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Prevalence of Caryospora Species (Apicomplexa: Eimeriidae) in Falcons in the United Arab Emirates.

Abstract: A total of 3975 fecal samples, originated from the same number of individual birds, from 7 dedicated falcon hospitals, were examined to determine the prevalence of Caryospora species in the falcon population used in the sport of falconry in the United Arab Emirates (UAE). From that total, 297 (7.5%) were positive for the presence of Caryospora species. The falcons were all captive bred within the UAE and abroad, mainly from Germany, Spain, the United States, and Canada. Positive samples for the presence of Caryospora species were sporulated, and the taxonomy was established based on morphologic characteristics. The results showed the prevalence of the following Caryospora species: C kutzeri 41.4%, C neofalconis 25.6%, C megafalconis 18.2%, C falconis 10.4%, C cherrughi 3.7%, and C boeri 0.7%. The prevalence of Caryospora species among the various falcon species in this study was: gyr X peregrine hybrid falcons (Falco rusticolus X Falco peregrinus), 27.3%; gyr falcons (Falco rusticolus), 25.6%; peregrine falcons (Falco peregrinus), 20.5%; saker falcons (Falco cherrug), 16.5%; gyr X saker hybrid falcons (Falco rusticolus X Falco cherrug), 8.1%; Eurasian kestrels (Falco tinnunculus), 1%; red-napped shaheen (Falco pelegrinoides babylonicus), 0.7%; and American kestrels (Falco sparverius), 0.3%.

Key words: Apicomplexa, Caryospora, coccidiosis, Eimeriidae, Middle East, prevalence, falcons, Falco species

Introduction

Taxonomically, Caryospora species, belong to Eukaryota domain, Corticata superkingdom, Chromista kingdom, Harosa subkingdom, Halvaria infrakingdom, Alveolata superphylum, the Miozoa phylum, Myzozoa subphylum, Avicomplexa infraphylum, the Sporozoa superclass, Coccidiomorphea class, Coccidia subclass, the Eimeriida order, and the Eimeriidae family and consists of cyst-forming protozoan parasites found in the intestine of various species of reptiles and birds. (1-7) The genus Caryospora is considered the third largest genus in the Eimeriidae family. (8)

Morphologically, the oocysts are spherical to ovoid and do not present a micropyle. They also contain a single spherical to subspherical sporocyst, without a Stieda body. The sporocyst contains 8 sporozoites and a round or granular residium body. The species is determined postsporulation, based on size and morphologic characteristics. (1,4)

As many as 150 different Caryospora species may exist in raptorial birds worldwide. (9) In falcons specifically, 8 Caryospora species are described, including C boeri, C biarmicusis, C cherrughi, C henryae, C kutzeri, C neofalconis, C megafalconis, and C falconis. All 8 species have been previously identified in falcons in the Middle East. (10-12)

Frequently, Caryospora species infection in captive falcons is acquired by direct transmission, (13,14) ingesting the oocyst-contaminated meat or water. Nevertheless, it is also possible by an indirect route (8) or facultative diheteroxenic life cycle, in which rodents act as transport hosts. (13,15,16) Experimental studies have demonstrated indirect transmission of C kutzeri by rodents in Eurasian kestrels (Falco tinnunculus), (17,18) although inside the paratenic hosts, there were no developmental stages or increased number of oocysts. (18) Oral inoculation of sporulated oocysts to host-specific species could produce patent infections, and oocysts fed to rodents are capable of transmitting to the definitive host. (19) Developmental stages in the definitive host consist of merogony, gamogony, fertilization, and formation of new oocysts in the intestinal epithelium, (1,14) and it takes 7 to 13 days to complete. (1,2) If the birds are treated during that period, they may develop an immune response and will not shed further oocysts. (20)

The presence of Caryospora species has been demonstrated often in free-living birds of prey, (3,7,8,21) although reports have shown that greater prevalence occurs in captive-bred falcons. (5,16,20,21) These studies demonstrated that the prevalence of caryosporiosis may vary from 12% to 86%. (9,16,20,21)

The clinical signs of Caryospora species infection in falcons depend on the age of the bird and the infective dose16 and consist of abdominal cramps, lethargy, fluffed appearance, weight loss, inappetence, vomiting, brownish or hemorrhagic diarrhea, and death in severe cases. (2,5,20,21) Falcons might suffer from thiamine deficiency, which occurs in infected falcons because of the vitamin use by the protozoan. (2)

The highest incidence and most severe clinical signs are seen in juvenile birds, especially birds younger than 3 months. (5,16,20) In juvenile raptors, such as merlins (Falco columbarius) (2) and Eurasian kestrels, (21) clinical caryosporiosis is characterized by severe diarrhea (7) or acute death in young chicks aged between 28 to 45 days, (3,22) although they do not show clinical signs until 27 days old, even if exposed earlier to the caryosporan oocysts. (2,22)

Caryosporiosis is difficult to control because of the lack of immunity in young birds and the persistence of infective oocysts in the environment. (9) The treatment combines targeted medication with husbandry management. (1) In falcons, the different types of therapeutic protocols tested currently have given unsatisfactory results for long-term protection. (2,3,5,16,19,20) With many therapeutic agents, the shedding of the oocysts stopped for a relative period but recommenced afterward. (2)

The significance of caryosporiosis in captive falcons is great, (8) and it considered one of the most important causes of morbidity in captive raptors, with a high mortality, particularly in small falcons, such as merlins. (22,23) A high infection load decreases the ability of falcons to perform well in training, hunting, and competitions, although in some cases, that was not found significant. (24) Extreme weight loss and even death may occur in severe cases, (9,12,21) especially when caryosporiosis is associated synergistically with clostridiosis. (25)

The main objective of this study was to determine the prevalence of Caryospora species in the falcon population present in the United Arab Emirates (UAE) and to establish the taxonomy of Caryospora species observed in fecal analyses, based on morphologic characteristics.

Materials and Methods

Source of oocysts

Between August 2015 and March 2016, a total of 3975 fecal samples, from the same number of individual birds, were collected from 7 dedicated falcon hospitals and microscopically evaluated by direct smear as part of the general examination. Positive samples for the presence of Caryospora species were stored and collected once a week. All falcons included in the study originated from captive-breeding centers within the UAE and abroad, but mainly from Germany, Spain, the United States, and Canada. The falcon species studied were: gyr falcon (Falco rusticolus), peregrine falcon (Falco peregrinus), gyr X peregrine hybrid falcon (F rusticolus X F peregrinus), saker falcon (Falco cherrug), gyr X saker hybrid falcons (F rusticolus X F cherrug), Eurasian kestrel, rednapped shaheen (Falco pelegrinoides babylonicus), black shaheen (Falco peregrinus peregrinator), lanner falcon (Falco biarmicus), American kestrel (Falco sparverius), and Eurasian hobby falcon (Falco subbuteo).

Processing and data collection

Samples were stored and processed in the Clinical Diagnostic Laboratory, Wildlife Division, Wrsan. The methodology included microscopic examination, sporulation, oocyst measurements, and photography. The species determination was done morphometrically, as sporulated coccidian oocysts differ in size and morphology. (1)

Fresh fecal samples were collected into 60-mL plastic tubes containing 1 mL 2.5% aqueous potassium dichromate solution (KyCryOy), (11,20) placed in cardboard boxes to avoid light, and allowed to sporulate. Most oocysts completed sporulation within 72-94 hours at 22 [+ or -] 2[degrees]C (71.6 [+ or -] 3.6[degrees]F). After that procedure, samples were mixed separately in Sheather's sucrose solution 1 : 1 (2.5 mL [K.sub.2][Cr.sub.2][O.sub.7] containing sporulated oocysts + 2.5 mL Sheather's solution) for floatation of oocysts and collection under a coverslip for 20 minutes in 5-mL plastic tubes. The coverslip was lifted and placed onto a slide for microscopic examination (Olympus BX41, with viewing mounted camera, Olympus DE71, Olympus Corp, Tokyo, Japan). The oocysts were identified with X10 magnification and measured at X40 and XI00 magnification with a calibrated ocular micrometer (eyepiece adapter CFIUW Xl0:25, Nikon Inc, Tokyo, Japan). The morphologic characteristics of the oocyst, wall, sporocyst, sporozoite, and residual body were determined in micrometers. Representative positive samples were stored under refrigeration at 4[degrees]C (39.2[degrees]F) in 2.5% [K.sub.2][Cr.sub.2][O.sub.7] for subsequent measuring, and identification. (2,11,26-28) Statistical analyses were performed with the SPSS Statistics 23.0 software (IBM, Armonk, NY, USA).

Results

From the 3975 fecal samples examined, 297 (7.5%) were positive for the presence of Caryospora species and the distribution was as follows: C kutzeri, 41.4% (123/297); C neofalconis, 25.6% (76/ 297); C megafalconis, 18.2% (54/297); C falconis, 10.4% (31/297); C cherrughi, 3.7% (11/297); and C boeri, 0.7% (2/297) (Fig 1).

In this study, measurements of oocysts, sporocysts, and sporozoites of the Caryospora species observed were obtained. The following measurements were established in micrometers: for C kutzeri, oocyst, 39.1 X 33.1 (33-46 X 28-40), sporocyst, 22.5 X 21.3 (18-26 X 16-26), and sporozoites, 4.6 (2-7 X 2-7); for C neofalconis, oocyst, 25.6 X 22.5 (20-30 X 19-28), sporocyst, 17.2 X 15.2 (13-19 X 12-19), and sporozoites, 9.9 X 2.4 (8-12 X 2^1); for C megafalconis, oocyst, 42.2 X 35.9 (39-49 X 30^10), sporocyst, 23.6 X 22.7 (21-27 X 20-26), and sporozoites, 16.5 X 4.2 (11-20 X 36); for C falconis, oocyst, 32.4 X 29.8 (29-36 X 2335), sporocyst, 21.7 X 20.6 (15-25 X 14-25), and sporozoites, 13.2 X 4.6 (10-17 X 2-4); for C cherrughi, oocyst, 33.7 X 28 (29-35 X 23-32), sporocyst, 22.6 X 18.9 (20-25 X 15-22), and sporozoites, 15 X 4(12-20 X 3-5); and for C boeri, oocyst, 38.5 x 31 (38-39 X 30-32), sporocyst, 24.5 X 20.5 (24-25 x 20-21), and sporozoites, 19 X 3.5 (18-20 X 3-4) (Table 1; Fig 2).

The prevalence of Caryospora species in the falcon species studied, from highest to the lowest percentage, was as follows: gyr X peregrine falcons 27.3% (81/297), gyr falcons 25.6% (76/297), peregrine falcons 20.5% (61/297), saker falcons 16.5% (49/297), gyr X saker falcons 8.1% (24/297), Eurasian kestrels 1.0% (3/297), red napped shaheen 0.7% (2/297), and American kestrel 0.3% (1/ 297) (Fig 3).

From the 297 cases with positive results for the presence of Caryospora species, 110 falcons were used for breeding, 71 for hunting, 67 for racing in competitions, and 49 were for sale at falcon centers. The age distribution of the falcons with positive results was 50.5% (150/297) adults (older than 1 year) and 49.5% (147/297) juveniles (3 to 10 months old). The sex distribution was 248 females and 49 males.

During this study, the presence of oocysts from 2 to 3 different Caryospora species was observed in the same falcon specimen, ie, in peregrine falcons, where C kutzeri and C neofalconis were identified. In a few cases, 3 Caryospora species were identified within the same peregrine falcon, namely C kutzeri, C neofalconis, and C falconis. In gyr falcons, the presence of C kutzeri and C neofalconis was observed in the same specimen.

Discussion

The results of this study showed that the falcon species with the greatest prevalence of Caryospora species in this population was the gyr x peregrine hybrid falcon (27.3%). This hybrid species is in great demand in the falcon trade for its high performance in hunting and competitions. However, the most valuable and desired species in Arab falconry is the gyr falcon. (29,30) The low number of individuals of this species within the study was due to the difficulty in breeding this species in captivity and their high price, making them less accessible to many falconers. Therefore, the most convenient solution is in the form of the gyr falcon crossed with the second most desired species, the peregrine falcon.

In a previous parasitologic study of falcons in Germany, a prevalence of Caryospora species of 12% was reported. (16) In a survey of free-living raptors in the United States, the prevalence was 31%.16 In Saudi Arabia, in a study regarding the causes of morbidity and mortality in falcons, Caryospora species was identified in 40% of the clinical cases brought into a veterinary facility. (31) In a similar survey done in the UK, the prevalence was reported to be as high as 24% (Fig 4). (22)

The Caryospora species with the greatest prevalence in the present study was C kutzeri at 41.4%. That could be the result of its wide distribution among falcon species and its high infectivity. This species represents an important health issue for falcons kept in rehabilitation and breeding centers and for raptors kept for falconry purposes. (4,5,32)

In a previous study, C kutzeri was reported as causing death in a Eurasian kestrel. (21) Moreover, that species was used successfully in previous studies of experimental transmission with laboratory mice (Mus musculus) and common voles (Microtus arvalis) in Eurasian kestrels. (16-18) In those studies, indirect transmission of C kutzeri by rodents was demonstrated. Moreover, C kutzeri was one of the species used to prepare a vaccine in an attempt to prevent the infection in falcons in the UK. (3) One parasitologic study from the Czech Republic demonstrated oocysts of C kulzeri in 11 of the 77 birds examined (14%). (32)

Although C kutzeri had the highest prevalence in our study, C neofalconis was reported as the source for the most severe cases of infections, especially in small-size falcons. (2,8,9,27) In the Czech Republic, 30 of 68 falcons (44%) were found infected with C neofalconis, showing clinical signs of diarrhea and lethargy. (32)

The size ranges of Caryospora species oocysts presented in this study were compared with those previously reported. The ranges of the oocyst size were similar to those previously reported, without significant differences in measurements. (1,11)

The host range of caryosporan species infecting birds of prey was not reported as crossing the Falco genus, and all cross-generic transmission, experimental attempts have failed. Attempts to induce the infection have failed when C neofalconis was inoculated into northern goshawks (Accipiter gentilis), long-eared owls (Asia otus), Eurasian eagle owls (Bubo bubo), common buzzards (Buteo buteo), and red kites (Milvus milvus). (13,26)

In our study, concurrent infection was observed in peregrine and gyr falcons, where C kulzeri and C neofalconis were identified. In addition, C falconis was found as the third concurrent species in some peregrine falcons. In other studies, oocysts of C kutzeri and C neofalconis were found in one Eurasian kestrel. (21) Repeated fecal examinations showed that C neofalconis was replaced by C kulzeri in 2 hobby falcons (Falco subbuteo) and 2 saker falcons. (20)

According to our results, the age of the falcons did not have an important role in the prevalence of Caryospora species. The number of juvenile falcons infected was similar to the number of adults (147/ 150), although reports have shown that the highest incidence and most severe clinical signs are identified in juvenile falcons, (5,16,20) especially falcons younger than 3 months. (2,22) The prevalence in the captive-bred falcons was high, reflecting the number of falcons bred in captivity worldwide, which is increasing annually. (29,31)

The worldwide spread of Caryospora species is facilitated when falcon breeders produce birds carrying Caryospora species and supply such birds to falconers throughout the world. (22) Studies have confirmed that the higher prevalence in raptors occurs in captive-bred birds. (5,16,20,22) Studies performed in the UK reflected 24% of captive-bred raptors were positive for the presence of Caryospora species, but none of the 72 samples from freeliving merlins had positive results. (22)

Caryosporiosis may have a considerably higher effect in captive-bred falcons and less importance in free-living birds because of the confined space of aviaries. Nevertheless, the loss or release of falcons carrying Caryospora species has a high risk of spreading the protozoan to the wild population, (2) mainly through mating and, rarely, through rodent vectors. (13,15,16)

The sex of the falcons with positive results in our study had an important role. Results showed remarkably greater prevalence in females (91.8%). However, that result is considered less relevant because Arab falconers have a high preference for the big size and aggressivity of the females. For that reason, the number of female birds was disproportional to males in the study.

The greatest prevalence was found in the breeding falcons (37%), followed by the hunting (23.9%), and the falcons used for competitions (22.5%). This was likely because of the seasonal examination of the birds: the breeder birds were brought to the clinics for general examination after relatively long periods of resting in the pens without prophylactic anticoccidials. Falcons that are used actively for hunting and competitions are generally examined at shorter intervals, and anticoccidial medication is often given prophylactically or for confirmed presence of Caryospora species.

Direct transmission of Caryospora species (13) is believed to occur when falcons from diverse localities are brought together into one confined place. In such falcon sales centers, overcrowding, poor hygiene, and handling and feeding with the same glove usually occur, and so, the distribution is facilitated. Previously identified factors that influence the prevalence in surveys of caryosporiosis are the source of the birds, the level of infection of the breeder falcons, and the age of birds. (2,5,16)

Most falconers and breeders have acknowledged the importance of caryosporiosis in falcons, and many were using preventative anticoccidial treatment at various times without the knowledge of their veterinarians. Studies have shown that sample collection during a 3-day period has a greater chance of detecting positive cases because of the alternating shedding of oocysts by infected falcons. (2) In the current study, single sample collection was used to assess the prevalence of Caryospora species among the falcons. Because of that, the prevalence of the Caryospora species could be much higher than the results shown in this study.

Acknowledgments: We thank HH Sheikh Sultan bin Zayed al Nahyan who supported this work. We thank all the people involved in this study, including Drs Lito Salazar, Jess Naldo, Raj Raghav, Modasir Malik, Marino Garcia Montijiano, Nelson Libanan, Naddim Uddin, Antonio Di Somma, and Panos Azmanis. We thank Drs Gheorghe Darabus and Narcisa Mederle for supervision of the PhD program of the junior author. We thank Merle Samour and Dr Melodiya Magno for their constant support and involvement and Angelito Viola for the consistent technical laboratory assistance.

References

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Victor D. S. Mateuta, DVM, and Jaime H. Samour, MVZ (Hons), PhD, Dipl ECZM (Avian)

From the Dubai Falcon Center, PO Box 1520, Dubai, United Arab Emirates (Mateuta); and the Wildlife Division, Wrsan. PO Box 77338, Abu Dhabi, United Arab Emirates (Samour).

Caption: Figure 2. Photomicrographs showing sporulated oocysts of Caryospora species identified in 297 falcons in the United Arab Emirates.

Caption: Figure 4. Prevalence of Caryospora species infection reported in falcons in different global regions.
Table 1. Caryospora species and descriptive morphologic
characteristics identified in 297 falcons (Falco species) of various
species in the United Arab Emirates.

                                       Oocysts size,
Caryospora                       [micro]m (range, [micro]m)
species           Oocyst shape     reference interval (1)

C kutzeri         Subspherical          39.1 X 33.1
                                      (33-46 X 28-40)
                                        38.7 X 34.1

C neofalconis     Subspherical          25.6 X 22.5
                                      (20-30 X 19-28)
                                         27 X 23.8

C megafalconis    Subspherical          42.2 X 35.9
                                      (39 49 X 30-40)
                                        43.6 X 35.8
C falconis        Spherical             32.4 X 29.8
                                      (29-36 X 2.3-35)
                                        29.5 X 36.5
C cherruglii      Ovoid                  33.7 X 2 8
                                      (29-35 X 23-32)
                                        32.1 X 29.3
C boeri           Subspherical           38.5 X 31
                                        (39 X 30-32)
                                        36.6 X 33.4

                                   Sporocysts size,
Caryospora        Sporocyst   [micro]m (range, [micro]m)
species             shape       Reference interval (1)

C kutzeri         Ovoid              22.5 X 21.3
                                   (18-26 X 16-26)
                                      24.6 X 21

C neofalconis     Ovoid              17.2 X 15.2
                                   (13-19 X 12-19)
                                     18.8 X 14.8

C megafalconis    Spherical          23.6 X 22.7
                                   (21-27 X 20-26)
                                         23.8
C falconis        Spherical          21.7 X 20.6
                                   (15-25 X 14-25)
                                       21 X 23
C cherruglii      Ovoid              22.6 X 18.9
                                   (20-25 X 15-22)
                                     24.1 X 19.6
C boeri           Ovoid              24.5 X 20.5
                                   (24-25 X 20-21)
                                     27.8 X 19.6

Caryospora             Sporozoite size,
species           [micro]m (range, [micro]m)        Host

C kutzeri                    4.6               F rusticolus
                         (2-7 X 2-7)           F peregrinus
                                               F cherrug,
                                               F tinnunculus
C neofalconis             9.9 X 2.4            F rusticolus
                         (8-12 X 2-4)          F peregrinus
                                               F peregrinus
                                               peregrinator
                                               F cherrug.
                                               F sparverius
C megafalconis            16.5 X 4.2           F rusticolus.
                        (11-20 X 3-6)          F peregrinus
                                               F cherrug
C falconis                13.2 X 4.6           F peregrinus
                        (10-17 X 2-4)

C cherruglii                 15X4              F cherrug
                        (12-20 X 3-5)

C boeri                    19 X 3.5            F tinnunculus
                        (18-20 X 3-4)

Figure 1. Prevalence of different Caryospora species identified in 297
falcons in the United Arab Emirates.

C. cherrughi      3.70%
C. falconis       10.44%
C. megafalconis   18.18%
C. neofalconis    25.59%
C. kutzeri        41.41%
C. boeri          0.67%

Note: Table made from pie chart.

Figure 3. Prevalence of Caryospora species by falcon species in 297
falcons in the United Arab Emirates.

Gyrx Saker         8.1%
Eurasian kestrel   1.0%
Red naped
shaheen            0.7%
American kestrel   0.3%
Gyrx Peregrine     27.3%
Gyr                25.6%
Peregrine          20.5%
Saker              16.5%

Note: Table made from pie chart.
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Title Annotation:Original Study
Author:Mateuta, Victor D.S.; Samour, Jaime H.
Publication:Journal of Avian Medicine and Surgery
Geographic Code:7UNIT
Date:Dec 1, 2017
Words:4379
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