Experimental and Applied Acarology

, Volume 58, Issue 2, pp 167–174

Autochthonous and migratory birds as a dispersion source for Ixodes ricinus in southern Italy

Authors

  • Alessandro Falchi
    • Dipartimento di Sanità Pubblica e ZootecniaUniversità degli Studi di Bari
  • Filipe Dantas-Torres
    • Dipartimento di Sanità Pubblica e ZootecniaUniversità degli Studi di Bari
    • Departamento de ImunologiaCentro de Pesquisas Aggeu Magalhães (Fiocruz-PE)
  • Vincenzo Lorusso
    • Division of Pathway MedicineUniversity of Edinburgh Medical School
  • Egidio Malia
    • Parco Regionale Gallipoli Cognato Piccole Dolomiti Lucane
  • Riccardo Paolo Lia
    • Dipartimento di Sanità Pubblica e ZootecniaUniversità degli Studi di Bari
    • Dipartimento di Sanità Pubblica e ZootecniaUniversità degli Studi di Bari
Article

DOI: 10.1007/s10493-012-9571-8

Cite this article as:
Falchi, A., Dantas-Torres, F., Lorusso, V. et al. Exp Appl Acarol (2012) 58: 167. doi:10.1007/s10493-012-9571-8

Abstract

The present study was carried out in a protected wooded area, which is part of the Parco Regionale Gallipoli Cognato Piccole Dolomiti Lucane, one of the most important ecological reserves in southern Italy. From April 2010 to April 2011, 212 birds, comprising 22 species from 12 families, were captured and examined for ticks. A total of 75 (35.4 %) birds were found infested by ticks, with 451 ticks being collected. All ticks were identified as Ixodes ricinus, of which 241 (53.4 %) were larvae and 210 nymphs (46.6 %). The highest intensity of infestation was found in April 2010, when 117 ticks were retrieved on 25 birds. No ticks were found on birds (n = 5) netted in December 2010. High infestation rates were recorded on blackbirds (Turdus merula) (90 %; 29 birds examined) and on mistle thrushes (Turdus viscivorus) (100 %; 2 birds examined). The highest intensity of infestation by larvae was found on wrens (5.6 larvae/bird) and by nymphs on mistle thrushes (11.5 nymphs/bird). Temperature and number of hours of light showed to influence the activity of larvae and nymphs. These data support the notion that birds may be responsible for the heterogeneous distribution of I. ricinus in Europe, thus playing a role in the epidemiology of certain tick-borne pathogens.

Keywords

TicksEcologyBirdsDisease

Introduction

The European Castor bean tick, Ixodes ricinus is a parasite of great medical and veterinary relevance, causing significant losses to the livestock and transmitting a number of pathogens not only to animals but also to human beings (Jongejan and Uilenberg 2004). It infests a wide range of wildlife species (e.g., rodents, hares, lizards, birds, wild boars, and roe deer), livestock (e.g., cattle), domestic animals (e.g., dogs) and eventually humans (Nuttall and Warburton 1911; Manilla 1998). Importantly, immature stages (larvae and nymphs) of I. ricinus feed primarily on small-sized animals (e.g., birds, and small rodents) whereas adults feed on large animals (Nuttall and Warburton 1911; Manilla 1998; Estrada-Peña et al. 2005).

Primarily found in wooded areas, I. ricinus is usually associated to habitats characterized by high levels of relative humidity (RH), with medium to low temperatures (Knap et al. 2009). However, I. ricinus presents a quite ample geographical distribution (Kolonin 2009) and can be found in a variety of environments. In this respect, it has been shown that migrating birds can act as dispersal agents for immature stages of I. ricinus and some associated pathogens in Europe (Estrada-Peña et al. 2005; Hasle et al. 2011). In fact, tick-borne diseases (TBDs) such as anaplasmosis, babesiosis and Lyme borreliosis constitute an emerging concern in temperate regions of Europe (Špitalská et al. 2006). Undoubtedly, I. ricinus is the most important vector of pathogens infecting humans in this continent, where it transmits numerous disease agents, including viruses (e.g., tick-borne encephalitis virus), bacteria (e.g., Anaplasma phagocytophilum, Borrelia burgdorferi, and Rickettsia helvetica), and protozoa (e.g., Babesia divergens) (Jongejan and Uilenberg 2004).

Southern Italy represents one of the southernmost foci of I. ricinus in Europe. Interestingly, this tick species can be found infesting wildlife species during all seasons (unpublished data), but cases of Lyme diseases are rare in this region. Accordingly, the study of such a particular population of I. ricinus might be interesting to gain more information about the risk of dispersion of pathogens such as B. burgdorferi in southern Europe. In this context, the present study was aimed to investigate the importance of autochthonous and migratory birds as hosts of I. ricinus in one of the largest natural reserves of southern Italy.

Materials and methods

Study area

This study was carried out in a protected, wooded area in the Parco Regionale Gallipoli Cognato Piccole Dolomiti Lucane, one of the most important ecological reserves in southern Italy. This natural park has an area of 27.027 hectares that encompasses the municipalities of Accettura, Calciano and Oliveto Lucano in the province of Matera, and Castelmezzano and Pietrapertosa in the province of Potenza (40°53′N, 16°12′E) with an average altitude of 800 m above sea level. Oaks, Holm oaks, chestnuts, lindens, elms, and maples, with undergrowth of holly, characterize the local vegetation. Hornbeam and broom are usually found in the highest areas (1,400 m above sea level, a.s.l.). Several watercourses in the form of streams cross the entire reserve.

The mammal fauna is quite diverse and consists of wild boars (Sus scrofa), gray wolves (Canis lupus), red foxes (Vulpes vulpes), badgers (Meles meles), porcupines (Erinaceus europaeus), wild cats (Felis silvestris), and European hares (Lepus europaeus), among others. Ticks are commonly found in some of these animals (Dantas-Torres et al. 2011; Lorusso et al. 2011). In the same way, the avifauna is extremely diverse and represents a resource to the park, which is recognized as one of the most important bird watching spots in Italy. Indeed, big birds of prey such as red kites (Mylvus mylvus), buzzards (Buteo buteo), kestrels (Falco tinnunculus), and peregrine hawks (Falco peregrinus) are common in the area, together with nocturnal birds such as barn owls (Tyto alba), tawny owls (Strix aluco), long-eared owls (Bubo bubo), and little owls (Athene noctua). Green woodpeckers (Picus viridis), nuthatches (Sitta europaea), jays (Garrulus glandarius), hoopoes (Upupa epops), and golden orioles (Oriolus oriolus) are usually found in the woods, whereas robins (Erithacus rubecola), long-tailed tits (Aegithalos caudatus), blackcaps (Sylvia atricapilla), skylarks (Alauda arvensis), and nightingales (Luscinia megarhynchos) are usually found in the clearings, near the pastures. Importantly, migratory birds such as pied flycatchers (Ficedula hypoleuca), blackcaps (Sylvia atricapilla), turtle doves (Streptopelia turtur), golden orioles (Oriolus oriolus), and Chaffinches (Fringilla coelebs) can be seen within the boundaries of the reserve, mainly during spring.

Bird netting and identification

From April 2010 to April 2011, birds were netted in mist nets (Fig. 1a) at different localities located 930 m a.s.l., halfway between Oliveto Lucano and Pietrapertosa (40°53′N, 16°12′E). Nine mist nets (with a 12 m × 2.5 m) were displayed in different sites in the same locality, some of which were located in the middle of the dense vegetation in the undergrowth near a seasonal stream, and others in scrubs rich with medicinal plants near human dwellings. Two days of bird netting were performed each month. During each day, mist nets were left open from dawn to sunset and were checked approximately every 40 min. Netted birds were firstly identified (Svensson et al. 2009) and then examined for tick infestation, being immediately released at the same site of capture to minimize disturbance. Bird netting was authorized by Superior Institute for Environmental Protection and Research (ISPRA, Bologna, Italy).
https://static-content.springer.com/image/art%3A10.1007%2Fs10493-012-9571-8/MediaObjects/10493_2012_9571_Fig1_HTML.jpg
Fig. 1

Mist nets used to trap the birds (a) and an engorged nymph of I. ricinus on a European greenfinch (Carduelis chloris chloris) (b)

Tick collection and identification

Ticks from birds were collected using steel tweezers, and placed in glass tubes containing 70 % ethanol, labelled according to bird number and species, and collection date. Once in the laboratory, ticks were identified using the morphological keys of Manilla (1998) under a stereomicroscope (LEICA MS5, Germany).

Data analysis

Ecological parameters of tick infestation were calculated as previously described (Bush et al. 1997). In particular, prevalence, mean intensity (number of ticks/number of infested birds) and mean abundance (number of ticks/number of examined birds) of infestation were calculated for each bird species found infested by ticks.

Results

A total of 212 birds, comprising 22 species from 12 families, were captured and examined for the presence of ticks during the study period (Table 1). Most (59 %) of the birds netted were autochthonous (native) species, but migratory birds (i.e., T. merula, F. coelebs, and S. atricapilla) were also frequently captured. Ticks were found infesting 35.4 % (n = 75) of the birds, with 451 tick specimens collected and identified as I. ricinus, of which 241 (53.4 %) were larvae and 210 nymphs (46.6 %). No single adult tick was found. The highest prevalence of infestation was recorded on mistle thrushes (Turdus viscivorus) (100 %), followed by blackbirds (Turdus merula) (89.7 %), Eurasian wrens (Troglodytes troglodytes) (75 %), F. coelebs (60 %), European greenfinches (Carduelis chloris chloris) (57.1 %) (Fig. 1b), great tits (Parus major) (50 %), Eurasian nuthatches (Sitta europaea) (42.9 %), Robin (Erithacus rubecola) (25 %), house sparrow (Passer domesticus) (20 %), blue tits (Cyanistes caeruleus) (13.8 %), and blackcaps (Sylvia atricapilla) (7.7 %).
Table 1

Birds trapped in southern Italy and data on their infestation by Ixodes ricinus

Bird species

Birds infested/examined

Ticks collected

Prevalence (%)

Mean abundance

Mean intensity

Turdus merula

26/29

261

89.7

9

10.0

Cyanistes caeruleus

4/29

6

13.8

0.2

1.5

Sylvia atricapilla

2/26

3

7.7

0.1

1.5

Erithacus rubecola

6/24

23

25.0

1.0

3.8

Fringilla coelebs

12/20

63

60.0

3.2

5.3

Passer domesticus

4/20

4

20.0

0.2

1.0

Parus major

8/16

26

50.0

1.6

3.3

Carduelis chloris chloris

4/7

14

57.1

2.0

3.5

Sitta europaea

3/7

5

42.9

0.7

1.7

Regulus ignicapillus

1/4

3

25.0

0.8

3.0

Troglodytes troglodytes

3/4

17

75.0

4.3

5.7

Turdus viscivorus

2/2

26

100

13.0

13

Total

75/212

451

35.4

2.1

6.0

Birds trapped but not infested by ticks (number of trapped individuals are between parentheses): Dendrocopos medius (6), Emberiza cirlus (4), Certhia brachydactyla (3), Serinus serinus (3), Phoenicurus ochruros (3), Parus palustris (1), Picus viridis (1), Motacilla alba (1), Dendrocopos minor (1), and Turdus philomelos (1)

The overall mean intensity and abundance of infestation were 6.0 and 2.1, respectively being the intensity of infestation by larvae (3.2) higher than that by nymphs (2.8). The highest overall intensity and abundance (Fig. 2) of tick infestation was recorded in April 2010, when 117 ticks were retrieved on 25 birds (Table 2) belonging to 6 species. Conversely, no tick was found on birds captured in December. The highest overall intensity of infestation was found on T. viscivorus and T. merula for larvae, and on T. troglodytes and T. viscivorus for nymphs.
Table 2

Monthly variation in the number of birds and ticks collected from April 2010 to April 2011

Month

Birds infested/examined

Ticks collected

Prevalence (%)

Mean abundance

Mean intensity

April 2010

13/25

117

52.0

4.7

9.0

May

14/42

116

33.3

2.8

8.3

June

9/32

80

28.1

2.5

8.9

July

8/14

27

57.1

1.9

3.4

August

7/10

44

70.0

4.4

6.3

September

4/9

9

44.4

1.0

2.3

October

1/15

1

6.7

0.1

1.0

November

4/11

6

36.4

0.5

1.5

December

0/5

-

-

-

-

January 2011

1/18

1

5.6

0.1

1.0

February

1/10

1

10.0

0.1

1.0

March

4/11

12

36.4

1.1

3.0

April

9/10

37

90.0

3.7

4.1

https://static-content.springer.com/image/art%3A10.1007%2Fs10493-012-9571-8/MediaObjects/10493_2012_9571_Fig2_HTML.gif
Fig. 2

Monthly variation in temperature (red line) and relative humidity (blue line) and the mean abundance (grey columns) of tick infestation on birds netted in southern Italy. (Color figure online)

The intensity of infestation by larvae peaked in spring and summer, decreasing during autumn and winter months. On the other hand, nymphs were more frequent during spring, autumn, and winter.

Discussion

The present study demonstrates that autochthonous and migratory birds may play a role in the dispersion of I. ricinus immature stages in southern Italy. While most of the birds netted during this study were represented by autochthonous species, migratory birds were also netted and eventually infested by larvae and nymphs of I. ricinus. In particular, a high prevalence of tick infestation was recorded on T. merula, which is in accordance to previous reports (Estrada-Peña et al. 2005). Remarkably, this bird has been found carrying ticks infested by B. burgdorferi sensu lato in northern Italy (Manelli et al. 2005). This finding indicates that blackbirds could act as disseminators of ticks and associated pathogens from northern to southern Italy, for example.

It is acknowledged that birds play a role as long-distance carriers for some tick species and many associated pathogenic microorganisms (e.g., bacteria, parasites, viruses, and protozoa) some of which (e.g., B. burgdorferi) are of zoonotic importance (Kolonin 2008; Dubska et al. 2009; Gern 2009). Italy is at the centre of migratory routes of numerous bird species flying between Northern Africa and Central Europe, accounting for a total number of about 600 million (Manilla and Sobrero 1982). These birds might represent an eminent risk for the dispersion and introduction of tick-borne pathogens in previously free areas.

Previous studies have reported I. ricinus as the only tick species infesting birds in northern Italy (Meneguz et al. 2002; Paulauskas et al. 2009), which is in consonance to what was found in the present survey. Interestingly, a recent survey on ticks infesting hares in the same ecological reserve of southern Italy (Dantas-Torres et al. 2011) demonstrated the presence of other tick species as Dermacentor marginatus, Rhipicephalus bursa, Rhipicephalus turanicus, and Hyalomma marginatum, which are known parasites of birds (Manilla and Sobrero 1982). While the present study does not rule out the hypothesis that additional tick species may eventually parasitize birds in the studied area, it suggests that I. ricinus is the predominant species on birds. Additionally, this study places passerines as one of the main hosts of immature stages of I. ricinus in the studied area. Further studies focused on small terrestrial animals (e.g., rodents) should assess their role in the maintenance of the life cycle of this important tick in this region.

Ticks were found on 13 bird species, with blackbirds, finches, wrens and robins being the most infested passerines. Interestingly, these birds usually nest on the ground or in bushes and hedges near the ground, well protected from direct sunlight, which constitute a suited environment for some ticks, particularly for immature stages of I. ricinus (Manilla 1982). On the contrary, the other bird species, such as the spotted woodpecker and the green woodpecker, typically nest at the top of the trees and rarely coming to the ground, which ultimately reduces their risk of exposure to ticks. The presence of larvae and nymphs as well as the absence of adults is consistent with the existing knowledge on the bio-ecology of I. ricinus, whose immature stages parasitize small mammals, lizards, and birds (Manilla 1987).

Relative humidity, temperature, precipitation, and photoperiod are important factors determining the seasonality of I. ricinus, which is characterized by a peak in spring and early summer and a second one in autumn (Perret et al. 2004; Zákovská et al. 2007; Tagliapietra et al. 2011), although differences may be seen across Europe. In this study, a peak of tick infestation on birds was recorded during spring. Indeed, a substantial reduction of tick burdens was recorded from spring to fall. The variation of proportion between larvae and nymphs during the different period of the year was also worthy of note. A slight predominance of larvae was recorded in late spring, especially in May, followed by fair balance in terms larva: nymph ratio during the summer months until September. However, nymphs predominated over larvae during late autumn and winter.

In conclusion, this study supports the notion that birds may be partly responsible for the heterogeneous distribution of I. ricinus in Europe. Further studies are necessary to evaluate the influence of different bird species on I. ricinus ecology and their role in the eco-epidemiology of tick-borne diseases in southern Europe.

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© Springer Science+Business Media B.V. 2012