Subalar cutaneous cysts with Harpirhynchus nidulans in bearded tits and hawfinches in Central Europe

Abstract

In wild bearded tits (Panurus biarmicus) and hawfinches (Coccothraustes coccothraustes) trapped in the Czech Republic and Slovakia from 1999 to 2003, characteristic yellow thin-walled subalar cutaneous cysts filled with friable material containing mites Harpirhynchus nidulans were found. The biggest cysts were 14 mm and 20 mm in size in bearded tits and in hawfinches, respectively. Histologically, the relatively thick wall of cysts contained erythrocytes (extravased or in small vessels) and heterophils; mononuclear cells were not found. The prevalences of subalar cysts in bearded tits at Nesyt (Czech Republic), Pusté Úl'any (Slovakia) and Parížské Močiare (Slovakia) were 6.1% (11 positive/180 examined), 12.7% (13/102) and 4.2% (4/96), respectively. The overall prevalence of subalar cutaneous cysts in bearded tits was 7.4% (28/378). The cutaneous cysts were found on adult birds only. Subalar cysts of H. nidulans in hawfinches were also found in four other locations in the Czech Republic and Slovakia

Kystes cutanés sous alaires contenant Harpirhynchus nidulans chez des mésanges à moustaches et des gros-becs en Europe Centrale

Chez des mésanges à moustaches (Panurus biarmicus) et des gros-becs (Coccothraustes coccothraustes) piégés en République Tchèque et en Slovaquie de 1999 à 2003, des kystes caractéristiques jaunes, cutanés sous alaires avec une paroi mince remplis de matériel friable contenant des mites Harpirhynchus nidulans ont été observés. Les plus gros kystes mesuraient respectivement 14 mm et 20 mm chez les mésanges à moustaches et chez les gros-becs. En histologie, la paroi des kystes relativement épaisse, contenait des érythrocytes (en épanchement ou dans de petits vaisseaux) et des hétérophiles. Il n'a pas été observé de cellules mononucléaires. Les prévalences des kystes sous alaires chez les mésanges à moustaches à Nesyt (République Tchèque), à Pusté Úl'any et à Parížské Močiare (deux localités en Slovaquie) ont été respectivement de 6,1 % (11 positifs/180 examinés), 12,7 % (13/102) et 4,2 % (4/96). La prévalence générale des kystes cutanés sous alaires chez les mésanges à moustaches a été de 7,4 % (28/378). Les kystes cutanés ont été trouvés uniquement chez les oiseaux adultes. Les kystes de H. nidulans chez les gros-becs ont également été observés dans quatre autres localités en République Tchèque et en Slovaquie.

Subalare Hautzysten mit Harpirhynchus nidulans in Bartmeisen und Kernbeißern in Zentraleuropa

Bei wildlebenden Bartmeisen (Panurus biarmicus) und Kernbeißern (Coccothraustes coccothraustes), die in den Jahren 1999 bis 2003 in der tschechischen Republik und der Slowakei eingefangen wurden, wurden unter den Flügeln charakteristische gelbe dünnwandige mit bröckeligem Material gefüllte Hautzysten festgestellt, die Harpirhynchus nidulans-Milben enthielten. Die größten Zysten bei Bartmeisen und Kernbeißern hatten einen Durchmesser von 14 bzw. 20 mm. Histologisch, enthielten die relativ dicken Zystenwände Erythrozyten (extravaskulär oder in kleinen Gefäßen) und Heterophile. Mononukläre Zellen wurden nicht gefunden. Die Prävalenz der subalaren Zysten bei Bartmeisen betrug in Nesyt (Tschech. Rep.) 6,1 % (11 positive/180 untersuchten), in Pusté Ùl'any (Slowakei) 12,7 % (13/102) und in Parížske Močiare (Slowakei) 4,2 % (4/96). Die Hautzysten wurden nur bei adulten Vögeln festgestellt. Bei Kernbeißern wurden die subalaren H. nidulans-Zysten in vier anderen Orten in der Tschechischen Republik und der Slowakei nachgewiesen.

Quistes cutáneos subalares con Harpirhynchus nidulans en bigotudos y picogordos en Europa Central

Se observaron quistes cutáneos subalares recubiertos de una fina membrana amarilla y llenos de un material friable que contenía ácaros Harpirhynchus nidulans en bigotudos (Panurus biarmicus) y picogordos (Coccothraustes coccothraustes) salvajes recogidos en la República Checa y Eslovaquia desde el año 1999 al 2003. El quiste de mayor tamaño fue de 14 mm y 20 mm en bigotudos y picogordos, respectivamente. Histológicamente, los quistes con una pared relativamente gruesa contenían eritrocitos (extravasados o en pequeños vasos) y heterófilos, no se encontraron células mononucleares. La prevalencia de quistes subalares en bigotudos en Nesyt (República Checa), Pusté Úl'any y Parížské Močiare (ambos en Eslovaquia) fueron de 6.1% (11 positivos/180 examinados), 12.7 % (13/102) y 4.2 % (4/96), respectivamente. La prevalencia en conjunto de quistes subalares en bigotudos fue del 7.4 % (28/378). Los quistes cutáneos sólamente se observaron en aves adultas. Los quistes subalares de H. nidulans en picogordos también se hallaron en otras cuatro localizaciones dentro de la República Checa y Eslovaquia.

Introduction

Mites of the family Harpirhynchidae (Acari, Prostigmata) parasitizing avian species can be found on the skin, in feather follicles and in the epidermis. They are generally oligoxenous parasites (Bochkov et al., 1999). Several mite species of the family Harpirhynchidae may accumulate in the skin and form voluminous subcutaneous cysts, yellowish-orange in colour (Fain, 1994, 1995). The cysts are located mainly on the breast and at the base of the wing. The following mite species are known to produce parasitophorous cysts: Harpirhynchus nidulans (Nitzsch, 1818), Harpirhynchus longipilus Banks, 1905, Harpirhynchus brevis Ewing, 1911, Harpirhynchus monstrosus Fritsch, 1954 and Harpirhynchus rosellacinus Lawrence, 1959 (Fain, 1994, 1995).

In our ornithological research involving bird trapping with nets and banding, we noticed prominent cutaneous cysts, from yellow to yellow–orange in colour, under the wings of some of the birds. A microscopic examination of the cyst content revealed the presence of mites. The cutaneous cysts were produced by the mites H. nidulans. Because there is little information about these mite infestations and their pathological effects, the aim of this paper was to study the prevalence of the lesions caused by H. nidulans and their pathological aspects in two species of passerine birds (i.e. bearded tits and hawfinches).

Materials and Methods

Wild birds were trapped with nets at Nesyt in the Czech Republic, and at Pusté Úl'any and Parížské Močiare in Slovakia, and were examined and banded for further ornithological monitoring. In a number of bearded tits, cysts characteristic of Harpyrhynchidae were found under their wings. The cysts were examined to establish their aetiology, and the species of mites found in the cysts was identified. The prevalence of these cutaneous cysts found at Nesyt from 1999 to 2003, and from 2001 to 2003 at Pusté Úl'any and Parížské Močiare was subsequently computed. Some cysts were measured. Cutaneous cysts similar to those found in bearded tits were also incidentally recorded in hawfinches trapped from 2000 to 2003 at four other sites in the Czech Republic and Slovakia. Their cutaneous cysts also contained mites.

The material contained in cysts was stored in 70% ethanol. Permanent preparations of mites were made using Canada balsam. The mites were identified under the light microscope by the criteria of A. Fain. For the histological examination, some of cysts were fixed in 10% neutral buffered formalin and embedded in paraffin. Sections were stained with haematoxylin and eosin.

Results

Characteristics of subalar cutaneous cyst in bearded tits and hawfinches

The cutaneous cysts were found under the wing, close to the wing base. The thin-wall cysts were oval, spherical or nodular in shape (Figure 1). The cysts of bearded tits were 2 to 14 mm in size, and those of hawfinches were up to 20 mm in size. Smaller cysts were usually flatter than the bigger ones. The cyst walls were smooth and dry. Grossly, the cysts were yellow to yellow–orange tinged. In the walls of some cysts, thin red vessels were identifiable. The cysts ruptured at the apex, and the contents gradually extruded in pieces both large and small, with bits of dry skin still hanging around the cyst. A microscopic examination of the cysts revealed the presence of large numbers of mites dispersed in hard, dry friable yellow-coloured debris.

Figure 1. Cutaneous cyst with H. nidulans in a bearded tit P. biarmicus. (Photographed by J. Chytil.)

Histologically, a relatively thick wall of cysts lined by keratinizing stratified squamous epithelium was found. The wall of cysts contained erythrocytes (extravasated or in small vessels) diffusely and heterophils. The infiltration of mononuclear cells in the wall of cysts was not found. Parts of parasites and tissue debris were seen within the cysts (Figure 2).

Figure 2. Histologic section through a parasitophorous cyst caused by mites H. nidulans. A thick wall of cysts lined by keratinizing stratified squamous epithelium, parasites and tissue debris are seen. (Photographed by V. Tukač.)

Prevalence of subalar cutaneous cysts and H. nidulans in bearded tits

Mites from a cyst of an adult female bearded tit collected on 17 July 2001 were used for identification. They belonged to H. nidulans, and specimens are deposited in the collection of the Parasitological Institute of the Academy of Sciences of the Czech Republic in České Budějovice, Czech Republic (collection number, PAU AVCR 1996).

All of the cutaneous cysts were uniform as far as colour, structure and location on the bird's body. The only difference was their size. The prevalences of cutaneous cysts of this type in bearded tits were 6.1% (11 birds with cysts/180 birds examined) at Nesyt, 12.7% (13/102) at Pusté Úlany and 4.2% (4/96) at Parížské Močiare. The overall prevalence of the cysts in bearded tits at the three sites was 7.4% (28/378). Cutaneous cysts were found on adult birds only.

One adult banded (Budapest A 182911) male bearded tit with a subalar cutaneous cyst was trapped at Pusté Úl'any on 3 May 2003; the same bearded tit was then trapped and examined on 7 July 2003, and the same subalar cutaneous cyst was found on it. This bird was banded on 27 November 2002 at Ócsa, Hungary.

Presence of subalar cutaneous cysts and H. nidulans in hawfinches

In a flock of about 15 hawfinches observed at Zbraslav, Czech Republic, one hawfinch exhibiting atypical behaviour was monitored for several days. The hawfinch kept raising its wing and often tucked its head under the wing. The hawfinch was trapped on 26 December 2000. Under its left wing near the wing base there were two characteristic yellow spherical cutaneous cysts about 4 and 17 mm in size. The hawfinch was in good physical condition and was released after the cysts had been removed. The cysts contained friable material with mites H. nidulans.

Characteristic yellow subalar cutaneous cysts with H. nidulans were found also on an adult female in Pavlov, Czech Republic, on an adult female trapped in Zástřizly, Czech Republic, and on one adult male trapped in Spišská Nová Ves, Slovakia.

In one hawfinch, two cysts, one under each wing, contained friable material and tiny mites, and were about 10×5×5 mm³ in size. Four months later, the cyst under the right wing was 20×15×10 mm³ in size. Later, another small spherical cyst about 2 mm in size appeared about 20 mm from this cyst. Only a structure of about 5 mm in diameter remained of the cyst under the left wing, with bits of skin (i.e. remains of the cyst wall) hanging loose around it. The cysts remained in place for 11 months. At that time, there were four round to oval cysts in size from 4 to 12 mm on the upper part of right wing base, and the cyst under the left wing disappeared. After 14 months of observation in captivity, only two cysts remained under the right wing. The hawfinch was in good condition throughout the entire period.

Discussion

The mite H. nidulans occurs in wild birds in Europe. It was found in the greenfinch (Carduelis chloris), skylark (Alauda arvensis), and hawfinch (Nitzsch, 1818; Mégnin, 1877; Oudemans, 1939; Fritsch, 1954; Fain, 1995). Recently, H. nidulans was the cause of cutaneous cysts in bearded tits in France, and cutaneous cysts of the same characteristics found in bearded tits were reported also from Austria, Croatia and Poland (Henry et al., 2004). The first findings of H. nidulans in the Czech Republic and Slovakia are reported here.

Because a bearded tit with a subalar cyst was found to have travelled from a site in Hungary to a site in Slovakia, it may be assumed that H. nidulans will also be found among Hungarian populations of bearded tits. Banding recoveries of bearded tits documented that a connection exists among populations in the Czech Republic, Slovakia, Poland, Austria and Hungary (Hořák et al., 2003). Infected birds can move in this part of Central Europe among those areas and maintain foci of this parasitic infection. It seems that there are two main areas where subalar H. nidulans cysts in bearded tits occur: Central Europe and France. However, data from other large areas where bearded tits occur are lacking.

Cutaneous cysts were found on adult bearded tits only, and not on young birds. Henry et al. (2004) reported the same observation. The most probable route for the mite transfer is the close mutual contact between infected and uninfected birds. This contact may be assumed when parents are taking care of their offspring. The rupturing of a part of the mite-containing cyst and its transfer to young is very likely. Henry et al. (2004) suggested that the development of dermal cysts takes several months and is connected with the reproductive cycle of the mite. They also proposed that rupturing of the cysts and release of mites has been synchronizated with the host reproduction cycle; that is, at the same time as cysts rupture, the bearded tits population reaches its highest level with all juveniles being fledged and birds aggregating in flocks of several tens of individuals. Moreover, bearded tits are highly gregarious outside the breeding season, gathering in communal autumnal and winter roosts where individuals cluster in close contact (Cramp & Perrins, 1993).

The first known report of subalar cutaneous cysts in hawfinches in Central Europe probably due to the H. nidulans mites dates back to the fourteenth century. Bartholomaeus de Solentia dictus Claretus (1366) mentioned hawfinches in his manuscript Physiologiarius in paragraph [84]: Et quocunque volat, semper habet secum nucleos sub pelle retro alas, ut deficiens edat … [No matter where it flies, it always has seeds tucked under its wings to eat when tired …]. The explanation of subalar structures as feed pouches for hawfinches will certainly sound naïve today. On the other hand, it is also a testimony to the powers of observation of birders of those days, and it also shows that hawfinch as a species has been afflicted with characteristic subalar cysts for more than six centuries.

Henry et al. (2004) did not find a marked negative impact of the lesions on the health status of birds infected. In our case, the histological finding was not too serious and it seems that birds with cysts survived for a long period.

The authors are grateful to V. Bádr, P. Klvaňa and L. Bryndza for their assistance in our study on hawfinches. Their thanks are also due to P. Procházka for turning our attention to the work by Master Claretus, and to P.-Y. Henry for the valuable comments to an early draft of the paper.