Local knowledge to enhance wildlife population health surveillance: Conserving muskoxen and caribou in the Canadian Arctic

Biological Conservation Volume 217, January 2018, Pages 337-348 Biological Conservation Author links open overlay panelMatildeTomaselliaSusanKutzabCraigGerlachcSylviaCheckleyad https://doi.org/10.1016/j.biocon.2017.11.010 Get rights and content a Department of Ecosystem and Public Health, Faculty of Veterinary Medicine, University of Calgary, 3280 Hospital Drive NW, Calgary, Alberta T2N 4Z6, Canada b Canadian Wildlife Health Cooperative, Faculty of Veterinary Medicine, University of Calgary, 3280 Hospital Drive NW, Calgary, Alberta T2N 4Z6, Canada c Department of Anthropology and Archaeology, Faculty of Arts, University of Calgary, 2500 University Drive NW, Calgary, Alberta T2N 1N4, Canada d Alberta Provincial Laboratory for Public Health, 3030 Hospital Drive NW, Calgary, AB T2N 4W4, Canada Received 31 August 2017, Revised 4 November 2017, Accepted 6 November 2017, Available online 24 November 2017. Abstract Monitoring and surveillance of wildlife populations, including demographics and health, is often challenging, particularly in resource-constrained and remote settings. However, in areas characterized by subsistence oriented societies, the users of renewable resources hold a vast and holistic ecological knowledge about the natural environment. This knowledge can be instrumental for understanding and early detection of changes in wildlife populations. Using qualitative research methods and participatory epidemiology techniques we documented the local knowledge from resource users of the community of Iqaluktutiaq (Nunavut, Canada) to assess the health and population status and trends for muskoxen and caribou in the area. Semi-structured individual interviews, followed by group interviews, were implemented with 38 participants, and research findings were summarized and then verified with 31 interviewees. Local knowledge identified major declines in the number of muskoxen and caribou in the study area that were corroborated by subsequent aerial population estimates for both species. Observations made by participants allowed inference of possible mechanisms for the recent population declines, including poor recruitment, poor body condition, and increased morbidity and mortality (including endemic and emerging diseases). Engaging resource users in the process of knowledge generation was useful to identify further research priorities and fostered trust among parties that facilitated the subsequent collaborative development of management plans for these species. We use our experience to illustrate that local knowledge contributes to a holistic understanding of wildlife health and can serve as an early warning system to detect changes in wildlife populations. These participatory approaches are portable to other species and settings and can enhance conservation and co-management efforts for wildlife species worldwide. Previous article in issue Next article in issue 1. Introduction The importance of understanding wildlife health for sound management and conservation efforts (Deem et al., 2001, Peterson and Ferro, 2012, OIE, 2014, Stephen, 2014, Decker et al., 2016), and the importance of including resource users in both knowledge generation and decision making processes (e.g., co-management) (Berkes et al., 2000, Decker et al., 2012, Jordan et al., 2016, Predavec et al., 2016), have emerged as conservation priorities in recent years. However, measuring wildlife population health, including demographics and the diversity and status of infectious and non-infectious diseases (Hanisch et al., 2012, Stephen, 2014), faces major technical, logistical, economic, and even political constraints (Wobeser, 2007, Ryser-Degiorgis, 2013) that make establishing wildlife health status difficult. Additionally, although the use of indigenous and resource users' knowledge is not new to conservation biology (Gadgil et al., 1993, Berkes, 2004, Brook and McLachlan, 2008), its specific application to enhance wildlife health assessment is in its infancy. Despite many challenges, effective wildlife management in an increasingly complex world requires a shift to a conservation paradigm that simultaneously incorporates wildlife population health assessment and meaningful participation of local resource users, recognizing the breadth and depth of their knowledge and their ‘holistic way of knowing’. Users of natural resources, especially those who live in subsistence-oriented communities, have firsthand experiential knowledge, as well as a long oral tradition of sharing knowledge about the status of, and ecological processes occurring in, their local environment, with this providing a holistic perspective for interpretation of their and other's observations (Gadgil et al., 1993, Berkes et al., 2000, Huntington, 2000, Rist and Dahdouh-Guebas, 2006, Berkes and Berkes, 2009, Huntington, 2011). Capturing this rich body of knowledge in a systematic manner may provide new and valuable information that cannot be obtained through scientific investigations alone and can greatly improve wildlife management. In the past decades, there have been increasing efforts to include knowledge of indigenous and local people in natural resource co-management (Berkes et al., 2000), conservation of biodiversity (Johannes, 1989, Gadgil et al., 1993, Drew, 2005), and wildlife biology and ecology research (Ferguson et al., 1998, Huntington and the communities of Buckland, Elim, Koyuk, Point Lay, Shaktoolik, 1999, Mallory et al., 2003, Steinmetz et al., 2006, Butler et al., 2012). In wildlife health and disease research, although collaboration with hunters is a common practice to enhance capacity for sample and data collection (OIE, 2014, Carlsson et al., 2016), only a few published studies use observations of resource users as a source of epidemiological data for disease detection (Madslien et al., 2011, Chen et al., 2012), or to record interspecific interactions at the wildlife-domestic livestock interface that may increase pathogen transmission (Brook and McLachlan, 2009, Brook, 2010). While there have been some efforts to use local knowledge to identify wildlife health issues and to inform better research questions (Brook et al., 2009, Carlsson et al., 2016), the formal and direct use of local knowledge to assess the health of wildlife populations, including status and trends, is currently missing. One barrier to the use of resource users' knowledge in wildlife management may be the perception that it is not gathered in a rigorous scientific manner; consequently, it may be dismissed as little more than anecdotal (Gilchrist et al., 2005, Brook and McLachlan, 2005, Drew, 2005). The use of standardized and repeatable methods for documenting local knowledge is thus essential if results are to be trusted by wildlife professionals and are to be used in making critical wildlife management and conservation decisions. Participatory epidemiology (PE) and participatory disease surveillance (PDS) provide the framework for incorporation of local knowledge into wildlife management. These methods, developed in the 1990s from participatory rural appraisal (Chambers, 1994) and implemented extensively in pastoral communities in developing countries, have been invaluable for enhancing veterinary surveillance capacity (Mariner and Paskin, 2000, Jost et al., 2007, Catley et al., 2012). Reliance on indigenous knowledge networks, particularly ethnoveterinary knowledge of participants, is a key concept in PE and PDS. Resource users are empowered in these systems, being the keepers of epidemiological data that is useful in multiple contexts, including detection of disease emergence (Jost et al., 2010), collection of historical and baseline morbidity/mortality data (Thrusfield, 2005), understanding disease impacts (Catley and Admassu, 2003), and contributing to disease eradication (Mariner and Roeder, 2003). The Canadian Arctic serves as an ideal location for implementation and evaluation of participatory wildlife health surveillance programs using PE and PDS methods for several reasons. First, communities are physically remote and isolated and traditional scientific investigations are logistically difficult and extremely expensive. These communities have maintained a close connection with the natural ecosystem, including a historic continuity of subsistence use of natural resources, and have maintained traditional and local ecological knowledge systems (Usher, 2000). In these regions, climate change is rapidly altering ecosystem processes, including host-parasite interactions, (McCarty, 2001, Altizer et al., 2013, Kutz et al., 2014) the effects of which are unlikely captured by ‘scientific’ monitoring alone (Dowsley, 2009). Finally, wildlife co-management is a legislated requirement through aboriginal land claims agreements. For example, the Nunavut Wildlife Act (2003) mandates the integration of Inuit Qaujimajatuqangit or Inuit knowledge into wildlife management (Armitage et al., 2011). As part of a broad project focused on the development of a participatory health surveillance system for wild muskoxen (Ovibos moschatus) in the Canadian Arctic, we investigated how indigenous and local knowledge can contribute to understanding wildlife population health status and trends. The objective of this paper is to illustrate a systematic approach for gathering important and often missing historic and contemporary epidemiological data about free-ranging wildlife. We do this by presenting a participatory study that documents local knowledge on muskox and caribou (Rangifer tarandus) populations in the Canadian Arctic. This work has the potential to be transferable to other wildlife species and settings, with this increasing the ability to include wildlife population health assessment into conservation programs while ensuring participation and empowerment of local resource users in co-management systems. 2. Methods 2.1. Terminology Various terms have been proposed and used in the literature to refer to experience-based knowledge, including traditional and local knowledge, traditional and local ecological knowledge, indigenous knowledge, folk knowledge, and wisdom (Berkes et al., 2000, Usher, 2000; Huntington et al. 2002; Rist and Dahdouh-Guebas, 2006, Brook and McLachlan, 2008). In this paper, we use the term local knowledge (LK) to refer to a local body of knowledge, not associated with aboriginal ethnicity, but characterized by both historical and contemporary knowledge acquired through extensive observation of the environment and its species. Therefore, here LK includes, but it is not limited to, Inuit knowledge. In addition, we use the term ethnoveterinary knowledge (Mariner and Paskin, 2000) with specific reference to LK on wildlife health and diseases. In this paper, we use the term wildlife health in the broadest sense, referring not only to the occurrence and/or exposure to infectious and non-infectious disease, but also including body condition, and population demographics and trends (Hanisch et al., 2012, Stephen, 2014). 2.2. Study area Our study occurred in the community of Iqaluktutiaq (also known as Cambridge Bay) in the Kitikmeot Region, Nunavut, Canada. Iqaluktutiaq, with a population of approximately 1600 people, 79% Inuit (Statistics Canada, 2011), is situated on south-east Victoria Island in the Arctic Archipelago. The two ungulate species harvested by residents of this community are muskoxen, mainly island muskoxen (Ovibos moschatus wardi), and caribou, mainly of the Dolphin and Union herd (Rangifer tarandus groenlandicus). Muskoxen are resident on the island (Gunn and Adamczewski, 2003), while caribou migrate seasonally between the island (summer) and the mainland (winter) (Dumond and Lee, 2013). Hunting of both species, for subsistence by residents and for sport by guided hunters, contributes largely to local food security and community revenue (Kutz et al., 2017, Tomaselli et al., 2018). This research program was initiated in response to community concerns about invasion and spread of two species of lungworms (Kutz et al., 2013), widespread mortalities of muskoxen (associated with the bacteria Erysipelothrix rhusiopathiae) (Kutz et al., 2015), and the local decline of muskoxen resulting in the suspension of the commercial muskox harvest in 2012 (Tomaselli et al., In press). 2.3. Study design Data collection occurred in three phases: individual semi-structured interviews, small group interviews, and feedback sessions. Color topographic maps of the area (scale 1:500,000) were used to assist participants in their narratives. A translator was present through all stages. Participation in the study was voluntary and with written informed consent, confidentiality was protected, and participants could withdraw at any time. Monetary compensation, the amount set by the Kitikmeot Inuit Association (KIA), was given to participants after interviews (hourly rate of $100 for Elders and $50 for other participants). The study obtained community approval through the KIA and Ekaluktutiak Hunters and Trappers Organization (EHTO); the research was approved by the Conjoint Faculties Research Ethics Board at the University of Calgary (REB14-0646) and the Nunavut Research Institute (license 04017 14N-M and renewals). 2.3.1. Individual semi-structured interviews Semi-structured individual interviews (Huntington, 2000) were designed to gather LK about muskoxen in the Iqaluktutiaq area using a check-list of open-ended questions on participants' observations for hunted and non-hunted animals. Topics included hunting experience, and muskox distribution, abundance, health, and diseases (see Appendix A for interview guide). Participant recruitment followed the methods recommended for both LK (Davis and Wagner, 2003) and PE studies (Mariner and Paskin, 2000), directed to identify key informants that fit with study objectives. ‘Muskox experts’ were selected by purposive sampling through the KIA and the EHTO, and by snowball technique by asking participants to identify other key informants to include in the study (Green and Thorogood, 2014a). The sample size was defined using the thematic saturation approach (Green and Thorogood, 2014a). Interviews were audio-recorded, field notes were taken, and key information was later systematically transcribed to provide the basis for thorough thematic content analysis (Mariner and Paskin, 2000, Green and Thorogood, 2014b). During the individual interviews, participants also described changes in abundance and health of the Dolphin and Union caribou herd (hereafter referred to as caribou) in the study area. As this added an important observational component, possibly linked with changes in muskox population health, we further probed participant observations on caribou in the small group interviews. Study participants, although purposefully selected as muskox experts, also had deep knowledge about caribou and often were primary caribou harvesters (Tomaselli et al., In press). Individual interviews were useful to understand the study system with reference to the interactions between interviewees and muskoxen/caribou (see Tomaselli et al., In press), as well as gather baseline information on muskox and caribou health, including diversity of observed abnormalities. Themes that emerged from the individual interviews were used to design and were further explored in small-group interviews. 2.3.2. Small group interviews Semi-structured interviews were used to collect primarily quantitative data on participants' observations and perceptions on muskox and caribou health, including information on demography, body condition, morbidity and mortality over time. To do so, we used a checklist of participatory analytical activities, adapting PE methods described by Mariner and Paskin (2000) to our research needs and context (Fig. 1; for detailed methods see Appendix B). Participatory activities helped through visual techniques (e.g., drawing, proportional piling, mapping, etc.) to reach consensus among participants and generate quantitative data as the outcome of the discussion process (Mariner and Paskin, 2000). In this phase, we also applied the triangulation technique recommended in social science studies as a way to improve data quality and reliability (Mathison, 1988, Green and Thorogood, 2014c). This involved recruitment of new participants through the purposeful sampling and the snowball technique described above. Each group was composed of key informants who participated in the individual interviews, along with at least one new interviewee. Participants were grouped according to age, hunting experience, and hunting areas of preference. 2.3.3. Feedback sessions As a final step of data analysis, findings were corroborated and refined with study participants (Burke, 1997, Green and Thorogood, 2014b). All interviewees were invited to view and comment on a PowerPoint presentation that summarized the interview data analyses and interpretation. If participants disagreed with the information presented, we were ready to further probe on the specific theme/s, understand the motivations behind such disagreement, and, if needed, repeat the interview process. To facilitate participation in the validation phase, multiple feedback sessions were organized as individual or group meetings. Fig. 1 Download high-res image (325KB)Download full-size image Fig. 1. Checklist of participatory exercises performed in the small group interview setting. 2.4. Data analysis and visualization Descriptive statistics were used to summarize quantitative data and a cubic regression model was used to summarize data on relative population abundance over time. Analyses were performed using IBM SPSS Statistics 22.0 software. The software ArcGis 10.2 was used to visualize georeferenced data. 3. Results Thirty key informants were interviewed individually from July to September 2014. Participants included year-round residents (Inuit, n = 23; non-Inuit, n = 5) and summer residents (commercial pilots, n = 2). Themes that emerged included changes in muskox and caribou demography, body condition status, morbidity and mortality, and observations of muskox ‘acute mortality’ cases consistent with disease outbreaks. From November to December 2014, 19 community members, 11 previously interviewed and 8 new interviewees (triangulation), participated in 7 small-group interviews with 2 to 3 participants/group. From June to July 2015, 31 of the 38 interviewees participated in the feedback sessions and agreed with the results presented. Observations covered a vast area of land from the Arctic mainland to as far northeast as Ellesmere Island in the High Arctic. However, the area consistently observed by the majority of the participants, and consequently used as the ‘area of observation’ for the context of this paper, was approximately 150 km, or 93 miles, radius of land around Iqaluktutiaq (Appendix C). 3.1. Muskox and caribou demography 3.1.1. Abundance Participants in individual and group interviews all reported recent declines in muskox and caribou numbers. In individual interviews, an Elder (Interviewee 6) said: “not only muskox have declined, caribou too … [Caribou declined] the same way and the same time [as muskoxen]” (for other representative quotes see Appendix Appendix D, Appendix E). In group interviews, participants did a drawing exercise to characterize the relative abundance of muskoxen and caribou over time. A cubic regression line fit to these abundance curves provided the best model for muskox (R2 = 0.651) and caribou (R2 = 0.607) population trends. For both species populations peaked and then began to decline around the mid-2000s, with a major decline after 2010 (Fig. 2) Descriptive narratives from both the individual and group interviews provided a richer understanding of the trends. Participants reported that in the 1960s and 1970s it was rare to see muskoxen, but from the 1980s to early 2000s, muskox numbers increased and it was common to see herds in the vicinity of the community, and in numbers large enough to make it unnecessary to go further away to hunt muskoxen for personal consumption (Appendix D). Regarding caribou abundance, participants observed low numbers of animals in the 1960s and 1970s and further noted that they were not close to the community. In the mid-1980s, caribou started migrating within a few miles of the community and in the autumn it was typical to observe big herds gathered on the shoreline both to the east and west side of the community, waiting for the sea ice to freeze (Appendix E). The abundance curves generated during group interviews identified ‘pre-decline’ (from the 1990s to mid-2000s) and ‘decline’ (from mid-2000s to the end of 2014) periods. These periods were then used for context in subsequent participatory exercises to assess changes in abundance, groups (size, composition, distribution), body condition, morbidity and mortality (Fig. 1; Appendix B). 3.1.2. Decline in abundance Using a proportional piling exercise, participants reported an 85% (IQR and range: 75–90; n = 7) decrease of muskoxen and 80% (IQR: 75–90; range: 50–95; n = 7) decrease of caribou, from the pre-decline period to the end of 2014. Increase in predators, changes in migratory routes (caribou) or emigration events (muskoxen), as well as, human disturbance, environmental changes, and changes in the health status of the animals were among the factors that participants associated with the decline of both ungulate species. During the feedback sessions (summer 2015), participants emphasized that they were still observing a declining trend for both species. Fig. 2 Download high-res image (242KB)Download full-size image Fig. 2. Participants' observations on relative abundance (%) over time of muskoxen (A) and caribou (B) in the Iqaluktutiaq area (Victoria Island, Nunavut, Canada). The number of groups providing the information is specified in parenthesis under each year. 3.1.3. Group size and distribution According to individual narratives (Appendix D) and group interviews the size of muskox groups and the distance between groups changed over time: “within the last ten years is when it started to be more difficult to see herds [of muskoxen] and then more recently within the last 3 to 5 years I would say that it is extremely difficult to find certainly any larger, and if you do find muskox they are usually loners or very small herds” (Interviewee 17). Using a categorization exercise, six of seven groups indicated that in the pre-decline period, the average size of a muskox herd was more than 30 animals with an average of 5 to 10 miles (8 to 16 km) between herds. Progressively, smaller and more scattered groups were observed and, by the end of 2014, interviewees observed fewer than 10 muskoxen per herd, with more than 20 miles (32 km; n = 4 groups), and often more than 50 miles (80 km; n = 3 groups), between herds. Fig. 3 Download high-res image (118KB)Download full-size image Fig. 3. Participants' observations on relative proportion (%) of adults and juveniles muskoxen (A) and caribou (B) in the pre- and decline periods in the Iqaluktutiaq area (Victoria Island, Nunavut, Canada). The thick horizontal lines correspond to the medians; the distance between the thin longer horizontal lines to the interquartile range; the whiskers to the range of the data except for outliers. Circles and asterisks represent outliers (i.e., extend for more than 1.5 times the interquartile distance) and extreme outliers (i.e., extend more than 3 times the interquartile distance), respectively. Regarding caribou herd size, all groups reported that prior to the decline, during the fall migration from late October to mid-November, they used to see “hundreds of caribou gathered in a single herd” near the shoreline, waiting for the sea ice to freeze, before migrating to the mainland. Progressively, fewer caribou were noticed in the usual areas, and, by the end of 2014, participants observed “very small, very few, and very scattered herds” of caribou, ranging from 3 to 30–40 individuals, but more frequently less than 10 caribou. The observations regarding caribou herd size emerged also from the analysis of the individual narratives (Appendix E). 3.1.4. Sex and age structure Although participants were not directly asked, the observation of fewer calves in declining muskox herds emerged as a theme from individual interviews. This was followed up in group interviews using a proportional piling exercise to determine sex and age structure of muskox and caribou herds. For calves, the aggregate observation throughout the year was reported (as opposed to attempting to estimate calving, survival, or recruitment rates). Because of this, possible misclassification between calves and yearling might have arisen (e.g., late winter calf mistakenly referred to as yearling), especially for muskoxen; therefore, we report ‘juveniles’ as the sum of observations for calves plus yearlings. Observations for calves and yearlings separately are presented in Appendix F. The proportion of adult muskoxen increased from 75% in the pre-decline to 90% in the decline period (n = 7). All interviewed groups reported a decrease in the observed proportion of juveniles from 25 to 10% (n = 7) over this period (Fig. 3A). Four of 7 groups reported a relative increase in adult females from 47.5% (IQR: 42.5–50; range: 40–50) to 65% (IQR: 57–75; range: 54–80), whereas the proportion of males remained similar across periods (Appendix F). Three groups did not feel confident in providing the relative proportion of adult muskoxen divided by gender. Similarly, for caribou, groups reported an increase in the proportion of adults, from 65% in the pre-decline to 80% in the decline period (n = 7). Concurrently, there was a decrease in the proportion of juveniles from 35% to 20% (n = 7) (Fig. 3B). Not all the groups felt confident in providing the proportions of adults by sex, but for those that did, the proportion of adult female caribou increased from 42% (IQR: 34.5–45; range: 30–45; n = 4) in the pre-decline to 50% (IQR and range: 50–55; n = 3) in the decline, while the proportion of adult males did not vary between the two periods (Appendix F). 3.2. Muskox and caribou body condition Changes in the body condition of muskoxen emerged voluntarily as a theme in the individual interviews. This was explored further in group interviews where participants did a proportional piling exercise to indicate the proportion of animals that they observed in different body condition classes: excellent, good, fairly good and poor. Overall, from the pre-decline to decline period, fewer animals were classified in excellent condition and more in fairly good and poor condition (Fig. 4a). Narratives supported these findings, with many participants in group interviews reporting that it was common to hunt both muskoxen and caribou with 5 to 8 cm of back fat during the pre-decline; whereas, at the time of the interview, “you would be very lucky to get an animal with 3 cm of back fat, but usually they have 1 cm or nothing”. Fig. 4 Download high-res image (269KB)Download full-size image Fig. 4. Participants' observations on muskoxen (A) and caribou (B) in the pre- and decline periods in the Iqaluktutiaq area (Victoria Island, Nunavut, Canada): a) body condition status expressed as relative proportion (%) of excellent, good, fairly good and poor animals; b) relative proportion (%) of health, diseased and dead animals; relative proportion (%) of mortality attributed to predation and acute death. The thick horizontal lines correspond to the medians; the lower and upper lines of the boxes to the first and third quartiles, respectively (interquartile distance); the whiskers to the range of the data except for outliers. Circles and asterisks represent outliers (i.e., extend for more than 1.5 times the interquartile distance) and extreme outliers (i.e., extend more than 3 times the interquartile distance), respectively. 3.3. Muskox and caribou morbidity and mortality Increased observation of abnormalities in hunted and observed muskoxen and caribou, recent observations of muskox carcasses with attributes that we infer to be suggestive of a disease outbreak, and increased observations of muskox and caribou mortality due to predators were among the themes that consistently arose from the individual narratives. Using a proportional piling exercise, group interview participants were asked what proportion of animals observed were healthy, sick or dead. For both muskoxen and caribou, from the pre-decline to the decline period, the proportion of animals observed healthy had decreased and the proportion of diseased had increased. For muskoxen, there was also an increase in the proportion of animals observed dead, but no change was observed in the proportion of dead caribou (Fig. 4b). 3.3.1. Relative prevalence of diseases Participants in the individual interviews reported a variety of lesions or more generic syndromes in hunted and observed muskoxen and caribou (Table 1). The relative prevalence and trend over time were assessed through proportional piling in group interviews (Table 2, Table 3). Rarer, but more recent observations reported by individual participants and not captured by the proportional piling, included lesions described as “white eyes” consistent with corneal opacity in adult male muskoxen (attributed by participants to injuries incurred during the rut, however noticed only since 2010). In caribou the lesions described included “scabs on the nose and mouth” (an adult female hunted between 2005 and 2007 and an adult female and her calf observed in 2010), hard and swollen testicles consistent with orchitis (noticed since the 1990s but with increased reports in 2014), “different color patches” in the lung “that was stuck in the rib cage” consistent with pneumonia (described in one caribou hunted in 2013), and liquid cysts in the lung parenchyma (one caribou hunted in 2008). In addition, observations of yellow coloration of subcutaneous tissue associated with pale skeletal muscle were described in both muskoxen and caribou, and in particular in individuals with poor body condition since 2008. Table 1. List of lesions and syndromes observed by participants in the hunted and observed muskox and caribou populations in the Iqaluktutiaq area (Victoria Island, Nunavut, Canada) and their most likely differential etiologies in this context. Observed lesions Differential etiology Warble flies larvae Hypoderma spp. Nasal worms Cephenemyia spp. Swollen jaw Actinomyces spp. Actinobacillus spp. Non-specific tooth root infection White muscle cysts Taenia spp. Liver cysts Taenia spp. Echinococcus canadensis Lung cysts solid cysts liquid cysts Umingmastrongylus pallikuukensis (only muskox) Echinococcus canadensis Swollen joints – limping Brucella spp. Erysipelothrix rhusiopathiae Chlamydia spp. Mycoplasma spp. Injuries Swollen and hard testicles Brucella spp. Besnoitia spp. Sand paper Besnotia spp. Scabby lesions (nose and mouth) Orf virus (Parapoxvirus) Mechanical damage Hoof anomalies/infections Mycotic infections (e.g., Spherophorous spp.) Bacterial infections (e.g., Actinomyces spp.) Parasitic infections (e.g., Besnoitia spp.) Nutritional deficiencies/imbalances White eye Herpesvirus Bacterial infections (e.g., Chlamydia spp.) Injuries Yellow color of subcutaneous tissue Nutritional deficiencies Resolution of hematoma Bacterial/parasitic infections Traumatic lesions/abscesses Injuries Bacterial infections Table 2. Group interviews: participants' perceptions on diseases (lesions/syndromes), expressed as relative prevalence (%), and observations of disease occurrence (provided by the groups that reported the specific disease), in the hunted and observed muskoxen in the Iqaluktutiaq area (Victoria island, Nunavut, Canada) during the decline period. Observed lesions Relative prevalence Disease occurrence N Median IQR Range N Observations Warble flies 7 3 0–5 0–30 5 Noticed since 1985 as an occasional finding (1/5). The majority of the groups started to notice it after 2000–2005 (4/5). White muscle cysts 7 15 0–30 0–35 5 Noticed since 1985 as an occasional finding (1/5). The majority of the groups started to notice it with an increasing trend after 2000–2005 (4/5). Liver cysts 7 5 0–15 0–50 4 Noticed since the 1980s–1990s as an occasional finding (3/4). One group believes that it is increasing since 2005 (1/4). Lung cysts 7 1 0–5 0–10 4 Noticed since the 1980s–1990s as an occasional finding (2/4; description of the cysts is consistent with Echinococcuss canadensis). Two groups noticed it since late 2000s with an increasing trend (2/4; description of the cysts consistent with muskox lungworm Umingmastrongylus pallikkukensis). Swollen joints - limping 7 5 3–25 0–30 6 Noticed since the 1980s as an occasional finding (3/6). The majority of the groups noticed and increasing trend of the finding since 2005 (4/6). Sand paper 7 5 0–5 0–5 5 Noticed since the 1980s–1990s as an occasional finding (2/5). The majority of the groups started to notice it after 2000 (3/5). Scabby lesions (nose and mouth) 7 1 0–10 0–10 4 First noticed in one adult male in 2004 (1/4). Then in two bulls that were sport hunted in 2008 (1/4), and in one adult male sport hunted in 2014 (2/4). Also a dead calf was observed with these lesions in 2012. Hoof anomalies/infections 7 1 0–3 0–10 4 Noticed since the 1990s as an occasional finding (2/4). Two groups started to notice it with an increasing trend since the declining period (2/4). Traumatic lesions/abscesses 7 20 5–30 0–50 6 Always noticed (6/6) with a stable (5/6) or slightly increasing trend (1/6). Due to inter- (i.e., predators, including hunters) or intra-specific interactions (i.e., other muskoxen, especially during the rutting season), and other natural causes. Table 3. Group interviews: participants' perceptions on diseases (lesions/syndromes), expressed as relative prevalence (%), and observations of disease occurrence (provided by the groups that reported the specific disease), in the hunted and observed caribou in the Iqaluktutiaq area (Victoria island, Nunavut, Canada) during the decline period. Observed lesions Relative prevalence Disease occurrence N Median IQR Range N Observations Warble flies 7 40 30–50 20–70 7 Always noticed in almost all the animals during spring and summer time (7/7). It was even a source of food when Inuit lived in outpost camps and prior to life in the community. Nasal worms 7 2 0–10 0–30 4 Noticed since the 1980s, especially on the mainland hunting grounds (4/4). Considered an occasional and stable finding since then (3/4). White muscle cysts 7 15 10–25 3–25 7 Noticed since 1980s–1990s (3/7). The majority of the groups noticed an increasing trend after 2000–2005 (5/7). Liver cysts 7 2 0–3 0–5 4 Noticed since the 1990s as an occasional finding (2/4). Two groups noticed it starting from 2005 (2/4). Swollen joints - limping 7 5 5–15 2–15 7 Noticed since the 1980s as an occasional finding (3/7). Considered more frequent in the 1990s and since 2007–2008 had decreased being occasional again (3/7). However, one group reported an increase in the limping animals since the declining period (1/7). Sand paper 7 5 4–10 0–10 6 Noticed since the 1980s as an occasional finding (4/6). Either stable (3/7) or slightly increasing since 1990–2000 (3/7) Hoof anomalies/infections 7 1 0–10 0–10 4 Noticed since the 1990s as an occasional finding (1/4). The majority of the groups started to notice it with an increasing trend after 2000 (3/4). Traumatic lesions/abscesses 7 5 3–30 0–35 6 Always noticed (6/6) with a stable (5/6) or slightly increasing trend (1/6). Due to inter- (i.e., predators, including hunters) or intra-specific interactions (i.e., other caribou, especially during the rutting season), and other natural causes. 3.3.2. Causes of mortality Causes of mortality described during individual interviews included predation, ‘acute death’, and a variety of other causes that we categorized afterward as ‘other causes’. Other causes ranged from unknown causes (when partial remains of carcasses were observed), to deaths due to drowning (e.g., caribou during the fall migration), injuries due to both natural and anthropogenic causes, starvation (e.g., muskoxen stranded on islands and reported primarily in pre-decline), and “old muskoxen”. A proportional piling exercise was then used in group interviews to determine the proportion of muskox and caribou mortalities attributable to predation, acute death, and other causes (Appendix B). For both muskox and caribou, from the pre-decline to the decline, there was an increase in mortalities attributable to predation (Fig. 4c). Although wolves were considered the primary predators of both species, the proportion of predation attributed to grizzly bears increased for muskoxen from 7% (IQR and range: 0–25; n = 6) in the pre-decline to 25.5% (IQR: 25–40; range: 15–40; n = 6) during the decline. Grizzly bears were also indicated as caribou predators exclusively during the decline by two groups of interviewees. Acute mortality was observed only in muskoxen during the decline period and by 6 of the 7 groups interviewed and it was considered to contribute to the 25% of the total muskox mortality (Fig. 4c). One Inuk hunter described: “There was a bunch of dead muskoxen … They looked like they just fell down and die, it's almost like somebody came and went bang, bang, bang. But they weren't shot they just died”. 3.3.3. Patterns of acute mortalities in muskoxen Twenty-six of 38 interviewees had observed acute deaths of muskoxen. The first reported case was from the early 1980s. From the early 1980s until 2005, 6 participants reported observing a total of 9 to 12 cases. Beginning in 2010, observations of acute mortality increased and peaked in 2012 (Fig. 5). These observations were confirmed by individual narratives. A pilot said “In a normal year during the summer we would see on average a dozen carcasses, but scattered…in that big area we fly in…But then, all of the sudden, in those years ‘10, ‘11, ‘12, we saw a lot more [carcasses] and concentrated in a smaller area ... In Suxess Hills and Surrey Lake, there was at least the double of what you would see in a normal year”. Fig. 5 Download high-res image (772KB)Download full-size image Fig. 5. Characteristics of muskox acute mortalities observed in the Iqaluktutiaq area (Victoria Island, Nunavut, Canada) in the decline period: a) spatial and temporal distribution of cases; b) number of cases from 2009 until the end of 2014; c) relative proportion (%) of cases by season. The thick horizontal lines correspond to the medians; the distance between the thin longer horizontal lines the interquartile range; the whiskers to the range of the data except for outliers. In group interviews, acute mortalities were further characterized through proportional piling and mapping exercises. Among all the muskoxen observed dead, the 95% were adults (IQR: 85–95; range: 60–95; n = 5) and 5% were juveniles (IQR: 5–15; range: 5–40; n = 5) (Appendix G). The seasonal pattern and the spatio-temporal distribution of mortalities are presented in Fig. 5. 4. Discussion Traditional methods of wildlife population monitoring and health surveillance is logistically and financially challenging in remote settings. Through the use of well-established PE techniques (e.g., Mariner and Paskin, 2000, Catley et al., 2012), adapted to the wildlife context and implemented with a robust qualitative research design, we have demonstrated that local and ethnoveterinary knowledge can contribute valuable information on the health, status, and trends of wildlife populations as well as provide insights into possible drivers. The data that we gathered highlighted significant population declines for both muskoxen and the Dolphin and Union caribou herd. These were characterized by poor recruitment, deterioration of body condition status, and increased observations of morbidity for both species, as well as unusual mortality events in muskoxen. These collective observations suggest declining population health of muskoxen and caribou in the study area. Here, we discuss the novel epidemiological observations that originated from this research and provide additional considerations for the broader applicability of these methods for conservation, research and wildlife health surveillance. 4.1. Novel epidemiological observations on muskoxen and the dolphin and union caribou herd Local knowledge confirmed major population declines for muskoxen and caribou, beginning in the mid-2000s. The occurrence and magnitude of these declines reported by interviewees were consistent with the results of aerial population surveys that occurred at the same time and immediately after our study (L-M. Leclerc, 2015, Environment and Climate Change Canada, 2017). Moreover, LK indicated that the body condition of both muskoxen and caribou had deteriorated. We suggest that these data likely underestimated the magnitude of body condition decline. When analyzing the individual narratives, it became clear that while the overall body condition of muskoxen and caribou was deteriorating, the subjective scale of measure by the observers was adapting to the new reality and their assessments were made relative to that new reality. That is, the animals classified in excellent body condition during the decline period would have been classified in poorer categories of condition in the pre-decline period. Concurrent with the declines, morbidity increased (especially for caribou), with increased observations of endemic and emerging syndromes. Some of these endemic syndromes (e.g., swollen joints and limping animals) and emerging (e.g., scabby lesions on nose and mouth) were of interest as they could be associated, among other causes, with pathogens that reduce reproductive success (e.g., Brucella suis biovar 4) and recruitment (e.g., orf virus) and thus may be linked to the population declines. These pathogens have recently been confirmed in muskoxen in the study area (Tomaselli et al., 2016). Local knowledge was invaluable for learning about previously undocumented mortality events. Prior to our study, we were aware of mid-summer acute mortality events of muskoxen on Banks Island (2012 − 2013) and on Victoria Island (2009–2011), including 10 cases reported in 2010 within our study area (Kutz et al., 2015). The interview process documented at minimum 120 more dead muskoxen from 2010 to 2014, with the peak in 2012. The descriptions of these mortalities, entire carcasses, various age classes (although dominated by adults), and no evidence of predation, suggest that were similar to those described by Kutz et al. (2015), and if so, attributable to acute infectious disease. The unexpectedly high number of mortalities reported through our interviews revealed a critical deficiency in the existing standard, passive surveillance system in this region (and likely elsewhere) and the incredible value of using participatory surveillance as an ongoing tool for early detection of disease onset. Despite this value of LK, we suspect that the extent of the morbidity and mortality during this time period was still underestimated because of limitations in the search techniques, carcass removal by scavengers (although this system may have been saturated as the die-offs continued), misclassification of mortalities as primary predatory events because carcasses were scavenged, and predator removal of diseased and weak animals (see Wobeser, 2007). Additionally, carcasses of juveniles would likely be more difficult to detect and would disappear more rapidly (Wobeser, 2007), thus juvenile mortality would be disproportionately underestimated. Of all of the LK data gathered in this study, attribution of muskox and caribou mortality to predation had the widest interquartile ranges, suggesting disagreement among groups. However, grizzly bears were consistently identified as new predators, especially for muskoxen, on Victoria Island during the decline. The high level of uncertainty in the attribution of mortalities to predators could be influenced by the fact that study participants were not selected as ‘predator experts’ and possibly had substantially different expertise on predators. Also, we suspect that explanatory inference or perception that predators might be the primary cause of muskox and caribou declines influenced the observations of increased predation in the decline period. This could have also been overestimated if scavenging was misinterpreted as predation during the mortality events, or may also have been a real increase associated with increased susceptibility of muskoxen and caribou to predation because of poorer body condition and increased incidence of infectious diseases. Important to note is that observations of overall mortality of caribou remained stable between pre-decline and decline, while muskox mortality increased, however, this was mainly due to the increase in acute mortality. Finally, in addition to describing the declines in both muskoxen and caribou, and changes in population structure, LK provided further insights into possible mechanisms for changing demographics. For example, poor body condition and increased burdens of disease, including syndromes consistent with brucellosis and orf, were observed and both may have played a role in the decreased trend of juveniles reported by interviewees. It is well established that body condition of the cow is directly linked to conception and calf survival rates for both species (Kofinas et al., 2002, Miller, 2003, Gunn and Adamczewski, 2003). Similarly, pathogens like Brucella spp. and orf virus are linked to reduced pregnancy rates and increased calf mortality, respectively (Vikøren et al., 2008, Tomaselli et al., 2016). Finally, poor condition and a high burden of disease can lead to increased direct mortality and susceptibility to predation. Together, these are all mechanisms that are likely influencing key demographic rates and ultimately, the dynamics of the declining muskox and caribou populations. 4.2. Key considerations for interpretation of local knowledge Evaluation of possible sources of bias and familiarity with the local context are key for interpretation of LK. Due to their inductive nature, LK studies are likely to generate unexpected findings (Huntington, 2000). Ensuring that the participants included in LK studies are actual experts on the subject of inquiry is essential for correct interpretation of the findings. For example, in this study, participants, selected as muskox experts, provided important insights also on caribou trends and status. Knowing that in Iqaluktutiaq muskox harvesters are also, and often primary, caribou harvesters (Tomaselli et al., In press) allowed us to consider the LK gathered on caribou valid. On the other hand, we believe that information regarding predators should be further explored with participants primarily selected as ‘predator experts’ (e.g., trappers), as these individuals might have been excluded from this study. Knowledge of the local harvesting context, particularly how animals are butchered and what organs are consumed, is also of key importance when interpreting the relative prevalence of diseases gathered through PE. For instance, muskox harvesters included in this study did not consume muskox lungs but left them on the field with only minimal inspection (Tomaselli et al., In press). We thus expected that observations of abnormalities in the lungs, such as muskox lungworm, and that do not cause a pleuritis, were underestimated and may not correspond to the scientific knowledge available (e.g., Kutz et al., 2013, Tomaselli et al., 2016). Personal experience and observation, but also explanatory inference and interpretation, as well as indirect experience and oral history, are all mechanisms that contribute to generating local knowledge (Berkes et al., 2000). Identifying those mechanisms can assist in data interpretation. For example, in this study, changes in participants' perceptions over time might have led to underestimating the magnitude of deterioration of body condition status for muskoxen and caribou in the decline period. On the other hand, changes in perceptions due to a ‘biased’ explanatory inference can lead to overestimation of events. With respect to predators, we think that LK data could largely overestimate the role of predators as a primary driver of the decline of prey species when the latter experience disease outbreaks and/or declining health. Recall and ‘seasonal’ bias must be considered and assessed when focusing on retrospective and seasonal observations, respectively. Regarding the interpretation of seasonal data, differences in seasonal use of the land by LK holders may lead to ‘seasonal bias’ in the LK reported, which likely resulted in the wide interquartile range of the seasonal observations about dead muskoxen. Finally, although we cannot eliminate the possibility that recall errors occurred, especially when exploring historic events, we think that the effects of recall bias on interpretation were minimized by the application of thematic saturation, triangulation, and participants' feedback techniques. 4.3. Key consideration for using local knowledge Local knowledge is well suited to serve as an early warning system to detect changes in wildlife health both at the population and individual level. In this study, LK documented major local declines of muskoxen and caribou prior to the aerial surveys, and provided higher resolution information on key demographic characteristics, as well as individual and population health. Initial LK results, suggesting a population decline, poor body condition, and increased morbidity for the Dolphin and Union caribou herd, resulted in a delay in the assessment of the conservation status of this herd by the Committee on the Status of Endangered Wildlife in Canada (COSEWIC) until population estimates could be completed through aerial surveys. Local knowledge on this herd has continued to inform this assessment, complementing recent scientific data in projecting future trends and understanding threats. As demonstrated by this case, LK is valuable for real-time monitoring of local wildlife population trends, demography, distribution, and patterns in health and disease. It can complement, inform, and target scientific population estimate/census efforts, as well as facilitate timely adaptive management actions, especially when financial restrictions limit the ability to conduct regular systematic surveys. Additionally, observations on individual animals are valuable for early detection of emergent or re-emergent diseases and feedback into scientific monitoring and study design (e.g., see Carlsson et al., 2016). For instance, on Victoria Island, lesions in muskoxen and caribou that are consistent with orf were observed by interviewees in 2005 and 2008. These observations were not gathered until 2014, in the course of this LK study, and the virus itself was not definitively identified until after hunters engaged in a sample collection program reported lesions in a hunted animal, triggering a field disease investigation (Tomaselli et al., 2016). Local knowledge also identified substantial mortality of muskoxen that were undetected by the existing routine passive surveillance system. Thus, observations of resource users, when collected and analyzed in a regular systematic manner, can increase the timeliness and sensitivity of disease detection in wildlife, and greatly contribute to understanding wildlife population health and disease epidemiology. Collaborative identification of research priorities, development of mutual trust among stakeholders, and ultimately, enhanced co-management of wildlife, are invaluable benefits derived from the implementation of participatory research for wildlife health assessment. For instance, results from this study, based on data gathered from and by the local stakeholders, were included in regional co-management plans for muskoxen and the Dolphin and Union caribou herd (see Environment and Climate Change Canada, 2017). The participatory process in knowledge generation fostered dialogue and trust between Inuit and community residents, researchers, and local and territorial organizations. These are the first steps to identify common conservation goals and solution strategies for co-management decisions, while actively promoting the “wildlife trust administration” paradigm as advocated by Decker et al. (2016). Finally, when Indigenous peoples are included in the process of knowledge generation, as in our study, intercultural dialogue among stakeholders and democratization of the research process are also promoted (Rist and Dahdouh-Guebas, 2006). 4.4. Ingredients for success Standardized methodologies are required to appropriately collect, compile, and analyze LK, and to avoid misinterpretation. Moving beyond anecdote, the methods used in this study, which are repeatable, provided quantitative data, supported through narratives and validated through follow-up meetings, contributing critical insights into caribou and muskox population trends and health. This study offers a pragmatic framework that can be broadly applied to other wildlife species and settings. Key ingredients for success include: i) identification of key stakeholders (i.e., local experts) and application of purposeful sampling and thematic saturation to define the sample and its size; ii) triangulation of results to improve data quality and reliability (e.g., individual and group interviews); iii) interpretation of quantitative and qualitative data together (e.g., proportional piling data and participants' narratives) as opposed to relying strictly on one source of data or the other; and finally and most importantly, iv) presentation to, and discussion with, study participants of the overall analyses and interpretations of the findings so as to avoid misinterpretation. If disagreement arises at any level during the study, we suggest that efforts should be directed to understanding the reasons behind such disagreement, rather than focusing on achieving agreement alone. While researchers need to be flexible and ready to adapt the methods to the specific context and research questions, these procedural key points should be maintained. Scaled up and implemented consistently across a network of communities on an ongoing basis, this framework could help in understanding the status and trends of a variety of different wildlife populations across much of their range and inform conservation, monitoring, and research priorities. While we do not provide a comprehensive list of participatory techniques (with both relative and absolute scales of assessment) applied to wildlife health, we rather offer a robust methodological approach for the collection and interpretation of LK data for wildlife population health assessment that can be transferable and adaptable to other settings and species. In addition, LK data similarly gathered and interpreted can be applied to other fields of study (e.g., ecosystem health, disease ecology). Engaging in transdisciplinary research, and adapting to the wildlife context participatory techniques used in other disciplines will be a critical asset to realize the full potential of LK for wildlife population health assessment and beyond. 4.5. Conclusion Assessing wildlife population health is rarely an easy task, due to the difficulty, if not inability, to gather and interpret data that holistically capture the dynamic and adaptive processes that characterize wildlife population health (Hanisch et al., 2012, Stephen, 2014). In our view, the holistic way that local resource users experience and interpret the natural environment makes their knowledge and perspectives pivotal for understanding the health and status of free-ranging populations, along with its drivers. Moving beyond the long-lasting debate focused on the evaluation of LK against scientific knowledge (Gilchrist et al., 2005, Brook and McLachlan, 2005), it is time to direct our efforts to actively promote the use of these two complementary knowledge systems in a synergistic way for effective, evidence-based management. This work moves in such direction. Here we have demonstrated that LK, when gathered and interpreted in a robust way, is a reliable source of data on wildlife population health and trends that can provide new and valuable information and holistic interpretation to complement and guide scientific research and inform wildlife management. Robust methods and interpretations, together with data validation, are key elements to ensure reliability and acceptability of LK for wildlife population health assessment. Here we have outlined procedural key points that can guide the collection and interpretation of LK, allowing the implementation of a repeatable method that minimizes subjective interpretation. We emphasize that LK studies applied to wildlife health should be undertaken as team efforts with the inclusion of experts from different fields. In our study, interpretation of the ethnoveterinary knowledge was greatly improved because the interviewer had a core knowledge in animal health and was able to explore and interpret these themes in greater depth. Similarly, the team also included experts in wildlife management and in social and participatory research methods, which ensured appropriate methodological approaches and interpretation. Using LK to measure and understand wildlife health opens new avenues for the implementation of health surveillance programs for free-ranging species, especially in remote rural areas. Although the spatial resolution of LK may be considered a limitation when studying free-ranging populations with large home ranges, the implementation of participatory programs for wildlife health across a network of communities can offer expand the geographic scope. In addition, such approach can further foster intercommunity dialogue, and, in so doing, promote collaboration at larger scales. Finally and, perhaps most importantly, the process of gathering LK is associated with enhanced dialogue and trust among stakeholders. This ultimately contributes to creating common grounds for collaborative actions that can greatly improve co-management and conservation of wildlife at a time where species are facing ever-increasing threats to their persistence. The following are the supplementary data related to this article. Download Word document (15KB) Help with docx files Appendix A. Interview guide used during the individual interviews. Download Word document (1MB) Help with docx files Appendix B. Group interview methods. Download Word document (3MB) Help with docx files Appendix C. Area observed by interviewed participants. Download Word document (22KB) Help with docx files Appendix D. Individual interviews: selected quotes from participants that represent muskox abundance over time in the Iqaluktutiaq area (Victoria Island, Nunavut, Canada). Download Word document (22KB) Help with docx files Appendix E. Individual interviews: selected quotes from participants that represent caribou abundance over time in the Iqaluktutiaq area (Victoria Island, Nunavut, Canada). Download Word document (26KB) Help with docx files Appendix F. Group interviews: participants' perceptions of the relative proportion (%) of adults (males and females) and juveniles (yearling and calves) in the observed muskoxen and caribou in the Iqaluktutiaq area (Victoria Island, Nunavut, Canada) during the pre-decline and decline periods. Download Word document (19KB) Help with docx files Appendix G. Group interviews: participants' perceptions of the relative proportion (%) of adults (males and females) and juveniles (yearling and calves) in the dead muskoxen (acute mortality) observed in the Iqaluktutiaq area (Victoria Island, Nunavut, Canada) during the decline period. Acknowledgments We are extremely grateful to the study participants of the community of Iqaluktutiaq for their essential contribution to this project. We are also particularly grateful to E. Kakolak and H. Ohokanoak who collaborated as interpreters and translators during the field work. We thank the Kitikmeot Inuit Association, the Ekaluktutiak Hunters and Trappers Organization and the Nunavut Research Institute for their continued support. We are particularly grateful to M. Cote, P. Emingak, J. Ogina, F. Peterson, C. Evalik, S. Anablak, J. Evalik, S. Janke, M. Buchan, J. Haniliak, J. Panioyak, B. Greenley, B. Sitatak, A. Maghagak, and B. 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