BIHAREAN BIOLOGIST 14 (1): 25-29 ©Biharean Biologist, Oradea, , 2020 Article No.: e191306 http://biozoojournals.ro/bihbiol/index.html

Causes of morbidity of Common ( buteo) and Long-Eared (Asio otus) at a Hungarian wildlife rescue centre between 2014 and 2016

Viktória SÓS-KOROKNAI1,*, János GÁL2, Miklós MAROSÁN2, Tamás TÓTH1 and Endre SÓS1

1. Budapest Zoo and Botanical , Conservation and Veterinary Directorate, H-1146 Budapest, Állatkerti krt. 6-12., Hungary. 2. University of Veterinary Science, Department of Exotic and Wildlife Medicine, H-1078 Budapest, István u. 2, Hungary. *Corresponding author, V. Sós-Koroknai, Phone: +36305045451; E-mail: [email protected]

Received: 31. January 2019 / Accepted: 04. June 2019 / Available online: 05. July 2019 / Printed: June 2020

Abstract. The aim of our study was to examine the cases of Common Buzzards (Buteo buteo) and Long-eared Owls (Asio otus) treated at the Wildlife Rescue Center at the Budapest Zoo and Botanical Garden in Hungary over the course of a three-year period. These were chosen as part of this study as they are the most abundant diurnal and nocturnal raptors at the rescue facility and the causes, which warranted rescue in their cases could be extrapolated to other species and raptor-related conservation problems in a broader sense. Emphasis was placed on determining the cause of admittance of these individuals and whether or not rehabilitation was possible with various ailments. We found that in Common Buzzards (n=42), rehabilitation and release was achieved in 31.0% of the cases (n=13), with orphaned juvenile having the highest rate of success, 31.0% (n=13) were humanely euthanized, 28.6% (n=12) died at the rescue center and 9.5% (n=4) were placed in captive facilities for breeding and education purposes. Of the Long- eared Owls (n=35) brought into the rescue center during this timeframe, altogether 37.1% (n=13) were released back into the wild with juvenile individuals being the most highly represented, 22.8% (n=8) were humanely euthanized, 20.0% (n=7) died and 20.0% (n=7) were placed in a captive setting. We were thus able to see, that raptor and patients which were orphaned had highest rate of rehabilitation compared to the other categories in our study. Traumatic injuries were presented in the greatest number in both the Common and the Long-eared Owl.

Key words: Common Buzzard (Buteo buteo), Long-eared Owl (Asio otus), rehabilitation, wildlife rescue, free-ranging raptors, Hungary.

Introduction Montesdeoca et al. 2016, Molina-López et al. 2017) and was thus the primary goal of this study as well. Furthermore, our There are many factors that can be denoted as hindrances in aim was to establish the rate of rehabilitation of various al- the natural habitat of free-living birds of prey that can cause terations and whether or not, there was a trend among or injury to these charismatic species. These can be categorized within the species studied. The Common Buzzard (Buteo bu- as naturally occurring or manmade objects and conditions, teo) and the Long-eared Owl (Asio otus) were chosen as diur- but they are all considered obstacles to raptors and nocturnal nal and nocturnal predatory species respectively, as predators in the wild. Power lines have been implicated in these are represented in relatively high numbers to the Wild- the latter category and have in fact been deemed the number life Rescue Center at the Budapest Zoo and Botanical Garden one cause of predatory bird mortality (Guil et al. 2011, and it was hypothesized that trends seen in these birds Melero et al. 2013, Kagan 2016). However, collisions with would provide insight into the conservation issues with vehicles (Punch 2001, Rodríguez et al. 2010, Molina-López et these species and could even be extrapolated to other rap- al. 2011), gunshot injuries (Jager et al. 1996, Richards et al. tor-related conservation problems in a broader sense. 2005, Molina-López et al. 2011), intoxications (Komnenou et al. 2005, Rodríguez et al. 2010, Murray, 2011, Sós et al. 2013) and heavy metal load (Jager et al. 1996, Kim & Oh 2016, Material and Methods

Kitowski et al. 2017, Grúz et al. 2018) have also been de- The Wildlife Rescue Center at the Budapest Zoo and Botanical Gar- scribed in various species of nocturnal and diurnal predato- den sees approximately 1,000 avian patients each year and out of ry birds as human inflicted causes or morbidity and can lead these, about 10% are comprised of various raptor and nocturnal to their admittance to rescue centers. However, it is im- predatory bird species. During the course of the study, rescued birds portant to note that variation is to be expected based on dif- were brought in from all around the country, though the vast majori- ferences between species, habitat and geographical regions. ty from the Budapest area. Upon arrival, each bird underwent a full Nonetheless, naturally occurring factors as starvation (Punch veterinary examination and was housed in an individual compart- 2001, Komnenou et al. 2005) and infectious diseases (Molina- ment. These enclosures had wooden walls, a chicken wire covering on the top for ventilation and were fitted with removable glass doors López et al. 2011) prove to be the reason for various free- in order to visualize the patients. Owing to the size differences be- living predatory birds to be brought into a captive setting as tween species, different sized crates were at our disposal according well. Admittance of orphaned young birds have also been to the individual needs of our patients. Furthermore, larger rehabili- found to be common in wildlife rescue facilities (Komnenou tation aviaries were also used for rehabilitation purposes prior to et al. 2005, Molina-López et al. 2011, Molina-López et al. their release back into the wild. 2017), though these cases often appear to be naturally occur- Individuals were categorized based on the type of alterations ring, they can also be associated with human intervention. found following physical examination. The classification was as fol- lows (listed in alphabetical order): “electrocution” (alterations con- Focusing on the cause of admittance to a wildlife rehabilita- sistent with lesions caused typically by collisions with powerlines as tion facility appears to be a common factor analyzed in vari- described by Kagan [2016]), “intoxication” (patients with clinical ous studies in the literature (Wendell et al. 2002, Komnenou signs consistent with carbofuran poisoning as described by Sós et al. et al. 2005, Rodríguez et al. 2010, Molina-López et al. 2011, [2013]), “metabolic or nutritional disease” (low body condition and 26 V. Sós-Koroknai et al. generalized weakness caused by ailments not listed in the other - Zoo and Botanical Garden Wildlife Rescue Center received a egories), “orphaned” (juvenile birds that would be still be cared for total of 42 Common Buzzards (Buteo buteo) and 35 Long- by their parents in the wild and which were hand-reared by the staff eared Owls (Asio otus). Of the 26 Common Buzzards, 47.6 % at our institution until fledging) and “traumatic injuries” (lesions (n=20) of the patients were admitted with traumatic injuries. consistent with external trauma). The latter was categorized further according to the affected body part or tissue type: “wing injuries” 19.0% (n=8) were victims of electrocution, 11.9% were juve- (fracture or alteration to one or more of the bones of the wings or soft nile orphaned individuals (n=5) brought in to be hand- tissue injuries), “leg injuries” (injuries affecting either the bony or reared. Furthermore, 16.7% (n=7) of our patients were ad- soft tissue structures of the limbs), “vertebral injury” (injuries to the mitted with metabolic or nutritional disease and there were vertebral column, suspected by clinical signs of paraplegia and con- two birds (4.8%) that were brought in showing clinical signs firmed through radiology) and “other injuries” (those pertaining typical of carbofuran intoxication (see Fig. 1). The traumatic body parts not disclosed in the other categories). injury category was further broken down into fractured Physical examination was always performed either directly up- wings, which accounted for 50.0% (n=10) of the cases, 5.0% on arrival or shortly thereafter following our own protocol. Before handling our patients, we performed a distance examination to visu- (n=1) were vertebral column injuries (definitively diagnosed alize how the bird responded to its environment, their level of con- through radiology), 25.0% (n=5) had lesions affecting the sciousness as well as their range of motion (where this was possible). legs and in 20.0% (n=4) of the cases the injuries were in the Subsequently, a detailed physical examination was conducted on “other” category. Of the raptors with wing fracture, two in- those individuals where it did not pose further threat to their health. dividuals underwent surgery (wing amputation was per- This decision was made subjectively in all cases. The systematic formed, where, owing to the vast area of necrosis caused by physical examination was initiated with the inspection of the wings open fractures in the majority of cases, osteosynthesis was and the legs. All joints and bones were palpated and their range of motion was determined. Following the examination of the locomo- no longer a feasible option) and recovered successfully. The tory system, the sensory organs were evaluated. The eyes were fate of these birds was also summarized (see Table 1.). The checked for symmetry, integrity as well as the presence of any patho- four different categories denoting the fate of our patients logical changes on the eyelids, the ears for signs trauma or bleeding, was as follows: released, euthanized, deceased (after arrival) whilst the beak and the cere were examined both from outside and and placement (for long-term captive keeping). In total, from within for any alterations or lesions. A full neurological as- 31.0% (n=13) of the Common buzzards were released back sessment of the patient was also performed. Where necessary, fur- into the wild, 31.0% (n=13) were humanely euthanized, ther diagnostic methods such as radiology, endoscopy, and various 28.6% (n=12) died at the rescue center and 9.5% (n=4) were sampling procedures were employed. The latter included oral and cloacal swabs, and blood sampling. In cases were emergency inter- placed in captive setting and to the best of our knowledge vention was required for a patient in a critical condition, certain were still alive at the end of the study period. steps of the diagnostic protocol were omitted until the individual On the Long-eared Owl (Asio otus) front, 35 patients was stabilized in order to minimize handling time. were included in this study out of which 54.2% (n=19) were Following the diagnostic procedure, the fate of the patient was victims of traumatic injuries, 31.4% (n=11) were orphaned decided depending on the prognosis established through the above individuals, 5.7% (n=3) were admitted with metabolic or nu- listed protocol. In cases where the welfare of the individual was in tritional disease and in 5.7% (n= 2), signs of electrocution question, humane euthanasia was performed with embutarmid (T61®, Intervet International B.V. Boxmeer, Holland) administered were found (see Fig. 2.). Of the traumatic injuries, in 63.2% intramuscularly to prevent needless suffering of the individual. Fur- (n=12) of the cases, the wings were affected (out of these thermore, those birds deemed healthy enough to survive in the wild 15.8% [n =3] underwent surgical procedures) whilst in 10.5% were released as soon after admittance as possible to avoid damage (n=2), vertebral fractures were diagnosed through radiology, to their plumage. Treatment plans were individually established and in 10.5% (n=2) injuries were seen to the legs and 15.8% (n=3) tailored to the needs of our patients. The protocol used for patients of the cases the type of lesion was not recorded (listed as undergoing general anesthesia for surgical procedures consisted of “other injuries”). Similarly to the Common Buzzards, the the use of the following medications and dosages: pre-operative bu- fate of these individuals was also summarized (see Table 2.) torphanol (Butomidor, Richter Pharma AG, Austria) 1-2 mg/kg in- tramuscularly for analgesia, ketamine (Ketamidor®, Richter Pharma according to the same four categories: released, euthanized, AG, Austria) 5-15 mg/kg and midazolam (Dormicum, F. Hoff- deceased (after arrival) and placement (long-term captive mann-La Roche AG, Basel, ) 0.5 mg/kg intravenously or keeping). Altogether 37.1% (n=13) Long-eared Owls were re- intramuscularly for induction, isoflurane or sevoflurane for mainte- leased back into the wild, 22.8% (n= 8) were humanely eu- nance and amoxicillin trihydrate (Clamoxyl LA®, Pfizer Kft., Hunga- thanized, 20.0% (n=7) died and 20.0% (n=7) were placed. ® ry) 100 mg/kg intramuscularly and meloxicam (Metacam , Boehringer Ingelheim Vetmedica, Inc.) 0.5-1 mg/kg intramuscularly as postoperative antibiotic and analgesic respectively. Discussion Individuals that, either subsequently to or following treatment, were deemed not releasable to the wild were placed in aviaries either within the Budapest Zoo or in other locations for display, education To the best of our knowledge, this is the first peer-reviewed and captive breeding purposes. These included those patients with publication documenting clinical cases of free-ranging pred- amputated wings or individuals where release into the wild was not atory birds and their fates in a rescue center setting in Hun- possible for other reasons. All measures were taken to ensure that gary. Though only two species were incorporated into this the welfare of individuals kept in a captive setting were not com- study, we do believe that our results have given some in- promised at any point in time. sight into the potential fate of the birds admitted to the wild-

life rescue facility at the Budapest Zoo and Botanical Garden.

Results Furthermore, our results may have implications on other charismatic and strictly protected species in Hungary, such as the Eastern Imperial (Aquila heliaca), Saker Fal- Between 1 January 2014 and 31 December 2016, the Budapest

Causes of morbidity of Common Buzzards and Long-Eared Owls at a Hungarian wildlife rescue centre between 2014 and 2016 27

Figure 1: Diagram showing the causes of admittance of Com- Figure 2. Diagram showing the causes of admittance of Long-eared mon Buzzards (Buteo buteo) as a percentage of the total for Owls (Asio otus) as a percentage of the total for the given species. the given species.

Table 1. The fate of Common Buzzard (Buteo buteo) patients over the timeframe of the study expressed as the number of individuals (n), and as a percentage of the total for a given cause of ad- mittance.

Cause of admittance Number Released Euthanized Deceased Placed (in alphabetical order) of cases (n) (n / %) (n / %) (n / %) (n / %) electrocution 8 - 6 / 75 1 / 12.5 1 / 12.5 intoxicated 2 1 / 50 - 1 / 50 - leg injuries 5 2 / 40 - 3 / 60 - metabolic/nutritional disease 7 3 / 42.3 - 4 /57.1 - orphaned 5 5 / 100 - - - other injuries 4 1 / 25 1 / 25 1 / 25 1 / 25 vertebral injuries 1 - 1 /100 - - wing injuries 10 1 / 10 5 /50 2 / 20 2 / 20 total 42 13 / 31.0 13 / 31.0 12 / 28.6 4 / 9.5

Table 2. The fate of Long-eared Owl (Asio otus) patients over the timeframe of the study expressed as the number of individuals (n), and as a percentage of the total for a given cause of admittance.

Cause of admittance Number Released Euthanized Deceased Placed (in alphabetical order) of cases (n) (n / %) (n / %) (n / %) (n / %) electrocution 2 - - - 2 / 100 leg injuries 2 - 2 / 100 - - metabolic/nutritional disease 3 2 / 66.6 - 1 / 33.3 - other injuries 3 1 / 33.3 - 1 / 33.3 1 / 33.3 orphaned 11 9 / 81.8 1 / 9.1 1 / 9.1 - vertebral injuries 2 - 1 / 50 1 / 50 - wing injuries 12 1 / 8.4 4 / 33.3 3 / 25.0 4 / 33.3 total 35 13 / 37.1 8 / 22.8 7 / 20.0 7 / 20.0

con (Falco cherrug) or the Eagle Owl (Bubo bubo), or else in implicated in 38% of cases (Gál et al. 2003), though in differ- rescue centers across the continent. Through the findings of ent species from those described in this study. Additionally, this study, we can clearly see that both Common Buzzards through the literature we can see that in similar studies done (Buteo buteo) and Long-eared Owls (Asio otus) arriving to our around the world found such injuries to be present in 75.8% rescue center had a relatively low rehabilitation and release (Komnenou et al. 2005), 66.3% (Wendell et al. 2002), 49.5% rate. However, though this statement can apply to all the (Molina-López et al. 2011) and 33.8% (Montesdeoca et al. birds of prey in this study, it is important to note that vari- 2016) of their cases respectively. The afore mentioned studies ous causes of admittance did indeed have variable results, were mainly retrospective, encompassing a great deal of cas- which did not necessarily reflect the overall trends. This low es and an expansive number of species as well, but nonethe- percentage of rehabilitation was present in the case of indi- less, the trends were comparable to our results. Juvenile or viduals of both species presented to us with various catego- orphaned birds also accounted for almost a third of our ries of traumatic injuries (see results section for details). In a Long-eared Owl patients. Molina-López et al. (2011) found previous study done on the causes of mortality in predatory similar tendencies, also mainly in Strigiformes in , birds in Hungary, it was noted that trauma was primarily whilst Komnenou et al. (2005) also obtained comparable re-

28 V. Sós-Koroknai et al. sults from and in both instances, orphaned birds ac- tion in these species could provide us with insight into the counted for approximately a similar proportion of their cas- cause of admittance of these individuals, aid us in the treat- es. It has been stated, that the reason for this occurrence is ment of these birds and furthermore, may be useful in ana- resultant from unwarranted human intervention (Komne- lyzing the prevalence of various infectious agents in wild nou et al. 2005) and the collection of otherwise healthy populations as was done by Randall et al. (2012) for West chicks, however most of the individuals in this category Nile . Additionally, intoxication has been widely doc- were hand-reared and eventually returned to the wild. With umented in eagle species in Hungary (Sós et al. 2013) and re- these patients, our experience has shown, that care must al- cent studies showed the highest incidence of deliberate poi- ways be taken to prevent imprinting of hand-reared chicks soning in the Common Buzzard (Deák et al. 2015, Deák and as their reintroduction can be prolonged or even prevented Horváth, 2016). As only two cases were presented as part of if they become to accustomed to the presence of humans. this study, we can only say that it was present, but we can- Such a favorable survival and reintroduction rate cannot not state that is was a common cause for admittance of the be said in instances where electrocution or traumatic injury species in question. In addition to raptors, anticoagulant ro- was the cause of admittance of individuals to our facility. In denticides pose a considerable threat to nocturnal predatory the former not a single bird was deemed non-releasable and species (Albert et al. 2010, Christensen et al. 2012, Ruiz- in the case of the Common Buzzards, the majority of our pa- Suárez et al. 2014) including the Long-eared Owl, but partic- tients were euthanized for humane reasons. Though in our ularly those where small comprise a large propor- study we did not find that electrocution was the primary tion of their diet (Ruiz-Suárez et al. 2014). Though at the threat to the species we focused our research on, the trends Wildlife Rescue Center at the Budapest Zoo we have not yet of the fate of wild raptors in Spain do justify the above seen cases of anticoagulant rodenticide toxicosis in Long- statement (Guil et al. 2011) going so far as to say, collisions eared owls, recently we did have a diagnosed case of brodi- with powerlines are the primary non-natural cause of death facoum poisoning in an Eagle Owl Bubo bubo (unpubl. data) of wild predatory birds. In fact, Guil et al. (2011) listed the suggesting that this may pose a threat in the very near fu- Common Buzzard as the species with the highest incidence ture. of electrocution cases, and though this was not reflected in From our results we can conclude that various alteration our results, a recent study in Hungary did show this species were commonly seen in the two species studied, the success to be the most commonly affected raptor by this alteration of rehabilitation is relatively low on a whole, but favorable (Tóth 2016). Strigiformes have also been seen as victims of in specific instances and that our results were more or less in electrocution, but in comparatively lower numbers to their line with the literature. The constraints of the project both diurnal counterparts (Guil et al. 2011, Molina-López et al. through the low number of species reviewed and the short 2011). On the other hand, birds in the “metabolic and nutri- timeframe studied are aspects of our work that can be ex- tional disease” category had an approximately 50:50 chance panded upon in future studies. A longer timeframe project of survival and all individuals that recovered were subse- involving a greater number of species would also provide quently released. These cases were the most difficult to further valuable information about the threats to these char- judge and classify owing to their subjective nature and it ismatic birds of prey and their probability of survival, reha- was not in scope the project to devise an objective diagnosis bilitation and reintroduction following certain injuries. Ad- in these cases. Investigation into the grounds of such an ob- ditionally, it would be beneficial to further evaluate the effi- scure and general clinical picture would provide beneficial cacy of our reintroductions through various methods such as information in future studies, as infectious diseases can often radiotelemetry as done by Fischer et al. (2014). In the past, be in the background where generalized symptoms are pre- this method, along with ringing and color ringing have been sent. Reports have shown a high incidence of gastrointesti- used in order to confirm that the birds released from our res- nal parasitism, particularly in buzzards in Spain (Ferrer et al. cue facility have indeed integrated themselves into their 2004) and in a study done in Hungary, 20% of the cases pre- wild populations. sented with internal parasites on necropsy (Gál et al. 2003). Additionally, the presence of various hemoparasites have al- so been studied in this species (Svobodová et al. 2015). Fur- Acknowledgements. We would like to thank the Budapest Zoo and thermore, Schettler et al. (2003) showed that Chlamydophila Botanical Garden for providing the financial background to the psittaci is commonly found in free-living birds of prey in study; the keepers and staff at the Wildlife Rescue Center (István and the occurrence of Mycobacterium avium has al- Czuczor, Gabriella Fekete, Éva Fonád, Barbara Kiss, Noémi Papp, so been documented in both diurnal and nocturnal predato- Andrea Szima and Tamás Verőczey) for all their hard work with the ry bird species (Millán et al. 2010). Further studies provide patients involved in this study. Furthermore, we are very grateful for evidence of fungal infections, such as aspergillosis and can- the help of Gábor Szelényi and the Hungarian Bird Rescue didiasis, to be present in free-ranging raptor species (Deem Foundation for supporting our project throughout. 2003), West Nile Virus has also been reported in many pred- atory bird species in (Nemeth et al. 2009) and

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