Epidemiological Perspectives of Wildlife-Associated Bacteria and Parasites

A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Wildlife".

Deadline for manuscript submissions: closed (31 January 2021) | Viewed by 30971

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Department of Veterinary Medicine and Animal Productions, Università degli Studi di Napoli Federico II, 80137 Naples, Italy
Interests: veterinary medicine; microbiome studies; zoonotic diseases; infectious disease epidemiology
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

Wildlife is an underexplored world, and wildlife-associated bacteria and parasite research, included in the biggest microbiome studies, is still a developing field. Wildlife bacteria and parasite exploration might be an important goal for wildlife health monitoring, evolutionary biology, conservation, and ecology, acting also as reservoirs in the epidemiological studies of antibiotic and antiparasitic resistance in the community and environment. Wildlife has also been considered a biomonitor of the direct and indirect effects of anthropogenic environmental disturbances. Climate change, land-use change, environmental contamination, new infectious disease, and drug resistance are some of the most global crucial threats to biodiversity and should indirectly modify host-associated bacteria and parasite diversity in wildlife populations. Therefore, it is necessary to increase our knowledge in this field, and investigations into composition and function bacteria and parasites are welcome in this topic.

All research and authors are invited to examine:

1) The importance, transmission, and prevalence of bacteria and parasites in a given wild host;

2) Original information to better understand the dynamics among wildlife species, humans, and domestic animals assessing the factors that can drive the transmission of bacteria and parasites and the risk factors for human and animal health;

3) Bacterial and parasitic zoonoses of wildlife and the role of potential hosts for transmission of a zoonotic disease in urban or peri-urban areas, considered very attractive for adaptable wild animals;

4) The role of wildlife in antimicrobial resistance distribution and the factors that affect its evolution, dissemination, and persistence;

5) The development of comprehensive diagnostic and treatment strategies for wildlife and discovery of markers and molecules.

Prof. Luca Borrelli
Guest Editor

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Keywords

  • bacterial and parasitic diseases
  • zoonoses
  • antimicrobial resistance
  • wildlife health monitoring

Published Papers (11 papers)

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9 pages, 2366 KiB  
Article
Monitoring Campaign over an Edible Dormouse Population (Glis glis; Rodentia: Gliridae) in Sicily: First Report of Mesocestodiasis
by Giorgia Schirò, Domenico Pieri, Mario Lo Valvo, Luigi Gradoni, Simone Mario Cacciò, Francesco Severini, Gianluca Marucci, Lucia Galuppo, Valentina Cumbo, Roberto Puleio and Guido Ruggero Loria
Animals 2021, 11(4), 934; https://doi.org/10.3390/ani11040934 - 25 Mar 2021
Cited by 1 | Viewed by 1857
Abstract
This study reports on the health status of the edible dormouse (Glis glis) living in Nebrodi Park (Sicily, Italy), responsible for nut crop damage in the area. In the frame of a monitoring campaign for potential zoonotic risk involving 30 dormice, [...] Read more.
This study reports on the health status of the edible dormouse (Glis glis) living in Nebrodi Park (Sicily, Italy), responsible for nut crop damage in the area. In the frame of a monitoring campaign for potential zoonotic risk involving 30 dormice, rectal and conjunctival swabs and fur and nest content were collected for bacteriological and parasitological examinations, respectively. A large presence of fleas belonging to Monopsyllus sciurorum was found. Necropsy of a dead dormouse revealed an infection of Mesocestoides lineatus, whose cysts were found in the abdomen cavity and on the liver; this is the first report of this in this species. Further studies are necessary to identify their role in the environment, considering the limited knowledge of this species in Italy. Full article
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8 pages, 546 KiB  
Communication
The Prevalence of Staphylococcus aureus and the Occurrence of MRSA CC398 in Monkey Feces in a Zoo Park in Eastern China
by Yuanyue Tang, Zhuang Qiao, Zhenyu Wang, Yang Li, Jingwei Ren, Liang Wen, Xun Xu, Jun Yang, Chenyi Yu, Chuang Meng, Hanne Ingmer, Qiuchun Li and Xinan Jiao
Animals 2021, 11(3), 732; https://doi.org/10.3390/ani11030732 - 08 Mar 2021
Cited by 6 | Viewed by 2085
Abstract
Methicillin-resistant Staphylococcus aureus (MRSA) is one of the important antibiotic resistant pathogens causing infections in humans and animals. The increasing observation of MRSA in wildlife species has raised the concern of its impact on animal health and the potential of zoonotic transmission. This [...] Read more.
Methicillin-resistant Staphylococcus aureus (MRSA) is one of the important antibiotic resistant pathogens causing infections in humans and animals. The increasing observation of MRSA in wildlife species has raised the concern of its impact on animal health and the potential of zoonotic transmission. This study investigated the prevalence of S. aureus in fecal samples from non-human primates in a zoo located in Jiangsu, China, in which 6 out of 31 (19.4%) fecal samples, and 2 out of 14 (14.3%) indoor room floor swab samples were S. aureus-positive. The antibiotic susceptibility tests of the eight isolates showed that the two isolates were resistant to both penicillin and cefoxitin, the three isolates were resistant only to penicillin, while three isolates were susceptible to all detected antibiotics. The two isolates resistant to cefoxitin were further identified as MRSA by the presence of mecA. Five different spa types were identified including t034 of two MRSA isolates from Trachypithecus francoisi, t189 of two methicillin-susceptible S. aureus (MSSA) isolates from Rhinopithecus roxellana, t377 of two MSSA isolates from Colobus guereza, and two novel spa types t19488 and t19499 from Papio anubis. Whole genome sequencing analysis showed that MRSA t034 isolates belonged to ST398 clustered in clonal complex 398 (CC398) and carried the type B ΦSa3 prophage. The phylogenetic analysis showed that the two MRSA t034/ST398 isolates were closely related to the human-associated MSSA in China. Moreover, two MRSA isolates contained the virulence genes relating to the cell adherence, biofilm formation, toxins, and the human-associated immune evasion cluster, which indicated the potential of bidirectional transfer of MRSA between monkeys and humans. This study is the first to report MRSA CC398 from monkey feces in China, indicating that MRSA CC398 could colonize in monkey and have the risk of transmission between humans and monkeys. Full article
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15 pages, 2419 KiB  
Article
Is Intestinal Bacterial Diversity Enhanced by Trans-Species Spread in the Mixed-Species Flock of Hooded Crane (Grus monacha) and Bean Goose (Anser fabalis) Wintering in the Lower and Middle Yangtze River Floodplain?
by Zhuqing Yang and Lizhi Zhou
Animals 2021, 11(1), 233; https://doi.org/10.3390/ani11010233 - 19 Jan 2021
Cited by 9 | Viewed by 2481
Abstract
Diversity of gut microbes is influenced by many aspects, including the host internal factors and even direct or indirect contact with other birds, which is particularly important for mixed-species wintering waterbird flocks. In this study, Illumina high-throughput sequencing was used to analyze the [...] Read more.
Diversity of gut microbes is influenced by many aspects, including the host internal factors and even direct or indirect contact with other birds, which is particularly important for mixed-species wintering waterbird flocks. In this study, Illumina high-throughput sequencing was used to analyze the intestinal bacteria of the hooded crane and bean goose whose niches overlap at Shengjin Lake. We tested whether contact time enhances the trans-species spread of gut bacteria. Results indicate alpha-diversity and microbial composition displayed significant separation between the two hosts in every wintering period, although the number of bacteria types shared increased with increasing contact time. For the same species, with the lengthening of contact time, alpha-diversity and the number of operational taxonomic units (OTUs) in the host intestine augmented, and the common OTUs and structural similarity of microflora in the middle and late periods were more than in the early and middle periods. In addition, we found a very high proportion of shared pathogens. Our results indicate that, although intestinal microflora of different species were separated, direct or indirect contact in the mixed-species flock caused the spread of gut bacteria trans-species, indicating that more attention should be paid to intestinal pathogens in wild birds. Full article
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18 pages, 1364 KiB  
Article
Assessment of Risk Factors in Synanthropic and Wild Rodents Infected by Pathogenic Leptospira spp. Captured in Southern Chile
by Jhuliana Luna, Miguel Salgado, Carlos Tejeda, Manuel Moroni and Gustavo Monti
Animals 2020, 10(11), 2133; https://doi.org/10.3390/ani10112133 - 17 Nov 2020
Cited by 5 | Viewed by 2296
Abstract
Leptospirosis is caused by pathogenic Leptospira, and synanthropic and wildlife species of rodents are an important source of infection; however, much of the information about infection progression was obtained from murine models. The aim of this study was to assess infection status [...] Read more.
Leptospirosis is caused by pathogenic Leptospira, and synanthropic and wildlife species of rodents are an important source of infection; however, much of the information about infection progression was obtained from murine models. The aim of this study was to assess infection status and risk factors associated with pathogenic Leptospira in synanthropic and wild rodent species and describe histopathological lesions in several organs from naturally infected animals. In a cross-sectional study, 121 rodents from three synanthropic species and two wild species were trapped in dairy farms in Southern Chile. Liver, heart, kidney, and lungs from trapped animals were fixed in formalin and stained with hematoxylin–eosin. Tissues with lesions consistent with Leptospira infection were tested by immunohistochemistry (IHC) and real-time polymerase chain reaction (qPCR) using the LipL32 antigen. Risk factors were assessed by a conditional mixed-logistic regression model. More than half (56.7%) of the negative reactors to the microscopic agglutination test were identified as infected either by IHC/qPCR. A lower risk of infection compared to the rest of the seasons was found in the fall, and the synanthropic species have a lower risk of infection in comparison with the wildlife species. IHC and qPCR contributed to the identification of pathogenic Leptospira in related histological lesions and 50% more infections than serology. Full article
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8 pages, 561 KiB  
Article
Identification of Hepatitis E Virus in the Feces of Red Foxes (Vulpes vulpes)
by Zsófia Lanszki, Kornélia Kurucz, Safia Zeghbib, Gábor Kemenesi, József Lanszki and Ferenc Jakab
Animals 2020, 10(10), 1841; https://doi.org/10.3390/ani10101841 - 10 Oct 2020
Cited by 6 | Viewed by 2070
Abstract
Orthohepeviruses (HEV) can infect a wide range of animals, showing a relatively strict host specificity; however, its zoonotic potential, natural transmission in the wildlife are less known. Several new HEV-like viruses have been identified in various animal species, including carnivores; however, the phylogenetic [...] Read more.
Orthohepeviruses (HEV) can infect a wide range of animals, showing a relatively strict host specificity; however, its zoonotic potential, natural transmission in the wildlife are less known. Several new HEV-like viruses have been identified in various animal species, including carnivores; however, the phylogenetic relationship among these viruses is poorly resolved, since some of them were known as rodent-related so far. The red fox, the most widespread carnivore worldwide, is a known reservoir of several viruses that transmit from wildlife to humans or domestic animals; they might have a defined role in the circulation of rodent-borne HEV. In this study, we performed a HEV survey by heminested RT-PCR (Reverse Transcription PCR) on red fox fecal samples to investigate the presence of HEV in red foxes living in natural conditions, and to explore the origin of the virus via phylogenetic analysis. Out of the 26 investigated samples, HEV RNA was identified in one sample. Following Sanger sequencing, the novel sequence displayed 91% identity on the nucleotide level with recently published European common vole-HEV derived from Microtus arvalis. In contrast, it shared 85% nucleotide similarity with HEV strains described previously in red foxes. Our results strongly support “the dietary-origin” of unclassified HEV-like strains described from predators that usually prey on rodents. Full article
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16 pages, 5432 KiB  
Communication
A Culture-Based ID of Micromycetes on the Wing Membranes of Greater Mouse-Eared Bats (Myotis myotis) from the “Nietoperek” Site (Poland)
by Rafał Ogórek, Klaudia Kurczaba, Magdalena Cal, Grzegorz Apoznański and Tomasz Kokurewicz
Animals 2020, 10(8), 1337; https://doi.org/10.3390/ani10081337 - 03 Aug 2020
Cited by 6 | Viewed by 3506
Abstract
Bats play important functions in ecosystems and many of them are threatened with extinction. Thus, the monitoring of the health status and prevention of diseases seem to be important aspects of welfare and conservation of these mammals. The main goal of the study [...] Read more.
Bats play important functions in ecosystems and many of them are threatened with extinction. Thus, the monitoring of the health status and prevention of diseases seem to be important aspects of welfare and conservation of these mammals. The main goal of the study was the identification of culturable fungal species colonizing the wing membranes of female greater mouse-eared bat (Myotis myotis) during spring emergence from the “Nietoperek” underground hibernation site by the use of genetic and phenotypic analyses. The study site is situated in Western Poland (52°25′ N, 15°32′ E) and is ranked within the top 10 largest hibernation sites in the European Union. The number of hibernating bats in the winter exceeds 39,000 individuals of 12 species, with M. myotis being the most common one. The wing membranes of M. myotis were sampled using sterile swabs wetted in physiological saline (0.85% NaCl). Potato dextrose agar (PDA) plates were incubated in the dark at 8, 24 and 36 ± 1 °C for 3 up to 42 days. All fungi isolated from the surface of wing membranes were assigned to 17 distinct fungal isolates belonging to 17 fungal species. Penicillium chrysogenum was the most frequently isolated species. Some of these fungal species might have a pathogenic potential for bats and other mammals. However, taking into account habitat preferences and the life cycle of bats, it can be assumed that some fungi were accidentally obtained from the surface of vegetation during early spring activity. Moreover, Pseudogymnoascus destructans (Pd)—the causative agent of the White Nose Syndrome (WNS)—was not found during testing, despite it was found very often in M. myotis during previous studies in this same location. Full article
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10 pages, 250 KiB  
Article
Wild Micromammals as Bioindicators of Antibiotic Resistance in Ecopathology in Northern Italy
by Giovanna Zanardi, Tiziano Iemmi, Costanza Spadini, Simone Taddei, Sandro Cavirani and Clotilde Silvia Cabassi
Animals 2020, 10(7), 1184; https://doi.org/10.3390/ani10071184 - 13 Jul 2020
Cited by 10 | Viewed by 2017
Abstract
Antimicrobial resistance (AMR) is an increasing threat to human health and an important issue also in the natural environment. For this study, an ecopathological approach was applied to the monitoring of the antimicrobial resistance in the province of Parma, Northern Italy. Fourteen monitoring [...] Read more.
Antimicrobial resistance (AMR) is an increasing threat to human health and an important issue also in the natural environment. For this study, an ecopathological approach was applied to the monitoring of the antimicrobial resistance in the province of Parma, Northern Italy. Fourteen monitoring sites and seventy-four faecal samples from four species of wild micromammals (Apodemus sylvaticus, Microtus savii, Mus domesticus and Suncus etruscus) were collected. Samples were subjected to bacteriological examination and antimicrobial susceptibility testing. Antibiotics belonging to 13 different antibiotic classes were tested. Collected data showed a prevalence of multi-drug resistant (MDR) strains of 55.13% and significant differences in the prevalence of MDR strains among the different micromammal species, while sex, age and anthropization level did not significantly affected MDR strains prevalence. Moreover, a high prevalence of bacterial strains resistant to colistin (95%), gentamicin (87%) and amikacin (83%) was observed. To our knowledge, this is the first report on antibiotic resistance in wild micromammals in the province of Parma. Full article
14 pages, 2431 KiB  
Article
Microorganisms Resistant to Antimicrobials in Wild Canarian Egyptian Vultures (Neophron percnopterus majorensis)
by Alejandro Suárez-Pérez, Juan Alberto Corbera, Margarita González-Martín, José Antonio Donázar, Rubén Sebastián Rosales, Manuel Morales and María Teresa Tejedor-Junco
Animals 2020, 10(6), 970; https://doi.org/10.3390/ani10060970 - 03 Jun 2020
Cited by 6 | Viewed by 2450
Abstract
Due to their predatory habits, raptors may serve as indicators of the presence of antimicrobial-resistant bacteria in the environment, but they also represent a public health risk for livestock and humans because they can act as reservoirs, sources and spreaders of these bacteria. [...] Read more.
Due to their predatory habits, raptors may serve as indicators of the presence of antimicrobial-resistant bacteria in the environment, but they also represent a public health risk for livestock and humans because they can act as reservoirs, sources and spreaders of these bacteria. Our objective was to determine the presence of antimicrobial-resistant bacteria in cloacal samples of Canarian Egyptian vultures (Neophron percnopterus majorensis), an endemic bird of prey. One hundred and forty-two cloacal swabs were obtained; Escherichia coli was isolated from 80.28% and Salmonella from 6.3% of these samples. Low levels of susceptibility to ampicillin, tetracycline and trimethoprim/sulfamethoxazole were found. About 20% of the isolates were resistant or presented intermediate susceptibility to fluoroquinolones. Surprisingly, we found isolates resistant to imipenem (6.96%). Isolates from chicks were more susceptible to antimicrobial drugs than adult and immature birds. About 50% of E. coli isolates were resistant to ampicillin, tetracycline and trimethoprim/sulfamethoxazole, and about 20% to piperacillin, enrofloxacin and marbofloxacin. High percentages of isolates of Salmonella were found to be resistant to cephalexin (88%) and aminoglycosides (greater than 77%). Our results support the idea that raptors could act as reservoirs of Salmonella and antimicrobial-resistant bacteria, posing a risk not only to wildlife but also to livestock and the human population, thus reinforcing the need to minimize the exposure of wildlife to antimicrobial agent through human and livestock waste. Full article
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15 pages, 647 KiB  
Article
Salmonella in Free-Ranging Quokkas (Setonix brachyurus) from Rottnest Island and the Mainland of Western Australia
by Pedro Martínez-Pérez, Timothy H. Hyndman and Patricia A. Fleming
Animals 2020, 10(4), 585; https://doi.org/10.3390/ani10040585 - 31 Mar 2020
Cited by 6 | Viewed by 3920
Abstract
Salmonella is a genus of Gram-negative, motile, and facultative anaerobic bacteria with a worldwide distribution that contaminates multiple substrates (vegetation, food, soil, and water) and inhabits the gastrointestinal tract of birds, reptiles, and mammals, including humans. Rottnest Island is a popular tourist destination [...] Read more.
Salmonella is a genus of Gram-negative, motile, and facultative anaerobic bacteria with a worldwide distribution that contaminates multiple substrates (vegetation, food, soil, and water) and inhabits the gastrointestinal tract of birds, reptiles, and mammals, including humans. Rottnest Island is a popular tourist destination and is abundantly inhabited by quokkas (Setonix brachyurus), a charismatic small wallaby. Current data on the association between Salmonella and quokkas on Rottnest Island are outdated by approximately 30 years. Additionally, previous studies on quokkas on this island and mainland Western Australia did not perform physical examinations or any diagnostic tests. The aim of the project was to assess the prevalence of Salmonella spp. in quokkas from Rottnest Island and mainland Western Australia and correlate the presence of the bacterium with the health of the animal. Ninety-two quokkas from Rottnest Island (n = 71) and populations on the mainland (n = 21) were screened for Salmonella, and a prevalence of 47.9% and 4.8%, respectively, was determined. A total of 16 serovars were identified from 37 isolates; five of these serovars had previously not been described in the quokka. Salmonella appeared to have an effect on the haematology and blood chemistry of quokkas on Rottnest Island consistent with subclinical salmonellosis. The health of Rottnest Island quokkas, and their potential impact on the health of the visitors to the island, should continue to be monitored carefully. Full article
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10 pages, 583 KiB  
Brief Report
Biopsy and Tracheobronchial Aspirates as Additional Tools for the Diagnosis of Bovine Tuberculosis in Living European Bison (Bison bonasus)
by Anna Didkowska, Blanka Orłowska, Lucjan Witkowski, Katarzyna Olbrych, Sylwia Brzezińska, Ewa Augustynowicz-Kopeć, Monika Krajewska-Wędzina, Andrzej Bereznowski, Wojciech Bielecki, Michał Krzysiak, Alicja Rakowska, Wanda Olech, Michele A. Miller, Wade R. Waters, Konstantin P. Lyashchenko and Krzysztof Anusz
Animals 2020, 10(11), 2017; https://doi.org/10.3390/ani10112017 - 02 Nov 2020
Cited by 14 | Viewed by 2482
Abstract
The diagnosis of bovine tuberculosis (BTB) in living wildlife remains a complex problem, and one of particular importance in endangered species like European bison (Bison bonasus). To identify infection and avoid the unnecessary culling of such valuable individuals, current best practice [...] Read more.
The diagnosis of bovine tuberculosis (BTB) in living wildlife remains a complex problem, and one of particular importance in endangered species like European bison (Bison bonasus). To identify infection and avoid the unnecessary culling of such valuable individuals, current best practice requires the collection and culture of material from living animals, as mycobacteria isolation remains the gold standard in BTB diagnosis. However, such isolation is challenging due to the need for the immobilization and collection of appropriate clinical material, and because of the sporadic shedding of mycobacteria. In the present study, we evaluated the potential of sampling for the detection of BTB in a group of seven living European bison suspected of being infected with Mycobacterium caprae. The specimens were collected both as swabs from the nasal and pharyngeal cavities, tracheobronchial aspirates (TBA), ultrasound-guided biopsies from lateral retropharyngeal lymph nodes, and post mortem, from mandibular, retropharyngeal and mediastinal lymph nodes. Clinical samples were tested for mycobacterial species via mycobacteriological culture and PCR. M. caprae was isolated from collected material in two out of four living infected individuals (TBA, biopsy) and mycobacterial DNA was detected in three out of four (TBA, pharyngeal swab) bison. This is the first report of isolation of M. caprae in living European bison. Our findings demonstrate the value of diagnostic tests based on both molecular testing and culture in European bison and confirm the respiratory shedding of viable M. caprae in this host species. Full article
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6 pages, 1529 KiB  
Technical Note
Fecal Sample Collection Method for Wild Birds-Associated Microbiome Research: Perspectives for Wildlife Studies
by Luca Borrelli, Adriano Minichino, Antonino Pace, Ludovico Dipineto and Alessandro Fioretti
Animals 2020, 10(8), 1349; https://doi.org/10.3390/ani10081349 - 04 Aug 2020
Cited by 4 | Viewed by 4890
Abstract
Gut microbial communities play important roles in host health, modulating development, nutrient acquisition, immune and metabolic regulation, behavior and diseases. Wildlife microbiome studies and host–microbe interaction and exploration might be an important goal for evolutionary biology, conservation, and ecology. Therefore, collection and sampling [...] Read more.
Gut microbial communities play important roles in host health, modulating development, nutrient acquisition, immune and metabolic regulation, behavior and diseases. Wildlife microbiome studies and host–microbe interaction and exploration might be an important goal for evolutionary biology, conservation, and ecology. Therefore, collection and sampling methods must be considered before choosing a microbiome-based research plan. Since the fecal microbial community reflects the true gut community better than that of cloacal swab samples and only few nondestructive methods have been described, we propose an easy-to-build box for a noninvasive fecal collection method. The main components of the collection box include a plastic storage box, a plastic tray, a vinyl-coated hardware cloth, and a 10% bleach solution. In the plastic box, the tray is positioned under the raised grate, where the bird is placed, to reduce the risk of contamination of the fecal samples. This procedure could simplify handling and processing phases in wild birds or other animals. It might represent a cheap and useful method for research studies, wildlife rescue center activities, veterinary practices, and conservation practitioners. Full article
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