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20 pages, 25566 KiB  
Article
Reassortants of the Highly Pathogenic Influenza Virus A/H5N1 Causing Mass Swan Mortality in Kazakhstan from 2023 to 2024
by Kulyaisan T. Sultankulova, Takhmina U. Argimbayeva, Nurdos A. Aubakir, Arailym Bopi, Zamira D. Omarova, Aibarys M. Melisbek, Kobey Karamendin, Aidyn Kydyrmanov, Olga V. Chervyakova, Aslan A. Kerimbayev, Yerbol D. Burashev, Yermukhanmet T. Kasymbekov and Mukhit B. Orynbayev
Animals 2024, 14(22), 3211; https://doi.org/10.3390/ani14223211 - 8 Nov 2024
Viewed by 1022
Abstract
In the winter of 2023/2024, the mass death of swans was observed on Lake Karakol on the eastern coast of the Caspian Sea. From 21 December 2023 to 25 January 2024, 1132 swan corpses (Cygnus olor, Cygnus cygnus) were collected [...] Read more.
In the winter of 2023/2024, the mass death of swans was observed on Lake Karakol on the eastern coast of the Caspian Sea. From 21 December 2023 to 25 January 2024, 1132 swan corpses (Cygnus olor, Cygnus cygnus) were collected and disposed of on the coast by veterinary services and ecologists. Biological samples were collected from 18 birds for analysis at different dates of the epizootic. It was found that the influenza outbreak was associated with a high concentration of migrating birds at Lake Karakol as a result of a sharp cold snap in the northern regions. At different dates of the epizootic, three avian influenza A/H5N1 viruses of clade 2.3.4.4.b were isolated from dead birds and identified as highly pathogenic viruses (HPAIs) based on the amino acid sequence of the hemagglutinin multi-base proteolytic cleavage site (PLREKRRRKR/G). A phylogenetic analysis showed that the viruses isolated from the swans had reassortations in the PB2, PB1, and NP genes between highly pathogenic (HP) and low-pathogenic (LP) avian influenza viruses. Avian influenza viruses A/Cygnus cygnus/Karakol lake/01/2024(H5N1) and A/Mute swan/Karakol lake/02/2024(H5N1) isolated on 10 January 2024 received PB2, PB1, and NP from LPAIV, while A/Mute swan/Mangystau/9809/2023(H5N1) isolated on 26 December 2023 received PB1 and NP from LPAIV, indicating that the H5N1 viruses in this study are new reassortants. All viruses showed amino acid substitutions in the PB2, PB1, NP, and NS1 segments, which are critical for enhanced virulence or adaptation in mammals. An analysis of the genomes of the isolated viruses showed that bird deaths during different periods of the epizootic were caused by different reassortant viruses. Kazakhstan is located at the crossroads of several migratory routes of migratory birds, and the possible participation of wild birds in the introduction of various pathogens into the regions of Kazakhstan requires further study. Full article
(This article belongs to the Special Issue Interdisciplinary Perspectives on Wildlife Disease Ecology)
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Figure 1

Figure 1
<p>Wild bird death site in the winter of 2023/2024.</p>
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<p>Dynamics of swan mortality on Lake Karakol in the winter of 2023/2024 (according to data from the veterinary service of the Mangystau region).</p>
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<p>Remains of a swan’s corpse.</p>
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<p>Swan corpse with signs of diarrhea and without a right leg (with a gnawed leg).</p>
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<p>Stray dog on the shore of Lake Karakol.</p>
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<p>Whooper swan (<span class="html-italic">Cygnus cygnus</span>) (an adult).</p>
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<p>Whooper swan (<span class="html-italic">Cygnus olor</span>) (a cygnet).</p>
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<p>Sick bird (a cygnet).</p>
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<p>Heart. Haemorrhages in the myocard.</p>
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<p>Haemorrhages in the liver.</p>
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<p>Lung edema.</p>
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<p>Phylogenetic trees, including complete PB2 (<b>A</b>), PB1 (<b>B</b>), PA (<b>C</b>), HA (<b>D</b>), NP (<b>E</b>), NA (<b>F</b>), M (<b>G</b>), and NS (<b>H</b>) genes, of Kazakhstani HPAIV H5N1 strains isolated from swans on the coast of Lake Karakol, located on the eastern shore of the Kazakhstani part of the Caspian Sea from 2023 to 2024 and publicly available sequences (GenBank). The strains investigated in this study are marked with triangles, squares, and circles: <span class="html-fig-inline" id="animals-14-03211-i001"><img alt="Animals 14 03211 i001" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i001.png"/></span>—A/<span class="html-italic">Mute swan</span>/Mangystau/9809/2023(H5N1); <span class="html-fig-inline" id="animals-14-03211-i002"><img alt="Animals 14 03211 i002" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i002.png"/></span>—A/<span class="html-italic">Cygnus cygnus</span>/Karakol lake/01/2024(H5N1); <span class="html-fig-inline" id="animals-14-03211-i003"><img alt="Animals 14 03211 i003" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i003.png"/></span>—A/Mute swan/Karakol lake/02/2024(H5N1); <span class="html-fig-inline" id="animals-14-03211-i004"><img alt="Animals 14 03211 i004" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i004.png"/></span>—A/mute swan/Mangystau/1-S24R-2/2024(H5N1) (virus isolated at NVRC and KazNARU by Tabynov K et al. in 2024 [<a href="#B27-animals-14-03211" class="html-bibr">27</a>]).</p>
Full article ">Figure 12 Cont.
<p>Phylogenetic trees, including complete PB2 (<b>A</b>), PB1 (<b>B</b>), PA (<b>C</b>), HA (<b>D</b>), NP (<b>E</b>), NA (<b>F</b>), M (<b>G</b>), and NS (<b>H</b>) genes, of Kazakhstani HPAIV H5N1 strains isolated from swans on the coast of Lake Karakol, located on the eastern shore of the Kazakhstani part of the Caspian Sea from 2023 to 2024 and publicly available sequences (GenBank). The strains investigated in this study are marked with triangles, squares, and circles: <span class="html-fig-inline" id="animals-14-03211-i001"><img alt="Animals 14 03211 i001" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i001.png"/></span>—A/<span class="html-italic">Mute swan</span>/Mangystau/9809/2023(H5N1); <span class="html-fig-inline" id="animals-14-03211-i002"><img alt="Animals 14 03211 i002" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i002.png"/></span>—A/<span class="html-italic">Cygnus cygnus</span>/Karakol lake/01/2024(H5N1); <span class="html-fig-inline" id="animals-14-03211-i003"><img alt="Animals 14 03211 i003" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i003.png"/></span>—A/Mute swan/Karakol lake/02/2024(H5N1); <span class="html-fig-inline" id="animals-14-03211-i004"><img alt="Animals 14 03211 i004" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i004.png"/></span>—A/mute swan/Mangystau/1-S24R-2/2024(H5N1) (virus isolated at NVRC and KazNARU by Tabynov K et al. in 2024 [<a href="#B27-animals-14-03211" class="html-bibr">27</a>]).</p>
Full article ">Figure 12 Cont.
<p>Phylogenetic trees, including complete PB2 (<b>A</b>), PB1 (<b>B</b>), PA (<b>C</b>), HA (<b>D</b>), NP (<b>E</b>), NA (<b>F</b>), M (<b>G</b>), and NS (<b>H</b>) genes, of Kazakhstani HPAIV H5N1 strains isolated from swans on the coast of Lake Karakol, located on the eastern shore of the Kazakhstani part of the Caspian Sea from 2023 to 2024 and publicly available sequences (GenBank). The strains investigated in this study are marked with triangles, squares, and circles: <span class="html-fig-inline" id="animals-14-03211-i001"><img alt="Animals 14 03211 i001" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i001.png"/></span>—A/<span class="html-italic">Mute swan</span>/Mangystau/9809/2023(H5N1); <span class="html-fig-inline" id="animals-14-03211-i002"><img alt="Animals 14 03211 i002" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i002.png"/></span>—A/<span class="html-italic">Cygnus cygnus</span>/Karakol lake/01/2024(H5N1); <span class="html-fig-inline" id="animals-14-03211-i003"><img alt="Animals 14 03211 i003" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i003.png"/></span>—A/Mute swan/Karakol lake/02/2024(H5N1); <span class="html-fig-inline" id="animals-14-03211-i004"><img alt="Animals 14 03211 i004" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i004.png"/></span>—A/mute swan/Mangystau/1-S24R-2/2024(H5N1) (virus isolated at NVRC and KazNARU by Tabynov K et al. in 2024 [<a href="#B27-animals-14-03211" class="html-bibr">27</a>]).</p>
Full article ">Figure 12 Cont.
<p>Phylogenetic trees, including complete PB2 (<b>A</b>), PB1 (<b>B</b>), PA (<b>C</b>), HA (<b>D</b>), NP (<b>E</b>), NA (<b>F</b>), M (<b>G</b>), and NS (<b>H</b>) genes, of Kazakhstani HPAIV H5N1 strains isolated from swans on the coast of Lake Karakol, located on the eastern shore of the Kazakhstani part of the Caspian Sea from 2023 to 2024 and publicly available sequences (GenBank). The strains investigated in this study are marked with triangles, squares, and circles: <span class="html-fig-inline" id="animals-14-03211-i001"><img alt="Animals 14 03211 i001" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i001.png"/></span>—A/<span class="html-italic">Mute swan</span>/Mangystau/9809/2023(H5N1); <span class="html-fig-inline" id="animals-14-03211-i002"><img alt="Animals 14 03211 i002" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i002.png"/></span>—A/<span class="html-italic">Cygnus cygnus</span>/Karakol lake/01/2024(H5N1); <span class="html-fig-inline" id="animals-14-03211-i003"><img alt="Animals 14 03211 i003" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i003.png"/></span>—A/Mute swan/Karakol lake/02/2024(H5N1); <span class="html-fig-inline" id="animals-14-03211-i004"><img alt="Animals 14 03211 i004" src="/animals/animals-14-03211/article_deploy/html/images/animals-14-03211-i004.png"/></span>—A/mute swan/Mangystau/1-S24R-2/2024(H5N1) (virus isolated at NVRC and KazNARU by Tabynov K et al. in 2024 [<a href="#B27-animals-14-03211" class="html-bibr">27</a>]).</p>
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<p>Hypothetical reassortment events of the A/<span class="html-italic">Cygnus cygnus</span>/Karakol lake/01/2024(H5N1) viruses. The eight genes are shown in <a href="#animals-14-03211-t001" class="html-table">Table 1</a> and are as follows: PB2, PB1, PA, HA, NP, NA, M, and NS. The colors of the bars indicate the different sources of the gene segments.</p>
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<p>Hypothetical reassortment events of the A/<span class="html-italic">mute swan</span>/Mangystau/1-S24R-2/2024(H5N1) viruses.</p>
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<p>Hypothetical reassortment events of the A/<span class="html-italic">Mute swan</span>/Mangystau/9809/2023(H5N1) viruses.</p>
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17 pages, 4654 KiB  
Article
Multi-Scale Habitat Selection by the Wintering Whooper Swan (Cygnus cygnus) in Manas National Wetland Park, Northwestern China
by Han Yan, Xuejun Ma, Weikang Yang and Feng Xu
Diversity 2024, 16(5), 306; https://doi.org/10.3390/d16050306 - 20 May 2024
Viewed by 1476
Abstract
Habitat selection has been a central focus of animal ecology, with research primarily concentrating on habitat choice, utilization, and evaluation. However, studies confined to a single scale often fail to reveal the habitat selection needs of animals fully and accurately. This paper investigates [...] Read more.
Habitat selection has been a central focus of animal ecology, with research primarily concentrating on habitat choice, utilization, and evaluation. However, studies confined to a single scale often fail to reveal the habitat selection needs of animals fully and accurately. This paper investigates the wintering whooper swan (Cygnus cygnus) in Manas National Wetland Park, Xinjiang, using satellite tracking to determine their locations. The Maximum Entropy model (MaxEnt) was applied to explore the multi-scales habitat selection needs of Manas National Wetland Park’s wintering whooper swans across nighttime, daytime, and landscape scales. This study showed that the habitat selection of the wintering whooper swans varied in different scales. At the landscape scale, wintering whooper swans prefer habitats with average winter precipitations of 6.9 mm and average temperatures of −6 °C, including water bodies and wetlands, indicating that climate (precipitation and temperature) and land type (wetlands and water bodies) influence their winter habitat selection. During daytime, whooper swans prefer areas close to wetlands, water bodies, and bare land, with a more dispersed distribution of water bodies. For nighttime, they tend to choose areas within the wetland park where human disturbance is minimal and safety is higher. This study can provide scientific basis and data support for habitat conservation and management of wintering waterbirds like whooper swans, recommending targeted conservation measures to effectively manage and protect the wintering grounds of whooper swans. Full article
(This article belongs to the Section Animal Diversity)
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Figure 1

Figure 1
<p>The study area.</p>
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<p>Habitat utilization distribution of whooper swans at various scales during the wintering period.</p>
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<p>Receiver operating characteristic curves for the landscape, daytime, and nighttime scales of the habitat suitability model of wintering whooper swans.</p>
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<p>Receiver operating characteristic curves for the landscape, daytime, and nighttime scales of the habitat suitability model of wintering whooper swans.</p>
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<p>Variable importance influencing the habitat selection of wintering whooper swans at the landscape, daytime, and nighttime scales in the MaxEnt model.</p>
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<p>The most important variables for wintering whooper swans at the landscape scale.</p>
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<p>The distribution of suitable habitats for wintering whooper swans at the landscape scale.</p>
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<p>The most important variables for wintering whooper swans at the daytime scale. Notes: The grey line represent mean value of variables and shadow means the stand error.</p>
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<p>The distribution of suitable habitat for wintering whooper swans at the daytime scale.</p>
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<p>The most important variables for wintering whooper swans at the nighttime scale. Notes: The grey line represent mean value of variables and shadow means the stand error.</p>
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<p>The distribution of suitable habitat for wintering whooper swans at the nighttime scale.</p>
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11 pages, 1884 KiB  
Article
Descriptive Pathological Study of Avian Schistosomes Infection in Whooper Swans (Cygnus cygnus) in Japan
by Mohamed S. Ahmed, Reda E. Khalafalla, Ashraf Al-Brakati, Tokuma Yanai and Ehab Kotb Elmahallawy
Animals 2020, 10(12), 2361; https://doi.org/10.3390/ani10122361 - 10 Dec 2020
Cited by 3 | Viewed by 3113
Abstract
Cercarial dermatitis, or Swimmer’s itch, is one of the emerging diseases caused by the cercariae of water-borne schistosomes, mainly Trichobilharzia spp. Since the zoonotic potential of Allobilharzia visceralis is still unknown, studies on this schistosome would be helpful to add knowledge on its [...] Read more.
Cercarial dermatitis, or Swimmer’s itch, is one of the emerging diseases caused by the cercariae of water-borne schistosomes, mainly Trichobilharzia spp. Since the zoonotic potential of Allobilharzia visceralis is still unknown, studies on this schistosome would be helpful to add knowledge on its possible role in causing human infections. In the present study, 54 whooper swans (Cygnus cygnus) from rescue/rehabilitation centers in Honshu, Japan, were necropsied to identify the cause of death. Grossly, 33 (61.11%) swans were severely emaciated and 23 (42.59%) had multiple reddened areas throughout the length of the intestine with no worms detected in the internal organs. Microscopically, adult schistosomes were found in the lumen of the mesenteric, serosal, portal, and testicular veins, in the capillaries of the intestinal lamina propria, and in the sinusoids of the adrenal gland, spleen, and liver of 23 (42.59%) swans. Hypertrophy of veins containing adult worms was identified in 15 (27.77%) swans, and vascular lumen obliteration was observed in 8 (14.81%) swans. Mild to severe villous atrophy and superficial enteritis were observed in 8 birds (14.81%), whereas bile pigments and hemosiderin were detected in the livers of 14 (25.92%) and 18 (33.33%) swans, respectively. In three swans (5.55%), schistosome parasites were found in the subcapsular veins of the testes. The schistosomes in the present study were assumed to be A. visceralis based on the microscopical and histological evidence of adult schistosomes found in the lumen of veins as well as the infection pathology, which was very similar to the schistosome-induced pathology previously reported in swans infected by A. visceralis in Europe and Australia. The swans examined herein most likely died from obstructive phlebitis associated with A. visceralis, but further molecular confirmation is required for identification of this species. However, the present study does not provide new data on the zoonotic potential, but only on the pathogenic potential of this schistosome in swans. Furthermore, our study provides a novel contribution to the description of the pathological effects of avian schistosomes infection in whooper swans in Japan. Full article
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Figure 1

Figure 1
<p>Effect of the parasite in the intestine. (<b>A</b>) Adult worms (W) are seen in the thickened walls of the serosal vein (H). Note the normal thickness of the artery (black arrow). (<b>B</b>) Brownish pigment–laden macrophages (white arrow) around the worm (W) in the thickened wall of the mesenteric veins (H). (<b>C</b>) The vein lumen was almost occluded due to marked myointimal hyperplasia in the veins of the muscular layer of the intestine (white star), with perivascular inflammatory reaction (I). (<b>D</b>) Several schistosome eggs (white arrowheads) present in the intestinal lamina propria and surrounded by an inflammatory reaction of lymphocytes and plasma cells (I); the intestinal villi are markedly blunted (g). Hematoxylin and eosin stain (100×).</p>
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<p>Effect of the parasite in the liver. (<b>A</b>) Adult worms (W) present in the thickened walled of the portal vein (H) with hemosiderin pigment deposition (white arrow) and bile duct hyperplasia (b). (<b>B</b>) Schistosome parasite (W) found in the hepatic sinusoids surrounded by degenerated hepatocyte (d) and massive inflammatory reaction (I). Hematoxylin and eosin stain (100×). (<b>C</b>) Emerald green–colored clumps of bile pigment (bi), Hall stain (400×). (<b>D</b>) Macrophages laden with bluish pigment (He), Berlin blue stain (100×).</p>
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<p>Effect of the parasite in the adrenal gland, spleen, and testis. (<b>A</b>, <b>B</b>) Multiple cross-sections of adult worms (W) found in the sinusoids of the adrenal gland surrounded by infiltration of mononuclear inflammatory cells (I). (<b>C</b>) Adult worms (W) found in the splenic veins. Note the oral sucker (Os) and acetabulum (Ac) of the parasite. (<b>D</b>) Multiple cross-sections of adult schistosomes (W) completely occlude the subcapsular veins of the testis and were surrounded by the infiltration of mononuclear inflammatory cells (I). Note the seminal vesicles of the parasite (Sv) and the presence of female (f) in the ventral groove of the male (m) parasite. Hematoxylin and eosin stain (100×).</p>
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8 pages, 1066 KiB  
Article
First Detection of Cryptosporidium spp. in Migratory Whooper Swans (Cygnus cygnus) in China
by Ke Wang, Azhar Gazizova, Yuexin Wang, Kaihui Zhang, Yifan Zhang, Yankai Chang, Yuan Cui, Yuxi Zhang, Sumei Zhang and Longxian Zhang
Microorganisms 2020, 8(1), 6; https://doi.org/10.3390/microorganisms8010006 - 18 Dec 2019
Cited by 13 | Viewed by 2694
Abstract
Cryptosporidium is an important protozoan parasite that can cause gastrointestinal diseases in humans and that also causes respiratory and gastrointestinal diseases in birds. In this study, we investigated the occurrence of Cryptosporidium species in migratory whooper swans in China. Fecal samples (n [...] Read more.
Cryptosporidium is an important protozoan parasite that can cause gastrointestinal diseases in humans and that also causes respiratory and gastrointestinal diseases in birds. In this study, we investigated the occurrence of Cryptosporidium species in migratory whooper swans in China. Fecal samples (n = 467) from whooper swans were collected from Sanmenxia Swan Lake National Urban Wetland Park, China. The samples were analyzed for Cryptosporidium species and genotypes with PCR along a sequence analysis of the small subunit rRNA. Cryptosporidium was detected in eight of the 467 (1.7%) samples. The analysis of the small subunit rRNA sequence data revealed two zoonotic species (Cryptosporidium parvum and Cryptosporidium andersoni) and one genotype (Cryptosporidium goose genotype II). These are the first data on the positive rate of Cryptosporidium spp. in whooper swans in China, and they suggest that whooper swans can harbor the zoonotic species C. parvum and C. andersoni in China. Full article
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Graphical abstract

Graphical abstract
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<p>Location of the city (▲) in which the samples were collected.</p>
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<p>Neighbor-joining tree based on small subunit (SSU) rRNA gene sequences of <span class="html-italic">Cryptosporidium</span>. GenBank accession numbers are shown in parentheses after the isolate identifiers. Numbers on the branches are percentage bootstrap values &gt;50% that were calculated from 1000 replicates. Genotypes marked with filled triangles are known genotypes identified in the present study.</p>
Full article ">
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