Next Article in Journal
O-Serogroups and Pathovirotypes of Escherichia coli Isolated from Post-Weaning Piglets Showing Diarrhoea and/or Oedema in South Korea
Previous Article in Journal
Cat and/or Dog Ownership, Cardiovascular Disease, and Obesity: A Systematic Review
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Veterinary Sciences
Volume 8
Issue 12
10.3390/vetsci8120334
vetsci-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Potential Role of Avian Populations in the Epidemiology of Rickettsia spp. and Babesia spp.

by
Valentina Virginia Ebani
1,2,3,* and
Francesca Mancianti
1,3
1
Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124 Pisa, Italy
2
Centre for Climate Change Impact, University of Pisa, Via del Borghetto 80, 56124 Pisa, Italy
3
Interdepartmental Research Center “Nutraceuticals and Food for Health”, University of Pisa, Via del Borghetto 80, 56124 Pisa, Italy
*
Author to whom correspondence should be addressed.
Vet. Sci. 2021, 8(12), 334; https://doi.org/10.3390/vetsci8120334
Submission received: 7 November 2021 / Revised: 15 December 2021 / Accepted: 16 December 2021 / Published: 17 December 2021
Versions Notes

Abstract

:
Birds often are carriers of hard and/or soft ticks harboring pathogens of humans and veterinary concern. Migratory avian species, which cover long distance by their flight, may deeply influence the ticks’ distribution worldwide; in particular, they can introduce in a given geographic area new tick species and related tick-borne pathogens. Studies about the detection of tick-borne agents in birds are not numerous, whereas more attention has been turned to the presence of these microorganisms in ticks carried by birds. The present review focused on the role of avian populations in the epidemiology of rickettsioses and babesioses, which represent two severe problems for the health of humans and other mammals.

1. Introduction

Ticks are considered the most important vectors of microbial pathogens, zoonotic too, after mosquitoes [1]. These Arachnids can harbor more than one pathogen simultaneously and although Ixodidae are the most common vectors, Argasidae can also be involved, being able to transmit viruses, bacteria and, to a lesser extent, protozoan parasites such as Babesia [2]. Another relevant aspect of ticks’ parasitism is linked to the transportation of these Acharina, by affected hosts.
Birds with different lifestyles are, in fact, often carriers of ticks harboring pathogens, which can affect other animal species and humans. Tick infestation of birds is related to the rhythms of tick seasonal activity and birds’ migrations. Migratory birds, which cover long distances during their seasonal migrations, can introduce ticks and related tick-borne pathogens into new geographic areas [3].
Climatic changes, as well as consequent changing of environmental conditions, are factors that are influencing the tick distribution in several areas of the world. This feature is of capital importance for Ixodidae, which spend longer periods on hosts in respect to Argasidae. Birds are parasitized by both ticks’ Families [4] and play an important role in the dispersal of tick-borne diseases, acting both as cyclic hosts and as carriers of viruses, bacteria, and protozoa.
The role of avian populations in the epidemiology of some pathogens transmitted by hematophagous arthropods has been defined. For example, several investigations have clarified the involvement of wild birds in the cycle of Borrelia spp. and West Nile virus [5]. On the other hand, some arthropod-borne agents have been found in ticks removed from birds, but several aspects related to these microorganisms are currently not clear: duration of pathogens’ presence in blood, target organs, potential pathogenicity for birds.
The present review focused on the role of birds in the epidemiology of Rickettsia spp. and Babesia spp., which are some of the most important bacterial and protozoan agents of veterinary and human concern, because they may cause diseases characterized by mild or severe clinical forms in different mammal species, including humans.

2. Rickettsia spp.

2.1. Etiology

The genus Rickettsia comprises obligate intracellular Gram-negative bacteria, whose sizes range from 0.3–2.0 µm. These bacteria multiply by binary fission in the cytoplasm of eukaryotic host cells and consequently, they must be cultivated in tissue culture; no axenic media has been formulated for their cultivation. Rickettsiae are difficult to stain with ordinary bacterial stains but, conveniently, are stained by the Gimenez method.
Members of this genus are currently classified into four groups: the typhus group (TG) with R. typhi and R. prowazekii; the spotted fever group (SFG) with 21 species; R. bellii group; R. canadensis group. Many other isolates exist, but they are not fully characterized [6].
Rickettsiae have a life cycle typically involving hematophagous arthropod vectors and vertebrate hosts. They enter the host cells by phagocytosis and escape from the phagocytic vacuole into the host cytoplasm to evade phagosome-lysosome fusion, replicate within the host cytoplasm, and exit from the host cell by actin-mediated motility (SFG) or lysis of host cells (TG).
TG rickettsiae are responsible for severe human diseases: murine typhus and epidemic typhus are caused by R. typhi and R. prowazekii, respectively.
SFG members are the cause of different diseases, often serious, that may affect both humans and other mammals. Among them, R. conorii is the most widespread SFG species in the countries of Mediterranean basin, responsible for the Mediterranean spotted fever (MSF) that affects humans, but also dogs [7]. Other SFG species are present worldwide, often associated to human clinical cases, with different distribution in relation to geographic areas. Among them, R. helvetica has been reported in several European countries, other than in Africa and Asia. It is associated in humans to aneruptive fever, headache, arthralgia, myalgia, perimyocarditis, whereas its pathogenic role in animals is not clarified [8]. Similarly, R. monacensis causes diseases in humans, but its potential pathogenicity for animals is not known. It has been reported mainly in Europe, even though reports come from South Korea, Algeria, and USA [9]. Rickettsia massiliae can affect dogs and mainly humans, in which causes a febrile illness with rash, inoculation eschar and neck lymphadenopathy. It is distributed in tropical African countries, southern Europe, and USA [10,11]. Rickettsia monacensis has been reported in Europe, Asia, northern Africa, and USA, as well as R. aeschlimannii in southern Europe, several African countries and central Asia; both species induce clinical pictures similar to MSF in affected persons [10]. Rickettsia slovaca and R. raoultii, present in Europe and Asia, are associated to the human disease tick-borne lymphadenopathy (TIBOLA), Dermacentor-borne necrosis erythema and lymphadenopathy (DEBONEL) and scalp eschars neck lymphadenopathy (SENLAT) [10]. African-tick-bite fever (ATBF) is caused by R. africae and is frequently diagnosed in Europe in patients returning from African endemic areas [10].

2.2. Rickettsia spp. in Birds and Their Ticks

Studies carried out to verify the role of avian populations in the epidemiology of rickettsiosis mainly regard investigations about the presence of rickettsiae in ticks collected from birds. Otherwise, surveys about Rickettsia infection directly in birds are scanty (Table 1).
During an investigation carried out in Cyprus from 2004 to 2006 by Ioannou and coworkers [12], 131 blood pools were obtained from 557 wild birds belonging to 51 avian species. Among them, four (3%) (common moorhens Gallinula chloropus and American flamingos Phoenicopterus ruber) were PCR-positive for Rickettsia spp.; furthermore, ticks and lice were removed from the tested animals and Rickettsia spp. DNA was found in three Ixodes vellantoi [12].
During the 2009 and 2010 spring migration seasons, 2064 northward-migrating passerine songbirds were examined for ticks at Johnson Bayou, Louisiana (USA) [13]. A total of 91 ticks were collected from 35 songbirds and they were identified as Haemaphysalis juxtakochi (42%), Amblyomma longirostre (24%), Amblyomma nodosum (19%), Amblyomma calcaratum (12%), Amblyomma maculatum (2%), and Haemaphysalis leporispalustris (1%). Most of the identified ticks were exotic species originating outside of the United States. Two genotypes, found in 28 ticks, were included in the Candidatus Rickettsia amblyommii clade, 2 genotypes, detected in 14 ticks, clustered with Rickettsia sp. “Argentina”, and 2 genotypes, found in 27 ticks, exhibited sufficient genetic divergence to possibly constitute a new rickettsial genotype. Moreover, blood samples were collected from the 35 birds and 20 rickettsial strains were detected. Analyses of the detected rickettsial DNA identified 18 strains identical to Rickettsia sp. “Argentina” and to Rickettsia endosymbiont of Amblyomma maculatum, one strain different only for 2 base pairs, while the quality of the last strain did not allow the identification.
Interesting results were observed comparing the presence of rickettsiae in ticks and birds. In fact, 14 ticks were not infected and were found on infected birds, 18 were infected, but found on noninfected birds, and 6 were not infected and were found on non-infected birds. Furthermore, only in 5 cases, the rickettsia found in the tick from a given bird was the same as that detected in that bird, while in the remaining cases the rickettsia detected in the ticks did not correspond to the strain from the bird [13].
Successively, Hornok et al. [14] collected, in spring and autumn migration periods of 2013, blood specimens from 128 wild birds in Hungary. Five robins (Erithacus rubecula) and one dunnock (Prunella modularis), for a total prevalence of 4.7%, were PCR-positive with R. helvetica. All ticks on the body of each examined bird were removed and analyzed. A total of 140 ticks were collected from 68 birds; Ixodes ricinus was found on most of the tick-infested birds (92.6%) and it was the most abundant tick species (86.4%). Haemaphysalis concinna was present on 11.8% of the infested birds; four animals were co-infested with I. ricinus and H. concinna; one wood warbler (Phylloscopus sibilatrix) carried a Hyalomma larva. Of the 140 ticks, 61, I. ricinus and H. concinna, were PCR-positive for R. helvetica and 11, all I. ricinus, for R. monacensis. The no-correlation between the PCR results testing birds and their ticks is interesting. In fact, among the six birds resulted positive for R. helvetica, no ticks were found on four of them and one PCR-negative tick was found on another. The remaining R. helvetica positive birds had 11 ticks, of which two resulted PCR-positive. On the other hand, 59 ticks positive for R. helvetica were removed from 38 PCR-negative birds.
The authors supposed that rickettsiaemia in avian hosts persists after the detachment of the ticks, as corroborated by the no-findings of ticks on the majority of R. helvetica positive birds. Moreover, they hypothesized that the transmission of rickettsiae is possible from ticks to birds, whereas the transmission from birds to ticks rarely occurs, as suggested by the fact that among 11 ticks removed from a rickettsiaemic bird, only two were PCR-positive for R. helvetica. However, the finding of PCR-positive ticks removed from PCR-negative birds could be related to potentially intermittent rickettsiaemia of the animals [14]. Moreover, PCR-negative results could not correspond to absence of rickettsiae in the tested samples, because PCR is not always able to detect DNA of pathogens; in fact its sensitivity is in relation to the assay’s protocol, type of samples, and amount of pathogens present in the specimens [19].
Feral pigeons (Columba livia domestica) were found infected by Rickettsia spp. with a prevalence of 5.95% in central Italy. In fact, DNA of these pathogens was found in spleen samples collected from five pigeons captured in urban/peri-urban areas [15], suggesting that feral pigeons, which are traditionally considered a hazard for the human health as source of pathogens excreted with feces, such as salmonellae and chlamydiae, may be also involved in the epidemiology of rickettsiosis.
Few studies documented the exposure of birds to rickettsiae by the detection of specific antibodies. A serological survey was carried out in pheasants (P. colchicus) to verify the occurrence of antibodies against some tick-borne pathogens. All the tested pheasants lived in an area of central Italy with conditions favorable for ticks’ diffusion, such as a rich vegetation and various large and small mammals [17]. The 17.75% of the examined animals were positive to R. conorii antigen [17]. The detected prevalence could include antibodies against R. conorii, as well as other SFG rickettsiae due to the common antigens [7]. In fact, several SFG rickettsiae, mainly R. conorii, R. helvetica, R. massiliae, R. slovaca, R. aeschlimannii, R. africae, R. monacensis, R. roultii were circulating in Italy at the sampling time, as observed in molecular investigations in animals and ticks [17].
A previous serological survey detected antibodies to R. africae antigen in 35% in ostriches (Struthio camelus) living in farms in Zimbabwe [18]. Additionally in this case, the detected antibodies could be due to other SFG rickettsiae, such as R. conorii that circulated in the area in that period. However, the authors supposed that the examined ostriches were exposed to R. africae, because this rickettsia had been identified in Amblyomma hebraeum that usually parasitized ostriches in Zimbabwe, whereas R. conorii was traditionally associated to Rhipicephalus sp. that were not known to feed on these birds.
Most numerous data available in literature are focused on the presence of DNA rickettsiae in hard and soft ticks removed from birds.
Santos-Silva and coworkers [20] analyzed ticks removed from wild birds in Portugal from 2002 to 2004, but they did not verify if the animals were rickettsaemic. However, three Hyalomma marginatum had rickettsial DNA exhibiting nucleotide sequence of gltA (citrate synthase) and ompA genes 100% similar to R. aeschlimannii. One Rhipicephalus turanicus had a rickettsial agent showing 100% homology to R. massiliae, as well as one I. vellantoi had a rickettsia 100% homologous to R. helvetica.
A survey investigated the tick infestation in populations of the migratory passerine bird Riparia riparia, the sand martin, in northwest England in June 2009. A total of 194 birds were sampled and ticks removed from infested birds and all ticks were identified as females of Ixodes lividus. A single Rickettsia spp., designated as Rickettsia sp. IXLI1, was detected in 100% of the ticks examined by PCR. Partial sequences of 17-kDa and ompA genes showed greatest similarity to the strain Rickettsia sp. TCM1, etiological agent of the Japanese spotted fever-like illness, previously described in Thailand. Moreover, phylogenetic analysis showed that the strain Rickettsia sp. IXLI1 perfectly fitted into a group containing Rickettsia japonica, Rickettsia sp. strain Davousti, and Rickettsia heilongjiangensis [21].
A molecular survey, carried out in autumn 2010, involved 2,793 migratory birds captured by nets in a ringing station located in northern Italy; in particular, the birds were captured in a woodland zone (Arosio, Como, Italy) located ~30 km north of Milan, one of the most populated and interconnected areas in Europe [22]. The animals were checked for the presence of ticks and 251 nymphs and larvae of I. ricinus were collected and examined by PCR. Twenty-five (10%) ticks were positive for Rickettsia spp.: 1 was removed from a chaffinch (Fringilla coelebs), 1 from a common blackbird (Turdus merula), 2 from robins (E. rubecula), 5 from redwings (Turdus iliacus), 16 from song thrushes (Turdus philomelos). The detected amplicons were reportable to R. monacensis and R. helvetica, but it is mainly interesting the detection of Candidatus Rickettsia mendelii [22] that was recently described as a non-SFG Rickettsia in I. ricinus from Czech Republic [23]. This finding is the typical example of the potential role of avian population in carrying infected ticks from one geographic area to another.
An interesting survey was carried out by Wallmenius et al. [24] on many samples. Ticks were collected from a total of 14,789 birds during their seasonal migration northwards in spring 2009 and 2010 at bird observatories on two Mediterranean islands: Capri (Italy) and Antikythera (Greece). All ticks were subjected to RNA extraction followed by cDNA synthesis and individually assayed with a real-time PCR targeting the gltA gene. For species identification of Rickettsia, multiple genes were sequenced. Three hundred and ninety-eight (2.7%) of all captured birds were tick-infested; some birds carried more than one tick. A total number of 734 ticks were analyzed and 48% were Rickettsia-positive; 96% were infected with R. aeschlimannii, and 4% with R. africae or unidentified Rickettsia species. The predominant tick taxon, H. marginatum sensu lato constituted 90% of the ticks collected. The remaining ticks were Ixodes frontalis, Amblyomma sp., Haemaphysalis sp., Rhipicephalus sp., and unidentified ixodids. Most ticks were nymphs (66%), followed by larvae (27%), and adult female ticks (0.5%). The majority (65%) of ticks were engorged and nearly all ticks contained visible blood.
A similar screening for multiple tick-borne pathogens in I. ricinus ticks collected from wild birds in Denmark, during spring and autumn migration seasons in 2016, found that 10.6% of the examined ticks were PCR-positive for SFG rickettsiae [25].
Rickettsia sp. DNA were found in 12.3% of I. ricinus removed from wild birds in Switzerland during breeding periods and fall migrations from 2007 to 2010. In particular, R. helvetica and R. monacensis DNA were detected with prevalences of 10.5% and 0.4%, respectively [26]. More in detail, larvae (13.6%) were more infected than nymphs (10.1%); the prevalence found in ticks feeding on migrants (11.9%) was lower than in ticks feeding on breeding birds (17.3%). The common blackbird T. merula (25%) and the tree pipit Anthus trivialis (23.3%) were the species most frequently infested with Rickettsia-infected ticks.
The reservoir competence of tree pipits for R. helvetica was suggested by the authors, in this study, since 5.8% of tree pipits were infested by at least two infected larvae and larvae (17.3%) were more infected than nymphs (11.8%). However, rickettsiae could be transmitted transovarially to larvae, thus the reservoir competence of avian hosts should be otherwise demonstrated. Furthermore, during the same study it was observed that larvae feeding with nymphs (16.3%) showed a very similar infection prevalence as larvae feeding alone on host (without nymphs) (17.9%), suggesting that co-feeding transmission is not the main means of transmission and that birds may be the source of infection. The same authors concluded that T. merula are also important in the life cycle of rickettsiae, since they are the species carrying the most frequently infected [26].
Similarly, the reservoir competence of some avian genus for Rickettsia spp. was suggested by some authors. For example, Elfving et al. [27] found one European Blue Tit (Parus caeruleus) which carried seven ticks of which six were positive for R. heilongjiangensis-like Rickettsia. The authors supposed that the bird was rickettsiaemic and that the ticks had acquired the bacteria from its blood.
On the other hand, there were also several examples of multiple ticks on a single bird where only one of the ticks was infected with Rickettsia, for instance a European robin that carried 27 ticks, only one of which was positive for R. helvetica [27].
A potential role of some avian species as reservoirs was supposed also by Spitalska et al. [28], who detected rickettsiae in 44.0% larvae and 24.5% nymphs of I. arboricola collected from great tits (Parus major), marsh tits (Poecile palustris), and Eurasian nuthatches (Sitta europaea). Rickettsiae-positive I. ricinus larvae (13.7%) were collected from P. major, Cyanistes caeruleus (Euraian blue tits) and S. europaea, and 2.6% of nymphs from robins (Erithacus rubecula) and dunnocks (Prunella modularis) [28].
Recently, Rollins and coworkers [29] collected ticks from 151 birds captured on Ponza Island (south Italy), which represents an important migratory stopover off the western coast of Italy. In total, 16 captured birds carried ticks from four tick species: Hyalomma rufipes (n = 14), Amblyomma variegatum (n = 1), Amblyomma sp. (n = 1), and Ixodes ventalloi (n = 2). All specimens were either larvae (n = 2) or nymphs (n = 16). R. aeschlimannii was detected in six of the 14 collected H. rufipes ticks and the singular A. variegatum nymph tested positive for R. africae.
Ticks carried by wild birds may be source of rickettsiae at high altitudes, too, as demonstrated by a study conducted in the Tropical Andes in Colombia from 2015 to 2019. Ticks were collected from birds at elevations ranging from 178m to 3845m. Rickettsia DNA was found in 11% of the examined ticks, which were removed from six resident bird species and one migratory boreal species. Rickettsia amblyommatis was found in A. longirostre, Amblyomma varium and Ixodes sp. (closely related to Ixodes auritulus) collected from resident avian species. Candidatus Rickettsia colombianensi was detected in Amblyomma dissimile taken from the migratory bird Opornis agilis, whereas a possible novel agent closely related to Candidatus Rickettsia tarasevichiae and R. canadensis was detected in Ixodes sp. (closely related to Ixodes tanuki) [30].
R. amblyommatis, as well as R. bellii, was also found in A. longirostre and A. calcaratum recovered from wild birds in Brazil [31,32]. Amblyomma spp. ticks infesting wild avian population in Brazil resulted carriers of Rickettsia rhipicephali, Rickettsia parkeri, and Candidatus Rickettsia amblyommii, too [33].
Cold geographic areas are not free from this problem. A Rickettsia-like microorganism was isolated from ticks of the species Ixodes uriae collected from penguins (Pygoscelis papua) bred on Mayes Island, Kerguelen Archipelago, French Subantarctic Territories [34]. More recently, a king penguin (Aptenodytes patagonicus) recovered and dead in a rehabilitation center in South Africa resulted infected by a Rickettsia-like organism. Post-mortem blood smears of this animal showed pleomorphic rickettsia-like inclusions within the cytoplasm of erythrocytes. It was supposed that the animal died because of bacterial enteritis with complicating septicemia to which the rickettsial agent may have been related [16].
Even though hard tick species result the main hematophagous vectors of rickettsiae among birds, soft ticks (Argasidae) seem to be involved in the transmission of these pathogens, too.
Rickettsia hoogstraali was found in 41% of Argas (Persicargas) giganteus ticks removed from wild birds recovered in a wildlife rehabilitation center in Arizona. However, the blood samples of birds, from which positive ticks were collected, resulted PCR-negative for Rickettsia spp. [35].
Rickettsia fournieri sp.nov., a novel SFG species, was isolated from an Argas lagenoplastis tick collected from the nest of a Petrochelidon ariel (fairy martin) in Australia in 2013 [36].
Ornithodoros sawaii and Ornithodoros capensis were assessed for the presence and identification of rickettsiae by Kim et al. [37] in Gugul Island, Republic of Korea. Ticks collected from samples of nest litter and soil from seabird nests were identified individually by morphological techniques, and species confirmed by sequencing of the mt-rrs gene. A total of 134 soft ticks belonging to O. sawaii and O. capensis were collected; Rickettsia lusitaniae DNA was detected and identified in 11 (8.8%) O. sawaii ticks collected from nest litter and soil of the Japanese murrelet (Synthliboramphus wumizusume) [37].
Rickettsia sp. was first detected in seabird soft-bodied ticks, Carios capensis and Carios sawaii in Japan by Kawabata and coworkers from 2003 to 2005 [38]. Ticks were collected from colonies of streaked shearwaters (Calonectris leucomelas) and black-footed albatross (Diomedea nigripes). The sequence of this Rickettsia strain was identical to that of a Rickettsia strain (scc31) previously found in C. capensis in South Carolina, U.S.A. This finding suggested that an environmental circulation had consisted among microorganisms, ticks, and long-distance migratory seabirds around the Pacific Ocean [38].
Carios capensis, well known as a tick of seabirds, often infests the nests of brown pelicans (Pelecanus occidentalis) and other ground nesting birds along the coast of South Carolina. Reeves et al. 2006 [39] collected ticks from a pelican rookery on Deveaux Bank, South Carolina and R. felis and two undescribed Rickettsia spp. DNA were detected. Rickettsia felis, which causes a murine typhus like human disease, is related to cat populations and fleas Ctenocephalides felis. The susceptibility of pelicans to this rickettsia as well as its source in C. capensis were not defined. It was supposed that pet dogs, which in South Carolina are frequently infested with C. felis, could be the source of fleas infected by R. felis. In fact, even though pets are not allowed on Deveaux Bank, dog footprints were noted by the researchers near human footprints among the pelican nests [39].
From 2012 to 2014 soft ticks of the species C. capensis were collected from yellow-legged gull (Larus michaellis) nests in Algeria [40]. Sequences of the gltA gene of the detected rickettsial DNA suggest that the microorganism is a novel SFG Rickettsia strain, probably a strain of R. hoogstraalii. Based on other findings, this species seems to be the most common rickettsial species infecting C. capensis ticks, confirming that this hematophagous arthropod likely represents a major host reservoir for the bacteria. An unclassified rickettsial lineage genetically related to R. hoogstraalii was also detected in C. capensis in Réunion (Europe) and the Tromelin Islands, showing that two distinct Rickettsia spp. strains cocirculate in these tick populations [41].
During the same survey by Dietricht et al. [41] on Réunion Island, R. bellii was detected in 2 C. capensis ticks collected within the same nest of the wedge-tailed shearwater (Puffinus pacificus).
R. bellii has been most frequently documented in the Americas, but recent studies have detected the presence of closely related R. bellii strains also in Australia [42] and Europe [43]. The presence of Rickettsia agents on Réunion Island, considered as a remote island, is a further suggestion of the role of bird hosts in the dispersal of ticks and their associated infectious agents over large distances.

3. Babesia spp.

3.1. Etiology

Babesia spp. are apicomplexan parasites that, together with Theileria, belong to piroplasms. They are so called for their pear-shaped morphology, although oval or round forms can be detected, and appear as small endocellular organisms (1–5 μm in length) [44]. These parasites can be differentiated by pigment forming Plasmodium and Haemoproteus, lacking pigment into erythrocytes. Theileria differs from Babesia for its ability to form schizonts, to colonize lymphocytes, besides red cells and to transmit only transstadially in ticks. Furthermore, babesiae are classified in Babesia sensu stricto (transstadial and transovarial transmission) and Babesia sensu lato (transstadial transmission only). Life cycle of Babesia consists in asexual multiplication in red blood cells of the vertebrate host and in gametogony followed by sporogony in salivary glands of ticks that have acquired the infection during the blood meal [45,46]. More than 100 parasite species have been described in animals. They are often pathogenic, mostly for domestic animals and human beings, showing a strong economic impact, negatively influencing animal welfare and public health. Babesiosis in wildlife can be fatal, too when associated with stressful management practices [45]. Mammals and birds are involved in life cycles as vertebrate (intermediate) hosts although the specificity of babesia for vector ticks (final hosts) has not been fully elucidated [47].
Babesia spp. accomplish merogony into red blood cells of birds and gametogony and sporogony in both Ixodidae and Argasidae ticks, [48,49]. Argasidae, mostly Ornithodoros seem to be involved in Babesia transmission in colonial birds nesting on ground or near rocks, whose crevices would represent breeding sites for these invertebrate hosts. The occurrence of Ornithodoros capensis on African penguins seems to be strongly related with Babesia infection higly supporting the hypothesis that this tick would be the main vector of the parasites [50,51]. These findings have been corroborated by the occurrence of Babesia DNA in this argasid species from New Zealand too [52].

3.2. Babesia in Birds and Their Ticks

The first record of Babesia in birds goes back to the beginning of last century and the parasite was identified as Sogdianella moshkovskii [53], then modified in B. moshkovskii [54]. Sixteen species of avian Babesia, namely B. moshkovskii, B. kazachstanica, B. uriae, B. kiwiensis, B. ardeae, B. frugilegica, B. emberizica, B. shortti, B. balearicae, B. rustica, B. bennetti, B. mujunjumica, B. peircei, B. poelea, B. krylovi, and B. ugwidiensis have been recognized to date [48,55,56,57], along with other Babesia spp. although, B. poelea is suggested to be a synonym of B. peircei, able to infect seabirds from several orders [48,58]. Each species would be host specific at the family level [59]. Since only a limited number of morphological characters are available (chromatin of merozoites of B. peircei, B. krylovi, B. poelea, B. uriae, and B. bennetti has a distal position, when compared with other species whose nuclei are in a proximal position), species cannot always be differentiated morphologically [60].
Some of these species have been molecularly characterized [58], indicating that these avian parasites are not monophyletic, and belong to three paraphyletic groups namely Peircei, Kiwiensis, and Bennetti. Peircei group is distributed worldwide in aquatic birds and comprehends B. ardeae, B. poelea, B. peircei, B. ugwidiensis, B. uriae and other not identified Babesia spp. Kiwiensis group is reported from the Pacific Ocean, only and Bennetti, containing B. bennetti as a unique species, has been registered only in Mediterranean Sea.
Small subunit ribosomal RNA gene sequences are available only for B. poelea, B. uriae, B. bennetti, B. kiwiensi, B. ugwidiensis, and B. uriae, but not for B. peircei, so the piroplasms found in healthy little penguins from Australia affected only by round forms molecularly closely related to B. poelea and B. uriae, could be B. peircei, confirming the specificity of this species for penguins [61], although, as above reported, B. poelea was suggested be a synonym of B. peircei, considered as a generalist parasite species, infecting seabirds, belonging to different orders. Furthermore, New Zealand seabirds were found infected by novel variants of B. poelea-like protozoa (named genotypes I and II) and by a B. kiwiensis-like piroplasm. All the three variants were isolated from gannets and gulls, whilst terns scored positive for B. poelea-like genotype I B. kiwiensis-like parasites, only [52], suggesting a lack of stratification by avian species.
The prevalence of infection in birds is low [62,63] and the finding of Babesia in different unrelated avian species would suggest that such infections have followed many independent colonization events [56,62].
The pathogenicity of Babesia spp. for birds is still unclear [59], and B. shortii and B. uriae seem the only pathogenic avian piroplasms. B. uriae has been identified in dead murres, showing associated lesions [56], while B. shortii has been described in Falconidae that are probably the only susceptible species and is considered a pathogenic piroplasm in its avian hosts [64]. For these reasons B. shortii is considered as the most important avian Babesia species, both from a conservation and veterinary standpoint [48]. However, B. peircei was isolated from diseased penguins, affected by other haemoparasites, too: these piroplasms seem to have contributed to the death of a king penguin [65]. Infected penguins are reported to show sometimes mild anaemia, leucocytosis, and impairment of hepatic function [66,67]. Thus, it is assumed that these protozoan species would contribute to the overall morbidity and mortality when other pathogens occur. Furthermore, B. ugwidiensis was reported from young cormorans showing high mortality rates and with parasite stages in blood. However, a relationship between the occurrence of high parasite load and mortality is still debated [65].
The hypothesis of pathogenic actions by these piroplasmic species is supported by the good response to antibabesial therapy in falcons treated with imidocarb dipropionate [64] and in African penguins and cormorants empirically administered with primaquine [68]. Avian Babesia spp. are listed in Table 2.

3.3. Carriage of Zoonotic Babesia Infected Ticks

Ticks recovered from avian species result infected by different Babesia spp., however, in the present study attention will be paid to zoonotic agents, only.
The role of migratory birds in spreading ticks across the Europe has recently been reviewed by Buczek et al. [3]. Birds not migrating and/or migrating are carriers of several ticks along with several tick pathogens and would play a role in spreading such agents [3,77]. Transport of tick-borne pathogens from one endemic area to another could have an impact, although the pathogens already occur there, by spreading new strains to new areas, too [78]. Birds usually bear larval and nymphal stages of Ixodes ricinus at a latitude 58°N, and H. marginatum in areas below 42°N [3], furthermore Haemaphysalis concinna is the second more prevalent ixodid species isolated from birds in Central Europe [79] and has been recently recognized to contain Babesia sp. (related to B. crassa) and B. microti DNA [80].
Tickborne zoonotic protozoa belonging to Babesia genus, namely B. divergens, B. microti and B. venatorum (formerly Babesia sp., EU1) are the most involved species [81]. However, B. duncani (Babesia sp. WA1), B. crassa-like, Babesia sp. KO, Babesia sp. CN1 (Babesia sp. XXB/HangZhou) [82] and B. odocoilei [83] have been recently included. B. divergens mostly occurs in Europe [84,85].
Zoonotic piroplasms are mostly transmitted by Ixodes ticks [86,87]. The vectors in Europe are I. ricinus, while in Asia and in America Ixodes persulcatus and Ixodes scapularis, respectively would occur [88]. Interestingly, B. microti transmitted by I. ricinus is not common in Europe, being reported in few cases per year, while, when transmitted by I. scapularis this piroplasm is responsible for several hundred cases per year [89].
Human babesiosis is considered as an emergent worldwide disease, potentially life threatening and severe, mostly for immunocompromised people. Clinical signs of B. microti infection range from asymptomatic to fulminating, fatal disease. The most common symptoms are fever, fatigue, malaise, anorexia, and myalgia. Immunocompromised patients would show severe babesiosis characterized by anemia, acute respiratory distress syndrome, disseminated intravascular coagulation, congestive heart failure, renal failure, and coma. B. divergens is reported mostly in asplenic patients from Europe and cases appeared severe, with a fulminant course and parasitaemia 80%. Babesiosis by B. venatorum from Europe is more severe than from China, where the course of disease appears milder. The clinical cases caused by B. duncani are less than 20 and symptomatology is similar to those of B. microti [44]. Finally, babesiosis by B. odocoilei, until today, has been described in two spleen-intact patients from USA, only, showing night sweats, chills, fevers, profound fatigue, increased thirst, muscle aches, and sleep disturbance [90].
Questing larvae are usually found on the ground, so ground-foraging birds (Passeriformes and Galliformes) are more frequently involved in hard ticks’ life cycle. Furthermore, migrating birds can shed engorged ticks to stopover sites, able to colonize further hosts which will carry them over longer distances [3].
Birds migrating southwards have high rates of infestation and I. ricinus is the predominant tick species [91]. For these reasons, epidemiological studies from Europe deal with identification of Babesia spp from I. ricinus. Passeriformes seem more frequently involved in carriage of infected ticks. B. divergens and B. microti DNA were found in specimens of I. ricinus mostly on blackbirds from Germany [92,93]. The same piroplasm species along with B. venatorum, was identified in ticks on Passeriformes from Latvia [94]. B. venatorum DNA has been identified in nymphs carried by Turdus philomelos in Northwestern Russia [95] and in Norway by passerine birds [78], while B. microti and B. venatorum infected both larval and nymphal stages of I. ricinus from Sweden [96]. Furthermore, DNA of B. microti was detected in Ixodes granulatus found on Emberiza spadocephala in Taiwan [97].
Similar studies from North America dealing with I. scapularis, revealed B. microti [98] while B. odocoilei was identified in ticks from Canada, occurring on songbirds [99,100,101]. The occurrence of a pathogen in a tick found on a host does not demonstrate in fact that the tick is the vector of the pathogen, and data would be misleading when the presence of pathogens has not been ascertained in the host [47].
However, for Babesia organisms the knowledge of vector identity is still incomplete and there are a lot of studies concerning the detection of parasite DNA in vectors, compared with properly controlled transmission studies to evaluate the vector competence of ticks [89].

3.4. Carriage of Zoonotic Babesia by Infected Birds

The role of birds as reservoir of zoonotic piroplasms has not been fully elucidated. The reservoirs can be identified by comparing the infection rates of questing preadult stages with larvae feeding on the hosts. When larvae show a higher infection prevalence it is reasonable to assume that the host is a reservoir [25], mostly when the pathogen fails to be transmitted transovarially, as in case of B. microti [92,98]. B. divergens and B. venatorum are, conversely, transmitted both transstadially and transovarially [102]. Furthermore, since the life cycle is quite complex, the hypothesis of a route of transmission by cofeeding should be ruled out [92].
Birds are considered as reservoir for zoonotic babesiae [92], namely B. microti, B. divergens and B. venatorum. These features have been confirmed by the ability to infect more than ten larvae of I. scapularis with B. microti showed by different avian species [98].

4. Conclusions

Birds have the capacity of flying across large intercontinental areas in short periods of time to exploit seasonal opportunities for food supplies and breeding habitats [103]. They fly along migration routes that connect several geographic areas. Numerous flyways are known in all continents. Millions of wild birds are flying from some areas to others twice a year in just a few weeks, and during this movement they can carry pathogens which may affect other birds, as well as humans and other mammals. Moreover, during their intercontinental movements birds can also carry hematophagous arthropods harboring microorganisms. The pathogens’ transmission continues in the stopover areas where numerous birds of different species are concentrated. The migratory routes, thus, can be considered a relevant cause of spreading of a given pathogen from an initial site of contagion to new remote areas [104].
Rickettsiae are tick-borne microorganisms with different distribution in relation to the geographic areas and are frequently the cause of severe human diseases. Migratory birds, which are often involved in the epidemiology of tick-borne pathogens, have been proven to be carriers of ticks harboring several Rickettsia species worldwide. In some cases, in relation to the species of ticks, rickettsiae and birds, high altitudes and low temperatures seem to not reduce the risk of circulation of arthropods and bacteria in avian populations [30,34].
Through flight of birds, migratory routes connect geographic areas with different climatic features and allow ticks and their related pathogens to arrive in new environments. Resident birds, that live in the same place throughout the year, may act as carriers of infected ticks, too. Among them, synanthropic species, such as pigeons, frequently live in urban and peri-urban areas representing a serious risk for humans not only as source of salmonellae or chlamydiae, but also tick-borne pathogens [15].
However, most of the data available in literature prove that avian species are carriers of Rickettsia-infected ticks, but only few studies have been carried out to verify the rickettsial infection in these animals. Further investigations are necessary to clarify this concern because the finding of Rickettsia DNA in ticks could be simply related to the presence of the pathogens in the gut blood reaming from the last feeding on host [13].
Tick-borne avian protozoa such as Babesia spp. do not represent a threat for public health, however birds can carry early stages of hard ticks infected with zoonotic species—although only a few studies dealing with the vector competence of ticks have been accomplished [89]. However, birds are considered as reservoir for zoonotic piroplasms, and this feature has been demonstrated for B. microti in different birds’ species [98]. For these reasons further studies are needed to fully evaluate the impact of avian species in the epidemiology of such pathogens.

Author Contributions

Conceptualization, V.V.E. and F.M.; methodology, V.V.E. and F.M.; writing—original draft preparation and writing—review and editing, V.V.E. and F.M. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by University of Pisa, grant number PRA_2020_88.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study is contained within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Toledo, A.; Olmeda, A.S.; Jado, I.; Gil, H.; Valcárcel, F.; Anda, P.; Escudero, R.; Casado-Nistal, M.A.; Rodríguez-Vargas, M. Tick-borne zoonotic bacteria in ticks collected from central Spain. Am. J. Trop. Med. Hyg. 2009, 81, 67–74. [Google Scholar] [CrossRef]
  2. Battsetseg, B.; Matsuo, T.; Xuan, X.; Boldbaatar, D.; Chee, S.H.; Umemiya, R.; Sakaguchi, T.; Hatta, T.; Zhou, J.; Verdida, A.R.; et al. Babesia parasites develop and are transmitted by the non-vector soft tick Ornithodoros moubata (Acari: Argasidae). Parasitology 2006, 134, 1–8. [Google Scholar] [CrossRef] [PubMed]
  3. Buczek, A.M.; Buczek, W.; Bartosik, K. The Potential Role of Migratory Birds in the Rapid Spread of Ticks and Tick-Borne Pathogens in the Changing Climatic and Environmental Conditions in Europe. Int. J. Environ. Res. Public Health 2020, 17, 2117. [Google Scholar] [CrossRef] [Green Version]
  4. Víchová, B.; Reiterová, K.; Špilovská, S.; Blaňarová, L.; Hurníková, Z.; Turčeková, Ľ. Molecular screening for bacteria and protozoa in great cormorants (Phalacrocorax carbo sinensis) nesting in Slovakia, central Europe. Acta Parasitol. 2016, 61, 585–589. [Google Scholar] [CrossRef]
  5. Harner, S.A.; Goldberg, T.L.; Kitron, U.D.; Brawn, J.D.; Anderson, T.A.; Loss, A.R.; Walker, E.D.; Harner, G.L. Wild birds and ecology of ticks and tick-borne pathogens, Chicago, Illinois, USA, 2005–2010. Emerg. Infect. Dis. 2012, 18, 1589–1595. [Google Scholar] [CrossRef]
  6. Parola, P.; Paddock, C.D.; Socolovschi, C.; Labruna, M.B.; Mediannikov, O.; Kernif, T.; Abdad, M.Y.; Stenos, J.; Bitam, I.; Fournier, P.-E.; et al. Update on Tick-Borne Rickettsioses around the World: A Geographic Approach. Clin. Microbiol. Rev. 2013, 26, 657–702. [Google Scholar] [CrossRef] [Green Version]
  7. Brouqui, P.; Parola, P.; Fournier, P.E.; Raoult, D. Spotted fever rickettsioses in southern and eastern Europe. FEMS Immunol. Med. Microbiol. 2007, 49, 2–12. [Google Scholar] [CrossRef] [Green Version]
  8. Scarpulla, M.; Barlozzari, G.; Salvato, L.; De Liberato, C.; Lorenzetti, R.; Macrì, G. Rickettsia helvetica in human-parasitizing and free-living Ixodes ricinus from urban and wild green areas in the metropolitan City of Rome, Italy. Vector Borne Zoonotic Dis. 2018, 18, 404–407. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  9. Kim, Y.-S.; Choi, Y.-J.; Lee, K.-M.; Ahn, K.-J.; Kim, H.-C.; Klein, T.; Jiang, J.; Richards, A.; Park, K.-H.; Jang, W.-J. First isolation of Rickettsia monacensis from a patient in South Korea. Microbiol. Immunol. 2017, 61, 258–263. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  10. Oteo, J.A.; Portillo, A. Tick-borne rickettsioses in Europe. Ticks Tick-Borne Dis. 2012, 3, 271–278. [Google Scholar] [CrossRef] [PubMed]
  11. Cascio, A.; Torina, A.; Valenzise, M.; Blanda, V.; Camarda, N.; Bombaci, S.; Iaria, C.; De Luca, F.; Wasniewska, M. Scalp Eschar and Neck Lymphadenopathy Caused by Rickettsia massiliae. Emerg. Infect. Dis. 2013, 19, 836–837. [Google Scholar] [CrossRef] [Green Version]
  12. Ioannou, I.; Chochlakis, D.; Kasinis, N.; Anayiotos, P.; Lyssandrou, A.; Papadopoulos, B.; Tselentis, Y.; Psaroulaki, A. Carriage of Rickettsia spp., Coxiella burnetii and Anaplasma spp. by endemic and migratory wild birds and their ectoparasites in Cyprus. Clin. Microbiol. Infect. 2009, 15, 158–160. [Google Scholar] [CrossRef] [Green Version]
  13. Mukherjee, N.; Beati, L.; Sellers, M.; Burton, L.; Adamson, S.; Robbins, R.G.; Moore, F.; Karim, S. Importation of exotic ticks and tick-borne spotted fever group rickettsiae into the United States by migrating songbirds. Ticks Tick-Borne Dis. 2013, 5, 127–134. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  14. Hornok, S.; Kováts, D.; Csörgő, T.; Meli, M.L.; Gönczi, E.; Hadnagy, Z.; Takács, N.; Farkas, R.; Hofmann-Lehmann, R. Birds as potential reservoirs of tick-borne pathogens: First evidence of bacteraemia with Rickettsia helvetica. Parasites Vectors 2014, 7, 128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Ebani, V.V.; Bertelloni, F.; Mani, P. Molecular survey on zoonotic tick-borne bacteria and chlamydiae in feral pigeons (Columba livia domestica). Asian Pac. J. Trop. Med. 2016, 9, 324–327. [Google Scholar] [CrossRef] [PubMed]
  16. Parsons, N.J.; Gous, T.A.; Cranfield, M.R.; Cheng, L.I.; Schultz, A.; Horne, E.; Last, R.P.; Lampen, F.; Ludynia, K.; Bousfield, B.; et al. Novel vagrant records and occurence of vevctor-borne pathogens in King Penguins (Aptenodytes patagonicus) in South Africa. Polar Biol. 2018, 41, 79–86. [Google Scholar] [CrossRef]
  17. Ebani, V.V.; Bertelloni, F.; Mani, P. Serological evidence of exposure to zoonotic tick-borne bacteria in pheasants (Phasianus colchicus). Ann. Agric. Environ. Med. 2017, 24, 82–85. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Kelly, P.J.; Masanvi, N.; Cadman, H.F.; Mahan, S.M.; Beati, L.; Raoult, D. Serosurvey for Cowdria ruminantium, Coxiella burnetii, and Spotted Fever Group Rickettsiae in Ostriches (Struthio camelus) from Zimbabwe. Avian Dis. 1996, 40, 448. [Google Scholar] [CrossRef] [PubMed]
  19. Zemtsova, G.E.; Montgomery, M.; Levin, M.L. Relative Sensitivity of Conventional and Real-Time PCR Assays for Detection of SFG Rickettsia in Blood and Tissue Samples from Laboratory Animals. PLoS ONE 2015, 10, e0116658. [Google Scholar] [CrossRef] [PubMed]
  20. Santos-Silva, M.M.; Sousa, R.; Santos, A.S.; Melo, P.; Encarnação, V.; Bacellar, F. Ticks Parasitizing Wild Birds in Portugal: Detection of Rickettsia aeschlimannii, R. helvetica and R. massiliae. Exp. Appl. Acarol. 2006, 39, 331–338. [Google Scholar] [CrossRef]
  21. Graham, R.I.; Mainwaring, M.C.; Du Feu, R. Detection of spotted fever group Rickettsia spp. from bird ticks in the U.K. Med. Vet. Entomol. 2010, 24, 340–343. [Google Scholar] [CrossRef] [PubMed]
  22. Pajoro, M.; Pistone, D.; Boccazzi, I.V.; Mereghetti, V.; Bandi, C.; Fabbi, M.; Scattorin, F.; Sassera, D.; Montagna, M. Molecular screening for bacterial pathogens in ticks (Ixodes ricinus) collected on migratory birds captured in northern Italy. Folia Parasitol. 2018, 65, 8. [Google Scholar] [CrossRef]
  23. Hajduskova, E.; Literak, I.; Papousek, I.; Costa, F.B.; Novakova, M.; Labruna, M.B.; Zdrazilova-Dubska, L. ‘Candidatus Rickettsia mendelii’, a novel basal group rickettsia detected in Ixodes ricinus ticks in the Czech Republic. Ticks Tick-Borne Dis. 2016, 7, 482–486. [Google Scholar] [CrossRef] [PubMed]
  24. Wallménius, K.; Barboutis, C.; Fransson, T.; Jaenson, T.G.; Lindgren, P.-E.; Nyström, F.; Olsen, B.; Salaneck, E.; Nilsson, K. Spotted fever Rickettsia species in Hyalomma and Ixodes ticks infesting migratory birds in the European Mediterranean area. Parasites Vectors 2014, 7, 318. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  25. Klitgaard, K.; Højgaard, J.; Isbrand, A.; Madsen, J.J.; Thorup, K.; Bødker, R. Screening for multiple tick-borne pathogens in Ixodes ricinus ticks from birds in Denmark during spring and autumn migration seasons. Ticks Tick-Borne Dis. 2019, 10, 546–552. [Google Scholar] [CrossRef] [PubMed]
  26. Lommano, E.; Dvořák, C.; Vallotton, L.; Jenni, L.; Gern, L. Tick-borne pathogens in ticks collected from breeding and migratory birds in Switzerland. Ticks Tick-Borne Dis. 2014, 5, 871–882. [Google Scholar] [CrossRef]
  27. Elfving, K.; Olsen, B.; Bergström, S.; Waldenström, J.; Lundkvist, A.; Sjöstedt, A.; Mejlon, H.; Nilsson, K. Dissemination of Spotted Fever Rickettsia Agents in Europe by Migrating Birds. PLoS ONE 2010, 5, e8572. [Google Scholar] [CrossRef] [Green Version]
  28. Špitalská, E.; Literák, I.; Kocianová, E.; Taragel’Ová, V. The Importance of Ixodes arboricolain Transmission of Rickettsia spp., Anaplasma phagocytophilum, and Borrelia burgdorferi Sensu Lato in the Czech Republic, Central Europe. Vector-Borne Zoonotic Dis. 2011, 11, 1235–1241. [Google Scholar] [CrossRef] [PubMed]
  29. Rollins, R.E.; Schaper, S.; Kahlhofer, C.; Frangoulidis, D.; Strauß, A.F.; Cardinale, M.; Springer, A.; Strube, C.; Bakkes, D.K.; Becker, N.S.; et al. Ticks (Acari: Ixodidae) on birds migrating to the island of Ponza, Italy, and the tick-borne pathogens they carry. Ticks Tick-Borne Dis. 2020, 12, 101590. [Google Scholar] [CrossRef] [PubMed]
  30. Martínez-Sánchez, E.T.; Cardona-Romero, M.; Ortiz-Giraldo, M.; Tobón-Escobar, W.D.; Moreno-López, D.; Ossa-López, P.A.; Pérez-Cárdenas, J.E.; Labruna, M.B.; Martins, T.F.; Castaño-Villa, G.J.; et al. Rickettsia spp. in ticks (Acari: Ixodidae) from wild birds in Caldas, Colombia. Acta Trop. 2020, 213, 105733. [Google Scholar] [CrossRef] [PubMed]
  31. De Abreu, D.P.B.; Peixoto, M.P.; Luz, H.R.; Zeringóta, V.; Santolin, D.A.C.; Famadas, K.M.; Faccini, J.L.H.; McIntosh, D. Two for the price of one: Co-infection with Rickettsia Bellii and spotted fever group Rickettsia in Amblyomma (Acari: Ixodidae) ticks recovered from wild birds in Brazil. Ticks Tick-Borne Dis. 2019, 10, 101266. [Google Scholar] [CrossRef] [PubMed]
  32. Rocha, J.M.; de Oliveira, P.B.; Martins, T.F.; Faccini, J.L.H.; Sevá, A.P.; Luz, H.R.; Albuquerque, G.R. Diversity of ticks and detection of Rickettsia Amblyommatis infecting ticks on wild birds in anthropogenic landscapes in Bahia state, northeast Brazil. Exp. Appl. Acarol. 2021, 84, 227–239. [Google Scholar] [CrossRef] [PubMed]
  33. Zeringóta, V.; Maturano, R.; Luz, H.R.; Senra, T.O.S.; Daemon, E.; Faccini, J.L.H.; McIntosh, D. Molecular detection of Rickettsia rhipicephali and other spotted fever group Rickettsia species in Amblyomma ticks infesting wild birds in the state of Minas Gerais, Brazil. Ticks Tick-Borne Dis. 2017, 8, 81–89. [Google Scholar] [CrossRef]
  34. Chastel, C.; Demazure, M.; Chastel, O.; Genevois, F.; Legrand, M.C.; Grulet, O.; Odermatt, M.; Le Goff, F. A rickettsia-like organism from Ixodes uriae ticks collected on the Kerguelen Islands (French Subantarctic Territories). Acta Virol. 1993, 37, 11–20. [Google Scholar] [PubMed]
  35. Latas, P.; Auckland, L.D.; Teel, P.D.; Hamer, S.A. Argas (Persicargas) giganteus soft tick infection with Rickettsia hoogstraalii and relapsing fever Borrelia on wild avian species of the desert southwest, USA. J. Wild. Dis. 2020, 56, 113–125. [Google Scholar] [CrossRef] [PubMed]
  36. Diop, A.; Barker, S.; Eberhard, M.; Barker, D.; Nguyen, T.T.; Di Pinto, F.; Raoult, D.; Mediannikov, O. Rickettsia fournieri sp. nov., a novel spotted fever group rickettsia from Argas lagenoplastis ticks in Australia. Int. J. Syst. Evol. Microbiol. 2018, 68, 3781–3784. [Google Scholar] [CrossRef]
  37. Kim, H.-C.; Jiang, J.; Hang, J.; Kim, S.Y.; Yun, S.-M.; Park, C.-U.; Kim, M.; Chong, S.-T.; Farris, C.M.; Richards, A.L.; et al. Detection of Rickettsia lusitaniae Among Ornithodoros sawaii Soft Ticks Collected from Japanese Murrelet Seabird Nest Material from Gugul Island, Republic of Korea. J. Med Entomol. 2021, 58, 1376–1383. [Google Scholar] [CrossRef] [PubMed]
  38. Kawabata, H.; Ando, S.; Kishimoto, T.; Kurane, I.; Takano, A.; Nogami, S.; Fujita, H.; Tsurumi, M.; Nakamura, N.; Sato, F.; et al. First Detection of Rickettsiain Soft-Bodied Ticks Associated with Seabirds, Japan. Microbiol. Immunol. 2006, 50, 403–406. [Google Scholar] [CrossRef]
  39. Reeves, W.K.; Loftis, A.D.; Sanders, F.; Spinks, M.D.; Wills, W.; Denison, A.; Dasch, G. Borrelia, Coxiella, and Rickettsia in Carios capensis (Acari: Argasidae) from a brown pelican (Pelecanus occidentalis) rookery in South Carolina, USA. Exp. Appl. Acarol. 2006, 39, 321–329. [Google Scholar] [CrossRef] [PubMed]
  40. Lafri, I.; Leulmi, H.; Baziz-Neffah, F.; Lalout, R.; Mohamed, C.; Mohamed, K.; Parola, P.; Bitam, I. Detection of a novel Rickettsia sp. in soft ticks (Acari: Argasidae) in Algeria. Microbes Infect. 2015, 17, 859–861. [Google Scholar] [CrossRef] [PubMed]
  41. Dietrich, M.; Lebarbenchon, C.; Jaeger, A.; Le Rouzic, C.; Bastien, M.; Lagadec, E.; McCoy, K.D.; Pascalis, H.; Le Corre, M.; Dellagi, K.; et al. Rickettsia spp. in Seabird Ticks from Western Indian Ocean Islands, 2011–2012. Emerg. Infect. Dis. 2014, 20, 838–842. [Google Scholar] [CrossRef] [PubMed]
  42. Vilcins, I.-M.E.; Old, J.; Deane, E.M. Molecular detection of Rickettsia, Coxiella and Rickettsiella DNA in three native Australian tick species. Exp. Appl. Acarol. 2009, 49, 229–242. [Google Scholar] [CrossRef] [PubMed]
  43. Sprong, H.; Wielinga, P.R.; Fonville, M.; Reusken, C.; Brandenburg, A.H.; Borgsteede, F.; Gaasenbeek, C.; van der Giessen, J.W. Ixodes ricinus ticks are reservoir hosts for Rickettsia helvetica and potentially carry flea-borne Rickettsia species. Parasites Vectors 2009, 2, 41. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  44. Krause, P.J. Human babesiosis. Int. J. Parasitol. 2019, 49, 165–174. [Google Scholar] [CrossRef] [PubMed]
  45. Schnittger, L.; Rodriguez, A.E.; Florin-Christensen, M.; Morrison, D.A. Babesia: A world emerging. Infect. Genet. Evol. 2012, 12, 1788–1809. [Google Scholar] [CrossRef] [PubMed]
  46. Jalovecka, M.; Sojka, D.; Ascencio, M.; Schnittger, L. Babesia Life Cycle—When Phylogeny Meets Biology. Trends Parasitol. 2019, 35, 356–368. [Google Scholar] [CrossRef]
  47. Bajer, A.; Dwużnik-Szarek, D. The specificity of Babesia-tick vector interactions: Recent advances and pitfalls in molecular and field studies. Parasites Vectors 2021, 14, 507. [Google Scholar] [CrossRef] [PubMed]
  48. Pierce, M.A. A taxonomic review of avian piroplasms of the genus Babesia Starcovici, 1893 (Apicomplexa: Piroplasmorida: Babesiidae). J. Nat. History 2000, 34, 317–332. [Google Scholar] [CrossRef]
  49. Remple, J.D. Intracellular Hematozoa of Raptors: A Review and Update. J. Avian Med. Surg. 2004, 18, 75–88. [Google Scholar] [CrossRef]
  50. Brossy, J.; Plös, A.; Blackbeard, J.; Kline, A. Diseases acquired by captive penguins: What happens when they are released into the wild? Mar. Ornithol. 1999, 27, 185–186. [Google Scholar]
  51. Snyman, A.; Vanstreels, R.E.T.; Nell, C.; Schaefer, A.M.; Stracke, T.; Parsons, N.J.; Ludynia, K.; Pistorius, P.A. Determinants of external and blood parasite load in African penguins (Spheniscus Demersus) admitted for rehabilitation. Parasitology 2020, 147, 577–583. [Google Scholar] [CrossRef] [PubMed]
  52. Paparini, A.; McInnes, L.M.; Di Placido, D.; Mackereth, G.; Tompkins, D.M.; Clough, R.; Ryan, U.M.; Irwin, P.J. Piroplasms of New Zealand seabirds. Parasitol. Res. 2014, 113, 4407–4414. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Schurenkova, A.I. Sogdianella moshkovskii gen. nov. sp. nov. A parasite belonging to the Pinoplasmidea in a raptorial bird, Gypaetus Barb. (L.). Med. Parazitol. Parazitar. Bolezni 1938, 7, 932–937. [Google Scholar]
  54. Laird, M.; Lari, F.A. The avian blood parasite Babesia moshkosvkii (Schunenkova, 1938), with a record from Corvus splendens. Vieillot in Pakistan. Can. J. Zool. 1957, 35, 783–795. [Google Scholar] [CrossRef]
  55. Peirce, M.A.; Jakob-Hoff, R.M.; Twentyman, C. New species of haematozoa from Apterygidae in New Zealand. J. Nat. Hist. 2003, 37, 1797–1804. [Google Scholar] [CrossRef]
  56. Yabsley, M.J.; Greiner, E.; Tseng, F.S.; Garner, M.M.; Nordhausen, R.W.; Ziccardi, M.H.; Borjesson, D.L.; Zabolotzky, S. Description of Novel Babesia Species and Associated Lesions from Common Murres (Uria aalge) from California. J. Parasitol. 2009, 95, 1183–1188. [Google Scholar] [CrossRef] [PubMed]
  57. Peirce, M.; Parsons, N. Babesia ugwidiensis, a new species of Avian piroplasm from Phalacrocoracidae in South Africa. Parasite 2012, 19, 375–379. [Google Scholar] [CrossRef] [Green Version]
  58. Yabsley, M.J.; Vanstreels, R.E.; Shock, B.C.; Purdee, M.; Horne, E.C.; Peirce, M.A.; Parsons, N.J. Molecular characterization of Babesia peircei and Babesia ugwidiensis provides insight into the evolution and host specificity of avian piroplasmids. Int. J. Parasitol. Parasites Wildl. 2017, 6, 257–264. [Google Scholar] [CrossRef] [PubMed]
  59. Willette, M.; Ponder, J.; Cruz-Martinez, L.; Arent, L.; Padilla, I.B.; De Francisco, O.N.; Redig, P. Management of Select Bacterial and Parasitic Conditions of Raptors. Vet. Clin. North Am. Exot. Anim. Pract. 2009, 12, 491–517. [Google Scholar] [CrossRef]
  60. Chavatte, J.-M.; Okumura, C.; Landau, I. Redescription of Babesia ardeae Toumanoff, 1940, a parasite of Ardeidae, including molecular characterization. Parasitol. Res. 2017, 116, 1089–1097. [Google Scholar] [CrossRef] [PubMed]
  61. Vanstreels, R.E.T.; Woehler, E.J.; Ruoppolo, V.; Vertigan, P.; Carlile, N.; Priddel, D.; Finger, A.; Dann, P.; Herrin, K.V.; Thompson, P.; et al. Epidemiology and molecular phylogeny of Babesia sp. in Little Penguins Eudyptula minor in Australia. Int. J. Parasitol. Parasites Wildl. 2015, 4, 198–205. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Quillfeldt, P.; Martínez, J.; Bugoni, L.; Mancini, P.L.; Merino, S. Blood parasites in noddies and boobies from Brazilian offshore islands—Differences between species and influence of nesting habitat. Parasitology 2013, 141, 399–410. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  63. Vanstreels, R.E.T.; Braga, E.; Catão-Dias, J.L. Blood parasites of penguins: A critical review. Parasitology 2016, 143, 931–956. [Google Scholar] [CrossRef] [PubMed]
  64. Tarello, W. Effective imidocarb dipropionate therapy for Babesia shortti in falcons. Vet. Rec. 2006, 158, 239–240. [Google Scholar] [CrossRef] [PubMed]
  65. Parsons, N.; Voogt, N.; Schaefer, A.; Peirce, M.; Vanstreels, R. Occurrence of blood parasites in seabirds admitted for rehabilitation in the Western Cape, South Africa, 2001–2013. Vet. Parasitol. 2017, 233, 52–61. [Google Scholar] [CrossRef]
  66. Sergent, N.; Rogers, T.; Cunningham, M. Influence of biological and ecological factors on hematological values in wild Little Penguins, Eudyptula minor. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2004, 138, 333–339. [Google Scholar] [CrossRef]
  67. Parsons, N.J.; Gous, T.A.; Schaefer, A.M.; Vanstreels, R.E. Health evaluation of African penguins (Spheniscus demersus) in southern Africa. Onderstepoort J. Vet. Res. 2016, 83, 13. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  68. Vanstreels, R.E.T.; Hurtado, R.; Snyman, A.; Roberts, D.G.; Parsons, N.J.; Pistorius, P. Empirical Primaquine Treatment of Avian Babesiosis in Seabirds. J. Avian Med. Surg. 2019, 33, 258–264. [Google Scholar] [CrossRef]
  69. Yakunin, M.P.; Krivkova, A.M. New blood parasite species of the family Babesiidae (Piroplasmidae) in birds. Parazitol. Leningr. 1971, 5, 462–465. [Google Scholar]
  70. Peirce, M. Nuttallia França, 1909 (babesiidae) preoccupied by Nuttallia Dall, 1898 (psammobiidae): A re-appraisal of the taxonomic position of the avian piroplasms. Int. J. Parasitol. 1975, 5, 285–287. [Google Scholar] [CrossRef]
  71. Toumanoff, C. Le parasite sanguin endoglobulaire du héron cendré de L’Indochine (Ardea cinerea var. rectirostris Gould), Babesia (Nicollia) ardeae nov. sp. Revue Medicale Francaise d’Extreme Orient 1940, 19, 491–496. [Google Scholar]
  72. Mohammed, A.H.H. Systematic and Experimental Studies on Protozoal Blood Parasites of Egyptian Birds; Cairo University Press: Cairo, Egypt, 1958; pp. 77–104. [Google Scholar]
  73. Corradetti, A.; Scanga, M. Segnalazione in Europa di Babesia shortti (Mohammed, 1958) in Falco tinnunculus tinnunculus e brevi note su questo parassita. Parassitologia 1964, 6, 77–80. [Google Scholar]
  74. Merino, S. Babesia bennetti n. sp. from the yellow-legged gull (Larus cachinnans, Aves, Laridae) on Benidorm Island, Mediterranean Sea. J. Parasitol. 1998, 84, 422. [Google Scholar] [CrossRef]
  75. Earlé, R.; Huchzermeyer, F.; Bennett, G.; Brossy, J. Babesia peircei sp. nov. from the jackass penguin. S. Afr. J. Zool. 1993, 28, 88–90. [Google Scholar] [CrossRef]
  76. Work, T.; Rameyer, R.A. Description and Epizootiology of Babesia poelea n. sp. in Brown Boobies (Sula leucogaster (Boddaert)) on Sand Island, Johnston Atoll, Central Pacific. J. Parasitol. 1997, 83, 734–738. [Google Scholar] [CrossRef] [Green Version]
  77. Karshima, S.N.; Karshima, M.N.; Ahmed, M.I. Animal reservoirs of zoonotic Babesia species: A global systematic review and meta-analysis of their prevalence, distribution and species diversity. Vet. Parasitol. 2021, 298, 109539. [Google Scholar] [CrossRef]
  78. Hasle, G. Transport of ixodid ticks and tick-borne pathogens by migratory birds. Front. Cell. Infect. Microbiol. 2013, 3, 48. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  79. Flaisz, B.; Sulyok, K.M.; Kováts, D.; Kontschán, J.; Csörgő, T.; Csipak, Á.; Gyuranecz, M.; Hornok, S. Babesia genotypes in Haemaphysalis concinna collected from birds in Hungary reflect phylogeographic connections with Siberia and the Far East. Ticks Tick-Borne Dis. 2017, 8, 666–670. [Google Scholar] [CrossRef] [PubMed]
  80. Dwużnik-Szarek, D.; Mierzejewska, E.J.; Alsarraf, M.; Alsarraf, M.; Bajer, A. Pathogens detected in the tick Haemaphysalis concinna in Western Poland: Known and unknown threats. Exp. Appl. Acarol. 2021, 84, 769–783. [Google Scholar] [CrossRef] [PubMed]
  81. Madison-Antenucci, S.; Kramer, L.D.; Gebhardt, L.L.; Kauffman, E. Emerging Tick-Borne Diseases. Clin. Microbiol. Rev. 2020, 33, e00083-18. [Google Scholar] [CrossRef] [PubMed]
  82. Yang, Y.; Christie, J.; Köster, L.; Du, A.; Yao, C. Emerging Human Babesiosis with “Ground Zero” in North America. Microorganisms 2021, 9, 440. [Google Scholar] [CrossRef]
  83. Scott, J.; Pascoe, E.; Sajid, M.; Foley, J. Detection of Babesia odocoilei in Ixodes scapularis Ticks Collected in Southern Ontario, Canada. Pathogens 2021, 10, 327. [Google Scholar] [CrossRef] [PubMed]
  84. Gray, J.; Zintl, A.; Hildebrandt, A.; Hunfeld, K.-P.; Weiss, L. Zoonotic babesiosis: Overview of the disease and novel aspects of pathogen identity. Ticks Tick-Borne Dis. 2010, 1, 3–10. [Google Scholar] [CrossRef]
  85. Young, K.M.; Corrin, T.; Wilhelm, B.; Uhland, C.; Greig, J.; Mascarenhas, M.; Waddell, L.A. Zoonotic Babesia: A scoping review of the global evidence. PLoS ONE 2019, 14, e0226781. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Homer, M.J.; Aguilar-Delfin, I.; Telford, S.R., III; Krause, P.J.; Persing, D.H. Babesiosis. Clin. Microbiol. Rev. 2000, 13, 451–469. [Google Scholar] [CrossRef] [PubMed]
  87. Hamšíková, Z.; Kazimírová, M.; Haruštiaková, D.; Mahríková, L.; Slovák, M.; Berthová, L.; Kocianová, E.; Schnittger, L. Babesia spp. in ticks and wildlife in different habitat types of Slovakia. Parasites Vectors 2016, 9, 292. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  88. Acharyya, S.G.; Khandelwal, A.; Kain, V.; Kumar, A.; Samajdar, J. Surface working of 304L stainless steel: Impact on microstructure, electrochemical behavior and SCC resistance. Mater. Charact. 2012, 72, 68–76. [Google Scholar] [CrossRef]
  89. Gray, J.S.; Estrada-Peña, A.; Zintl, A. Vectors of Babesiosis. Annu. Rev. Entomol. 2019, 64, 149–165. [Google Scholar] [CrossRef] [PubMed]
  90. Scott, J.; Sajid, M.; Pascoe, E.; Foley, J. Detection of Babesia odocoilei in Humans with Babesiosis Symptoms. Diagnostics 2021, 11, 947. [Google Scholar] [CrossRef]
  91. Poupon, M.-A.; Lommano, E.; Humair, P.-F.; Douet, V.; Rais, O.; Schaad, M.; Jenni, L.; Gern, L. Prevalence of Borrelia burgdorferi Sensu Lato in Ticks Collected from Migratory Birds in Switzerland. Appl. Environ. Microbiol. 2006, 72, 976–979. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  92. Franke, J.; Fritzsch, J.; Tomaso, H.; Straube, E.; Dorn, W.; Hildebrandt, A. Coexistence of Pathogens in Host-Seeking and Feeding Ticks within a Single Natural Habitat in Central Germany. Appl. Environ. Microbiol. 2010, 76, 6829–6836. [Google Scholar] [CrossRef] [Green Version]
  93. Hildebrandt, A.; Franke, J.; Meier, F.; Sachse, S.; Dorn, W.; Straube, E. The potential role of migratory birds in transmission cycles of Babesia spp., Anaplasma phagocytophilum, and Rickettsia spp. Ticks Tick-Borne Dis. 2010, 1, 105–107. [Google Scholar] [CrossRef] [PubMed]
  94. Capligina, V.; Salmane, I.; Keišs, O.; Vilks, K.; Japina, K.; Baumanis, V.; Ranka, R. Prevalence of tick-borne pathogens in ticks collected from migratory birds in Latvia. Ticks Tick-Borne Dis. 2014, 5, 75–81. [Google Scholar] [CrossRef]
  95. Movila, A.; Reye, A.L.; Dubinina, H.V.; Tolstenkov, O.O.; Toderas, I.; Hübschen, J.M.; Muller, C.P.; Alekseev, A.N. Detection of Babesia Sp. EU1 and Members of Spotted Fever Group Rickettsiae in Ticks Collected from Migratory Birds at Curonian Spit, North-Western Russia. Vector-Borne Zoonotic Dis. 2011, 11, 89–91. [Google Scholar] [CrossRef] [PubMed]
  96. Wilhelmsson, P.; Pawełczyk, O.; Jaenson, T.G.T.; Waldenström, J.; Olsen, B.; Forsberg, P.; Lindgren, P.-E. Three Babesia species in Ixodes ricinus ticks from migratory birds in Sweden. Parasites Vectors 2021, 14, 183. [Google Scholar] [CrossRef] [PubMed]
  97. Kuo, C.-C.; Lin, Y.-F.; Yao, C.-T.; Shih, H.-C.; Chung, L.-H.; Liao, H.-C.; Lo-Hsuan, C.; Wang, H.-C. Tick-borne pathogens in ticks collected from birds in Taiwan. Parasites Vectors 2017, 10, 587. [Google Scholar] [CrossRef] [Green Version]
  98. Hersh, M.H.; Tibbetts, M.; Strauss, M.; Ostfeld, R.; Keesing, F. Reservoir Competence of Wildlife Host Species for Babesia microti. Emerg. Infect. Dis. 2012, 18, 1951–1957. [Google Scholar] [CrossRef]
  99. Scott, J.D.; Clark, K.L.; Durden, L.A. Presence of Babesia odocoilei and Borrelia burgdorferi Sensu Stricto in a Tick and Dual Parasitism of Amblyomma inornatum and Ixodes scapularis on a Bird in Canada. Healthcare 2019, 7, 46. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  100. Milnes, E.L.; Thornton, G.; Léveillé, A.N.; Delnatte, P.; Barta, J.R.; Smith, D.A.; Nemeth, N. Babesia odocoilei and zoonotic pathogens identified from Ixodes scapularis ticks in southern Ontario, Canada. Ticks Tick-Borne Dis. 2019, 10, 670–676. [Google Scholar] [CrossRef] [PubMed]
  101. Scott, J.D.; Pascoe, E.L.; Sajid, M.S.; Foley, J.E. Detection of Babesia odocoilei in Ixodes scapularis Ticks Collected from Songbirds in Ontario and Quebec, Canada. Pathogens 2020, 9, 781. [Google Scholar] [CrossRef] [PubMed]
  102. Øines, Ø.; Radzijevskaja, J.; Paulauskas, A.; Rosef, O. Prevalence and diversity of Babesia spp. in questing Ixodes ricinus ticks from Norway. Parasites Vectors 2012, 5, 156. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  103. Georgopoulou, I.; Tsiouris, V. The potential role of migratory birds in the transmission of zoonozis. Vet. Ital. 2008, 44, 671–677. [Google Scholar] [PubMed]
  104. Mircea, G.B.; Ioana, D.; Emoke, P.; Mihaela, N.; Marina, S. Wild birds as potential vectors for pathogen dissemination on migration routes in the Danube Delta Wetlands. Int. J. Curr. Microbiol. App. Sci. 2014, 3, 890–897. [Google Scholar]
Table
Table 1. Rickettsia agents detected in different avian species.
Table 1. Rickettsia agents detected in different avian species.
Bird SpeciesCommon NameTest (Sample)Rickettsia Agent DetectedGeographical
Distribution		Reference
Gallinula chloropusCommon moorhenPCR (blood)Rickettsia sp.Cyprus[12]
Phoenicopterus ruberAmerican flamingoPCR (blood)Rickettsia spCyprus[12]
Hylocichla mustelinaWood thrushPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Passerina cirisPainted buntingPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Wilsonia citrinaHooded warblerPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Passerina cyaneaIndigo buntingPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Geothlypis trichasCommon yellowthroatPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Helmitheros vermivorusWorm-eating warblerPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Pheucticus ludoviacianusRose-breasted grosbeakPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Oporomis formosusKentucky warblerPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Catharus ustulatusSwainson’s thrushPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Melospiza georgianaSwamp sparrowPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Empidonax virescensAcadian flycatcherPCR (blood)Rickettsia sp. “Argentina”/REALouisiana (USA)[13]
Erithacus rubeculaRobinPCR (blood)Rickettsia helveticaHungary[14]
Prunella modularisDunnockPCR (blood)Rickettsia helveticaHungary[14]
Columba livia domesticaFeral pigeonPCR (spleen)Rickettsia sp.Italy[15]
Aptenodytes patagonicusKing penguinSmear (blood)Rickettsia-likeSouth Africa[16]
Phasianus colchicusPheasantIFI (blood serum)SFG Rickettsia sp.Italy[17]
Struthio camelusOstrichIFI (blood serum)SFG Rickettsia sp.Zimbabwe[18]
Legend. IFI: indirect immunofluorescence test; PCR: polymerase chain reaction; REA: Rickettsia endosymbiont of Amblyomma maculatum; SFG: spotted fever group.
Table
Table 2. First description of avian Babesia spp. (modified from Pierce, 2000).
Table 2. First description of avian Babesia spp. (modified from Pierce, 2000).
Bird FamilyTestBabesia SpeciesGeographical DistributionReferences
AccipitridaeMicroscopyBabesia moshkovskiiTadjikistan, Pakistan[53,54]
AlaudidaeMicroscopyBabesia kazachstanicaKazachstan[69,70]
ApterygidaeMicroscopyBabesia kiwiensisNew Zealand[55]
ArdeinaeMicroscopyBabesia ardeaeIndochina[71]
CorvidaeMicroscopyBabesia frugilegicaKazachstan, Pakistan[69,70]
EmberyzinaeMicroscopyBabesia emberizicaKazachstan[69,70]
FalconidaeMicroscopyBabesia shorttiEgypt, Italy[72,73]
GruidaeMicroscopyBabesia balearicaeEgypt[70,72]
HirundinidaeMicroscopyBabesia rusticaKazachstan, Kenya[69,70]
LaridaeMicroscopyBabesia bennettiSpain[74]
PasseridaeMicroscopyBabesia mujunkumicaKazachstan[69,70]
SpheniscidaeMicroscopyBabesia peirceiSouth Africa[75]
SulidaeMicroscopyBabesia poeleaSand Island, Johnston Atoll, Central Pacific[76]
UpupidaeMicroscopyBabesia kryloviKazachstan[69,70]
AlcidaeMicroscopy and PCRBabesia uriaeCalifornia (US)[56]
PhalacrocidaeMicroscopyBabesia ugwidiensisSouth Africa[57]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Ebani, V.V.; Mancianti, F. Potential Role of Avian Populations in the Epidemiology of Rickettsia spp. and Babesia spp. Vet. Sci. 2021, 8, 334. https://doi.org/10.3390/vetsci8120334

AMA Style

Ebani VV, Mancianti F. Potential Role of Avian Populations in the Epidemiology of Rickettsia spp. and Babesia spp. Veterinary Sciences. 2021; 8(12):334. https://doi.org/10.3390/vetsci8120334

Chicago/Turabian Style

Ebani, Valentina Virginia, and Francesca Mancianti. 2021. "Potential Role of Avian Populations in the Epidemiology of Rickettsia spp. and Babesia spp." Veterinary Sciences 8, no. 12: 334. https://doi.org/10.3390/vetsci8120334

APA Style

Ebani, V. V., & Mancianti, F. (2021). Potential Role of Avian Populations in the Epidemiology of Rickettsia spp. and Babesia spp. Veterinary Sciences, 8(12), 334. https://doi.org/10.3390/vetsci8120334

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop