Slovak Raptor Journal 2010, 4: 45–48. DOI: 10.2478/v10262-012-0045-z. © Raptor Protection of Slovakia (RPS)

The ecology of ectoparasitic hemapterus on nestlings of common kestrel (Falco tinnunculus) in Bratislava K ekológii ektoparazitického druhu na mláďatách sokola myšiara (Falco tinnunculus) v Bratislave

Martin KAĽAVSKÝ & Barbora POSPÍŠILOVÁ

Abstract: The time course and abundance of Carnus hemapterus on common kestrel’s nestlings depends on their age and the type of nest. Ectoparasites were found in 97% of nests and the majority of nestlings (83%) were observed to be infested between their 10th and 15th day of life. The highest infestation rate of Carnus hemapterus was recorded on 5- to 10-day old nestlings. We have confirmed that the Carnus hemapterus species feeds on blood; however no negative impact on nestlings and the breeding success of common kestrel was confirmed. Abstrakt: Doba výskytu a početnosť jedincov druhu Carnus hemapterus na mláďatách sokola myšiara závisí od veku mláďat a typu hniezda. Napadnutých bolo 97 % hniezd, pričom najviac mláďat (83 %) bolo napadnutých medzi 10. a 15. dňom života. Najväčší počet C. hemapterus bol zaznamenaný na mláďatách starých 5 až 10 dní. Potvrdili sme, že druh C. hemapterus sa živí krvou, ale negatívny vplyv na mláďatá a hniezdnu úspešnosť sokola myšiara sa nepotvrdil.

Key words: hematocrit, hematophagy, abundance, Slovakia

Martin Kaľavský, Department of Zoology, Faculty of Natural Sciences, Comenius University in Bratislava, Mlynská dolina, SK–842 15. E-mail: [email protected]. Barbora Pospíšilová, Department of Ecosozology and Physiotactics, Faculty of Natural Sciences, Comenius University in Bratislava, Mlynská dolina, SK–842 15. E-mail: [email protected]. Acknowledgement: We would like to thank to Michal Noga, Zlatica Országhová, Ivan Országh and Mária Melišková for their assistance in the completion of this research. The work was supported by grant of Comenius University UK/230/2009.

Introduction (1973) noted that all females of Carnus hemapterus in Ectoparasitic diptera Carnus hemapterus can be found in the nest were wingless, where as one third of males were the Holarctic region (Sabrosky 1987) and was also found observed to have wings; from which they suggested in ’s nests in North America, Europe and northern Af- that the males move between nests for the purpose of rica (Grimaldi 1997). The long list of hosts (approximately reproduction. 45 bird species from 18 families) suggests that Carnus There have only been a few papers published about this hemapterus does not have any specific host (Grimaldi ectoparasitic species in Slovakia. From older records there 1997). It mainly attacks species nesting in hollows or are papers covering the region of Gbelce (Gregor 1986) in nest boxes; it avoids nests lined with fresh vegetation and National Nature Reserve (NPR Beckovské Skalice; (Valera 2006). The infestation rate differs from host to Straka in verb.), however they don’t comment anything host. According to Fargalla et al. (2001) common kestrels specific about the host. Carnus hemapterus abundance on living in nest boxes were more likely to be attacked by nestlings of European bee-eater (Merops apiaster) was ectoparasites than pairs living in other types of nests. noted by Krištofík et al. (1996) in the research of parasites Adult individuals of Carnus hemapterus can be found and in their nests. Jánošková et al. (2005) on bald areas, usually under the wings. They feed on observed the occurrence of Carnus hemapterus occu- blood, while larvae are saprotrophic (Grimaldi 1997). rrence on chicks of some hollow-nesting namely After the adult individuals find the right host, they lose on nestlings of common (Sturnus vulgaris). their wings and remain in the nest. Capelle & Whitworth Jamriška & Melišková (2007) found Carnus hemapterus

45 Kaľavský M & Pospíšilová B: The ecology of ectoparasitic species Carnus hemapterus on nestlings of common kestrel (Falco tinnunculus) in Bratislava on nestlings of tawny (Strix aluco). Papers about the in 75% alcohol. The nestlings‘ weight, the length of their occurrence of Carnus hemapterus in the birds of prey tarsometatarsus and the fourth tectrices were measured. nests in Slovakia are absent. As it is one of the common For any individuals where the age could not be ascertai- ectoparasites of raptors and (Capelle & Whitworth ned, the calculation according to Voříšek & Lacina (1998) 1973, Fitzner & Woodley 1985, Kirkpatrick & Colvin was used. The occurrence of blood in the digestive system 1989, Roulin & Riols 2001, Wieliczko et al. 2003, Adam of C. hemapterus was determined by HbCl testing. The & Daróczi 2003), our research was focused on its occur- blood was extracted immediately after the extraction of rence on common kestrel (Falco tinnunculus) with the ectoparasites from the hosts smeared on a microscope aim to determine the factors affecting the abundance and slide and left to dry out. infestation rate on nestlings of various types of nests, to The hematocrits from the blood of the nestlings aged study the impact on breeding success of its host; addition- 15 to 25 days were determined (Dawson & Bortolotti ally to try to confirm its hematophagy. 1997). The blood of 22 nestlings was collected for this purpose, from which we then set the amount of hematocrit Materials and methods for individual nestlings. We took out the blood and put it The presence of ectoparasitic diptera C. hemapterus on into 40 µl capillaries coated with anticoagulant NH4-He- nestlings of common kestrel were found in 27 nests of in- parin. The blood was then centrifugated on a hematocrit ner city (n = 6) and outskirts (n = 21) of Bratislava. In total centrifuge and the amount of hematocrit was determined 88 nestlings were checked in 2008 and 2009. The area of in per cents using a ruler. interest was represented by the outskirt area of Bratislava situated on the Podunajská nížina Lowland in the vicinity Results and discussion of the villages Most pri Bratislave, Miloslavov, Alžbetin There were 1096 individuals, comprised of 497 males and dvor and in Záhorie Region near Devínska Nová Ves. 599 females of C. hemapterus collected from 88 nestlings Within the inner city of Bratislava the studied nests were of common kestrel (n = 88). From the total number of situated in the city parts Devínska Nová Ves, Dúbravka, 27 nest examined 97% were found to have nestlings of Karlova Ves and Rača. The occurrence of ectoparasites common kestrel attacked by ectoparasite C. hemapterus. on nestlings was monitored weather permitting, every 3 to The type of nest was suggested as one factor, having an 5 days from hatching until nestlings left the nest. impact on the occurrence and the number of C. hemap- The individuals of C. hemapterus were collected from terus in the nests of common kestrel. Common kestrels each bird using an exhaustor and ectoparasites were fixed living in the hollows or in nest boxes were attacked with greater frequency and by a larger number of ectoparasites than nestlings inhabiting open nests (Fig. 1). On average 100.57 individuals of C. hemapterus were recorded per pair (n = 7) of kestrels nesting in hollows and nest boxes. This equates to an average of 4.2 individuals of C. he- mapterus per nestling. On average 37.28 individuals of C. hemapterus was recorded per pair occupying a Eurasian magpie’s (Pica pica) nest (n = 8), which equals to 1.96 in- dividuals of C. hemapterus per nestling. On average 16.28 individuals of C. hemapterus were found per pair living in nest pads or flowerpots, equating to 0.74 individuals of C. hemapterus per nestling. Fargallo et al. (2001) studied the nesting biology of common kestrel, focusing on nest predation frequency, prevalence and intensity of infection of ectoparasites in relation to the nest type. He found that the number of fledglings from pairs Fig. 1. The abundance of Carnus hemapterus in different types breeding in nest boxes was higher than those breeding in of nests. Black – hollows and nest boxes (n = 7), grey – magpie’s old stick nests in trees, however chicks from nest boxes nests (n = 8), white – nest bases and flower pots (n = 7). showed a higher intensity of infection. Roulin (2000) re- Obr.1. Početnosť Carnus hemapterus v rôznych typoch hniezd. Čierna – dutiny a búdky (n = 7), sivá – stračie hniezda (n = 8), biela ported a significantly higher prevalence of C. hemapterus – hniezdne podložky a kvetináče (n = 7). individuals on the nestlings of (Tyto alba) in

46 Slovak Raptor Journal 2010, 4: 45–48. DOI: 10.2478/v10262-012-0045-z. © Raptor Protection of Slovakia (RPS) nest boxes used in consecutive years than in those, which Hematophagy of C. hemapterus ectoparasite was also ob- remained unoccupied. served by Heddergott (2003), Fitzner & Woodley (1985), From the total number of nests (n = 27), 90% were who found traces of dried blood in the axillary area. found to have all nestlings infected, 7% nests were par- According to Grimaldi (1997) the question of how the tially infected and only in 3% of nests C. hemapterus was C. hemapterus obtains its food has not been sufficiently not recorded. Fargallo et al. (2001) reported an occurrence answered. Bequaert (1942) noted that the oral organs of of C. hemapterus in 80% of all examined nests. Dawson these parasites are dissimilar to those of blood-sucking & Bortolotti (1997) in their research of the American ; which may likely enable them to cut the host’s skin kestrel (Falco sparverius) found that more than 70% of and suck its blood. nests with at least one nestling infected where as in 30% The negative impact of of C. hemapterus of nests were either none or all nestlings infected. on infected nestlings was tested in relation to the decrease The infestation rate of nestlings showed some correla- tion with their age which can be linked to the develop- ment of their plumage. The nestlings were observed to be attacked by parasites between the 2nd and 25th day after hatching and the highest infestation rate (in average 9.56 individuals per nestling) was recorded between the 5th and 10th day (Fig. 2). The highest number of common kestrel nestlings (83%) was infected between their 10th and 15th day of life (Fig. 3). The low level of infestation of nestlings of common kestrel inhabiting the area of inner city was recorded, which could be attributed to the distinc- tive habitat condition created by the city environment and the height of nest (in average 30 m), in comparison with nests located in outskirts (8–12 m high). Dawson & Bor- tolotti (1997) reported the highest infestation rate between 0- and 5-day old nestlings (40–50%). Gottfried & Hudde (1987) studied distribution and seasonal dynamics of C. Fig. 2. The occurrence of Carnus hemapterus on the host related hemapterus on several raptors and songbirds species. to the age of nestlings. X-axis – age of common kestrel nestlings (days), y-axis – average number of C. hemapterus individuals in The nestlings were attacked from the first day of their one nest of F. tinnunculus. life, the majority of them was infested around their 6th Obr. 2. Výskyt Carnus hemapterus na hostiteľovi v závislosti to 7th day of life. Similar results were recorded by Liker od veku mláďat. Os x – vek mláďat sokola myšiara (dni), et al. (2001), who studied distribution of C. hemapterus os y – priemerný počet jedincov C. hemapterus na jedno hniezdo in the colony of the common (Sturnus vulgaris). F. tinnunculus. He found eight individuals of C. hemapterus per nestling and the highest infestation rate on 5 to 8 day old nestlings. The ratio of females and males of C. hemapterus per nestling of the common kestrel was 1:1.2, respectively. Individuals with wings formed only 1.1% of the total col- lected sample, from which nine were females and three males. The sample collected by Dawson & Bortolotti (1997) contained 3.9% of individuals with wings. One third of males with wings were recorded in a sample of 95 individuals by Capelle & Whitworth (1973). In the same sample all females were wingless. Hematophagy of C. hemapterus was tested by creating HbCl crystals in blood samples obtained from the females Fig. 3. Percentage of affected nestlings in the nests. X-axis – age intestines of studied ectoparasites. Additionally, individu- of nestlings (days), y-axis – affected nestlings (%). als of C. hemapterus were observed to be sucking blood Obr. 3. Percento napadnutých mláďat v hniezdach. Os x – vek from the edges of an open wound of the nestling’s wing. mláďat (dni), os y – napadnuté mláďatá v hniezdach (%).

47 Kaľavský M & Pospíšilová B: The ecology of ectoparasitic species Carnus hemapterus on nestlings of common kestrel (Falco tinnunculus) in Bratislava of hematocrit. The correlation between the infestation rate in amber (Diptera: ). American Museum of and decreased level of hematocrit on common kestrel Natural History, 30. nestlings were tested using the Spearman’s rank correlation Heddergott M 2003: Parasitierung nestjunger Turmfalken coefficient; however this was not confirmed. Moreover, Falco t. tinnunculus durch die Gefiederfliege Carnus despite a higher infestation rate, greater average number of hemapterus (Insecta: Milichiidae, Diptera). Vogelwelt nestlings from hollows and nest boxes (3.4) were recorded 124: 201–205. in comparison to the open nests (2.9). Our results suggest Jamriška J & Melišková M 2007: The first record of Car- that the breeding success is more significantly affected by nus hemapterus (Diptera: Carnidae) on nestlings of the weather conditions, food supply and predation as opposed tawny owl (Strix aluco). Acta Zoologica Universitatis to the occurrence of C. hemapterus. This assumption is Comenianae 47(2): 143–144. supported by Dawson & Bortolotii (1997), who also did not Janošková V, Jamriška J & Országhová Z 2005: Carnus observe any negative impact of parasitism on nestlings’ fit- hemapterus (Diptera: Carnidae) and its occurence in ness, breeding success or decreased level of hematocrit on Slovakia. Entomofauna Carpathica 17(3–4): 84–85. nestlings affected by C. hemapterus. Liker (2001) stated in Kirkpatrick CE & Colvin BA 1989: Ectoparasitic the conclusion of his work that the abundance of parasites Carnus hemapterus (Diptera, Carnidae) in a nest- did not show a correlation with the mortality curve, nor did ing population of common barn-owls (Strigiformes, it have any impact on the growth of the nestlings. Tytonidae). Journal of Medical Entomology 26(2): 109–112. References Krištofík J, Mašán P & Šustek Z 1996: Ectoparasites Adam C & Daróczi S 2003: Carnus hemapterus Nitzsch, of bee-eater (Merops apiaster) and arthropods in its 1818 (Diptera: Carnidae) parasite on Buteo buteo nests. Biologia 51(5): 557–570. L. (Aves: Accipitridae) in central Romania. Revista Liker A, Markus M, Vozar A, Zemankovics E & Ro- Romana de Parazitologie 8(2): 46–47. zsa L 2001: Distribution of Carnus hemapterus in Bequaert J 1942: Carnus hemapterus Nitzsch, an ecto- a starling colony. Canadian Journal of Zoology 79(4): parasitic fly of birds, new to America (Diptera). Bulletin 574–580. of the Brooklyn Entomological Society 37: 140–149. Sabrosky CW 1987: Carnidae, 909–912. In: McAlpine Capelle KJ & Whitworth TL 1973: The distribution and JF (ed), Manual of Nearctic diptera. Vol. 2. Canadian avian hosts of Carnus hemapterus (Diptera: Milichii- Government Publishing Centre, Que., 1332. dae) in North America. Journal of Medical Entomol- Roulin A, Riols C, Dijkstra C & Ducrest AL 2001: Fe- ogy 10(5): 526–527. male plumage spottiness signals parasite resistance in Dawson RD & Bortolotti GR 1997: Ecology of parasitism the barn owl (Tyto alba). Behavioral Ecology 12(1): of nestling American kestrels by Carnus hemapterus 103–110. (Diptera: Carnidae). Canadian Journal of Zoology Valera F, Martín-Vivaldi M & Carles-Tolrá M 2006: 75: 2021–2026. Life-history variation in three coexisting species of Fargallo JA, Blanco G, Potti J & Viñuela J 2001: Nestbox carnid flies (Diptera: Carnidae), Carnus hemapterus, provisioning in a rural population of Eurasian kestrels: Hemeromyia anthracina and Hemeromyia longirostris. breeding performance, nest predation and parasitism. European Journal of Entomology 103(2): 347–353. Bird Study 48: 236–244. Voříšek P & Lacina D 1998: Určování věku mláďat káně Fitzner RE & Woodley NE 1985: Carnus hemapterus lesní (Buteo buteo) a poštolky obecné (Falco tinnun- Nitzsch from Swainson’s hawk. Raptor Research culus) s využitím biometrických dat [Determination 17(1): 28–29. of age in the juveniles of the common buzzard (Buteo Gottfried W & Hudde H 1987: Die Gefiederfliege Carnus buteo) and the common kestrel (Falco tinnunculus) hemapterus (Milichiidae, Diptera), ein Ektoparasit der using biometric data]. Buteo 10: 35–50. [In Czech Nestlinge. Journal of Ornithology 128(2): 251–255. with English summary] Gregor F 1986: Čeľaď Carnidae [Family Carnidae], 183– Wieliczko A, Piasecki T, Dorrestein GM, Adamski A 184. In: Čepelák J (eds), Diptera Slovenska II [Diptera & Mazurkiewicz M 2003: Evaluation of the health of Slovakia II]. Veda, Bratislava, 435. [In Slovak] status of goshawk chicks (Accipiter gentilis) nesting in Grimaldi D 1997: The bird flies, Carnus: species Wroclaw vicinity. Bulletin of the Veterinary Institute revision, generic relationships, and a fossil Meoneura in Pulawy 47(1): 247–257.

48