Introduction
Large carnivores play an important role in ecological processes. They affect the density and dynamics of prey species, with cascade effects on ecosystems (Ripple et al., Reference Ripple, Estes, Beschta, Wilmers, Ritchie and Hebblewhite2014). Habitat fragmentation disturbs the behaviour of carnivores with large home ranges (Woodroffe, Reference Woodroffe2000), and brings them into conflict with people (Thirgood et al., Reference Thirgood, Woodroffe, Rabinowitz, Woodroffe, Thirgood and Rabinowitz2005). Inadequate livestock husbandry is considered a major threat in this regard, particularly in non-industrialized countries (Hull et al., Reference Hull, Zhang, Zhou, Huang, Viña and Liu2014) where livestock production is badly managed (Ripple et al., Reference Ripple, Estes, Beschta, Wilmers, Ritchie and Hebblewhite2014). On the American continent, jaguars Panthera onca are considered to be a threat to livestock, and conflicts between rural communities and jaguars are common (Caso et al., Reference Caso, Lopez-Gonzalez, Payan, Eizirik, de Oliveira and Leite-Pitman2008; Peña-Mondragón & Castillo, Reference Peña-Mondragón and Castillo2013). In Mexico the jaguar has been extirpated from 60% of its original distribution (Chávez & Ceballos, Reference Chávez and Ceballos2006); meanwhile livestock production has developed extensively (Chauvet, Reference Chauvet and Hernández2001), and in 2003 cattle occupied 110 million ha (INE, 2004). The land occupied by jaguars is owned by rural inhabitants, with 60–70% of Mexico's forested areas owned by indigenous and mestizo communities (Bezaury-Creel & Gutiérrez Carbonell, Reference Bezaury-Creel, Gutiérrez Carbonell, Soberón, Halffter and Llorente-Bousquets2008). The term peasant is commonly used (corresponding to campesino in Spanish) to refer to these groups, and denotes a way of living that includes multiple uses of natural resources.
The tropical rainforest of the Selva Lacandona in the state of Chiapas is a priority site for jaguar conservation in Mexico (Chávez & Ceballos, Reference Chávez and Ceballos2006), although illegal hunting occurs throughout the species’ range in Mexico (Amador-Alcalá et al., Reference Amador-Alcalá, Naranjo and Jiménez-Ferrer2013). In 1978 the 3,312 ha Montes Azules Biosphere Reserve was designated to secure the long-term maintenance of regional biodiversity (SEMARNAP, 2000). Agriculture and livestock production are important livelihood activities in the region, with the latter representing one of the main sources of income for rural people. Thus, perceived and actual predation of livestock by jaguars puts the species at risk of persecution and elimination (SEMARNAT, 2009). Although predation of livestock by large mammals has been widely studied (Conforti & Azevedo, Reference Conforti and Azevedo2003; Hoogesteijn & Hoogesteijn, Reference Hoogesteijn and Hoogesteijn2008; Rumiz et al., Reference Rumiz, Polisar and Maffei2011; Peña-Mondragon & Castillo, Reference Peña-Mondragón and Castillo2013) it remains unclear which livestock husbandry practices may trigger predation. If livestock husbandry influences levels of predation by carnivores such as jaguars, there is clearly a need to understand the motivations and needs of the people involved, and the various aspects of their practices. Thus our main objective was to characterize livestock husbandry practices to identify those that increase the risk of predation of livestock by jaguars in the rural communities adjacent to the Montes Azules Biosphere Reserve.
Study area
The study was conducted in ‘ejidos’ (a system of land tenure that combines individual and communal possession; Warman, Reference Warman2001) adjacent to the Montes Azules Biosphere Reserve in the Selva Lacandona (Fig. 1), which hosts a high diversity of Neotropical flora and fauna (Miller et al., Reference Miller, Chang and Johnson2001). Deforestation rates of up to 33% were recorded in the study area during 1986–2010 (Carabias et al., Reference Carabias, Meli and Hernandez2010). Culturally, the Selva Lacandona comprises indigenous and mestizo communities, which have migrated there since the beginning of the 20th century, mainly from the mountainous regions of Chiapas (De Vos, Reference De Vos1988). The Reserve is important for jaguar conservation (Chávez & Ceballos, Reference Chávez and Ceballos2006) but there may be only 51–132 individuals remaining there (de la Torre & Medellín, Reference de la Torre and Medellín2011).
Fig. 1 Sites where livestock were attacked by jaguars Panthera onca in ejidos adjacent to the Montes Azules Biosphere Reserve, in the Mexican state of Chiapas. 1, Zamora Pico de Oro; 2, Reforma Agraria; 3, Nuevo San Isidro; 4, López Portillo; 5, Adolfo López Mateos; 6, Galacia; 7, Playón de la Gloria; 8, Flor Marques; 9, Boca Chajúl; 10, Loma Bonita.
Methods
We used a socio-ecological systems research approach (Berkes & Folke, Reference Berkes, Folke, Berkes and Folke2000). As our questions were related to human practices we used research instruments from the social sciences applied to the environmental sciences (Supplementary Material 1; Newing et al., Reference Newing, Eagle, Puri and Watson2011). We also collected ecological information related to the identification of sites of livestock predation and landscape fragmentation, to construct an overview of the human–jaguar conflict.
We conducted four exploratory visits during 2008–2010. As a first step, following our ethical code of conduct, we explained the project to local people and asked the local authorities for permission to conduct the research. Gaining trust and empathy was essential, as jaguars are a protected species and their elimination is sanctioned with fines and prison sentences (Tarrés, Reference Tarrés2004). We collected data during five 20-day visits, in February and October 2011, March and September 2012 and January 2013, using participant observation, surveys (closed-ended questionnaires) and semi-structured interviews in which we asked open questions and allowed participants to talk freely (Table 1; Taylor & Bogdan, Reference Taylor and Bogdan1987; Patton, Reference Patton2002). For practical purposes the surveys and interviews were integrated into a single instrument, and we recorded the answers to both types of questions on a form. Localities were selected based on evidence of jaguar presence nearby; key actors were identified as those whose livestock had been attacked by jaguars. Thirty-two heads of families agreed to participate in the study; these were enlisted using the snowball sampling method (Newing et al., Reference Newing, Eagle, Puri and Watson2011), where participants were asked to refer others who may have had similar problems. People were willing to talk and were open to providing information. During the fieldwork 17 attacks on livestock by jaguars were confirmed through examining carcasses (Fig. 1).
Table 1 Methods used for data collection.
Data analysis consisted of quantifying responses to specific closed-ended questions, and constructing categories based on the responses provided to open questions (Strauss, Reference Strauss1995; Newing et al., Reference Newing, Eagle, Puri and Watson2011). The categories are intended to reflect the ideas and actions of people according to their own perspectives, motivations and needs. Frequencies and percentages were calculated for each category. As participants could give more than one response to the same question, in some cases the percentages exceed 100%. A first analysis consisted of spatially locating each category of livestock practices reported. A qualitative indicator of the vulnerability of livestock to predation by jaguars was constructed to identify the variables involved and their relative importance, which was useful for informing recommendations (Table 2). Forage, capture and prey consumption were the three elements used to determine whether vulnerability was high, medium or low, following optimal foraging theory (Gutiérrez, Reference Gutiérrez, Ardila, López, Pérez and Quiñones1998). A value was then assigned for each activity involved in livestock management.
Table 2 Indicator of vulnerability of livestock to predation in relation to various management activities, with recommendations for mitigation, and the type of change needed.
10, no influence; 1, low influence; 2, medium influence; 3, high influence
2Sum of vulnerability indicators: 1–3, low; 4–6, medium; 7–9, high vulnerability
Results
Figure 2 relates livestock practices with the type of surroundings where these take place (i.e. human settlement, corral, pastureland, border or transition zone, or tropical rain forest). Decisions concerning issues such as the location of family plots and rainforest units are taken at the ejido community level. In the corral zone, animals may be removed and kept closer to the family home to avoid the spread of disease or attacks by predators. Livestock are grazed on plots of pasture delimited by barbed wire fences, which in some cases are adjacent to borders or transition areas with forest patches. Livestock reproduction occurs in the corral and pasture units. Livestock move within border zones and forested lands to obtain water from streams or natural springs.
Fig. 2 Spatial distribution of the major components of livestock practices in ejidos adjacent to the Montes Azules Biosphere Reserve (Fig. 1). The shading indicates the intensity of the activity (black, high intensity; dark grey, medium intensity; light grey, low intensity).
The various aspects of livestock husbandry practices are illustrated in Fig. 3. Four broad themes emerge from the data: (1) general aspects of livestock practices, (2) herd improvement, (3) economic income, and (4) economic losses. These themes encapsulate the main aims of rural families in raising livestock: to increase production and economic income to improve their well-being.
Fig. 3 Categories and specific practices relating to general livestock husbandry, herd improvement, income and economic losses in south-eastern Mexico (Table 3), and the relationships between them (solid and dashed lines represent positive and negative relationships, respectively). The categories within the grey-shaded boxes correspond to management practices that affect livestock predation by jaguars, and those within white boxes indicate responses of interviewees.
More than half of those interviewed (62%) had subdivisions within their fenced grazing areas, and rotated livestock every 15–30 days within each subdivision. Access to water for livestock was limited to natural sources such as rivers, streams and springs, which are abundant in the area; all participants expressed a commitment not to log trees, and to protect vegetation surrounding sites that provided water. The disposal of animal waste was another important aspect of animal husbandry; dead animals were left where they were found and were not buried or burned. Reproduction was carried out through free mounting, in which a male is released close to females. Sometimes directed mounting was carried out with a borrowed male stud. Reproduction was conducted in corrals and in the grazing zones (Fig. 2). None of the interviewees reported a schedule of vaccinations, and veterinary assistance would be sought only after considerable losses had occurred. Only 18% of interviewees had control of their herd (by means of ear tags or burn marks); 46% reported individual numbering of each head of livestock, mainly to meet the requirements of governmental assistance programmes, such as the Program of Stimuli for Livestock Productivity. Ear tags or brands are used to identify individuals within a herd. In relation to infrastructure, possession of corrals (59%) and internal subdivisions (50%) were most commonly reported by interviewees (Table 3).
Table 3 Categories and specific practices relating to the general management of livestock, herd improvement, income and economic losses, with the percentage of interviewees (n = 32) who used each practice.
Herd improvement Herd improvement is based on nutrition, and the only food supplement interviewees could provide was mineral salt. Stud males, used to maintain the genetic health of livestock herds, are acquired at livestock auctions or are loaned from other producers (Table 3). Females are returned to their reproductive condition through early weaning of calves, and are crossed with a new male.
Family income Families seek to increase their herds to sell animals or derivatives. For 96% of interviewees, live animals < 6 months of age were the most lucrative product; only 6% of respondents produced milk and cheese. Other sources of income included economic support from governmental agencies (21% of interviewees) and self-employment (12%). Families also engaged in agricultural activities such as the cultivation of maize (71%) and beans (75%; Table 3).
Economic loss Diseases were perceived to be one of the main factors affecting livestock production; 56% of interviewees reported rabies (viral encephalomyelitis) and 50% reported anthrax (Bacillus sp.). Predators were another relevant factor in economic losses, according to 50% of interviewees. Although we did not ask directly about livestock theft, as it is a sensitive subject, it was mentioned by at least 15 interviewees (Table 3).
Vulnerability to predation The management practices that expose livestock to risk of predation by jaguars are outlined in Table 2. The qualitative indicator of livestock vulnerability allows us to identify factors that impede or restrict changes in practices that could mitigate predation.
Discussion
Few studies have examined the role of rural peoples’ livestock practices in relation to predation by jaguars. Our field experience indicates that the conflict is accepted among rural inhabitants, government authorities and conservationists working in the Selva Lacandona region. However, campaigns and mitigation programmes have been conducted without a deep understanding of the views of those affected by the conflict. Our results may be restricted to the Selva Lacandona region but the context of our study is similar to that in other places in Mexico, as well as in Central and South America (Burgas et al., Reference Burgas, Amit and Lopez2014; Tortato et al., Reference Tortato, Layme, Crawshaw and Izzo2015).
Livestock grazing near well-preserved portions of jaguar habitat has been reported as a major cause of predation throughout the jaguar's natural range (Azevedo & Murray, Reference Azevedo and Murray2007; Palmeira et al., Reference Palmeira, Crawshaw, Haddad, Ferraz and Verdade2008; Donikar et al., Reference Donikar, Patil, Narkhede, Rane, Mokat and Bhave2011; Soto-Shoender & Giuliano, Reference Soto-Shoender and Giuliano2011; Garrote, Reference Garrote2012; Zarco-González et al., Reference Zarco-González, Monroy-Vilchis and Alaníz2013; Soh et al., Reference Soh, Carrasco, Miquelle, Jiang, Yang and Stokes2014). We also identified this pattern, with cattle becoming vulnerable to predation when they move near natural areas to obtain food and water. Another factor that contributes to livestock vulnerability is the handling of dead animals. In the study area carcasses are not removed, and this can encourage carnivores to attack livestock, and may even create some dependency or preference for livestock as a source of food (Hoogesteijn & Hoogesteijn, Reference Hoogesteijn and Hoogesteijn2011). Thus incineration or burying of dead animals is a recommended practice (Sander et al., Reference Sander, Warbington and Myers2002; Hoogesteijn & Hoogesteijn, Reference Hoogesteijn and Hoogesteijn2011). Proper handling of reproduction activities and management of calves are also important factors in reducing predation by carnivores (Schiess-Meier et al., Reference Schiess-Meier, Ramsauer, Gabanapelo and König2007). Providing special confinement corrals for vulnerable young calves (< 6 months) provides security (Van Bommel et al., Reference Van Bommel, Bij de Vaate, De Boer and De Iongh2007; Hoogesteijn & Hoogesteijn, Reference Hoogesteijn and Hoogesteijn2011) and facilitates vigilance by livestock keepers.
A relevant issue that emerged is the need for a written record of every animal that is sold or has died, whether by natural or other causes (e.g. disease, drowning, snake bite or attack by a predator). This practice was not evident in our study, resulting in overestimation of the damage caused by jaguars (Hoogesteijn & Hoogesteijn, Reference Hoogesteijn and Hoogesteijn2011). We found that the approach to disease management was remedial rather than preventive, and this behaviour has been passed down through generations. Good health management results in fewer losses at birth and in general, which in turn increases productivity, and thus losses caused by predation are not as devastating to the family economy. In most cases livestock losses to predators are fewer than those caused by other factors, including disease (Hoogesteijn & Hoogesteijn, Reference Hoogesteijn and Hoogesteijn2011). At present, disease management is mostly confined to vaccination programmes administered by government agencies. This economic incentive accompanied by an educational campaign could raise awareness of the benefits of more efficient livestock practices.
Early weaning is a harmful practice used to increase animal production. It is not recommended as it can lead to low meat production; a young calf left with its mother can be more productive (Arias et al., Reference Arias, Revidatti, Slobodzian, Capellari and Benítez1998). It can also lead to digestive and respiratory illnesses, as well as diseases related to poor adaptation as a result of weak body state and/or retarded growth (Soni, Reference Soni1998). Thus, early weaning produces weaker individuals that may be more susceptible to diseases, and vulnerable to predation by carnivores such as the jaguar. Changing this practice will require training to ensure that producers understand the infrastructure required for the appropriate management of both mothers and young.
Livestock production in the Selva Lacandona represents a source of complementary income for families, as in other parts of Mexico and elsewhere (FAO, 2009; Davies et al., Reference Davies, Niamir-Fuller, Kerven, Bauer, Steinfeld, Mooney, Schneider and Neville2010). There is a need to supplement the family economy with governmental support and subsistence agriculture partly because livestock production does not provide the yields expected. However, this creates a circular problem: because livestock does not provide the necessary earnings people do not invest in better management of their livestock, although this would increase their returns in the long term.
Taking into account factors such as disease and predation, livestock production becomes an activity that requires high levels of investment, which is impossible for the majority of families in the Selva Lacandona. Livestock theft must also be evaluated as it results in significant losses for producers, as has occurred in South America (Hoogesteijn & Arenas-Avella, Reference Hoogesteijn, Arenas-Avella, Romero, Salomón, De Venanzi and Arias2008).
A broad conclusion derived from our findings is that several specific livestock husbandry practices make herds in the Selva Lacandona more vulnerable to attack by jaguars (these practices and our recommendations are outlined in Table 2). Two broad types of changes were identified to implement these recommendations: (1) economic investment, and (2) behavioural changes in communities and in relation to the cultural and educational histories of families. Both matters require technical and communication interventions, with the provision of financial support. Mitigation programmes already in existence should consider not only a payment for animals lost in attacks by carnivores (which is helpful) but also the implementation of a more integral strategy that includes a capacity-building perspective (Abella & Fogel, Reference Abella and Fogel2000). Training workshops that provide technical advice should be accompanied by visual educational materials designed for people with poor literacy skills or who have little experience of using written materials. Provision of certificates for good livestock practices may help people to get access to economic support and resources such as materials for fences or veterinary assistance. One important recommendation relates to the monitoring of livestock herds. We advise the use of written records of all livestock, which could be maintained by marking in special notebooks designed for those with a low level of literacy (Supplementary Fig. S1).
Finally, we recommend that agents such as the government and NGOs provide educational interventions (awareness-raising and training) as well as economic support to help families improve their livestock husbandry practices. Conversion to efficient and productive practices would improve families’ economic circumstances, which could translate into greater investment in infrastructure and veterinary care, and ultimately increase productivity. Such actions can be effective in mitigating conflict, and may create a scenario of greater tolerance for jaguars in the Selva Lacandona.
Acknowledgements
This paper constitutes a partial fulfilment of the Graduate Programme in Biological Science (Posgrado en Ciencias Biológicas) of the National Autonomous University of Mexico (UNAM). AC acknowledges the PhD scholarship received from the National Council of Science and Technology (CONACYT) and the support received from the Instituto de Investigaciones en Ecosistemas y Sustentabilidad of UNAM. Funding was provided by Idea Wild, Cleveland Metroparks Zoo and the Cleveland Zoological Society. We thank Keith MacMillan and Mary-Ann Hall for editing the English. We are especially grateful to all those in the rural communities who kindly participated in this research.
Biographical sketches
Juan L. Peña-Mondragón is interested in the socio-ecology of large carnivores, and human–wildlife conflict. He works to develop measures to mitigate livestock depredation by large carnivorous mammals, involving local people in the conservation of species and the ecosystems they share with wildlife. Alicia Castillo is interested in the social aspects of ecosystem management, with a particular focus on common pool resources and human–wildlife conflict. Almira Hoogesteijn is a veterinarian and has worked on wildlife conservation projects in the Americas and Europe for > 20 years. Her main research focus is on the impact of pesticides and heavy metals on human and animal health, and stock management strategies to decrease predation. Enrique Martínez-Meyer is interested in understanding how environmental changes affect biodiversity, and how this pressure can be reduced. He has worked on global change biology issues, focusing on the application of ecological niche theory and methods, conservation biology, climate change and biogeography.
