEHAVIOR
Parasitism by Ixodiphagus Wasps (Hymenoptera: Encyrtidae) in Rhipicephalus sanguineus and Amblyomma Ticks (Acari: Ixodidae) in Three Regions of Brazil ´ NIOR,1 CLA´UDIO G. SILVA,1 ALBERTO J. O. LOPES,1 JOSE´ R. S. NASCIMENTO–JU ˆANGELO P. PRADO,2 MARCELO B. LABRUNA,3 AND LIVIO M. COSTA–JU ´ NIOR1,4
J. Econ. Entomol. 105(6): 1979Ð1981 (2012); DOI: http://dx.doi.org/10.1603/EC12012
ABSTRACT Hymenopteran parasitoids have been shown to be of potential value in tick biocontrol. Tick parasitoids has been reported only once in Brazil, over 95 yr ago when Ixodiphagus hookeri (Howard) was reported parasitizing Rhipicephalus sanguineus (Latreille) nymphs in Rio de Janeiro. Herein, we report the occurrence of Ixodiphagus spp. in ticks from three different regions of Brazil. In the state of Maranha˜o, in northeastern Brazil, parasitoids were detected in R. sanguineus nymphs on three occasions, during August 2009 and September 2010 (dry season), and January 2011 (rainy season). All parasitoids found in northeastern Brazil were identiÞed as I. hookeri. In the state of Mato Grosso do Sul (westÐ central Brazil), one Amblyomma sp. engorged nymph was shown to be parasitized by I. hookeri. In the state of Rondoˆ nia (northern Brazil), one Amblyomma sp. engorged nymph was parasitized by Ixodiphagus texanus (Howard). Because Ixodiphagus spp. are present in ecologically distinct and geographically distant areas of Brazil, they are of potential use for biocontrol in the country. KEY WORDS Ixodiphagus, Rhipicephalus sanguineus, Amblyomma, tick, biological control
The development of tick resistance to acaricides, and our awareness that chemicals are harmful to environment, have increased our need for alternative control strategies, such as habitat modiÞcation, use of pheromones and hormones, improvement of host resistance, and biological control. Ticks possess a number of natural enemies, namely viruses, bacteria, fungi, protozoa, nematodes, other arthropods, amphibians, reptiles, birds, and mammals (Samish and Rehacek 1999, Samish et al. 2004). This represents a signiÞcant arsenal for the selection of species for potential use as efÞcient biocontrol agents (Samish and Rehacek 1999). However, only a few species have been evaluated as tick biocontrol agents (Samish et al. 2004). Parasitoids are widely used for biological control of arthropod pests of plants, for which two thirds of cases of success were achieved through use of parasitic Hymenoptera (De Bach and Rosen 1991). Among ticks, eight hymenopteran parasitoid species of the genus Ixodiphagus have been reported. In addition, inundative release of these parasitoids has been shown to be of potential value in tick biocontrol (Hu et al. 1998, Knipling and Steelman 2000, Samish et al. 2004, 1 Centro de Cie ˆ ncias Agra´rias e Ambientais, Universidade Federal do Maranha˜oÐUFMA, Chapadinha, MA, Brazil. 2 Departamento de Parasitologia, Universidade Estadual de CampinasÐUNICAMP, Campinas, SP, Brazil. 3 Faculdade de Medicina Veterina ´ria e Zootecnia, Universidade de Sa˜o PauloÐUSP, Sa˜o Paulo, SP, Brazil. 4 Corresponding author, e-mail:
[email protected].
Heath and Cane 2010). In fact, successful rearing of Ixodiphagus hookeri (Howard) under laboratory conditions led to several attempted mass releases of this parasitoid for tick control during the Þrst half of the 20th century in different regions of the United States, the former Soviet Union (reviewed by Hu et al. 1998), and more recently in Kenya (Mwangi et al. 1997). While earlier attempts were apparently unsuccessful in noticeably reducing tick populations, a signiÞcant reduction of tick numbers was observed in the Þeld trial in Kenya. These Þndings provided new insights into how this wasp species could be used strategically for tick control (Hu et al. 1998). Tick parasitoids have been previously noted only once in Brazil, over 95 yr ago when I. hookeri was reported parasitizing Rhipicephalus sanguineus (Latreille) nymphs in Rio de Janeiro (CostaÐLima 1915). Herein, we report the occurrence of Ixodiphagus spp. in ticks from three different regions of Brazil. Materials and Methods Engorged nymphs of R. sanguineus were collected from naturally infested domestic dogs and from the walls of kennels during both dry and rainy seasons of 2009 (n ⫽ 124), 2010 (n ⫽ 89), and 2011 (n ⫽ 152), respectively, at the rural area of Chapadinha Municipality (03⬚ 44⬘ S; 43⬚ 21⬘ W). The elevation at this site is around 105 m and it is in the state of Maranha˜o, Northeastern Brazil (Fig. 1), within a transition area
0022-0493/12/1979Ð1981$04.00/0 䉷 2012 Entomological Society of America
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JOURNAL OF ECONOMIC ENTOMOLOGY
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formed under a stereomicroscope according to Howard (1908), Gahan (1934), and Noyes (1980).
Results and Discussion
Fig. 1. Location (●) and distance among the three cities where ticks were found infested with Ixodiphagus spp. in Brazil. Prior record of Costa-Lima (1915) also shown ([*]).
from pre-Amazon forest to vegetation typical of the Northeast (Cerrado and Caatinga biomes). The weather is tropically hot and semiarid, with maximum temperatures averaging 35⬚C; depending on the season the heat index reaches 40⬚C. The average annual rainfall in the region of Chapadinha is ⬇1,800 mm, concentrated between January and June. Engorged nymphs were taken to the laboratory, where they were held in petri dish at 27 ⫾ 1⬚C and relative humidity ⬎85%. Three engorged nymphs of Amblyomma sp. were collected from a naturally infested jaguar (Panthera onca L.) during the dry season of 2000 (June) at Anaurilaˆndia Municipality (22⬚ 11⬘ S; 52⬚ 42⬘ W, elevation around 300 m), state of Mato Grosso do Sul, west central Brazil (Fig. 1), within the Cerrado biome. The weather there is subtropical, characterized by a rainy and warm summer, and a dry and cool winter. The annual rainfall is around 1,500 mm, mostly from October to March. January is the warmest month, with mean maxima of 34⬚C; July experiences the coolest temperatures, with mean maxima around 25⬚C. Engorged nymphs were taken to the laboratory, where they were held as above. One engorged nymph of Amblyomma sp. was collected from a naturally infested domestic dog at Monte Negro Municipality (10⬚ 17⬘ S; 63⬚ 19⬘ W, elevation around 200 m), state of Rondoˆ nia, northern Brazil (Fig. 1) within the Amazon biome. The weather is tropical, characterized by high rainfall averaging 2,000 mm annually; there is a moderate drought period from April through October. Mean temperature ranges from 25 to 29⬚C and the relative humidity is 70 Ð 80% throughout the year. Engorged nymphs were taken to the laboratory and held as above. After incubation for 15 d, parasitoids found in the vials were removed and preserved in 70% ethanol. IdentiÞcation was per-
In the state of Maranha˜o (northeastern Brazil), parasitoids were detected in R. sanguineus nymphs on three occasions. During August 2009 (dry season), wasps emerged from 32 engorged nymphs (25.8%); during September of 2010 (dry season), wasps emerged from 47 nymphs (52.8%); and during January 2011 (rainy season), wasps emerged from 54 nymphs (35.5%). Emerged adults were all identiÞed as I. hookeri. From the three Amblyomma engorged nymphs collected from a jaguar in the state of Mato Grosso do Sul (west central Brazil), two molted to adults of Amblyomma cajennense (F.), whereas the third one died because of the presence of parasitoid. In total, 12 chalcidoids wasps, identiÞed as I. hookeri, emerged from this nymph, who had the same morphotype of the other two nymphs. The single Amblyomma engorged nymph collected from a dog in the state of Rondoˆ nia (northern Brazil) died because of the presence of parasitoids. In total, seven chalcidoids wasps, identiÞed as Ixodiphagus texanus (Howard), emerged from this nymph. In all cases, infested nymphs possessed one hole in the posterior portion of the idiosoma, from which adult wasps emerged. Ixodiphagus parasitoids have been reported in ticks of the genera Amblyomma, Dermacentor, Haemaphysalis, Hyalomma, Ixodes, Ornithodoros, and Rhipicephalus, always with mortality of tick hosts (Hu et al. 1998). Here we describe I. texanus and I. hookeri parasitizing the genera Amblyomma and/or Rhipicephalus, in Brazil. The present records, plus a previous report of I. hookeri parasitizing R. sanguineus nymphs in Rio de Janeiro, southeastern Brazil (CostaÐLima 1915), suggest that Ixodiphagus parasitoids are widespread in Brazil, with at least four records encompassing the northern, northeastern, centralÐwestern, and southeastern regions of the country (Fig. 1). Ixodiphagus spp. are potentially important natural enemies of ticks. Successful biocontrol of ticks requires substantial research effort on ecology and behavior (Samish et al. 2004) and local adaptation acclimation to weather by these parasitoids can be a factor (Larousse et al. 1928). Herein, we show that Ixodiphagus are present in ecologically distinct and geographically distant areas of Brazil. Indeed, they merit further study in Brazil to further quantify host range, natural impact, and potential for manipulation to improve biological control.
Acknowledgments The authors thank CNPq (The Brazilian National Council for ScientiÞc and Technological Development) for fellowship to L.M.C-J. and M.B.L., and FAPEMA (Maranha˜o State Research Foundation).
December 2012
LOPES ET AL.: PARASITISM BY IXODIPHAGUS WASPS IN TICKS IN BRAZIL References Cited
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