RESEARCH NOTES
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J. Parasitol., 93(6), 2007, pp. 1531–1532 䉷 American Society of Parasitologists 2007
Hyperparasitism in Amblyomma rotundatum (Acari: Ixodidae) M. B. Labruna, S. M. M. Ahid*, H. S. Soares*, and A. C. D. Suassuna*, Departamento de Medicina Veterina´ria Preventiva e Sau´de Animal, Faculdade de Medicina Veterina´ria e Zootecnia, Universidade de Sa˜o Paulo, Sa˜o Paulo, SP, 05508-270, Brazil; *Departamento de Cieˆncias Animais, Universidade Federal Rural do Semi-A´rido, Mossoro´, RN, Brazil 59625-900. e-mail:
[email protected] ABSTRACT: In the present study, we report a case of hyperparasitism in Amblyomma rotundatum. During examination of live ticks immediately after collecting them from Boa constrictor snakes held in a reptile facility in Mossoro´, RN, northeastern Brazil, 1 unengorged tick female was seen attached to the venter of a partially engorged female. The hypostome and chelicerae of the unengorged female had penetrated the integument of the partially engorged female to the level of the basis capitulli and the palps were splayed outward. To our knowledge, we present the second report of hyperparasitism for the genus Amblyomma.
The process of ticks feeding on other ticks of the same or different species is called hyperparasitism. Other names reported in the literature for this feeding process are tick cannibalism or homoparasitism (the latter is used only for conspecific ticks). Hyperparasitism has been frequently observed among immature and adult Ornithodoros species (Helmy et al., 1983; Beck et al., 1986; Oliver et al., 1986; Endris et al., 1991). In ixodid ticks, hyperparasitism seems to be relatively common for some Ixodes species, always with male ticks parasitizing females (Moorhouse, 1966; Moorhouse and Heath, 1975; Ntiamoa-Baidu, 1986). In the present study, we report a case of hyperparasitism in Amblyomma rotundatum, a Neotropical tick species with established populations extending from Florida (where it was introduced with toads) to Argentina (Oliver et al., 1993; Guglielmone et al., 2003). It feeds primarily on cold-blooded animals, mainly toads and several snakes. Although there have been at least 2 reports of the existence of the A. rotundatum male, this tick has been considered to reproduce exclusively by parthenogenesis (Oba and Schumaker, 1983; Keirans and Oliver, 1993; Labruna et al., 2005). On 11 January 2007, a sample of 85 ticks was collected from 4 Boa constrictor snakes kept in the reptile facility of the Rural Federal University of the Semi-Arido, in Mossoro´ (05⬚11⬘S, 37⬚20⬘W), northeastern Brazil. Snakes in this facility have been seen infested by all parasitic stages of A. rotundatum for at least 4 yr. During this period, ovipositing females, egg masses, and unfed ticks were observed inside cracks and
crevices of the facility several times (data not shown). Additional evidence for A. rotundatum presence within the facility is the fact that the 4 snakes sampled in the present study were born in there and had permanently remained there. Collected ticks were immediately taken alive to a nearby laboratory, held in a large Petri dish, and examined by stereomicroscopy. Ticks were identified as 81 females and 1 nymph of A. rotundatum. Within 15 min of tick removal from the snakes, a single unengorged female was seen attached to the venter (on the internal side of the right coxa II) of a partially engorged female. The hypostome and chelicerae of the unengorged female had penetrated the integument of the partially engorged female to the level of the basis capitulli, whereas the palps were splayed outward (Fig. 1). When this attached female (here referred to as a parasitic female) was lifted up without detaching it from the partially engorged female (here referred to as a parasitized female), we could see a large scar immediately below the genital opening of the parasitized female (Fig. 2). A few minutes after this examination, the parasitic female detached by itself from the parasitized female. Detachment left a wound in the integument that quickly dried, leaving a permanent scar. Hence, 2 scars were observed on the ventral side of the parasitized female, a large scar below the genital opening, and a smaller scar on the internal side of the right coxa II (Fig. 3). The small scar refers to the attachment site of the parasitic female, as shown in Figures 1 and 2. No other scars were observed on the body of the parasitized female. All ticks were preserved in alcohol, and they have been deposited in the National Tick Collection (CNC) of the Faculty of Veterinary Medicine of the University of Sa˜o Paulo (accession no. 1006). Although the small scar on the ventral side of the partially engorged female was probably the result of hyperparasitism, the second, much larger scar could be definitively attributed to hyperparasitism. The larger scar could have been the result of a much longer parasitic period (in comparison with the smaller scar) because of the presence of more abundant material that could be derived from the parasitic tick’s saliva, i.e., cement. Alternatively, the large scar could have been caused by multiple ticks, resulting in the larger lesion on the tick idiosoma. Mul-
FIGURES 1–3. Hyperparasitism in Amblyomma rotundatum. (1) General view of the parasitic female attached to the parasitized female. (2) The parasitic female was lifted up without detaching it, showing a large scar (arrow) to the right, posterior to the genital opening of the parasitized female. (3) A view of the scars on the ventral side of parasitized female after detachment of the parasitic female. Arrowhead, genital opening. Small arrow, fresh scar where the parasitic female was attached to. Large arrow, old scar. Bar ⫽ 1 mm in all figures.
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tiple scars due to hyperparasitism on a single tick specimen have been reported for several tick species (Moorhouse and Heath, 1975; NtiamoaBaidu, 1986). The literature has reported that hyperparasitism scar is typically dark-colored (Ntiamoa-Baidu, 1986). In fact, the 2 scars observed in A. rotundatum female were dark-colored when the tick was still alive (note the large scar in Fig. 2, taken when the tick was alive). However, after this female was preserved in alcohol for several weeks, the scar turned to white (Fig. 3, taken after the tick was alcohol-preserved). Among previous reports of hyperparasitism in ticks, Ixodes sp. males of various species attached to conspecific females in advanced state of engorgement (Moorhouse, 1966; Norval, 1974; Moorhouse and Heath, 1975; Ntiamoa-Baidu, 1986). Similarly, hyperparasitism among argasid ticks (mostly Ornithodoros spp.) have generally referred to unengorged ticks feeding on engorged ticks (London˜o, 1976; Helmy et al., 1983; Endris et al., 1991). To our knowledge, a previous report of hyperparasitism in Amblyomma ticks has been restricted to the study of Barber (1895), who documented a male of Amblyomma variegatum (reported as Hyalomma venustum, a current synonym of A. variegatum [Camicas et al., 1998]) attached to a conspecific engorged female in Antigua. Thereafter, hyperparasitism among metastriata ticks was reported for adults of both sexes of Hyalomma detritum (Usakov, 1961, cited by Moorhouse, 1966) and for nymphs of Hyalomma mauritanicum (Sergent, 1930); this latter taxon has been synonymized to H. detritum (Camicas et al., 1998). Hyperparasitism was reported for females of both Aponomma auruginans and Boophilus microplus; however, both reports refer to Ixodes sp. males parasitizing metastriata females, under natural and laboratory conditions, respectively (Moorhouse and Heath, 1975). Additionally, there is 1 report of a female Boophilus annulatus attached to and sucking blood from another conspecific female (Klyushkina, 1956, cited by Oliver et al., 1986). Similarly, our report also refers to a female attached to a conspecific female, although a parthenogenetic tick species. To our knowledge, we present the second report of hyperparasitism for the genus Amblyomma. It has been suggested that hyperparasitism is an efficient method by which male ticks feed, providing some biological significance for the tick life cycle (Moorhouse, 1966; Ntiamoa-Baidu, 1986). On the contrary, the significance of hyperparasitism between 2 conspecific females over a natural host (likely observed in the present study) remains unknown for the standpoint of tick biology. However, both hemolymph and blood fluids have been found in the gut of ticks that had fed by hyperparasitism on engorged ticks (London˜o, 1976). Thus, hyperparasitism may be an efficient method for horizontal transmission of tickborne agents, resulting in some significance for the maintenance of these agents in nature. In fact, laboratory tick-to-tick transmission of Dipetalonema vitae microfilariae by hyperparasitism has been reported in Ornithodoros tartakowskyi ticks (Votava et al., 1974; London˜o, 1976), as well as the transmission of Borrelia crocidurae from infected to uninfected Ornithodoros erraticus ticks during the hyperparasitism feeding process (Helmy et al., 1983). This work was supported by FAPESP (Sa˜o Paulo, Brazil) and CNPq (Brazil). LITERATURE CITED BARBER, C. A. 1895. The tick pest in the tropics. Nature 52: 197–200. BECK, A. F., K. H. HOLSCHER, AND J. F. BUTLER. 1986. Life cycle of
Ornithodoros turicata americanus (Acari: Argasidae) in the laboratory. Journal of Medical Entomology 23: 313–319. CAMICAS, J. L., J. P. HERVY, F. ADAM, AND P. C. MOREL. 1998. Les tiques du monde. Nomenclature, stades de´crits, hoˆtes, re´partition (Acarida, Ixodida). Orstom, Paris, France, 233 p. ENDRIS, R. G., T. M. HASLETT, M. J. MONAHAN, AND J. G. PHILLIPS. 1991. Laboratory biology of Ornithodoros (Alectorobius) puertoricensis (Acari: Argasidae). Journal of Medical Entomology 28: 49–62. GUGLIELMONE, A. A., A. ESTRADA-PENA, J. E. KEIRANS, AND R. G. ROBBINS. 2003. Ticks (Acari: Ixodidae) of the zoogeographic region. International Consortium on Ticks and Tick-borne Diseases (ICTTD-2), Atlanta, Georgia, 173 p. HELMY, N., G. M. KHALIL, AND H. HOOGSTRAAL. 1983. Hyperparasitism in Ornithodoros erraticus. Journal of Parasitology 69: 229–233. KEIRANS, J. E., AND J. H. OLIVER, JR. 1993. First description of the male and redescription of the immature stages of Amblyomma rotundatum (Acari: Ixodidae), a recently discovered tick in the U.S.A. Journal of Parasitology 79: 860–865. LABRUNA, M. B., F. A. TERRASSINI, AND L. M. CAMARGO. 2005. First report of the male of Amblyomma rotundatum (Acari: Ixodidae) from a field-collected host. Journal of Medical Entomology 42: 945–947. LONDON˜O, I. M. 1976. Transmission of microfilariae and infective larvae of Dipetalonema viteae (Filarioidea) among vector ticks, Ornithodoros tartakowskyi (Argasidae), and loss of microfilariae in coxal fluid. Journal of Parasitology 62: 786–788. MOORHOUSE, D. E. 1966. Observations on copulation in Ixodes holocyclus Neumann and the feeding of the male. Journal of Medical Entomology 3: 168–171. ———, AND A. C. HEATH. 1975. Parasitism of female ticks by males of the genus Ixodes. Journal of Medical Entomology 12: 571–572. NORVAL, R. A. I. 1974. Copulation and feeding in males of Ixodes pilosus Koch 1844 (Acarina: Ixodidae). Journal of the Entomological Society of South Africa 37: 129–133. NTIAMOA-BAIDU, Y. 1986. Parasitism of female Ixodes (Afrixodes) moreli (Acari: Ixodidae) by males. Journal of Medical Entomology 23: 484–488. OBA, M. S. P., AND T. T. S. SCHUMAKER. 1983. Estudo da biologia de Amblyomma rotundatum (Koch, 1844) em infestac¸o˜es experimentais de Bufo marinus (L., 1758) sob condic¸o˜es variadas de umidade relativa e de temperatura do ar. Memo´rias do Instituto Butantan 47: 195–204. OLIVER, J. H., JR., M. P. HAYES, J. E. KEIRANS, AND D. R. LAVENDER. 1993. Establishment of the foreign partheonogenetic tick Amblyomma rotundatum (Acari: Ixodidae) in Florida. Journal of Parasitology 79: 786–790. ———, S. MCKEEVER, AND J. M. POUND. 1986. Parasitism of larval Ixodes ticks by chigger mites and fed female Ornithodoros ticks by Ornithodoros males. Journal of Parasitology 72: 811–812. SERGENT, A. 1930. Presentation d’une nymphe de tique parasitant une autre nymphe de la meˆme espe`ce. Bulletin de la Societe d’Histoire Naturelle de l’Afrique du Nord. 21: 195. VOTAVA, C. L., F. C. RABALAIS, AND D. C. ASHLEY. 1974. Transmission of Dipetalonema viteae by hyperparasitism in Ornithodorus tartakovskyi. Journal of Parasitology 60: 479.
