Smart carnivores think twice: Red fox delays scavenging on conspecific carcasses to reduce parasite risk

M.M. was supported by a research contract Ramon y Cajal from the MINECO (RYC-2015-19231) . This study was partly funded by the Spanish Ministry of Economy, Industry and Competitiveness and EU ERDF funds through the project CGL2017-89905-R.The recent SARS-CoV-2 epidemic has highlighted the need to prevent emerging and re-emerging diseases, which means that we must approach the study of diseases from a One Health perspective. The study of pathogen transmission in wildlife is challenging, but it is unquestionably key to understand how epidemiological interactions occur at the wildlife-domestic-human interface. In this context, studying parasite avoidance behaviours may provide essential insights on parasite transmission, host-parasite coevolution, and energy flow through food-webs. However, the strategies of avoiding trophically transmitted parasites in mammalian carnivores have received little scientific attention. Here, we explore the behaviour of red foxes (Vulpes vulpes) and other mammalian carnivores at conspecific and heterospecific carnivore carcasses using videos recorded by camera traps. We aim to determine 1) the factors influencing the probability of foxes to practice cannibalism, and 2) whether the scavenging behaviour of foxes differ when facing conspecific vs. heterospecific carcasses. We found that red foxes were generally reluctant to consume mesocarnivore carrion, especially of conspecifics. When recorded, consumption by foxes was delayed several days (heterospecific carcasses) or weeks (conspecific carcasses) after carcass detection. Other mammalian scavengers showed a similar pattern. Also, meat-borne parasite transmission from wild carnivore carcasses to domestic dogs and cats was highly unlikely. Our findings challenge the widespread assumption that cannibalistic or intra-specific scavenging is a major transmission route for Trichinella spp. and other meat-borne parasites, especially for the red fox. Overall, our results suggest that the feeding decisions of scavengers are probably shaped by two main contrasting forces, namely the nutritional reward provided by carrion of phylogenetically similar species and the risk of acquiring meat-borne parasites shared with these species. This study illustrates how the detailed monitoring of carnivore behaviour is essential to assess the epidemiological role of these hosts in the maintenance and dispersion of parasites of public and animal health relevance.MINECO RYC-2015-19231Spanish Ministry of Economy, Industry and CompetitivenessEuropean Commission CGL2017-89905-

Assessing DESS solution for the long-term preservation of nematodes from faecal samples

Preservation of biological samples is a relevant issue for many scientific disciplines. Although traditional preservers, such as formaldehyde or ethanol, imply major disadvantages related to health risks, DNA degradation and distortion of structures, they are widely used. Hence, the search for viable alternatives preserving morphometry and genetics seems necessary. Here we assess the suitability of DESS solution to preserve adult nematodes and their eggs in faeces. Concretely, faecal samples of terrestrial tortoises with oxyurids were used to: (i) compare the 1-month storage efficacy of eggs from different conservation protocols (faeces without preserver at -20 °C, faeces with DESS solution at room temperature, faeces with DESS solution at -20 °C and faeces with ethanol 70% at room temperature); (ii) address morphological nematode identification after 2 years of storage with DESS. We also corroborated that nematode DNA remained viable after 2 years. Overall, our results showed that DESS solution at room temperature is an advisable alternative to conserve both parasite eggs and adult nematodes for morphological identification and genetic purposes. It also offers the advantages of being low-cost, safe and suitable for fieldwork conditions and shipments without refrigeration for nematode preservation.MG was supported by a contract for postdoctoral researchers from the Generalitat Valenciana with reference APOSTD/2021/181. RCRC was supported by the European Union-Next Generation EU in the Maria Zambrano Program (ZAMBRANO 21-26). This research had the financial support of project PID2019-105682RA-I00, funded by the Spanish Ministry of Science and Innovation MCIN/AEI/10.13039/501100011033

Helmintos gastrointestinales en liebres (Lepus granatensis) del sureste de la Península Ibérica

The abdominal cavity and digestive organs of 85 Iberian hares (Lepus granatensis) from the Altiplano of the Region of Murcia (southeastern Spain) were studied. The overall prevalence of helminths was 87.7%, including nematodes (82.2% of prevalence), metacestodes (44.7%) and adult cestodes (5.9%). Three nematode species were found: Nematodiroides zembrae (78.8%), Passalurus ambiguus (9.4%) and Trichostrongylus retortaeformis (2.4%), while two cestode species were detected: Cittotaenia denticulata (5.9%) and Cysticercus pisiformis (44.7%). Our results show a positive relationship between N. zembrae intensity and the presence of C. pisiformis.La liebre ibérica (Lepus granatensis) es un mamífero ubicuo en la península ibérica con importantes implicaciones ecológicas y económicas. Para conocer el estatus sanitario de esta especie, se han estudiado la cavidad abdominal y órganos del aparato digestivo de 85 liebres ibéricas procedentes del Altiplano de la Región de Murcia (sureste de España). La prevalencia total de helmintos hallada fue del 87,7%, siendo la prevalencia de nematodos del 82,2%, la de metacestodos del 44,7% y, en el caso de las formas adultas de cestodos, del 5,9%. Las especies de nematodos encontradas fueron Nematodiroides zembrae (78.8%), Passalurus ambiguus (9,4%) y Trichostrongylus retortaeformis (2,4%), en tanto que las especies de cestodos detectadas fueron Cittotaenia denticulata (5,9%) y Cysticercus pisiformis (44,7%). Los resultados obtenidos demuestran la existencia de una relación positiva entre la intensidad de parasitación de N. zembrae y la presencia de C. pisiformis

El papel de los cadáveres de carnívoros silvestres en la transmisión de agentes infectocontagiosos: aspectos epidemiológicos y ecológicos

Esta tesis doctoral profundiza en las consecuencias epidemiológicas de las interacciones entre la fauna silvestre y los cadáveres de mamíferos carnívoros en tres zonas montañosas del sureste de España. Además, se evalúa el grado de interdisciplinaridad, el uso de terminología ecológica y los argumentos que sustentan la transmisión trófica de patógenos en estudios en la interfaz silvestre-doméstico-humano. En el Capítulo 1 realizamos una revisión sistemática para conocer el estado actual del conocimiento sobre la transmisión de parásitos por consumo de carne en la interfaz silvestre-doméstico-humano. También evaluamos el grado de interdisciplinaridad de los equipos de investigación y la precisión en el uso de términos ecológicos, así como la base científica de los argumentos que sustentaron las conclusiones epidemiológicas. La mayoría de los artículos justificaron la transmisión trófica de parásitos utilizando exclusivamente referencias bibliográficas o afirmaciones sin base científica. Además, los términos ecológicos en muchas publicaciones estaban ausentes y, cuando se mencionaban, solían ser imprecisos o incorrectos. Esta falta de precisión y rigor puede deberse a que las publicaciones han sido mayoritariamente realizadas por equipos unidisciplinares. Estos resultados remarcan la necesidad de establecer colaboraciones entre investigadores formados en Ecología y Epidemiología en estudios epidemiológicos en la interfaz silvestre-doméstico-humano. En los Capítulos 2 y 3 investigamos el comportamiento de los vertebrados ante cadáveres de carnívoros, con especial atención a la interacción entre el zorro rojo (Vulpes vulpes) y los cadáveres de congéneres para la transmisión de parásitos vía trófica y no trófica. Se monitorizaron 56 cadáveres de zorro y 10 de otros mesocarnívoros durante 7-10 semanas utilizando cámaras trampa en tres zonas montañosas del sureste de España, con diferentes comunidades de vertebrados y grados de antropización. Los zorros fueron muy eficientes en detectar la carroña de mesocarnívoro. No obstante, el comportamiento generalizado consistió en evitar el consumo o retrasarlo varias semanas, sobre todo entre congéneres. Las especies carroñeras contactaron más frecuentemente con los cadáveres, probablemente por sus hábitos alimenticios. En cuanto a los eventos de zorros, el contacto fue más frecuente y temprano en cadáveres heteroespecíficos, retrasándose varias semanas en congéneres. Para el frotamiento se observó un patrón similar entre ambos tipos de carroña, aunque la frecuencia fue mayor en cadáveres de zorro. En cambio, el marcaje fue más frecuente en cadáveres de congéneres, probablemente porque son utilizados como puntos de información de larga persistencia. Nuestros resultados sugieren que la decisión de consumir cadáveres de congéneres está probablemente condicionada por dos fuerzas contrarias: el alto valor nutritivo de los congéneres y el riesgo de adquirir parásitos. Demostramos que la carroña de carnívoro es un componente fundamental en el "paisaje de la aversión" de los carnívoros. En relación con las interacciones no tróficas, los zorros evitaron el contacto temprano con la carroña probablemente para reducir el riesgo de infección por parásitos de transmisión no trófica, especialmente en congéneres. Sin embargo, el estrecho contacto causado por el frotamiento puede jugar un papel importante en la transmisión de ectoparásitos. Los eventos de marcaje también podrían suponer un riesgo epidemiológico en los lugares donde se encuentran los cadáveres, ya que algunos patógenos excretados por orina y heces pueden permanecer en el cadáver o en sus inmediaciones durante mucho tiempo. Por ello, la estrategia del zorro para reducir el riesgo de infección parece ineficaz frente a algunos parásitos de transmisión no trófica. En general, esta tesis doctoral proporciona un conocimiento detallado de las interacciones ecológicas entre la carroña de carnívoro y los vertebrados. Esta información es una base fundamental para inferir las consecuencias epidemiológicas derivadas de estas relaciones. Además, animamos a incrementar las colaboraciones interdisciplinares en estudios epidemiológicos en la interfaz silvestre-doméstico-humano desde una perspectiva One Health.This PhD dissertation has delved into the epidemiological consequences of interactions between wildlife and mammalian carnivore carcasses in three mountainous areas of southeastern Spain. Moreover, the degree of interdisciplinarity, the use of ecological terminology and the arguments supporting the trophic transmission of pathogens in studies at the wildlife-livestock-human interface have been evaluated. In Chapter 1 we conducted a systematic review to address the current state of knowledge about parasite transmission by meat consumption at the wildlife-livestock-human interface. Also, we evaluated the degree of interdisciplinarity of the research teams and the accuracy in the use of ecological terms, just as the scientific reliability of arguments used to support the epidemiological conclusions. Most of the articles justified the trophic transmission of parasites using exclusively bibliographic references or non-science-based assertions. Besides, ecological terms in many publications were absent and, when mentioned, were mainly inaccurate or misused. This lack of precision and rigor may be due because scientific publications are mostly carried out by unidisciplinary research teams. These results highlight the need to establish collaborations between researchers trained in Ecology and Epidemiology in epidemiological studies at the wildlife-livestock-human interface. In Chapter 2 and 3 we investigated the behavior of vertebrates at carnivore carcasses, with special focus on interaction between red fox (Vulpes vulpes) and conspecific carrion for the transmission of meat-borne and non-trophically transmitted parasites. For this, 56 fox carcasses and 10 carcasses of other mesocarnivore species were monitored for 7-10 weeks using camera traps in three mountainous areas of southeastern Spain, with different community of vertebrates and degrees of anthropization. Foxes were very efficient in detecting mesocarnivore carrion. Notwithstanding, the widespread behavior consisted of avoiding consumption or delaying it several weeks, especially at conspecific carcasses. Scavenger species contacted more frequently with carcasses than non-scavengers, probably as a result of their scavenging habits. Regarding fox, contact occurred more frequently and earlier at heterospecific carcasses, being delayed several weeks at fox carcasses. In relation to rubbing, a similar pattern was observed for both type of carrion, although its frequency was greater at conspecific carcasses. Instead, marking behavior was most frequently recorded at fox carcasses, probably because they are used as information points of longer persistence. Our results suggest that the decision to consume conspecific carrion is probably conditioned by two contrasting forces: the high nutritional value of conspecifics and the risk of acquiring shared parasites. We demonstrate that carnivore carrion is a fundamental component in the "landscape of disgust" of carnivores. Related to non-trophic interactions, foxes avoided the early contact with carrion, probably to reduce the risk of infection by non-trophically transmitted parasites, especially in conspecific carcasses. However, close contact caused by rubbing could play an important role in the transmission of ectoparasites. Marking events also may pose an epidemiological risk in carcass sites, since pathogens excreted by urine and feces could be present on the carcass or its vicinities for a long time. Consequently, the fox’ strategy to reduce the risk of infection seems ineffective for some non-trophically transmitted parasites. In general, this doctoral thesis provides a detailed knowledge about the ecological interactions between carnivore carrion and vertebrate wildlife. This information is a fundamental basis for inferring the epidemiological consequences derived from these relationships. Moreover, we encourage the increase of interdisciplinary collaboration in epidemiological studies at the wildlife-livestock-human interface from a One Health perspective

What do we know about Angiostrongylus cantonensisin Spain? Current knowledge and future perspectives in a globalized world

© 2021 Wiley-VCH GmbH. This document is made available under the CC-BY-NC-ND 4.0 license http://creativecommons.org/licenses/by-nc-nd/4.0/ This document is the published version of a published Work that appeared in final form in Transboundary and Emerging Diseases. To access the final edited and published work see https://doi.org/10.1111/tbed.14393Angiostrongylus cantonensis is an important emerging and zoonotic nematode that has been reported worldwide since its first description in Asia 86 years ago. Among places where this parasite has been recently described, insular regions of northwest Africa seem to be particularly relevant. We performed a systematic review in scientific databases to search and extract information about all reports describing cases of A. cantonensis in Spain until July 2021. As a result, seven surveys about the presence of this pathogen in Spanish insular regions were found, especially in the Canary Islands, as well as a non-autochthonous report of A. cantonensis in the mainland Spain. The lack of reliable information about the presence or absence of this nematode in the Iberian Peninsula highlights the need for further studies concerning this emerging pathogen since rodents acting as competent definitive hosts of A. cantonensis are widely distributed in the mainland. Moreover, the high maritime traffic daily registered in Spanish ports could be a main entrance pathway for A. cantonensis or its intermediate hosts in the country due to the frequent and direct connection between these points and regions where this pathogen is endemic. We encourage to focus further efforts on investigating the current epidemiological situation of A. cantonensis in the Iberian Peninsula, just as in other Mediterranean countries with similar epidemiological, ecological and geographical characteristics. In this sense, the relevant implications of this parasite for animal and public health make necessary to act integrating different viewpoints under the One Health perspectiv

El papel de los centros zoológicos como reservorios de leishmaniosis en áreas urbanas

A questionnaire to evaluate the importance of Leishmaniosis in zoological centers was designed to gather information about suspected and confirmed clinical cases of the disease. The questionnaire was sent to members of the Iberian Association of Zoos and Aquariums (n=38). Although a limited response (26.32%) was obtained three suspected and three verified cases were reported suggesting Leishmaniosis is a disease of little relevance in zoos. A further study was carried out to analyze the presence and persistence of infected animals and vectors in Oasys zoological center in southeast Spain where a wolf with leishmaniosis was diagnosed eight years before. RealTime PCR from skin biopsies of eight carnivorous was performed and fifty percent (n=4) were positive (three swift foxes (Vulpes velox) and one tiger Panthera tigris). Furthermore, 70 sand flies were captured using castor-oil sticky interception traps and were identified using morphological and DNA barcoding methods as Phlebotumus perniciosus (76.90%), P. papatasi (12.30%), Sergentomyia minuta (7.60%) and P. ariasi (3%). Sand fly abundance was greatest in areas protected from direct sunlight. Our results suggest that animals in zoological centers could be reservoirs of Leishmania spp. However more studies are needed to assess the epidemiological implications of these presumed hosts.Se diseñó un cuestionario que requería información sobre casos sospechosos y confirmados para evaluar la importancia de la leishmaniosis en los centros zoológicos. Las encuestas enviadas a los miembros de la Asociación Ibérica de Zoos y Acuarios obtuvieron una respuesta escasa (26.32%), con sólo tres informes de casos sospechosos y tres de casos confirmados. Estos datos parecen constatar la escasa relevancia de esta enfermedad en zoológicos. Con el fin de detectar la presencia/persistencia de animales infectados y de vectores en centros zoológicos situados en zonas endémicas en los que se hayan detectado infecciones sintomáticas, se realizó el presente estudio en Oasys, un zoológico en el sureste de España, y en el que se diagnosticaron casos de leishmaniosis ocho años atrás. Se realizaron PCR en tiempo real de biopsias de piel obtenidas de ocho carnívoros, de los que el 50% de ellos (n=4) resultaron positivos (tres zorros swift (Vulpes velox) y un tigre (Phantera tigris). Por otra parte, se capturaron flebotomos mediante trampas de intercepción. Se emplearon estudios morfológicos y ADN barcoding para identificar las especies. Se encontraron P. perniciosus (7.90%), P. papatasi (12.30%), S. minuta (7.60%) y P. ariasi (3%), evidenciando además una cantidad de flebotomos mayor en espacios cubiertos. Cuando se evaluaron los factores de riesgo, las zonas sin exposición directa a luz solar presentaron una mayor abundancia de flebotomos. Nuestros resultados sugieren que los animales en los centros zoológicos podrían suponer un reservorio de Leishmania spp. Sin embargo, se necesitan más estudios para evaluar las implicaciones epidemiológicas de estos presuntos hospedadores

Gastrointestinal helminths in hares (Lepus granatensis) in the southeast of the iberian peninsula

La liebre ibérica (Lepus granatensis) es un mamífero ubicuo en la península ibérica con importantes impli-caciones ecológicas y económicas. Para conocer el estatus sanitario de esta especie, se han estudiado la cavidad abdominal y órganos del aparato digestivo de 85 liebres ibéricas procedentes del Altiplano de la Región de Murcia (sureste de España). La prevalencia total de helmintos hallada fue del 87,7%, siendo la prevalencia de nematodos del 82,2%, la de metacestodos del 44,7% y, en el caso de las formas adultas de cestodos, del 5,9%. Las especies de nematodos encontradas fueron Nematodiroides zembrae (78.8%), Passalurus ambiguus (9,4%) y Trichostrongylus retortaeformis (2,4%), en tanto que las especies de cestodos detectadas fueron Cittotaenia denticulata (5,9%) y Cysticercus pisiformis (44,7%). Los resultados obtenidos demuestran la existencia de una relación positiva entre la intensidad de parasitación de N. zembrae y la presencia de C. pisiformis.Palabras clave: Lagomorfo, nematodos, cestodos, Murcia, EspañaThe abdominal cavity and digestive organs of 85 Iberian hares (Lepus granatensis) from the Altiplano of the Region of Murcia (southeastern Spain) were studied. The overall prevalence of helminths was 87.7%, including nematodes (82.2% of prevalence), metacestodes (44.7%) and adult cestodes (5.9%). Three nema-tode species were found: Nematodiroides zembrae (78.8%), Passalurus ambiguus (9.4%) and Trichostron-gylus retortaeformis (2.4%), while two cestode species were detected: Cittotaenia denticulata (5.9%) and Cysticercus pisiformis (44.7%). Our results show a positive relationship between N. zembrae intensity and the presence of C. pisiformis

Plastinated macroparasites, an alternative resource for use in practical lessons

© 2020. OIE.. This document is made available under the CC-BY-NC-ND 4.0 license http://creativecommons.org/licenses/by-nc-nd/4.0/ This document is the published version of a published Work that appeared in final form in Revue scientifique et technique - Office international des épizooties,.The plastination technique is a recently developed option to preserve biological tissues widely used in human and veterinary anatomy. This process allows one to obtain real, safe, clean, dry, resistant and permanently stable material without any additional treatment or maintenance. All these advantages are associated with the rapid expansion of plastination during recent decades in a high number of educational institutions. However, the studies of parasite conservation through plastination are scarce, although the material obtained has a high quality, as prior references have shown. In this study, 141 students of veterinary medicine and pharmacy university degrees used, in a blind study, plastinated specimens (experimental group) or wet specimens (control group) during three consecutive practical sessions. Afterwards all the students completed anonymous questionnaires on both knowledge and satisfaction. The results demonstrated that plastinated parasites are a valid and satisfactory alternative to be used as a teaching/learning tool during practical lessons. Moreover, with regard to the knowledge of morphological structures, the results from the questionnaire of assimilated knowledge showed no differences between the use of plastinated and formaldehyde-preserved parasite

Exposure to severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) in the endangered Iberian lynx (Lynx pardinus)

The severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) is an emerging zoonotic virus of public and animal health concern, of which felids have been suggested as potential reservoirs. Although SARS-CoV-2 exposure has been detected in domestic and wild captive animals belonging to Felidae family, surveillance has not been carried out in free-ranging wild felids so far. The aim of the present study was to assess SARS-CoV-2 exposure in the Iberian lynx (Lynx pardinus), the most endangered felid in the world. Between 2019 and 2022, we conducted a seroepidemiological study of SARS-CoV-2 in 276 free-ranging and captive Iberian lynxes. Our results evidenced limited (0.4%; 95%CI: 0.0–1.1) but not negligible exposure to this emerging virus in this endangered felid species, increasing the SARS-CoV-2 host range. The circulation of this virus in wildlife evidences the need of integrated European wildlife monitoring.This study is part of the TED2021-132599B-C22 project, funded by MCIN/AEI/10.13039/501100011033 and by the European Union "NextGenerationEU"/PRTR. Recovery, Transformation and Resilience Plan - Funded by the European Union - NextGenerationEU. It was also partially funded by the research project LifeWATCH INDALO - Scientific Infrastructures for Global Change Monitoring and Adaptation in Andalusia (LIFEWATCH-2019-04-AMA-01), financed with FEDER funds (POPE 2014-2020). This research was also partially supported by the Galileo Innovation and Transfer Plan of the University of Cordoba (UCO-SOCIAL-INNOVA) and CIBER -Consorcio Centro de Investigacion Biomedica en Red- (CB 2021/13/00083), Instituto de Salud Carlos III, Ministerio de Ciencia e Innovacion and Union Europea – NextGenerationEU. The authors also acknowledge the crowdfunding initiative #Yomecorono, available online at: https://www.yomecorono.com (accessed on 8 August 2021). IRTA is supported by CERCA Programme/ Generalitat de Catalunya. M. Gonzalvez was supported by a postdoctoral contract Margarita Salas (University of Murcia) from the Program of Requalification of the Spanish University System (Spanish Ministry of Universities) financed by the European Union-NextGenerationEU. J. Caballero-Gomez was supported by the CIBER -Consorcio Centro de Investigacion Biomedica en Red-(CB21/13/00083), Instituto de Salud Carlos III, Ministerio de Ciencia e Innovacion and Union EuropeaNextGenerationEU. We are grateful to Raúl García-San Pedro, (OAPN, Centro de Cría en cautividad de lince iberico de Zarza de Granadilla), Mª Teresa Ríos-Moya, (TRAGSATEC, Centro de cría en cautividad de lince iberico de Zarza de Granadilla) and Arnau Vedrell-Mir, (TRAGSATEC, Centro de Cría en cautividad de lince iberico de Zarza de Granadilla) for their support during this study. Funding for open access charge: Universidad de Cordoba/ CBUA.info:eu-repo/semantics/publishedVersio