Abstract
Blackbirds (Turdus merula) and song thrushes (Turdus philomelos) were found to carry 95% of all spirochete-infected tick larvae among 40 bird species captured in Central Europe. More than 90% of the infections were typed as Borrelia garinii and Borrelia valaisiana. We conclude that thrushes are key players in the maintenance of these spirochete species in this region of Central Europe.
Lyme borreliosis is a tick-transmitted zoonosis caused by spirochete bacteria from the genus Borrelia. This genus comprises 13 named species, and at least 4 of these cause disease in humans, namely, Borrelia burgdorferi, Borrelia spielmanii, Borrelia afzelii, and Borrelia garinii (1, 14). All known strains of Lyme borreliosis spirochetes are maintained in nature by vertebrate hosts and ixodid ticks, with humans being ecological dead-end hosts.
For Europe, pheasants (Phasianus colchicus), a few seabird species, and some passerine bird species have been shown to be reservoir competent for B. garinii and B. valaisiana but not for B. afzelii, a rodent specialist (4, 5, 6, 7, 13). However, little is known about the roles of the numerous European woodland bird species in the ecology of Lyme borreliosis spirochetes (2, 13). Therefore, we captured birds of a wide range of species, many of which are migratory, and determined their importance as hosts to ticks and as reservoirs for Lyme borreliosis spirochetes in selected sites of Central Europe.
Ticks were collected from birds captured in four woodlands in Slovakia (16) during 2001 and 2002 and, in 2003, at one woodland in the southeastern Czech Republic. Questing adult and nymphal Ixodes ricinus ticks were collected from Slovak sites. Extracted DNA (3) was subjected to nested PCR targeting the 5S-23S intergenic spacer and also, in some cases, the flaB gene of Lyme borreliosis spirochetes (8, 15). Spirochete infections determined in ticks were assigned to species by the reverse line blot assay (5, 8, 15) or by DNA sequencing.
Risk factors for tick infestation and infection with B. burgdorferi genospecies were investigated in negative binomial and logistic regression models, respectively. Explanatory variables were month, year, site, and bird species. Data from the Czech Republic were excluded because of differences in collection year and bird species range. The level of significance was set at a P value of <0.05. Because of the poor fit of Poisson regression models, the negative binomial models were used. For detailed statistical methods and results, see the supplemental material.
Tick infestations of birds.
Of 529 birds captured (345 and 184 at sites in Slovakia and the Czech Republic, respectively, comprising 40 species of 17 families), 187 (145 in Slovakia and 42 in the Czech Republic) carried I. ricinus (463 and 157 larvae and 375 and 495 nymphs in Slovakia and the Czech Republic, respectively) (Table 1). In Slovakia, blackbirds (Turdus merula), song thrushes (Turdus philomelos), and European robins (Erithacus rubecula) carried 55.6% of all collected I. ricinus ticks. In the Czech Republic, European robins were less common and blackbirds and song thrushes carried 78.8% of I. ricinus ticks. When significant differences in infestation levels among months were accounted for, interspecies differences in tick infestations were found to be highly significant in Slovakia (Table 2). Five species/species groups carried significantly more larvae than all other bird species, being, in descending order, song thrushes, blackbirds, wheatears, finches and weaver finches, and tits (Table 2). Three species/species groups carried significantly more nymphs than other species, being, in descending order, blackbirds, song thrushes, and finches and weaver finches combined (Table 2).
TABLE 1.
List of birds captured in Slovakia and the Czech Republic and prevalence of their infestation with I. ricinus ticks
| Bird speciesa | No. of birds infested/no. captured | No. of larvae | No. of nymphs |
|---|---|---|---|
| Aegithalos caudatus (Linnaeus, 1758) (long-tailed tit) | 0/8 | ||
| Certhia familiaris (Linnaeus, 1758) (Eurasian treecreeper) | 0/6 | ||
| Prunella modularis (Linnaeus, 1758) (dunnock)b,c | 5/6 | 16 | 64 |
| Garrulus glandarius (Linnaeus, 1758) (Eurasian jay)b,d | 2/2 | 1 | 27 |
| Emberiza cia (Linnaeus, 1758) (rock bunting) | 1/3 | 1 | 0 |
| Emberiza citrinella (Linnaeus, 1758) (yellowhammer)d | 2/6 | 3 | 10 |
| Carduelis carduelis (Linnaeus, 1758) (European goldfinch) | 0/1 | ||
| Carduelis chloris (Linnaeus, 1758) (European greenfinch) | 0/3 | ||
| Coccothraustes coccothraustes (Linnaeus, 1758) (hawfinch)b | 15/23 | 33 | 45 |
| Fringilla coelebs (Linnaeus, 1758) (chaffinch)b | 8/20 | 72 | 21 |
| Serinus serinus (Linnaeus, 1758) (serin) | 1/1 | 0 | 1 |
| Hirundo rustica (Linnaeus, 1758) (barn swallow) | 0/6 | ||
| Lanius collurio (Linnaeus, 1758) (red-backed shrike) | 2/9 | 0 | 3 |
| Anthus trivialis (Linnaeus, 1758) (tree pipit) | 1/1 | 1 | 0 |
| Ficedula albicollis (Temminck, 1815) (collared flycatcher) | 0/2 | ||
| Muscicapa striata (Pallas, 1764) (spotted flycatcher) | 1/6 | 0 | 1 |
| Parus caeruleus (Linnaeus, 1758) (blue tit) | 4/16 | 0 | 8 |
| Parus major (Linnaeus, 1758) (great tit)b,d | 29/147 | 41 | 37 |
| Parus montanus (Baldenstein, 1824) (willow tit) | 1/5 | 3 | 4 |
| Parus palustris (Linnaeus, 1758) (marsh tit) | 8/22 | 4 | 6 |
| Parus ater (Linnaeus, 1758) (coal tit)c | 3/14 | 5 | 1 |
| Passer domesticus (Linnaeus, 1758) (house sparrow) | 1/1 | 0 | 1 |
| Passer montanus (Linnaeus, 1758) (Eurasian tree sparrow) | 0/2 | ||
| Dendrocopos major (Linnaeus, 1758) (great spotted woodpecker) | 0/5 | ||
| Picus canus (Gmelin, 1788) (gray-headed woodpecker) | 0/1 | ||
| Sitta europaea (Linnaeus, 1758) (nuthatch)d | 8/19 | 14 | 6 |
| Acrocephalus palustris (Bechstein, 1798) (marsh warbler) | 1/6 | 0 | 2 |
| Phylloscopus collybita (Vieillost, 1817) (chiffchaff)d | 3/8 | 2 | 2 |
| Phylloscopus sibilatrix (Bechstein, 1793) (wood warbler) | 0/1 | ||
| Regulus regulus (Linnaeus, 1758) (goldcrest) | 0/1 | ||
| Sylvia atricapilla (Linnaeus, 1758) (blackcap)b,d | 16/60 | 18 | 19 |
| Sylvia borin (Boddaert, 1783) (garden warbler) | 0/1 | ||
| Sylvia communis (Latham, 1787) (common whitethroat) | 0/1 | ||
| Sylvia curruca (Linnaeus, 1758) (lesser whitethroat) | 3/3 | 2 | 2 |
| Sylvia nisoria (Bechstein, 1795) (barred warbler) | 1/2 | 0 | 1 |
| Troglodytes troglodytes (Linnaeus, 1758) (winter wren) | 0/1 | ||
| Erithacus rubecula (Linnaeus, 1758) (European robin)b,d | 24/45 | 118 | 25 |
| Luscinia megarhynchos (Brehm, 1831) (nightingale) | 6/7 | 8 | 9 |
| Turdus merula (Linnaeus, 1758) (blackbird)b,d | 26/31 | 148 | 390 |
| Turdus philomelos (Brehm, 1831) (song thrush)b,d | 22/27 | 130 | 185 |
| Total | 194/529 | 620 | 870 |
Bird species with no mark were captured in Slovakia only.
Bird species with Borrelia-infected ticks.
Bird species captured in the Czech Republic only.
Bird species captured in Slovakia and the Czech Republic also.
TABLE 2.
Variables significantly associated with infestation of birds with larval and nymphal Ixodes ricinus ticks (in the most parsimonious negative binomial regression models) and with infection with B. burgdorferi sensu lato and its genospecies in larvae and nymphs collected from the birds (in the most parsimonious logistic regression models)a
| Outcome, explanatory variable, and factor | Coefficient SE | OR (95% CI) | Wald z | P |
|---|---|---|---|---|
| Infestation with nymphal I. ricinus | ||||
| Mo | ||||
| July | −1.60 (0.46) | −3.48 | <0.001 | |
| October | −1.90 (0.50) | −3.79 | <0.001 | |
| Otherb | ||||
| Bird species/species group | ||||
| Blackbird | 2.80 (0.43) | 6.57 | <0.001 | |
| Song thrush | 2.56 (0.43) | 5.90 | <0.001 | |
| Finches and weaver finches | 0.99 (0.27) | 3.64 | <0.001 | |
| Otherb | ||||
| Constant | −0.08 (0.37) | −0.21 | ||
| Infestation with larval I. ricinus | ||||
| Mo | ||||
| May | 1.97 (0.84) | 2.34 | <0.05 | |
| June | 2.37 (0.97) | 2.44 | <0.05 | |
| July | 1.91 (0.84) | 2.28 | <0.05 | |
| September | 3.74 (1.14) | 3.26 | <0.05 | |
| Bird species/species group | ||||
| Song thrush | 3.32 (0.68) | 4.88 | <0.001 | |
| Blackbird | 3.17 (0.71) | 4.46 | <0.001 | |
| Wheatears (robin and nightingale) | 2.33 (0.46) | 5.00 | <0.001 | |
| Finches and weaver finches | 2.14 (0.43) | 4.92 | <0.001 | |
| Tits | 1.20 (0.45) | 2.68 | <0.01 | |
| Otherb | ||||
| Constant | −3.26 (0.86) | −3.79 | ||
| Infection of larvae with B. burgdorferi sensu lato | ||||
| Bird species/species group | ||||
| Blackbird and song thrush | 1.495 (81-27 × 103) | 4.93 | <0.001 | |
| Otherb | ||||
| Constant | 0.002 (0-0.01) | −5.96 | ||
| Infection of nymphs with B. burgdorferi sensu lato | ||||
| Mo | ||||
| May to July | 32.46 (3.03-343.77) | 2.88 | <0.01 | |
| Otherb | ||||
| Constant | 0.004 (0-0.05) | −4.34 | ||
| Infection of larvae with B. garinii | ||||
| Yr | ||||
| 2001 | 22.42 (1.16-103.01) | −2.06 | <0.05 | |
| 2002b | ||||
| Bird species/species group | ||||
| Blackbird and song thrush | 4.817 (44-44 × 104) | 3.54 | <0.001 | |
| Otherb | ||||
| Constant | 0.004 (0-0.15) | −3.02 | ||
| Infection of nymphs with B. garinii | ||||
| Bird species/species group | ||||
| Blackbird and song thrush | 28.79 (4.35-190.57) | 3.49 | <0.001 | |
| Otherb | ||||
| Constant | 0 (0-0.01) | −4.56 | ||
| Infection of nymphs with B. valaisiana | ||||
| Bird species/species group | ||||
| Blackbird and song thrush | 7.48 (2.08-26.84) | 3.09 | <0.01 | |
| Otherb | ||||
| Constant | 0.03 (0.01-0.08) | −6.55 |
For both negative binomial and logistic regression models, the most parsimonious models were those in which no explanatory variables could be removed without significantly (P < 0.05) affecting model deviance. OR, odds ratio; 95% CI, 95% confidence interval.
Reference factor.
Infection of I. ricinus ticks collected from birds.
A total of 1,461 I. ricinus ticks (607 larvae and 854 nymphs) derived from 189 birds were tested for infection with Lyme borreliosis spirochetes. One-third of these birds, belonging to nine species, carried infected ticks (Table 3). The overall prevalences of infection in bird-derived larvae and nymphs with spirochetes were 22.4% and 25.3%, respectively. Blackbirds and song thrushes were significantly more likely to carry spirochete-infected larvae (43.8% and 51.9%, respectively) (Table 2). There was no significant difference among bird species in the prevalence of infection in nymphs.
TABLE 3.
Prevalence of Borrelia genospecies in I. ricinus ticks feeding on birdsa
| Bird species | Stage | No. of infected ticksc/no. tested (%) | No. of birds yielding infected ticks/no. tested (%) | No. of ticks infected with indicated Borrelia genospeciesb (no. infested with infected ticks)
|
||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| BGA | BVA | BAF | BBSS | BGA + BVA | BGA + BAF | BVA + BAF | BGA + BVA + BAF | ND | ||||
| Prunella modularis (dunnock) | L | 2/16 (12.5) | 1/5 (20) | 2 (1) | ||||||||
| N | 20/63 (31.7) | 4/5 (80) | 7 (4) | 8 (2) | 3 (1) | 2 (2) | ||||||
| Garrulus glandarius (Eurasian jay) | L | 0/1 (0) | 0/2 (0) | |||||||||
| N | 3/27 (11.1) | 2/2 (100) | 1 (1) | 2 (2) | ||||||||
| Coccothraustes coccothraustes (hawfinch) | L | 1/33 (3) | 1/15 (6.7) | 1 (1) | ||||||||
| N | 8/44 (18.2) | 6/15 (40) | 2 (2) | 4 (4) | 2 (2) | |||||||
| Fringilla coelebs (chaffinch) | L | 1/71 (1.4) | 1/8 (12.5) | 1 (1) | ||||||||
| N | 1/21 (4.8) | 1/8 (12.5) | 1 (1) | |||||||||
| Parus major (great tit) | L | 1/40 (2.5) | 1/24 (4.2) | 1 (1) | ||||||||
| N | 5/37 (13.5) | 4/24 (16.7) | 2 (2) | 2 (2) | 1 (1) | |||||||
| Sylvia atricapilla (blackcap) | L | 0/16 (0) | 0/16 (0) | |||||||||
| N | 1/18 (5.6) | 1/16 (6.3) | 1 (1) | |||||||||
| Erithacus rubecula (European robin) | L | 0/114 (0) | 0/23 (0) | |||||||||
| N | 1/24 (4.2) | 1/23 (4.3) | 1 (1) | |||||||||
| Turdus merula (blackbird) | L | 64/146 (43.8) | 13/26 (50) | 29 (6) | 23 (6) | 6 (5) | 6 (2) | |||||
| N | 126/383 | 20/26 (76.9) | 53 (8) | 38 (15) | 6 (5) | 1 (1) | 16 (3) | 1 (1) | 1 (1) | 1 (1) | 9 (6) | |
| Turdus philomelos (song thrush) | L | 67/129 (51.9) | 11/22 (50) | 27 (8) | 36 (6) | 1 (1) | 3 (3) | |||||
| N | 51/181 (28.2) | 14/22 (63.6) | 31 (13) | 8 (2) | 1 (1) | 5 (3) | 1 (1) | 5 (4) | ||||
| Total | L | 136/566 (24) | 28/141 (19.9) | 58 (16) | 61 (13) | 0 (0) | 0 (0) | 7 (6) | 0 (0) | 0 (0) | 0 (0) | 10 (6) |
| N | 216/798 (27.1) | 53/141 (37.6) | 97 (31) | 62 (27) | 11 (8) | 1 (1) | 22 (7) | 1 (1) | 2 (2) | 1 (1) | 19 (15) | |
BGA, B. garinii; BVA, B. valaisiana; BAF, B. afzelii; BBSS, B. burgdorferi sensu stricto; ND, not determined; L, larvae; N, nymphs.
In some cases, the sum of Borrelia species infections was greater than the number of infected ticks because of mixed infections.
Number of ticks that tested positive for Borrelia species.
B. garinii and B. valaisiana were the most frequent genospecies (infecting 50.3% and 43.8%, respectively). No larvae were infected with B. afzelii and B. burgdorferi, but 3.7% and 0.3% of nymphs, respectively, were infected with these species. Mixed infections were detected in 33 ticks, with the most frequent combination being B. garinii and B. valaisiana (87.8%) (Table 3).
Most B. garinii-infected larvae (96.5%) and nymphs (86.7%) were collected from song thrushes and blackbirds, which was highly significant at the Slovak sites (Table 2). All B. valaisiana-infected larvae and nearly all B. valaisiana-infected nymphs from birds in Slovakia came from song thrushes and blackbirds. There were no significant differences among years, sites, months, or bird species in the prevalence of B. afzelii infection in nymphs collected from the birds. Most of the sequenced untypeable samples (80%) clustered with B. garinii, except for two infections in nymphs from birds that clustered with B. afzelii and one sample with B. valaisiana.
Four species of the Lyme borreliosis group were identified in 914 questing I. ricinus ticks, of which 40.5% were assigned to B. valaisiana, 33% to B. garinii, 23% to B. afzelii, and 2.2% to B. burgdorferi (Table 4).
TABLE 4.
Prevalence of Borrelia genospecies in questing I. ricinus ticksa
| Locality (yr) | Stage | No. of infected ticksc/no. tested (%) | No. of ticks infected with indicated Borrelia genospeciesb (%)
|
|||||||
|---|---|---|---|---|---|---|---|---|---|---|
| BGA | BVA | BAF | BBSS | BGA + BVA | BGA + BAF | BGA + BVA + BAF | ND | |||
| Site 1, Šúr (2001, 2002) | N | 57/205 (27.8) | 18 (31.6) | 22 (38.6) | 3 (5.3) | 8 (14) | 2 (3.5) | 2 (3.5) | 2 (3.5) | |
| A | 78/232 (33.6) | 23 (29.5) | 33 (42.3) | 6 (7.7) | 2 (2.6) | 1 (1.3) | 13 (16.7) | |||
| Site 2, Malacky (2002) | N | 31/215 (14.4) | 1 (3.2) | 4 (12.9) | 24 (77.4) | 1 (3.2) | 1 (3.2) | |||
| A | 13/56 (23.2) | 2 (15.4) | 6 (46.2) | 2 (15.4) | 3 (23.1) | |||||
| Site 3, Drienovec (2002) | N | 4/27 (14.8) | 2 (50) | 1 (25) | 1 (25) | |||||
| A | 20/75 (26.7) | 5 (25) | 8 (40) | 2 (10) | 5 (25) | |||||
| Site 4, Brzotín (2002) | N | 14/70 (20.0) | 3 (21.4) | 1 (7.1) | 8 (57.1) | 1 (7.1) | 1 (7.1) | |||
| A | 10/34 (29.4) | 4 (40) | 3 (30) | 2 (20) | 1 (10) | |||||
| Total | N | 106/517 (20.5) | 22 (20.8) | 27 (25.5) | 37 (34.9) | 2 (1.9) | 9 (8.5) | 3 (2.8) | 2 (1.9) | 4 (3.8) |
| A | 121/397 (30.5) | 34 (28.1) | 50 (41.3) | 10 (8.3) | 3 (2.5) | 4 (3.3) | 1 (0.8) | 19 (15.7) | ||
BGA, B. garinii; BVA, B. valaisiana; BAF, B. afzelii; BBSS, B. burgdorferi sensu stricto; ND, not determined; N, nymphs; A, adults.
In some cases, the sum of Borrelia species infections was greater than the number of infected ticks because of mixed infections.
Number of ticks that tested positive for Borrelia species.
Here, we show that among 40 bird species captured in woodlands of Slovakia and the Czech Republic, 2 species of thrushes (i.e., blackbird and song thrush) constitute the core reservoir of B. garinii and B. valaisiana. The comparison of the genospecies richness in tick larvae derived from the birds with that determined for questing nymphs and adults collected at the same sites confirms previous observations that birds are not involved in the maintenance of B. afzelii (6, 8, 9, 10).
The statistical analyses show that the relative roles of song thrushes and blackbirds as hosts for ticks and reservoirs of B. garinii and B. valaisiana in Slovakia are not due to confounding factors, such as variations among sites and months for the birds captured (see the supplemental material). The data from the Czech Republic could not be included in the statistical analyses, because it differed in terms of times of collection and in the range of species of birds that were captured. However, it also showed that the roles of thrushes and blackbirds as hosts for ticks and reservoirs of B. garinii and B. valaisiana are similar in both countries. Infestation of blackbirds and song thrushes with large numbers of Borrelia-infected tick larvae has also been observed in Asia (11, 12).
In conclusion, blackbirds and song thrushes (both members of the thrush group) appear to constitute a core functional group among the avian reservoir host community for Lyme borreliosis spirochetes in the region. Thus, the ecology of these two avian species is likely to be key to the eco-epidemiology of B. garinii, the causative agent of borreliosis in Central Europe.
Nucleotide sequence accession numbers.
The GenBank accession numbers of the sequences obtained in this study are DQ520861, DQ520872, DQ520863, DQ520871, DQ520870, DQ458997, DQ520865, DQ517433, DQ520862, DQ520864, DQ520869, DQ520866, DQ520868, DQ520867 (5S-23S ribosomal DNA intergenic spacer), DQ490971, DQ490973, DQ490972, DQ490977, DQ490978, DQ490967, DQ490970, DQ490976, DQ490974, DQ490968, DQ490975, and DQ490969 (flaB gene).
Supplementary Material
Acknowledgments
We thank Milan Olekšák, Rožňava, Slovakia, for help with the field work.
This study was supported by the Slovak Research and Development Agency under contract no. APVV-51-009205 (to M.D.) and no. APVV-51-004505 (to M.L.), the Wellcome Trust London, United Kingdom (to K.K.), and grant no. MSM6215712402 from the Ministry of Education, Youth and Sports of the Czech Republic (to I.L.).
Footnotes
Published ahead of print on 21 December 2007.
Supplemental material for this article may be found at http://aem.asm.org/.
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Associated Data
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