Introduction
Rapid urbanisation leads to the decline of populations and the narrowing of living areas for many animal species, including birds (Devictor et al. Reference Devictor, Julliard, Denis, Lee and Jiguet2007). At the same time, urbanisation has had a positive impact on several species that have adapted to the new environment and increased their populations in cities (Chamberlain et al. Reference Chamberlain, Cannon, Toms, Leech, Hatchwell and Gaston2009). Such species are often referred to as urban exploiters, and they have several benefits from living in the city. These benefits include, but are not limited to, more accessible food sources, lower predation pressure, longer daylight hours increased due to illumination, and unnecessity of migrations (Bonnet-Lebrun et al. Reference Bonnet-Lebrun, Manica and Rodrigues2020; Chamberlain et al. Reference Chamberlain, Cannon, Toms, Leech, Hatchwell and Gaston2009; Kark et al. Reference Kark, Iwaniuk, Schalimtzek and Banker2007; Ruß et al. Reference Ruß, Rüger and Klenke2015).
Changes in the biology and ecology of urban species, together with generally reduced and homogeneous biodiversity, also lead to the reorganisation of interspecies interactions, often shortening food chains. It is known that urbanisation has changed the food spectrum of many species. For example, studies by Chamberlain et al. (Reference Chamberlain, Cannon, Toms, Leech, Hatchwell and Gaston2009), Cowie and Hinsley (Reference Cowie and Hinsley1988), and Kark et al. (Reference Kark, Iwaniuk, Schalimtzek and Banker2007) have demonstrated this particularly in birds that began feeding on anthropogenic sources such as landfills or supplemental feeding by people. Meanwhile, high population densities can elevate contact rates within and among synanthropic animals, which favour the transmission of parasites spread by direct contact or alimentary routes (such as ectoparasites, monoxenous helminth species), causing disease outbreaks (Bradley and Altizer Reference Bradley and Altizer2007; Wright and Gompper Reference Wright and Gompper2005; Yamaç et al. Reference Yamaç, Dik and Cavus2023). On the other hand, the availability of anthropogenic food and the low diversity of animal food sources can help birds avoid parasitic infections, which can be one of the benefits for urban exploiters (Kark et al. Reference Kark, Iwaniuk, Schalimtzek and Banker2007). Therefore, urbanisation has a significant impact on parasites, their intermediate and definitive hosts in cities.
Studies on the impact of urbanisation on helminth infections in birds are scarce, with most focusing on ectoparasites, blood parasites, protozoans, bacteria, or viruses (Delgado-V. and French Reference Delgado-V and French2012; Peñuela et al. Reference Peñuela, Ferraguti, Martínez-de la Puente, Soriguer and Figuerola2021; Yamaç et al. Reference Yamaç, Dik and Cavus2023). Two studies (Rząd et al. Reference Rząd, Sitko, Sałamatin and Wysocki2014; Sitko and Zaleśny Reference Sitko and Zaleśny2014) documented degraded parasite communities in urban blackbirds (Turdus merula L.) compared with forest populations. The other study demonstrated the similarity of helminth infection of House Sparrows Passer domesticus (L.), from rural and urban landscapes (Calegaro-Marques and Amato Reference Calegaro-Marques and Amato2010). However, this aspect is still insufficiently explored overall.
The Hooded Crow Corvus cornix L. is widespread bird in Europe, Asia, and Northeast Africa (Egypt). Crows are omnivorous, consuming plant- and animal-based food. Their prey includes various invertebrates (insects, worms, snails), fish, amphibians, reptiles, small mammals, and even other birds – crows often hunt smaller ones, destroying their nests and consuming eggs and chicks. The Hooded Crow is also a notable scavenger (Berrow Reference Berrow1991; Berrow et al. Reference Berrow, Kelly and Myers1991; Horgan and Berrow Reference Horgan and Berrow2004; Houston Reference Houston1977; Krivosheev Reference Krivosheev2004; Vogrin and Vogrin Reference Vogrin and Vogrin1998; Zduniak et al. Reference Zduniak, Kosicki and Gołdyn2008). Being an adaptable species with a wide food range, the Hooded Сrow has expanded from natural habitats into urban areas. In the second half of the 20th century, the species rapidly expanded its range into European cities in Hungary (Kover et al. Reference Kover, Juhász and Gyüre2011), Finland (Vuorisalo et al. Reference Vuorisalo, Andersson, Hugg, Lahtinen, Laaksonen and Lehikoinen2003), Norway (Munkejord et al. Reference Munkejord, Hauge, Folkedal, Kvinnesland, Munkejord, Hauge, Folkedal and Kvinnesland1985), and Ukraine (Koshelev et al. Reference Koshelev, Koshelev, Kopylova and Borisov2020). The population density of these birds in urban landscapes has increased rapidly in recent decades. For example, from 2006 to 2012 in Debrecen (Hungary), the total density of crows’ nests increased from 1.2 to 3 pairs/km2, and on some territories, it grew from 2 to almost 8 pairs/km2 (Kover et al. Reference Kover, Gyüre, Balogh, Huettmann, Lengyel and Juhász2015).
The wide distribution range of the Hooded Crow and its omnivorousness cause a wide variety of helminths that can be found in it. Previous studies recorded 93 species of helminths of this bird, including 42 species of trematodes, 15 cestodes, 28 nematodes and eight acanthocephalans (Aliev et al. Reference Aliev, Mutalimova and Alieva2012; Andreyko and Shumilo Reference Andreyko and Shumilo1970; Ayupov et al. Reference Ayupov, Valiullin, Khaziev, Bayanov, Kazadaev and Antonov1974; Birová-Volosinovičová Reference Birová-Volosinovičová1968; Budkin Reference Budkin1977, Reference Budkin1979; Chernobai Reference Chernobai1969; Dubinin and Dubinina Reference Dubinin and Dubinina1940; Iskova et al. Reference Iskova, Sharpilo, Sharpilo and Tkach1995; Ivanizky Reference Ivanizky1940; Kolmykov and Strelkov Reference Kolmykov and Strelkov2018; Lisitsyna Reference Lisitsyna2019; Lugovoi and Kurochkin Reference Lugovoi and Kurochkin1962; Mikhelson Reference Mikhelson, Mikhelson and IaA1968; Odening Reference Odening1978; Paspalev et al. Reference Paspalev, Zhelyazkova-Paspaleva and Tsacheva1969; Paspalev and Paspaleva Reference Paspalev and Paspaleva1965; Rutkowska Reference Rutkowska1973; Salamatin Reference Salamatin1999, Reference Salamatin2000; Schmidt Reference Schmidt1986; Shigin Reference Shigin1983; Sitko and Heneberg Reference Sitko and Heneberg2024; Sitko and Okulewicz Reference Sitko and Okulewicz2010; Stoimenov Reference Stoimenov1963; Sultanov Reference Sultanov1963; Zekhnov Reference Zekhnov1954; Zverzhanovsky Reference Zverzhanovsky1995).
The successful adaptation of the Hooded Crow is confirmed by the fact that urban populations have a higher number and density compared to those from natural habitats. Previous studies on crows’ synanthropisation have mainly focused on various aspects of their biology and ecology, including adaptation to humans, changes in breeding biology, and increasing population density (Preininger et al. Reference Preininger, Schoas, Kramer and Boeckle2019; Vuorisalo et al. Reference Vuorisalo, Andersson, Hugg, Lahtinen, Laaksonen and Lehikoinen2003). However, the response of the parasitofauna to the urbanised environment has not been previously studied.
The mostly sedentary lifestyle of the Hooded Crow (Holyoak Reference Holyoak1971) is a key ecological trait that makes it an effective model for studying local environmental impacts on parasite communities. Unlike those of migratory birds, Hooded Crows’ helminth communities are expected to be influenced mainly by local ecological factors. Comparisons between natural and urbanised ecosystems allow the assessment of the effects of anthropogenic change on helminth communities of the species. In this study, we tested the hypothesis that urban environments lead to reduce parasite species richness and abundance in helminth communities of the Hooded Crow.
Materials and methods
Study area and localities
The study covered samples of Hooded Crows from three geographically close zones, but different in anthropogenic pressure. The first zone includes several spots within the city of Kyiv and is the most urbanised zone. The city of Kyiv is situated on both sides of the Dnipro River at the confluence of the Forest Steppe and Polissya ecozones. The second zone is located south of Kyiv and covers the Forest Steppe ecozone along the middle part of the Dnipro River. This zone is less urbanised than the city of Kyiv, though it includes several smaller towns. We refer to this zone as the Middle Dnipro River. The third one is the most natural and is located north of the city of Kyiv, being a part of Polissya.
Sampling of hosts
The three samples of helminths consist of archived material collected from 93 Hooded Crows from different localities between 1952 and 2024. The largest sample was collected from multiple locations in Kyiv city and included 41 birds. The sample from the Middle Dnipro sample included 24 Hooded Сrows from six settlements in Cherkasy Oblast (Kaniv, Zhovnyne, Buchak, Trakhtemyriv, Ukrainka) and Kyiv Oblast (Pereiaslav). Twenty-eight crows originated from 14 localities in the Polissya region: Chernihiv Oblast (Novi Borovychi, Khandobokivka, Budyshche, Stari Yarylovychi, Volodkova Divytsia, Kunashivka, Baklanove, and Mala Koshelivka); Kyiv Oblast (Dymer and Vyshhorod), Rivne Oblast (Bystrychi and Horodets’), Zhytomyr Oblast (Kopyshche), and Volyn Oblast (Moshne Lake) (Fig. 1, Table 1).
Map showing the sampling localities in the study area: I (red colour) – Kyiv city; II (yellow colour) – Middle Dnipro River; III (blue colour) – Polissia.
Localities: 1– Kyiv, 2 – Ukrainka, 3 – Pereiaslav, 4 – Trakhtemyriv, 5 – Buchak, 6 – Kaniv, 7 – Zhovnyne, 8 – Moshne Lake, 9 – Horodets’, 10 – Bystrychi, 11 – Kopyshche, 12 – Vyshhorod, 13 – Dymer, 14 – Budyshche, 15 – Stari Yarylovychi, 16 – Novi Borovychi, 17 – Khandobokivka, 18 – Volodkivska Divytsia, 19 – Mala Koshelivka, 20 – Baklanove, 21 – Kunashivka.
Studied localities and samples of hosts
Most of the material was obtained from the helminthological collection of the I. I. Schmalhausen Institute of Zoology NAS of Ukraine (IZSHK). This material included helminths from birds collected from 1952 to 2009. Additionally, 21 crows collected dead in Kyiv across different seasons were examined in 2022–2024. To collect these birds, we announced collection efforts via social media, and people who find dead crows either deliver them or report their locations.
In total, we studied material from 46 males, 27 females, and 20 individuals with unidentified sex. Of these, 43 birds were adults, 40 were juveniles (≤1 year old), one was a nestling, and 10 individuals were of an unidentified age. All information on the Hooded Crows and their parasites collected over 77 years at the I. I. Schmalhausen Institute of Zoology (including that used for the present study) is available as datasets on GBIF (Greben and Dupak Reference Greben and Dupak2024).
Collection and identification of helminths
The dead crows were collected from different localities and then transported to the laboratory for further storage (in the freezer) or immediate dissection. All internal organs and body cavities were examined for parasites. Helminths were gently removed, rinsed in saline, and fixed with 70% alcohol. Specimens were examined under the light microscope AmScope T690B and identified based on their morphology. Prior to the examination, nematodes were washed in distilled water for 10–30 minutes and cleared in lactophenol for 10-30 minutes, depending on the worm size. Trematodes were stained with iron acetocarmine, dehydrated in an ascending alcohol series, cleared in clove oil, and mounted in Canada balsam (according to Lutz et al. Reference Lutz, Tkach, Weckstein and Webster2017). All cestode specimens were collected without proglottids and represented only by their scolices. Cestodes were cleared and mounted in Berlese’s medium. Most of the collection material had not been previously identified; we therefore identified it based on morphology, using the same appropriate clearing and staining methods as for freshly collected specimens.
Statistical methods
Descriptive statistics and nonparametric analysis
For each helminth species in each separate sample, the infection prevalence (P), intensity (I), and mean abundance (MA) were calculated following Bush et al. (Reference Bush, Lafferty, Lotz and Shostak1997). Additionally, the relative abundance (RA) was calculated as the percentage of a species’ specimens in the whole sample of helminths. The dispersion index (DI) was calculated as the variance-to-mean ratio, following the recommendations of (Rózsa et al. Reference Rózsa, Reiczigel and Majoros2000). Confidence intervals for infection prevalence (using the Sterne method) and mean abundance (via the bootstrap method) were calculated using the Quantitative Parasitology 3.0 software (Rózsa et al. Reference Rózsa, Reiczigel and Majoros2000).
The SIMPER (Similarity Percentages) and nMDS (non-metric multidimensional scaling) were performed in PRIMER 6 software (Clarke and Gorley Reference Clarke and Gorley2006) to assess similarity among infracommunities and visualise patterns. The same program was used to calculate the diversity indices and to estimate species richness (based on Chao1, jackknife, and bootstrap methods) for helminth component communities.
Regression analysis
The modelling was conducted in the R (v. 4.4.2) programming environment (R Core Team, 2024) using the brms (v. 2.22.0) package (Bürkner Reference Bürkner2017) to fit Bayesian models. The tidyverse (v. 2.0.0) package collection (Wickham et al., Reference Wickham, Averick, Bryan, Chang, McGowan, François, Grolemund, Hayes, Henry, Hester, Kuhn, Pedersen, Miller, Bache, Müller, Ooms, Robinson, Seidel, Spinu, Takahashi, Vaughan, Wilke, Woo and Yutani2019 ) was used for data manipulation and visualisation. Because the temporal overlap in sampling between Kyiv and Polissya was somewhat greater than with the Middle Dnipro region (Supplement 1, p. 1), we excluded the Middle Dnipro region from further analysis. However, this exclusion did not fully resolve the issue, as our dataset contains no data for the Polissya region in the 21st century. Drawing on evidence for declines in biodiversity metrics from the 20th to the 21st century in both free-living animals (Pilotto et al. Reference Pilotto, Kühn, Adrian, Alber, Alignier, Andrews, Bäck, Barbaro, Beaumont, Beenaerts, Benham, Boukal, Bretagnolle, Camatti, Canullo, Cardoso, Ens, Everaert, Evtimova and Haase2020; Seibold et al. Reference Seibold, Gossner, Simons, Blüthgen, Müller, Ambarlı, Ammer, Bauhus, Fischer, Habel, Linsenmair, Nauss, Penone, Prati, Schall, Schulze, Vogt, Wöllauer and Weisser2019) and helminths (Behnke et al. Reference Behnke, Rogan, Craig, Jackson and Hide2021; Sitko and Heneberg Reference Sitko and Heneberg2024), we inferred a general negative temporal trend and incorporated this trend via an informative prior. Thus, the objective of the analysis was to assess the effect of region, used here as a proxy for the degree of urbanisation, on the species richness and infection abundance of helminth infracommunities of Hooded Crows, while accounting for the inferred temporal trend.
We fitted two generalised linear mixed models (GLMMs). Species richness was modelled using a Poisson distribution. To account for observed overdispersion typical of helminth counts, abundance was modelled using a negative binomial distribution. Both models included region as a fixed effect (Kyiv as reference), a centred continuous decade variable (Decade_c; centred at 1950) as a fixed effect to represent the linear temporal trend, and a random intercept for decade to capture additional between-decade variation. Each model was run with four chains of 4,000 iterations each (1,000 warmup and 3,000 post-warmup). We considered fixed effects to have meaningful support when the 95% credible interval (CrI) of their estimates (β) did not include zero.
To incorporate the established ecological knowledge, a moderately informative prior of a normal distribution with a mean of -0.05 and a standard deviation of 0.1 was placed on the Decade_c coefficient. All other parameters used the brms defaults. Post-fitting processing of the models included examining the potential scale reduction factor (
$ \hat{R} $
) and effective sample sizes (ESS), as well as performing posterior predictive checks and leave-one-out cross-validation (LOO-CV) diagnostics, all of which were accomplished using functions from the brms package. The sensitivity of the posterior to perturbations of the prior and likelihood was evaluated using the priorsense (v. 1.1.0) package (Kallioinen et al., Reference Kallioinen, Paananen, P-C and Vehtari2023). The dataset used for this analysis is provided in Supplement 2; model specifications are in Supplement 1.
Results
Helminth species and population parameters
In the examined material, we found 32 helminth species (Table 2). Two specimens of juvenile nematodes of the Acuariidae and three specimens of the Capillariidae, all from Kyiv city, were not identified due to a lack of diagnostic morphological characters. Among identified species were 14 trematodes, six species of cestodes, 11 species of nematodes, and one acanthocephalan species.
Parameters of helminth infection of the Hooded Crows at three studied localities. Infection prevalence is shown with 95% confidence intervals in parentheses; for infection intensity, mean is followed by median in brackets and range in parentheses; mean abundance is followed by 95% confidence intervals in parentheses and the total number of specimens in brackets
Sixteen helminth species were recorded in the crows from Kyiv. Only four trematode species were found there, namely Plagiorchis elegans, Prosthogonimus cuneatus, Strigea sphaerula, and Tamerlania zarudnyi (Table 2). Cestodes were represented by four species, and nematodes by eight species, considering unidentified capillariid and acuariid nematodes as separate species. Seventeen species of helminths were recorded in the Dnipro sample, including nine species of trematodes, four species of cestodes, the acanthocephalan Plagiorhynchus cylindraceus, and only three species of nematodes: Acuaria anturis, Eucoleus contortus, and Microtetrameres inermis. In the sample from Polissya, 20 species were identified, including 12 species of trematodes, five species of nematodes, and three species of cestodes: Dilepis undula, Passerilepis crenata, and Spiniglans constricta.
Despite the biggest host samples in Kyiv (41 birds vs 24 and 28 from other localities), the number of specimens here was the lowest, comprising 255 specimens. Of these, 115 specimens belonged to Trematoda, 86 to Nematoda, and 54 to Cestoda. In crows from the Middle Dnipro River (24 birds), 294 helminth specimens were collected. In this sample, representatives of Cestoda were the most common, with 170 specimens, followed by 118 specimens belonging to Trematoda, five specimens to Nematoda, and a single specimen of Acanthocephala. The largest number of helminths was collected from Polissya – 406 specimens. Here, 320 specimens belonged to Trematoda, 71 to Cestoda, and 15 to Nematoda (Table 2).
Considering the unidentified acuariid and capillariid nematodes as separate taxa, the similarity between the Kyiv and Polissya samples was the lowest, with a Sørensen similarity index (SI) of 0.33 (6 common species). Other pairwise similarities were somewhat higher, with SI = 0.54 between the Kyiv and Middle Dnipro River samples (9 common species) and SI = 0.49 between the Dnipro and Polissya samples (9 common species).
Five helminth species were present in all three samples: the trematodes P. elegans, P. cuneatus, and S. sphaerula; the cestode P. crenata; and the nematode A. anturis (Table 2). Acuaria anturis, P. crenata, and S. sphaerula had low but similar infection prevalence in all three localities, while P. elegans and P. cuneatus had the highest infection prevalence in Polissya.
Helminth infracommunities
In the combined sample of 93 crows, 65 individuals (69.9%) were found infected with at least one helminth species. The overall helminth prevalence was the lowest in the sample from Kyiv (61.0%) and the highest in the sample from Polissya (82.1%). In the Middle Dnipro River sample, the prevalence of helminth infection was 70.8%. In 25 infected crows from Kyiv, the species richness in the infracommunities ranged from 1 to 4 (mean 1.6; median 1), and the helminth abundance ranged from 1 to 61 (mean 10.2; median 2); the dispersion index was 24.7. In the Middle Dnipro River sample (17 infected crows), the species richness in helminth infracommunities also ranged from 1 to 4 (mean 1.9; median 2), while the abundance ranged from 1 to 104 (mean 17.3; median 8); the dispersion index was 36.3. In the sample from Polissya (23 infected crows), the species richness in the infracommunities ranged from 1 to 7 (mean 2.5; median 2); helminth abundance ranged from 1 to 63 (mean 17.6; median 11); the dispersion index was 18.7. In all three samples, a large proportion of infected crows harboured just one helminth species: 60.0% in the sample from Kyiv, 41.2% in the Middle Dnipro River sample, and 34.8% in the sample from Polissya.
According to the SIMPER analysis, the average similarity among the helminth infracommunities in each sample was relatively low, at 4.5% in the Kyiv sample, 11.5% in the Dnipro sample, and 9.3% in the Polissya sample. Low similarity among the infracommunities based on the Bray-Curtis similarity index is also evident from the nMDS visualisation (Fig. 2). The plot also demonstrates no separate groups of infracommunities related to the locality. The average dissimilarity between the samples was indicated by SIMPER analysis. The dissimilarity between the sample from Kyiv and the Middle Dnipro River sample was 95.6%, with P. crenata and P. elegans making the largest contribution to the dissimilarity (30.6% and 17.4%, respectively). The average dissimilarity between the Kyiv and Polissya groups was 95.7%; P. elegans, P. crenata, and P. cuneatus made the largest contribution to the dissimilarity (19.1%, 15.6%, and 13.6%, respectively). The dissimilarity between the Middle Dnipro River and Polissya groups was the lowest, at 91.8%; P. crenata, P. elegans, and P. cuneatus made the largest contribution to the dissimilarity (29.9%, 21.2%, and 12.0%, respectively).
nMDS ordination of helminth infracommunities of Hooded Crows from the three studied samples, based on Bray–Curtis similarity.
Helminth component communities
Species richness in component communities of helminths from the three localities corresponded to the observed number of species in the samples (Table 3). The lowest species richness was estimated in the helminth community from Kyiv (17–22 species), while the highest was in the helminth community from Polissya (24–30 species). These results were supported by Margalef’s index of species richness, which was the highest in the helminth community from Polissya (3.17) and the lowest in the helminth community from Kyiv (2.71); in the Middle Dnipro River sample, the index was calculated as 2.81.
Species richness and diversity indices in helminth component communities of the Hooded Crows from three localities
The diversity indices, however, followed a different pattern in the three component communities of helminths (Table 3). The highest values of Pielou’s evenness index and Shannon diversity index, as well as the lowest values of Simpson diversity (dominance) index and Berger-Parker dominance index, were observed in the helminth community from Kyiv. According to the diversity indices, the evenness in the helminth community from the Middle Dnipro River locality was the lowest, while that in the helminth community from Polissya was intermediate (Table 3).
In the sample from Kyiv, seven species had a relative abundance (RA) higher than 5%: P. elegans (RA = 24.7%), Baruscapillaria resectum (RA = 12.9%), Eucoleus frugilegi (RA = 12.5%), T. zarudnyi (RA = 10.2%), P. crenata (RA = 9.4%), S. sphaerula (RA = 9.0%), and Passerilepis stylosa (RA = 7.1%) (Fig. 3). On the other hand, three of these species, namely P. stylosa, S. sphaerula, and T. zarudnyi were classified as statistically uncertain based on confidence intervals of mean abundance (see Table 2). In the Middle Dnipro River sample, P. crenata was dominant (RA = 56.5%) and only two more species had a relative abundance higher than 5%, namely P. elegans (RA = 23.1%) and Echinostoma revolutum (RA = 5.8%). In the sample from Polissya, five species had a relative abundance higher than 5%: P. elegans (RA = 27.5%), P. cuneatus (RA = 25.5%), P. crenata (RA = 13.1%), P. ovatus (RA = 10.6%), and S. sphaerula (RA = 7.7%). The latter species, however, was statistically uncertain based on confidence intervals of mean abundance (Table 2).
Relative abundance (RA, %) of particular helminth taxonomic categories in Hooded Crows from the three samples.
Regression analysis
The species richness model did not reveal evidence of a difference between the urbanised (Kyiv) and natural (Polissya) regions, as the credible interval overlapped zero (β = 0.34, 95% CrI [–0.28, 0.95]). Similarly, the abundance model showed no meaningful difference between the regions, as the estimated effect was highly uncertain (β = –0.73, 95% CrI [–3.42, 1.3]). Both models converged successfully, and posterior predictive checks indicated an adequate fit to the observed data. The LOO-CV indicated no highly influential observations.
Discussion
Descriptive patterns
To date, no comprehensive studies of the helminth fauna of the Hooded Crow have been conducted in Ukraine. From the published faunistic studies and short communications, we know about 24 species of helminths recorded from that area. These included 13 species of trematodes, five species of cestodes, three species of nematodes, and three species of acanthocephalans (Gąsowska Reference Gąsowska1932; Iskova Reference Iskova1971, Reference Iskova1975, Reference Iskova1979; Iskova et al. Reference Iskova, Sharpilo, Sharpilo and Tkach1995; Ivanizky Reference Ivanizky1940; Lisitsyna Reference Lisitsyna2019; Salamatin Reference Salamatin1999, Reference Salamatin2000; Sergienko Reference Sergienko1963; Shevchenko Reference Shevchenko1965, Reference Shevchenko1965; Smogorzhevskaya et al. Reference Smogorzhevskaya, Iskova, Kornyushin and Shalimova1978). In the present study, we found two nematode species, namely E. delicata and H. truncatai, that have never been reported from the Hooded Crow, and also 13 helminth species that have not been previously reported in this host from Ukraine. These are three species of Trematoda (Tamerlania zarudnyi, Plagiorchis maculosus, and Lyperosomum longicauda), nine nematodes (Porrocaecum ensicaudatum, P. semiteres, Eufilariella delicata, Hadjelia truncata, Diplotriaena tricuspis, Eucoleus contortus, E. frugilegi, Microtetrameres inermis, Baruscapillaria resectum), and one cestode (Passerilepis passeris). Therefore, the present study expands the number of helminth species known from the Hooded Crow in Ukraine to 38, and increases the total number of known species worldwide to 95.
Despite the biggest host sample collected in Kyiv, the smallest number of helminth specimens was recorded in this zone. The diversity of helminths was also the smallest in Kyiv, compared to the less urbanised Middle Dnipro River and Polissya. On the other hand, the differences appeared to be not very large.
The most pronounced pattern in our data was the contrast in trematode diversity between the urban environment of Kyiv (only four species, with a markedly reduced presence of the common trematode P. elegans) and the more natural region of Polissya (14 species). We hypothesize that this difference results from urban-driven ecosystem degradation and loss of intermediate hosts in Kyiv (e.g., snails), whereas the more natural conditions of Polissya (humid climate and wetlands) support higher host diversity and thus greater trematode richness. This may support the hypothesis that higher host diversity promotes a greater number of parasite transmission pathways (Keesing et al. Reference Keesing, Belden, Daszak, Dobson, Harvell, Holt, Hudson, Jolles, Jones, Mitchell, Myers, Bogich and Ostfeld2010), whereas urbanisation limits such pathways, leading to reduced parasite diversity. It is also possible that differences in crow diet contribute to this pattern: in urban areas, crows and other corvids may rely more on anthropogenic food sources (e.g., refuse, food provided by humans) rather than foraging for invertebrates, which could reduce their exposure to trematode larvae and lower infection levels (García-Arroyo et al. Reference García-Arroyo, Gómez-Martínez and MacGregor-Fors2023; Kim et al. Reference Kim, Srygley, Lee, Lee and Choe2012).
However, temporal differences in sampling should also be considered when interpreting these patterns. The Kyiv dataset spans both historical and recent material, while other localities are represented primarily by older collections. This temporal asymmetry may contribute to the observed differences, as corvid trematode communities have experienced widespread simplification in recent decades due to anthropogenic factors including altered host diets, chemical contamination, and intensive agricultural practices (Sitko and Heneberg Reference Sitko and Heneberg2024).
In contrast to the observed trematode diversity, the number of cestode species remained similar across all three localities: four in both Kyiv and the Middle Dnipro River, and three in Polissya. More surprisingly, we observed the highest nematode infection in crows from Kyiv (see Table 2). Six nematode taxa appeared to be unique for Kyiv: P. semiteres, D. tricuspis, E. frugilegi, B. resectum, and unidentified capillariid and acuariid nematodes. Interestingly, three of these four species (D. tricuspis, E. frugilegi, B. resectum) have been recently recorded in wintering rooks (Corvus frugilegus L.) from Kyiv (Greben et al. Reference Greben, Dupak, Lisitsyna and Kuzmin2023). Moreover, E. frugilegi and B. resectum comprised 63.9% of all nematodes of Corvus cornix from Kyiv.
It should be noted that E. frugilegi is known as a specific parasite of rooks and has been previously recorded only once in Hooded Crows from Slovakia (Birová-Volosinovičová Reference Birová-Volosinovičová1968). On the territory of Ukraine, rooks are nesting, migrating, and wintering species, and they usually appear in big numbers in Ukrainian cities in October (Poluda and Tsukanova Reference Poluda and Tsukanova2012). The community of wintering rooks in Kyiv is rather big, counting 90 thousand birds in 2020–2022 (Greben et al. Reference Greben, Dupak, Lisitsyna and Kuzmin2023). Since rooks and crows often interact in cities, sharing feeding and roosting sites, this provides an opportunity for parasite exchange between the two species. Taking into account that B. resectum is monoxenous (Okulewicz and Frońska Reference Okulewicz and Frońska1998) and E. frugilegi uses earthworms as intermediate hosts (Rietschel and Zoologisches Reference Rietschel and Zoologisches1973), they can successfully circulate even in highly urbanised ecosystems. The abundance of earthworms, even in big cities (Rysavy Reference Rysavy1964), could also explain the presence of the cestode D. undula that uses them as intermediate hosts as well.
The trematode P. elegans and the cestode P. crenata demonstrated high prevalence in all three communities, remaining common even in Kyiv where their prevalence was the lowest. These two helminth species are known as generalists, parasitising a wide range of hosts. Plagiorchis elegans was found in at least 51 species of birds as definitive hosts and in more than 30 species of dragonflies as intermediate hosts. (Genov and Samnaliev Reference Genov, Samnaliev and Vasilvev1984; Iskova et al. Reference Iskova, Sharpilo, Sharpilo and Tkach1995). Passerilepis crenata is known from at least 50 species of birds from various families (Spasskaya Reference Spasskaya1966). This pattern of generalist species maintaining stable prevalence across different habitat types is consistent with the findings of Sitko and Heneberg (Reference Sitko and Heneberg2024), who identified several core trematode species that consistently dominate corvid communities across Central Europe. Their study revealed that species like Brachylecithum lobatum (dominant in Corvus spp.) and Lyperosomum petiolatum (dominant in Pica pica and Garrulus glandarius) represent stable components of corvid parasite communities, suggesting these species have evolved robust transmission strategies that function across various environmental conditions. Our results extend this pattern by showing that, despite generalist ecology, even core parasite species can exhibit reduced prevalence under intense urbanisation – as evidenced by the lower prevalence of P. elegans and P. crenata in Kyiv.
Helminth infracommunities in the sample from Kyiv may be characterised as depauperate based on the lowest values of the species richness and abundance. Moreover, the proportion of uninfected hosts (39%) and hosts infected with only one helminth species (60%) was the highest in the sample from Kyiv. The sample from Polissya, on the contrary, was characterised by the highest values of species richness in the helminth infracommunities (up to 7 species in one host) and the lowest proportion of uninfected hosts (18%) and hosts infected with only one helminth species (35%). Helminth infracommunities from the Middle Dnipro River sample had intermediate parameters. The scattered distribution of helminths in crows in all three samples is, presumably, the reason for a low similarity both among the helminth infracommunities and between the samples demonstrated by the SIMPER analysis.
Descriptive analyses indicated that species richness in helminth component communities declined with increasing urbanisation. The lowest richness was observed in Kyiv, the highest in the Polissya region, and an intermediate level in crows from the banks of the Dnipro River. Surprisingly, the evenness in the helminth community from Kyiv city, a highly urbanised locality, was the highest, even higher than in the community from Polissya (see Table 2). Presumably, this was due to the low abundance of all helminth species found in crows from Kyiv. On the other hand, the abundance of helminths in the infracommunities from Kyiv was more aggregated than in those from Polissya (DI = 24.7 in Kyiv vs. DI = 18.7 in Polissya). Despite the fact that descriptive analyses suggested lower helminth richness and abundance in Kyiv compared with Polissya, the regression models indicated high uncertainty and overlapping credible intervals. Therefore, these findings should be interpreted cautiously, as the evidence for a clear effect of urbanisation remains suggestive rather than statistically conclusive.
In the study of the blackbirds from Czechia (Sitko and Zaleśny Reference Sitko and Zaleśny2014), the degradation of the parasite diversity in an urbanised environment was also noted. The birds from the forest population harboured 29 species of parasites, which was almost twice as many as the birds from the city (parasitised by only 15 species). Helminth species richness was also significantly lower in the urban area than in the natural habitat (3.37 in the forested area versus 1.78 in the urban area). In our study, the difference in species diversity was comparatively lower. That can be explained by the fact that the blackbirds from the forests were migrating (which was confirmed by the presence of “southern species” of parasites which infected birds only in their wintering grounds) while the city ones were settled. At the same time, the Hooded Crow is a settled species and gets infected with parasites in the limited territory. However, it interacts with other migratory birds, which can have a significant impact on the parasites’ circulation, which is confirmed by our findings of common rooks’ nematodes in crows from Kyiv. It also worth mentioning that the difference in overall infection levels for crows from the city and natural environment in the present study (69.9% in Kyiv and 82.1% in Polissya) is bigger than the difference in a aforementioned study on blackbirds from the urbanised and forest populations (85.1% in the city and 97.2 in the forest) (Sitko and Zaleśny Reference Sitko and Zaleśny2014).
Meta-analysis of mammalian helminth infections revealed that parasites with different life cycles respond differently in mammals across urban and non-urban ecosystems (Werner and Nunn Reference Werner and Nunn2020). The authors concluded that there is no difference in the prevalence of parasites with direct life cycles in any of the host taxa in urban and non-urban areas. In contrast, parasites with complex life cycles were less prevalent in primate and carnivore populations from urban habitats than those from rural or forest habitats (Werner and Nunn Reference Werner and Nunn2020). Lafferty and Kuris (Reference Lafferty and Kuris2005) also cautioned against simplistic predictions of how anthropogenic changes affect parasite communities, emphasizing that environmental disturbances can simultaneously increase some infectious diseases while reducing others. Urban environments represent a complex form of habitat alteration that exemplifies this principle, where multiple stressors interact to create contrasting effects on different parasite groups. Our findings reveal similar patterns: a difference in trematode diversity from Polissya and Kyiv, contrasted with higher nematode diversity in a city of Kyiv, particularly species with direct life cycles such as B. resectum and E. contortus.
In addition, species with a wide host range (both definitive and intermediate) and a broad geographical range have a higher chance of successful circulation even in urbanised ecosystems. In this study, such species were the trematodes T. zarudnyi (Masalkova Reference Masalkova2019; Soboleva Reference Soboleva1980), P. elegans (Busta Reference Busta1985; Genov and Samnaliev Reference Genov, Samnaliev and Vasilvev1984), and S. sphaerula (Odening Reference Odening1976; Sharpilo Reference Sharpilo1976), as well as the cestodes P. crenata and D. undula (Spasskaya Reference Spasskaya1966).
Model-based inference, limitations, and future directions
Our study provides new information on the helminths of the Hooded Crow and allows us to trace certain patterns in their distribution across the studied samples. However, contrary to our initial expectation, this study did not find strong evidence for an effect of urbanisation on either the species richness or the infection abundance of helminth infracommunities of the Hooded Crow. The estimated differences between the Kyiv and Polissya regions were statistically indistinguishable from zero, with high uncertainty reflected in wide credible intervals.
The main limitation of this research is the sparse and unbalanced nature of the dataset, which is characterised by significant confounding between sampling region and decade. To mitigate this, we employed a Bayesian approach with an informative prior for the expected negative temporal trend. While this methodologically sound step stabilised the model, it is crucial to note that this trend was primarily driven by our prior choice rather than representing a strong signal from the data itself, as confirmed by sensitivity analysis (Supplement 1). The wide credible intervals for the region effects suggest that the study was underpowered to detect a small or moderate effect if one truly exists.
Conclusions
Our statistical analysis, designed to account for the sparse and unbalanced nature of the historical data, did not find credible evidence to support the hypothesis that urbanisation affects helminth communities in the Hooded Crow. The high uncertainty in model estimates suggests that the available data are insufficient for a robust assessment of the urbanisation effect. Nevertheless, this study contributes significantly to the knowledge of helminth diversity in crows at both regional and broader scales. The raw data presented here provide a valuable resource for future meta-analyses and targeted investigations into the impact of urbanisation on avian helminth communities.
Supplementary material
The supplementary material for this article can be found at http://doi.org/10.1017/S0022149X25100850.
Acknowledgements
We sincerely thank the Armed Forces of Ukraine for enabling us to continue our work despite the challenges posed by Russia’s full-scale aggression.
Financial support
This study was financially supported by a grant from the National Academy of Sciences of Ukraine for research laboratories and groups of young scientists (Grant No. 0124U002245).
Competing interests
The authors declare that they have no conflicts of interest relevant to this article. They have no financial, personal, or professional relationships that could be construed to influence the work reported in this manuscript.
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