Abstract
We have conducted the first study of trematodes in wetland birds of the Samara region (European Russia). A total of 25 trematode species from 12 families were identified in 8 species of birds. Eight digenean species (Echinochasmus beleocephalus, Petasiger radiatus, P. exaeretus, Metorchis xanthosomus, Uroproctepisthmium bursicola, Leyogonimus polyoon, Hysteromorpha triloba, Cyathocotyle prussica) were registered for the first time in birds of the Middle Volga region. The first data on helminths in Ardea cinerea, Fulica atra, Phalacrocorax carbo, Larus cachinnans and Cygnus olor inhabiting this territory were obtained. Fifteen species of trematodes we found have veterinary significance as causative agents of dangerous helminthiases.
Acta Biologica Sibirica 10: 1359–1369 (2024)
doi: 10.5281/zenodo.14203853
http://zoobank.org/96B12DB9-43CD-4117-BFCB-3990E6CAEF0D
Citation: Kirillova NYu, Kirillov AA (2024) First data on the trematode fauna of wetland birds in the Samara region (European Russia). Acta Biologica Sibirica 10: 1359–1369. https://doi.org/10.5281/zenodo.14203853
Keywords
Helminths, Digenea, Anseriformes, Charadriiformes, Gruiformes, Pelecaniformes, Suliformes, Middle Volga region
Introduction
Wetland birds inhabit the coasts of various fresh and sea water bodies. In the territory of the Middle Volga region, many waterfowl nest or are encountered during spring or autumn migration. Most wetland birds are valuable game species. In this regard, it is important to study their helminths and, in particular, trematodes, which cause mass epizootics.
Wild birds are vectors of pathogens causing helminthiasis in fish, poultry, domestic animals and humans. Thus, wetland birds play a significant role in the spread and maintenance of the number of helminthiasis pathogens, such as echinostomatosis, prostogonymosis, bilharziellosis (Smogorzhevskaya 1975).
Among avian trematodes, the trematode fauna associated with wetland birds is usually the most diverse and abundant (Sitko and Heneberg 2020). Therefore, it is necessary to conduct monitoring studies of waterfowl, the structure and dynamics of their trematode fauna. Such studies contribute to the prediction of the epidemiological and epizootological situation in a certain area.
The study of the helminth fauna of waterfowl and, in particular, their trematodes has always attracted the attention of parasitologists (Lapage 1961; Bykhovskaya-Pavlovskaya 1962; Smogorzhevskaya 1975; McDonald 1981; Iskova 1985; Ekimova 1989; Nasinkova et al. 1993; Kulisic et al. 2004; Bayssade-Dufour et al. 2006; Sitko et al. 2006; Rudolfova et al. 2007; Kavetska et al. 2008; Kanarek and Zalesny 2013; Kirillov and Kirillova 2013; Sitko and Heneberg 2020).
In recent years, a number of studies have been devoted to the fauna and distribution of wetland birds in Russia and neighboring countries (Vinogradova et Skvortsov 2002; Serbina 2005, 2018; Akramova et al. 2009, 2022; Shabunov and Radchenko 2012; Yakovleva et al. 2012, 2015; Makhmudova 2013; Syrota et al. 2018; Dugarov et al. 2020; Makhmudova and Ibrahimov 2020; Dorzhiev et al. 2021; Yakovleva 2024). Unfortunately, studies of helminth fauna in wetland birds of the Samara region (European Russia) are still missing. This paper presents the first data on trematodes from waterfowl inhabiting the Samara region.
Materials and methods
Study area
The territory of the Samara region is located in the southeast of European Russia in the Middle Volga region and occupies an area approximately within 51°47,0´– 54°41,0´ north latitude and 47°55,0´–52°35,0´ east longitude. The area of the Samara region is 53 565 km2 (Gorelov et al. 1990; Dmitrieva and Kabytov 1996). Within the region, the Volga riverbed is regulated and forms the Kuibyshev and Saratov water reservoirs. The territory of the Samara region is distinguished by its varied relief. On the right bank of the Volga are the Zhiguli Mountains, around which the Volga forms the well-known Samarskaya Luka. There are many natural and artificial water reservoirs in the Samara region: small rivers, lakes, ponds and streams. The region is located on the border of two natural zones – forest-steppe and steppe, which determines the richness of the flora and fauna of the region. There are 379 species of vertebrates, including 235 species of birds from 9 orders, of which 195 species nest in the region (Gorelov et al. 1990; Dmitrieva and Kabytov 1996).
Trematodes collection and examination
During a comprehensive parasitological survey of vertebrates in the Samara region (Middle Volga region) in the 2023 and 2023 field seasons, the trematode fauna was studied from 15 individuals of eight species of wetland birds: Anas platyrhynchos Linnaeus, 1758 (4), Cygnus olor (Gmelin, 1789) (4), Phalacrocorax carbo (Linnaeus, 1758) (2), Fulica atra Linnaeus, 1758 (1), Chroicocephalus ridibundus (Linnaeus,1766) (1), Larus cachinnans Pallas, 1811 (1), Sterna hirundo Linnaeus, 1758 (1), and Ardea cinerea Linnaeus, 1758 (1).
The birds were examined using the method of complete helminthological necropsy according to Dubinina (1971). No birds were killed intentionally for our study. We examined only dead wetland birds that died naturally and were kindly provided by the staff of the Togliatti Zoo Corner with a bird shelter and the Zhiguli Nature Reserve. Frozen entrails (mainly the gastrointestinal tract) of four mallards were kindly provided by local hunters.
Trematode specimens were collected from birds in six districts of the Samara region. Digeneans were recovered from the internal organs of the birds and immobilized by heating in a saline. Then the trematodes were stained with acetic carmine, dehydrated, cleared with clove oil, and mounted in Canada balsam. To characterize the trematode infection of birds, the following indices were used: prevalence of infection (P, %) and mean abundance (MA).
The taxonomic identification of wetland birds was carried out according to Spiridonov et al. (2019). Trematode species were identified according to Bykhovskaya-Pavlovskaya (1962), Sudarikov (1984), Iskova (1985), Sonin (1985), Shigin (1993), Faltynkova et al. (2008), Zazornova (2012), and Vainutis et al. (2023). The taxonomy of digeneans is given according to the GBIF database (https://www.gbif.org/, accessed on 28 September 2024) and the work of Kanarek et al. (2017). Trematode specimens are stored in the parasitological collection of the Institute of Ecology of Volga Basin of RAS (Togliatti).
This study was approved by the Bioethics Committee of the Institute of Ecology of Volga River Basin of RAS (Registration number: 6/24; 22 October 2024). Our research was conducted in accordance with the ethical standards of humane treatment of animals and recommended standards described in Directive of the European Parliament and of the Council of the European Union of 22 September 2010, “On the protection of animals used for scientific purposes” (EU Directive 2010/63/EU).
Results and discussion
As a result of the first helminthological study of wetland birds from the orders Anseriformes, Charadriiformes, Gruiformes, Pelecaniformes and Suliformes in the Samara region, we registered 25 trematode species (Table 1). All digeneans found in the avifauna were represented by adult individuals.
Trematodes found in wetland birds of the Samara region belong to 12 families (Table 1). The most represented family of trematodes in the studied birds is Echinostomatidae, which includes six species. Less represented in the birds are the families Strigeidae (4) and Diplostomidae (3). The families Echinochasmidae, Opisthorchiidae and Schistosomatidae include two species each. The remaining six families are represented in the wetland birds by only one species each.
All 15 examined individuals of birds were infected with trematodes. A total of 4905 parasite specimens were collected. The overall infection rate of birds with digeneans was 100%, MA = 319.6. The highest trematode infection was revealed in Ph. carbo. The overall trematode infection rates for the other wetland bird species examined were significantly lower (Fig. 1).
Species | D1 | Host | Site | Locality | P, % | IR, spec. | MA |
---|---|---|---|---|---|---|---|
Family Plagiorchiidae | |||||||
Plagiorchis laricola Skrjabin, 1924 | P | Chroicocephalus ridibundus | small intestine | Krasnoyarskiy district | 100 (in one examined) | 15 | 15.0 |
Family Echinochasmidae | |||||||
Echinochasmus beleocephalus (Linstow, 1873) | P | Anas platyrhynchos | small intestine | Pokhvistnevskiy district | 100 (in two examined) | 10–60 | 35.0 |
Stavropolskiy district | 50.0 (in one of 2 examined) | 35 | 17.5 | ||||
Uroproctepisthmium bursicola (Creplin, 1837) | P | Ardea cinerea | liver | Stavropolskiy district | 100 (in one examined) | 16 | 16.0 |
Family Echinostomatidae | |||||||
Echinostoma revolutum (Fröhlich, 1802) | C | Anas platyrhynchos | small intestine | Stavropolskiy district | 50.0 (in one of 2 examined | 2 | 1.0 |
Cygnus olor | - | Bezenchukskiy district | 50.0 (in one of 2 examined) | 3 | 1.5 | ||
- | Pestravskiy district | 50.0 (in one of 2 examined) | 4 | 2.0 | |||
Echinostoma miyagawai Ishii, 1932 | P | Anas platyrhynchos | small intestine | Pokhvistnevskiy district | 50.0 (in one of two examined) | 6 | 3.0 |
Echinoparyphium recurvatum (Linstow, 1873) | P | Chroicocephalus ridibundus | small intestine | Krasnoyarskiy district | 100 (in one examined) | 3 | 3.0 |
Anas platyrhynchos | small intestine | Pokhvistnevskiy district | 100 (in two examined) | 5–12 | 8.5 | ||
Petasiger radiatus (Dujardin, 1845) | P | Phalacrocorax carbo | small intestine | Privolzhskiy district | 100 (in two examined) | 98–145 | 121.5 |
Petasiger exaeretus Dietz, 1909 | P | Phalacrocorax carbo | small intestine | Privolzhskiy district | 100 (in two examined) | 22–30 | 26.0 |
Hypoderaeum conoideum (Bloch, 1782) | C | Anas platyrhynchos | small intestine | Pokhvistnevskiy district | 50.0 (in one of 2 examined) | 1 | 0.5 |
Family Psilostomidae | |||||||
Psilochasmus oxyurus (Creplin, 1825) | C | Anas platyrhynchos | small intestine | Pokhvistnevskiy district | 50.0 (in one of 2 examined) | 2 | 1.0 |
Family Renicolidae | |||||||
Renicola lari Timon- David, 1933 | H | Sterna hirundo | kidneys | Stavropolskiy district | 100 (in one examined) | 1 | 1.0 |
Family Notocotylidae | |||||||
Notocotylus attenuatus (Rudolphi, 1809) | C | Anas platyrhynchos | intestinal caeca | Pokhvistnevskiy district | 100 (in 2 examined) | 17–31 | 24.0 |
Stavropolskiy district | 50.0 (in one of 2 examined) | 67 | 33.5 | ||||
Family Pleurogenidae | |||||||
Leyogonimus polyoon (Linstow, 1887) | H | Fulica atra | small intestine | Stavropolskiy district | 100 (in one examined) | 1 | 1.0 |
Family Opisthorchiidae | |||||||
Metorchis xanthosomus (Creplin, 1846) | p | Phalacrocorax carbo | liver | Privolzhskiy district | 50.0 (in one of 2 examined) | 4 | 2.0 |
Apophallus muehlingi (Jägerskiöld, 1899) | P | Phalacrocorax carbo | small intestine | Privolzhskiy district | 100 (in two examined) | 1260– 2100 | 1680.0 |
Chroicocephalus ridibundus | small intestine | Krasnoyarskiy district | 100 (in one examined) | 7 | 7.0 | ||
Larus cachinnans | small intestine | Stavropolskiy district | 100 (in one examined) | 230 | 230.0 | ||
Sterna hirundo | small intestine | Stavropolskiy district | 100 (in one examined) | 6 | 6.0 | ||
Family Diplostomidae | |||||||
Diplostomum chromatoforum (Brown, 1931) | H | Larus cachinnans | small intestine | Stavropolskiy district | 100 (in one examined) | 2 | 2.0 |
Diplostomum helveticum (Dubois, 1929) | P | Larus cachinnans | small intestine | Stavropolskiy district | 100 (in one examined) | 4 | 4.0 |
Hysteromorpha triloba Rudolphi, 1819 | H | Phalacrocorax carbo | small intestine | Privolzhskiy district | 50.0 (in one of 2 examined) | 292 | 146.0 |
Family Schistosomatidae | |||||||
Bilharziella polonica (Kowalewski, 1895) | C | Anas platyrhynchos | blood vessels | Pokhvistnevskiy district | 100 (in two examined) | 9–25 | 17.0 |
Stavropolskiy district | 50.0 (in one of 2 examined) | 7 | 3.5 | ||||
Dendritobilharzia pulverulenta (Braun, 1901) | C | Fulica atra | blood vessels | Stavropolskiy district | 100 (in one examined) | 10 | 10.0 |
Family Strigeidae | |||||||
Cotylurus cornutus (Rudolphi, 1809) | P | Cygnus olor | small intestine | Bezenchukskiy district | 100 (in two examined) | 15–23 | 19.0 |
Pestravskiy district | 100 (in two examined) | 8–14 | 11.0 | ||||
Cotylurus flabelliformis (Faust, 1917) | H | Anas platyrhynchos | - | Pokhvistnevskiy district | 100 (in two examined) | 7–100 | 53.5 |
Cotylurus brevis Dubois & Rausch, 1950 | H | Anas platyrhynchos | small intestine | Pokhvistnevskiy district | 100 (in two examined) | 12–20 | 16.0 |
Ichthyocotylurus pileatus (Rudolphi, 1802) | H | Sterna hirundo | small intestine | Stavropolskiy district | 100 (in one examined) | 12 | 12.0 |
Family Cyathocotylidae | |||||||
Cyathocotyle prussica Mühling, 1896 | P | Phalacrocorax carbo | small intestine | Privolzhskiy district | 100 (in two examined) | 69–83 | 76.0 |
Note: 1 – D – distribution, P – Palearctic, H – Holarctic, C – Cosmopolitan.
Figure 1.Overall mean abundance index of trematodes in wetland birds from the Samara region.
The richest trematode fauna was found in the mallard (A. platyrhynchos), as it included 10 parasite species. Six trematode species were found in the great cormorant (Ph. carbo). Few trematodes were identified in Ch. ridibundus, L. cachinnans and S. hirundo – 3 species each. Two trematode species were recorded in C. olor and F. atra. Only one trematode species was found in Ardea cinerea (Table 1, Fig. 2).
For the studied bird species, the most common parasite was A. muehlingi, recorded in four host species. Echinostoma revolutum and E. recurvatum occurred in two hosts each. Twenty-two trematode species were recorded in only one host species.
Most of the identified trematode species (16 species) are obligate parasites of wetland birds. Four species (R. lari, D. chromatoforum, D. helveticum, I. pileatus) are host-specific parasites of gulls. Metorchis xanthosomus is an obligate parasite of birds of prey. Trematodes of the genus Petasiger are host-specific parasites of Phalacrocorax carbo, and Leyogonimus polyoon is a common parasite of rallid birds. The trematode Plagiorchis laricola can parasitize birds of different orders.
Twelve species of trematodes that we found in wetland birds of the Samara region are common in the Palearctic, seven trematode species are widespread in the Holarctic, and the remaining six species are cosmopolitan (Table 1).
Conclusion
Thus, we have obtained the first data on the trematode fauna in wetland birds in the Samara region. A total of 25 trematode species were identified in 8 species of birds. For the first time, data on these parasites of Ardea cinerea, Fulica atra, Phalacrocorax carbo, Larus cachinnans and Cygnus olor were obtained for the Middle Volga region. Previously, 72 digenean species were recorded for wetland birds in this area (Kostyunin 2010; Kirillov et al. 2012). As a result of our research, the list of trematodes in the wetland avifauna was expanded by eight species of parasites (E. beleocephalus, P. radiatus, P. exaeretus, M. xanthosomus, U. bursicola, L. polyoon, H. triloba, C. prussica) and currently includes 80 digenean species.
Fifteen species of trematodes found in wetland birds of the Samara region have veterinary significance as pathogens of dangerous helminthiases, namely: E. revolutum, E. miyagawai, E. recurvatum, H. conoideum, E. beleocephalus, N. attenuatus, B. polonica, D. pulverulenta, A. muehlingi, D. chromatoforum, D. helveticum, C. cornutus, C. flabelliformis, C. brevis, and I. pileatus.
Our first study of trematodes in wetland birds in the Samara region showed interesting results. Therefore, the prospect of further parasitological study of wetland birds requires both an expansion of the number of host bird species and an increase in the number of individuals of the already studied birds for examination.
Figure 2.Species richness (number of species) of trematodes in wetland bird from the Samara region.
Acknowledgements
This research was supported by the Russian Science Foundation, grant number 23- 24-10021, https://rscf.ru/en/project/23-24-10021/.
The authors express their deep gratitude to the head of the Togliatti Zoo Corner with a bird shelter Natalya I. Goncharova and the senior researcher of the Zhiguli Nature Reserve Galina P. Lebedeva for providing materials on wetland birds.
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