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The Effect of Livestock on the Physiological Condition Of www.nature.com/scientificreports OPEN The efect of livestock on the physiological condition of roe deer (Capreolus capreolus) is modulated by habitat quality Fernando Horcajada-Sánchez 1*, Gema Escribano-Ávila2, Carlos Lara-Romero 3, Emilio Virgós3 & Isabel Barja4,5 Free-range livestock grazing is a widespread human activity that not only modifes natural vegetation but also leads to interactions with wild ungulates. Most commonly, the interactions between cattle and wild ungulates have been studied with a focus on competition for high-quality forage. However, other mechanisms, such as the risk of parasite infection, might better describe this interaction. We aim to determine whether livestock afect roe deer (Capreolus capreolus Linnaeus, 1758) by reducing habitat quality and increasing the probability of infection by shared parasites. We measured noninvasive fecal cortisol metabolites as an indicator of habitat quality as well as the lung nematode larvae burden from the Dictyocaulus genus. A higher Dictyocaulus larvae load was found in the presence of livestock in pines, and feces collected in winter had a higher parasite load than feces collected in autumn. Additionally, fecal cortisol metabolite levels in the roe deer were afected by the interaction between habitat quality and livestock presence and were higher in the poorest habitat and when living in sympatry with cattle. Our results suggest that physiological stress responses in roe deer were mediated by the habitat type and the presence of competitors. The long-term implications of altered physiological responses such as those demonstrated here should be considered in management strategies for deer. Habitat loss, fragmentation and degradation are among the main causes of the biodiversity crisis. Because hab- itat alterations are associated with changes in the spatiotemporal availability of key resources for animals, these changes can produce strong consequences in the life history of animals (e.g., food, cover, refuges and nesting sites)1. Free-range livestock grazing, also known as extensive grazing, is one of the most common and widespread human activities throughout the world and greatly modifes the natural vegetation structure and composition. Livestock forage according to their food preferences and plant availability2. Generally, they prefer to graze on highly nutritious forbs, generating a high impact in pasture communities, but livestock also consume shrubs, afecting the understory cover3. Even a low level of livestock grazing can contribute to a decrease in food resources for wild ungulates (but could also lead to an increase in or a neutral efect on food resources)4. During winter and early spring (i.e., peri- ods of reduced forage availability) in mountain areas, the efect of livestock grazing can be particularly negative, as this is a period of higher starvation risk for wild ungulates5. During these seasons, the diets of livestock and wild ungulates present a strong overlap4 (and references therein), leading to food depletion for wild ungulates, which is a form habitat degradation. Several studies report behavioral variations in wild ungulates, such as the avoidance of areas used by livestock, probably due to competition for food resources, as previously mentioned6,7. However, additional mechanisms, 1Centro de Investigación, Seguimiento y Evaluación, Parque Nacional de la Sierra de Guadarrama, Ctra. M-604, km 28, 28740, Rascafría, Madrid, Spain. 2Departamento de Ciencias Naturales, Universidad Técnica Particular de Loja, San Cayetano Alto s/n, Marcelino Champagnat, Loja, Ecuador. 3Área de Biodiversidad y Conservación, Escuela Superior de Ciencias Experimentales y Tecnología, Universidad Rey Juan Carlos, Departamental 1, C/Tulipán s/n, 28933, Móstoles, Madrid, Spain. 4Unidad de Zoología, Departamento de Biología, Facultad de Ciencias, Universidad Autónoma de Madrid. C/Darwin 2. Campus Universitario de Cantoblanco, km 15, 28049, Madrid, Spain. 5Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM), Universidad Autónoma de Madrid, C/Darwin 2, 28049, Madrid, Spain. *email: [email protected] SCIENTIFIC REPORTS | (2019) 9:15953 | https://doi.org/10.1038/s41598-019-52290-7 1 www.nature.com/scientificreports/ www.nature.com/scientificreports Model S L H E adj.R2 df logLik AICc ΔAICc Wi 6 + + 0.15 4 −160.069 328.5 0 0.32 8 + + + 0.16 5 −159.292 329.1 0.62 0.24 14 + + + 0.15 5 −159.808 330.1 1.66 0.14 W+ 1 1 0.34 0.2 Table 1. Te highest-ranked linear models using AICc-based model selection for Dictyocaulus larvae load. S: season; L: livestock presence/absence; H: Habitat; E: Elevation. Wi: Akaike weight, W+: relative importance of variables. See Table S2 for a complete description of the candidate models considered. such as the reduced risk of parasite infection and transmission, may explain such changes in the behavior of wild ungulates8. Parasite transmission rate is a density-dependent process; therefore, for parasites that are shared between wild ungulates and livestock, a larger amount of parasites are expected to be available to infect animals in the presence of livestock. Tus, wild ungulates that feed in areas shared with livestock may face a higher risk of parasitic infection, leading to an increased parasite load9. When parasite loads are below a certain threshold and/ or animals are in good body condition, increased parasite loads may not afect animals’ capacity of survival or reproduction10. However, in other cases, a higher parasite load could dramatically reduce the survival probabili- ties of the animals11,12. Accordingly, to fully understand the relationships of livestock and wild ungulates living in sympatry, not only competition for food resources but also other mechanisms such as parasite infection should be taken into account. Te measurement of stress levels indexed by fecal cortisol metabolites (FCM) has been used in a range of studies to infer environmental factors that may harm ftness, including poor habitat quality or habitat degra- dation13 (for a review). FCM are the result of the activation of the hypothalamic-pituitary-adrenal axis (HPA). When an animal perceives a stressor, its HPA activates, generating a cascading efect from the brain to the adrenal system. Tis reaction produces an increase in cortisol levels (generally cortisol or corticosterone depending on the species), thereby leading to an increase in glucose availability to help the animals overcome the stressful sit- uation14–16. However, prolonged exposure to stressors, such as reduced or poor forage quality, causes increased levels of glucocorticoids in the long term, which leads to ‘chronic stress’17. Under these conditions, detrimental efects such as depressed immune responses, reduced reproductive success, suppressed growth, and decreased survival have been observed15–18. According to previous studies, the presence of livestock in the habitat of wild ungulates may lead to increased stress levels as a result of habitat quality reduction that are detectable by means of measuring FCM19,20. Additionally, an increased parasite load in wild ungulates could be expected in the presence of livestock owing to higher levels of cross-transmitted parasites. Parasite load itself can be an additional stressor21, but increased stress levels may also lead to a poorer performance of the immune function, compromising the capacity of wild ungu- lates to control parasite infections22. Unfortunately, the relationship between stress levels and immune function (that condition parasite load and its consequences on animal health) are far from clear. Detrimental, positive and neutral efects of stress levels on immune function have been found depending on genetic factors, social status and duration of stress23 (for a review). In this study, the aim was to evaluate the efect of livestock on wild ungulate stress levels and parasite load. Among ungulates, the roe deer (Capreolus capreolus Linnaeus, 1758) is a typical species in the pine and oak habitats forested in the study area in both the presence and absence of livestock. Tus, we indexed stress levels by measuring FCM and the lung nematode load from the genus Dictyocaulus. Cross-transmission between domes- tic ruminants and roe deer through ingesting larvae of lung nematodes has been reported in previous studies24. We performed this study during the forage-limited seasons, and we used two habitats of roe deer that difer in forage quality. Oak forests are a superior habitat compared with pine forests due to their better thermal coverage and more dense and diverse understory (oak forests have a higher abundance of legume and bramble species)20. Legumes and brambles are preferred by the roe deer and have been previously related to better body condi- tion25,26. In a previous study, several parasite genera were found to be more common in the presence of livestock in pines, which is a poorer habitat than oaks24; however, the study did not provide further information on roe deer body condition or physiological status. Here, we frst evaluate how the presence of livestock may afect the parasite load of the Dictyocaulus genus, many species of which are known to be cross-transmitted between livestock (Bus taurus) and roe deer27,28. Second, we evaluate how parasite load may afect stress levels of roe deer, in addition to habitat quality and the presence of livestock, in two seasons that vary in their capacity to provide food resources. We hypothesize a higher Dictyocaulus larvae load and higher stress levels in the presence of livestock
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