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Ramos, R.A.N.; De Macedo, L.O.; Bezerra-Santos, M.A.; De Carvalho, G.A.; Verocai, G.G.; Otranto, D. Biology of Ixodiphagus spp. and Geographic Distribution. Encyclopedia. Available online: https://encyclopedia.pub/entry/44382 (accessed on 30 June 2024).
Ramos RAN, De Macedo LO, Bezerra-Santos MA, De Carvalho GA, Verocai GG, Otranto D. Biology of Ixodiphagus spp. and Geographic Distribution. Encyclopedia. Available at: https://encyclopedia.pub/entry/44382. Accessed June 30, 2024.
Ramos, Rafael Antonio Nascimento, Lucia Oliveira De Macedo, Marcos Antônio Bezerra-Santos, Gílcia Aparecida De Carvalho, Guilherme Gomes Verocai, Domenico Otranto. "Biology of Ixodiphagus spp. and Geographic Distribution" Encyclopedia, https://encyclopedia.pub/entry/44382 (accessed June 30, 2024).
Ramos, R.A.N., De Macedo, L.O., Bezerra-Santos, M.A., De Carvalho, G.A., Verocai, G.G., & Otranto, D. (2023, May 16). Biology of Ixodiphagus spp. and Geographic Distribution. In Encyclopedia. https://encyclopedia.pub/entry/44382
Ramos, Rafael Antonio Nascimento, et al. "Biology of Ixodiphagus spp. and Geographic Distribution." Encyclopedia. Web. 16 May, 2023.
Biology of Ixodiphagus spp. and Geographic Distribution
Edit
This entry is adapted from the peer-reviewed paper 10.3390/pathogens12050676

Species within the genus Ixodiphagus (Hymenoptera: Encyrtidae) are natural parasitoid wasps of ticks (Acari: Ixodida), which were first described more than a century ago, in Haemaphysalis leporispalustris from Texas, United States (USA).

Ixodiphagus hookeri biological control ixodid argasid

1. Introduction

Species within the genus Ixodiphagus (Hymenoptera: Encyrtidae) are natural parasitoid wasps of ticks (Acari: Ixodida) [1], which were first described more than a century ago, in Haemaphysalis leporispalustris from Texas, United States (USA) [2]. The etymology of the genus name Ixodiphagus (from Greek ixod = tick and phage = eater) alludes to its parasitoid behavior. After its first description, other species of “tick eaters” within this genus were formally described worldwide [3][4][5][6].
Currently, at least ten species of these parasitoids are considered valid, namely Ixodiphagus texanus Howard, 1907; Ixodiphagus hookeri Howard, 1908; Ixodiphagus mysorensis Mani, 1941; Ixodiphagus hirtus Nikolskava, 1950; Ixodiphagus theilerae Fielder, 1953; Ixodiphagus biroi Erdos, 1956; Ixodiphagus sagarensis Geevarghese, 1977; Ixodiphagus taiaroaensis Heath and Cane, 2010; Ixodiphagus sureshani Hayat and Islam, 2011; and Ixodiphagus aethes Hayat and Veenakumari, 2015. These insects are small, generally measuring less than 1 cm in length, blackish in color, and exhibiting the typical appearance of members of the superfamily Chalcidoidea, and display similar biological and ecological features [7].
Despite being known for over a century, many knowledge gaps remain about the biology of these parasitoid wasps, with most information limited to I. hookeri [5][8]. The life cycle of these wasps starts when gravid females lay eggs inside the tick’s body. After an incubation period, the larvae hatch and feed on the internal content of the tick [7]. Approximately 30–57 days after oviposition, new adult male and female wasps emerge from the dead tick, mating and continuing their life cycle [9]. Based on this life cycle, the use of Ixodiphagus spp. as an agent for biological control of ticks has inspired the interest of the scientific community [10]. In addition, populations of I. hookeri may have different developmental times, parasitism rates, and host preferences according to the geographical area of occurrence [10], which may explain the failure, or the limited efficacy, of these wasps in the control of ticks in field studies [11][12].

2. Biology of Ixodiphagus spp. and Geographic Distribution

Information on the biology of Ixodiphagus species is insufficient and mainly limited to experimental studies [10]. The entire life cycle ranges from 28 to 70 days, and starts when female wasps lay eggs into ticks through the penetration of their ovipositor into the tick’s body (Figure 1). After hatching, larvae (Figure 2) develop inside the tick. While no information is available about the pupal stage, adult wasps emerge from their tick hosts through a hole at the posterior end, with mating occurring soon after the emergence [9]. There have been no studies assessing the number of Ixodiphagus eggs released by females in natural conditions. However, based on experimental studies, it is estimated that during the entire life span, I. hookeri and I. texanus lay about 120 and 200 eggs, respectively [13][14].
Pathogens 12 00676 g001
Figure 1. Life cycle of Ixodiphagus spp.
Pathogens 12 00676 g002
Figure 2. Ixodiphagus sp. larva in a Rhipicephalus sanguineus s.l. tick (Scale bar = 200 μm).
Information about the preference for certain tick developmental stage remains unclear. For instance, some researchers reported that larvae of Ixodiphagus are mostly detected in tick nymphs and adults when the latter are engorged, suggesting that parasitism is likely to occur in blood-fed ticks rather than in unfed ones [15]. However, an experimental study demonstrated that unfed nymphs of I. ricinus were more parasitized than other stages [10]. This observation was later confirmed with the finding of I. hookeri DNA in unfed I. ricinus nymphs collected from the environment [3]. Furthermore, it has been demonstrated that unfed ticks can be collected from vegetation, and after feeding them on laboratory animals (e.g., mice) the parasitoids emerge [16]. In their searching for ticks, Ixodiphagus spp. females may be driven by chemical attractants produced by vertebrate animals hosting ticks [10], as well as by tick feces [17]. In fact, some experiments have demonstrated that I. hookeri females appear to be attracted by odors produced by the haircoat of roe deer (Capreolus capreolus) and wild boar (Sus scrofa) [10] but not from those of mice, cattle, and rabbits [10]. This mechanism of attraction is crucial for facilitating the encounter of Ixodiphagus spp. with their preferred tick species [8], increasing the chances of completion of their lifecycle. Despite this observation, this is most likely not the general scenario in nature. It is believed that in most cases, hosts are attractive for ticks, in which eggs of the parasitoids are already present. The development of wasp larvae is directly dependent on nutrients contained in the engorged blood meal of the ticks; hence it is unlikely that Ixodiphagus larvae could develop in unfed ticks due to the depletion of nutrients [18]. This translates into a correlation between the occurrence of Ixodiphagus larvae, tick density, and infestation rate in vertebrate hosts [8][19]. For example, in I. scapularis nymphs the infestation of wasp parasitoids occurred only in individuals parasitizing white-tailed deer (Odocoileus virginianus) in the northeastern USA, and in areas with deer population density of 13–20 animals per km2 or higher [19]. In addition, no association was observed between the occurrence of wasps and I. ricinus infesting rodents in northern Europe [8], suggesting that the species of vertebrate host is crucial for the behavior of Ixodiphagus spp.. Despite the lack of an association between wasps and ticks of rodents, it is known that in laboratory conditions parasitoids develop and emerge from ticks that feed on mice. The dynamic of Ixodiphagus has been poorly assessed in field conditions. Based on the few studies conducted so far, adults fly for a short period of time. In Germany, adult wasps were found during 3–5 weeks, in late summer/early fall [10]. This seasonal activity overlaps with a high density and feeding activity of I. ricinus immature stages in the same area, which incidentally occurs when vertebrate hosts are also more abundant. For example, it has been demonstrated that wasps from ticks fed before July have a shorter developmental time compared with those from ticks engorged later on [10]. This finding is similar to those previously observed in field conditions in Texas (USA), where wasps required a development time of 25 and 33 days for ticks fed in May and September, respectively [9].
In southern Italy, the majority of ticks that tested positive for I. hookeri (i.e., 92%) were collected during fall–winter (from October to March) [3], when I. ricinus peaked [20]. Overall, the detection in ticks is related to developmental time of Ixodiphagus and to the synchronization with tick development [10]. Curiously, non-embryonated eggs of I. hookeri are able to survive over winter inside unfed nymphs of I. ricinus [21] and I. scapularis [6][15]. From a biological perspective, this characteristic allows wasp populations to survive through different seasons in spite of unfavorable climate conditions (e.g., extreme cold).
The molecular detection of Wolbachia endosymbionts in I. hookeri [22] suggests that it could be the reason for the presence of Wolbachia pipientis in I. ricinus [23], with a role in their parthenogenesis (i.e., development from unfertilized eggs). This is demonstrated in other hymenopteran species (e.g., Encarsia pergandiella) [24]. Despite the suggested parthenogenesis for Ixodiphagus [14], the potential involvement of Wolbachia has never been demonstrated. Recently, the assessment of the microbiota in I. ricinus in high-throughput sequencing revealed the presence of a wide plethora of microorganisms, including I. hookeri and Wolbachia [25]. These multiple interactions among microorganisms in I. ricinus may affect a wasp population, influencing differences in its biology observed in different tick populations worldwide [10][26][27]. Ixodiphagus spp. have been widely reported in various species of ixodid ticks, with a broad distribution across all five inhabited continents [4][28][29], but more commonly reported from Europe and the US [3][6][19]. In fact, several hard tick species within the genera Amblyomma, Dermacentor, Haemaphysalis, Hyalomma, Ixodes, and Rhipicephalus, in various life stages, have been found parasitized by Ixodiphagus wasps (Table 1). So far, the only argasid soft tick found parasitized by an Ixodiphagus species (I. mysorensis) was Ornithodoros sp. [30].
Table 1. Distribution of Ixodiphagus spp. parasitizing different tick species in the world.
Parasitoid Tick Tick Life Stage Country Reference
I. texanus H. leporispalustris Nymph United States [2]
I. hookeri R. sanguineus Nymph United States [31]
I. hookeri R. sanguineus, D. marginatus Nymph United States [9]
I. hookeri I. ricinus Nymph France [32]
I. hookeri H. concinna, D. reticulatus, D. venustus,
R. sanguineus		 NA France [33]
I. hookeri R. sanguineus Nymph Brazil [34]
I. hookeri R. sanguineus NA India [35]
I. hookeri D. nitens NA United States [36]
I. hookeri D. variabilis NA United States [11]
I. hookeri H. aegyptium NA South Africa [37]
I. hookeri R. sanguineus Nymph Nigeria [38]
I. hookeri I. cookei Nymph United States [39]
I. hookeri R. sanguineus NA United States [40]
I. texanus H. leporispalustris Nymph United States [41]
I. hookeri R. sanguineus Nymph United States [42]
I. mysorensis Ornithodorus sp. NA India [30]
I. texanus I. persulcatus Nymph Russia [43]
I. hookeri I. ricinus Nymph Czech Republic/Slovakia (Czechoslovakia) [44]
I. hookeri R. sanguineus Nymph Kenya [45]
I. hookeri R. sanguineus Nymph Africa [46]
Ixodiphagus sp. H. bancrofti, H. bremneri, I. holocyclus, I. tasmani NA Australia [47]
I. hookeri R. sanguineus NA Indonesia [48]
I. hookeri R. sanguineus Nymph Malaysia [49]
I. texanus H. leporispalustris Larva, Nymph Canada [50]
I. hookeri I. dammini Nymph United States [51]
I. hookeri H. punctata Nymph Spain [52]
I. hookeri A. variegatum Nymph Kenya [53]
I. hookeri I. ricinus NA France [54]
I. texanus I. dammini Nymph United States [55]
I. hookeri R. sanguineus Nymph Mexico [56]
I. hookeri I. scapularis Nymph United States [57]
I. hookeri I. scapularis Nymph United States [15]
I. hookeri A. variegatum Nymph Kenya [58]
I. hookeri I. scapularis Nymph United States [19]
I. hookeri R. sanguineus Nymph Venezuela [59]
I. hookeri A. variegatum Nymph Kenya [27]
I.hookeri H. concinna Nymph Slovakia [16]
I. taiaroaensis I. uriae, I. eudyptidis Larva, Nymph New Zealand [60]
I. hookeri I. ricinus Nymph Germany [10]
I. hookeri I. ricinus Nymph Netherlands [22]
I. hookeri, I. texanus R. sanguineus, Amblyomma sp. Nymph Brazil [61]
I. hookeri I. ricinus Nymph France [22]
I. hookeri, I. texanus R. sanguineus Nymph Panama [62]
I. hookeri I. ricinus Nymph, Adult Italy [3]
I. hookeri I. ricinus Nymph Slovakia [63]
Ixodiphagus sp. R. sanguineus Nymph, Adult Brazil [4]
I. hookeri I. ricinus Nymph Finland [5]
I. hookeri R. sanguineus Nymph United States [64]
I. hookeri R. microplus, I. persulcatus,
D. silvarum, H. concinna		 Adult Côte d’Ivoire, Senegal, Russia [29]
I. hookeri I. ricinus Larva, Nymph Netherlands [8]
I. hookeri I. ricinus, H. concinna Nymph Slovakia [1]
I. hookeri I. ricinus Nymph France [25]
I. hookeri I. ricinus Nymph United Kingdom [65]
I. hookeri A. nodosum Nymph, Adult Brazil [66]
I. hookeri I. ricinus Nymph Hungary [6]
NA: Not available.

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Subjects: Parasitology
Contributors MDPI registered users' name will be linked to their SciProfiles pages. To register with us, please refer to https://encyclopedia.pub/register :
Rafael Antonio Nascimento Ramos
,
Lucia Oliveira de Macedo
,
Marcos Antônio Bezerra-Santos
,
Gílcia Aparecida de Carvalho
,
Guilherme Gomes Verocai
,
Domenico Otranto
View Times: 438
Revisions: 2 times (View History)
Update Date: 17 May 2023
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