Antimicrobial resistant and extended-spectrum β-lactamase producing Escherichia coli in common wild bird species in Switzerland.

A total of 294 fecal swabs from 294 wild birds in Switzerland were cultivated for antimicrobial resistant (AMR) Escherichia coli. Samples were also subcultivated to detect E. coli with extended-spectrum β-lactamases (ESBL), carbapenemases, and plasmid-mediated aminoglycoside or colistin resistance, respectively. Samples from 17 (5.8%) of the birds contained 19 AMR E. coli, whereof 26.3% were multidrug resistant. Five (1.7%) ESBL-producing E. coli were detected. The isolates harbored blaCTX-M-1 (two isolated from carrion crows and from one great spotted woodpecker, respectively), blaCTX-M-15 (originating from a grey heron), blaCTX-M-55 (from a carrion crow), and blaCTX-M-65 (from a common blackbird). Phylogenetic analysis assigned three isolates to commensal phylogroups A and B1, one to extraintestinal pathogenic group B2, and one to phylogroup F. Multilocus sequence typing identified sequence types (STs) that have been found previously in ESBL E. coli in wild birds (ST58, ST205, ST540). One isolate harboring blaCTX-M-55 was assigned to the recently emerged fluoroquinolone-resistant, extraintestinal pathogenic E. coli clone ST1193. Wild birds have the potential to disperse AMR, including clinically important resistance genes, from anthropogenic-influenced habitats to diverse areas, including vulnerable natural environments such as surface waters or mountain regions.

Antimicrobial resistance (AMR) is one of the major threats to public health. AMR affects humans, animals, and the environment and intervention requires a one health approach (World Health Organization, 2014). Although wildlife is rarely directly exposed to antimicrobial agents, wild birds may be colonized or infected with resistant bacteria (Guenther, Ewers, & Wieler, 2011; Oteo et al., 2018). The emergence of AMR in wild birds is thought to be due to the dissemination of resistant bacteria or AMR genes from anthropogenic‐influenced habitats to the natural environment via contaminated water or feed (Guenther et al., 2010). In turn, wild birds may represent a reservoir for bacteria harboring clinically important resistance determinants (Arnold, Williams, & Bennett, 2016). Migratory wild birds in particular, are known to be disseminators of AMR into geographically distant ecosystems (Agnew, Wang, Fanning, Bearhop, & McMahon, 2015). There is a growing number of reports of bacteria with clinically relevant AMR isolated from wild birds worldwide, including strains harboring extended‐spectrum β‐lactamase (ESBL) genes (bla ESBL), carbapenemase genes, aminoglycoside, and quinolone resistance genes (Bonnedahl et al., 2010; Guenther et al., 2012; Oteo et al., 2018). By contrast, information on the occurrence of AMR in wild and peri‐domesticated birds in Switzerland is scarce. In one study, feral pigeons and great cormorants were identified as potential reservoirs of ESBL‐producing Escherichia (E.) coli (Zurfluh, Nüesch‐Inderbinen, Stephan, & Hächler, 2013). However, there is a lack of data regarding the occurrence of AMR among other wild birds, including resident and migratory birds.

The Swiss Ornithological Institute in Sempach is a nongovernmental organization that monitors the populations of breeding birds, migrants, and winter visitors in Switzerland. In addition, it maintains a rescue, care, and rehabilitation center for orphaned or injured wild birds. In this study, we aimed to investigate fecal samples from wild birds admitted to the care center for the occurrence of AMR E. coli, and to identify Enterobacteriaceae with transmissible resistance to third‐generation cephalosporins, carbapenems, aminoglycosides, and colistin.

Between May and October 2018, fecal swabs were collected in the rehabilitation center from 294 birds representing 55 different species. The majority (246/83.7%) were nestlings, pulli, or juvenile birds. A complete list of the birds is available in Appendix Table A1 From live birds, swabs of freshly passed feces were sampled directly from a sterile surface, and from dead birds a fecal swab was collected from the cloaca. Swabs were numbered consecutively and admitted to the laboratory for analysis. For nonselective isolation of E. coli, swabs were inoculated onto Rapid’E. coli 2 Agar Plates (Bio‐Rad Laboratories, Reinach, Switzerland). For selective isolation of resistant Enterobacteriaceae, the same swabs were thereafter placed in 5 ml tubes containing Enterobacteriaceae Enrichment broth (BD, Franklin Lakes) and incubated at 37°C for 24 hr. One loopful of each enrichment was inoculated onto Brilliance ESBL Agar (Oxoid/Thermo Fisher Scientific, Waltham, MA), chromID® CARBA SMART (bioMérieux, Marcy l'Etoile, France), amikacin‐Luria Bertani agar (200 mg/L amikacin, 10 mg/ml vancomycin, and 5 mg/L amphotericin B), and colistin‐bromothymol blue lactose agar (4 mg/L colistin, 10 mg/ml vancomycin, and 5 mg/L amphotericin B). Plates were incubated at 37°C for 24 hr. Species identity was confirmed by matrix‐assisted laser desorption/ionization time‐of‐flight mass spectrometry (Biotyper® MALDI‐TOF‐MS system by Bruker Daltonics, Billerica, MA) using Compass FlexControl version 3.4 software with the Compass database version 4.1.80.

From 158 fecal samples (53.7% of all samples), a total of 256 E. coli isolates were obtained by nonselective cultivation. Antimicrobial susceptibility testing using the disk‐diffusion method according the Clinical and Laboratory Standards Institute performance standards (Clinical and Laboratory Standards Institute, 2017) detected antibiotic resistance in 19 (7.4%) of the E. coli isolates which originated from 17 (5.8%) of the 294 analyzed birds (Table 1). One sample from a feral pigeon yielded three E. coli strains with distinct resistance profiles (Table 1). Multidrug resistance (MDR), defined as resistance to three or more classes of antimicrobials was identified in 5 (26.3%) of the 19 resistant E. coli isolates, thus in 2% of the 256 isolated E. coli (Table 1).

Table 1

Antimicrobial resistant Escherichia coli obtained by nonselective isolation from fecal swabs of wild birds

Isolate	Resistance profile	Wild birds
		Species	Common name	Migratory behavior	Age
191 C1	AM, CZ, TE	Columba livia domestica	Feral pigeon	Resident	Juvenile
273 C1	AM, TE	Columba livia domestica	Feral pigeon	Resident	Adult
151 C1	AM, NA, SXT, S, C, TE	Columba livia domestica	Feral pigeon	Resident	Juvenile
151 C2	AM, NA, CIP, SXT, AZM, F/M, S, GM, C, TE
151 C3	AM, NA, CIP, S, K, C, TE
070 C1	CZ, SXT	Cygnus olor	Mute swan	Resident	Nestling
255 C1	AM, NA, CIP, SXT, C, TE	Streptopelia decaocto	Eurasian collared dove	Resident	Adult
039 C1	S	Anas platyrhynchos	Mallard	Resident to short distance	Pullus
046 C4	AM, CZ, AMC, AZM	Anas platyrhynchos	Mallard	Resident to short distance	Pullus
193 C1	K	Anas platyrhynchos	Mallard	Resident to short distance	Juvenile
277 C1	AM, S, GM	Buteo buteo	Common buzzard	Resident to short distance	Adult
009 C3	CZ	Corvus corone	Carrion crow	Resident to short distance	Nestling
114 C1	TE	Corvus corone	Carrion crow	Resident to short distance	Nestling
202 C1	TE	Larus michahellis	Yellow‐legged gull	Resident to short distance	Juvenile
200 C1	NA, TE	Milvus milvus	Red kite	Resident to short distance	Juvenile
203 C1	NA	Milvus milvus	Red kite	Resident to short distance	Juvenile
147 C1	NA, CIP, SXT, C	Turdus merula	Common blackbird	Resident to short distance	Juvenile
198 C1	NA	Falco subbuteo	Eurasian hobby	Long distance	Adult
263 C1	TE	Hirundo rustica	Barn swallow	Long distance	Juvenile

AM: ampicillin; AMC: amoxicillin/clavulanic acid; AZM: azithromycin; C: chloramphenicol; CIP: ciprofloxacin; CZ: cefazolin; F/M: nitrofurantoin; GM: gentamicin; K: kanamycin; NA: nalidixic acid; S: streptomycin; SXT: sulfamethoxazole/trimethoprim; TE: tetracycline.

Among the 17 birds with AMR E. coli, 5 (29.4%) were resident birds, 10 (58.8%) were birds with resident to short‐distance migratory behavior, and 2 (11.8%) were long‐distance migrants (Table 1). The majority (13/76.5%) were nestlings, pulli, or juvenile birds (Table 1). Their AMR E. coli are likely acquired via parental transfer. Therefore, it cannot be excluded that the occurrence of AMR in adult birds, which are exposed to a diverse pool of AMR, may be higher than our data suggest.

Within the set of AMR E. coli, high rates of resistance to ampicillin (8/19 isolates), nalidixic acid (8/19), and tetracycline (10/19) were observed. Resistance to chloramphenicol (5/19), ciprofloxacin (4/19), cefazolin (4/19), streptomycin (5/19), and sulfamethoxazole/trimethoprim (5/19) were less often detected, and resistance to amoxicillin/clavulanic acid (1/19), azithromycin (2/19), nitrofurantoin (1/19), gentamicin (2/19), and kanamycin (2/19) occurred rarely (Table 1). The high rate of resistance to ampicillin and tetracycline correlates with AMR data reported by the Federal Office of Public Health for E. coli isolated from livestock in Switzerland (Federal Office of Public Health and Federal Food Safety and Veterinary Office, 2018), indicating potential transmission events of AMR between livestock and wildlife.

By selective cultivation, five ESBL‐producing E. coli were detected in samples from five (1.7%) of the 294 birds, including two carrion crows, a common blackbird, a great spotted woodpecker, and a grey heron (Table 2). Phylogenetic groups, multilocus sequence types (STs), and bla ESBL genes were determined by PCR and sequencing as described previously (Clermont, Christenson, Denamur, & Gordon, 2013; Wirth et al., 2006; Woodford, Fagan, & Ellington, 2006; Zurfluh, Hächler, Nüesch‐Inderbinen, & Stephan, 2013) (Table 2). Two isolates belonging to commensal phylogroups A and B1 harbored bla CTX‐M‐1. A further strain assigned to phylogroup B1 carried bla CTX‐M‐65. One isolate belonged to extraintestinal pathogenic phylogenetic group B2 and carried bla CTX‐M‐55. One isolate harboring bla CTX‐M‐15 was assigned to phylogenetic group F (Table 2). This particular phylogroup is rarely identified, but of particular interest, since strains belonging to this group are associated with extraintestinal infections of companion animals and have been frequently detected in wild birds being treated in wildlife rehabilitation centers (Vangchhia et al., 2016). Overall, five different STs were detected among the ESBL E. coli (Table 2). The majority of these, including ST58, ST205, ST540, and ST1722, have already been reported in ESBL‐producing E. coli from waterfowl in Pakistan (Mohsin et al., 2017), gulls in Chile (Hernandez et al., 2013) Portugal (Guenther et al., 2011) and Sweden (Atterby et al., 2017). Interestingly, E. coli ST1193 belongs to extraintestinal pathogenic pandemic clonal group associated with urinary tract infections (UTIs) in humans and is, similar to the E. coli ST131 H30 clone, an important contributor to fluoroquinolone resistance worldwide (Tchesnokova et al., 2019). This clone has very recently emerged as an MDR bla CTX‐M‐14 and bla CTX‐M‐15 harboring nosocomial pathogen in Germany (Valenza et al., 2019). Further, E. coli ST1193 harboring bla CTX‐M‐55 represents one of the most prevalent ESBL‐producing E. coli associated with UTI in China (Xia et al., 2017). Our results indicate that wild birds may contribute to the global dissemination of this important clonal lineage.

Table 2

Characteristics of extended‐spectrum β‐lactamase (ESBL)‐producing Escherichia coli isolates from wild birds in Switzerland

Isolate	PG	ST	ESBL	Resistance profile	Wild birds
					Species	Common name	Migratory behavior	Age
127	A	540	CTX‐M‐1	AM, CZ, CTX, K, TE	Dendrocopos major	Great spotted woodpecker	Resident	Juvenile
114	B1	205	CTX‐M‐1	AM, CZ, CTX, NA, CIP, SXT, S, K, TE	Corvus corone	Carrion crow	Resident to short distance	Nestling
9	B2	1193	CTX‐M‐55	AM, CZ, CTX, NA, CIP, SXT, AZM, GM	Corvus corone	Carrion crow	Resident to short distance	Nestling
59	B1	58	CTX‐M‐65	AM, CZ, CTX, C, TE	Turdus merula	Common blackbird	Resident to short distance	Nestling
235	F	1722	CTX‐M‐15	AM, CZ, CTX, FEP, SXT, S, TE	Ardea cinerea	Grey heron	Short distance	Adult

AM: ampicillin; AZM: azithromycin; C: chloramphenicol; CIP: ciprofloxacin; CTX: cefotaxime; CZ: cefazolin; FEP: cefepime; GM: gentamicin; K: kanamycin; NA: nalidixic acid; PG: phylogenetic group; S: streptomycin; ST: sequence type; SXT: sulfamethoxazole/trimethoprim; TE: tetracycline.

Using selective cultivation with colistin, two Enterobacter asburiae and one Enterobacter cancerogenus were found (data not shown). Screening for plasmid‐mediated colistin resistance genes mcr‐1 through mcr‐5 was undertaken by PCR (Rebelo et al., 2018), but remained negative for all isolates. Selective isolation using chromID® CARBA SMART or amikacin did not yield any strains.

Of the ESBLs detected in this study, CTX‐M‐15, isolated from E. coli from a grey heron in this study, is one of the most important ESBLs in human medicine. E. coli producing this enzyme has emerged worldwide as an important cause of bloodstream infections and of community‐acquired UTIs (Cantón, González‐Alba, & Galán, 2012). Its single amino acid variant, CTX‐M‐55, identified in a sample from a carrion crow, was first detected in Thailand from E. coli and Klebsiella pneumoniae causing community‐ and hospital‐acquired infection and has since been found widely in food‐producing animals and humans in China (Zhang et al., 2014). Similarly, CTX‐M‐65 is a prevalent ESBL in animal and human E. coli strains and Salmonella spp. in China (Bai et al., 2016). By contrast, CTX‐M‐1 is prevalent within the poultry industry and other livestock in Europe (Zurfluh et al., 2014). In Switzerland, all four ESBL variants described in this study have been detected in E. coli isolated from healthy humans, livestock, food, surface water, and fish from Swiss lakes (Müller, Stephan, & Nüesch‐Inderbinen, 2016). Notably, the ESBL variants were all isolated from birds frequently observed in urbanized areas, thus, the occurrence of these variants in wild birds is likely associated with proximity to human and livestock‐associated settings, as well as exposure to contaminated surface waters (Guenther et al., 2012).

Reassuringly, bla ESBL genes were rare among the birds analyzed in this study, and no acquired carbapenemase genes, mcr genes, or transmissible aminoglycoside genes were detected. Our results contrast with data reported in a study that identified bla ESBL genes, the carbapenemase gene bla OXA‐48, and mcr in 8.7%, 0.8%, and 0.1%, respectively, of 28 species of wild birds in Spain (Oteo et al., 2018). However, caution should be used when comparing data obtained using different methods for screening for ESBL producers. In contrast to Oteo et al. (2018), we used a semi‐selective enrichment step prior to plating on selective ESBL agar, which may have affected the recovery rate. The difference in the performance of semi‐selective (using broth selecting for Gram negative rods) and selective enrichment (i.e., broth additionally containing a third‐generation cephalosporin) remains to be elucidated and comparative data are limited (Blane et al., 2016; Jazmati, Hein, & Hamprecht, 2016; Kluytmans‐Van Den Bergh et al., 2015).

Migratory birds in particular have been identified as potent disseminators of AMR, because they may cover long distances and impact diverse ecological niches by introducing new or emerging AMR (Agnew et al., 2015). Whilst the majority of the birds from this study were resident or short‐distance migratory birds, they nonetheless have the potential to disperse AMR to diverse areas, including vulnerable environments such as surface waters or mountain regions. Moreover, they can be considered indicators for the occurrence and distribution of AMR in the environment.

CONFLICT OF INTERESTS

None declared.

AUTHOR CONTRIBUTIONS

RS and BRV contributed to design of the study. PM performed sampling. KZ and PK performed laboratory analysis. KZ, SA, RS, BRV, and MN‐I performed data analysis. KZ and MN‐I drafted the manuscript. All authors contributed helpful comments and approved the final version of the manuscript.

ETHICS STATEMENT

This study conformed to the legal requirements of Switzerland and in accordance with the guidelines of the Swiss Ornithological Institute.

Table A1

Overview of 294 wild birds screened for fecal cloacal occurrence of antimicrobial resistant Escherichia coli

Strain ID	Species	Common name	No. birds/species	Migratory behavior	Age
AMR 0194	Tachymarptis melba	Alpine swift	3	Long distance	Juvenile
AMR 0227	Tachymarptis melba	Alpine swift		Long distance	Juvenile
AMR 0238	Tachymarptis melba	Alpine swift		Long distance	Juvenile
AMR 0285	Tyto alba	Barn owl	1	Resident	Juvenile
AMR 0231	Hirundo rustica	Barn swallow	5	Long distance	Juvenile
AMR 0263	Hirundo rustica	Barn swallow		Long distance	Juvenile
AMR 0279	Hirundo rustica	Barn swallow		Long distance	Juvenile
AMR 0290	Hirundo rustica	Barn swallow		Long distance	Juvenile
AMR 0294	Hirundo rustica	Barn swallow		Long distance	Juvenile
AMR 0144	Milvus migrans	Black kite	1	Long distance	Adult
AMR 0026	Phoenicurus ochruros	Black redstart	7	Short distance	Nestling
AMR 0069	Phoenicurus ochruros	Black redstart		Short distance	Adult
AMR 0091	Phoenicurus ochruros	Black redstart		Short distance	Juvenile
AMR 0092	Phoenicurus ochruros	Black redstart		Short distance	Juvenile
AMR 0137	Phoenicurus ochruros	Black redstart		Short distance	Adult
AMR 0145	Phoenicurus ochruros	Black redstart		Short distance	Adult
AMR 0274	Phoenicurus ochruros	Black redstart		Short distance	Adult
AMR 0006	Corvus corone	Carrion crow	13	Resident to short distance	Nestling
AMR 0009	Corvus corone	Carrion crow		Resident to short distance	Nestling
AMR 0028	Corvus corone	Carrion crow		Resident to short distance	Juvenile
AMR 0071	Corvus corone	Carrion crow		Resident to short distance	Pullus
AMR 0072	Corvus corone	Carrion crow		Resident to short distance	Nestling
AMR 0081	Corvus corone	Carrion crow		Resident to short distance	Nestling
AMR 0103	Corvus corone	Carrion crow		Resident to short distance	Nestling
AMR 0114	Corvus corone	Carrion crow		Resident to short distance	Nestling
AMR 0117	Corvus corone	Carrion crow		Resident to short distance	Nestling
AMR 0118	Corvus corone	Carrion crow		Resident to short distance	Nestling
AMR 0119	Corvus corone	Carrion crow		Resident to short distance	Nestling
AMR 0169	Corvus corone	Carrion crow		Resident to short distance	Juvenile
AMR 0192	Corvus corone	Carrion crow		Resident to short distance	Adult
AMR 0005	Turdus merula	Common blackbird	45	Resident to short distance	Juvenile
AMR 0010	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0017	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0024	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0031	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0033	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0059	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0060	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0061	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0064	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0066	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0076	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0077	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0084	Turdus merula	Common blackbird		Resident to short‐distance	Nestling
AMR 0085	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0105	Turdus merula	Common blackbird		Resident to short distance	Pullus
AMR 0106	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0109	Turdus merula	Common blackbird		Resident to short distance	Adult
AMR 0115	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0124	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0130	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0133	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0135	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0143	Turdus merula	Common blackbird		Resident to short distance	Adult
AMR 0147	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0154	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0161	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0162	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0163	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0171	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0175	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0176	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0211	Turdus merula	Common blackbird		Resident to short distance	Nestling
AMR 0213	Turdus merula	Common blackbird		Resident to short‐distance	Juvenile
AMR 0223	Turdus merula	Common blackbird		Resident to short distance	Adult
AMR 0239	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0240	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0241	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0242	Turdus merula	Common blackbird		Resident to short distance	Adult
AMR 0247	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0254	Turdus merula	Common blackbird		Resident to short distance	Adult
AMR 0257	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0258	Turdus merula	Common blackbird		Resident to short distance	Juvenile
AMR 0264	Turdus merula	Common blackbird		Resident to short distance	Adult
AMR 0297	Turdus merula	Common blackbird		Resident to short distance	Adult
AMR 0197	Buteo buteo	Common buzzard	2	Resident to short distance	Adult
AMR 0277	Buteo buteo	Common buzzard		Resident to short distance	Adult
AMR 0102	Fringilla coelebs	Common caffinch	4	Resident to short distance	Juvenile
AMR 0150	Fringilla coelebs	Common caffinch		Resident to short distance	Nestling
AMR 0220	Fringilla coelebs	Common caffinch		Resident to short distance	Nestling
AMR 0222	Fringilla coelebs	Common caffinch		Resident to short distance	Adult
AMR 0204	Delichon urbicum	Common house martin	3	Long distance	Adult
AMR 0205	Delichon urbicum	Common house martin		Long distance	Nestling
AMR 0284	Delichon urbicum	Common house martin		Long distance	Adult
AMR 0123	Falco tinnunculus	Common kestrel	6	Resident to short distance	Pullus
AMR 0146	Falco tinnunculus	Common kestrel		Resident to short distance	Nestling
AMR 0157	Falco tinnunculus	Common kestrel		Resident to short distance	Juvenile
AMR 0160	Falco tinnunculus	Common kestrel		Resident to short distance	Juvenile
AMR 0190	Falco tinnunculus	Common kestrel		Resident to short distance	Juvenile
AMR 0196	Falco tinnunculus	Common kestrel		Resident to short distance	Juvenile
AMR 0120	Alcedo atthis	Common kingfisher	1	Resident to short distance	Nestling
AMR 0011	Mergus merganser	Common merganser	6	Resident to short distance	Juvenile
AMR 0012	Mergus merganser	Common merganser		Resident to short distance	Juvenile
AMR 0013	Mergus merganser	Common merganser		Resident to short distance	Juvenile
AMR 0014	Mergus merganser	Common merganser		Resident to short distance	Juvenile
AMR 0015	Mergus merganser	Common merganser		Resident to short distance	Juvenile
AMR 0016	Mergus merganser	Common merganser		Resident to short distance	Juvenile
AMR 0030	Sturnus vulgaris	Common starling	3	Short distance	Nestling
AMR 0080	Sturnus vulgaris	Common starling		Short distance	Nestling
AMR 0281	Sturnus vulgaris	Common starling		Short distance	Adult
AMR 0063	Apus apus	Common swift	16	Long distance	Adult
AMR 0107	Apus apus	Common swift		Long distance	Nestling
AMR 0108	Apus apus	Common swift		Long distance	Adult
AMR 0149	Apus apus	Common swift		Long distance	Nestling
AMR 0153	Apus apus	Common swift		Long distance	Juvenile
AMR 0159	Apus apus	Common swift		Long distance	Nestling
AMR 0167	Apus apus	Common swift		Long distance	Juvenile
AMR 0170	Apus apus	Common swift		Long distance	Juvenile
AMR 0172	Apus apus	Common swift		Long distance	Juvenile
AMR 0173	Apus apus	Common swift		Long distance	Nestling
AMR 0174	Apus apus	Common swift		Long distance	Nestling
AMR 0182	Apus apus	Common swift		Long distance	Pullus
AMR 0195	Apus apus	Common swift		Long distance	Juvenile
AMR 0218	Apus apus	Common swift		Long distance	Nestling
AMR 0248	Apus apus	Common swift		Long distance	Juvenile
AMR 0262	Apus apus	Common swift		Long distance	Juvenile
AMR 0185	Columba palumbus	Common wood pigeon	5	Resident to short distance	Juvenile
AMR 0207	Columba palumbus	Common wood pigeon		Resident to short distance	Juvenile
AMR 0244	Columba palumbus	Common wood pigeon		Resident to short distance	Nestling
AMR 0265	Columba palumbus	Common wood pigeon		Resident to short distance	Adult
AMR 0283	Columba palumbus	Common wood pigeon		Resident to short distance	Juvenile
AMR 0089	Sylvia atricapilla	Eurasian blackcap	6	Short distance	Juvenile
AMR 0090	Sylvia atricapilla	Eurasian blackcap		Short distance	Juvenile
AMR 0093	Sylvia atricapilla	Eurasian blackcap		Short distance	Juvenile
AMR 0094	Sylvia atricapilla	Eurasian blackcap		Short distance	Juvenile
AMR 0140	Sylvia atricapilla	Eurasian blackcap		Short distance	Juvenile
AMR 0221	Sylvia atricapilla	Eurasian blackcap		Short distance	Nestling
AMR 0018	Cyanistes caeruleus	Eurasian blue tit	9	Resident to short distance	Nestling
AMR 0021	Cyanistes caeruleus	Eurasian blue tit		Resident to short distance	Nestling
AMR 0022	Cyanistes caeruleus	Eurasian blue tit		Resident to short distance	Nestling
AMR 0087	Cyanistes caeruleus	Eurasian blue tit		Resident to short distance	Nestling
AMR 0097	Cyanistes caeruleus	Eurasian blue tit		Resident to short distance	Nestling
AMR 0098	Cyanistes caeruleus	Eurasian blue tit		Resident to short distance	Juvenile
AMR 0099	Cyanistes caeruleus	Eurasian blue tit		Resident to short distance	Nestling
AMR 0100	Cyanistes caeruleus	Eurasian blue tit		Resident to short distance	Nestling
AMR 0101	Cyanistes caeruleus	Eurasian blue tit		Resident to short distance	Juvenile
AMR 0255	Streptopelia decaocto	Eurasian collared dove	4	Resident	Adult
AMR 0269	Streptopelia decaocto	Eurasian collared dove		Resident	Juvenile
AMR 0272	Streptopelia decaocto	Eurasian collared dove		Resident	Juvenile
AMR 0291	Streptopelia decaocto	Eurasian collared dove		Resident	Juvenile
AMR 0122	Fulica atra	Eurasian coot	3	Resident to short distance	Juvenile
AMR 0125	Fulica atra	Eurasian coot		Resident to short distance	Juvenile
AMR 0180	Fulica atra	Eurasian coot		Resident to short distance	Juvenile
AMR 0266	Bubo bubo	Eurasian eagle‐owl	1	Resident	Juvenile
AMR 0198	Falco subbuteo	Eurasian hobby	1	Long distance	Adult
AMR 0065	Garrulus glandarius	Eurasian jay	1	Resident to short distance	Adult
AMR 0003	Pica pica	Eurasian magpie	10	Resident	Nestling
AMR 0004	Pica pica	Eurasian magpie		Resident	Nestling
AMR 0068	Pica pica	Eurasian magpie		Resident	Nestling
AMR 0079	Pica pica	Eurasian magpie		Resident	Pullus
AMR 0083	Pica pica	Eurasian magpie		Resident	Juvenile
AMR 0129	Pica pica	Eurasian magpie		Resident	Juvenile
AMR 0152	Pica pica	Eurasian magpie		Resident	Adult
AMR 0201	Pica pica	Eurasian magpie		Resident	Juvenile
AMR 0206	Pica pica	Eurasian magpie		Resident	Nestling
AMR 0237	Pica pica	Eurasian magpie		Resident	Juvenile
AMR 0245	Acrocephalus scirpaceus	Eurasian reed warbler	1	Long distance	Juvenile
AMR 0275	Accipiter nisus	Eurasian sparrowhawk	1	Short distance	Juvenile
AMR 0008	Passer montanus	Eurasian tree sparrow	4	Resident to short distance	Nestling
AMR 0208	Passer montanus	Eurasian tree sparrow		Resident to short distance	Juvenile
AMR 0209	Passer montanus	Eurasian tree sparrow		Resident to short distance	Nestling
AMR 0210	Passer montanus	Eurasian tree sparrow		Resident to short distance	Nestling
AMR 0062	Carduelis carduelis	European goldfinch	8	Resident to short distance	Juvenile
AMR 0168	Carduelis carduelis	European goldfinch		Resident to short distance	Adult
AMR 0178	Carduelis carduelis	European goldfinch		Resident to short distance	Nestling
AMR 0217	Carduelis carduelis	European goldfinch		Resident to short distance	Juvenile
AMR 0219	Carduelis carduelis	European goldfinch		Resident to short distance	Juvenile
AMR 0243	Carduelis carduelis	European goldfinch		Resident to short distance	Juvenile
AMR 0250	Carduelis carduelis	European goldfinch		Resident to short distance	Adult
AMR 0276	Carduelis carduelis	European goldfinch		Resident to short distance	Juvenile
AMR 0075	Picus viridis	European green woodpecker	4	Resident	Juvenile
AMR 0189	Picus viridis	European green woodpecker		Resident	Juvenile
AMR 0252	Picus viridis	European green woodpecker		Resident	Adult
AMR 0287	Picus viridis	European green woodpecker		Resident	Juvenile
AMR 0228	Chloris chloris	European greenfinch	2	Resident to short distance	Juvenile
AMR 0253	Chloris chloris	European greenfinch		Resident to short distance	Juvenile
AMR 0261	Ficedula hypoleuca	European pied flycatcher	1	Long distance	Juvenile
AMR 0082	Erithacus rubecula	European robin	2	Short distance	Juvenile
AMR 0296	Erithacus rubecula	European robin		Short distance	Adult
AMR 0187	Serinus serinus	European serin	1	Short distance	Nestling
AMR 0112	Columba livia domestica	Feral pigeon	11	Resident	Nestling
AMR 0142	Columba livia domestica	Feral pigeon		Resident	Nestling
AMR 0151	Columba livia domestica	Feral pigeon		Resident	Juvenile
AMR 0165	Columba livia domestica	Feral pigeon		Resident	Nestling
AMR 0191	Columba livia domestica	Feral pigeon		Resident	Juvenile
AMR 0199	Columba livia domestica	Feral pigeon		Resident	Nestling
AMR 0232	Columba livia domestica	Feral pigeon		Resident	Juvenile
AMR 0268	Columba livia domestica	Feral pigeon		Resident	Juvenile
AMR 0273	Columba livia domestica	Feral pigeon		Resident	Adult
AMR 0286	Columba livia domestica	Feral pigeon		Resident	Adult
AMR 0298	Columba livia domestica	Feral pigeon		Resident	Nestling
AMR 0095	Turdus pilaris	Fieldfare	3	Short distance	Juvenile
AMR 0138	Turdus pilaris	Fieldfare		Short distance	Juvenile
AMR 0179	Turdus pilaris	Fieldfare		Short distance	Nestling
AMR 0282	Sylvia borin	Garden warbler	1	Long distance	Adult
AMR 0088	Dendrocopos major	Great spotted woodpecker	3	Resident	Juvenile
AMR 0127	Dendrocopos major	Great spotted woodpecker		Resident	Juvenile
AMR 0156	Dendrocopos major	Great spotted woodpecker		Resident	Pullus
AMR 0019	Parus major	Great tit	7	Resident to short distance	Nestling
AMR 0020	Parus major	Great tit		Resident to short distance	Nestling
AMR 0041	Parus major	Great tit		Resident to short distance	Nestling
AMR 0042	Parus major	Great tit		Resident to short distance	Nestling
AMR 0139	Parus major	Great tit		Resident to short distance	Nestling
AMR 0166	Parus major	Great tit		Resident to short distance	Adult
AMR 0225	Parus major	Great tit		Resident to short distance	Juvenile
AMR 0235	Ardea cinerea	Grey heron	2	Short distance	Adult
AMR 0260	Ardea cinerea	Grey heron		Short distance	Juvenile
AMR 0230	Coccothraustes coccothraustes	Hawfinch	1	Resident to short distance	Nestling
AMR 0002	Passer domesticus	House sparrow	40	Resident	Nestling
AMR 0025	Passer domesticus	House sparrow		Resident	Nestling
AMR 0029	Passer domesticus	House sparrow		Resident	Nestling
AMR 0053	Passer domesticus	House sparrow		Resident	Nestling
AMR 0054	Passer domesticus	House sparrow		Resident	Nestling
AMR 0055	Passer domesticus	House sparrow		Resident	Nestling
AMR 0056	Passer domesticus	House sparrow		Resident	Nestling
AMR 0057	Passer domesticus	House sparrow		Resident	Nestling
AMR 0067	Passer domesticus	House sparrow		Resident	Nestling
AMR 0073	Passer domesticus	House sparrow		Resident	Nestling
AMR 0074	Passer domesticus	House sparrow		Resident	Nestling
AMR 0086	Passer domesticus	House sparrow		Resident	Nestling
AMR 0096	Passer domesticus	House sparrow		Resident	Adult
AMR 0110	Passer domesticus	House sparrow		Resident	Nestling
AMR 0111	Passer domesticus	House sparrow		Resident	Nestling
AMR 0113	Passer domesticus	House sparrow		Resident	Nestling
AMR 0116	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0121	Passer domesticus	House sparrow		Resident	Adult
AMR 0126	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0128	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0131	Passer domesticus	House sparrow		Resident	Nestling
AMR 0134	Passer domesticus	House sparrow		Resident	Nestling
AMR 0141	Passer domesticus	House sparrow		Resident	Nestling
AMR 0158	Passer domesticus	House sparrow		Resident	Adult
AMR 0186	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0212	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0214	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0215	Passer domesticus	House sparrow		Resident	Nestling
AMR 0224	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0226	Passer domesticus	House sparrow		Resident	Nestling
AMR 0229	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0236	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0246	Passer domesticus	House sparrow		Resident	Adult
AMR 0251	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0256	Passer domesticus	House sparrow		Resident	Adult
AMR 0259	Passer domesticus	House sparrow		Resident	Adult
AMR 0270	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0271	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0278	Passer domesticus	House sparrow		Resident	Adult
AMR 0293	Passer domesticus	House sparrow		Resident	Juvenile
AMR 0037	Asio otus	Long‐eared owl	3	Resident to short distance	Adult
AMR 0132	Asio otus	Long‐eared owl		Resident to short distance	Juvenile
AMR 0136	Asio otus	Long‐eared owl		Resident to short distance	Nestling
AMR 0032	Anas platyrhynchos	Mallard	21	Resident to short distance	Pullus
AMR 0034	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0035	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0036	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0038	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0039	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0040	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0043	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0044	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0045	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0046	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0047	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0048	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0049	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0050	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0051	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0052	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0078	Anas platyrhynchos	Mallard		Resident to short distance	Juvenile
AMR 0155	Anas platyrhynchos	Mallard		Resident to short distance	Adult
AMR 0181	Anas platyrhynchos	Mallard		Resident to short distance	Pullus
AMR 0193	Anas platyrhynchos	Mallard		Resident to short distance	Juvenile
AMR 0001	Poecile palustris	Marsh tit	1	Resident	Juvenile
AMR 0234	Turdus viscivorus	Mistle thrush	1	Short distance	Juvenile
AMR 0070	Cygnus olor	Mute swan	1	Resident	Nestling
AMR 0200	Milvus milvus	Red kite	2	Resident to short distance	Juvenile
AMR 0203	Milvus milvus	Red kite		Resident to short distance	Juvenile
AMR 0104	Netta rufina	Red‐crested pochard	1	Resident to short distance	Juvenile
AMR 0233	Turdus philomelos	Song thrush	3	Short distance	Adult
AMR 0267	Turdus philomelos	Song thrush		Short distance	Juvenile
AMR 0295	Turdus philomelos	Song thrush		Short distance	Juvenile
AMR 0027	Muscicapa striata	Spotted flycatcher	2	Long distance	Adult
AMR 0183	Muscicapa striata	Spotted flycatcher		Long distance	Nestling
AMR 0249	Strix aluco	Tawny owl	1	Resident	Nestling
AMR 0148	Ciconia ciconia	White stork	2	Short‐ to long distance	Juvenile
AMR 0184	Ciconia ciconia	White stork		Short‐ to long distance	Nestling
AMR 0058	Motacilla alba	White wagtail	3	Short distance	Juvenile
AMR 0177	Motacilla alba	White wagtail		Short distance	Juvenile
AMR 0216	Motacilla alba	White wagtail		Short distance	Nestling
AMR 0292	Emberiza citrinella	Yellowhammer	1	Resident to short distance	Adult
AMR 0164	Larus michahellis	Yellow‐legged gull	4	Resident to short distance	Nestling
AMR 0188	Larus michahellis	Yellow‐legged gull		Resident to short distance	Juvenile
AMR 0202	Larus michahellis	Yellow‐legged gull		Resident to short distance	Juvenile
AMR 0280	Larus michahellis	Yellow‐legged gull		Resident to short distance	Adult

AMR: antimicrobial resistant.