Lice, Flies, Mites, and Ticks on Raptors (Accipitriformes, Falconiformes and Strigiformes) in Rescue Centers in Central Italy

This study aims to assess the occurrence of external arthropods on deceased raptors in rescue centers in Tuscany, central Italy. The examined diurnal raptors include 17 common buzzards (Buteo buteo), two European honey buzzards (Pernis apivorus), seven sparrowhawks (Accipiter nisus), six common kestrels (Falco tinnunculus), a western osprey (Pandion haliaetus), and a peregrine falcon (Falco peregrinus). Nocturnal raptors included seven barn owls (Tyto alba), ten tawny owls (Strix aluco), 22 little owls (Athene noctua) and two scops owls (Otus scops). The skin and the feathers of each animal were examined, and arthropods were collected, fixed, and microscopically identified. In 48 out of the 75 examined birds (64%), at least a single arthropod species was found. Identified arthropods included chewing lice (Degeeriella fulva, D. rufa, Colpocephalum turbinatum, C. apivorus, Nosopon lucidum, N. clayae, Craspedorrhyncus platystomus, Laemobothrion tinnunculi, Kurodaia subpachygaster, Strigiphilus cursitans), hippoboscid flies (Ornithomya avicularia), chigger and feather mites (Kramerella lunulata, K. lyra, Kramerella sp., Glaucalges attenuatus, Hieracolichus nisi, Hieracolichus sp., Neotrombicula autumnalis) and ticks (Haemaphysalis sp.). Most of the identified mite, fly and tick species are the first records in raptors in Italy. Moreover, this study presents the first record of Hieracolichus sp. and N. autumnalis mites in P. haliaetus and F. tinnunculus, respectively.

This study aimed to assess the occurrence of arthropods associated with diurnal and nocturnal deceased raptors in wildlife rescue centers in different areas of Tuscany (central Italy).

Results and Discussion
In the geographical area considered in the present study [20], and in Italy [21,22], the buzzard (Buteo buteo) and the little owl (Athene noctua) are included among the prevalent diurnal and nocturnal raptor species, respectively. This could explain the high number of deceased specimens of these two raptor species examined in this study.
This study showed a high prevalence of external arthropods in examined raptors, as 48 out of the 75 examined birds (64%) scored positive for at least one arthropod species. Out of the ten raptor species examined, eight species were found to be positive for the presence of external arthropods. Only the two scops owls (Otus scops) and the single peregrine (Falco peregrinus) scored negatively. However, the found prevalence may be underestimated considering that several ectoparasite species may leave their deceased bird hosts.
In most positive birds, intensity was high (Table 1), especially in the case of lice and feather mites. More specifically, a high intensity of at least a single identified louse and/or mite species was observed in each positive diurnal and nocturnal raptor (Table 1). Although lesions associated with some arthropod species identified in this study were previously described in raptors [1,7], no macroscopic lesions were found in the skin or in the feathers of birds found positive for lice and feather mites.
On another buzzard, adults of the hematophagous hippoboscid fly O. avicularia, were identified (Table 1; Figure 1(11)). O. avicularia has been reported to infest a high number of bird species, including raptors [25], in which it may cause severe anemia, especially in younger subjects [26]. Moreover, this fly species can be the vector of several pathogens of raptors, including Haemoproteus spp. and Trypanosoma spp. [25,27,28]. Interestingly, hippoboscid flies may act as phoretic hosts for several Degeeriella species that can be transported to new bird hosts [29].
A high number of N. autumnalis larvae were identified on a kestrel (F. tinnunculus) and in the bag used to transport this animal (Table 1; Figure 2(1)). In birds, larvae of Neotrombicula spp. mites can be found mainly between the keel of the sternum and the cloaca or on the skin of the wings [30,31], as in the kestrel that scored positive in this study. After about 2-5 days from the beginning of the infestation, larvae leave the birds to reach the ground and molt to nymphs [30]. In heavily infested birds, parasitic larvae of N. autumnalis may cause dermatitis and intense pruritus, starvation, self-induced lesions, and secondary bacterial infections [30,31]. However, no lesions were observed in the N. autumnalis-infested kestrel in this study.
In Italy, parasitic larvae of N. autumnalis generally infest birds during the summer [30]. However, in this study the positive kestrel was examined in January. Interestingly, in the Czech Republic some chigger mites (Ascoschoengastia latyshevi) were also rather frequently found on birds, even during winter months [32].
Eight ticks were counted in another kestrel and identified as larvae of Haemaphysalis sp. (Table 1; Figure 2(12)). Among species of the genus Haemaphysalis, larvae and nymphs of the species Haemaphysalis punctata are commonly found on birds, especially passerines but also other birds in the Apennine areas of Italy, as Tuscany [16,33].
Haemaphysalis punctata is a three-host tick known to be from Europe, northwestern Africa, and southwestern Asia [34]. Haemaphysalis punctata larvae and nymphs may infest birds [35,36]. In Europe, H. punctata has mainly a Mediterranean distribution [37]. However, migrating birds are considered to play an important role in introducing this tick species to other European areas [38,39]. Under conditions of high parasite load, this tick may be responsible for anemia, reduced growth, and weight loss and may be the vector of several bacterial and viral pathogens in infested birds [40].
Raptors were wounded or diseased and died from a few hours (40/75) to ten days after their arrival in wildlife rescue centers located in different areas of Tuscany (central Italy), including the districts of Florence (43 •  The examined birds had not been treated with antiparasitic drugs and were singlecaged. In most cases (44/75 birds), deceased birds were placed in clean bags, refrigerated, and transported to the laboratory soon after their death. In other cases, birds were placed in a bag and refrigerated about 24-48 h after the death. The skin and the feathers of each animal and the respective bags were macroscopically inspected, and the feathers were also microscopically observed under a stereomicroscope. Arthropods were collected by means of needles, fine brushes, or tweezers, counted, and fixed in 70% ethanol. Collected and fixed arthropods were mounted in Hoyer medium and microscopically examined under an optical or a stereomicroscope equipped with an ocular micrometer, and species/genus identification was based on morphological and metrical features.
The overall prevalence was calculated as the number of birds among those examined that were found to be positive with one or more individual of at least a single external arthropod. The prevalence of each arthropod species in each bird species was also calculated. Furthermore, concurrent arthropod species found in a single bird host and the intensity of infestation of each arthropod species in a single bird host were also evaluated [43]. Intensity was considered high when the number of each arthropod species counted in a bird host was higher than 100. However, a mean number of 50 mites per feather upon examination of at least 15 feathers was considered as indicative of high intensity in the case of feather mites [44,45].

Conclusions
External arthropods identified in this survey were previously reported in examined raptor species in different areas worldwide [1,2,5,8,25,[46][47][48][49]61]. However, most of the mite, fly, and tick species identified in this study are the first record in raptors in Italy. Moreover, this study is the first report of Hieracolichus sp. in the osprey (P. haliaetus) and of N. autumnalis in the kestrel (F. tinnunculus).