Efficient Transovarial Transmission of Babesia Spp. in Rhipicephalus microplus Ticks Fed on Water Buffalo (Bubalus bubalis)

Abstract

Water buffaloes can be infected by tick-borne pathogens (TBPs) in endemic areas where cattle and buffalo coexist. Among TBPs affecting buffaloes is the Apicomplexan hemoparasites Babesia bovis and B. bigemina, transmitted by Rhipicephalus microplus ticks. However, little empirical evidence exists on whether buffalo can support TBPs’ infection and transmission. A cohort study was designed to measure the infestation levels of R. microplus in buffaloes as well as the ability of buffalo-fed ticks to transmit B. bovis and B. bigemina to their offspring. Tick infestation of different life stages was quantified in cattle and buffalo kept in field conditions in western Cuba. Engorged adult female ticks were allowed to lay eggs in controlled conditions of humidity and temperature, and reproductive parameters were measured and analyzed. Hosts and tick larvae were tested for the presence of Babesia spp. using species-specific qPCR assays. Tick infestation was not observed in adult buffaloes. However, buffalo and cattle calves were equally infested, although the larval survival rate was higher in cattle calves than in buffalo calves. All larval pools (31) obtained from the adult female ticks were positive for B. bovis, whereas only 68% (21/31) was positive for B. bigemina. Among the 10 larval pools negative for B. bigemina, three proceeded from adult females fed on Babesia-negative buffaloes. The other seven pools were from Babesia-positive animals, three from cattle and four from buffalo calves. Babesia infection levels in tick larvae, quantified by qPCR, were similar in female ticks fed on buffalo and bovine calves. We conclude that water buffalo can sustain tick vector populations and support Babesia infection in levels high enough as to be infective for ticks. Our results also validated the hypothesis that adult female ticks fed on buffalo can transmit the pathogens B. bovis and B. bigemina to their offspring. Nevertheless, further laboratory studies are needed to address the question of whether the transovarial transmission of Babesia occurs in the following settings: (1) When adult females are infected previous to the feeding on the buffalo or/and (2) when the adult females acquire the infection while feeding on the buffalo.

Challenges in Tick-Borne Pathogen Detection: The Case for Babesia spp. Identification in the Tick Vector

“…Despite ticks being found only in calves (80%) and adult buffalo not showing tick infestation, the reproductive performance of female ticks was similar in those obtained from water buffalo calves than those from cattle calves. Additionally, a similar Babesia positivity was found in the progeny of female ticks fed in cattle calves and water buffalo calves, with a higher presence of B. bovis in ticks as compared to B. bigemina [50].…”

Ticks and Tick-Borne Diseases in Cuba, Half a Century of Scientific Research

“…Interestingly, the infestation by R. microplus tick is scarce in adult buffaloes, even when these animals are reared close to bovines. However, the prevalence of ticks in infested buffalo calves was similar to that of adult and calf cattle [ 69 , 70 ]. It was also observed that the tick burden in buffalo calves was higher when raised in immediate proximity to cattle herds, although the larval survival rate was higher in cattle calves than in buffalo calves [ 70 ].…”

“…The buffaloes are also infested by R. microplus [ 69 ] and A. mixtum [ 68 ] in the Cuban grassland. The buffalo calves are most affected by ticks, registering parasitic loads similar to cattle [ 69 , 70 ]. Furthermore, although the survival rate of R. microplus larvae on buffaloes is lower than on cattle, engorged females fed on buffaloes have a reproductive performance similar to ticks fed on cattle [ 70 ].…”

“…Remarkably, A. marginale strains infecting buffalo were genetically related to those infecting cattle in the same region [ 100 ], suggesting circulation of this pathogen between buffalo and cattle. Furthermore, the transovarial transmission of B. bovis and B. bigemina in R. microplus engorged female ticks fed on buffalo suggests that this host species can support the life cycle of some TBPs in Cuba [ 70 ]. Nevertheless, the reservoir capacity of buffaloes for CTF pathogens, and the role of these animals in the epidemiological process of CTF disease across the country, should be further evaluated.…”

“…The multiplex qPCR described by Díaz-Sánchez et al [ 14 ] proved to be a rapid, specific and cost-effective means for the simultaneous detection of A. marginale and T. annulata , confirming a high prevalence of A. marginale infection of carrier cattle in Cuba. On the other hand, a SYBR Green-based real-time PCR system developed for the detection and quantification of B. bovis and B. bigemina [ 101 ] detected low parasitemia levels in carrier buffaloes, and R. microplus tick larvae [ 70 ]. Likewise, a TaqMan-based real-time PCR assay enabled exploration of the reservoir competence of water buffalo for A. marginale in endemic areas of Cuba [ 100 ].…”